Epidemiology, Gastrointestinal Parasite Infections, Dairy Cattle, Kiambu District, Kenya Denmark

v\ EPIDEM IOLOGY AND CONTROL O F GASTROINTESTINAL PARASITE
INFECTIONS OF DAIRY CATTLE IN KIAMBU DISTRICT, KENYA A ND IN
DENM ARK W ITH EMPHASIS ON PARASITIC GASTROENTERITIS //
BY
g B ■V» B9' 9
1 - t r i»»
\SO A c „
v,USlV'<
ROBERT MAINA W ARUIRU, BVM (Nairobi), M .Sc. (Cornell, USA)

1
UNIVERSITY of NAIROBI
LIBRARV
P. O. Box 30197
NAIROBI
A thesis submitted in fulfilm ent of the requirements for the degree of
Doctor o f Philosophy in Veterinary Parasitology
of the University of Nairobi
Departm ent of Veterinary Pathology and Microbiology,
Faculty o f Veterinary Medicine
University of Nairobi, Kenya
1998
11
DECLARATION
(a) This thesis is my original work and has not been presented for a degree in any other
University.
--------------------------------------
Robert M aina Waruiru
(b) This thesis has been submitted for examination with our approval as University
supervisors
Prof. W.K. Munyua, B .V .Sc., M .Sc., Dip.A.t.H.. Ph.D.
Prof. J.M. Gathuma, M .Sc., Ph.D.
Faculty o f Veterinary Medicine (Kabete Campus), University o f Nairobi, P. O. Box
29053 Nairobi, Kenya
EXTERNAL SUPERVISOR
Prof. Peter Nansen, DVM ., Dr. Vet. Sci., Ph.D.
Danish Centre fo r Experimental Parasitology, Department o f Veterinary
Microbiology, Royal Veterinary and Agricultural University, Bulowsvej, DK-1870
Frederiksberg C, Denmark
I l l
TABLE O F CONTENTS
Page
TITLE AND AUTHOR .................................................................................................................. j
DECLARATION ...................................................................................................................................jj
TABLE OF C O N T E N T S .....................................................................................................................jjj
LIST OF TABLES ...........................................................................................................................xiii
LIST OF F IG U R E S .................................................................... xviii
LIST OF A P P E N D IC E S .............................................................. xxiii
ACKNOWLEDGEMENTS ...................................................................................................... xxiv
D E D IC A T IO N ............................................................................................................................... xxvi
ABSTRACT ..................................................................................................................................... xxvii
CHAPTER 1 GENERAL IN T R O D U C T IO N ............................................................... I
CHAPTER 2 LITERATURE REVIEW ..................................................................... II
2 .1 Farm ing systems and livestock populations
in K e n y a ................................................................................................... II
2.1.1 Farming sy stem s....................................................................................... 12
2 .1 .2 Population dynamics .............................................................................. 16
2 .1.3 Offtake estimates by en te r p r ise ........................................................... 17
2.2 Epidemiology o f helminth infections of
rum inants in the tropics .................................................................... 20
2.2.1 Epidemiology o f nematodoses in K e n y a ............................................. 22
2 .2 .2 Bovine parasitic g a stro en teritis........................................................ 23
2.2.2.1 Aetiology, mode of transmissionand species sp ectru m ................... 23

iv
TABLE OF CONTENTS (continued)
Page
2 .2 .2 .2 Nematode life c y c l e s .............................................................................. 24
2 .2 .2 .3 Parasitic development and tissue changes
caused by strongylid nem atodes........................................................... 27
2.2 .2 .3 .1 Haemonchus spp S . ................................................................................. 27
2 .2 .2 .3 .2 Trichostrongylus spp.................................................................................. 28
2 .2 .2 .3 .3 Cooperia spp................................................................................................ 29
2 .2 .2 .3 .4 Oesophagostomum radiatum ............................................................... 30
2 .2 .2 .4 Factors influencing ep id em io lo g y ...................................................... 32
2 .2 .2 .4 .1 Extrinsic fa c to r s....................................................................................... 32
2 .2 .2 .4 .1 .1 Climate and weather .............................................................................. 32
2 .2 .2 .4 .1 .1 .1 Bionomics of free-living s t a g e s ............................................................ 33
2 .2 .2 .4 .1 .1 .2 Seasonal patterns of in fe c tio n .............................................................. 34
2 .2 .2 .4 .1 .1 .3 Livestock production systems and
husbandry p ra ctices................................................................................ 36
2 .2 .2 .4 .2 Intrinsic factors ........................................................................................ 38
2 .2 .2 .4 .2 .1 Nutrition .................................................................................................... 38
2 .2 .2 .4 .2 .2 Host age, sex, acquired resistance and
genotype ................................................................................................... 39
2 .2 .2 .4 .2 .3 Arrested larval developm en t.................................................................. 42
2 . 2 .2 .4 .2 .4 Concurrent in fection s.............................................................................. 44

V
Page
2 .2.2.5 Pathophysiology and clinical effects of
nem atode in f e c t io n s .............................................................................. 45
2.2 .2 .5 .1 P athophysiology...................................................................................... 45
2 .2 .2 .5 .1 .1 Decreased feed intake ......................................................................... 45
2 .2 .2 .5 .1 .2 Gut motility, digestion and absorption.............................................. 46
2 .2 .2 .5 .1 .3 Protein and energy m eta b o lism .......................................................... 47
2 .2 .2 .5 .1 .4 Mineral metabolism ............................................................................ 47
2 .2 .2 .5 .1 .5 Water and electrolyte balance .......................................................... 48
2 .2 .2 .5 .2 Clinical effects ..................................................................................... 49
2 .2 .2 .6 Impact o f nematodosis on livestock
production ............................................................................................. 50
2 .2 .2 .7 Diagnosis of parasitic gastroenteritis ........................................... 52
2 .2 . 2 .7.1 Clinical d ia g n o s is .................................................................................. 52
2 .2 .2 .7 .2 Laboratory d ia g n o s is ............................................................................. 52
2 .2 . 2 .7 . 2.1 Faecal egg counts ................................................................................ 53
2 .2 .2 .7 .2 .1 .1 Factors affecting egg counts ............................................................. 54
2 .2 .2 .7 .2 .1 .2 Faecal cultures ..................................................................................... 55
2 .2 .2 .1 .2 2 Pasture larval counts .............................................................................. 55
2 .2 .2 .1 .2 2 Blood parameters .................................................................................... 56
2 .2 .2 .7 .2 .3 .1 Pepsinogen ............................................................................................ 56
2 2 .2 .1 .2 2 .2 Gastrin .................................................................................................... 57
2 2 .2 .1 .2 2 2 Albumin 58
V I
Page
2 . 2 .2.7 . 2.3.4 Immuno-diagnosis (serodiagnosis) .................................................... 58
2 .2 2 .1 .2 Biotechnology and the diagnosis o f
nematode infections ............................................................................. 59
2.3 Principles of helminth control ......................................................... 61
2.3.1 Control of parasitic gastroenteritisin cattle .................................... 62
2.3.1.1 Pasture management and grazing h y g ie n e ......................................... 62
2.3.1.2 Control based on anthelmintic usage ............................................... 63
2.3.1.2.1 Strategic d ren ch in g ................................................................................. 63
2 .3 .1 .2 .2 Tactical drenching ................................................................................. 64
2 .3 .1 .2 .3 Anthelmintic treatment strategies
in the tropics .......................................................................................... 65
2.3.1.3 Integrated worm control ........................................................................ 66
2.3.2 Availability and distribution of
anthelm intics .......................................................................................... 68
2.3.2.1 Dosing m e th o d s ........................................................................................ 69
2.3.2.1.1 Slow and pulse release methods ............................ \ . ...................... 70
2.3.2.2 Anthelmintic characteristics o f morantel
and albendazole ...................................................................................... 73
2.3.2.2.1 Morantel .................................................................................................... 73
2 .3 .2 .2 .2 Albendazole .............................................................................................. 73
2 .3 .3 Anthelm intic resistance ..................................................................... 74
2.3.3.1 Factors associated with resistance ..................................................... 75

v ii
Detection of r e sista n c e ............................... 77
Alternative control methods ................... 77
Prospects of vaccines ............................... 79
Genetic resistance ..................................... 80
Medicinal plants ........................................ .. 82
Biological control ........................................ 82
Nematophagous fungi .................................. 83
Endoparasitic f u n g i ........................................ 84
Nematode-trapping f u n g i............................... 84
Nematophagous fungi as biocontrol agents
o f parasitic nematodes o f livestock . . . . 85
PREVALENCE AND INTENSITY OF
HELMINTH AND COCCIDIAL
INFECTIONS: A FIELD SURVEY . . . 91
Introduction ................................................. 91
M aterials and M e t h o d s ............................... 92
Study area .................................................... 92
Location and s i z e ........................................... 92
Topography and geology ........................... 92
C lim a t e ............................................................. 95
Livestock production 95
Experimental design 97
v iii
Page
Statistical analysis ........................................................... 101
R e s u l t s ................................................................................ 101
Meteorological data ........................................................ 101
Parasitological findings .................................................. 102
D is c u s s io n .......................................................................... 116
Stronylid infections ........................................................ 116
Coccidia infections ........................................................... 119
Liver fluke infections ..................................................... 119
FATAL HAEMONCHOSIS IN HEIFERS
AT IGANJO FARM: A CASE STUDY ..................... 121
Introduction ....................................................................... 121
Case history .......................................................................... 122
Clinical o b serv a tio n s........................................................... 122
Post mortem findings in calf No. 1625 ...................... 123
Treatment ............................................................................. 123
D is c u s s io n ............................................................................. 123
GASTROINTESTINAL NEMATODE INFECTIONS:
AN ABATTOIR SURVEY ........................................... 126
Introduction ....................................................................... 126
M aterials and Methods ................................................. 126
Experimental design 126
Statistical analysis . 127

IX
Page
Results ............................................................................. . 127
Parasitological findings .............................................. . 127
Age/worm burden relationship .................................. 128
D is c u s s io n ....................................................................... 131
EPIDEMIOLOGY OF GASTROINTESTINAL
NEMATODES: A ONE-YEAR S T U D Y ................ 135
Introduction ................................................................. 135
M aterials and M e t h o d s .............................................. 135
Experimental design ..................................................... 135
Results ............................................................................. 137
Meteorological d a t a ........................................................ 138
Faecal egg and herbage larval counts ...................... 138
Worm burdens in yearling c a t t l e ............................... 143
Worm burdens in tracer calves and resident animals 143
Haematology and serum pepsinogen analysis . . . 146
Weight gains ................................................................. 150
D is c u s s io n ....................................................................... 150
DEVELOPMENT AND SURVIVAL
(PLOT STUDIES) OF INFECTIVE
LARVAE ON P A S T U R E ........................................... 155
Introduction ................................................................. 155
M aterials and Methods 156

x
Page
Experimental design ................................................................. 156
Results ......................................................................................... 157
Discussion ................................................................................... 159
COMPARATIVE EFFICACY OF MORANTEL
SUSTAINED RELEASE TRILAMINATE BOLUS
A N D CONVENTIONAL ANTHELMINTIC
TREATMENT AGAINST GASTROINTESTINAL
N E M A T O D E S............................................................................. 163
Introduction ................................................................. 163
M aterial and Methods ........................................................... 164
Experimental design ................................................................. 164
Statistical a n a ly sis....................................................................... 166
Results ......................................................................................... 166
Pasture larval counts ................................................................. 166
Faecal egg c o u n t s ....................................................................... 167
Worm counts in tracer c a l v e s ................................................. 167
Worm burdens at termination o f the trial ......................... 170
Liveweight gains ....................................................................... 170
Blood parameters and clinical observations ...................... 174
Discussion ................................................................................... 174
OVERWINTERING RESIDUAL GRASS INFECTIVITY
IN PASTURES PREVIOUSLY GRAZED BY

xi
Page
DUDDINGTONIA FLAGRANS FED CALVES . . . . 178
Introduction .................................................................... 178
M aterials and Methods .............................................. 181
Study area .......................................................................... 178
Experimental design ........................................................ 179
Herbage larval co u n ts........................................................ 179
Faecal egg c o u n t s .............................................................. 180
Post mortem worm c o u n t s .............................................. 180
Results ................................................................................ 180
Herbage larval co u n ts........................................................ 180
Faecal egg c o u n t s .............................................................. 181
Faecal cultures ................................................................. 181
Post mortem worm counts ........................................... 181
Body w e i g h t ....................................................................... 185
Discussion .......................................................................... 185
THE INFLUENCE OF EGG COUNTS
AND FUNGAL DOSE LEVELS ON
THE NEMATODE-TRAPPINIG CAPABILITY
OF DUDDINGTONIA FLAGRANS AGAINST
FREE-LIVING STAGES OF GASTROINTESTINAL
NEMATODES OF CATTLE 189

x ii
Page
10.1 Introduction ............................................................................................. 189
10.2 M aterials and M e t h o d s .......................................................................... 190
10.2.1 Parasite m aterial.......................................................................................... 190
10.2.2 Fungal material .......................................................................................... 191
10.2.3 Experimental design .................................................................................191
10.2.4 Faecal culture a s s a y .................................................................................... 191
10.2.5 Trapping efficacy and statistical analysis ............................................192
10.3 R esults ......................................................................................................... 193
10.4 D is c u s s io n .................................................................................................. 203
CHAPTER 11 GENERAL D ISC U SSIO N ........................................................................ 206
11.1 C o n c lu s io n s ................................................................................................. 211
REFERENCES...............................................................................................................................212
x iii
LIST O F TABLES
Table No. Page
Table 2.1 Livestock populations by zones and production
systems in 1990 ................................................................................................. 14
Table 2.2 Herd structures, and herd offtake o f dairy and beef
herds at three levelso f inputs................................................................................ 19
Table 2.3 Distribution o f major nematode parasites o f
large herbivores and their relative importance
(rank) within thetropics.......................................................................................... 25
Table 2.4 Anthelmintic available for the control of
nematodes in cattle.................................................................................................. 76
Table 2.5 Nematodes o f cattle with reported resistance
to broad-spectrum anthelmintics.......................................................................... 78
Table 3.1 Livestock enterprise and 1991/92 population.................................................... 98
Table 3.2 Livestock production trend 1991/92.................................................................... 99
Table 3.3a The prevalence (five months sampling) of strongylids,
liver fluke, tapeworm eggs and coccidial oocysts in
faecal samples in relatioin to age and sex of
cattle on 16 farms in Kiambu District
during the dry and wet seasons.............................................................................. 104
Table 3.3b The prevalence percentages of eggs o f strongylids,
Fasciola, Moniezia and coccidial oocysts in faecal
samples from all sampling locations during dry (D)
and wet (W) seasons..................................................................................................105

x iv
LIST OF TABLES (continued)
Table N o. Page
Table 3.4 Percentage distribution of infective larvae (L3) o f
different genera of nematodes found in faecal culture
o f pooled samples of three categories of dairy cattle
averaged across 5 months in the dry and wet seasons
(mean o f farms and range').................................................................................. 113
Table 3.5 Prevalence and intensity o f infection with individual
species o f gastrointestinal nematodes in tracer calves
examined during the dry and wet seasons........................................................ 115
Table 4 .1 Number and percentage o f nematode species recovered at
post mortem o f calf No. 1625............................................................................... 124
Table 5.1 Spectrum, prevalence and mean burdens o f nematodes
found in cattle in Kiambu District in 672 post mortem
examinations between August 1992 and July 1993........................................ 129
Table 6 .1 Recovery o f gastrointestinal nematodes from yearling
dairy cattle necropsied bi-monthly ( n = 2) during
the study period.......................................................................................................... 144
Table 6.2 Monthly changes in the composition o f Haemonchus placei
in tracer calves in Iganjo and Kambaa farms.................................................. 147
Table 6.3 Mean and range o f worm burdens o f resident yearling
animals necropsied at studytermination................................................................ 148

XV
Table N o . Page
Table 8.1 Worm counts recovered from tracer calves
(2 calves per group) and in parenthesis
the percentage worm reduction on paddocks
T-2, T-3, and T-4 compared to T - l...................................................................171
Table 8.2 Mean number and, in parenthesis, the percentage
worm reduction after anthelmintic treatment of adult
and immature worms from 3 calves per group
necropsied at trial termination..............................................................................172
Table 8.3 Mean body weights and weight gains of control (T -l)
and treated (T-2-4) calves.................................................................................. 172
Table 9.1 Mean worm counts of two groups o f calves at necropsy
on 22nd o f June 1994. Five animals were slaughtered
from each group o f calves. The experimental group (B)
of calves grazed on a plot previously grazed by calves
fed with the nematode-trapping fungus D. flagrans.
The control group (A) o f calves grazed on a plot
previously grazed by calves not offered any
nematode-trapping fu n gu s................................................................................... 186
Table 9 .2 The average ( ± S.D) increase in body weight
(kg) o f experimental (group B) and control
(group A) calves from 2nd May (week 0)
to 22nd June (week 7 ) ......................................................................................... 187

Table No
Table 10.1 Mean number o f infective H. placet larvae (L3)
recovered from lOg of cattle faeces mixed with
1000, 5000 and 25000 D. flagrans chlamydospores
per gram o f faeces............................................................
Table 10.2 Mean number o f infective T. axel larvae (L3)
per gram o f faeces.............................................................
Table 10.3a Mean number o f infective C. oncophora larvae (L3)
per gram o f faeces (batch A )..........................................
Table 10.3b Mean number o f infective C. oncophora larvae (L3)
per gram o f faeces (batch B)..........................................
Table 10.4a Mean number o f infective O. radiatum larvae (L3)

x v ii
Table No Page
per gram o f faeces (batch A )............................................................................... 196
Table 10.4b Mean number o f infective 0 . radiatum larvae (L3)
recovered from lOg o f cattle faeces mixed with
per gram o f faeces (batch B)................................................................................196

x v iii
LIST OF FIGURES
Figure No. Pape
Fig. 3.1a Sketch map o f Kenya showing location of
Kiambu District.................................................................................................... 93
Fig. 3.1b Sketch map o f Kiambu District showing
administrative divisions and approximate location
of farms used for this study.................................................................................. 94
Fig. 3 .2 Meteorological data for Kiambu District
(at least 10 years o f records up to 1995).......................................................... 96
Fig. 3 .3 Rainfall distribution in study area during1991-92 ............................................ 103
Fig. 3 .4 Geometric mean strongylid, liver fluke eggs and
coccidial oocyst counts o f calves,yearlings and
adult cattle.................................................................................................................... 107
Fig. 3 .5 Geometric mean strongylid, liver fluke eggs and
coccidial oocyst counts o f female and
male animals................................................................................................................ 108
Fig. 3 .6 Individual faecal egg counts (epg) for yearlings
in May grouped according to farm
(each point represents oneobservation)................................................................. 109
Fig. 3 .7 The distribution o f strongylid faecal egg counts in
relation to age groups in the dry (September) and
wet (May) seasons. I ll

XXX
LIST OF FIGURES (continued)
Figure No. Page
Fig. 3.8 Observed frequencies o f faecal strongylid egg counts
in all age groups in the dry (September) and
wet (May) seasons......................................................................................................112
Fig. 3.9 Overall percentage distribution o f strongylid
genera found in faecal cultures................................................................................114
Fig. 5.1 Seasonal pattern of nematode burdens and faecal
egg output o f cattle slaughtered during the abattoir
su rv ey ........................................................................................................................... 130
Fig. 5 .2 The relationship between gastrointestinal worm
burdens and the age of cattle examined during
the abattoir s u r v e y ................................................................................................... 132
Fig. 6 . la Monthly number of raindays and monthly pattern
of rainfall for Iganjo and Kambaa farms
from April, 1993 to April, 1994............................................................................ 139
Fig. 6.1b Mean relative humidity (R.H), mean monthly
maximum and minimum temperatures for Iganjo
and Kambaa farms from April, 1993
to April, 1994....................................................................................................... 140
Fig. 6 .2 Faecal egg counts expressed as eggs/g of faeces
and larval recovery from herbage expressed as
Lj/kg o f dry matter....................................................................................................141
Fig. 6.3 Strongylid nematode infective larvae recovered

XX
Figure No. Page
from faecal egg output o f resident cattle.......................................................... 142
Fig. 6.4 Mean monthly worm burden and frequency
o f occurence o f the dominant gastrointestinal
nematode species in tracer calves...........................................................................145
Fig. 6.5 Mean ( ± S .D ) haematological, serum protein
and pepsinogen values for resident cattle
at Iganjo and Kambaa farms....................................................................................149
Fig. 6.6 Mean ( ± S .D ) liveweight changes in resident
cattle at Iganjo and Kambaa farms........................................................................ 151
Fig. 7.1 Recoveries (average of 5 plots) o f infective
larvae per kilogram of pasture dry matter, log
transformed, (log 10 (x + 1) and corrected for
the numbers o f eggs deposited, on plots contaminated
sequentially from July 1995 to June 1996. H,
Haemonchus\ C, Cooperia\ 0 , Oesophagostomum\
T, Trichostrongylus................................................................................................ 158
Fig. 7.2 Meteorological data for Kimende, Kiambu District
(study site) from July 1995 to June 1996..................................................... 160
Fig. 8.1 Pasture contamination with strongylid infective larvae................................. 168
Fig. 8.2 Mean strongylid eggs per gram o f faeces......................................................... 169
Fig. 8.3 Mean Iiveweights o f treated and control
calves..........................................................................................................................173
xxi
Figure No. Page
Fig. 9.1 Herbage trichostrongylid larval counts on the
plots previously grazed by calves fed with
nematode-trapping fungus D. flagrans (plot B)
and by calves not offered any nematode-trapping
fungus (plot A )........................................................................................................ 182
Fig. 9 .2 Mean trichostrongylid faecal egg counts from
experimental (group B) and control (group A)
calves grazed on plots previously grazed by calves
fed with the nematode-trapping fungus D. flagrans
(plot B) and by calves not offered any nematode-trapping
fungus (plot A )............................................................................................................183
Fig. 9 .3 Number of trichostrongylid larvae harvested
from faecal cultures of experimental (group B)
and control (group A) calves from 30th May
(week 4) to 20th June (week 7) 1994................................................................... 184
Fig. 10.1 Effects of D. flagrans on the recovery o f H. placet
infective la r v a e .........................................................................................................197
Fig. 10.2 Effects of D. flagrans on the recovery o f T. axel
infective la r v a e .........................................................................................................198
Fig. 10.3a Effects of D. flagrans on the recovery of C. onchophora
infective larvae (batch A ) ................................................................................ 199

X X II
Figure No. Page
Fig. 10.3b Effects o f D. flagrans on the recovery of C. onchophora
infective larvae (batch B ) .......................................................................... 200
Fig. 10.4a Effects o f D. flagrans on the recovery of O. radiation
infective larvae (batch A ) ..........................................................................201
Fig. 10.4b Effects of D. flagrans on the recovery of O. radiation
infective larvae (batch B ) ..........................................................................202
Fig. 11 Schemic representation o f the equipments
and the technique for faecal culture..................................................................... 294

XX111
LIST O F APPENDICES
Appendix No. Page
Appendix 3.1 The recovery and identification of
gastrointestinal nematodes post m o r te m ............................................... 282
Appendix 6.1 The serum pepsinogen test ..................................................................... 285
Appendix 9.1 Technique for recovery o f gastrointestinal
nematode larvae from herbage ................................................................ 287
Appendix 9.2 Modified McMaster technique ............................................................... 290
Appendix 9.3 Techniques for faecal cultures ...............................................................291

x x iv
ACKNOW LEDGEM ENTS
This thesis is based on studies undertaken in Kenya (5 experiments) and Denmark (2
experiments) during the years 1991 to 1996.
This work was financially supported by the Danish International Development Agency
(DAN IDA) to whom I extend my sincere appreciation.
I wish to express my deepest gratitude to my supervisors, Professor, D .Sc. Peter
Nansen o f the Centre for Experimental Parasitology (C .E .P .), Royal Veterinary and
Agricultural University in Denmark, Professors W.K. Munyua and J.M. Gathuma both of
the University o f Nairobi for their invaluable advice, suggestions, guidance and
encouragement throughout the study period.
My sincere thanks are also due to Senior Scientist Dr. Michael Larsen, Co-ordinator
of Predacious Fungi Project in Denmark for his invaluable assistance and support in my
biocontrol research work and interpretation o f the results. Thanks are further due to
Laboratory Technicians Margrette Pearman and Eva Jensen for always extending a helping
hand, when needed. I fully appreciated pleasant daily cooperation and unforgettable
friendship given by Professor Nansen (head, C. E. P.) and his staff during my one year stay
in Denmark.
I am grateful to Dr. Henrik 0 . Bogh, Professor Stig. M. Thainsborg, Niels, Chr.
Kyvsgaard, Co-ordinators, ENRECA Ruminant Helminth Research Project, for their
inspiring support, guidance and constructive criticism while conducting experiments and
preparing the manuscripts.
Special thanks are extended to academic staff members o f parasitology section.
Department o f Veterinary Pathology and Microbiology for their encouragement and support
during various phases of this work. Sincere thanks are also extended to Messrs J.N. Ngotho,
XXV
E.W. Weda, S.O. Ojiayo, R.O. Otieno, J.W. Gaita and A.K. Murathi for their technical
assistance in the field and laboratory, respectively.
My sincere thanks go to my employer, University of Nairobi for allowing me to go
on study leave to do part o f this work. They also provide laboratory facilities and the
laboratory staff. The administrative support provided by Professor T.A. Ngatia, Chairman,
Department of Veterinary Pathology and Microbiology is also highly appreciated.
My gratitudes also goes to the farmers particularly Kariku Kariuki (Iganjo farm, Juja)
and John Chege William (Kambaa farm, Lari) who were very Cooperative during this study
in their respective farms. Also acknowledged are Mrs Anne W. Ngaii and Miss Edith W.
Kabure for typing and proof reading parts o f this thesis.
To my w ife Lydiah W. Maina, I ow e a continuing debt o f gratitude for your
uninterrupted support and forbearance during the long periods o f study. To my brothers and
sisters and their respective families, I say thanks for your encouragement and moral support.
xxvi
DEDICATION
This work is dedicated to my son, Fred W aruiru Maina.

X X V I1
ABSTRACT
a) Field survey
The present study was designed to establish a profile of gastrointestinal (Gl) parasites
and to determine the influence of season, farm, age and sex on their prevalence, burden and
distribution in dairy cattle. A survey o f GI parasite infections o f young ( < 6 months old),
yearlings (6-12 months old) and adult ( > 12 months old) cattle on 16 farms in Kiambu
District was conducted during an exceptionally dry season (September 1991 to January 1992)
and during a wet season (March to July 1992). The survey was based on monthly
coproparasitological examination of cohorts and worm counts in tracer calves. The effects
of age, sex, farm and season on the prevalence and intensity o f helminth and coccidia
infections were determined. Faecal egg and oocyst counts revealed that the overall
prevalences were: strongylids (85.5% ), liver flukes (34.0% ), coccidia (30.9% ) and
tapeworms (9.6% ). Eight species o f the protozoan Eimeria were identified and the most
prevalent species were E. bovis and E. zuernii. The most prevalent nematode genera were
Haemonchus, Cooperia, Oesophagostomum and Trichostrongylus. Season, farm and age of
the animals had a significant influence on the intensity (P < 0 .0 5 ) of infection with
strongylids, liver flukes and coccidia, whereas the sex o f the animals had no significant
(P > 0 .0 5 ) effect on the prevalence or intensity o f infections. A higher intensity of infection
with strongylids and coccidia was found in the wet season compared to the dry season
(P < 0 .0 5 ). The age specific intensity was in the following order: for strongylids, yearlings
had the highest egg counts, followed by calves and adults. Calves had significantly (P < 0.05)
higher oocyst counts compared to yearlings and adults. Liver fluke egg counts did not differ
significantly (P > 0 .0 5 ) between yearlings and adult cattle.

x x v iii
b) Case study
The aim o f this study was to investigate the cause o f poor condition and death among
weaner calves at Iganjo farm. Parasitic gastritis due to H. placei was found at necropsy of
a nine month weaner calf while, clinical signs and history of other sick animals examined
included occasional diarrhoea, unthrifty coats, submandibular oedema, anaemia, weakness
and progressive emaciation. The animals, however, had continued to eat until shortly before
death. At necropsy, lesions were predominantly haemorrhagic gastritis, generalized oedema,
pale mucus membranes and fat degeneration. Adult and immature Haemonchus worms were
recovered in large numbers from the lumen o f the abomasum. Relatively small numbers of
other worm species, including T. axei, Cooperia spp. Nematodirus helvetianus, 0. radiation
and Trichuris globulosa were recovered. On treatment of other cases with albendazole and
supportive drugs there was gradual recovery. The cause of the outbreak was attributed to the
release o f highly susceptible calves onto a highly contaminated pasture during the wet season.
c) Abattoir survey
The objective o f this survey conducted from August 1992 to July 1993 was to provide
information on the spectrum and prevalence o f GI nematodes o f cattle and to assess the
occurrence o f hypobiosis in H. placei. Gastrointestinal (Gl) tracts o f 672 crossbred cattle
were examined for the presence of GI nematodes. Eight nematode species were found in 583
( 86. 8 %) o f the animals. The nematodes were, in order of prevalence: H. placei (67.0% ), C.
pectinata (53,0% ), C. punctata (41.7%), O. radiation (38.4% ), T. axei (24.3% ), N.
helvetianus (19.6% ), T. globulosa (9.7%) andStrongyloidespapillosus (3.6%). The intensity
of the nematode infections was moderate: the mean burden being less than 7,000 worms. H.
placei accounting, on average, for 52.3% o f the total nematode burden. The total burden was
X X IX
least during dry seasons and increased gradually during the rainy seasons. Adult //. placei
persisted in the host throughout the year and there was no indication of hypobiosis. The
heaviest GI worm burdens were detected in 1.5 to 3 year-old animals.
d) One-year epidemiological observations
The purpose of the present work was to more precisely define seasonal prevalence,
abundance and importance o f GI nematodes o f weaner-yearling cattle over a 13-month
period. The epidemiology o f H. placei and other GI nematodes in yearling dairy cattle was
examined monthly in two farms during the period running from April 1993 to April 1994.
In each farm, 32 head of newly weaned dairy calves were given a single dose o f albendazole
and then placed on experimental pastures. Twelve o f the animals were designated for bi
monthly slaughter (n = 2) and analysis o f worm population characteristics and 20 were
designated for blood and faecal collection and for weighing. Parasite-free tracer calves were
grazed alongside the weaner calves each month ( n = 2) throughout the study period and were
also slaughtered for analysis o f worm populations. Faecal egg counts, haematological and
serum pepsinogen determinations, herbage larval counts, and animal liveweight changes were
recorded monthly. The study revealed that H. placei, T. axei, Cooperia spp. and O. radiation
were responsible for parasitic gastroenteritis (PGE) and H. placei was the predominant
nematode present in young cattle of both farms. Faecal egg counts from resident cattle and
necropsy worm counts revealed that pasture larval levels were directly related to the level
of rainfall. Total worm burdens present in the animals were highest during the rainy seasons
(March/June and October/December) and lowest during the dry seasons (July/September and
■lanuary/February). The very low recovery of H. placei immature larvae in tracer calves
indicated that arrested development is not a feature o f the life cycle o f this parasite in central
XXX
Kenya. The maintenance o f the parasite population depended on the continuous cycle of
infection between the host and the pasture. The agro-climatic conditions o f the study area
revealed that, in general, favourable weather conditions for the development and survival of
the free-living stages of GI nematodes existed ail the year round.
e) Plot studies
The objective of this work was to determine the annual pattern of development of
strongylid eggs to infective larvae (L3) on pasture, and relates environmental factors on their
abundance. On a series o f pasture plots, 2 kg pats of bovine faeces containing known
numbers o f strongylid (Haemonchus, Cooperia, Oesophagostomuni and Trichostrortgylus)
eggs were deposited at intervals of 4 weeks from July 1995 to June 1996. The plots were
sampled every two weeks after contamination and infective larvae identified and counted.
Larvae o f all genera developed throughout the year but the pats exposed during the rainy
seasons yielded abundant larvae on to herbage. Irrespective o f season o f deposition o f the
pats, larval counts were found in larger numbers from 2 to 6 weeks after deposition and
generally declined to below detectable levels within 12 to 16 weeks o f contamination. The
comparatively short survival times noted in this experiment may present opportunities for
manipulation o f Gl nematode population dynamics in the tropical environment o f Kenya.
f) Control studies using morantel sustained release trilaminate bolus
The aim of this 10-month study was to determine the comparative efficacy o f morantel
sustained release trilaminate (MSRT) bolus and conventional anthelmintic treatments against
GI nematodes o f cattle under field conditions. Forty weaner calves were randomly divided
into 4 groups o f 10 calves each and grazed from March to December 1993 on adjacent.
xxxi
similarly contaminated paddocks. Group 1 calves (T -l) served as untreated controls while
group 2 calves (T-2) were dosed at turnout with MSRT boluses designed to release morantel
tartrate continously for 90 days. Group 3 calves (T-3) were drenched with albendazole on
day zero, and group 4 calves (T-4) on day zero and day 14, respectively. The efficacy of
these dosings was assessed by comparison o f weight gains, clinical status o f the animals and
parasitological data (faecal worm egg counts, herbage larval counts, worm counts from
tracers and set-stocked trial calves, determination o f haematological parameters and
pepsinogen levels). Faecal egg counts from the treated groups (T-2, T-3 and T-4) remained
significantly (P < 0 .0 5 ) lower than counts from control T -l calves for the first three months
post-treatment; notably, egg counts were reduced by 100% 28 days after treatment in T-2 and
T-4 groups and by 97% in T-3 treated calves. Egg counts in T-2 calves remained
significantly (P < 0 .0 5 ) lower than counts from T -l, T-3 and T-4 calves up to trial
termination. The use o f MSRT boluses resulted in a reduction o f 92% ( P < 0.001) in the
number o f GI nematodes in set-stocked calves at the end of the study and a 55 to 85.7%
reduction in herbage larval infectivity as reflected in lowered parasite burdens in tracer
calves. At the trial termination, the control (T -l) calves had gained on average ( ± S .D ) 59.4
± 4 .8 kg (200 ± 7.4 g day'1) and the T-2 ones on average 128.6 ± 10.5 kg (530 ± 13.1
g day'1). T-3 calves gained on average 52.5 ± 5.7 kg (170 ± 6 .9 g day'1) and T-4 ones on
average 82.6 ± 6.3 kg (270 ± 9.1 g day'1).
g) Duddingtonia flagrans: a study on herbage infectivity
The present investigation, conducted in 1994 was designed to determine the
overwintering residual grass infectivity in a pasture previously grazed by D. flagrans treated
and untreated calves. Herbage infectivity was monitored by use of tracer calves over a period
x x x ii
of 7 weeks. The experimental pasture had previously been divided into two comparable plots,
1 and 2 which were grazed by two sets o f calves, groups 1 and 2 respectively. Group 1
calves had been fed fungal material (D. flagrans in barley grains) once daily over a three
month period from turnout. The controls, group 2 calves received barley grains as a placebo.
In the present experiment, 10 parasite naive male Jersey calves aged 6 months were randomly
allocated to either an experimental group (B) or a control group (A). Each group was grazed
on adjacent plots, group B on the previous group 1 plot and group A on the previous group
2 plot for 4 weeks before being housed for three weeks prior to slaughter upon termination
of the experiment. Body weights were recorded and individual faecal samples taken at regular
intervals throughout the experimental period. Pasture nematode contamination was monitored
by larval counts on herbage and worm counts o f tracer calves grazed on each plot. The
results demonstrated that fungal treatment did not significantly lower the overwintering larval
population in plot B compared to plot A as tracer calves grazing Plot A acquired worm
burdens roughly comparable, or perhaps slighly lower, than those o f the plot B tracers.
h) Duddingtonia flagrans: fungal dose-nematode larvae interactions
The present esperiment was designed to quantify the influence of egg counts and
fungal dose levels on the nematode-trapping capability o f D. flagrans against free-living
stages o f GI nematodes o f cattle. In an in-vitro experiment, the interactions between free-
living stages of four bovine GI parasites and the nematode-trapping fungus D. flagrans were
evaluated using a faecal culture assay. Faeces were collected from donor calves infected with
monocultures of H. placei, T. axei, C. oncophora and O. radialum, and the number of
parasitic eggs per gram of faeces (epg) were determined. The assay consisted o f four faecal
worm egg levels: low (40-50 epg), medium (200-280 epg), high (600-680 epg) and very high
x x x iii
(1288-4800) and four fungal concentrations: 0 (controls), 1000, 5000 and 25000
chlamydospores g 1 faeces. The number of infective third stage larvae (L3) which developed
in faecal cultures were determined after cultures had been incubated for two weeks in
darkness at 25°C and 95% relative humidity. Results showed that the nematode-trapping
capability o f D. flagrans was dependent on the fungal concentration and number o f eggs in
the faecal cultures. Thus, percent reductions increased with corresponding increase in fungal
concentration and epg levels in all the four species of parasitic nematodes examined. The
average trapping efficacy o f D. flagrans at the medium epg level exceeded 80% for //.
placei, T. axei and C. oncophora compared to 53% for O. radiatum at the 1000 and 5000
fungal spore concentrations.
In conclusion, the results of this study suggest that GI nematode infections, especially
haemonchosis, are major constraints to the health o f young dairy cattle o f the study area. To
increase the productivity o f cattle, helminthosis control should be based on epidemiological
observations and should not rely on anthelmintics only. Alternative ways of control, such as
biological control of free-living stages of strongylid nematodes o f cattle by using
nematophagous fungi merit serious consideration.

GENERAL INTRODUCTION
There is a growing recognition of the contribution of livestock and their products to
the national economies as well as the socio-economic development and welfare o f rural
communities in developing countries. This is evident from the research and development
programmes o f a number o f international agencies and organizations such as European
Union, the International Livestock Research Institute (ILRI), the Food and Agriculture
Organisation (FAO) of the United Nations and the United Nations Environment Programme
(UNEP), which are aimed at the improvement o f the health and productivity o f livestock in
Kenya. However, in the animal health sector, these programmes, over the years, have been
concerned largely with the major epidemics caused by viral and bacterial pathogens such as
rinderpest, foot and mouth disease and contagious bovine pleuropneumonia. The only
parasitic diseases which have received worthy attention are trypanosomosis and East Coast
Fever.
Until recently, there appeared to be no comparable nationally or internationally
sponsored or coordinated programmes on helminth diseases and infections o f farm animals
in Kenya, probably because, under field conditions, helminth diseases are characteristically
insidious and subclinical or chronic in nature and therefore attract relatively little attention.
This ignores the fact that they are probably the most prevalent endemic parasitoses o f all
classes o f livestock and that the hidden production losses which they cause can be very
considerable, even in subclinically infected animals (Chiejina, 1991). These losses arise
primarily through loss o f draught power, poor meat and milk yield, carcass and offal
condemnation and impaired reproductive efficiency (Fabiyi, 1987; Chiejna, 1991). In Kenya
recent observations in situations of subclinical infections, have shown that growth can be
depressed by 25-50%, fecundity by 30% and milk yields by up to 30% (Carles, 1992).
1
Gastrointestinal (G l) nematode parasitism is one o f the major animal health problems
facing the ruminant livestock enterprises in Kenya (Mango et al., 1974; Allonby and
Urquhart, 1973). These enterprises are based predominantly on year-round grazing of
pastures on which infective larvae are always potentially available, albeit with seasonal
fluctuations dependent mainly on rainfall. It is widely believed by farmers that nematode
parasites are more important to the sheep and goat industry than to the cattle industry
(Barger, 1993a). This is probably a consequence of the ability o f pathogenic species such as
Haemonchus contortus and, to a lesser extent, Trichostrongylus colubriformis to cause the
death o f large numbers o f small ruminants, whereas death of cattle attributable to nematode
infection are less common. However, nematode infections in both cattle and small ruminants
cause similar reduction in weight gains (Barger, 1982; Holmes, 1994).
It is generally believed that o f all the internal parasites of cattle, the GI nematodes are
of the most serious economic consequence. This is based on the overall numbers o f worms,
numbers o f genera and species present, general levels o f pathogenicity and widespread
distribution (Gibbs and Herd, 1986; Nansen, 1987). The most common nematodes present
in cattle on pasture in the tropics include H. placei, T. axei, Cooperia spp., (C. pectinata,
C. punctata and C. onchophora) and Oesophagostomum radiation (Round, 1962; Winks et
al., 1983; Chiejna, 1994). O f these, H. placei and O. radiatum are recognized as being the
most pathogenic and economically important parasites of cattle in the tropics (Roberts et al..
1951; Hutchinson et al., 1980; Waruiru et al., 1993a).
The epidemiology o f GI parasitism in grazing cattle has been well documented in
several countries, especially in Europe (Armour, 1980; Nansen et. a l., 1990), North America
(Williams et al, 1987; Rickard and Zimmerman, 1992), South America (Benitez-Usher et al.,
1984; Bianchin and Honer, 1987) and Australia (Henderson and Kelly, 1978; Winks et al..
2
1983). This has lead to the improvement in control measures and a decrease in production
losses (Michel, 1985). In contrast, little knowledge is available on the epidemiology and
severity o f bovine strongylosis in Kenya (Straat, 1979). The literature, especially on the
ecology o f the free-living stages of the nematodes concerned, is scarce and concentrates
mainly on sheep (Dinnik and Dinnik, 1958; 1961; Allonby and Urquhart, 1973) and no
systematic epidemiological studies have been undertaken on bovine GI nematodes in Kenya.
Thus, extensive applied research on the epidemiology of GI nematode infections is absolutely
necessary as this information is important in the formulation o f parasite control strategies.
As opposed to other infections, helminthosis is closely associated with the local soil,
climate and management systems. Thus, external larval development and survival are
dependent on specific ecological conditions and/or existence of vectors and intermediate hosts
which are dependent on characteristic geoclimatographic factors. This implies that the impact
and character o f the infections vary widely from locality to locality. Although very little
work has been done on the ecology and bionomics of nematodes in Kenya, Round (1962)
stated that there is such a wide diversity of environmental conditions in Kenya that studies
carried out in one area would almost undoubtedly not be applicable to other areas.
Therefore, to develop strategic preventive measures against nematodosis, it is necessary to
have a fairly precise knowledge of the seasonal dynamics o f nematode infections of an area
(Arambulo and Moran, 1981), and one should ideally analyze the representative local herd
situation (Nansen, 1991).
Further information is needed on the effect o f the environment on the ecology o f the
free-living stages o f cattle parasitic nematodes, as a better understanding o f the characteristics
of pasture stages o f these parasites may lead to the development o f alternative strategies of
control aimed at improved managerial practices, or directly at free-living stages on pasture
3
(Krecek et al., 1991; Gronvold et al., 1993a).
The effects o f environmental conditions on the development of cattle nematodes
infective larvae (L,) have been studied under wet tropical conditions in Australia (Fabiyi et
al., 1988), in wet and dry seasons in Nigeria (Fakae and Chiejina, 1988), and in South
Africa both under semi-arid conditions (Reinecke, 1960) and on irrigated pasture (Horak and
Louw, 1978). Gatongi et al. (1988) reported on the influence o f weather on the bionomics
of L, of cattle in Kenya. While many o f these investigators used tracer calves to assess larval
abundance on pasture, those with a focus on the microhabitat and pasture larval counts are
few in number (Krecek et al., 1991).
The main constraint on larval development and survival o f ruminant nematodes, is
availability of moisture inside the faeces (Berbigier et al., 1990) and herbage (Gruner et al.,
1989; Besier and Dunsmore, 1993). Since weather conditions vary from place to place,
studies o f the bionomics o f the larvae under local conditions are needed in planning locally
applicable control strategies (Okon and Enyenihi, 1977).
Presently the primary factor for the control of parasitic strongylids is by curative,
strategic or tactical treatment o f the animals with anthelmintics (Van Wyk, 1990a). The
implementation o f different pasture management practices is another way o f reducing the
effects o f the parasite infection (Van Wyk, 1990b). However, in the tropics, these methods
are limited by the high costs of anthelmintics, their uncertain availability, increasing
frequency o f drug resistance (particularly in small ruminants) and limited scope in many
communal pastoral systems for controlled grazing.
In Kenya, anthelmintics are used on a considerable scale in the more important
livestock producing areas like dairy farming (Kinoti et al., 1994). Outside these areas, they
are utilized in intensive livestock operations such as government farms and large commercial
4
enterprises. Use o f anthelmintics in small and nomadic production systems is limited and is
based on rare haphazard anthelmintic treatments with no account of epidemiological
principles (Mbaria et al., 1995).
The benefits o f the strategic use o f anthelmintics to control parasitic nematode
infections in ruminants are well known (McKeller, 1988) and in cattle especially these
regimes have been refined into a variety of systems of intraruminal boluses based on either
continuous or intermittent release of the anthelmintic drug. The intermittent release system
has been designed to release therapeutic doses o f the drug at intervals close to the prepatent
period of the parasites. However, the continuous release devices releases a subtherapeutic
dose and relies on the persistence o f the drug in the environment o f the parasites to deter
their establishment in the host.
With respect to continuous release devices, the release profile o f the drug is
particularly important in relation to the likelihood that the device will increase selection for
resistant parasites (Donald, 1985). The preferable release profile for a continuous release
device is a constant level o f anthelmintic release followed by a rapid decline once the device
is exhausted, avoiding the potential for underdosing with its associated implications for the
development of resistance (Anderson, 1985). In the light of these possibilities, it is important
that there is detailed study o f those features o f controlled release technology that have a
direct bearing upon the development o f resistance, i.e., efficacy, release rate characteristics
and duration of release (Bell et al., 1996). The FAO recommended high priority be given
to maintaining the efficacy and availability o f low-cost parasiticides, and more research on
livestock production systems in developing countries that apply strategic drug management
be undertaken (FAO, 1991).
Anthelmintics will continue to constitute a major control measure, but it is unlikely
5
that there will be any acceleration in the rate o f commercial release of new compounds.
However, ongoing modifications and new formulations o f existing anthelmintics will continue
to be produced, and implementation at the farm level o f the proper use of anthelmintics and
other control measures will be one o f the important tasks o f the coming century. Until now,
the development o f anthelmintic resistance in cattle has been negligible, but it may possibly
pose a potential risk over the coming decades. With regard to some new anthelmintics that
have environmental concerns related to their faecal excretion (Herd et al., 1993; Strong et
al., 1996), this should be carefully examined in the future.
A general review o f chemical control o f livestock parasites (Strong and Wall, 1990)
suggests chemical and non-chemical control be integrated and more specific reviews of
anthelmintic resistance reach similar conclusions (Waller, 1994). Control in the form of
vaccination or biological control by microfungi or others would be attractive alternatives that
should be given a high research priority (Nansen, 1993). Barger (1993a) suggestssustainable
control will be achieved by combined use o f drugs, vaccines, biological control agents and
genetically resistant hosts.
One option of a non-chemical control method o f ruminant parasitic nematodes is
biological control, which is operationally defined as the action o f natural enemies which
maintain a host population at levels lower than would occur in the absence o f the enemies
(Waller and Faedo, 1996). Biological control does not assume to be a substitute for
chemotherapy where the expectation, if not the reality, is that parasites may be eradicated
by the frequent use o f drugs with efficacies approaching 100%. Biological control agents
rarely eliminate the target organism, but reduce the numbers to acceptable levels and
maintain a balance between the pathogen and the antagonist. In contrast also to chemical
control of nematode parasites which are directed entirely at the parasitic stage within the
6
host, biological control almost certainly will be focused on the free-living stages on pasture.
Within this environment the pre-parasitic stages o f nematodes are subjected to a variety of
abiotic (temperature, humidity and oxygen) and biotic (coprophilic fauna and flora) factors
which profoundly influence their development and survival. Among the vast assemblage of
biota which may exploit nematodes as nutrient source are bacteria, protozoa, and
invertebrates such as collembola, mites and predatory soil nematodes (Waller, 1997a).
However, the most important amongst these, and from which may emerge a biological
control agent o f the free-living stages o f nematode parasites o f livestock, are the
nematophagous fungi (Waller and Larsen, 1993; Gronvold et al., 1993a).
Nematophagous fungi are a diverse and ubiquitous group o f microfungi which exploit
nematodes either as their primary source of nutrients, or opportunistically to supplement their
normal saprophytic existence. They belong to the class Deuteromycetes, or Fungi Imperfecti,
and include those which are trapping predators, endozoic parasites or egg parasites of
nematodes (Barron, 1977). Considerable progress has been made, in both laboratory and plot
studies, in defining the nematode-destroying capabilities o f a range o f fungal species, but
interest is now turning to the ability o f these organisms to survive gut passage in ruminants.
This is because it is recognized that to become a feasible control proposition, fungi need to
withstand the harsh environmental condition o f the gut so that they can be deployed in feed
additives or intraruminal sustained release devices (Waller, 1997b). Certain fungal species
selected because o f their superior nematode-destroying capabilities in-vitro have also been
shown to be capable o f surviving ruminant gut passage and exert a significant nematode
killing effect in dung (Larsen et al., 1991; 1992; Waller et al., 1994). By reducing the
number o f the infective stage o f the parasitic nematodes to a minimum, the transmission of
the parasite to new hosts is expected to be restricted to levels where production losses can
7
be avoided (Larsen, 1991).
Recently, workers in Denmark have shown that daily feeding o f yearling calves with
microfungus Duddingtonia flagrans during the first 2 months o f the season led to a lowered
herbage infectivity and a reduced acquisition o f Ostertagia spp. and Cooperia spp. later in
the season and in addition, the procedure delayed the onset o f clinical disease (Larsen et al.,
1995a). Simulation studies o f sheep nematodes also suggest that the use of fungi is a viable
alternative to chemotherapy (Barnes et al., 1995).
Biological control has several advantages over other non-chemotherapeutic means.
Firstly, it will be applicable to a wider range o f helminth parasites both between and within
species o f domestic animals. Secondly, it will provide the opportunity for farmers to
capitalise on the increasing public concern about chemical residues in animal products and
in the environment (Strong, 1993). Thirdly, it is also difficult to envisage the development
of resistance mechanisms as has occurred with anthelmintic drugs (Waller and Larsen, 1993;
Prichard, 1994).
The Kenyan Ministry o f Agriculture, Livestock Development and Marketing estimates
the present national livestock population to be composed of ten and three million head of
indigenous and grade cattle, respectively; 19 million sheep and goats, 22 million birds,
110.000 pigs, 900,000 camels and 250,000 rabbits (KARI, 1994). There are 1.5 million and
200.000 traditional and Kenya top bar beehives, respectively. The sector produces a total of
2.5 billion kg o f milk; 310,000 tonnes o f meat, a billion eggs, 20,000 tonnes o f honey, 2,000
tonnes o f bees wax and 857 tonnes o f greasy wool clip. Besides these direct products, the
livestock sector produces hides and skins, manure which is used to improve soil fertility for
better harvests, draught power for haulage and land preparation, conversion o f crop waste
and by-products into useful economic products (KARI, 1994).
8
The above national production levels from the livestock sector need to be increased
considerably if the policy o f broad self-sufficiency in food supplies is to be attained and
sustained in the face of an increasing human population. Moreover, the demand for livestock
products tends to have a higher income elasticity and will also increase in response to higher
levels of average health education and the knowledge of the role o f livestock food products
in balanced nutrition of growing children and nursing mothers (KARI, 1994). To achieve an
increase in production, there is a need to improve both management practices and the control
of production-limiting diseases like helminthosis. However, to promote sound management
practices (i.e. pasture preparation, stocking rate, strategic drenching etc.) requires a thorough
knowledge of the epidemiology of the parasites (Murrell, 1994).
Between January 1985 and December 1995, the Veterinary Clinical Services in
Kiambu District treated an average o f 2916 GI helminthosis cases per month in cattle
compared to 1713 mastitis and 906 tick-borne disease cases. During the same period, an
average o f 1407 pimply gut cases and 4723 cases o f liver condemnation due to liver flukes
were reported annually in various abattoirs in the district (Anonymous, 1996). These statistics
show in a broad view the significance o f GI parasites in animal health in this area.
The aim o f the present study was to define the seasonal prevalence and importance
of GI nematodes in weaner-yearling dairy cattle and to further elucidate epidemiological
events o f these parasites over a four year period. This study was based on the following
hypotheses:
1. That nematode infections of the GI tract o f young cattle is widespread in the area of
study and is the cause o f considerable economic loss which is derived primarily
from the failure o f parasitised cattle to grow at a satisfactory rate.
9
2. That climatic factors like rainfall, temperature and relative humidity have a significant
influence on the development o f GI nematode larvae on pasture and good
knowledge o f these factors is essential for planning effective control strategies.
3. That a sustained release anthelmintic bolus could be highly effective in controlling
GI nematodes of set-stocked yearling cattle in the tropical environment of Kenya.
4. That nematode-destroying capabilities o f the microfungus D. flagrans may be
enhanced by increasing fungal concentration and nematode larval densities.
The above hypotheses were tested with the aim of achieving the following objectives:
1. To determine the identity, prevalence and intensity of GI nematodes in dairy cattle
in Kiambu District o f Kenya in relation to seasonal weather factors, sex, age structure
o f the host and management practices on the farms.
2. To determine seasonal patterns o f development and survival o f Haemonchus,
Trichostrongylus, Cooperia and Oesophagostomum eggs to infective larvae (L,) on
pasture and relate environmental factors to their abundance and availability.
3. To assess and compare the efficacy of morantel sustained release trilaminate bolus and
conventional anthelmintic treatment in controlling GI parasitism in naturally infected
grazing yearlings.
4. To quantify the effects of D. flagrans on free-living stages o f H. placei, T. axei, C.
oncophora and O. radiatum in faecal cultures. The effect o f increasing doses of
nematode eggs admixed to the faecal cultures, was also examined.
10
-C hapter 2-
LITERATURE REVIEW
2.1 Farming systems and livestock populations in Kenya
One o f the most important goals for Kenya as a developing country is to become self-
sufficient in food production which is clearly expressed in the National Food Policy Paper
No. 4 o f 1981 and the sessional paper No. 1 o f 1986 (Anonymous, 1986). Ruminants play
an important role in the agricultural sector in Kenya, contributing approximately 20% o f the
total agricultural production. Only 25% of land in Kenya is suitable for arable fanning and
the current demand for meat and milk is estimated to exceed production by approximately
32% and 23%, respectively (Wafula et a l., 1994). With the rapid increase in human
population, it is becoming increasingly important to maximise agricultural production through
improved management practices and control o f production-limiting diseases such as
helminthosis o f domestic ruminants.
Domestic animals are found in all parts o f the country often as mixed species on any
individual farm. Cattle, sheep, goats, pigs and poultry are kept under various production
systems to produce meat, milk and eggs as the main economic products. Other animals which
are farmed include camels, rabbits, donkeys and bees. The livestock component o f a farm
provides food for subsistence and/or animal products for sale to generate farm income. At
the national level, the livestock industry is expected to contribute towards the attainment of
the natural goals and objectives including production o f sufficient products to meet the
domestic demand, creation o f gainfall employment and utilization o f national productive
resources of land, capital and entrepreneurship efficiently to warrant the continued
a v a ila b ility o f these r e s o u r c e s fo r liv e sto c k production. The latter process should be carried
11
out on environment friendly and sustainable basis. The livestock sector thus has an important
role to play in development o f the rural areas. Its economic importance varies considerably
depending on the alternative enterprises competing for land use and availability of other non
land production factors. Thus, livestock constitutes the preeminent source o f livelihood for
communities in the range and arid lands; accounts for more than 60% o f household revenue
in dry farming areas and a significant source o f income for mixed small scale and other
farms (KARI, 1994).
At the macro level, livestock industry contributes a tenth o f the recorded national
gross domestic product and provides a half o f the employment in the agricultural sector. It
has been estimated that nearly 48% o f the land used for food crop and livestock production
is accounted for by dairying in wetter districts (KARI, 1994).
2.1.1 Farming systems
Most statistics on livestock populations published by the Ministry o f Agriculture,
Livestock Development and Marketing are aggregated by district, which allows a broad
subdivision into production systems. It is hypothesised that production goals o f livestock
owners differ and influence their offtake strategies which depend on the functions that
livestock fulfil. Pastoralists, who almost entirely rely on subsistence and cash from their
herds, have sales policies that deviate from small-scale dairy farmers in the highlands and
from large-scale ranchers in the semi-arid rangelands. Therefore, a simple classification in
four major producers groups was adopted consisting of pastoralists, low-input smallholder
mixed farmers and small-scale dairy producers; large-scale producers (either engaged in beef,
milk production or both) are grouped under the umbrella term o f ranching (de Leeuw and
Reynolds, 1994).
12
Although few o f the districts can be entirely allocated to one single system of
production, they have been grouped according to the dominant system as shown in Table 2.1.
The four major groups roughly coincide with the agro-ecological zonation from arid to
highland environments. As infrastructures, distance from and access to markets vary,
geographical subdivision created further subgroups.
The rangelands o f Kenya are areas o f marginal agricultural potential which comprise
about 80% of the country’s land surface (Field, 1986). Using the percentage distribution of
Too et al. (1986) the range population of cattle, sheep, goats and camels is about 76% o f the
total in the country. The Maasai, Rendille, Samburu and Turkana who are the principal
inhabitants of this zone, practice pastoralism as their main activity. The pastoral sector plays
an important role in the national economy through provision o f livestock and their products
to the heavily populated crop/livestock farming systems o f the high potential areas. Mbogoh
(1984) and ILCA (1984) have analysed and discussed meat and milk production from the
Kenyan rangelands, including economic indices o f productivity and experiences with group
ranches. Despite suggestions for improvements, productivity has remained low in the
range/livestock ecosystem. In 1983 the offtake rate from pastoral lands was estimated at 12%
from about 3.8 million zebu cattle (Anonymous, 1983). Reasons for this include a harsh
environment that is as yet little understood (Carles, 1986) and a complicated social and
cultural organization that is often sceptical o f the advantages of new innovations (Maranga,
1990). Kenya’s high population growth rate o f 4% per annum (Anonymous, 1986) has also
resulted in increased migration of mixed farmers from arable to rangeland districts especially
into the dry season grazing reserve areas (Abate et al., 1995). Considerations of the subject
are many and recent ones include those of Amuyunzu (1990), Maranga (1990) and Njanja
(1991).
13
Table 2.1: Livestock populations by zones and production system in 1990
Zone Production system Population ( ‘000) Percent increase”
Cattle Sheep Goats TLUa Cattle
Arid 1.1 Pastoralists, 1002 1499 1398 0.18 82
Northeast
1.2 Pastoralists,
Northwest 2045 3011 1342 0.38
59
Semi-arid 1.3 (Agro)-pastoralists 1666 2778 1689 0.25 55
Subtotal 4713 7288 4429 0.27 65
Semi-arid and 2. Small-holdings
subhumid 2.1 East and ranching 409 1608 1281 0.16 21
2.2 West 1434 1383 2695 0.10 53
3. Small-holding
(low input/
dairying) and
ranching 750 1380 998 0.21 45
Subtotal 2593 4371 4974 0.16 40
Highlands 4. Small- and large-
scale dairying and
ranching 1575 3292 781 0.1 36
Total 8881 14951 10184 0.20 50
Sources: Sloane (1986); Reynolds (1993). aTLU = Tropical livestock unit o f 250 kg: zebu cattle 0.7 TLU/head; dairy cows 1.0;
hair sheep and goats 0.1; wool sheep 0.15 TLU/head. b1990-l versus 1981-83.
Aggregation of districts: 1.1: Mandera, Wajir, Garrisa, Tana River, Lamu; 1.2: Isiolo, Marsabit, Samburu, Turkana; 1.3: Kajiado,
Narok, 2.1: Kilifi, Kwale, Taita Taveta, Kitui, Machakos; 2.2: Laikipia, West Pokot, Western and Nyanza provinces; 3: Meru,
Embu, Baringo, Marakwet; 4: Central Province, Kericho, Nandi, Uasin Gishu, Trans Nzoia.
In Table 2 .1 , populations have been separated into cattle, sheep and goats, excluding
camels, which are rarely traded outside their arid realm. Three pastoralist groups are
distinguished; two represent the arid zone in the north, while the two Maasai-dominated
districts constitute the third group. In 1990, this amalgam o f pastoralists owned (or managed)
one third o f Kenyan cattle and more than half of its small ruminants (de Leeuw and
Reynolds, 1994).
The second major grouping consists predominantly o f small-scale mixed farmers
engaged in low input livestock enterprises in the wetter parts o f the semi-arid zone
intermingling with larger-scale commercial and cooperative ranches in the drier parts. Over
35% o f the cattle are owned by this group, most o f which are zebu. In the better-watered
areas, a third group o f farmers predominates, keeping either zebus or grade cattle, but often
both in mixed herds (Tessema et al., 1989). In these districts (Meru etc. see Table 2.1),
grade cattle in small-scale dairy operations increased from 0.4 million in 1981-83 to 0.7
million in 1990, or about 40% of the total. Due to the importance o f cattle for dairying and
as oxen for traction, small ruminants are less numerous, constituting only 14% of the overall
livestock mass and about one third o f the national flock.
The fourth grouping joins together all production systems associated with the
highlands and is characterized by a predominance o f grade cattle, most o f which are used for
intensive milk production; overall, they represent three quarters o f the total dairy herd,
ranging from 90% of all cattle in Central Province to 60% in Nakuru District. Small
ruminants are unimportant, but in contrast to most other production systems, sheep are more
numerous than goats.
In Kenya, smallholder dairy farms account for between 75 and 90% of all milk
produced (Mbogoh, 1984; Brumby and Gryseels, 1985). However, most o f the increased
15
production in the smallholder sector has been due to increased use o f land and livestock
resources rather than from higher individual cow productivity (Walshe et al., 1991). A
number o f pressures (including rapid population growth, and limited land resources) already
have pushed the smallholder to more intensive dairy production (Christiansen, 1989; Walshe
et a l., 1991). In Kenya, approximately 10% o f cattle are stall-fed for the greater part o f the
year (Goldson and Ndeda, 1985). Such intensification will require improved management and
increased resources per cow . An important step in evaluating potential development
alternatives is to identify the major constraints (including helminthosis) and opportunities for
increased productivity on smallholder dairies (Gitau et al., 1994a). Major disease constraints
in smallholder sector are diarrhoea, mastitis and helminth infections (Anonymous, 1993). A
recent study conducted in Kiambu District by Gitau and others (1994b) showed that diarrhoea
was the most common cause o f calf morbidity and mortality o f 27% and 22% per year,
respectively.
2.1.2 Population dynamics
The census data for 1990-91 compiled by Ministry o f Agriculture, Livestock
Development and Marketing (Anonymous, 1993) have been compared with those from 1981-
83 as summarized by Sloane (1986). In the aggregate, cattle numbers rose from 10.3 million
to 13.2 million ( + 28%) as compared to a 50% increase in small ruminants climbing from
13.8 m illion to 20.8 million. Growth varied between systems: the most rapid growth
occurred in the northern districts; where cattle increased from 1.8 million to 2.8 million
(+64% ) and small stock from 4.5 to 7 .6 million ( + 66%); thus 36% o f all sheep and goats
are kept by pastoralists in the north. Upward changes in the other systems have been less
dramatic and diminish inversely with land potential and population diversity, being lowest
16
in the highlands. However, in all the systems there appears to be an overall trend o f faster
growth in smallstock than in cattle numbers (Table 2.1).
As a result o f these shifts between species, the composition o f the overall livestock
mass has changed in favour o f small ruminants, from 15% to 17% o f the total biomass. This
change is lower than that suggested by the population data, because, although cattle numbers
increased less, the shift from zebu to grade cattle boosted mass per head.
2.1.3 Offtake estimates by enterprise
Except during the 1984/85 drought, Kenya has been self-sufficient in milk; during the
drought about 16,000 metric tonnes (MT) of skim milk powder and 2,500 MT of butter oil
had to be imported (Mbogoh and Ochuonyo, 1992). During 1980-87, domestic milk output
rose by 2.7% (Mbogoh and Ochuonyo, 1992) increasing to 4.2% during 1988-91 (Reynolds,
1993). Reynolds (1993) estimated an overall milk offtake for human consumption o f 1.2
million MT per year from 13 million cattle, 90% o f which was produced by grade dairy
cattle. Muriuki (1992) and Mbogoh and Ochuonyo (1992) quoted total milk yields o f the
cattle herd o f 2,0 million MT for 1990 and 1.6 million MT for 1988. In 1990, 0.8 million
MT o f milk was marketed, satisfying an estimated demand of 730,000 MT for liquid milk
(Reynolds (1993). The output o f meat from the national herd and flock is less transparent
than that o f milk (de Leeuw and Reynolds, 1994).
Upton (1990) divided the Kenyan livestock sector into six major groups: three for
cattle (small and large scale dairy, and traditional systems) and three for small ruminants
(wool and traditional sheep, goat production). For each, output o f milk and meat was
presented and when multiplied with the estimated population the monetary contribution to the
Kenyan economy was calculated. Total output was close to 20 billion Kenya shillings per
17
year, 60% of which was generated by dairy products. Sloane (1986) distinguished four major
systems: dairying and pastoral enterprises for cattle, sheep and goats. However, output of
each was assessed at three levels o f inputs and management intensity.
Both Sloane (1986) and Upton (1990) provided a useful segregation of offtake by
sex/age groups as determined by enterprise production goals. The dairy sector produces
mainly culled females as a by-product, which are sold for slaughter. Surplus grade heifers
destined for sale, may not enter the terminal market; instead, they remain in the system as
milk cows until culled. The same happens to male stock; they are either slaughtered as young
calves or sold for further growing out elsewhere or to be used as traction oxen in mixed
farming systems for up to 10 years o f age before being sold for slaughter. Offtake rates
expressed as percentage o f total mass varied because of different culling rates o f females ( 11 -
23%) and weights (300-400 kg). The offtake documented by Reynolds (1993) of 4.2% was
more conservative than that o f Upton (1990) o f 6.1 % (Table 2 .2 ).
Of equal interest to overall marketing are the mixed systems, which produces both
milk (mainly for subsistence) and animals for sale. These producers keep mainly zebus, but
at the upper end o f the input level range may also have grade cattle. These enterprises
produce immature males and heifers, bulls for breeding, but only steers and culled females
for slaughter. It is assumed that most of the culled females will enter local trade circuits
ending up in abattoirs and butcheries, representing mostly unrecorded slaughter. Due to high
population densities combined with a large urban sector dispersed in small and medium size
towns, local demand is likely to absorb most o f this supply.
Projections for dairy herds are summarized in Table 2.2. Culled females produce all
potential meat which, expressed as kg liveweight per head, increases with the level o f milk
yield per cow, as intensification of dairy production usually involves higher culling rates and
18
Table 2.2: Herd structures, and herd offtake of dairy and beef herds at three levels of inputs
Dairv herds input levels Beef herd input levels

Parameters Low Medium High Low Medium High
Herd structure (%)
Cows 48 42 52 46 43 35
Calves 34 15 22 15 17 18
Heifers 18 38 26 23 21 22
Steers/males - 2 - 10 13 20
Bulls - 3 - 6 5 5
Calving % 72 86 85 50 50 67
Milk offtake 1/cow/yr 1040 1740 2020 89 97 116
Offtake, cows
Culling % 11 25 17 7 9 14
% LW o f herd 7.0 12.2 10.3 4.4 5.5 7.1
% o f total N in herd 5.3 10.5 8.8 3.1 3.8 5.0
Offtake, males
% LW o f herd - - - 5.3 7.4 11.2
% o f total N in herd - - - 3.1 4.3 6.4
Total, kg LW/herd 15.6 30.6 35.2 17.0 22.6 30.2
Source: Adapted from Sloane (1986) and Upton (1990).

heavier cow s because o f upgrading to pure exotic breeds. The output o f 30-35 kg liveweight
per head is higher than the projections given by Reynolds (1993) o f 20 kg liveweight per
head.
In beef systems the output range is similar to that o f dairy herds, despite the fact that
both culled females and mature males contribute to sales. The lower outputs represent
subsistence-oriented herds o f pastoralists, containing mainly females (up to 82% of the total),
whereas high outputs relate to more commercially managed herds aimed at marketing male
stock and showing herd structures similar to Maasai herds (de Leeuw and Reynolds, 1994);
these herds produce closest to the level projected by Reynolds (1993) (15 % offtake 125 kg
carcass or 3 7 .7 kg liveweight per head) and by Upton’s (1990) estimate o f 35 kg liveweight
per head o f traditionally managed zebu cattle. The unresolved problem of how to partition
beef production systems according to the projected offtake levels remains.
U sing the offtake parameters by Reynolds (1993), ruminant meat output in 1990-1
totalled 2 8 2 ,0 0 0 MT, 68% being supplied by zebu cattle, 11 % by grade cattle and 21 % by
small ruminants. Adding illegal imports o f cattle at 100,000 head (or 12,500 MT meat) and
the 18,500 MT from poultry and pigs, the total supply amounted to 313,300 MT or 11.8 kg
per caput for a human population of 26.5 million people; this output is 8 % above the earlier
consumption rate estimated by ILCA (1993) for 1985-87.
2.2 Epidemiology o f helminth infections o f ruminants in the tropics
Helminthosis remains one of the world’s most prevalent and economically important
parasitosis o f man and his livestock. This is particularly the case in the developing countries,
many o f which lie within the tropics, where, for most part, systems o f livestock production,
environmental and socio-economic conditions are highly conducive for the development.
20
maintenance and transmission o f infection (Chiejina, 1994). Helminth infections in ruminants
are characteristically chronic and insidious in nature and in East Africa, in particular, have
attracted very little attention, including research funds, when compared with viral, bacterial
# and som e protozoal diseases (FAO, 1991). This is inspite of the fact that they undoubtedly
exert a heavy toll on the health and productivity of this important livestock resource, with
obvious implications for the rural and national economies o f the African continent (Fabiyi,
1987; Carles, 1992).
Parasites, along with viral, fungal, and bacterial diseases, are major contributors of
economic losses in developing countries (Murrell, 1994). In Africa, for example,
trypanosomosis causes an estimated annual loss o f US$ 5 billion (excluding milk and hide
losses) and theileriosis kills a million cattle yearly across eastern and southern Africa, and
causes losses worth more than US$ 165 million (Murray and Gray, 1984; S.K. Mbogo,
personal communication, 1996). Although less well publicized, toxoplasmosis is responsible
for considerable abortion and mortality among newborn lambs and pigs in developing
countries (Dubey and Kirkbride, 1989).
The problem o f helminth infections in animals, as in humans, is o f paramount
importance in the tropics. Bovine cysticercosis in Africa may account for more than a billion
US$ in lost revenue from beef production, especially to the export sector (Murrell, 1991).
In addition, diseases caused by liver and stomach flukes result in major economic losses in
cattle, buffaloes, sheep and goats amounting to more than US$ 3 billion per year (FAO,
1994). In Kenya, annual losses due to fasciolosis in cattle, sheep and goats have been
estimated at aproximately US$ 326 million (Agricultural Research Foundation Report, 1986).
Among the economically important helminth infections o f ruminants in the tropics are
parasitic gastroenteritis, fasciolosis, and lungworm infection (Arambulo and Moran, 1981).
21
Gastrointestinal (GI) nematodes have been identified as one of the causes of
production losses, which arises primarily through mortality, severe weight loss, poor meat,
milk and wool production, carcase and offal condemnation and impaired reproductive
performance (FAO, 1991). In addition, the cost o f obtaining anthelmintics, a primary tool
for the control o f GI nematodes, places additional stress on the already strained foreign
exchange o f developing countries.
2.2.1 Epidemiology o f nematodoses in Kenya
The epidemiology o f GI nematodes is heavily influenced by weather conditions. In
Kenya, different agro-ecological zones have been identified, which have relatively different
climatic conditions (Stotz, 1979). Available information indicates that GI helminths occur in
all the zones, and production and economic losses may be high due to both clinical and
subclinical infections (Round, 1962, Mango et al., 1974; Allonby and Urquhart, 1975;
%
Carles, 1992).
Until recently, little information on the epidemiology of GI nematode infections of
cattle in Kenya was available. Several studies have, however, been conducted in recent years
in the arid and semi-arid lands, and in the medium to high agricultural potential areas.
The prevalence o f nematode infections in cattle in the arid area o f Marsabit District
was studied by Omara-Opyene (1985). Marsabit District has a typical arid climate with low
rainfall ( < 2 5 0 mm annually) occurring in two short rainy seasons (April and November),
which are separated by dry 4-5 months. Faecal strongyle egg counts were high in the sub
humid mountainous areas but low in the arid lowlands, and the frequency of strongylosis was
highest during the dry season compared to the rainy seasons. The rainy seasons in this area
are very short and it was postulated that animals became infected during the short rainy
22
season but high strongyle egg counts were detected during the following dry season (Omara-
Opyene, 1985). Studies undertaken in Samburu District have shown that, the main effect of
G1 nematodes, is during the dry season when nutrition is very poor (Kariuki, 1997).
A prevalence survey conducted in Maasai group ranches in Kajiado District (semi-arid
area) showed that strongylosis was the most prevalent GI parasite infection, and the rate of
infection correlated with age in cattle. Most o f the cases occurred in calves, which also
suffered heavier parasitism (Ndarathi et al., 1989).
In a medium to high potential area of Kenya, Gatongi and colleagues (1988) examined
the influence of weather factors on the level o f pasture infectivity in Tetu Division, Nyeri
District. It was observed that larval population increased with rainfall peaks. Immediately
following the onset o f rains after a dry season, a high pasture larval population was detected,
presumably due to reappearing o f L, on the grass mat after having burrowed into the soil
during the preceding dry season. Alternatively, these larvae may have come from the faecal
pats after being softened by the rains (Gatongi et a\., 1988).
2.2.2 Bovine parasitic gastroenteritis
2.2.2.1 Aetiology, mode of transmission and species spectrum
Naturally-occuring bovine parasitic gastroenteritis (PGE) is a gastroenteropathy caused
by mixed infections with several species of GI nematodes. It is the commonest helminth
polyparasitism of ruminants in the tropics (Troncy, 1989), typically o f young animals and
may be acquired through a variety of ways (Lyon et al., 1970; Soulsby, 1982a). Toxocara
vitulorum is unique in being parasitic exclusively in young animals (Pandey et al., 1990),
particularly, young buffalo calves and patent infections can only be acquired through
prenatal and lactogenic routes (Gupta, 1986; Swain et al., 1987).
23
Gastrointestinal (GI) nematode fauna o f cattle does not differ significantly between
regions o f the tropics, as animals are usually infected with a range o f different species, and
the following parasites seem s to be representative for the mixed infection o f cattle and
buffaloes. The trichostrongylids Haemonchus spp., //. placei, H. contortus and H. similis are
found unless the climate is too dry. The Ostertagia and Nematodirus species are not very
common due to the fact that most species prefer a temperate climate (FAO, 1992). O f the
other trichostrongylids, Trichostrongylus axei is common as are the Cooperia spp., C.
pectinata, C. punctata and C. oncophora. Other common nematodes are the strongylid
Oesophagostomum radiatum , the hookworm Bunostomum phlebotomum, the rhabditoid
Strongyloides papillosus and the trichuroids Trichuris spp. The wide spread nature o f the
important parasitic diseases and their impact on livestock production in the developing
countries is illustrated in Table 2.3.
Although several species o f nematodes can contribute to PGE syndrome, only a few
are primarily responsible for disease outbreaks under field conditions. For example, disease
in cattle is caused mainly by H. placei , H. contortus , C. pectinata, C. punctata and O.
radiatum (Fabiyi et al., 1979; Chiejina, 1986; Waruiru et al., 1993a). B. phlebotomum is
occasionally important in muddy unhygienic environments (Troncy, 1989), while, clinical
strongyloidosis and toxocarosis are mainly diseases o f neonates and juveniles (Ikeme, 1971).
22.2.2 Nematode life cycles
The life cycles of trichostrongylid nematodes, Oesophagostomum and Bunostomum
are simple and direct, each adult worm being derived from an infective larva separately
24
Table 2.3: Distribution o f major parasites o f large herbivores and their relative importance (rank) within the region*
Nematode species Latin America North Africa Equitorial India and South Central East South East Asia
Africa West Asia Asia
Haemonchus 1 - 1 2 2 1
Cooperia 2 1 2 2 2 2
Trichostrongylus 2 2 2 1 2 3
Ostertagia - 4 - - - -
Toxocara - 3 4 1 1 1
Lungworms - - 5 3 - -
Hookworms 3 4 4 2 - 2
Oesophagostomum 4 2 3 3 2 3
Mecistocirrus - - - 1 2 1
*From FAO report AGA-815 (1991).

acquired from pasture. Adult nematodes inhabit the GI tract. Eggs produced by the female
are passed out in the faeces and given appropriate environmental conditions, hatch in the
faecal deposits to become first-stage larvae (L ,). The L, feed on bacteria, grow and moult
to second-stage larvae (L^), shedding their protective cuticle in the process. The larvae
moult into third-stage larvae (L3) but retain the cuticle from the previous moult. These
double-cuticled L, is the infective larvae. The time required for the eggs to develop into
infective larvae depends on temperature. Under optimal conditions (i.e. high humidity and
warm temperatures), the development process requires 7 to 10 days (Hansen and Perry,
1994).
The parasitic phase o f the life cycle begins with the ingestion o f L3. The protective
sheath is shed in response to specific stimuli such as temperature, C 0 2 concentration and pH
which occur within the organs preceding the site where parasitic development is completed.
The third moult takes place within a few days after exsheathment and fourth stage larvae
(L4), either closely applied to or within the mucosal surface, undergo major changes in
morphology, differentiate sexually and increase considerably in size. Further growth and
maturation occurs after the final moult to the adult form and shortly afterwards female worms
commence egg laying to complete the cycle. Generally, parasitic development in most
trichostrongylids is completed within 3 to 4 weeks after infection but for O. radiatum a
longer period of 5 to 6 weeks is required (Anderson and Bremner, 1983).
There are some exceptions to the general pattern described as in species o f
Nematodirus, development to the L3 stage occurs entirely within the egg; the larva then
hatches and is infective to the host. Infective larvae of hookworms ( Bunostomum) and
Sirongyloides can also infect the host by penetrating its skin; the worms reach the intestine
via the blood stream and lungs. The infective larval stage of Trichuris is contained within the
26
egg and is only released after the egg is ingested by the host (Hansen and Perry, 1994).
2 .2 .2 .3 Parasitic development and tissue changes caused by strongylid
nematodes
2 .2 .2 .3 .1 Haemonchus spp.
Considerable evidence has been advanced in favour of H. placei, the species usually
associated with cattle, being distinct from H. contortus , a common parasite among sheep and
goats (Whitlock and Le Jambre, 1979; Zarlenga et al., 1994). Both species infect cattle, H.
contortus occurring frequently when sheep and cattle are grazed together (Whitlock and Le
Jambre, 1979). Haemonchus spp. are the largest o f the worms found in the abomasum of
cattle and measure 14 to 25 mm in length. Adult worms are readily seen on the mucosal
surface and the females have a barber’s pole appearance due to the spiral intertwining o f a
blood filled gut and white egg filled uteri.
Thirty-six hours after infection, exsheathed L3 can be found in the pits of the gastric
glands, some penetrating to the deeper parts. Except where inhibition o f development occurs,
4th stage development is completed by the 10th day and is accompanied by a progressive
inflammatory reaction, hyperaemia and fluid exudation. The fourth moult takes place around
12 to 14 days after infection and the immature adult worms attach to the mucosa for feeding,
giving rise to circumscribed erosions on the mucosal surface and the formation o f a coagulum
of blood, mucus and desquamated epithelial cells. Infiltration at the base o f the glands by
mononuclear and eosinophil cells is slight during the 4th stage of development but intensifies
when adult worms are present (Bremner, 1956).
Pathophysiological changes and disease signs are all referable to the haemorrhagic
anaemia caused by the voracious blood sucking o f the adult worms. The severity o f the
27
changes and their speed o f onset being determined by the numbers o f larvae initially ingested
(Hunter and Mackenzie, 1982).
2 .2 .2 .3 .2 Trichostrongylus spp.
Trichostrongylus spp. are slender, hair-like worms 3 to 6 mm in length. T. axei is the
smallest o f the worms found in the abomasum o f cattle. T. colubriformis, a predominant
pathogen o f small ruminants is the smallest o f the intestinal species; and only occasionally
gives rise to a significant infection in cattle (Seddon, 1967).
One week after infection, T. axei larvae have entered the 4th larval stage of
development and a further week is required to complete this phase before the final moult to
the adult stage. During this period the heads o f the developing larvae are located beneath the
layer o f cells lining the upper half of the gastric glands in the abomasum and their bodies lie
free in the lumen o f the glands. Displaced cells and those in the vicinity are destroyed. Cells
lining deeper parts and others in adjacent glands lose their specialised secretory function
causing decreased gastric acid production which in heavy infections leads to an increase in
the pH o f abomasal contents.
Within 2 weeks after infection, white raised circular plaques up to l cm in diameter
can be observed in areas where aggregations o f worms have occurred. Between 3 and 8
weeks after infection inflammatory changes intensify, plaques are enlarged and become more
clearly defined and shallow ulcers appear in the mucosa, especially on the free edges o f the
abomasal folds (Ross et al., 1971).
Experimental innoculations showed that calves dosed with 100,000 L3 were not
associated with signs of disease although, decreased albumin levels and moderate increases
in plasma pepsinogen concentrations were detected 3 to 4 weeks after infection. With higher
28
doses (range 150,000 to 1.5 million Lj) however, young calves died within 3 to 8 weeks after
infection. Acute and severe inflammation of the abomasal mucosa with oedema of the folds
and patches o f white necrotic debris on the mucosal surface was typical of these high levels
of infection (Ross et al., 1968).
2.2.2.3.3 Cooperia spp.
Three species of the genus Cooperia (C. pectinata, C. punctata and C. oncophora)
are com m only found in cattle in the tropics and are regularly associated with outbreaks of
PGE in calves (Seddon, 1967; Fabiyi et al., 1979). There are small differences between
species in the time needed for parasitic development and in the size o f mature worms (4 to
7 mm in length) but all are found in the anterior half of the small intestine (Winks, 1974;
Bremner, 1982).
During the first 2 days after infection, most C. pectinata larvae are recovered from
the abomasum where some enter the gastric glands and from day 4 onwards, 85% o f the
worms are located in the proximal 40% of the small intestine. The parasitic phase of
development is relatively short, with the 3rd moult to the 4th stage occurring about 2 days
after ingestion of L,. Adult worms are found from the 8th day of ingestion onwards and eggs
first appear in the faeces between days 13 and 17. Fourth stage larvae (L4) are found either
deep in the intervillous crypts or coiled around the tips of the villi. Adult worms lie in close
contact with the mucosal surface frequently intertwined among the villi.
Destruction o f the tips of the villi, an intense inflammatory response and exudation
of plasma proteins are the main pathological changes induced by Cooperia infections. The
severity o f the lesions and the associated diarrhoea are directly related to the level of
infection. Resistance to the establishment o f infective larvae develops rapidly after moderate
29
to heavy initial infections (W inks, 1974).
2.2.2.3.4 Oesophagostomum radiaturn
The large white adult (nodular) worms o f cattle, 14 to 22 mm in length, are found
in the lumen o f the caecum and large intestine regardless o f the site o f larval penetration.
W ithin 2 days of infection, most of the exsheathed Lj penetrate the wall o f the
posterior part o f the small intestine and a few enter the wall of the caecum and colon. The
moult from L3 to L4 takes place about 9 days after infection, a period marked by profound
gut inflammation even in animals with primary infection (Elek and Durie, 1967). The final
moult commences on the 19th day and eggs can be detected in the faeces between days 32
and 42 after infection (Roberts et al., 1962).
Extensive tissue changes occur as a consequence o f O. radiaturn infections. In the
posterior small intestine the points of larval entry are clearly defined as circular, slightly
raised dark red patches. During the first week, larvae are surrounded by a clear serous fluid
in a cavity outlined by dislodged muscle cells and the resulting nodule protrudes into the
lumen where erosion of its surface occurs forming small crater-like apical ulcers. Vasculitis
of the small blood vessels occurs in the vicinity o f nodules. On the serosal surface, nodules
are associated with circular blister-like lesions with bright red centres and protruding above
the surface. Five to 6 weeks after infection most nodules appear as slight circular elevations
consisting o f dense fibrous plaques in the submucosa. A few large abscessed nodules persist
after adult worms reach maturity; most contain calcified remnants o f larvae (Elek and Durie,
1967).
During the first 2 weeks of infection, the mucosa of both caecum and colon become
increasingly congested and oedematous, and an abundant slimy turbid mucus is produced,
30
■
and haemorrhages are common in the submucosal tissue. The net effect is a marked
thickening o f the wall o f the caecum and proximal colon. The acute catarrhal inflammation
persists w hile worms are present and is frequently associated with diarrhoea and a decrease
in food intake. During the repair o f abscesses, granulomata containing multinucleated giant
cells o f various shapes and sizes appear in the mucosal crypts and extensive fibrosis occurs
in the gut wall. Periglandular lymphatic tissue, without obvious germinal centres, increases
to form a continuous sheet in the colon. Infiltration by eosinophils is intense at all sites of
infection (Elek and Durie, 1967).
Experimental infection o f calves with O. radiatum, even at relatively low numbers
of worms per animal, results in severe weight loss, anorexia, anaemia and diarrhoea
(Bremner, 1961; Gasbarre and Douvres, 1987). Doses o f 100,000 L, produced a severe
haemorrhagic necrotic enteritis which resulted in the death o f calves before maturity o f the
parasites (Elek and Durie, 1967; Bremner, 1969). Anaemia due to O. radiatum infection may
be caused by a worm product that either directly affects haematopoiesis (Andrews and
Maldonado, 1943), or induces severe inflammation that results in ulceration o f the gut and
subsequent blood loss (Elek and Durie, 1967). Alternatively, anaemia may develop due to
blood loss resulting from mechanical disruption o f the intestinal mucosa by the feeding adults
(Bremner and Keith, 1962).
Reinfection o f previously infected animals gives rise to an allergic enteritis which
causes elimination o f most o f the infective larvae within 24 h. This reaction is associated
with oedem a, hyperaemia and hypersecretion in the intestine and is often followed by a
transient but intense bout o f diarrhoea. The infiltration of the oedematous intestinal tissues
with eosinophil and neutrophil leucocytes and the vasculitis in the vicinity o f histotropic
larvae, and the subsequent proliferative granulomatous reaction with the appearance of
31
plasma cells, conform with descriptions of the Arthus type of immediate hypersensitivity
(Elek and Durie, 1967).
Although the nodular worms o f ruminants are severe pathogens in young calves and
lambs, older animals are much less affected due to the strong protective immunity elicited
by these parasites. Primary infection with as few as 1000 L, protects calves against
reinfection (Roberts et al., 1962).
2 .2 .2 .4 Factors influencing epidemiology
The transmission, incidence and intensity o f GI nematode infections are determined
by several interacting factors. These include extrinsic factors o f climate, weather and,
methods o f husbandry and systems of livestock production and intrinsic host factors o f age,
heredity and physiological state (Barger et al., 1983; Chiejina, 1995). A general account of
the role o f each factor in determining the dynamics o f worm populations found in grazing
cattle is outlined her^?elow:-
2 . 2 . 2 . 4.1 Extrinsic factors
2 .2 .2 .4 .1 .1 Climate and weather
Parasitologically, climate may be defined as the synthesis o f the day-to-day values of
the meteorological elements affecting a locality, expressed as seasonal or annual values,
while weather describes the day-to-day meteorological conditions which constitute the climate
(Thomas, 1974). Thus, climate (the long term pattern of atmospheric events which is used
to divide areas of the world into regions with similar characteristics) influences the general
epidemiological pattern, while weather (which characterises the seasons) determines the
timing and magnitude of specific events that make up that pattern. The effects o f weather are
32
direct, acting on the rate o f development, migration and survival o f the free-living stages of
parasites and indirect, by regulating the growth, abundance and maturation of herbage
(Barger et a l., 1983).
2 .2 .2 .4 .1 .1 .1 Bionomics of free-living stages
Pasture provides the micro-environment in which preparasitic development and
survival o f nematodes must take place, worm eggs and larvae being distributed in an
unpredictable manner on pasture (Crofton, 1963; Thomas, 1974). Pasture infectivity depends
on the independent and interactive influences o f several factors in the macro- and micro
environment, and these include temperature, moisture, humidity, sunlight and oxygen supply
(Andersen et al., 1970; Waller and Donald, 1972), structure o f the soil, growth and
composition o f pasture herbage (Collis-George, 1959; Knapp, 1964), as well as size and
consistency o f faeces (Silverman and Campbell, 1959; Young and Anderson, 1981; Chiejina
and Fakae, 1989).
Field and laboratory studies have shown that: (i) Preparasitic stages o f nematode
parasites o f livestock differ in their response to environmental conditions, especially
temperature and moisture. These differences exist within and between nematode species.
Generally, Lj and embryonated eggs are the least susceptible to adverse environmental
conditions, followed by unembryonated eggs, L, and in that order, (ii) High moisture
levels are a general requirement for larval development and migration (Dinaburg, 1944;
Young and Anderson, 1981). Bunostomum spp. larvae generally require moist, slightly sandy
soil and temperature range o f 23°C to 30°C for optimum development and activity (Soulsby,
1982a; Troncy, 1989). On the other hand, excessive moisture or sustained torrential rainfall
adversely affects development of eggs and pasture larval densities through rapid
33
disintegration of faeces and washing away of eggs and larvae by rain and flood water (Ikeme
et al., 1986; Fakae and Chiejina, 1988; Bryan and Kerr, 1989) and also possibly through
reduced oxygen tension in water-logged faeces (Silverman and Campbell, 1959). In contrast,
because o f the high moisture content o f cattle dung pats, the hatching of nematode eggs and
subsequent development to L3 is mainly limited by ambient temperatures, and can be
completed within the dung pat, even during drought (Young and Anderson, 1981; Barger et
al’, 1984). (iii) Warm conditions and the presence o f moisture films both within the dung pat
and on herbage is essential for the migration o f L3 to sites making them available for
ingestion by cattle (Silangwa and Todd, 1964; Soulsby, 1982a). Thus, the amount and
distribution o f rainfall is therefore a major determinant o f the availabilty of L3 and also of
the occurrence o f PGE. Larval dispersal in pasture may be aided by various mechanical
agents such as farm machinery, implements and foot-wear o f farm personnel. Biotic factors
such as microfungi and psychodid flies, have been shown to transport the larvae o f C.
punctata and T. colubriformis (Bizzell and Ciordia, 1965) and Oesophagostomum and
Ostertagia spp. (Jacobs et al., 1968; Tod et al., 1971), respectively. Earthworms and dung
beetles may aid the distribution of the parasites by moving faecal material mechanically
(Gronvold, 1979). (iv) Once on herbage the longevity of L3 is extremely limited under hot
dry tropical conditions (Dinnik and Dinnik, 1961; Chiejina et. al., 1989). In the Trichuridae
and Ascarididae, the infective egg can survive in a warm humid environment for several
years (Troncy, 1989) but their longevity is also severely curtailed during the hot dry season
and by direct sunlight.
2 .2 .2 .4 .1 .1 .2 Seasonal patterns of infection
Two distinct patterns o f pasture infestation may be encountered in the tropics,
34
depending largely on the distribution of rainfall. The first is seen in the dry tropics and in
the subhumid zones having clearly defined favourable and unfavourable seasons for
preparasitic development. The latter season is sufficiently hot, dry and prolonged to cause
complete cessation o f development and survival o f preparasitic stages. Thus, except in
irrigated or other permanently wet pastures, transmission of PGE in such areas is restricted
to the w et season (Ogunsusi, 1979; Charles, 1989) and the only means of carry-over o f
infection from one rainy season to another is through animals harbouring adult worms and/or
arrested (hypobiotic) larvae (Chiejina et al., 1988; Kaufmann and Pfister, 1990; Ndao et al.,
1995).
In the less dry parts o f the subhumid and wet tropics, faecal reservoirs o f L3 are also
a very important additional source of the early rains herbage infestation in dry season-
contaminated cattle pastures (Chiejina and Fakae, 1989; Fabiyi, et a l., 1988). Such larvae
develop and accumulate inside faecal pats throughout the dry season but do not appear on
herbage until adequate moisture conditions return at the start o f the succeeding rainy season,
when a spontaneous and synchronous translation o f the entire faecal larval population takes
place, within 24 to 48 h o f the first substantial rainfall of the season (Fakae and Chiejina,
1988; Chiejina and Fakae, 1989).
During the rainy season, there is a continuous cycle of infection between the host and
pasture and herbage larval densities, and worm populations in animals fluctuate considerably
throughout the season (Chiejina and Emehelu, 1984; Fakae and Chiejina, 1988). This is in
response to variations in the size of contamination, grazing intensity and frequency, short
term fluctuations in weather conditions and host responses to infection. The relative short
survival o f L3 on herbage during the wet season is the net result o f several contributory
factors such as constant heavy rainfall which, causes accelerated disintegration o f faecal pats
tJNTBFP"TV nF NA1R° Bt
LtnKARY
and disappearance o f free-living larval stages from pasture. Also, rapid breakup and burying
of faeces in the soil by dung beetles, earthworms and termites may contribute to the fast
depletion o f pasture larval population (Gronvold, 1987; Bryan and Kerr, 1989). Predacious
fungi, w hich play a similar role in temperate climates (Hashmi and Connan, 1989) have yet
to be identified in the faeces o f tropical livestock.
The second major infection pattern is non-discontinuous and occurs under
continuously favourable climatic conditions in the humid tropics. In this zone there is no
clear-cut seasonality in the pattern o f larval availability in pasture (Okon and Akinpelu, 1982;
Ikeme et a l., 1986; Gupta et al., 1987) and several larval peaks and generations o f parasites
develop in pasture and animals, respectively throughout the year.
Acquisition o f infective eggs of T. vitulorum may also follow a seasonal pattern in the
dry tropics while in the permanently warm and humid zone infection may be constantly
present both in the environment and in calves in endemic areas. The pattern of lactogenic and
congenital infections is however, determined primarily by the dynamics of populations of
dormant L3 in maternal tissues, the reproductive state o f the dam and methods o f calf
husbandry (Roberts, 1989). Somatic larvae can probably survive in maternal tissues for
several months or years (Soulsby, 1982a).
2 .2 .2 .4 .1 .1 .3 Livestock production systems and husbandry practices
Livestock production systems and managerial practices influence the accessibility and
transmissibility of infection to a susceptible host population by creating opportunities for
contact between host and parasite. The methods o f management o f domesticated ruminants
in the tropics are varied (Payne, 1970; Chiejina, 1986; Upton, 1987; Ndamukong, et al.,
1989) and are linked with local traditions and beliefs (Payne, 1970; Ndamukong et al.,
36
1989). The likelihood o f disease increases with the intensity o f grazing. Thus, the
concentration o f infective stages in the environment is very low in those systems which utilise
extensive grazing areas, as they are thinly spread over a large territory. Nevertheless,
relatively intensive traditional methods o f village production of small and large ruminants
such as tethering and other forms o f confinement, including those which rely on zero-grazing
or other cut-and-carry feeding regimens (Reynolds and Adediran, 1987), may sometimes be
associated with clinical PGE (Ademosun, 1987). Similarly, true nomadic and, to a lesser
extent, transhumant herds harbour generally low infection levels (Pullan, 1980) except if they
accidentally encounter heavily contaminated foci, such as permanent swamps, during their
migration (Onyali, 1989) or if they camp in, and themselves contaminate a given area for an
extended period (Chiejina, 1991).
Certain management practices favour the transmission of parasitic infections and hence
increase the likelihood, and severity of disease. These practices are primarily concerned with
the density o f stocking in relation to the availability of pasture, season o f year and class of
livestock.
Intensified cattle grazing is often associated with high stocking rates and segregation
of stock into age classes whose nutritional requirements often exceed those provided by areas
allocated to them. Common examples o f this practice include the permanent calf paddock on
many dairy farms, set stocking of replacement heifers on less productive areas, grazing
young animals on the same area in successive years and the maintenance of bulls on small
paddocks for most o f the year (Banks and Mitton, 1960; Anderson et al., 1965; Hotson,
1967). To reduce the risk o f parasitic disease, higher stocking rates should be matched by
appropriate increases in pasture production or supplementary feeding. Failure to do this
forces cattle to graze close to the ground and closer to dung pats than they would by choice.
37
thus ensuring high intake o f L3. Weaned dairy calves and beef yearlings magnify this risk
because their rate o f pasture contamination is much greater than that o f mature cattle. High
levels o f infection on pasture often coincide with periods of inadequate nutrition, and
measures to avoid this situation are a feature o f effective control strategies (Barger et al.,
1983).
2. 2.2 . 4 .2 Intrinsic factors
2 .2 .2 .4 .2 .1 Nutrition
Host nutrition influences the outcome o f nematode infections in man and animals
(Whitlock, 1949; Reveron and Topps, 1970; Coop, 1995). It is well establishment that
inadequate intake or lack o f proteins, minerals and vitamins, leads to the lowering o f body
resistance and specifically to impaired cellular immune responses to infections (McGee and
McMurray, 1988). In helminth infections, this manifests as increased establishment, survival
and pathogenicity o f the parasite and hence production losses in the host (Gordon, 1964;
Abbot et al., 1988). Recently, Shaw et al. (1995) demonstrated that the development of
acquired immunity to Haemonchus infections in young sheep was enhanced in grazing
animals which received an additional supplementation with a protein rich concentrate. It is
likely that the supplement counterbalanced the parasite induced protein deficiency.
An area o f interest which has received attention recently is the question of whether
animals infected with GI nematodes can alter their diet selection to ameliorate the
pathological consequences o f parasitism. Sheep continuously infected with T. colubrifortnis
larvae and offered a free choice of low or a high protein ration increased the proportion of
the high protein consumed (Kyriazakis et al., 1994; 1996). This selection period coincided
with the commencement o f a reduction in serum albumin and phosphorus concentrations,
38
which have been shown to be associated with the damage o f the small intestine in
Trichostrongylus spp. infections (Poppi et al., 1985; 1986).
The crude protein content of most native tropical grasses is adequate for only
moderate levels o f animal production for a few months o f the year when the grasses are
young (Reynolds and Adediran, 1987). Consequently, there is usually severe seasonal
shortage leading to wide spread malnutrition and sometimes heavy parasitism, particularly
in the semi-arid and savanna zones (Schillhorn van Veen, 1974; Charles, 1989). The full
extent o f malnutrition and its impact on GI nematode infection in tropical livestock are at
present impossible to assess accurately. However, it is reasonable to conclude, based on the
widespread occurrences o f infections and undernutrition in animals that host nutrition is a
major contributory factor to the incidence and production effects o f helminthosis in general
and PGE in particular in ruminants in the tropics (Schillhorn van Veen, 1974; Kaufmann and
Pfister, 1990).
2 .2 .2 .4 .2 .2 Host age, sex, acquired resistance and genotype
Age influences the susceptibility and resilience of animals to helminth infections,
young animals being more susceptiple than adults (Soulsby, 1979). Comparisons between
mature cattle and calves have shown that older animals are better able to limit the number
of worms establishing from an infecting dose. When cattle reared worm-free were dosed with
larvae, burdens o f O. ostertagi, Cooperia spp., Nematodirus helvetianus and O. radiation
were significantly less in animals over 1 year old than in calves less than 6 months o f age
(Herlich, 1960; Bremner et al., 1976). Under field conditions, disease outbreaks are more
likely to occur in young than in adult ruminants, and the latter usually harbour chronic, low-
level infections and, acts as a constant source o f infection for more susceptible animals.
39
However, clinical PGE is known to occur in adult small and large ruminants (Hotson, 1967;
Wedderburn, 1970; Selman et al., 1976). Such outbreaks usually occurred either under
nutritional stress and intercurrent infection (Schillhorn van Veen, 1974) or as a result of
poorly developed and waning immunity. Age resistance is highly effective in T. vitulorum
infections in which expulsion o f adult worms commences as early as 38 days after birth
(Soulsby, 1982b) and is completed at 3 to 6 months o f age.
S ex , pregnancy and lactation have long been known to affect worm populations in a
wide variety o f hosts (Dunsmore, 1965; Connan, 1976; Copeman and Hutchinson 1979;
Gibbs and Barger, 1986; Bundy, 1988). Copeman and Hutchinson (1979) reported that bulls
had higher nematode egg counts than steers and both were higher than those of heifers in an
experiment where young bulls, steers and heifers o f the same age and breed grazed together.
The w eight gain response to anthelmintic treatment was in the same rank order.
A temporary loss o f acquired immunity to nematode parasites at around the time of
parturition and during lactation has been extensively documented in ewes and to a lesser
extent in cow s (Lloyd, 1983), and recently, goats (Rahman and Collins, 1992). This loss
of immunity typically involves a periparturient rise in faecal egg counts (PPR) in lactating
animals, often accompanied by clinical signs of PGE. All of the parasitological manifestations
of acquired immunity to nematodes appear to be compromised (Barger, 1993b). The
phenomenon is associated with lactation (O’Sullivan and Donald, 1970) rather than
pregnancy, although it may begin in late pregnancy, and can be abolished by removal o f the
sucking young (O’Sullivan and Donald, 1973). Its cause has been variously ascribed to poor
nutrition, stress, lack of antigenic stimulation, and hormonal suppression of immunity, of
which the latter is overwhelmingly favoured.
The net result of PPR is a substantial increase in host worm burden and pasture
40
contamination with worm eggs. The rise, which also occurs in cattle (Michel et al., 1972)
and goats (Okon, 1980; Rahman and Collins, 1992) is of considerable economic importance
in sheep in temperate climates where it is sometimes the sole source o f the first major wave
of worm infections in lambs during the summer (Boag and Thomas, 1971). There are no
reports o f its occurrence in large ruminants and its epidemiological significance in the tropics
is less w ell known.
Parasite populations in the host are regulated primarily by mechanisms and processes
associated with either natural or acquired resistance, the latter being under genetic control
(Wakelin, 1988). It is a result o f natural resistance that some nematode parasites which are
well adapted to one host species are unable to establish and reproduce successfully in another
host, and this forms the basis for using mixed and alternate grazing o f different species of
animals for the control o f animal helminthoses (Arundel and Hamilton, 1975). Acquired
resistance, on the other hand, occurs more widely and helps to control parasite populations
in field infections. O f its many manifestations (Michel, 1968a, Chiejina and Sewell, 1974a),
resistance to establishment o f new infections, reduced worm fecundity and worm rejection
are of epidemiological significance.
The self cure phenomenon, is the best-known iminunologically-mediated worm
rejection mechanisms in field infections (Stoll, 1928; 1939; Lee et al., 1960; Van Geldorp
and Schillhorm van Veen, 1976). This periodically results in spontaneous exponential
rejection o f worm infections and is sometimes also accompanied by protection from further
challenge infection (Gordon, 1968). However, self-cure is not always immunologically
mediated, as it has been observed in non immune Haemonchus-'infected sheep grazing worm-
free lush pasture. The stimulus responsible for inducing the latter type o f response is believed
to be either an anthelmintic or an allergic substance present in freshly growing grass or as
41
yet undetermined physiological alterations in the abomasum (Allonby and Urquhart, 1973).
Michel (1963; 1970) also described a non-immunologically-mediated mechanism for
regulating burdens o f Ostertagia spp. in calves in which worm populations were maintained
by a balance between existing worms and the acquisition o f new infection. However, this
mechanism may not apply to all host-parasite systems (Chiejina and Sewell, 1974a; b).
T h e genetic basis o f resistance o f animals to parasites, especially helminth infections
is now w id ely accepted based on work in laboratory animal models (reviewed by Wakelin,
1991) and in farm animals (reviewed by Windon, 1991). Generally, indigenous tropical
breeds are more resistant than their exotic counterparts (Knight et al., 1973; Piper and
Barger, 1988), while crosses between the two are intermediate in their response, particularly
with regard to establishment o f worms in the host, faecal worm egg output and pathogenicity
of infections, all o f which are o f epidemiological importance. The recognition of the potential
value o f this genetic characteristic in livestock selection and improvement schemes and in
parasite control has prompted the search for suitable markers such as haemoglobin
polymorphisms, lymphocyte antigen types (Altaif and Dargie, 1978; Stear et al., 1988;
Douch and Outteridge, 1989) and, more recently, DNA markers (Rohrer et al., 1991) for
predicting resistance to nematode parasites.
2 .2 .2 .4 .2 .3 A nested larval development
Inhibition, arrested larval development and hypobiosis are synonymous terms used to
describe the cessation of development at an early phase of parasitic existence in the host.
This temporary cessation o f development is important in many GI nematodes of domesticated
ruminants in which the L4 or sometimes the L3 is mostly affected (Michel, 1974; Schad,
1977). The factors which are known to induce larval hypobiosis are many and of these,
42
exposure o f L, to adverse environmental conditions is the most important stimulus in GI
nematodes o f ruminants. This is consistent with the observation that the phenomenon occurs
mostly in cold temperate (reviewed by Armour and Duncan, 1987) and in hot dry climates
(Hart, 1964; Chiejina et al., 1988). In both climatic zones, hypobiosis is highly seasonal in
its incidence and sets in just before the commencement, and terminates at the end, o f the
unfavourable season, which corresponds to the autumn/winter and the dry season in
temperate and tropical climates, respectively. In the dry savanna zone of Nigeria, for
example, the highest and lowest incidence are observed during the dry and wet seasons,
respectively. Thus, hypobiosis may be considered as an adaptation by the affected parasites
which enables them to survive in their host at a developmental stage which is unaffected by
the host immunological responses and at a time when environmental conditions are
unfavourable for free-living development and survival (Taylor and Michel, 1953; Waller and
Thomas, 1975). Consequently, it serves to synchronise the development o f the parasite with
events in the host and the environment (Soulsby, 1982a).
Reports from Kenya (Allonby and Urquhart, 1975; Gatongi, 1995), India (Gupta et
al., 1987), Malaysia (Ikeme et al., 1987), Egypt (El-Azazy. 1990) and Nigeria (Chiejina et
al., 1988; Fakae, 1990) indicate that only limited hypobiosis or none at all occurs in those
climatic zones where environmental conditions are permanently suitable for preparasitic
development and survival.
In the dry tropics, hypobiosis is the most important means o f survival and carry-over
of infection in the host, with species such as Haenionchus and Cooperia , from the end o f one
rainy season to the beginning o f another (Hart, 1964; Ogunsusi and Eysker, 1979; Ndao et
al., 1995). Its onset also serves to limit further increase in the number of adult worms
(Schad, 1977), which are the more pathogenic stages, at a time when pasture larval density
43
is still high. However, synchronous development o f large numbers o f hypobiotic larvae can
sometimes occur well before the end of the dry season, thereby resulting in a sudden increase
in the numbers o f pathogenic stages which may lead to dry season outbreaks of PGE (Fabiyi
e ta l., 1979).
2 .2 .2 .4 .2 .4 Concurrent infections
The capacity o f an animal to control a given parasitic infection may be markedly
compromised by concomitant infection with another related or unrelated parasite or pathogen
(Urquhart et al., 1973; Phillips et al, 1974; Bell et al, 1984). Laboratory studies have shown
that this phenomenon is subjected to host strain-dependent variability which is, in turn,
genetically-determined (Murray et al., 1973; McElroy and Befus, 1987).
The laboratory findings have been confirmed by field observations on concurrent
Trypanosoma congolense-H. contortus infections in indigenous and exotic breeds o f goats in
East Africa (Griffin et al., 1981). This and other species of trypanosomes have been shown
to suppress host immune responses to various important bacterial vaccines used in domestic
animals, including livestock, in the tropics (Holmes et al., 1974; Mackenzie et al., 1975).
Immunodepression in concurrent infections in tropical livestock is likely to be of
epidemiological importance in trypanosome-endemic areas where concurrent trypanosome-
helminth infections are common (Chiejina, 1987). These infections are frequently associated
with nutritional and climatic stresses, which are known to influence host resistance to
infections (Gordon, 1964; Abbot et al., 1988).
44
2.2.2.5 P a th o p h y s io lo g y a n d c lin ic a l e ffe c ts o f n e m a to d e in fe c tio n s
2 .2 .2 .5 .1 Pathophysiology
A dverse impacts of parasitism on productivity are expressed in a number of ways
which include loss in body weight (Sykes and Coop, 1977; Abbott et al., 1986), reduced
milk production (Michel et a l., 1982; Kloosterman et al., 1985) and poor quality and
quantity o f wool in sheep (Steel et al., 1982). Virtually all o f the detrimental effects o f the
nematodes o f major economic importance in cattle can be accounted for by decreased feed
intake; gut motility, digestion and absorption, protein, energy and mineral metabolism as well
as water and electrolyte balance.
2 .2 .2 .5 .1 .1 Decreased feed intake
Irrespective o f the site o f location, most GI nematodes, except possibly H. placei
(Anderson and Bremner, 1983), cause a reduction in voluntary feed intake, the severity o f
the effect being related to the level of intake o f L3, the species o f nematode and the
composition o f the feed (Parkins and Holmes, 1989). The cause of reduction in feed intake
is unknown but current evidence suggests that it is likely to be multifactorial (Coop, 1995).
Many GI nematode infections are associated with marked pathological changes and
it is possible that, in addition to pain or discomfort (Gibson, 1955), alterations in the rate o f
passage o f ingesta even in the absence o f diarrhoea could be associated with changes in
voluntary feed intake (Gregory et al., 1985). Others have suggested that the increased levels
of GI hormones such as gastrin and cholecystokin observed in parasitized ruminants, may be
responsible (Symons and Hennessy, 1981; Titchen, 1982; Fox et al., 1989; Fox, 1993).
Attempts have been made to study the impact o f parasite infection on the central neural
control at the hypothalamus. The data o f Dynes et al. (1990) from sheep continuously
45
infected w ith T. colubriformis suggest that the resulting depression in feed intake could be
alleviated b y inhibiting the satiety effect at the ventromedial hypothalamus, suggesting that
central satiety signals may play a role.
2 .2 .2 .5 .1 .2 Gut motility, digestion and absorption
In addition to reductions in voluntary feed intake, studies have shown that GI
parasitism reduces the efficiency o f feed utilization by interfering with GI motility, digestion
and absorption.
Experiments conducted on GI motility in parasitized ruminants have shown that
infection o f the abomasum, small intestines and possibly the large intestine can seriously
disturb the normal pattern o f GI motility and digesta flow, even in the absence o f diarrhoea
(Gregory, 1985). Where studied, the rate o f flow through the gut was reduced rather than
increased, an effect which appears to be partly due to reduced feed intake and partly to the
influence o f the parasite per se. With clinical infections, the onset o f diarrhoea is preceded
by the disruption of migrating myoelectric complexes (MMCs) and severe inhibition o f the
reticulo-rumen and abomasum, at which time there may be an increase in the bacterial
populations which could contribute to occurrence o f the diarrhoea (Holmes, 1994).
Numerous attempts have been made to determine whether impaired digestion and
absorption are major causes o f poor utilization of feed by parasitized animals. Although some
studies have clearly shown depressed absorption o f substrates in parasitized portions o f the
intestinal tract, absorption may be enhanced in non-parasitized portions and, as a result,
absorption overall may not be affected (Symons, 1976; Castro, 1981). Generally, these
studies have indicated that impaired digestion and absorption are not important causes o f the
poor utilization of nutrients by parasitized ruminants, rather, it is the increased metabolic
46
demands on the host as a result o f the parasites activities (Holmes, 1994). However, there
are situations in which malabsorption may be significant, especially, with mixed strongylid
infections in ruminants.
2 .2 .2 .5 .1 .3 Protein and energy metabolism
In GI parasitism, substantial protein losses occur in terms of exfoliated epithelial cells,
plasma, mucus and red blood cells (Bremner, 1969; Holmes and Mcleans, 1971; Abbott et
al., 1986; Poppi et al., 1986). Reduced nitrogen retention has been shown to be a
characteristic feature in helminth infections and has been associated with depressed growth
rates and other factors of productivity (Parkins et al., 1973; Roseby, 1977). It has further
been demonstrated that protein synthesis is reduced in skeletal muscles o f parasitised animals
(Symons and Jones, 1975). The overall effect o f infection with GI nematodes can be
summarised as diversion o f amino acids away from productive processes such as meat and
milk production into processes which sustain the integrity o f the GI tract and maintenance
of homeostatic mechanisms which are essential for life (Symons, 1985; Coop, 1995). The
protein requirements o f the parasitised ruminant are consequently increased (MacRae, 1993).
T he increased synthetic rates of protein in the liver and the gut tissue have been found
to draw heavily on the digestible energy (Jones and Symons, 1982; Symons and Jones, 1983)
and this has been shown to be substantially reduced in parasitised animals (Sykes and Coop,
1977; MacRae et al., 1982; Entrocasso et al., 1986a).
2 .2 .2 .5 .1 .4 Mineral metabolism
A number o f studies have shown that muscle growth and mineralisation are impaired
in parasitised ruminants (Reveron et al., 1974; Sykes et al., 1977; 1979). Deposition of bone
47
calcium and phosphorus has been shown to be reduced by as much as 65 % in infected lambs
compared with worm-free lambs (Sykes et al., 1977). The net result o f this has been calcium
and phosphorus deficiency which leads to stunted growth (Poppi et a l., 1985).
2 .2 .2 .5 .1 .5 Water and electrolyte balance
Diarrhoea is commonly seen among grazing cattle and often, without the necessary
justification, directly attributed to parasitism. However, phases of persistent or intermittent
diarrhoea occur during moderate to heavy infections o f all important GI parasites except H.
placei (Anderson and Bremner, 1983). With Ostertagia spp. infections, diarrhoea coincides
with maturation o f larvae into young adults and this also corresponds with the time that
pathological changes o f inappetance, plasma protein losses and negative nitrogen balance are
pronounced (Holmes and Mcleans, 1971; Parkins et al., 1973). During this stage o f
infection, there is a marked increase in water turnover in faeces to as much as 20 % greater
than normal average (Holmes and Bremner, 1971). Furthermore, potassium losses in infected
calves have been found to be 10 times that in non-parasitised calves (Parkins et al., 1982)
which is an indication o f massive sloughing of intestinal epithelial cells.
Although water loss through diarrhoeic faeces in parasitised animals has been shown
to be higher than in non-infected animals, their water loss through urine has been found to
be considerably below normal (Bremner, 1982). This increased water retention by parasitised
animals indicates that tissue loss attributable to parasite infections cannot be strictly
determined from losses in body weight alone (Halliday et al., 1965; Abbot et al., 1986;
Entrocasso et al., 1986b).
48
2 .2.2. 5.2 Clinical effects
Gastrointestinal (GI) parasitism is associated with a range of clinical signs, including
a failure to gain weight, inappetance and usually diarrhoea. Also, alterations in body
composition occur and these can be o f considerable importance in judging the impact o f Gl
parasitism. Changes in body composition as a result o f trichostrongylosis have been reported
in cattle by Halliday et al. (1965) and Entrocasso et al. (1986b).
There is evidences that milk production may be reduced in ruminants infected with
trichostrongylids (Bliss and Todd, 1976; Thomas and Ali, 1983). In addition, GI parasite
infections can also reduce conception and pregnancy rates, and delay the onset o f puberty in
cattle (Oakley et al., 1979; Kumar and Sharma, 1991).
M any o f the pathological findings reflect the clinical signs, for example, poor body
condition and weight loss, while others relate to specific changes within the GI tract. The
lesions associated with Haemonchus spp., are broadly similar to other trichostrongylid
infections o f the abomasum, although it is the haematophagic habit o f the L4 and adults
following their emergence from gastric glands which are most detrimental to the host.
Haemonchus is the most pathogenic of the blood suckers and infections with large numbers
of this parasite often result in severe anaemia in the host. Blood losses from Bunostomum and
Oesophagostomum infections may add to the severity o f the anaemia. In trichostrongylid
infections o f the small intestine, the main damage results from activity o f the adult worms.
Heavy infections are associated with severe enteritis and diarrhoea.
Migrating larvae of T. vitulorum may cause damage o f the liver and lungs. The
presence o f the adult parasites in the small intestine is often associated with diarrhoea and
reduced weight gain.
49
2 .2 .2 .6 Impact o f nematodosis on livestock production
Production losses due to PGE are high whenever adequate moisture is available for
prolonged periods o f the year and where animals are being grazed at high densities (Fabiyi,
1987). Mortalities o f over 30% were reported on heavily stocked farms in Burma (Griffiths,
1957) and on irrigated pasture in wet tropics o f North Queensland (Copeman and
Hutchinson, 1979), respectively. In western Nigeria, helminthosis was found to be an
obstacle o f prime importance to the cattle industry as it caused severe mortality, abortion and
stunted grow th, whenever animals were kept under high stocking rates (Lee, 1955).
Severe losses are known to occur in non-humid climatic areas including semi-arid
zones, although this is generally associated with poor nutrition and over stocking around
water holes. Thus, as high as 10-20% mortality was reported in Senegal (Vassiliades, 1974)
and extensive deaths, and up to 30% carcase condemnation due to severe emaciation was
recorded in Botswana (Carmichael, 1972); these are semi-arid areas. In a survey of Gl
parasitism under nomadic management in Marsabit District o f northern Kenya, strongyles
were found to be the most important parasites contributing to morbidity. Haernonchus spp.
was the most important parasite and was a major constraint to cattle production in this area
(Omara-Opyene, 1985).
The nodular worm, O. radiatum, do cause additional losses by rendering intestines,
which are important items o f diet in tropical Africa, unfit for human consumption. Thus in
Swaziland alone up to 28.1% sets o f intestines have been condemned annually, amounting
to 60 tons o f protein rich food (Mitchell, 1974). In a limited survey, condemnations in cattle
due to Oesophagostomum spp. (pimply gut) was 1.5% of all cattle slaughtered in five
abattoirs around Nairobi (Githigia et al., 1995).
While strongylids are the GI nematodes commonly involved in production loss, T.
50
vitulorum too can be important in wet areas. In untreated cases and heavy infections, the
mortality rate may be up to 35-40% of infected animals, and it is believed to be the most
serious d isease o f buffalo calves in Southeast Asia (FAO, 1992). Parasitological studies
carried out in Central African Republic (Vercruysse, 1980), Nigeria (Tekdekand Ogunsusi,
1987), Tanzania (Makundi, 1994) and Kenya (Kanyari et al., 1995) revealed that T.
vitulorum and S. papillosus were the main causes o f diarrhoea and mortality in calves.
E conom ic estimates o f the losses due to multiple nematode parasite infection o f
ruminants are difficult to obtain. However, some examples are available. In Uruguay it is
estimated that helminth infections account for losses in cattle of upto 50 kg body weight with
a total loss o f US$ 220 million per year (FAO, 1991), and the estimated annual costs to the
Australian sheep industry were A$ 400 million in 1984 and A$ 309 million in 1985, owing
to production losses and A$ 50 million and A$ 53 million, respectively, for the use and
administration o f anthelmintics (Gray, 1987; Windon, 1990). Estimates o f yearly costs owing
to GI nematode and lungworm infections in dairy cattle in The Netherlands amounted to
about U S$ 100 million. The estimate included losses from growth depression in calves and
yearlings, lower milk production in cows and the cost of lungworm vaccine, anthelmintic
treatments and preventive pasture management (Ploeger and Kloosterman, 1988).
There are few published estimates in Africa, but production losses are generally high
especially for small ruminants. Graber (1965) calculated an annual loss o f 11.3% o f the total
economic value o f sheep and goats in Chad due to GI nematodes. Akerejola and colleagues
(1979) estimated an annual loss o f over US$ 40 million due to GI nematodes in the Kano
area of northern Nigeria, and annual mortality rates o f 60% in lambs and 30% in ewes have
been reported (Eysker and Ogunsusi, 1980). In Zaire, Brito (1947) estimated an annual
mortality rate o f 54% due to GI trichostrongylosis alone and an additional 12% due to the
51
combined effects o f helminth and coccidial infections. In Kenya H. contortus infection in
;heep is estim ated to cause an annual loss o f US$ 26 million in the agricultural sector
; Preston and Allonby, 1979).
2 .2 .2 .7 Diagnosis of parasitic gastroenteritis
2 2 .2 .1 A Clinical diagnosis
The presenting signs in a typical case o f PGE depend on the predominant pathology
and parasites. They include poor body condition, anorexia, diarrhoea and anaemia. Anaemia
and its sequelae are associated with cases in which either of the following: Haemonchus,
Oesophagostomum, Bunostomum spp. or, sometimes, Trichuris spp. (Georgi et al., 1972) are
the dominant nematodes. By contrast, anorexia, poor body condition and diarrhoea
characterise infections dominated by Trichostronglus and Cooperia spp. The occurrence o f
these signs in several animals, taken together with a good history and seasonal factors, is
sufficient to suspect PGE. However, differential diagnosis o f PGE is important in all
suspected cases since it can easily be confused with, and indeed compounded by,
malnutrition, chronic fasciolosis, coccidiosis, intestinal paramphistomosis (Butler and
Yeoman, 1962) and trypanosomosis. Thus, where applicable laboratory diagnosis should be
encouraged.
2 2 .2 .1 .2 Laboratory diagnosis
Laboratory procedures and findings arising from them should be considered as aids
of diagnosis. The most useful o f these procedures include (1) qualitative and quantitative
faecal worm egg counting procedures, (2) faecal culture for differential strongylid larval
counts, (3) pasture larval counts (4) haematological and serum biochemical examinations for
52
the investigation o f anaemia and for pepsinogen estimation, respectively and (5) post mortem
examination for quantitative differential worm counts and for gross pathological observations.
T h e most widely used laboratory technique is faecal worm egg count. However, only
quantitative techniques such as the McMaster technique and its numerous modifications
(Whitlock, 1948; Thienpont et al., 1979; MAFF, 1986; Hansen and Perry, 1994) as well as
quantitative flotation techniques (Jackson, 1974; MAFF, 1986) should be employed for
diagnostic purposes in ruminants.
The clinical importance o f hypobiotic larvae in ruminants is now well recognised and
their isolation and counting depends on standard procedure for making post mortem mucosal
analysis (Herlich, 1956; M AFF, 1986).
2 .2 .2 .7 .2 .1 Faecal egg counts
The use o f faecal egg counts as an ante mortem means o f diagnosing naturally
acquired GI nematode infections o f domestic livestock has been practised for many years.
This procedure is well developed, standardized and has recently been presented in a FAO
technical manual (Hansen and Perry, 1994). Although it is possible to derive a correlation
between faecal egg counts and total burdens of parasitic nematodes o f sheep and calves, the
correlation is poor for cattle o f more than one year (Rubin, 1967; Michel, 1968b; Brunsdon,
1971; Ploeger et al. (1994). To obtain reliable counts, particular attention must be paid to
the sampling o f adequate numbers of animals as well as to the methods o f collection,
transportation, storage and the actual examination o f the samples. As suggested by Gordon
(1967), samples should be collected from some o f the heaviest, best conditioned animals and
some o f the lighest, poorest specimens; a comparison of egg counts between the two groups
is often useful. Moreover, the clinician or parasitologist must be thoroughly familiar with the
53
numerous factors which influence the accuracy and diagnostic significance o f faecal worm
egg counts, usually expressed as eggs per gram o f faeces (epg) (Soulsby, 1982a; MAFF,
1986).
2 .2 .2 .7 .2 .1 .1 Factors affecting egg counts
Factors limiting the significance o f faecal egg counts includes:-
(a) Resistance o f the host animal can result in both depression or suspension o f egg
production by adult worms. Also, immature worms do not betray their presence by
laying eggs, yet the immature stages o f a number o f species are highly pathogenic.
(b) The number o f eggs produced per adult female worm also varies considerably between
species, i.e. a few Haemonchus or Chabertia may produce a similar total count to that
produced by many thousands o f Trichostrongylus (Brunsdon, 1970). This can make
interpretation of individual strongyle egg count difficult, though counts in excess of
1,000 epg o f faeces are generally considered an indicator o f heavy infections and
those over 500 o f moderate infection (Urquhart et al., 1987).
(c) Eggs o f Nematodirus, Trichuris and Capillaria can be identified whereas eggs of
major strongylids cannot be differentiated readily from each other, and they are
generally referred to as typical strongyle eggs when doing total egg counts.
(d) A fairly regular diurnal fluctuation in faecal egg count has been shown to occur, and
it is recommended that sampling should be undertaken at the same time of the day
(Spedding, 1952; M AFF, 1986).
(e) The number o f epg varies considerably depending on the consistency o f the faeces.
Fluid faeces due to diarrhoea will have less epg whereas, fasting reduces faecal output
which in turn increases epg count (Gordon, 1967).
54
0 Inherent deficiencies in egg counting techniques and in the rectal methods o f faecal
sam pling arising from the fact that the eggs are not evenly distributed through the
faeces can influence the accuracy p e r se o f individual egg counts. However, this
source o f error is not unduly great.
2 .2 .2 .7 .2 .1 .2 Faecal cultures
Differentiation o f typical strongyle eggs can be achieved by the use o f faecal cultures.
These provide an environment suitable for the hatching of the strongyle eggs and larval
development to the L3 which can be identified to genus level. The cultures can be left at
room temperature for 14-21 days, by which time all the larvae should have reached the
infective stage.
It is important to remember that faecal cultures indicate only which parasites are
present and not their relative numbers either in the host or in the original faecal sample. This
is because (a) the biotic potential (i.e. egg-laying) of parasites varies; and (b) different
parasite eggs have different optimum conditions for hatching, development and survival
(MAFF, 1986). Faecal larval counts, like epg counts, should only be used as an aid to the
diagnosis o f PGE.
2 .2 .2.7.2.2 Pasture larval counts
Larval recovery from pasture samples may be required in (a) epidemiological studies
(sometimes as part o f anthelmintic control programmes); (b) the diagnosis o f parasitic
diseases in grazing animals; and (c) establishing whether pasture of unknown grazing history
is safe for young stock, even though, absence o f L3 at certain time of year does not
necessarily mean that a pasture is worm-free.
55
Pasture larval counts may be influenced by several factors such as, season, weather,
and host immunity. O f major importance is stocking density, as higher densities result in
heavier pasture contamination and, therefore, greater numbers o f larvae on pasture (Armour,
1980).
2 .2 .2 .7 .2 .3 Blood parameters
Traditionally, the diagnosis o f GI nematode infections relies largely on faecal egg
counts. In the case o f abomasal infection, diagnosis can also rely on serum pepsinogen and
serum gastrin measurements as indicators o f abomasal changes.
2 .2 .2 .7 .2 .3 .1 Pepsinogen
A n increase in pepsinogen concentration is mainly a reflection o f development and
emergence o f larval stages o f Ostertagia with subsequent mucosal damage. Ostertagia
infection causes hypo- and metaplasia o f the parietal cells resulting in a decrease in acid
production and a subsequent reduction o f the pepsinogen transformation into pepsin. The
accumulated pepsinogen may escape into the blood between the broken cell junctional
complexes (Mylrea and Hotson, 1969).
T he importance of serum pepsinogen linked to ostertagiosis was first reported by
Anderson and colleagues (1965). Although considerable variations in serum enzyme activity
are observed in naturally infected animals, the value of this parameter in diagnosing
gastroparasitic disease is widely accepted (Berghen et al., 1987; Williams et al., 1987).
Also, a good correlation between increasing levels o f infection and pepsinogen concentration
has been reported (Jennings et al., 1966; Mylrea and Hotson, 1969; Snider et al., 1981).
However, the relationship between pepsinogen and the actual internal worm burden is not as
56
strong as that o f the egg count in moderate infections (Murrell et al., 1989).
Other parasitic or non-parasitic diseases may be responsible for a moderate rise in
pepsinogen concentration. The abomasal parasites such as T. axei and Haemonchus spp.
produce inconsistent rises in blood pepsinogen (Ross et al., 1967; Bourdeau, 1985). Other
non-abomasal parasites such as Cooperia spp. and D. viviparus cause minor rises of serum
pepsinogen (Kloosterman and Frankena, 1988).
T h e only studies on variations of pepsinogen levels throughout ovine haemonchosis
were carried out by Mapes and Coop (1970) and Coop (1971). These authors showed that
massive infection with one million L3 of H. contortus caused lesions in abomasal mucosa and
rise in pepsinogen level above 1500m/z tyrosine compared to 300 to 600 in uninfected
animals. Under natural conditions, worm load is never so high; therefore pepsinogen level
is not a reliable parameter in assessment o f pathophysiological changes due to haemonchosis.
2 .2 .2 .7 .2 .3 .2 Gastrin
The use of the gastrin assay as a diagnostic tool for demonstrating ovine and bovine
ostertagiosis was mentioned by Anderson et al., (1981), Entrocasso et al. (1986c), Fox et
al. (1987) and Hilderson et al (1992).
As demonstrated for pepsinogen, other abomasal or intestinal parasites can result in
gastrin increase (Reinemeyer et al., 1981; Fox et al., 1988). Fox and colleagues (1991)
demontrated increased levels o f gastrin and pepsinogen in H. contortus experimentally
infected Malaysian goats. The magnitude o f the blood gastrin response was significantly
greater than that of pepsinogen during the period that both blood values were elevated. Other
effectors o f fluctuations in the level of bovine gastrin are lactation, abomasal lesions such as
ulcerations, sand impaction and abomasal leucosis (Luthman et al., 1979; Schillhorn van
57
Veen, 1 9 8 8 ).
Several authors have confirmed the usefulness of determining pepsinogen and gastrin
levels for confirm ing clinical disease in calves during their first grazing season (Entrocasso
et al., 1986c; Dorny et al., 1988; Berghen et a l., 1990). However, the value of these
parameters for detecting subclinical parasitism is questionable (Berghen et al., 1993). These
parameters are not really suitable for use by diagnostic laboratories because they are labour
intensive and expensive methods. Therefore, they have so far mainly been used for research
(Ploeger et al., 1994; Eysker and Ploeger, 1995).
2 .2 .2 .7 .2 .3 .3 Albumin
M any authors report a sharp decrease in total proteins and albumin after an infection
with GI nematodes in ruminants (Kuttler and Marble, 1960; Ross and Armour, 1960a). This
decrease has to be related to an increase in tissue permeability and a plasma leak towards
lumen o f the gut and a rise in the albumin catabolism. A decrease appeared as early as the
5th day after the lambs were infected with Teladorsagia ( Ostertagia) circumcinta (Holmes
and M cLeans, 1971). Ross and Armour (1960a) showed that serum albumin and packed cell
volume percentage were useful measures o f pathogenicity o f H. contortus in sheep, when
considered in conjunction with a series o f differential faecal egg counts.
2 .2 .2 . 7 . 2 . 3 . 4 Inununo-diagnosis (serodiagnosis)
Western blot and enzyme-linked immunosorbent assay (ELISA) have been used to
detect diagnostic antigens in O. ostertagi (Cross et al., 1988), D. viviparus (Leeuw and
Cornellissen, 1991) and H. placei (Schallig et al., 1995) infections in cattle. ELISA using
crude Ostertagia and Cooperia antigens correlate better with exposure levels when production
58
losses are lik ely to occur. In particular, crude Cooperia antigens appear to be useful because
a correlation with infection levels is observed from approximately six weeks after the
beginning o f exposure onwards (Ploeger et al., 1994). The ELISA is far less labour intensive
and can even be automated. Nevertheless, it has not yet been used for other purposes than
research.
The availability o f serological methods for the estimation o f nematode infection in
cattle and sm all ruminants in the tropics would be very useful, particularly for Haemochus
spp. the m ost important nematode in most tropical regions. These methods should be used
for herd monitoring and not for diagnosis in individual animals. The latter is probably not
feasible considering the wide variation in the humoral response against worm antigens
(Eysker and Ploeger, 1995).
2.2.2.7.3 Biotechnology and the diagnosis of nematode infections
Strongylid infections have mainly been diagnosed by determination of faecal egg
counts. However, the eggs o f most species (except for Nematodirus) are morphologically
indistinguishable at the generic level (Georgi and McCulloch, 1989); hence their
identification requires faecal culturing to produce L3. Even then, it is difficult to accurately
identify the larvae of some species using morphological characteristics (Hubert and Kerboeuf,
1984; Berrie et al., 1988). The development o f rapid and sensitive molecular techniques for
the identification of nematode species is o f significance for their control.
Recently, DNA sequences specific and sensitive for the four common cattle nematode
genera, Haemonchus, Ostertagia, Cooperia and Oesophagostomum were identified by
"Shortgun" cloning, to develop a rapid, reliable, and reproducible DNA-based test for ante
mortem identification o f these parasites (Christensen et al., 1994). At present, the major
59
drawback o f this technique is that parasite eggs still must be isolated from faeces; however,
the preparation need not be highly purified because these probes do not cross react with host
DNA (Zarlenga, 1994).
A second method, polymerase chain reaction-linked restriction fragment length
polymorphism (PCR-RFLP) o f ribosomal genes has been used to discriminate between
closely-related species o f trematodes (Anderson and Barker, 1993) and cestodes (Wachira et
al., 1993). Techniques o f this nature have been developed for identification and
differentiation o f the morphologically similar H. contortus and H. placei (Zarlenga, et al.,
1994). Prior to the development o f PCR primers, H. contortus and H. placei could be
differentiated with confidence only when a population o f worms was examined, because of
the overlapping range o f variation in the morphological characteristics.
A s it is possible to amplify ribosomal genes from single nematode eggs (Gasser et al.,
1993), the PCR-RFLP approach has potential to develop a rapid and sensitive diagnostic
system. It will be a useful experimental tool to identify female nematodes o f different
species, where morphological criteria are insufficient to delineate between species (Gasser
eta l., 1994).
However, to Eysker and Ploeger’s (1995) opinion, DNA probes in dot blots or in the
PCR will not be very helpful for routine diagnosis o f GI nematode infections because they
will not give useful quantitative information. These methods would certainly allow a more
accurate speciation o f nematode eggs in the faeces, giving a more accurate differential faecal
egg count. A more promising use for DNA technology may be in monitoring development
of anthelmintic resistance (Kwa, 1994).
60
.3 Principles of helminth control
Eradication o f most helminth infections is not practical and, generally, such a course
s not required in order to control economically important helminth diseases o f livestock
Gordon, 1957; Spedding, 1969). Rather, the aim o f control is to ensure that parasite
>opulations do not exceed levels compatible with economic production. This objective may
>e achieved by using one o f three interrelated approaches, namely chemotherapy involving
:he use o f anthelmintics at selected times, grazing management and provision of the animals
with a certain degree o f immunity. Potentially, the most efficient control requires the
complete integration o f all the three facets. This is possible only on the basis o f a full
understanding o f the epidem iology o f helminth infections (Brunsdon, 1980).
In developing countries o f Africa, there are hardly any set plans of prophylactic
control o f GI helminths. This is largely due to lack o f awareness o f the value o f routine
disease control measures, other than those for the well known killer diseases. Anthelmintic
use in sm all-scale and nomadic production systems is limited and, treatments are carried out
largely curatively only as livestock owners do not see the need to control until animals are
in extremis. The results are often unsatisfactory and not cost effective (Fabiyi, 1987).
Organised worm control is practical only in modern systems o f production found in large
privately-owned as well as in institutional farms and ranches. Parasite control under the latter
situation is carried out against a background of grossly inadequate epidemiological data,
unreliable backup veterinary advice and diagnostic services, lack o f competent farm
management and organisational skills necessary to understand and implement modern control
strategies, and chronic shortage and high cost of essential anthelmintics.
61
£ .3.1 Control o f parasitic gastroenteritis in cattle
There are three practical methods o f controlling PGE, namely, pasture management
ind grazing hygiene, anthelmintic medication and the integrated method, which combines
[ imited anthelm intic treatments with other measures such as grazing management (Brunsdon,
1972; D ow n ey, 1973; Michel, 1976).
2.3.1.1 Pasture management and grazing hygiene
The essential features o f this method of control which has been well perfected in
modern intensive systems o f production in other parts of the world, were outlined and
discussed by Michel (1976, 1982). It requires, among other things, detailed knowledge o f
the seasonal dynamics o f infection in pasture and animals as well as o f the infestation status
of all available pastures throughout the grazing season. Based on such detailed
epidemiological information, various managerial options have been devised which achieve
clearly defined objectives under given husbandry situations.
It is evident that these relatively sophisticated management practices cannot be easily
implemented under our local conditions without modifications, especially in the humid zones.
In these zon es, free-living development is very rapid, transmission of infection occurs all the
year round, resulting in several parasite generations per annum, and heavy pasture infestation
can build up soon after turn-out. Thus, "clean" and "safe" pasture, as defined by Michel
(1982), may be difficult to provide under intensive system o f management in the humid
zones. It would probably be necessary for pastures to remain free o f stock for at least 6 to
8 weeks before they can attain a "safe" pasture status (Fakae and Chiejina, 1988). On the
other hand, "clean" pastures occur naturally at the start of the rains in the dry tropics and
such pastures could be utilised to device appropriate grazing management programmes in
62
those localities where the relevant epidemiological data is available.
2.3.1.2 Control based on anthelmintic usage
A nthelm intic drenching may be empirical, curative or preventive. Empirical drenching
is not based on any strategy. Whereas, in curative drenching, treatment is often delayed until
pastures are heavily infested and clinical signs or death occur (Herd, 1988). It has the
disadvantage that considerable production losses have already been incurred by the time
clinical sign s are visible in the host (Michel, 1976), and reinfection takes place directly after
drenching unless the animals are removed from the infested pasture at the time o f treatment.
Despite the disadvantages, curative drenching is favoured by some, as it causes a relatively
low selection pressure for resistance, and because it is considered unnecessary to drench adult
animals routinely (Brunsdon et a l., 1983).
Preventive drenching is most important for forestalling excessive contamination o f the
pasture w ith free-living stages o f the worms, and thus minimising the exposure o f susceptible
hosts to nematodosis. Preventive drenching may be applied in the form o f strategic or tactical
drenching.
2.3. 1.2 .1 Strategic drenching
Strategic drenching comprises treatment at predetermined intervals, based on seasonal
fluctuations in the prevalence o f specific worm species; on managerial considerations such
as weaning; or on combination o f these. Thus, it can be regarded as a regular drenching
programme and when applied in conjunction with other methods o f control such as pasture
spelling, the system can be termed integrated strategic worm control.
Most often, strategic drenching consists o f a series o f drenches at the start of the
63
^orm season, when the worm species concerned commence egg production, and conditions
rjecome favourable for the development of free-living worm stages on pasture. This ensures
that worms d o not accumulate excessively at the beginning o f the season, and constitute a
threat to su sceptib le animals later.
Strategic drenching in the "off-season" when conditions are unsuitable for worm
development on pasture and the worms that do occur in the animal are usually hypobiotic is
referred to as offensive or "extended" drenching (Reinecke, 1983). Another variation o f
preventive treatment is suppressive drenching, also termed "protective" drenching. In this
approach, nematodosis is suppresed when it becomes an immediate threat to the animal. The
most important difference from other methods o f strategic drenching, is that treatment is
delayed until worms have substantially contaminated the pasture and are accumulating in the
host. Treatment therefore suppresses the parasite in the host, before it can do significant
damage.
T h e suppressive treatment is commonly applied as continuous low-level administration
of the drugs (in licks, or by means o f slow-release devices) or as repeated drenchings at
intervals as short as every 2-3 weeks while the worm threat remains. This form o f control
can be very effective (Brunsdon, 1980), but is dependent on the intensive use of drugs, thus
considerably in c re a s in g the chances o f selection for anthelmintic resistance (Martin, 1985).
2.3.1.2.2 Tactical drenching
Tactical drenching consists o f preventive drenching when an excessive accumulation
of worms is to be expected, e .g . after good soaking rains when the climate is suitable tor
development of the preparasitic worm stages on pasture. Usually, tactical drenching is used
to support the strategic drenching programme for those periods when the set drenches are not
64
sufficient for the expected worm challenge (Van Wyk, 1990a). Depending on the timing,
tactical drenching can be either preventive (e.g. at the time that the climate first becomes
favourable for the accumulation o f worms on pasture), or suppressive, after considerable
numbers o f L, have already become available on pasture.
N o hard and fast rule can be laid down for the timing o f tactical drenches. Thus, it
is advisable to drench tactically after rains have fallen over a period o f 15 to 30 days and
then to m o v e the animals to safe pastures if possible. The drenching should commence about
3 to 6 w eek s after the start o f the good rains, and the course o f the infection in the animals
should b e monitored by means o f the faecal worm egg counts, to guard against overwhelming
infections (van Wyk, 1990a).
2 .3 .1 .2 .3 Anthelmintic treatment strategies in the tropics
T h is is by far the most popular and in som e cases such as the ranching system, the
only realistic control measure. It relies exclusively on the use of drug treatment to control
worm infections. Theoretically, a single treatment o f all stock during the dry season, in the
dry tropics, with one o f the broad spectrum anthelmintics effective against adult worms and
arrested larvae should ensure that all animals are free of worms at the start of the succeeding
rainy season when all new pastures should also be clean. In such a situation, pastures should
remain relatively "safe" for the rest of the rainy season. However, this requires detailed
study and evaluation, particularly with regard to the optimum frequency and timing o f the
treatments, the associated pasture changes and their effects on pasture contamintions, worm
burden and performance of animals.
Worm control by anthelmintic treatment alone in the humid zones and in those parts
of the savanna areas with a long (6 to 7 months) rainy season is problematic and relatively
65
expensive since several treatments spread throughout the year are likely to be required and
the frequency and timing o f such treatments have not been properly determined. However,
Chiejina and Emehelu (1986) evaluated three anthelmintic programmes in intensively
managed N ’dama cattle in the Nigeria derived savanna and found that at least one dry season
and two w et season treatments were necessary to prevent significant infection and obtain
satisfactory growth rates in calves. Unfortunately, these studies do not provide a basis for
a firm recommendation o f treatment programmes for use in other situations.
2.3.1.3 Integrated worm control
Integrated worm control denotes different forms of rotational grazing, with or without
anthelmintic drenching at the time of withdrawal o f the livestock from the pasture. It is
mainly based on two phenomena: the adult worm does not have long life span in the host,
and the w orm ’s free-living stages on the pasture, develop at different rates during the various
seasons o f the year (Van W yk, 1990b). This control method demands even more careful
planning as well as experience and skill in the timing of treatments and movement o f stock
to clean or safe pastures. Potentially, it offers the best option for economic utilisation of
anthelmintics and available pastures as well as reduces the risks of anthelmintic resistance.
It is, t h e r e f o r e , ideally suited to modern intensive systems o f prodution but could be adapted
to small scale semi-intensive traditional systems such as those involving rotational tethering
or other forms of confinement o f relatively large numbers of small ruminants to limited
grazing plots.
Pasture spelling or rotational grazing, the cornerstone of integrated control, comprises
the resting o f the pasture until the free-living worm stages no longer constitute an immediate
threat to the host. There are various ways in which this reduction in pasture infectivity can
66
be achieved classical pasture spelling; alternation o f different host species on pasture;
alternation o f susceptible and insusceptible hosts o f same species; alternation of pasture and
crop aftermaths; combined alternation o f crops and different animal species; and creep
grazing for young animals (Van Wyk, 1990b).
T h e effectiveness o f rotational grazing system involving only cattle is questionable
(Michel, 1969a; 1976; Morley and Donald, 1980). Under the rotational grazing system part
of the pasture will be left ungrazed over a shorter or longer period, and the development
and/or survival o f free-living parasite stages will be favoured under the shelter o f growing
herbage. In contrast, continuous grazing o f set-stocked animals on pasture eliminate the
herbage covering the free-living stages with eventual increased harmful exposures to
dessication, sunlight etc. Brunsdon (1980) suggested that production o f "safe" pasture by
spelling would require an interval o f 3 months or more before regrazing. On the other hand,
efficient pasture utilization would normally dictate that grazing interval in a rotation could
be no longer than 6-8 weeks. Grazing susceptible stock on such pasture after this interval
may w ell subject them to peak levels of larval availability (Bisset et al., 1991).
Better control has been achieved by integrated rotational grazing with different age
categories, i.e. the so-called "leader/follower" or "dilution" systems (Leaver, 1970).
However, alternate or mixed grazing with two host species, i.e. sheep and cattle, is a feasible
control measure in areas with mixed husbandry systems. Both of these methods, which are
based on parasite-host specific relationships, will usually reduce pasture infectivity of a given
species and show benefits for both host species (Southcott and Barger, 1975; Helle, 1981).
The control o f helminth infections in Kenya is largely based on the use of
anthelmintics and pasture management is rarely practised. In the high rainfall districts,
internal parasite control is often based on repeated curative treatment during times o f high
67
transmission and there has been no attempt to control by strategic, preventive anthelmintic
treatment. Drenching is normally done at irregular intervals without following the
epidemiology o f the parasites. The most common practice is to treat animals, especially
young cattle at intervals o f approximately 3 months. A large proportion o f animals in the
arid/semi arid zones is probably never treated with any anthelmintic during their lives
because anthelmintics are not affordable or available to all farmers. However, in some areas,
peasant farm ers and pastoralists are using large amounts o f anthelmintics (Kinoti et al. 1994).
Attempts should be made to test strategic control schemes based on the epidemiological
investigations by Allonby and Urquhart (1975) and Straat (1979).
2.3.2 Availability and distribution of anthelmintics
A lthough there are increasing efforts to develop sustainable control programmes that
can reduce the dependence on anthelmintics, it is highly unlikely that these will be completely
replaced by alternative farming systems, vaccines or biological control methods. For the
short term , at least, protection o f the effectiveness and availability o f these modern
anthelmintics is critical as they have a great potential role to play in the control of
helminthosis in the tropics. However, the availability o f anthelmintic drugs at prices that are
locally acceptable, from values and marketability o f animals and animal products, vary much
from country to country and from one husbandry system to the other (FAO, 1991).
Anthelmintic treatment against helminth infections in the tropics is faced with two
major obstacles, namely, cost o f drugs and their proper use at farm level. The first problem
may be solved by the manufacturing and marketing of cheaper versions of the efficient
anthelmintics (i.e. benzimidazoles) introduced from the 1960’s and no longer protected by
the original invention patent. Whereas, the second problem is linked with the educational
68
levels, com m unity infra-structures and activities o f agricultural and veterinary extension
services (N an sen , 1991).
2.3.2.1 Dosing methods
Anthelm intics used against GI nematodes are given by parenteral, oral, topical or
intraruminal routes. Oral formulation involves the use o f tablets, gels, pastes, drenches or
granules or powders for inclusion in-feed or in-water. Accuracy of dose is best achieved by
oral or parenteral administration because in-feed or in-water applications are notoriously
inaccurate since the greedy animals consume more than others. It is also important to realise
that infections often suppresses appetite resulting in low uptake o f the drug by infected
animals (A bbott et al., 1985).
In-feed methods also run the risk o f promoting the development o f resistance since
overdosing will lead to high selective pressure on resistance genes. In spite of these
drawbacks, since handling and dosing are expensive on time and labour, in-feed preparations
will continue to be attractive to the farmer. Studies are being done on the incorporation ot
fenbendazole into molasses "blocks" (Miller et al., 1992; Sanyal et al., 1995).
Oral drenching of ruminants carries with it the risk that portions o f the drench will
bypass the rumen via the oesophageal reticular groove and hence pass directly to the
omasum/abomasum. In some animals this eosophageal groove reflex persists after weaning
and will occur in response to drenching. To circumvent this problem a special gun is now
available in some countries e.g . Australia (Bogan and Armour, 1986) and Britain (Coopers
Autoworm injector) which delivers oxfendazole through the skin and directly into the rumen.
This allow s the treatment o f large numbers of cattle over a short period o f time.
Working with oxfendazole, Ali and Hennessy (1993) have shown that anthelmintic
69
efficacy in sheep can be elevated by temporarily reducing feed intake. In practice, the
temporary feed restriction could be achieved by holding animals in a paddock which
contained little feed prior to and after drenching. After treatment, this paddock would also
serve as a quarantine area which would retain nematode eggs as they are passed in faeces
from the treated animals.
O nly levamisole and ivermectin are currently available as pour-on topical applications.
Levamisole is used for the treatment of GI nematodes of cattle. However, it does not give
as good a protection as that o f the subcutaneous or oral routes (Sievers and Guzman, 1991).
Furthermore, the uptake and hence its efficacy varies considerably depending on the climatic
conditions at the time o f administration with lower absorption at low temperatures (Forsyth
e ta l., 1983).
2.3.2.1.1 Slow and pulse release methods
For the control o f endoparasitic nematodes o f ruminants and cattle in particular, the
development o f sustained-release bolus technology for the administration o f anthelmintics is
viewed as an important advance (Zimmerman and Hoberg, 1988). The use o f a bolus allows
a measured quantity o f drug to be delivered directly to the rumeno-reticulum over an
extended time period. This allows for a reduction in labour costs to the farmer and handling
stress to the animal while giving sustained anthelmintic cover. These bolus delivery systems
are based on either continuous or intermittent release of the anthelmintic drug (McKeller,
1988).
Morantel has been incorporated into two sustained-release devices for cattle. The first
was a ruminal bolus (MSRB; ParatectR Bolus, Pfizer Inc.) designated to provide delivery o f
drug for 60-90 days (Jones, 1983). The second, more recent, device (MSRT; Paratect FlexR
70
Bolus, Pfizer Inc.) is a laminated ethylene vinyl acetate sheet containing 11. 8g o f morantel
tartrate. T he bolus is administered rolled in a cylinder with a cellophane retaining tape.
Following oral administration the tape and the sheet is retained in the reticulo-rumen by
virtue o f its geometry (M cKeller, 1994).
T he Paratect FlexR bolus releases morantel tartrate at a controlled and sustained rate
for 90 days (Cardinal et al., 1988) through holes punched in the laminate. It has a more
consistent release profile than the solid ParatectR bolus and has been shown to reach steady
state zero-order rate after 10 days (Boettner et al., 1988). The abomasal and ileal
concentrations o f morantel tartrate remain at approximately 1.0 ^g ml'1 for 98 days after
administration (Lanusse et a l., 1992). The release profile has been shown to confer
protection o f first year calves throughout a 90 day grazing period (Vercruysse et al., 1989).
A similar device (chronomintic) is also available for delivery of levamisole in the reticulo-
rumen o f calves (Probert, 1994). Ivermectin is now available as a sustained release bolus for
cattle. The IvomecR SR bolus (Merk & C o.) is based on the principle o f an osmotic pump
and has been developed to deliver approximately 8 mg or 12 mg day'1 (for 200 kg or 300 kg
animals, respectively) over a 135 day period. The bolus is held within the rumen by high
specific gravity conferred by an iron densifier at one end. Steady state plasma concentrations
of ivermectin are achieved within 14 days of administration of the bolus and the release-
plasma concentration relationship is linear (Pope et al., 1985). The ivermectin bolus has been
found to be highly effective against GI nematode and lungworm infections in first-year
grazing calves (Schneider et a l., 1996).
Bolus preparations are available for the convenient administration of benzimidazoles
to cattle and sheep. Weighted benzimidazole boluses for cattle have been designed to release
therapeutic doses o f drug at time intervals approximately equal to the prepatent period o f the
71
common parasitic nematodes. The oxfendazole pulse release bolus (Repidose, Autoworm,
Coopers A nim al Health) is designated to release 750 mg or 1.25 g tablets o f oxfendazole for
100-200 k g and 200-400 kg cattle, respectively (M itchell, 1987; Herbert and Probert, 1987).
T h e most sophisticated pulse release bolus is the E-Bolus (SmithKline Animal Health
Products) which is an electronic device delivering three doses o f albendazole at 31 days
intervals to cattle. Contact with the ruminal fluids activates a timing device run by alkaline
batteries which after 31 days interval generates a gas (mainly carbon dioxide) which drives
out the d ose o f anthelmintic (Gyurik and Bagnall, 1986). A biodegradable fenbendazole
sustained release bolus is now available for use in cattle. Approximately 0.2-0.4 mg of
fenbendazole per kilogram body weight per day are released over 130 days. This bolus has
been show n to prevent dictyocaulosis and heavy infection with GI trichostrongylids, thus
conferring a production benefit (Downey et al., 1992).
T he effect o f slow release formulations on the development o f resistance has yet to
be assessed but it seems likely that it will be enhanced by their use (Anderson, 1985; Donald,
1985). On the other hand, the successful use of ParatectRfor more than ten years has yet to
be associated with reports o f resistance (Coles et al., 1994). Donald (1983) suggested that
these d evices may not be hazardous in this respect provided the total release time is less than
the maximum life span of the parasite’s free-living stages, there is high kill rate and the
release rate declines rapidly to zero at the end o f its life. The device has to be infrequently
used (Probert, 1994). Sustained release devices are now being offered in the developing
countries at prices that are competitive with the oral formulations (FAO, 1991).
72
2. 3. 2 .2 Anthelmintic characteristics o f mo rantel and albendazole
2. 3.2 .2 .1 Morantel
Morantel and pyrantel are anthelmintic compounds that belong to a family classified
as tetrahydropyrimidines (Lynch and Bartolucci, 1982). Morantel (1-4-5-6-tetrahydro-l-
methyl-2-[trans-2-(3-methyl-2-thienyl) vinyl] pyrimidine) is a methyl ester analogue o f
pyrantel and is formulated as the tartrate salt for the control of nematode infections in
domestic animals.
Studies investigating the mechanism o f action o f morantel show that the drug inhibits
the enzym e, fumarate reductase, which plays an important role in energy metabolism of
parasites; the enzyme is not present in the tissues o f the vertebrate host (Behn and Bryant,
1979). Additionally, morantel affects the nervous system o f nematodes causing contraction
and death (Coles, 1977).
Morantel is a broad-spectrum group 2 anthelmintic highly effective against most
nematodes o f ruminants (Jones et al., 1978; Pott et al., 1979). Morantel tartrate at 10 mg
had high efficacy against adult and immature stages of the GI nematodes, including
Nematodirus battus , in cattle and sheep. Also, low level administration in feed (1.5 mg/kg
day1) resulted in reduced faecal egg counts and post mortem worm burden in cattle and
sheep (Jones et al., 1978). In lactating grazing adult dairy cows given a morantel sustained-
released bolus, Bliss et al. (1982) reported a highly significant improvement in milk
production, milk fat and protein content compared with untreated animals.
2 .3 .2 .2 .2 Albendazole
Albendazole (methyl|5-(propylthio)-lH-benzimidazole-2-yl] carbamate is a potent
member o f the benzimidazole group of anthelmintics with broad spectrum activity against GI
73
nematodes including larval stages, tapeworms, liver flukes, and lungworms in many host
species (Theodorides et al., 1976; Williams et al., 1977; Wescott, et a l., 1979).
A lbendazole has been w idely used in veterinary medicine and human clinical medicine
a s a safe anthelmintic with high activity against larval and adult stages o f many helminth
parasites. In addition to its vermicidal and larvicidal properties, albendazole is also ovicidal
and attention has focused on its use in systemic helminth infections such as hydatid disease,
cysticercosis and systemic nematode infections of man (Horton, 1990). The mode o f action
in such parasitic infections is believed to derive from the inhibition of tubulin polymerization
into m icrotubules, with a cascade o f other metabolic effects resulting from this (Lacey,
1990). T able 2 .4 shows anthelmintics available for the control o f nematodes in cattle.
2.3.3 Anthelmintic resistance
Anthelmintic resistance in nematodes can be a problem in small ruminants, horses,
cattle and swine. The most widespread resistance problems occur to benzimidazole
anthelmintics in nematodes o f sheep, goats and horses (Prichard, 1994; Waller et al., 1996).
In contrast to the situation in sheep and goats, resistance has been slow to develop in cattle
(Craig, 1993). Barger (1993a) suggests that bovine dung-pats may provide a relatively larger
refugia o f susceptible infective larvae, and hence, reduce the proportion o f the population
exposed to anthelmintic selection. Alternatively, less frequent use of anthelmintics in this host
may minimize selection pressure (Waller, 1994). It has been suggested (Eagleson and Bowie,
1986; W aller, 1993a) that selection for resistance in some parasites o f cattle occurs in other
species, such as goats, which can harbour species o f nematodes common to both species. As
noted in Table 2.5, few reports o f resistance are available, but in many cases the parasite
identified as being resistant is O. ostertagi. Since, with a single exception, all o f the reports
74
y i resistance to date are for levamisole/morantel or benzimidazole, both o f which provide
ess than op tim al protection against inhibited larval stages, it is possible that resistance has
developed in response to what amounts to subtherapeutic dosing of inhibited larvae (Conder
and C am pbell, 1995). Populations o f Haemonchus spp., T. axei and C. oncophora resistant
t o the benzim idazoles have also been identified sporadically. Boersema (1983) reported a
strain o f D . viviparus resistant to levamisole, and Watson (1993) has identified a Cooperia
spp. resistant to ivermectin.
T h ere is ample evidence that anthelmintic usage in certain regions of sub-Saharan
Africa is h ig h , particularly during the rainy seasons and this may lead to development o f
widespread, and possibly high levels of anthelmintic resistance (Waller, 1993b). This view
is supported by recent reports o f anthelmintic resistance and multiple anthelmintic resistance
in Tanzania (Bjorn et al., 1991), Cameroon (Ndamukong and Sewell, 1992), Nigeria (Mbah
et al., 1 9 9 2 ) and Kenya (Njanja et al., 1987; Mwamachi et al., 1995; Wanyangu et al.,
1996), In Africa, the development o f anthelmintic resistance and drug resistance in general,
is further compounded by the use of drug preparations of questionable efficacy (Baker,
1995b; W anyangu et al., 1996).
2.3.3.1 Factors associated with resistance
T h e main factors associated with anthelmintic resistance are frequent usage o f
anthelmintics, underdosing and continuous use o f anthelmintics from the same class,
irrespective o f whether different brands or formulations were used. Other factors such as the
relative importance o f parasite species, the percentage of the parasite population which is
under selection pressure, animal management practices and the degree to which resistance
has been specifically investigated, are also of significance in relation to the magnitude and
75
T ab le 2 .4 : A n th e lm in tic a v a ilab le fo r the c o n tro l o f n e m a to d e s in c a ttle 3
Chemical Trade Name Gastrointestinal Nematodes Dose (mg kg'1)
Adults Developing Inhibited larvae Lungworms

larvae
Thiabendazole Thibenzole + + ± ± 66-110
Parbendazole Topclip + + - - 20-30
Oxibendazole Anthdworm + + - - 10
Cambendazole Novazole + + - - 25
Fenbendazole Panacur + + + + 7.5
Oxfendazole Systemex + + + + 4.5
Albendazole Valbazen + + + + 7.5
Febantel Bayverm + + ± + 7.5
Thiophanate Nemafax + + ± ± 66-132
Levamisole Nilverm + + - + 7.5
Ivermectin Ivomec + + + + 0.2
Morantel* Paratect + + + - 90 day '1 for 60days
+ = effective; ± = variable activity; - = inactive.

Febantel, fenbendazole, oxibendazole and albendazole are also active against tapeworms while albendazole shows variable activity
against liveflukes and ivermectin shows activity against ectoparasites.
‘Used as a slow release bolus.
“Based on Marriner and Armour (1986).

prevalence o f anthelmintic resistance (Waller, 1987). There are also justifiable grounds for
concern that the trend to use anthelmintic sustained-release devices may accelerate the
appearance o f resistance in bovine parasites (Donald, 1985).
2 .3.3.2 Detection o f resistance
Several in-vitro techniques have been developed for the detection of anthelmintic
resistance, but the procedure o f choice for field survey investigation is the faecal egg count
reduction test (FECR) (Presidente, 1985; Waller, 1986; Johansen, 1989). FECRT involves
the treatment o f naturally infected animals and can be used with ruminants, horses and pigs,
with all types o f anthelmintics and with all species o f nematodes in which eggs are shed in
the faeces. T o overcome obvious limitations and deficiencies o f this procedure (Waller, 1986;
McKenna, 1987; Lacey et al., 1990), guidelines have been recommended for all phases o f
the procedure, and standardised microcomputer software has been developed so that data on
the epidem iology of resistant nematodes can be easier to produce and results widely accepted
(Coles et a l., 1992).
2.3.4 Alternative control methods
Resistance to anthelmintic drugs (Waller, 1987) and demand for lower levels o f
chemical residues in livestock products and in the environment (Strong et al., 1996), together
with diminishing prospects for new classes of drenches, has stimulated interest in helminth
control methods which are less reliant on chemotherapy. In Africa the high cost and poor
availability o f effective anthelmintics are further limitations on their use. Thus, there is
considerable incentive to develop alternative methods of control. This could be attractive if
such alternatives could be effected at lower costs.
77
Table 2.5: Nematodes o f cattle with reported resistance to broad-spectrum anthelmintics
Antehelmintic Class 2
Nematode Country Benzimidazoles Levamisole/Mora- Macrocylic lactones

ntel/Pyrantel
Haemonchus spp. Brazil 1 _b -
Ostertagia ostertagi Australia 2,3 2 -
Belgium - 4 -
New Zealand 5 - -
United States - 6,7 -
Trichostrongylus axei Australia 8,9 - -
New Zealand 10c - -
Cooperia onchophora New Zealand 5,11 - 12c

Dictyoculus viviparus Belgium - 13 1
References: (1) Pinheiro and Echevarria, 1990, (2) Anderson, 1977, Anderson and Lord, 1979, (4) Geerts et al., 1987,
(5)Hosking and Watson, 1991, ( 6) Williams, 1991, (7) Williams et al., 1991, ( 8) Eagleson and Bowie, 1986,
(9) Eagleson et al., 1992, (10) McKenna, 1991, (11) Jackson et al., 1987 (12) Watson, 1993, (13) Boersema, 1983.
b-, No known report. cGenus but not species identified.
2 . 3 .4.1 Prospects o f vaccines
T h e only effective vaccines against parasitic nematodes in domestic animals depend
on the u se o f irradiated larvae and whilst these have been successful against lungworms
(Peacock and Poynler, 1980; Dhar and Sharma, 1981; Armour, 1987) and successful
experimentally, although not commercially, against canine hookworm (Miller, 1978), they
are not effective against nematodes as pathogenic as H. contortus in lambs. However, with
the advent o f DNA technology, considerable progress towards development of commercially
available vaccines for the control o f helminth parasites of domestic animals has been made
for the last few years particularly with species that infect ruminants (Dineen, 1985; Emery
and W agland, 1991). The publication by Johnson et al. (1989), detailing the development of
a vaccine against Taenia ovis infection in sheep, was the first to describe a highly effective
recombinant vaccine against a parasite. The vaccine remains the most effective o f the defined
antigen vaccines described todate (Lightowlers, 1994). Current work on a commercial
recombinant vaccine against F. hepatica in ruminants appears to stand a good example for
the development o f recombinant vaccine in general (Zahner,1994).
One approach towards the immunological control of blood-feeding nematodes like H.
contortus has been to immunize the host with parasite gut proteins (Smith, 1993). Antigens
associated with the gut of H. contortus have been shown to be capable of inducing host
protective immune response in vaccinated sheep (Tavernor et al., 1992a,b). Antigen H l l ,
an integral membrane glycoprotein in the intestinal microvillar membrane has been
characterised, and expressed in baculovirus (Munn et al., 1993a; Newton, 1995). Gut
associated antigens, rich in H l l , have been tested experimentally in Merino Sheep in South
Africa with high efficacy (Munn et al., 1993b). Development and field-testing o f a
commercial product with suitable adjuvants is required (Reinecke, 1994). Vaccines will form
79
part o f sustainable comprehensive control programmes and will integrate with drenching,
grazing management, biological control methods and genetic selection to prolong the effective
life o f anthelmintics, protect highly susceptible young stock and reduce contamination o f
pasture in successive seasons and generations o f grazing livestock (Emery et al., 1993;
Barnes et a l ., 1995). The use o f vaccines however, will require careful cost-benefit analysis,
based on thorough epidemiological knowledge, prior to instituting vaccine-based control
programmes (FAO, 1991).
2.3.4.2 Genetic resistance
Another potential source for additional helminth parasite control is the enhancement
of genetically-based resistance to infection. Considerable research has been carried out on
sheep, less so on cattle, and the result clearly demonstrated that there is considerable
variability both between and within breeds in resistance to infection and its impact on certain
production traits (Esdale, et a l., 1986; Owen and Axford, 1991; Baker et al., 1993).
The most comprehensive research on breed difference has been carried out at the
CSIRO Tropical Cattle Research Centre at Rockhampton, Australia (Vercoe and Frisch,
1992). It has been clearly documented that Bos indicus cattle (i.e. Brahman and Brahman
crosses) are more resistant to both GI nematodes and tick (B. microplus) than Bos taurus
breeds (Hereford and Shorthorn). In West Africa there is also some limited evidence that the
trypanotolerant N ’Dama cattle are more resistant to endoparasites than Zebu cattle (Claxton
and Leperre, 1991). Ouedraogo et al. (1991) detected lower H. contortus burdens in Baole’
than Zebu cattle in Burkina Faso.
It has been shown that variation in resistance to nematode infection within sheep
breeds is as great as between breeds (Barger, 1989). In cattle, Ross and colleagues (1960b)
80
identified a Zebu-bull in Nigeria whose progeny showed much better weight gain and lower
.vorm egg counts (epg) than-offspring o f other bulls of the same breed. Much later,
Kloosterman and colleagues (1978) in Holland and Australian workers have found significant
differences in resistance to experimental infections to C. oncophora or to other worms within
the same breed (Barger et al., 1983). More recently, Kaufmann and colleagues (1990) made
similar observations with N ’Dama-bulls after experimental and natural infections with Gl
nematodes.
As genetic variation in resistance to nematode infections within breeds can be as great
as that betw een breeds (Barger, 1989; Kaufmann et al., 1990), Pfister (1991) suggested that
breeding programmes in developing countries should concentrate on genetic improvement o f
local indigenous breeds. However, there is limited evidence on the amount o f genetic
variation within indigenous African breeds for resistance to endoparasites (Baker et al.,
1993). T h u s, it is therefore likely that breeding programmes in Africa will utilize both
between- and within-breed genetic variations for resistance to nematode infections (Baker,
1995).
Pfister (1991) posed a number o f questions which need to be answered before
breeding programmes for resistance to endoparasites in Africa can be implemented
successfully. These include socioeconomic issues, profitability and the acceptability o f
programmes by local livestock owners. The breeding programme proposed by Pfister (1991)
did not envisage stopping the use of anthelmintics, but the development of genetically
resistant animals which would receive fewer anthelmintic treatments. Pfister’s proposal was
for on-farm recording and evaluation but this scheme could be increased in scope to include
aspects o f a group breeding system, including a nucleus herd as suggested by Cummins and
colleagues (1991).
81
. .
2 3 4 .3 M edicinal plants
T h e effects o f herbage, or plant extract, on parasites have been known for a long time
and many traditional de-worming preparations currently used by livestock owners in the
tropics and subtropics are based on such materials (Hammond et al., 1997). Pasture plants
such as legum es, have been reported to have anthelmintic properties, and at certain stages
of grow th, grasses and forage crops appear to act as vermifuges (Anderson et al., 1987).
Recently there has been considerable interest generated following the studies o f Niezen and
colleagues (1996) which suggests that forages containing condensed tannins provide sheep
with the ability to withstand parasite infection. This may be due to direct anthelmintic
properties o f tannins, or most probably due to the role of tannins in protecting dietary protein
from ruminal degradation and thus animals are on a better plane of nutrition (Waller, 1997a).
In Indonesia, extensive studies have been conducted to investigate materials from
papaya trees for anthelmintic properties. A high efficacy o f papaya latex was demonstrated
against Ascaridia galli in chicken (Mursof and He, 1991), against Ascaris suum in pigs
(Satrija et a l., 1994) and against H. contortus in sheep (Murdiati and Beriajaya, 1997).
In Kenya, medicinal plants are used especially among the pastoralists, who claim that
certain plants eliminate tapeworms; their only evidence o f helminthosis. However, the
s p e c ific anthelmintic efficacy o f these plants and herbal preparations has not been
experimentally documented.
2 .3 .4 . 4 Biological control
Control o f GI nematodes of domestic livestock is directed mainly at the parasitic
forms in the host using anthelmintic products. However, to complete their life cycle, parasitic
nematodes have to develop through a series of free-living stages on pasture. It is within this
82
nvironment that there is a wide variety of natural enemies that are constantly regulating their
»opulation. Bacteria, viruses, protozoa, other nematodes and fungi are among the principal
latural enem ies o f nematodes in the soil (Tribe, 1980; Pryodko et a l., 1985). In the past,
nost interest have been focused on those organisms producing chemical toxins which have
?een developed as anthelmintics, for example, Streptomyces avemutilis/avermeetim (Benz
and Ernst, 1979). However, the threats o f development of anthelmintic resistance, public
concern about chemical residuals in animal products and in the environment (Herd et al.,
1993; Strong et al., 1996) has stimulated attempts to develop alternative methods of PGE
control. One possible non-chemotherapeutic approach is biological control using
nematophagous fungi.
2.3.4.4.1 Nematophagous fungi
The nematode-destroying fungi are natural enemies o f nematodes, capable o f capturing,
killing, and digesting them. The nematodes have a due function in this relationship, o f
serving as prey and also, triggering fungal development in a way that infective structures
(traps or conidia) are formed (Nordbring-Hertz and Jansson, 1984). They are commonly
found world wide, occurring in natural and agricultural soils, in old faecal deposits and all
kinds o f decaying organic materials (Gray, 1983).
Nematophagous fungi consist o f over 150 species which include the nematode-
trapping, or predacious fungi and the endoparasitic fungi, being the most important groups.
Others include fungal parasites o f cyst and root-knot nematodes of plants which invade eggs
or females by vegetative hyphae (Nordbring-Hertz, 1988), and fungi that produce metabolites
which are toxic to nematodes.
i
83
\
J.3.4.4.2 E ndoparasitic fu n g i
According to Barron (1977), endoparasitic fungi belong to the classes Phycomycetes
i Oomycetidae, Chytridiomycetidae, Zygomycetidae), Basidiomycetes and Deuteromycetes.
Endoparasitic fungi infect nematodes by means o f spores. They have no extensive hyplial
developm ent outside the host except for fertile hyphae, such as evacuation tubes or
conidiospores that release the spores.
2 .3 .4 .4 .3 Nematode-trapping fungi
Nematode-trapping fungi produce trapping organs such as constricting (active) or non
constricting (passive) rings, sticky hyphae, sticky knobs, sticky branches or stick networks
along the vegetative hyphal system. Predacious fungi are prevalent in the class
Deuteromycetes, especially in the group Hyphomycetales. Others belong to the class of
Basidiomycetes (Barron ,1977).
Building o f trapping organs forms the basis for the activity o f the predacious fungi.
Some species form traps spontaneously while, most species only form traps when induced
by extracts from nematodes, chemical compounds, soils or earthworms (Rosenzweig, 1984;
Dowe, 1987). However, the living nematodes are still the most potent trap inducers
(Nordbring-Hertz and Jansson, 1984).
Lectins (Nordbring-Hertz and Mattiasson, 1979; Borrebaeck et al., 1985) as well as
an adhesive compound (Tunlid et al., 1991) have been shown to be involved in the actual
capture o f nematodes. A. oligospora secretes a nematotoxin which paralyses or kills trapped
nematodes (Olthof and Estey, 1963). Recent studies suggest that in A. oligospora, serine
proteases are involved in the process of immobilization of nematodes (Tunlid and Jansson,
1991).
84
2 .3 .4 .4 .4 Nematophagous fungi as bicontrol agents of parasitic nematodes
o f livestock
T h e use of nematophagous fungi as a possible means o f biological control o f parasitic
nematodes o f domestic livestock has been postulated (Roubaud and Deschiens, 1941;
Fernandez et al., 1985; Pryadko and Osipov, 1986; Gronvold et a l., 1985; 1988; 1989;
llyaletdinov and Pryadko, 1990; Larsen et al., 1992).
In one o f the earliest in-vitro studies conducted by Roubaud and Deschiens (1939),
it was show ed that the fungus Dactylella ellipsospora exhibited nematophagous activity
against infective larvae of Ancylostoma duodenale and Strongyloides spp. These workers also
demontrated the value of predatory fungi, D. ellipsospora and A. oligospora in the control
of S. papillosus and Bunostomum spp. (Roubaud and Deschiens, 1941).
A s reported by Soprunov (1966), Russian workers examined the impact of
Arthrobotrys, Trichothecium and Dactylaria spp. when added to faecal cultures derived from
a strongyle infected horse. Arthrobotrys spp. was the most effective in reducing the number
of larvae.
Parnell and Gordon (1963) reported that the predacious fungus, Acrostalagmus
verticiIlium markedly reduced H. contortus larvae in faecal cultures derived from sheep.
However, administration to sheep o f material from faecal cultures containing the fungus gave
inconclusive results.
Pandey (1973) examined the nematode-trapping capability of ten fungi (A. oligospora,
Dactylaria brochopaga, D. gamsospora , D. polycephala, D. thaumasia, D. vermicola ,
Monacrosporium (Dactylella) bembicodes, M. cionopaga, M. ellipsospora and Trichothecium
cystosporium) against the infective larvae of O. ostertagi and T. axei. Infective larvae were
attacked by all the 10 microfungi and species producing adhesive networks and adhesive
85
^ranches w ere the more efficient predators than those forming constricting rings and adhesive
-cnobs. The most efficient predatory fungus was D. thaumasia while, D. vermicola seemed
almost without any effect (Pandey, 1973).
Charles and colleagues (1996) reported that the endoparasitic fungus Harposporium
anguillulae which colonizes cattle pats, was 99.5% effective in reducing H. contortus Lj in
sheep faecal cultures. H. anguillulae, which can be produced artificially in pure culture
(Aschner and Kolin, 1958) have an advantage in watery substrates when compared to
predatory nematode-destroying fungi, as their spores are easily dispersed and have a high
likelihood o f being ingested by nematodes. Also, oral infection allows the fungus to spread
to other locations in the habitat, and once the nematode population declines, Harposporium
also dies o ff (Glockling, 1993). The above advantages are applicable to the control of cattle
strongylid nematodes, because cattle faeces have a high watery content (Charles et al., 1996).
W orking with A. oligospora, one o f the most common nematode-trapping fungi in
Danish agricultural soils (Shepherd, 1961), Nansen and colleagues (1986) demonstrated that
A. oligospora entrapped parasitic stages o f C. oncophora and the free-living nematodes
Panagrellus redivivus and Rhabditis wohlgemuthi with the same efficiency. The parasitic and
free-living nematodes were comparable in their ability to induce trap formation in the fungus.
The same workers examined the trap-inducing capabilities o f L3 o f nine animal parasitic
nematodes, and they revealed that the ability o f L3o f C. oncophora and 0 . ostertagi from
cattle, H. contortus, C. curticei from sheep, and Cyathostoma spp. from horses to induce
traps was high compared with L ,o f O. dentatum and 0. quadrispinulatum from pigs and
Neniatospiroides dubius from mice. The trap-forming potential o f the slow moving
Dictyocaulus viviparus was poor, suggesting that nematode species with highly motile larvae
are the most effective inducers of trap formation. It was also shown that larvae o f all
86
parasitic nematodes were rapidly captured in pre-formed traps (Nansen et al. , 1988).
Recent studies conducted using H. contortus L3 in sheep faecal cultures demonstrated
that addition o f 20,000 conidia o f Monacrosporium endermatum, A. oligospora and A.
robusta g '1 o f faeces caused a reduction of 95.7% , 98.3% and 10.1%, reprectively, compared
with the control group. Whereas, a 97% reduction was observed when combined conidia of
the three fungi were used (Mendoza-De and Vazqnuez-Prats, 1994). The addition o f the three
fungi at 100,000 conidia g '1 o f faeces resulted in total reduction of the larval population.
T h e ability o f A. oligospora and A. flagrans (syn. Trichothecium flagrans ,
Duddingtonia flagrans), to control the development o f L3 in faeces from naturally infected
horses w as recently assessed by Bird and Herd (1995). The two fungal species, significantly
reduced the number o f infective cyathostome L3 in horse faeces at concentration of 10 and
100 spore egg'1. These findings supported the work o f Nansen and colleagues (1988) showing
that L, were able to induce trap formation, become entrapped and killed by A. oligospora.
A series o f controlled plot experiments connducted in Denmark have shown that
admixture o f A. oligospora directly to cattle faeces may confer a significant reduction in the
numbers of L3 that develop from eggs of O. ostertagi and C. onchophora (Gronvold et a l .,
1987; 1988; 1989). In a field study, Gronvold et al. (1987) innoculated cow pats containing
m y c e lia l fragments and conidial spores o f A. oligospora and observed a 10-fold reduction in
the number o f C. onchophora L3 in innoculated cow pats, and surrounding herbage relative
to the control fungal-free pats. Using conidial spores only, Gronvold et al. (1988) found that
L3 of O. ostertagi were also significantly reduced in innoculated cow pats, and surrounding
herbage compared with fungal-free control pats. These results showed that the conidia o f A.
oligospora were able to germinate and develop trapping organs in cow pats. Working with
O. ostertagi, Gronvold and colleagues (1989) studied the effects on parasite control by
87
monitoring calves grazing either on a control plot or a plot in which cattle faeces containing
0.25 g m ycelial fragments o f A. oligospora k g 1 faeces was deposited. The calves on treated
plots w ere exposed to a lower level of parasitism compared to calves on the control plots,
as shown by lowered L, numbers on pasture, lower epg counts, lower pepsinogen levels and
higher body weights (Gronvold et al., 1989).
T h e results o f Gronvold and colleagues (1987; 1988; 1989) indicate that the prospect
of practical biological control o f GI nematodes o f ruminants could be enhanced markedly,
if the nematophagous fungi could pass through the GI tract without loss o f viability. Thus,
the effect o f introducing predacious fungi into fresh faeces by feeding fungal material to
various hosts has been investigated by several workers. Gruner and collegues (1985) and
Peloille (1991) reported that the nematode-trapping fungi Dactylaria Candida, Candelabrella
(Arthrobotrys ) musiformis, A. tortor and D. flagrans fed to sheep on millet grains successfully
passed the alimentary tract o f sheep. Investigations conducted in Russia have shown that A.
oligospora grown on chopped corn passed the alimentary tract of donkey (Soprunov 1966)
and when A. arthrobotryoides and A. flagrans were fed to ewes over a period o f 3 days, they
were effective in reducing the number o f GI nematode and lungworm larvae in the faeces
(Pryadko and Osipov, 1986). Hashmi and Connan (1989) reported that conidia o f A.
oligospora given by mouth were passed alive in faeces of cattle. In contrast, Descazeaux and
Capelle (1939) found no survival of A. oligospora and Dactylella bernbicodes given to horses
and guinea pigs, and in recent studies conducted in Denmark, A. oligospora was unable to
pass the alimentary tract of cattle alive (Gronvold et al., 1993b).
As a means o f screening predacious fungi for gut survival capabilities, Larsen and
colleagues (1991) developed an in-vitro assay designed to mimic environmental stresses of
rumen and abomasal passage. This study proved valuable in identifying D. flagrans as being
88
uperior to Arthrobotrys spp. which was confirmed in subsequent feeding trials in calves
Larsen et a l., 1992). In a semi-natural plot experiment, D. flagrans isolates when fed to
alves resulted in a significant reduction in numbers o f 0. ostertagi L, transmitted to the
lerbage from deposited dung pats (Grenvold et a l., 1993a).
Several field studies have corroborated the findings o f Gronvold and colleagues
; 1993b) o n the effectiveness o f D. flagrans as a potential biocontrol agent against GI
nematodes o f livestock, especially cattle. In an attempt to control O. ostertagi in calves
exposed to natural pasture infection, it was shown that feeding of calves with a D. flagrans
isolate reduced herbage infectivity and worm burdens in the animals (Wolstrup et al., 1994).
In this experim ent, where calves were fed daily with fungal material through the initial 2
months o f the season, results comparable with those o f anthelmintic strategies commonly
applied in north-west Europe were obtained. In a subsequent investigation, it was shown that
strategic feeding o f first season calves with D. flagrans over the first three months o f the
grazing season was able to prevent severe clinical trichostronglylosis in the late summer.
The results showed that larval populations of Ostertagia and Cooperia were significantly
reduced on the pasture grazed by fungal-treated calves. In contrast, the number of
Nematodirus larvae seemed less affected (Nansen et al., 1995). A study conducted in the
1993 grazing season with yearling calves exposed to a pasture with a natural mixed
trichostrongyle larval infection, has shown that daily feeding with D. flagrans during the first
2 months of the season led to a lowered herbage infectivity and a reduced acquisition of
Ostertagia spp. and Cooperia spp. later in the season. In addition, the procedure delayed the
onset o f clinical disease (Larsen et al., 1995a).
In another experiment, a study was undertaken to examine the potential o f D. flagrans
to survive passage through the GI tract o f horses and subsequently to destroy free-living
stages o f cyathostomes in faecal cultures. Results showed a positive relationship between dose
level and reduction in the number of L3. Fungi were recovered in faeces at times which
89
corresponded to high larval reduction (Larsen et al., 1995b). Other recent studies have shown
that D. fla gran s is highly effective against GI nematodes o f pigs (Nansen et al., 1996),
horses (Larsen et al., 1996) and sheep (Githigia et al., 1997). The effect o f an artificial
increase in nematophagous fungi in the environment is likely to be short lived due to
ecological factors that limit fungal populations in the field (Cooke and Satchuthananthavale,
1968). T h is transience should prevent ecological problems that might be associated with the
nonspecific, free-living nematodes in the field.
90
-Chapter 3-
PREVALENCE AND INTENSITY OF HELMINTH AND COCCIDIAL INFECTIONS:
A FIELD SURVEY
3.1 Introduction
Helminth and coccidia infections in cattle in Kenya are thought to be widespread
<Froyd, 1959; Mango et al., 1974; Omara-Opyene, 1985; Ndarathi et al., 1989). However,
information on the prevalence and intensity of particularly subclinical infections are limited.
Haemotichus spp. has been reported as the predominant species in cattle under
nomadic management in the arid Marsabit District o f northen Kenya (Omara-Opyene, 1985).
In more intensive grazing systems (agroclimatic zones 2 and 3, with medium altitude and
bimodal rainfall), Cooperia, Trichostrongylus and Ilaemonchus spp. were found to be
numerically dominant in Nyeri District (Gatongi et al., 1987); and Haemotichus and
Trichostrongylus spp. in Nyandarua District (Maingi and Gichigi, 1992). In an abattoir
survey o f parasitic worms o f slaughtered cattle throughout Kenya, Haemotichus spp. was
found to have the highest national prevalence followed by Cooperia spp. (Mango et al.,
1974). Elsewhere, the helminths listed above are known to depress growth rates in cattle
when burdens are sufficiently high, and Falvey and Bambridge (1975) found that
gastrointestinal helminthosis reduce liveweight gain in 6-month-old cattle grazing improved
pastures. Apart from the limited observations reported, no detailed epidemiological study has
been conducted in central Kenya. Thus, a preliminary survey was conducted to provide basic
information on the identity, prevalence and intensity o f helminth and coccidia infections in
dairy cattle. The effect o f age, sex, farm and season on the occurence and distribution of
these parasites was also determined as this information is important in formulating control
strategies.
91
3.2 M a t e r i a l s a n d m e th o d s
3.2.1 Study area
3.2.1.1 Location and size
T h is study was conducted in Kiambu District (which included Gatundu and Thika
divisions o f the newly created Thika District), one o f the seven districts in Central Province.
It is located at the southern part o f the province and has a total area o f 2451 km2. The district
shares com m on boundaries with several districts both within and outside Central Province
(Fig. 3. la ) and lies between 0° 25' and 1° 20 1 south o f the equator 36° 31' and 37° 15' East.
Fig. 3.1b shows the administrative divisions o f the district.
3.2.1.2 Topography and geology
The district is divided into four broad topographic regions viz. upper highland zone,
lower highland zone, upper midland zone and lower midland zone.
The upper highland zone is found in Lari Division and is an extention o f the Aberdare
Range and lies at an altitude o f 1800 m above sea level. It is dominated by highly dissected
ranges and the soils are o f high fertility and well drained. The area has very reliable rainfall
and is generally a sheep and dairy cattle zone though various food crops and fruits are also
grown.
The lower highland zone is mostly found in Limuru and parts o f Gatundu, Githunguri
and Kikuyu divisions. The area is characterized by hills, plateaus and high level structural
plains. The soils are o f moderate high fertility, well drained, though in some places they are
imperfectly drained. The area lies between 1500-1800 m above sea level and is generally a
tea-dairy cattle zone though crops like maize, pyrethrum, horticultural crops, fruits and sheep
farming are practised.
92
CO
cr>
F ig. 3 .1 a . S k etch m ap o f K en y a sh o w in g lo catio n o f C en tral P ro v in c e and K iam b u D istrict

NAKURU
X ^ n
O
H
^ fi O
D IS T R IC T B O U N D A R IE S
D IV ISIO N B O U N D A R IES
A LARGE SCALE FARM
• SMALL SCALE FARM
F ig . 3 .1 b . Sketch map o f Kiambu District showing administrative divisions and approximate location of farms used for this study
T h e upper midland zone lies below 1500 m above sea level. The zone covers mostly
Thika and parts o f other divisions with exception o f Lari and the landscape comprises
volcanic footridges and mid-level uplands. Fertility of soil varies between variable to
m oderate. Main crops grown include coffee, sisal, maize, sorghum, sunflower among others.
Livestock keeping is also undertaken.
T h e lower midland zone is found partly in Thika (Gatuanyaga) and Kikuyu (Ndeiya
and Karai) divisions. The area is dry with rainfall being very low and unreliable. Drought
resistant crops such as Katumani maize, sorghum, millet, groundnut are grown. Livestock
keeping is also undertaken.
3 .2 . 1.3 Climate
T h e climate in Kiambu District is largely influenced by altitude. Annual rainfall varies
from 5 0 0 mm in lower areas around Thika Divison and increases gradually to over 1300 mm
in the upper regions o f the district. Fig. 3.2 shows rainfall distribution, mean maximum and
minimum temperatures in °C o f Kiambu District. The rainfall regime is bimodal with the
long rains falling between April and May followed by a cool season during July and August,
which culminates to the short rains falling between October and November. Average
temperatures are also influenced by altitude. For example, in the upland zone, the
temperature ranges from 20 .4 °C in March/April to 12.5 °C in July/August.
3 .2 . 1.4 Livestock production
The majority of farmers in Kiambu District are smallholders, covering 94,820 ha and
practising mixed agriculture, including livestock production, and food and cash crops. With
a population of 1,012, 438 it has a population density of 463 persons km 2.
95
25
20
Temperature (Cel.)
Rainfall (mm)
15
10
0
J F M A M J J A S O N D
Month
f l Rainfall — Minimum Temp Maximum Temp.
F ig . 3 . 2 : M e te o ro lo g ic a l d a ta f o r K iam bu D is t r ic t
( a t least 10 y e a rs o f re c o rd s u p to 1995)
96
(A nonym ous, 1994; Gitau et al., 1994a)
Livestock production in Kiambu District is one of the enterprises that play a crucial
role as far as development in the district is concerned (Anonymous, 1994). The major
livestock enterprises include dairy animals, pigs, poultry, sheep and goats, beef in arid and
semi-arid areas. Due to the ever increasing population, land has been a major constraint to
all enterprises and most o f the residents are smallholder mixed farmers for whom the
livestock enterprise is mainly for milk production. Gatundu, Githunguri and Kikuyu divisions
have m ost smallholder farms in that order while Limuru and Kiambaa divisions have the
least. C onversely, Limuru Division has the highest number of large farms and the largest
acreage o f large farm land. The cattle population is mainly comprised o f dairy cross breeds
namely Fresians, Guernseys and Ayrshires. Zebu cattle are also found in parts o f Limuru and
Thika divisions (Anonymous, 1993). Table 3.1 shows the major livestock enterprises and
population 1991/92.
Table 3.2 shows the livestock production trend as o f 1991/92. The most important
livestock enterprise is dairying followed by beef. Dairying contributes the highest income
amounting to K £12,554,183. Milk is marketed through 14 functional Dairy Co-operative
Societies, with 75-80% o f milk produced by smallholder farmers owning fewer than ten
milking cows (Anonymous 1994). Due to the small land size, most farmers produce milk
under the intensive zero-grazing system. Beef and poultry keeping also contribute a high
percentage o f income to the local population and agricultural Gross Domestic Product (GDP)
in general (Anonymous, 1994).
3 .2 .2 Experimental design
The farms surveyed were selected by stratified random sampling (Plews, 1979) and
included 6 large ( > 30 animals) and 10 small scale ( < 20 animals) farms randomly
97
Table 3.1: Livestock enterprise and 1991/92 population_______________________
Enterprise _______________ 1991/92 population
Dairy 155,273
Beef-zebu 27,642
Dairy cows ATS (milk and meat) 47,510
Sheep (hair and wool) 81,851
Poultry (layers, broilers and
indigenous) 765,945
Bee-keeping (hives) 5,801
Pigs 29,770
Rabbits 35,276
Geese, ducks and turkey 5,875
Total 1,154,673
Source: District Livestock Production Office Kiambu, 1993.

Table 3.2: Livestock production trend 1991/92
Enterprise Products Estimated Estimated value

production (income) 1991/92
K£
Dairy Milk (litres) 61,129,080 12,554,183.0
Beef Beef (No. slaughtered) Cattle hides 177,201

(pieces) 178,217 1,560,608.2
Mutton Mutton (No. slaughtered) Sheep skins 20,802
(pieces) 40,163 659,269.8
Goats Goat meat (No. slaughtered) Goat skins 6,329

(pieces) 31,872 326,892.7
Pigs Pork (No. slaughtered) 815 97,800.0
Bee Keeping Honey (kg) 145,025 725,125.0
Rabbits Rabbit meat (No. slaughtered) 34,603 86,507.5
Poultry Poultry (No. slaughtered) 2,181,164 1,036,052.9
Eggs 150,662,250 22,599,337.5
Based on Anonymous (1993).

istributed within the 7 divisions o f the district. At least ten animals (range 10-20) in three
ge group cohorts o f cattle, o f mixed breeds and sexes (young, i.e. < 6 month o f age;
earlings, i.e . 6-12 months old; and adults, i.e. > 12 months old at the start o f the survey)
vere selected on each farm initially, individually ear-tagged and sampled. Rectal faecal
amples w ere collected monthly during an atypically dry spell (September 1991 to January
l992) as there were no short rains in 1991 (Fig. 3 .3 ), and during a wet period (March to
fuly 1992).
T h e number o f strongylid eggs and coccidian oocysts per gram (epg/opg) o f faeces
was determined for each sample by a modified McMaster technique (MAFF, 1986). The
number o f strongyle eggs counted in a McMaster slide chamber were assigned values, for
example, zero ( 0) to 100 eggs were assigned 0 value and so on to an assigned value o f 10
for 2 0 0 0 to 2100 eggs (Fig. 3.8). Presence o f tapeworm eggs was also noted. A
sedimentation technique as described by Hansen and Perry (1994) was used to detect the
presence o f trematode eggs. The modified Baermann method as described by Rode and
Jorgensen (1989) was used to search for lungworm larvae, but was discontinued after being
negative for 2 months in the dry and wet periods, respectively. Faecal samples from animals
of the sam e age groups on individual farms were pooled and cultured at 27°C for 14 days for
differential larval counts (Keith, 1953; MAFF, 1986).
Identification of Eimeria spp. was carried out in pooled faecal samples where
coccidial oocysts were concentrated by centrifugal flotation using saturated magnesium
sulphate solution. The oocysts were sporulated in a solution of potassium dichromate (2.5
w/v) incubated for one week at room temperature and with constant aeration. Eimeria spp.
were identified on the basis of morphological characteristics of the oocysts and sporocysts
(Joyner e ta l., 1966; Levine, 1973).
100
T he infectivity o f the pastures was tested using tracer bull calves o f mixed breeds, 5-6
»onths o f age and kept under worm-free conditions from birth. One calf was introduced
-»onthly on each farm in the dry and wet season, respectively (i.e. a total of 10 tracers per
arm) and grazed alongside the resident cattle population. After grazing for 28 days, tracers
>»ere held in confinement on concrete floor for 3 weeks prior to necropsy for parasite
ecovery. At necropsy, the gastrointestinal tract was removed from the carcass, and
lbom asum , small intestine and large intestines were separated, opened and washed within 5
•», according to standard procedures (MAFF, 1986). Worm counts were performed on 10%
o f the total washings. The species composition was determined as described by MAFF
(1986). (see Appendix 3.1).
3.2.3 Statistical analysis
Faecal egg/oocyst counts were log-transformed In ( x + 10) and examined by repeated
measures analysis o f variance to test the effects o f season o f sampling, age, sex, farm and
their interactions. The differences between means were tested for significance using a
Student’s t-test and a value o f P < 0 .0 5 was considered significant. These tests are contained
in SAS packages (PROC GLM; SAS, 1990; Schlotzhauzer and Littell, 1991). The period
prevalence rates o f parasite eggs/oocysts were defined as described by Durfee (1978) and
Margolis et al. (1982), and the proportions of infected animals were compared using the x 2
test.
3.3 Results
3.3.1 Meteorological data
The rainfall distribution of the study area is shown in Fig. 3.3 . An atypical bimodal
101
nfall o f 7 6 .9 and 500.1 mm was recorded during the short and long rains, respectively,
i is was b elow the expected average o f about 200 and 800 mm during the two rainy seasons.
3 .2 Parasitological findings
T he prevalence rates calculated from 5 consecutive samplings from September 1991
> January 1992 (dry period) and from March to July 1992 (wet period) are presented in
ables 3 .3 a and 3.3b. A total o f 165 animals were examined monthly and comprised o f 57
a lv es, 56 immature and 52 adult cattle. Strongylid followed by liver fluke eggs and coccidia
o c y s ts w ere the most prevalent infections while, the prevalence of Moniezia was low. In all
.ge groups, concurrent strongyle and liver fluke infections were most common, accounting
or 25.9% and 10.2% o f mixed helminth infections in the dry and wet periods, respectively.
The prevalence of strongylid infection was significantly higher (P < 0 .0 5 ) in the yearlings
( 94.0% ) compared with either the young calves (87.6% ) and adult cattle (75.9%) irrespective
o f season w hile, the prevalence o f coccidian oocysts was significantly higher (P < 0 .0 5 ) in
the young calves (69.3% ) relative to either yearlings (25.9%) or adult cattle (3.8% ). In both
seasons, the prevalence of liver fluke eggs was significantly higher (P < 0 .0 5 ) in adult cattle
(68.3%) compared with either the yearlings (24.1 %) or young calves (9.7% ). The wet season
prevalences o f strongylid and coccidia infections in calves and yearlings were significantly
higher (P < 0 .0 5 ) than for the dry season, whereas, for liver flukes, there was no significant
influence o f season on prevalences of age groups. Overall, the proportions of females and
males shedding strongylid, liver fluke eggs and coccidian oocysts were not statistically
(P > 0 .0 5 ) different (Table 3.3a).
Netnatodirus spp., Strongyloides spp. and Trichuris spp. eggs made minor
contributions to faecal egg counts. Faecal samples examined for the presence of larvae o f the
102
No. of wet days
Rainfall (mm)
Month
n No. of wet days — Rainfall
F ig . 3 . 3 : R a in fa ll d is t r ib u t io n in s tu d y area d u r in g 1991-92
103
Table 3.3a: The prevalence percentages (5 months sampling) o f strongylid, liver fluke, tapeworm eggs and coccidial oocysts in faecal
samples in relation to age group and sex o f cattle on 16 farms in Kiambu District during the dry and wet seasons
AGE GROUP SEX
Calves Yearlings Adults Female Male

n=57“ n=56 n=52 n = 100 n=65
Season Parasite %b % % % %
Dry Strongylid 83.9 93.0 75.4 87.7 82.9

Coccidia 61.4 10.7 3.8 23.0 30.8
Tapeworms 10.5 5.4 3.8 7.0 6.2
Liver flukes 10.5 23.2 71.2 39.0 26.2
Wet Strongylid 91.2 95.0 76.5 87.4 89.7

Coccidia 77.2 28.6 3.8 40.0 33.8
Tapeworms 24.6 9.6 3.8 12.0 12.3
Liver flukes 8.8 25.0 65.4 33.0 30.8
“Number o f animals examined. b% number o f animals diagnosed positive at least once during the 5 months period.
Table 3.3b: The prevalence percentages of eggs of strongylids, Fasciola. Moniezia and coccidial oocysts in faecal samples from all sampling locations during dry
(D) and wet (W) seasons ______________________________________
Sampling location
Internal Age Season Thika Lari Kikuyu Limuru Gatundu Kiambaa Githunguri Group
parasites group prevalence
Strongylids Calves D 76.6 88.1 83.9 83.6 85.0 87.9 82.2 83.9
(*57) W 87.5 92.2 89.7 90.8 91.2 92.7 94.3 91.2
Yearlings D 95.6 93.7 94.5 92.3 90.4 97.1 87.4 93.0
(*56) W 97.3 96.5 97.1 95.6 91.2 97.5 89.8 95.0
Adults D 68.6 71.1 76.5 80.4 66.8 87.7 76.7 75.4
(*52) W 70.2 72.9 76.9 81.5 80.4 76.1 77.5 76.5
Liver flukes Calves D 1.6 25.8 15.8 17.7 3.6 6.2 2.8 10.5
W 2.0 16.3 11.6 15.8 5.9 8.9 1.1 8.8
Yearlings D 18.9 42.2 32.4 32.8 11.6 9.4 15.1 23.2
W 17.8 48.2 27.9 40.1 14.4 8.6 18.1 25.0
Adults D 60.7 96.9 82.9 95.7 53.1 33.8 75.3 71.2
W 54.7 83.5 76.5 88.4 48.6 42.4 63.7 65.4
Coccidia Calves D 46.5 56.7 60.5 53.6 69.4 85.2 57.9 61.4
W 63.8 78.9 90.8 72.6 87.8 79.4 67.1 77.2
Yearlings D 2.9 2.1 22.4 8.7 19.9 15.2 3.7 10.7
W 23.8 10.6 20.1 17.7 49.8 42.1 36.1 28.6
Adults D 2.9 7.8 1.2 6.2 0 4.8 3.7 3.8
W 1.7 5.9 2.3 7.4 1.6 5.2 2.5 3.8
Tapeworms Calves D 5.2 18.8 10.8 4.2 9.4 10.5 14.6 10.5
W 22.4 24.9 17.7 20.4 29.4 21.3 36.1 24.6
Yearlings D 0 10.3 5.9 1.1 4.2 9.1 7.2 5.4
W 2.8 12.3 15.8 5.6 13.1 6.0 11.6 9.6
Adults D 0 5.7 0 5.3 9.1 3.9 2.6 3.8
W 1.5 2.4 1.8 4.2 10.3 5.2 1.2 3.8
“Number o f animals exanimed per age group

lungworm, Dictyocaulus viviparus were all negative.
T he mean epg/opg values for the two seasons are shown in Fig. 3.4 A repeated
measures analysis o f variance showed that yearlings had significantly higher (P < 0 .0 5 )
strongylid epg than either young calves and adult cattle. However, in both calves and
yearlings, strongyle epg counts increased significantly (P < 0 .0 5 ) after the onset o f the rains
in March. Young calves had significantly higher (P < 0 .0 5 ) opg compared to both yearlings
and adult cattle in both sampling seasons, and as with the strongylids, opg counts increased
significantly (P < 0.0 5 ) after the onset o f the rains. Yearlings and adult cattle had significantly
higher (P < 0 .0 5 ) liver fluke epg than young calves, and epg did not differ significantly
( P > 0 .0 5 ) between the two former groups in both sampling seasons. For the three parasites,
epg/opg did not differ significantly (P > 0 .0 5 ) between the females and males during the two
sampling seasons (Fig. 3.5).
There were significant (P < 0 .0 5 ) farm efffects on the intensity o f strongylid, coccidia
and liver fluke infections, even though analysis o f variance showed that strongylid epg counts
did not vary significantly (P > 0 .0 5 ) between small- and large-scale farms (Fig. 3.6).
Significant interractions (P < 0 .0 5 ) were observed between farm/season, farm/age for
strongylid and coccidia, and farm/season for liver fluke infections, respectively.
A scattergram showing the number of observations with strongylid epg relative to age
during the months o f September and May is presented in Fig. 3.7. On both occasions, the
intensity of infection was higher in yearlings, which also formed the group with the largest
number of infected animals. These were followed by calves and adult cattle, and in all age
groups, the intensity was higher during the wet season (May) (Fig. 3.7). The observed
frequencies o f strongylid egg counts for the three age groups combined, are presented in Fig.
3.8.
106
Calues
Yearlings
Oocgst c o u n ts /g o f fa eces (opg)
Egg c o u n ts /g o f faeces (epg) Adults
1991 ] 1992
Months
F ig . 3A : G e o m e tric mean s t r o n g y lid , liv e r flu k e eggs and c o c c id ia l

o o c y s t c o u n ts o f c a lv e s , y e a r lin g s a n d a d u lt c a ttle
107
cn
Egg e o u n ts /g o f foeces (ep
Males
Females
O ^ U ** c o u n ,,/* o f fa e c e s <0P9)
Eggs c o u n ts /g o f foeces (epg)
Months
F ig . 3 . 5 : G e o m e tric mean s t r o n g y lid , liv e r flu k e egg s and c o c c id ia l

o o c y s t c o u n ts o f fem ale and male anim a ls
108
FEC May - immatures '4
Farm
F ig . 3 . 6 : In d iv id u a l faecal egg c o u n ts (e p g ) f o r y e a r lin g s

in M a y g ro u p e d a c c o r d in g to fa rm
(e a ch p o in t r e p re s e n ts one o b s e rv a tio n )
109
The mean and overall larval distribution in the faecal cultures of young calves,
vearlings and adult cattle over the study period are presented in Table 3.4 and Fig. 3 .9 ,
respectively. Third stage larvae (L 3) o f Haemonchus, Trichostrongylus, Cooperia and
flesophagostomum were identified in the faecal cultures o f all farms and age groups.
Haemonchus was the predominant species in cultures followed by Cooperia, which became
more important in animals > 6 months o f age. Strongyloides spp. was only identified in
cultures o f calves.
The prevalence and intensity of infection with individual species o f GI nematodes in
tracer calves slaughtered during the dry and wet periods are shown in Table 3.5. Every calf
examined was infected by more than one species o f nematode. H. placei, Cooperia spp. (C.
punctata, C. pectinata) and O. radiatum were the most prevalent species in the abomasum,
small intestine and the large intestine, respectively. Total mean worm burdens o f 10,433 in
the wet period were significantly higher (P < 0 .0 5 ) compared to worm burdens of 4,884
during the dry period (Table 3.5).
A total of 8 species o f Eimeria were identified; in order of prevalence these were E.
bovis (42.2% ), E. zuernii (22.6%), E. ellipsoidalis (11.1%), E. cylindrica (8.9% ), E.
auburnensis (6.1% ), E. alabamensis (3.7% ), E. subspherica (3.1%) and E. wyomingensis
(2.3%). There were few differences in the prevalence o f these species from the 16 farms and
positive samples contained at least three species o f coccidia. However, a large proportion of
the samples (76.0%) had 4-6 species.
110
Dry seaso n (S e p te m b e r)
EPG
W e t season (May)
EPG
F ig . 3 . 7 : T h e d is t r ib u t io n o f s t r o n g y lid fa e ca l e g g c o u n ts
in re la tio n to age g r o u p s in th e d r y (S e p te m b e r)
a n d w e t (M a y ) se aso n s
111
Percentage infected
—^ ^ iv> rv> oo co
O U1 O Ol O U1 o on
J
o t ~t "t t t t t t t t t t t t t t t
.W.V.'.W
.V / vVA’A
□ September (dry period) E3May (wet period)

;.;.; ;>v.-v-v; A*. |•;•
■>:o :aaqaa »■;.
rv>
Assigned values of egg counts
co
cn
a>
-vl
00
co
F ig . 3 . 8 : O b s e rv e d fre q u e n c ie s o f faecal s t r o n g y lid e gg c o u n ts

in a ll age g ro u p s in th e d r y (S e p te m b e r) and
w e t (M a y ) seasons
112
Table 3.4: Percentage distribution o f infective larvae (L 3) o f different genera o f nematodes found in faecal culture o f pooled
samples o f three categories of dairy cattle averaged across 5 months in the dry and wet seasons (mean o f farms and
range3)
Percentage distribution o f Lj
Dry season Wet season Overall %
Parasite < 6 month 6-12 months > 1 2 months < 6 months 6-12 months > 12 months
Haemonchus 61 (37-86) 63 (54-72) 56 (34-70) 55 (39-68) 54 (36-60) 49 (36-62) 56
Cooperia 14 ( 4-30) 17 ( 6-36) 25 (16-30) 19 ( 8-32) 24 (10-46) 27 (16-40) 21

Oesophagostomum 9 ( 4-18) 14 ( 1-19) 11 ( 5-20) 14 ( 4-30) 10 ( 2 - 12) 14 ( 7-16) 12
Trichostrongylus 12 ( 5-28) 6 ( 2- 8) 8 ( 2- 12) 10 ( 5-20) 12 ( 2-35) 10 ( 4-17) 9
Strongyloides 4(1-8) 0 0 2(0-4) 0 0 2
3R ange=low est farm and month vs highest farm and month.

% larv a l c o u n t s
f\5 05 CD o
o o o o o
<
*<>•
Haemonchus
2 O
% T3
O
O
■■ CD
0>‘
% " ^ //////////////////^ ^ ^ ^ ^
Sampling location
<6.
^////////////sZVKZn
3 CO
m r
oCD
\ %
W
O
o
rr
o
TD in
=T
\ s sr r+
Q> “t
CD O
O D
(/) CQ
#♦ <
vV'aj’’ O c
%% 3
c
w
X 3
cvL’.v.yjr
s
F ig . 3 . 9 : O v e r a ll p e rc e n ta g e d is t r ib u t io n o f s t r o n g y lid
g e n e ra fo u n d in fa e ca l c u ltu r e s
114
Table 3.5: Prevalence and intensity o f infection with individual species o f gastrointestinal
nematodes in tracer calves examined during the dry and wet seasons
Dry season (n = 8 0 ) Wet season (n = 80)
Prevalence Worm burden Prevalence Worm burden

(%) (%)
115
Location Parasite Mean 1 Range Mean Range P-value
Abomasum H. placet 56.7 2768 375-5350 54.4 5674 606-9325 < 0 .0 5

T. axe i 7.4 361 21-1310 9.2 960 85-2325 < 0 .0 5
Small Cooperia spp2 17.8 869 96-2100 18.5 1936 46-3850 < 0 .0 5
intestine N. helvetianus 2.9 144 0-389 2.8 290 6-611 N.S
Large 0. radiatum 11.0 537 63-1900 13.4 1398 37-3960 < 0 .0 5

intestine T. globulosa 4.2 205 75- 755 1.7 175 26-810 N .S
‘Geometric mean. 2Cooperia pectinata or C. punctata. N.S-no significant differences between dry and wet season values.
3.4 D is c u s s io n
3 .4 .1 Strongylid infections
T his study clearly shows that GI parasites and particularly strongylids, are prevalent
in cattle within the study area. This is in agreement with other workers’ findings in Kenya
(Omara-Opyene, 1985; Ndarathi et al., 1989; Waruiru et al., 1993b). The spectrum of
strongylids found in cattle in this study confirms observations by Mango et al. (1974);
Gatongi et a/.(1987) and Maingi and Gichigi (1992) in Kenya, and elsewhere in Africa
(Sauvage et al. 1974; Assoku, 1983; Kaufmann and Pfister, 1990; Ndao et al., 1995; Moyo
et a l., 1996). The study revealed that Haemonchus was the most common genus and the level
of infection was generally moderate. However, with heavy parasite burdens in some animals
and in light o f previous findings by Waruiru et al. 1993a, it would be considered to be a
problem especially in yearlings and calves. Results of the present study demonstrate that
Cooperia and Oesophagostomum must also be regarded as common parasites o f cattle in the
area o f study.
The effect o f weather on the prevalence o f GI nematodes was evident as the level of
strongylid infection was higher during the wet period than during the dry period. This was
in agreement with earlier observations recorded in calves in Mathira Division, Nyeri District,
with similar climatic conditions (Waruiru et al., 1993b) but was in variance with the findings
reported by Omara-Opyene (1985) under arid conditions, where a higher frequency of
strongylosis and epg counts in calves occurred during the dry season. The rainy seasons in
this area are very short and Omara-Opyene (1985) suggested that animals became infected
during the short rainy season but high strongylid egg counts were detected during the
following dry season.
The effect of age on the prevalence o f strongylids was clearly demonstrated as
116
, reviously reported by Omara-Opyene (1985). Levels of strongylid eggs were highest in
carlings ( 6-12 months of age at the start o f the study), followed by calves (0-6 months age
z. roup). Adult cattle were the least affected. Available evidence shows that, usually, only
/ou n g cattle are affected clinically. Winks et al. (1983) reported that in the tropical and
subtropical zone o f Australia, the majority of strongylosis outbreaks among dairy cattle
occurred from 4-12 months o f age. This is in agreement with a recent report by Waruiru et
a l. (1993a) where an outbreak due to haemonchosis occurred in weaner calves at Iganjo farm
(s e e chapter 4). In a study conducted in Ankole District, Uganda, the number o f strongylid
e g g s in the faeces was highest for the calves ( < 1 year) and lowest for adults ( > 3 years)
under all systems o f husbandry (Sauvage et al., 1974). In Zimbabwe, the lowest epg counts
were found in steers and highest in calves (Pandey et al., 1993). These findings suggest that
strongylosis starts in young calves as they start grazing and then the rate o f infection
increases with both the age and pasture contamination with the peak in yearlings when the
young stock become entirely dependent on grazing (Omara-Opyene, 1985). Those which
survive develop some form o f resistance so that only low levels of parasitism is later possible
as shown by lower faecal egg counts and prevalence in adult cattle in the current study.
The sex o f the host did not influence the prevalence or intensity of infection with
nematode worms as was reported by Schad et al. (1984). This was in direct contrast with
Asanji and Williams (1987) who noted that female animals harboured a higher worm load
than the male host counterpart. Generally there is a tendency for males to be more
susceptible than females to GI nematode infections (Herd et al., 1992), and this can be
attributable to the differential effects of gonadal steroid hormones on immunity and to grazing
management (Barger, 1993b).
Strongylid egg counts differed between farms. However, no significant differences
117
ere ob served between small- and large-scale farms. The farm to farm variations in epg
r^unts are likely indicative o f variations in farm management (including helminth control),
ircal m icroclim atic conditions and other farm-level factors (Hassan Wan et al., 1989). One
arm -level variable associated with good animal husbandry is the farmers experience in dairy
arm in g. It has been argued that farmers with more experience were better farm managers
N artin et a l., 1975). However, in a recent study, in the present study area, calves of more-
;:xperienced farmers had lower daily weight gains (Gitau et al., 1994c). It was postulated that
>lder farmers tend to develop more off-farm interests over the years, thus directing less
attention to dairy farming. N ew farmers with all their investments in the farm, might pay
closer attention to their cattle (Gitau et al., 1994c).
T he strongylid epg counts followed a typical overdispersed distribution. This
observation was similar to that reported by Roberts and Swan (1982) and Maingi et al.,
1993) in sheep and goats, respectively.
T he lungworm (D. viviparus) was not found in faecal samples examined. However,
in an abattoir survey conducted at the Kenya Meat Commission, Athi River by Bwangamoi
and Kagonyera (1971), 8.3% o f the lungs examined had D. viviparus, but the origin o f the
slaughtered animals could not be ascertained. In a more recent study, D. viviparus larvae
were found in cattle from the highlands o f Tanzania (Thamsborg et al., 1997). A definite
statement concerning the absence of D. viviparus should be deferred until a larger number
of anim als from various regions of the country are examined, especially during the rainy
season. The very low occurrence of Nematodirus, Strongyloides, Trichuris and Moniezia
species would seem to suggest that they are not important problems o f livestock production
in the study area.
Most of the animals examined during the present survey had low to moderate
118
m
strongylid epg counts, suggesting that the infections are usually subclinical (Soulsby, 1965).
This has been described as the most economically important type o f helminthosis since it
occurs in the majority o f cases leading to retarded growth, reduced productivity and animals
are more susceptible to other infections, and continually contaminate pastures (Craig, 1988).
To m axim ize food nutrient intake and productivity of the animal, treatment of animals
suffering from such infections should be undertaken. Such treatments should reduce the egg
load and the chances o f infecting the more susceptible young animals (Ndarathi et al., 1989).
3.4.2 Coccidia infections
The prevalence o f coccidian oocysts and opg counts were significantly higher in
young calves and frequency o f occurrence was higher during the wet sampling period. These
findings are in agreement with those o f other workers (Ward et al., 1979; Omara-Opyene,
1985; Ndarathi et al., 1989; Waruiru et al., 1993b) showing that calves are the major source
of pasture contamination. The Eimeria spp. and their prevalence as found in this study are
in general agreement with those of other workers in Kenya (Munyua and Ngotho, 1990) and
elsewhere (McKenna, 1972; Ernst and Benz, 1981; Parker and Jones, 1987), where E. bovis
and E. zuernii were the most commonly encountered coccidia species of cattle. According
to Levine (1973) these two species represented the most pathogenic o f the bovine coccidia,
with E. zuernii in particular being associated with both acute and chronic type o f disease. In
the current study, no cases o f clinical coccidiosis were encountered.
3 .4 .3 Liver fluke infections
The results showed that liver fluke infections were widespread in Kiambu District.
This is in accordance with observations made by Mango et al. (1974), that fasciolosis was
119
o m m o n in cattle in Central Province of Kenya, with a prevalence o f 41.5% . This prevalence
„'as com parable with 34.0% obtained in faecal examination o f liver fluke eggs. Cheruiyot
1983) also reported that fasciolosis was endemic and o f high prevalence in high rainfall and
i igh altitude areas o f Kenya. One of the important factors in the distribution o f fasciolosis
s the presence o f the snail hosts. Brown (1980) showed that Lymnaea natalensis, the snail
-lost o f F. gigantica in Kenya has a limited distribution but is widespread in Central
P rovin ce. The relative increase o f liver fluke prevalence in the dry sampling period could
t>e attributed to management practises o f moving animals to low and swampy areas in search
o f fresh vegetation.
In accordance with reports of Castelino and Preston (1977) and Baldock and Arthur
<1985), prevalence rates o f liver flukes were higher in adult cattle than in either yearlings or
woung calves. It is reasonable to speculate that the prevalence increased with age because of
the longer period that animals are exposed to infected pastures and give some support to the
postulation that F. gigantica infections are not as well and rapidly expelled as F. hepatica
infections (Hammond and Sew ell, 1974). The sex o f cattle did not influence the prevalence
of liver fluke infection in the present study. This was in contrast with earlier reports where
incidence in females was generally higher than in males (Asanji and Williams, 1984).
However, in other studies, low prevalence in females of all ages was recorded, while there
was an increase in prevalence in males with age (Baldock and Arthur, 1985).
tfNIVFPr’ TV OF VATROBr
I i SUAR V
120
I
-C hapter 4-
FATAL HAEMONCHOSIS IN HEIFERS AT IGANJO FARM: A CASE
STUDY
4.1 Introduction
Helminthosis causes economic losses in ruminants world-wide. Haemonchus spp.
infection o f sheep and goats and, to a lesser extent, of cattle is one o f the most important
causes o f economic loss in Kenya (Allonby and Urquhart, 1975; Carles, 1992; Waruiru et
a/., 1993a). Dairy calves are the most commonly affected group among cattle but steers and
other young cattle up to 3 years o f age may also be affected (Blood et al., 1979). The disease
is characterized clinically by severe anaemia and anasarca. A chronic wasting disease has
also been described (Allonby and Dargie, 1973). Where the disease is unchecked, severe
morbidity and high mortality are common; in other areas the cost o f control in terms of
labour and prophylactic chemotherapy is often a significant factor in production costs
(Preston and Allonby, 1979; Urquhart et al., 1987).
Haemonchus contortus is the species most commonly found in the abomasum o f sheep
and goats, and H. placei is the usual species in the abomasum o f cattle. However, H.
contortus may also be present in cattle but usually only when they are grazing the same
pasture as sheep or goats.
Haemonchosis is for the most part a primary parasitosis. The predisposing causes for
infection include overcrowding, lush pastures and hot, humid climatic conditions. The
development of clinical illness is favoured by a fall in the plane o f nutrition, particularly in
calves. Under adequate nutritional levels, cattle may develop a subclinical infection but when
the nutritional level subsequently declines the disease develops (Blood et al., 1979).
Haemonchosis outbreaks due to //. contortus in sheep and goats are known to occur
121
n Kenya and are w ell documented (Allonby and Urquhart, 1975; Preston and Allonby,
L 978). H ow ever, a review o f literature indicates that only a limited number o f studies have
>hown that haemonchosis is a serious problem in young stock of cattle o f post-weaning age
COmara-Opyene, 1985). In this report, clinical haemonchosis in a herd o f young dairy cattle,
in ten sively managed is described.
•4.2 Case history
A farm visit was undertaken to Iganjo farm in Thika Division to investigate the
efficacy o f triclabendazole and oxyclozanide against F. gigantica in naturally infected dairy
cattle. H ow ever, on arrival at the farm the farmer related the following history. That 42
weaners which had not been drenched were released on to the field at the beginning o f June,
1992. Four o f these died and these losses occurred while the weaners (6-9 month o f age)
were confined to 1.5 acre "calf pasture". Those that died had all suffered severe chronic
diarrhoea, sub-mandibular swellings and progressive emaciation but had continued to eat until
shortly before death.
4.3 Clinical observations
On physical examination of most of the remaining weaners, the animals displayed
signs o f helminthosis such as being stunted, emaciated, dehydrated with sunken eyes and
some were unable to stand. Some had sub-mandibular swellings, their hindparts and tails
s m e a re d with faeces, and their mucous membranes were pale. Faecal examination o f the 37
surviving weaners revealed a moderate strongylid epg count of about 500 with a range of
100-2200 epg.
122
i-A Post mortem fin d in g s in c a lf No. 1625
P ost mortem examination o f a freshly dead case revealed pallor o f all body tissues,
depletion o f body fat reserves with serous atrophy o f pericardial fat and gelatinous peritoneal
tat. Other lesions were oedema o f the abomasal folds, subserosal oedema of the abomasum,
thickened and inflamed areas o f abomasal and duodenal mucosae and, an accumulation of
over 4 litres o f straw-coloured fluid in the abdominal and thoracic cavities.
As show n in Table 4. 1, massive H. placei adult and immature worms estimated to be in
excess o f 10,000 were recovered from the abomasum. Markedly fewer T. axei, Cooperia
spp. and O. radiatum were recovered from the abomasum, small and large intestines,
respectively.
4.5 Treatment
O n advice, the farmer removed the 12 critically sick yearlings to the pens and they
were put on supportive therapy which included glucose given intravenously, supplemented
with iron dextran and multiple vitamins administered intramuscularly. The above 12 animals
and 25 others were also drenched with albendazole at a dose rate o f 7.5 mg kg'1. The farmer
was also advised to supplement the yearlings’ diet with grain and minerals. All cases
gradually recovered after this treatment and no deaths were reported. The animals had zero
epg counts on subsequent faecal sampling on day 14 and 28 post-treatment.
4.6 Discussion
In the tropics and subtropics, where climatic conditions are characterised by wet and
dry seasons, outbreaks of haemonchosis have been reported only during and immediately
following the wet season (Lee et al., 1959; Reinecke, 1960). This is when the infective
123
T ab le 4 .1 : N u m b e r an d p e rc e n ta g e o f n e m a to d e sp ecies reco v ered at p o st m o rte m o f c a lf N o . 1625
Number (%) o f nematode species
Date of Haemonchus Trichostrongylus 1Cooperia Oesophagostomum Nematodirus Trichuris Strongyloides

necropsy placei axei sp. radiatum helvetianus ovis papillosus
2-8-92 11751 (58.4) 3474 (17.3) 2467 (12.2) 1974 (9.8) 281 (1.4) 125 (0.6) 57 (0.3)
124
1Cooperia pectinata or C. punctata

larvae (L 3) are on pasture (Sprent, 1946), and result from recently acquired infection as
demonstrated in the present study. However, a late dry season outbreak of clinical
haemonchosis and cooperiosis in cattle was reported by Fabiyi and others (1979) in Northern
Nigeria, and was attributed to the simultaneous maturation of a large number of arrested
worms acquired during the previous wet season period.
In the outbreak reported in this study, the history o f intact appetite in spite of chronic
intermittent diarrhoea and progressive emaciation displayed by young weaner calves at
pasture, and the favourable response to albendazole treatment suggested that the herd problem
was one o f primary GI strongylosis (Georgi et al., 1972). This outbreak was probably due
to high stocking rate for the available grazing area that led to inadequate nutrition. The stress
of inadequate nutrition can predispose any animal to disease (Hotson, 1973). The subsequent
improvement of the health o f the herd was partially attributed to effective anthelmintic
medication, and partially to supplementation o f the diet with grain. Another important aspect
of this outbreak is that the greater the number o f infected animals in a given area, the more
L3 there were to infect or reinfect the animals (Wade et a l ., 1979). This is seen especially
when young animals graze with adult animals or when susceptible animals are put into areas
such as dairy calf lots as in the present case (Hotson, 1973). The farmer was advised to raise
future replacement stock on larger pasture areas which have not been grazed for at least 12
weeks.
125
-C hapter 5-
GASTROINTESTINAL NEMATODE INFECTIONS : AN ABATTOIR
SURVEY
5.1 Introduction
Gastrointestinal nematode (GI) infections o f cattle have been investigated in different
climatic environments o f Kenya (Omara-Opyene, 1985; Gatongi et al., 1987; Maingi and
Gichigi, 1992), and much o f the data on epidemiology is based on faecal egg count to
estimate the corresponding worm burdens. However, in cattle the egg production of
nematodes was found to depend heavily on the season (Kaufmann and Pfister, 1990). During
the dry season, when conditions are unfavourable for the development o f infective larvae,
faecal eg g production is reduced. It is therefore more reliable to quantify the worm burden
by post mortem examinations, particularly during the dry season (Fritsche et al., 1993).
The present study describes the results obtained from 672 post mortem analyses of
cattle, with special emphasis on the seasonal dynamics of GI nematode infections.
5.2 M a te ria ls a n d m ethods
5.2.1 Experimental design
The investigation was conducted on crossbred cattle slaughtered at various abattoirs
and slaughter-slabs located throughout Kiambu District. The animals examined were procured
locally (animals raised within the abattoir location) and it was envisaged that their worm
burdens would reflect the general pattern o f worm population in animals of the area
surveyed. A total o f 672 GI tracts were analysed from freshly slaughtered animals between
August 1992 and July 1993. Fourteen GI tracts were collected each week. The samples were
taken at random from the animals presented for slaughter during the visits. Age (by number
126
o f teeth) and origin (with the help of cattle owners and butchers) were determined prior to
slaughter. A ges of the animals ranged from 13 months to more than 4 years (average age 57
months). Three hundred and ninety (390) animals were females and 282 males. The
m eterological data for each month accorded with the average values over the previous 10
years (A nonym ous, 1994).
A t slaughter, GI nematodes were recovered as described by MAFF (1986). Rectal
faecal sam ples were collected from all animals for strongylid worm egg counts (epg) using
a m odified McMaster technique (MAFF, 1986). The faecal material from each collection was
pooled and cultured at 27 °C for 14 days to harvest the third stage (L3) larvae which were
identified to generic level (M AFF, 1986; Keith, 1953).
5.2.2 Statistical analysis
One way analysis o f variance (ANOVA) was used to examine for differences in worm
burdens and faecal strongyle egg counts between age classes based on logarithmic
transformation similar to that o f Field et al. (1960).
5.3 Results
5.3.1 Parasitological findings
O f the 672 animals investigated, 583 (86.8% ) were found to be infected with one or
more species of nematode parasites. The prevalence and mean worm burdens o f 8 species
encountered in the present study are listed in Table 5.1. H. placei, C. pectinata, C. punctata
and O. radiatum were the most common species, followed by T. axei, Nematodirus
helvetianus, Trichuris globulosa and Strongyloides papillosus which, were generally only
127
found in moderate or low numbers.
The intensity o f nematode infections was moderate in most animals, the overall mean
nematode burden being 3,353 (range 260-18,300) and the overall mean faecal strongyle egg
count being 400 epg. Haemonchus placei, Cooperia spp. and O. radiatum accounted, on
average, for 52.3% , 28.5% and 6.9% o f the total worm burden, respectively.
The seasonal dynamics o f worm burdens and faecal egg output followed a similar
pattern (Fig. 5.1). Worm burdens increased with the onset o f the short rains in October and
reached a peak in November/December. A second peak was observed in May/June, during
the long rains, after which time worm numbers steadily decreased. Faecal egg output was
at its lowest during the dry seasons. However, it increased gradually through the rainy
seasons to reach peaks in December and May. The relative abundance o f H. placei, Cooperia
spp. O. radiatum and T. axei followed the same trend as that o f the total worm burden
during the different seasons o f the year. N. helvetianus, S. papillosus and T. globulosa
occurred only occasionally in very low numbers and their populations were apparently not
affected by seasonal fluctuations.
Digestion o f abomasal mucosae revealed negligible numbers o f developing stages of
H. placei with the proportion o f EL4 ranging between 0 and 5.8% throughout the year.
The mean and range values o f the proportion of the larval population o f H. placei ,
Cooperia spp. Oesophagostomum spp. and Trichostrongylus spp. were 56.7 (43-78), 29.3
( 18-39), 8.4 (6-21) and 5 .6 (1-20) %, respectively. H. placei (> 6 5 % ) and Cooperia spp.
(> 30% ) were prevalent in high proportions during the rainy seasons.
5.3.3 Age/worm burden relationship
There were 49 animals under 1.5 years, 140 (1.5-3 years), 209 (3-4 years) and 274
128
Table 5.1: Spectrum, prevalence and mean burdens o f nematodes found in cattle in Kiambu
District in 672 post mortem examinations between August 1992 and July 1993
Location/species Prevalence (%) Worm burden
Mean Range3
ABOMASUM
Haemonchus placei 67.0 3378 125-10375
Trichostrongylus axei 24.3 305 75-1785
SMALL INTESTINE
129
Cooperia pectinata 53.0 1050 150-5515

Cooperia punctata 41.7 779 40-4350
Nematodirus helvetianus 19.6 210 15-1675
Strongyloides papillosus 3.6 81 15-420
LARGE INTESTINES
Oesophagostomum radiatum 38.4 445 25-2275
Trichuris globulosa 9.7 175 30-426
“Range o f positive cases

Mean worm counts (Thousands)
Eggs per gram of faeces (epg)
Month
□ Worm counts — Egg counts
Fig. 5.1 : S easonal p a t t e r n o f nem atode b u r d e n s a n d fa e ca l

e gg o u tp u t o f c a ttle s la u g h te r e d d u r in g th e a b a t t o ir
130
^ver 4 years examined. Animals younger than 1.5 years had significantly (P < 0 .0 5 ) lower
burdens than older animals (Fig. 5.2). The highest burdens of nematodes (> 5 0 0 0 ) were
found in animals o f 1.5-3 years o f age, but the total number decreased only slightly in older
anim als. Cattle older than 4 years still carried an average load of more than 4700 nematodes
(range 446-6831) and their abomasal load was even higher than in animals less than 1.5
years.
Cattle older than 1.5 years had significantly (P < 0 .0 5 ) higher H. placei burdens,
■whereas counts o f S. papillosus were higher in younger animals (P < 0 .0 5 ). Faecal strongylid
egg counts were not influenced by age.
5.4 Discussion
Results obtained from 672 autopsies undertaken during an abattoir survey indicated
that helminth infections form a major disease complex in cattle, and with regard to both
prevalence and burden, H. placei was the most common nematode as has been reported by
others in Kenya (Mango et al., 1974; Omara-Opyene, 1985). A relatively short generation
interval probably enables Haemonchus spp. to take rapid advantage of favourable climatic
conditions (Grant, 1981) as occurred in the present study. The weather conditions in the
study area also seem to be well suited to the development and survival of the free-living
stages o f the other three species, Cooperia spp. and O. radiatum. The absence of
Bunostomum spp. was surprising, considering that the species has been reported in the
highlands of Kenya (Round, 1962). Probably the distribution of this parasite is focal affecting
only a few farms and localities.
O f the nematode species encountered, H. placei and O. radiatum are among those
which are serious pathogenic parasites o f cattle and are therefore o f considerable economic
131
Nematode worm counts
-*■ N> IV) CO CO
cn o cn o cn o cn
o o o o o o o
o o o 0 o o o
_l___ 1 1 1 1___ ____1
___ ____1
Ej Abomasum EH Small intestine @ Large intestine

Years
v
-n>
F ig . 5 .2 : T h e r e la tio n s h ip b etw e e n g a s tr o in te s tin a l w orm

b u r d e n s a n d th e age o f c a ttle e xa m in e d d u r in g
th e a b a tto ir s u r v e y
132
m portance. The significance o f Haemonchus spp. and O. radiation is due to the severe
irauma and blood loss caused by their migrating and feeding stages (Hutchinson et al., 1980).
Roberts and collegues (1951) observed that egg counts o f up to 1000 H. placei epg were
accom panied by serious clinical signs, while counts o f over 500-700 H. placei epg reflected
a dangerous infection if combined with 300 Oesophagostonuan epg and/or Bunostomum.
Trichostrongylus axei and Cooperia spp are of lower pathogenicity (Anderson et al., 1965)
and these parasites appear to have limited significance in central Kenya (Mango et al., 1974).
The total nematode counts showed a trend which was closely related to rainfall, and
generally, animals o f all ages were affected by the Haemonchus - Cooperia complex, age not
having any effect on faecal egg counts. The intensity and prevalence of the Haemonchus
infections in adult animals were unexpectedly high. Since supplementary feeding is rarely
practiced, nutritional deficiencies may have interfered with the development o f acquired
immunity in cattle as the nutritional state o f most o f the animals presented for slaughter
appeared poor. Malnutrition and concurrent diseases may impair host resistance against
helminths, resulting in higher worm burdens and/or egg counts (Blackburn et al., 1991).
Relatively higher worm burdens and/or egg counts observed in some animals during the wet
months may not have been a result o f higher availability o f infective larvae on pasture, but
rather o f increased susceptibility to infection (Dorny et a l., 1995). The present study supports
that o f Kaufmann and Pfister (1990) in The Gambia under different climatic conditions and
with N ’dama cattle. Older animals may be a major source of infection for young stock and
furthermore detailed studies should be undertaken in other areas o f Eastern Africa with
different climatic conditions. Although clinical helminthosis occurs more otten in calves,
older animals should also be included in future control strategies.
The post mortem and faecal examination results showed that the adults o f the various
133
GI nematodes were present throughout the year. The numbers of EL4 o f H. placei were very
low throughout the year. Thus, it appears that, in the area o f study, inhibition o f H. placei
L4 in cattle does not play a significant role in the biology of this nematode. There are
conflicting reports on the actual stimuli for hypobiosis in the field. For example, some
studies have indicated that where conditions are favourable for development of the free-living
stages, the faculty o f hypobiosis is discarded by the parasites (Gupta et al., 1987). By
contrast, Ikeme and colleagues (1987) observed that in spite o f the year-round tropical
rainfall in Malaysia there were still significant numbers of hypobiotic larvae o f H. contortus
in goats. Gatongi (1995) observed high levels o f inhibition o f Haemonchus spp. in sheep and
goats in a semi-arid area o f Kenya during the dry season. It seems therefore that the degree
of environmental adversity and probably other suggested stimuli for hypobiosis may not be
important in certain strains o f nematodes that are not hypobiotic-prone because, it seems
likely, that the prevailing climatic conditions (medium altitude bimodal rainfall) in central
Kenya are not severe enough to promote selection for seasonally arrested development, as
described elsewhere in Africa (Kaufmann and Pfister, 1990; Ndao et al., 1995).
134
-C hapter 6-
EPIDEMIOLOGY OF GASTROINTESTINAL NEMATODES : A ONE-YEAR STUDY
6.1 Introduction
For any form o f rational control of nematode parasites to be devised, it is essential
to understand interactions between worm populations, weather conditions and animal and
pasture management. Such basic information is required for the design of control measures
to reduce pasture infectivity. The transmission pattern o f GI nematodes is dependent on
geographic location in which they occur (Rickard and Zimmerman, 1992) and
epidem iological data should be developed for different areas. Such data do not exist for most
of K enya which has a variety of agroclimatic zones, each with definite environmental
conditions. Consequently, a study was initiated to investigate the seasonal prevalence and
importance o f the various GI nematodes in weaner-yearling dairy cattle and to further
substantiate epidemiological events o f H. placei.
6.2 Materials and methods
6. 2.1 Exeperimental design
This investigation was conducted from April 1993 through April 1994, starting at the
onset o f the long rains. In each o f the two farms (Iganjo and Kambaa), 32 Friesian/ Ayrshire
crossbred weaner calves o f mixed sexes and about 9-10 months o f age were used. They had
previously been exposed to nematode contaminated pastures and the mean strongyle worm
egg counts prior to the beginning of the experiments (March) was 150 (range 0-400). All the
calves were given a single dose of albendazole (ValbazenR, Smith Kline Beecham Animal
Health Products) at 7.5 mg k g 1 and were also given triclabendazole (FasinexR, Ciba-Geigy)
135
orally at a dose rate o f 12 mg kg'1 at the start o f the study in case o f Fasciola gigantica
infections. N o further anthelmintic treatment was given except in cases where individual
calves appeared to be affected by severe clinical parasitism. The commencing average weight
of calves was 120 kg (range 110-138 kg) and 114 (range 98-126 kg) at Iganjo and Kambaa
farms, respectively.
The basic design in each farm was to graze all calves together over a series o f four
2.6 ha pastures. They were rotated from one pasture to another at varying intervals
depending upon forage availability and the timing o f the moves depended on the farmer’s
judgement. Before initiation o f the experiment, the 32 calves in each farm were assigned to
each o f two groups based on equal distribution o f body weights: ( 1) from the first group of
12 anim als, 2 calves were randomly selected bi-monthly for slaughter and analysis o f worm
burdens; ( 2) the second group o f 20 resident animals were weighed and individualy sampled
for blood and faeces every month. Three o f the resident calves from each farm were
available for slaughter at the end of the study for analysis o f worm populations. The primary
forage present on pastures was Kikuyu grass (Penniselum clandestinurn), and the red oat
grass ( Themeda triandra) also made up a considerable part of herbage, especially at Iganjo
farm. All the animals were subjected to normal farm routines including continous free access
to water and mineral-salt.
The calves selected randomly for slaughter were removed from pasture and confined
in concrete-floored stalls for 3 weeks prior to slaughter. In addition, groups o f 3 tracer
Friesian/Ayrshire crossbred bull calves, 5-7 months of age and raised worm-free since birth,
were grazed alongside the resident herd in each farm for 1 month periods during each month
of the study period. The tracer calves were also held in confinement for 3 weeks before
slaughter.
136
Faecal egg counts were made using the modified McMaster technique (MAFF, 1986).
A sedim entation technique was used to detect the presence o f liver fluke eggs in the samples
(Hansen and Perry, 1994). Faeces were pooled and cultured (MAFF, 1986) and the first 100
third stage infective (L 3) larvae were differentiated into their genera (Keith, 1953). Herbage
samples were collected from all pastures each month for determination of numbers o f L3
available/kg o f dry matter based on techniques described by Hansen and Perry (1994). Larval
counts and differentiation at genus level were carried out using the morphological
characteristics described by Keith (1953). Jugular blood samples were also taken for
estimation o f packed cell volume (PCV), haemoglobin (Hb), total protein (TP), and serum
pepsinogen levels according to techniques described by Ross et al., (1967) (see Appendix
6.1) and C oles (1974).
A ll necropsies, adult worm recovery procedures, counting and identification
techniques were performed as previously described (MAFF, 1986). In addition, mucosal
scrapings o f each abomasum were digested as described by Herlich (1956) to retrieve
immature stages (including arrested larvae) which were identified according to Blitz and
Gibbs (1971) and counted.
6.3 Results
Following a single, initial anthelmintic treatment o f the weaner calves prior to
beginning of the grazing experiments (March), they were not subsequently treated except for
occasional treatment of individiual sick animals in Kambaa farm. However, due to clinical
signs o f haemonchosis at Iganjo farm, one anthelmintic treatment with albendazole was given
to all 20 resident weaner calves on 26th August 1993.
137
6.3.1 Meteorological data
The monthly rainfall, relative humidity and the mean monthly minimum and
maximum temperatures recorded at the study farms are shown in Figures 6. la and 6 . lb . The
rainfall has a bimodal pattern and amounts o f about 822 mm (Iganjo farm), and 1102 mm
(Kambaa farm) per annum divided into long and short rains, were well below a 10-year
average for the two farms. The long rains usually peak in May with the short rains peaking
in D ecem ber. On both farms, mean relative humidity varied from 73.5-100% in the wet
months, and 69.1-98.2% in the dry months (Fig. 6.1b). Minimum temperatures fluctuated
between 9 .7 -1 7 .5°C (Iganjo farm) and 7 .0 -1 0 .1°C (Kambaa farm) while maximum
temperature range was 2 1 .7 to 28.6 °C, and 18.3 to 25.6°C for Iganjo and Kambaa farms,
respectively.
6 .3 .2 Faecal egg and herbage larval counts
The mean number o f faecal strongylid eggs and pasture larval counts for the two
farms are shown in Fig. 6 .2 . Initial faecal egg counts were low in both farms since cattle had
previously been treated with albendazole 21 days earlier. Peak egg counts were observed in
July and August in Kambaa and Iganjo farms, respectively. A smaller, secondary egg count
peak occurred during January 1994, but larval counts remained consistently low except for
a small increase in December following the rains of October and November. Increased egg
counts and high rainfall (Fig. 6.1a) paralleled increased number o f herbage larval counts in
March and April 1994. Fasciola eggs were (epg range 0-300) sporadically observed from
6 animals at Kambaa farm.
The larval distribution in faecal cultures o f the yearling cattle are shown in Fig. 6.3.
The genera were identified as Haemonchus, Trichostrongylus, Cooperia and
138
No. o f Raindays
Iganjo
Kambaa
R a in fa ll (m m )
fl M J J R S o
1993
Months
F ig . 6 .1 a : M o n th ly n u m b e r o f ra in d a y s a n d m o n th ly p a tte r n
o f r a in fa ll fo r Ig a n jo and Kam baa fa rm s
fro m A p r il, 1993 to A p r il, 1994
139
Iganjo
Temp, (cel.) and R.H. (%)
Min. Temp.
MaH. Temp.
R.H. (%)
Temp, (cel.) and R.H. (%)
1993 ] 1994
Months
F ig . 6 .1 b : Mean re la tiv e h u m id ity ( R . H . ) , mean m o n th ly m axim um and

m inim um te m p e ra tu r e s fo r Ig a n jo a n d Kambaa fa rm s fro m
A p r i l , 1993 to A p r i l , 1994
140
E g g s /g
-Q----- Egg counts

-*— Larval counts
Months
Fig. 6 . 2 : Faecal egg counts expressed as eggs/g of faeces and larval recovery from herbage
expressed as L3/Kg of dry herbage
Larvae per gram of faeces
KEY
Haemonchus spp
Cooperia spp.
Larvae per gram of faeces
Trichostrongylus spp.
Oesophagostomum spp.
F'S- 6 .3 : Strongylate nematode infective larvae recovered from faecal egg output of resident
cattle
142
Oesophagostornum, with Haernonchus spp. always contributing the largest number o f eggs
to the total egg output produced during the period (Fig. 6.3).
The composition o f the L3 recovered from herbage showed that Haernonchus spp. and
Cooperia spp. were the predominant nematodes, accounting for 46 (32-74) % and 2 1 .6 (12-
39)% o f all L, identified, respectively. Trichostrongylus spp., Oesophagostornum spp.,
Nematodirus spp. and Strongyloides spp. were third, fourth, fifth and sixth in abundance and
accounted respectively for 15 (6-28)%, 9.7 (4-12)%, 3.7 (1-11)% and 0.8 (0-5)% o f all
larvae recovered in the study area. However, Nematodirus spp. were recovered in a high
proportion o f larvae on pasture (14.9%) at Kambaa farm compared to only 1.4% at Iganjo
farm.
6 .3 .3 Worm burdens in yearling cattle
Haernonchusplacei, Cooperia spp., T. axei and O. radiatum were the most numerous
species found at the 2 farms throughout the study period (Table 6 .1) and worm burdens were
generally higher during the wet months. Cooperia pectinata and C. punctata occurred in the
ratio 59:41 in Iganjo animals whilst in Kambaa cattle, C. oncophora was found together with
C. pectinata and C.punctata in the ratio 4:58:38. Animals in Iganjo had proportionally lower
numbers o f N. helvetianus worms than Kambaa cattle throughout the study period. In the two
farms, small numbers o f T. globulosa, S. papillosus and M. benedeni were recovered
sporadically. The mean (± S .E ) number of adult liver flukes in infected livers of 4 yearlings
at Kambaa farm was 1 6 .0 ± 7 .1 (range 3-39).
6 .3 .4 Worm burdens in tracer calves and resident animals
Worm counts from individual tracer calves ranged from 800 to 4700, with mean
143
T a b le 6 .1 : R ec o v e ry o f g a stro in te stin al n em ato d es fro m y e a rlin g d a iry c a ttle n e c ro p sied b i-m o n th ly ( n = 2 ) d u rin g the stu d y p e rio d
MONTHS
Farm Genera June 1993 August October December February 1994 April
Iganjo Haemonchus adults 5518 1352 2075 3210 1133 4774

Haemonchus aEL4 0 (0) 2 0 (1 .5 ) 47 (2.3) 0 (0) 33 (2.9) 69 (1.4)
Cooperia 2110 1493 1188 1210 647 3900
Nematodirus 37 21 219 137 26 210
144
Trichuris 0 47 53 13 45 160
Total 11183 4997 5038 6494 2922 11538
Kambaa Haemonchus adults 4248 1453 2551 2400 2055 5715
Haemonchus aEL4 81 (1.9) 38 (2.6) 0 ( 0) 55 (2.3) 36 (1.8) 69 (1.2)
Cooperia 3213 1124 1933 1467 647 1680
Nematodirus 2075 607 910 893 529 2568
Trichuris 33 27 0 0 72 105
Total 12418 4341 6887 6075 4121 12432
T h e percentage o f EL4 (early fourth stage larvae) to monthly worm burden are enclosed in brackets.
3000 - t
IGA NJ O
2500 -
Mean number 0< worms
KEY
Total
H. placei
Cooperia spp.
T. axei
Mean number of worms
O. radiatum
Fig~6.4 : Mean monthly worm burden and frequency of occurence of the dominant gastrointestinal
nematode species in tracer calves
145
numbers exceeding 1000 nematodes per calf in most of the study months. While the number
of each species recovered from month to month varied, //. placei dominated in the two farms
(Fig. 6 .4 ) and the highest total worm burdens were observed in May in 1993 and April in
1994.
The monthly mean worm burdens o f H. placei infection are shown in Table 6.2.
Except for few occasions, the mean numbers o f female worms were higher than those of
males. Analysis o f variance confirmed that there was a significant difference (P < 0.001)
between the sexes as a percentage of the total burden, but there was no significant difference
( P > 0 .0 5 ) in sex ratio in the dry and rainy months in either farm. The proportion o f EL„
of H. p lacei was between 0-3.9% and 0-6.8% at Iganjo and Kambaa farms, respectively and
there w as no indication o f accumulation of arrested Haemonchus EL4 at any sampling period
in either farm (Table 6.2).
Post mortem worm burdens o f resident animals killed at the end of the study period
are shown in Table 6.3. The composition o f the burdens broadly reflected the composition
of the pasture infestation. Thus, the H. placei-Cooperia spp. complex comprised the
majority o f the worm burden, 74.7% at Iganjo and 66.2% at Kambaa farm. The mean
( ± S .E ) number o f adult F. gigantica in infected livers of animals at Kambaa farm was
19.0 ± 10.4 (range 3-52).
6 .3.5 Haematology and serum pepsinogen analysis
The serum pepsinogen, PCV, Hb and TP levels recorded during the study are
presented in Fig 6.5. There were minor fluctuations in PCV (range 26.9-33.6% ), Hb (range
83-111 g/1) and TP (range 59-85 g/1) levels during the experimental period in cattle o f both
farms. The values o f each o f these indices were within the normal limits o f uninfected
146
T ab le 6 .2 : M o n th ly c h a n g e s in the c o m p o sitio n o f Haemonchus placei in tra c e r c a lv e s in Ig an jo an d K a m b a a farm s
Month/Farm IGANJO KAMBAA
Mean worm burden aEL 4 Mean worm burden aEL4
Total Female (%) Total Female (%)
April 1993 724 50 0 (0) 1285 62 0 (0)

May 945 75 0 (0) 1545 51 82 (5.3)
June 849 50 0 ( 0) 1059 59 0 ( 0)
July 774 60 0 ( 0) 985 63 0 (0)
August 478 63 19 (3.9) 942 50 14 (1.5)
September 502 63 6 ( 1 .2) 901 43 0 (0)
October 584 70 9 ( 1 .5 ) 1104 50 29 (2.6)
November 655 75 25 (3.8) 1001 75 0 (0)
December 690 70 13 (1.9) 1164 57 79 (6 . 8)
January 1994 516 60 7 (1.4) 736 40 21 (2.9)
February 579 40 6 ( 1 .0) 942 53 10 ( 1 . 1)
March 978 50 0 (0) 1625 58 60 (3.7)
April 1215 57 0 (0) 1732 53 0 (0)
T h e percentage o f EL4 (early fourth stage larvae) to monthly mean worm burden are enclosed in brackets
T a b le 6 .3 : M e an and ran g e o f w o rm b u rd en s o f resid e n t y e a rlin g a n im a ls n e c ro p sied at stu d y te rm in a tio n
Location/Farm 1GANJO (n = 3 ) KAMBAA (n = 3)
Number o f worms Number o f worms
Mean Range Mean Range
Abomasum
Haemonchus placet 3819 830-4768 3292 520-5760
Trichostrongylus axei 910 550-1270 887 33-1405
Small intestine
Cooperia spp. 1130 61-2351 1805 161-2760

148
Nematodirus helvetianus 85 0-170 1023 68-1550

Large intestine
Oesophagostomum radiatum 640 320-1360 610 110-1720
Trichuris globulosa 43 9-104 86 12-148
Total worm burden 6627 1928-8698 7703 1865-9675

Packed Cell Volume (%)
Months Months
ml)
(Gm/100
Haemoglobin
fig- 6 .5 : Mean (±S.D) haematological, serum protein and plasma pepsinogen values for resident
cattle at Iganjo and Kambaa farms
U9
animals. During the whole experiment, pepsinogen levels rarely exceeded the level o f 2.0
i.u./tyrosine and mean values were consistently around 1.5 i.u./tyrosine (range 0 .5 -2 .3 ) at
Iganjo farm and 1.8 i.u./tyrosine (range 1.4-2. 6) at Kambaa farm.
6 .3 .6 Weight gains
The mean liveweights o f the resident cattle recorded during the study are shown in
Fig. 6 . 6 . Most o f the animals displayed a gradual increase in body weight, and the general
condition o f some o f the calves was rather poor especially at Kambaa farm. Final average
w eights o f cattle at Iganjo and Kambaa in late April 1994 were, respectively 258 kg and 198
kg, with average total gain o f 138 kg (383 g day'1) and 84 kg (233 g day'1), respectively
from starting weights the previous April 1993 (Fig. 6. 6).
6 .4 Discussion
The tracer worm burdens and pasture larval counts revealed 7 different genera of
nematodes with Haemonchus, Cooperia , Trichostrongylus and Oesophagostomum spp.
predominant throughout. These genera appeared to be equally influenced by prevailing
weather conditions, although C. oncophora was only found at Kambaa farm which had
cooler temperatures than Iganjo farm.
Haemonchus spp. larvae were the most numerous on pastures and in faecal cultures
and infective L3, although available at all times, were most numerous during the rainy
months. The consistent high prevalence of //. placei infection indicate that the parasite is
ubiquitous in cattle in these farms; it is generally considered to be the most prevalent and
pathogenic nematode species of cattle in Kenya (Mango et al., 1974; Waruiru et al., 1993a).
The next most numerous species, Cooperia and Trichostrongylus, were also most prevalent
150
300
50
A M J J A S O N D J F M A
Month
-*-|ganjo ^K am baa
F ig . 6 . 6 : Mean (± S . D ) liv e w e ig h t c h a n g e s in re s id e n t
c a ttle a t Ig a n jo a n d Kambaa fa rm s
151
on the pastures during the wet months. The main feature o f 0. radiatum L, was the gradual
rise during the early months of the rains, compared to the L, of Haemonchus,
Trichostrongylus and Cooperia species. This can be explained by the longer pre-patent period
of oesophagostom es rather than by a delay in the onset of suitable climatic conditions (Lee
et a l., I960). Roberts and O’Sullivan (1950) suggested that temperature and rainfall
requirements o f H. placei and O. radiation are similar and Lee and colleagues (1960)
confirmed that the Lj develop readily at constant temperatures from 25 °C to 33 °C. The
slight increase in the proportionate contribution o f Oesophagostomum spp. L, with the onset
of the dry months may support the observations o f Vercruysse (1983) and Agyei (1991) who
found them to increase their contribution on dry season egg counts. The generally low
numbers o f Nernatodirus and the consistently very small numbers o f Strongyloides recovered
from tracer calves show that infective of these species were not numerous on the pastures
at any time o f the investigation. However, Nernatodirus spp. were more prevalent at Kambaa
farm, possibly due to its cooler temperatures and higher rainfall in this farm than Iganjo
farm. Temperature and rainfall are the principal climatic factors influencing the incidence of
internal parasites and can be used to predict outbreaks o f parasitism to be predicted with
reasonable accuracy (Gordon, 1948; Ross and Woodley, 1968). The pattern o f herbage larval
counts, strongyle egg counts and total worm counts in both yearling cattle and tracer calves
in the two farms reflected the rainfall patterns. The importance of rainfall in the development
of pre-parasitic stages is well known (Lee et al., 1960; Durie, 1961; Rose, 1964) as is its
effect in facilitating the migration of L, larvae from faecal pats onto pasture (Rose, 1962;
Chiejina and Fakae, 1984).
Total worm counts in both yearling and tracer animals increased during the wet
periods. The counts made from tracer calves demonstrated that this increase was associated
152
not o n ly with a possible lack of resistance but also with a greatly increased level of
contam ination o f the pastures with infective L3 during the wetter months (March-June and
O ctober-D ecem ber). The low counts over the drier months indicated a reduced larval
availability on pastures and a close relationship between level o f pasture contamination and
rainfall, as temperatures rarely fall below 10 °C which is the minimum limit for development
(D innik and Dinnik, 1958). The smaller nematode populations in yearling cattle in the drier
months (August and February) could be attributed, therefore, not only to increasing
resistance but also to a lower challenge from reduced infective L3 population on the pastures.
Persistence of a parasitic nematode infection may be due to the successful survival of
the pre-parasitic stages on the pasture and/or o f the adults or hypobiotic larvae in the host.
The post mortem and faecal examination results showed that adult worms o f various GI
nematodes and the digestion o f abomasal mucosa did not reveal the presence of significant
numbers o f hypobiotic H. placet worms in the digesta in the present study. The absence of
arrested H. placei larvae in cattle probably reflects the rainfall distribution and/or relative
mild climatic conditions in the study area. The dry hot (January-March) and the cold dry
(July-September) seasons, with occasional rainfall are short in comparison with the severe
dry seasons in West or Central Africa (Kaufmann and Pfister, 1990; Pandey et a\., 1993).
Hypobiosis therefore, does not seem to play any important role in the epidemiology o f H.
placei in the study area. Owing to the high fecundity o f H. placei, residual female worms
in the total population as shown in Table 6.2 could favour the transmission o f the parasite
from one rainy season to the other, and for the successful repopulation o f the pastures
during the favourable rainy season (Fakae, 1990).
Serum pepsinogen values were low and were not correlated with faecal worm egg
counts even though the abomasal nematodes (H. placei and T. axei) were among the
153
predominant species. However, it is evident from other studies that a rise in plasma
pepsinogen is not necessarily an important feature in the pathophysiology o f H. placei or
T. axei infections in calves (Ross et al., 1967; Gennari et al., 1991).
The lower haematological indices and weight gains o f yearling cattle at Kambaa farm
might be attributable to differences in farm management, other farm-level factors (Hassan
Wan et a l., 1989 ) and concurrent infection with F. gigantica as liver fluke eggs and adult
liver flukes were detected sporadically in their faeces and livers, respectively. Earlier studies
by others have shown that there is enhanced pathogenicity of simultaneous exposure to F.
hepatica and H. contortus in sheep (Presidente et al., 1973), and O. ostertagi in cattle
(Burden et al., 1978). Other workers have shown that bovine fasciolosis results in
considerable economic loss attributable to impaired feed conversion efficiency at the low
level o f (subclinical) infections, while at the higher (clinical) infection levels, inappetence
also contribute to the loss (Hope Cawdery et a l., 1977; Chick et al., 1980).
154
-C h a p te r 7-
DEVELOPMENT AND SURVIVAL (PLOT STUDIES) OF
INFECTIVE LARVAE ON PASTURE
7.1 Introduction
The size o f the populations of infective third-stage larvae (L 3) o f ruminant nematode
parasites on pasture are the result o f the number of eggs spread with the faeces by the
animals, their development rate into larvae and the survival and traslation o f these larvae
onto the grass (Rossanigo and Gruner, 1994).
The relationships between climatic factors and strongylid populations have been
established for several different objectives: determination o f areas and season favourable to
the development o f the different species (Levine, 1980; Fabiyi et al., 1988; Gatongi et al.,
1988), determination of factors o f parasitic risk between different herds (Suarez and Cabaret,
1991), mathematical modelling of the parasitic populations on pasture and/or in the hosts so
as to forecast periods with higher risk o f infection for the herd and the most efficient times
for deworming (Thomas and Starr, 1978; Callinan et al., 1982). For determining factors such
as the developmental rate o f larval populations on pasture, a primary feature is the use o f the
best climatological parameter (for example, rainfall in the present study) that is related to the
parasite population level and which can be easily measured (Rossanigo and Gruner, 1994).
For development o f ruminant nematodes, the main constraint is availability o f moisture inside
the faeces (Berbigier et al., 1990) and herbage (Gruner et al., 1989; Besier and Dunsmore,
1983).
Knowledge of the origin of larvae of the major GI nematodes of cattle and the time
course o f their availability on pasture is useful. A control system involving the movement
of calves at set times of the year to avoid exposure to high larval infestation has been based
on such information (Michael, 1969b). Various alternative procedures designed to prevent
the build-up o f dangerous numbers o f larvae on the pasture (Michael et al., 1981) also
depend on the knowledge o f seasonal pattern o f larval infestation on herbage.
The present study was aimed at providing such information relevant to central Kenya,
to guide in the formulation o f sound control strategies.
7.2 M aterial and methods
Within a fenced area o f pasture measuring about 50 m X 100 m a series of 72 plots
of 2 m 2 each were demarcated. Ditches were dug between the plots to avoid cross
contamination during heavy rains, and the array of plots was fenced to prevent the entry of
animals. Observations commenced in June 1995, when no further larvae from previous
grazing could be recovered from the pasture. The grass on each plot was periodically clipped
to maintain the herbage at a height and density similar to that found in adjacent paddocks
which were permanently grazed by cattle. The clippings remained on the plot.
At the beginning o f each month from July 1995 to June 1996, faecal pats, each
weighing 2 kg and with a known number of eggs per gram of faeces (epg), as determined
by a modified McMaster technique (MAFF, 1986), were deposited at the centre o f each of
5 plots. The faeces were obtained from 4 donor calves each previously artificially infected
with mixed cultures of between 10,000 and 20,000 infective larvae (L3) o f strongylid
nematodes o f cattle. The proportion of the eggs of each nematode genera ranged from 35 to
65 % for Haemonchus spp., 30-50 % for Cooperia spp., 10-25 % for Oesophagostomum
spp. and 5-15% for Trichostrongylus spp., as judged by differential larval counts from the
156
-ultures. T h e potential production of L, from the pats in each series was estimated by
-ulturing 4 separate 10 g samples and was found to be invariably high. Faecal cultures were
prepared by the method of Hansen and Perry (1994) and identification o f L3 was based on
[he characteristics described by Keith (1953). A sixth plot was not contaminated, but was
sampled each fortnight to detect any extraneous infection.
The plots were sampled fortnightly, after contamination, by collecting 60 uniformly
distributed plucks o f herbage per plot, taken at ground level. Sampling was continued until
no larvae w ere recovered from the herbage on 2 consecutive occasions (Gibson and Everett,
1967). Infective larvae were recovered from pasture samples using the technique of Hansen
and Perry (1994) and larval abundance was expressed as L, per kg o f herbage dry matter (L,
kg'1).
M eteorological measurements were supplied from the Keriita Forest Station, 1 km
from the experimental plots. The records were limited to the maximum and minimum air
temperatures, relative humidity and rainfall.
7.3 R esults
N o infective, third-stage larvae (L3) were recovered from any o f the control plots on
any sampling occasion throughout the experiment. Third-stage larvae of Haemonchus,
Cooperia, Oesophagostomum and Trichostrongylus were consistently recovered from the
second w eek after contamination in each month o f the year, with substantial numbers being
recovered between 2 and 6 weeks after contamination. Larval counts were substantially
higher during the rainy seasons but moderate levels of pasture infestation were obtained
throughout the rest o f the year. The concentrations on pasture o f L, o f the four genera,
corrected for the numbers o f eggs used to contaminate the plots, are shown for each month
in Fig. 7 .1 .
157
-o------ II
LOG IN F E C T IV E LARVAE/KG DRY PASTURE/MILLION EGGS
Weeks after egg deposition
Fig. 7.1: Recoveries (average of 5 plots) of infective larvae per

kilogram of pasture dry matter, log transformed,(log (X + 1)
and corrected for the numbers of eggs deposited, on plots
contaminated sequentially from July 1995 to June 1996.
It, Haemonchus; C, Cooperia; 0, Oesophagostomum;
T, Trichostrongylus
All the genera appeared to be remarkably similar in their ability to hatch, develop to
L, and survive under the local environmental conditions. The survival time of Lj was 12 to
16 weeks after the last faecal contamination. Generally, there was a higher proportion of
Haemonchus L, recovered than o f the other 3 genera.
The mean maximum and minimum temperatures, relative humidity, rainfall and the
number o f wet days recorded for each month are shown in Fig. 7.2. Generally, the weather
conditions during the period o f the study were about average for the area. The area received
1395 mm o f rain over the 12 months of the study, o f which 25.9% fell during the short rains
and 52.3% during the long rains, with rain falling on more than 10 days in each month
during these periods. During other months, low to moderate falls o f rain were recorded on
only a few days of each month.
7.4 Discussion
It was expected that the study site, which enjoys a bimodal rainfall pattern, a high
relative humidity and mean maximum temperatures ranging during the study from 17.5 °C
to 21.6 °C, would provide near-optimum conditions for the development o f strongylid larvae.
The results described here were consistent with this expectation, as not only were L3 o f the
four genera recovered from the pasture throughout the year, but maximum larval counts
almost invariably occurred within 2 to 6 weeks o f the last contamination of pasture.
It is evident from this work that more eggs completed their development following
contamination during the rainy seasons and this is consistent with other studies which relate
such warm, wet conditions to rapid development o f eggs to L3 (Reinecke, 1960) and their
roass migration onto the pasture (Durie, 1961). It is thus clear that measures directed at
substantially reducing the contamination o f pasture during such warm, wet seasons would
159
30 -i
Max
Min
o I— '— l— 1 I— >—I— i— I— '— I— 1 I— 1 1— >— I— ■— I— 1 1— '— I— 1

Ju ly Aug Sept Oct Nov Dec Jan Feb Mar A pril May June
Fig. 7 . 2 : Meteorological data for Kimcnde, Kianibu District (Study site)

from July 1995 to June 1996
160
forestall high larval infestation on herbage, as concluded previously by Fabiyi and Copeman
(1986). The temperature was more or less constant throughout the study period (Fig. 7.2)
and the present Findings suggest that under these climatic conditions, rainfall is the most
important limiting factor for the survival of the free-living larvae o f the GI nematodes of
cattle. In addition, since L3 o f all the genera were recovered from the herbage throughout
the period o f investigation, weather conditions do not appear to have a greater effect on one
than another (Okon and Akinpelu, 1982).
Lower yields of L3 were usual during the period o f scarce, erratic and non-soaking
rains (July-September and January-February), as is consistent with the findings o f other
workers (Reinecke, 1960; Durie, 1961; Fabiyi et al., 1988). It is notable, however, that pats
deposited in January and, to a lesser extent, in July produced relatively high numbers o f L3.
During these months rain fell on only 2 to 4 days, but the pasture was nevertheless moist,
especially in the morning, from very heavy dews. Also, the grass was particularly dense,
which according to Branagan (1973), retains residual moisture and contributes substantially
to transpirational humidity. It is likely that these conditions provided the necessary moisture
for the development and translation o f L3 (Riek et al., 1953; Krecek et al., 1995). Also, it
would appear that the high initial moisture and the large size of the pats used in this study
ensured that satisfactory moisture and temperature conditions were maintained inside the pats
during the crucial 7 days post-contamination when eggs probably developed to L3 (Chiejina
and Fakae, 1989).
Throughout the year, the survival times o f 12 to 16 weeks were relatively short when
compared to survival times o f up to 9 months reported from temperate countries (Rose,
1962). Similar short survival times for L3 of ruminant strongylids were recorded during the
wet season in Nigeria by Okon and Enyenihi (1977), in the wet tropical climate of Northern
161
Queensland (Fabiyi et al., 1988) , in the wet and dry zones of Fiji (Banks et al., 1990) and
in the w et tropical environment of the Pacific island of Tongatapu, Tonga (Barger et al.,
1994).
Several workers have correctly cast doubt on the practice o f pasture spelling and
rotational grazing as a means o f controlling internal parasites o f ruminants in temperate
regions, mainly because the time needed to ensure a significant reduction in larval numbers
is too long for economic management o f the pastures (Gibson and Everett, 1967; Michel,
1969b; Donald, 1974). The rapid decline in larval populations noted here, however, may
well make rotational control methods based on changing pasture practicable in this type of
climate, with no real dry season. In addition, if pasture could be maintained free from new
egg deposition for longer than the survival time of L3, the use of novel forms of
chemotherapeutic control like the sustained release devices (Waruiru et al., 1997) may also
be feasible. Both these possibilities are being explored in continued studies in Kenya.
16 2
- C h a p t e r 8-
COMPARATIVE EFFICACY OF MORANTEL SUSTAINED RELEASE
TR IL A M IN A T E BOLUS AND CONVENTIONAL ANTHELM INTIC
TREATEMENT AGAINST GASTROINTESTINAL NEMATODES
8.1 Introduction
Anthelmintics have been widely used for the treatment of clinical parasitic
gastroenteritis (PGE) in cattle, but in recent years the importance o f subclinical infection has
increasingly been recognized and attention has been more directed to the prevention of
infection. Although conventional single anthelmintic treatment effectively eliminates the
majority o f GI worms, the already infested herbage to which grazing cattle are exposed is
altered little by such treatment and re-exposure to new infections continues if the cattle
remain in the same environment after treatment (Prosl et al., 1983). A combination of
strategic treatment and movement to safe pasture as proposed by Michael (1969a) has since
been widely used together with other strategies (Nansen, 1993). However, in many places
pasture and management limitations have raised a need for preventive measures based on
continuous medication or repeated treatments with anthelmintics, in order to eliminate
existing worm burdens and reduce pasture contamination and reinfection (Thomas and Bell,
1988).
The use o f intraruminal sustained release bolus containing morantel tartrate (MSRB;
ParatectR Bolus, Pfizer) has provided a successful method to remove existing worm burdens
and prevent reinfection over a period of 60 to 90 days (Jones, 1983). The efficacy o f the
MSRB in controlling PGE in cattle under a variety o f field grazing conditions has been
confirmed by a number o f workers (Guldenhaupt and Burger, 1983; Hawkins et a l., 1985;
163
Ciordia et al., 1987). The release profile o f the morantel bolus now marketed (MSRT;
Paratect FlexR Bolus, Pfizer) has been shown to confer protection of first year calves
throughout a 90 day grazing period (Vercruysee et al., 1989).
The strategic use o f the MSRT bolus has been well documented under temperate field
conditions with distinct grazing season (Rickard et al., 1989; Grimshaw et al., 1989;
Vercruysee et al., 1992; Hertzberg et al., 1994). However, there is little information on the
use of MSRT in tropical environments and the aim o f this study was to determine the
efficacy o f MSRT in controlling Gl nematode parasitism in naturally infected grazing calves
in a Kenyan tropical environment.
8. 2.1 Experimental design
The experiment was conducted at Iganjo farm from 4 March to 30 December 1993,
starting at the onset o f the long rains. Forty Friesian/Ayrshire crossbred calves (24 male and
16 female) originating from the farm and previously grazed on infected pastures were
selected for the trial. Fourteen days prior to the start of the trial the calves were introduced
to the experimental pasture plots of 10 acres, grazed previously by infected young cattle, to
balance nematode levels in the calves and on the pasture. Prior to the trial, all calves were
sprayed with an acaricide once a week for ticks and were tested for haemoparasites.
At the start of the trial, the calves were treated with oral triclabendazole (FasinexR,
Ciba-Geigy; 12 mg kg ') for Fasciola gigantica infection. The calves were divided into 4
equal groups o f 6 male and 4 female calves on the basis of age and weight; the mean ( ±
S.D) weight and age of the calves was 159.2 ± 9.3 kg and 9.0 ± 0.5 months, respectively.
The experimental plot was divided into four 1 ha paddocks of similar configuration and the
16 4
four groups o f calves allocated to them. Throughout the trial the calves grazed Kikuyu grass
(.Pennisetum clandestinum) but due to grass shortage caused by drought, they were fed equal
amounts o f supplementary hay and wheat bran from late August to the end of the trial. Water
and mineral blocks were available at all times. Calves in group 1 (T -l) were non-medicated
controls and those in group 2 (T-2) each received one MSRT bolus on day zero. Calves in
group 3 (T-3) were drenched with albendazole on day zero while, those in group 4 (T-4)
were drenched with albendazole on day zero and day 14 post turnout. After MSRT
administration the calves in T-2 group were confined for 24 h to a pen for observations to
confirm retention o f the bolus and to monitor any adverse reactions. Thereafter the
experimental calves were placed in their respective paddocks for the entire experimental
period. The anthelmintic bolus was administered by a specially designed balling gun
according to the manufacturers recommendations. Albendazole (ValbazenR, SmithKline
Beecham Animal Health Products) was administered orally using a callibrated syringe at a
dose of 7.5 mg kg"1. The MSRT cost to farmer/ > 100 kg animal during the study period was
US$ 15 and the handling cost o f animals for set up, round up and treatment (average Kenyan
wage/day) US$ 2 giving a total o f US$ 17, while the basic costs per animal for conventional
anthelmintics (excluding veterinary costs) ranged from US$ 6.5, for ivermectin; 5 .9 , for
albendazole and fenbendazole and, 2 for levamisole, respectively.
Three calves from each o f the 4 groups were selected at random for slaughter at the
end of the trial for residual worm recovery. Pairs o f tracer calves, 5-6 months of age and
raised worm-free since birth, were introduced into each paddock to evaluate the initial
(March), interim (May and September) and final (December) levels o f pasture infectivity by
nematode larvae. These tracers were allowed to graze for 28 days after which they were
boused on concrete floor for 21 days prior to necropsy and worm recovery.
165
Herbage samples for strongylid larval counts and rectal faecal samples were collected
at the start o f the trial and monthly thereafter. Individual body weights were recorded for all
experimental calves before the trial commenced and then at monthly intervals until trial
termination. Jugular blood samples were taken monthly from all the calves for estimation of
packed cell volume (PCV), haemoglobin (Hb), total protein (TP), and serum pepsinogen
levels (R oss et a l., 1967; Coles, 1974). Animals were observed daily as part of the normal
management practices in the experimental farm and were examined thoroughly at each
sam pling.
Herbage and faecal samples were processed as described by Hansen and Perry (1994)
and M AFF (1986), respectively, while all necropsy, adult worm recovery procedures,
counting and identification techniques were performed as previously described (MAFF,
1 9 8 6 ).
8 .2 .2 Statistical analysis
A one way analysis o f variance was performed on the data for individual calves for
each sampling period to assess the effect o f treatments on nematode egg excretion, worm
counts, and iiveweight gains. To normalize distribution o f the data o f various parameters to
fulfill parametric test requirements, the data were transformed in the form o f In (x + 10).
Treatment comparisons were made by using Tukey’s test (Fowler and Cohen, 1990).
8.3 Results
8.3.1 Pasture larval counts
The pasture larval patterns for the 4 paddocks are shown in Fig. 8.1. Herbage
samples taken at the start o f the study (day 0) showed that the 4 paddocks were contaminated
16 6
with similar numbers o f strongylid infective larvae (L,). There was a gradual, parallel
decrease o f pasture larval concentration from May to August in the 4 paddocks followed by
an increase to a peak mean count of 1600, 1100 and 1300 L3Kg'1 dry matter in September
on paddocks T - l, T-3, and T-4, respectively. In the T-2 paddock only 495 L3 kg '1 were
recovered in September and over the rest of the experiment the larval counts remained lower
than those o f control T -l paddock (Fig. 8.1). There were no statistical significant differences
(P > 0 .0 5 ) between counts o f paddocks T -l, T-3 and T-4 during this period.
8.3.2 Faecal egg counts
The mean number o f strongylid egg counts from the four groups of calves throughout
the trial period are presented in Fig. 8.2. There were no significant differences between the
groups at the start of the trial. However, counts from the T-2 calves were reduced by 100
% (P < 0 .0 0 1 ) following treatment and remained significantly lower (P < 0 .0 5 ) than counts
from control T -l calves up to the end of the trial. Faecal egg counts in the albendazole
treated calves were significantly lower after treatment up to May for T-3 calves (P < 0 .0 1 )
and July for T-4 calves ( P < 0 .0 1 ), compared to control T -l calves. Thereafter, epg counts
rose steadily in both the T-3 and T-4 groups and were indistinguishable from those o f the T-l
control calves at the termination of the study (Fig. 8.2).
8.3.3 Worm counts in tracer calves
Worm numbers in tracer calves are presented in Table 8.1. Tracer calves grazing the
167
1.700 -
Larvae per Kg dry herbage
Month
T-1 ^ T - 2 -^T -3 T-4
F ig . 8 . 1 : P a s tu re c o n ta m in a tio n w ith s t r o n g y lid in f e c t iv e la rv a e
168
Eggs per gram of faeces (epg)
T-1 T-2 -^T-3 — T-4
F ig . 8 . 2 : Mean s t r o n g y lid e g g s p e r g ra m o f faeces
169
first month (March) became infected with similar worn burdens. The number of nematodes
recovered from subsequent T-2 and T-4 tracer calves decreased and remained at a low level
for the rest o f the trial, with a 55-85.7 % reduction in the worm counts o f the tracers grazing
the T-2 paddock. The infection acquired by the tracers grazing the T -l and T-3 paddocks
after turnout ranged from a mean worm count o f 4054 and 4390 (March) to 12751 and 7801
(September). Adult H. placei and Cooperia spp. (C. pectinata and C. punctata) were
recovered from all the tracer calves necropsied during the entire period, with intensities of
infections ranging from 56.9% to 65.3% and 21.6% to 27.0% o f total worm burdens,
respectively. T. axei was recovered from all but 2 o f the tracers during the entire period,
constituting between 3.7% and 9.2% o f the worm burden while O. radiatum was recovered
from all calves (intensity o f 3.5-10.4% ). Very few specimens o f Nematodirus helvetianus
(intensity o f 0 .3 -1 .9 %) and T. globulosa (intensity o f 0.2-0.7% ) were recovered.
8 .3 .4 Worm burdens at termination o f the trial
As shown in Table 8 .2 , the total worm counts were significantly lower (P < 0 .0 5 ) in
the MSRT-treated T-2 calves and represented a reduction o f 92% compared to 44% (T-3)
and 58% (T-4) relative to the T -l, control calves.
8 .3 .5 Liveweight gains
The comparative average body weights o f the calves are shown in Fig. 8.3 and I able
8.3. The 4 groups of calves had increasing but diverging liveweight gain up to September
after which the weight curves levelled off presumably due to lowering of grass quality and
quantity because o f lack o f rain. At the end o f the trial, the T-2 calves had a highly
significant (P < 0 .0 0 1 ) mean liveweight gain advantage o f 69.2 kg over the T-l control
calves, while the T-4 calves had an advantage o f 23.2 kg (P < 0 .0 5 ) over the controls ( lable
8.3).
170
Table 8.1: Worm counts recovered from tracer calves (2 calves per group) and in parenthesis the percentage worm reduction on paddocks T-2, T-3,
and T-4 compared to T -1 _____________________________________________________________________________________
Month Paddock H. placet T. axel Cooperia spp. N. helvetianus O. radiatum T. globulosa Total
March T-l 2710 359 578 11 695 6 4359
1668 607 864 7 592 11 3749
T-2 2679 744 912 0 611 4 4950
2147 324 694 0 819 2 3986
T-3 2567 516 678 19 588 7 4375
2175 538 902 9 816 0 4440
T-4 2100 539 929 40 713 0 4321
2540 493 617 75 663 0 4388
May T-l 3600 810 1338 75 910 33 6766
3326 730 774 121 1091 18 6060
T-2 1579 595 422 14 392 7 3009
1237 (59.3) 397 (35.6) 573 (52.8) 29 (75.0) 509 (54.9) 16 (53.8) 2761 (55.0)
T-3 2917 487 713 43 736 18 4914
171
1901 (30.4) 583 (30.5) 893 (23.9) 26 (64.8) 692 (28.6) 7 (50.9) 4102 (29.7)
T-4 2681 251 409 14 306 3 3664
1560 (38.8) 189 (28.6) 319 (65.5) 8 (88.8) 363 (66.6) 5 (84.3) 2444 (52.4)
September T-l 7824 761 1439 19 2182 16 12241
8838 353 2151 37 1854 28 13261
T-2 1119 0 451 0 518 11 2099
853 (59.3) 0 (100) 305 (78.8) 0 (100) 374 (77.9) 19(31.8) 1553 (85.7)
T-3 4767 970 1617 22 1254 16 8646
4566 (43.9) 891 (-) 1172 (22.3) 50 (-) 1365 (35.1) 12 (36.4) 8056 (34.5)
T-4 4118 471 1139 12 572 6 6318
2049 (62.9) 818 (-) 835 (53.5) 20 (42.9) 796 (66.1) 4 (77.3) 4522 (57.5)
December T-l 6355 338 2010 109 1299 64 10175

5165 552 1364 179 1715 90 9065
T-2 1285 0 340 18 275 22 1940
1421 (76.5) 0 (100) 494 (75.3) 8 (90.9) 339 (79.6) 12 (77.9) 2274 (78.1)
T-3 4100 770 1113 104 913 14 7014
3602 (33.1) 676 (-) 1055 (35.7) 68 (40.3) 1013 (36.1) 22 (76.6) 6436 (30.1)
T-4 2584 695 722 83 719 30 4833
2320 (57.4) 798 (-) 1463 (35.2) 59 (50.7) 669 (53.9) 46 (50.6) 5355 (47.0)
T « h lc H . ' M e a n n u m b e r a r x l.in p a r e n t h e s is , th e p e r c e n t a g e w o r m r c t lu c it o n a fte r a n th e lm in tic tr e a tm e n t o f a d u lt a n d i m m a i u n
w orm s from 3 calves per group nccropsiscd at trial term ination
Parasite/group T -l T-2 T-3 T -4
Haemonchus placei 2773* 233b (91) 1432*(44) 1154*(55)
Trichostrongylus axei 572a 25b (96) 418a (27) 189a (70)
oo
»n
00 (9
Cooperia spp. 65b (92) 425a (50) 319a (63)
X>
o<
o
o
r—
Nematodirus helvetianus 95a 0b ( 100) 53a (44)
Oesophagostomum radiatum 667a 53b (92) 32a (51) 329a (51)
Trichuris globulosa 0 3 0 4
All worms 4765a 379b (92) 2652a (44) 1995a (58)
Worm counts in the same row with different superscripts differ significantly (p < 0 .0 5 ).
Table 8.3: Mean bodyweight and weight gains of control (T-l) and treated (T-2, T-3 and T-4) calves
Groups No. of animals Mean initial Mean final Mean gain Mean daily gain
weights (kg) weights (kg) (kg) (g d ay1 )
T-l 10 159.8 ± 6 .1 2 1 9 .2 ± 5 .8 5 9 .4 + 4 .8 200 .0 + 7 .4
T-2 10 158.5±8.7 2 8 7 .1 + 6 .2 a128.6±7.5 530.0+13.1
T-3 10 161.2±9.7 2 1 3 .7 + 4 .3 5 2 .5 + 5 .7 170.0+6.9
T-4 10 162.2 ±9.1 244 .8 + 9 .1 “82.6+ 6.3 270.0+9.1
'Significantly different from group T-l (P < 0.05).

Liveweight (Kg)
T-1 ■*" T-2 "^T-3 — T-4
F ig . 8 . 3 : Mean liv e w e ig h ts o f tre a te d a n d c o n tro l ca lv e s
173
8.3.6 Blood parameters and clinical observations
Mean serum pepsinogen levels were within the range of 1-2 i.u. tyrosine per litre with
no significant differences (P > 0 .0 5 ) between the 4 groups, and did not correlate with epg
counts. There was a general decline in PCV, Hb and TP levels from September to December
in all groups although levels remained within the limits normally found in cattle and no
significant differences (P > 0 .0 5 ) were found between the groups. T-2 and T-4 calves had a
group mean PCV o f 30% and 31 % in November compared to 26% and 23% in T -l and T-3
calves. Clinical signs associated with strongylosis were recorded only in T-l and T-3 groups
during this period. These included diarrhoea, unthrifty coats, submandibular oedema,
anaemia, weakness and progressive emaciation. No adverse reactions were observed in the
T-2 calves during the study, including the time o f MSRT administration and the subsequent
24-h period.
8.4 Discussion
The efficacy of the MSRT-treatment regime was evident from the significant long
term reduction in epg levels o f the MSRT-treated T-2 calves as compared with untreated T -l
calves. This was supported by low herbage larval counts and reduced numbers of nematodes
recovered from the tracer calves and 3 T-2 calves slaughtered at the termination o f the trial.
These findings confirm earlier results obtained in the field in temperate climatic environments
(Vercruysse et al., 1992; Hertzberg et al., 1994).
The MSRT-treated T-2 calves gained significantly more weight than the control T -l
and albendazole (T-3 and T-4) treated calves. In addition to the pathophysiological changes
brought about by GI nematodes, parasite induced inappetence may also contribute to poor
performance (Entrocasso et al., 1986a; Thomas and Bell, 1988; Bell et a l., 1988). It is
174
therefore highly probable that GI nematodes caused a significant reduction in feed intake of
T-l and T-3 calves contributing to their poorer performance in liveweight gain compared
with the other groups (Holmes and Coop, 1994).
Although single conventional anthelmintic treatment leads to an immediate removal
of parasite burdens in the gut, the parasite load o f the grazing pastures is only altered little
by this treatment (Prosl et al., 1983). Thus, unless animals are moved to ‘safe pastures’ they
will quickly become reinfected with subsequent further damage and depression of
performance as observed in the albendazole-treated (T-3 and T-4) calves in the present study.
However, had the albendazole treatment been given at regular intervals (i.e. 3 months) over
the study period, one could expect a long-term preventive effect o f this drug as well.
The 92% reduction in mean total numbers of parasites at the end of the trial and the
improved weight gain o f the MSRT-treated (T-2) calves in this study was similar to the
results o f previous studies using the older morantel sustained release bolus (MSRB) (Jones
and Bliss, 1983; Sykes et al., 1987). These data indicate that in the Kenya highlands, MSRT
was as effective as in the temperate environments in reducing GI nematode infections and
pasture infectivity as well as providing a significant weight gain advantage over non-
medicated control calves (Vercruysse et al., 1992; Hertzberg et al., 1994).
There has been concern that use o f controlled release devices might promote
development o f drug resistant populations o f parasites (Donald, 1985). Administration of
anthelmintics in sustained release formulations, could cause an intense selection pressure
resulting in anthelmintic resistance. Little empirical evidence is currently available to assess
these potential effects (Anderson, 1985; Zimmerman and Hoberg, 1988). The MSRT bolus,
field tested and in use for more than 10 years, has yet to be directly associated with drug
resistance in helminths (Coles et al., 1994) although selection o f a morantel resistant strain
17 5
of O. ostertagi has been reported where the sustained release bolus was experimentally used
(Borgsteede,1988).
The advent of highly effective chemoprophylaxis has raised the question o f whether
or not animals so protected receive sufficient antigenic stimulation to induce immunity
(Vercruysse et al., 1994; Bell et al., 1996). Control systems in temperate environments based
on sustained release boli have a long active life, with expected duration of efficacy o f 90 to
135 days. This raises the question o f whether these systems allow sufficient larval challenge
for development o f immunity (Armour et al., 1988; Vercruysse et al., 1992; 1994). The
development o f immunity might not be affected to the same extent by use o f sustained release
boluses in those tropical areas where the animals graze all year round and trickle infections
occur continuously. However, the acquired immunity may be compromised during prolonged
dry spells leading to outbreaks of parasitic gastroenteritis (PGE).
For the control o f endoparasitic nematodes o f ruminants, the development of
sustained-release bolus technology for the administration of anthelmintics is viewed as an
important advance (Probert, 1994). The use o f a bolus allows a measured quantity o f drug
to be delivered directly to the rumeno-reticulum over an extended time period. This allows
for a reduction in labour costs to the farmer and handling stress to the animal while giving
sustained anthelmintic cover. However, for all classes o f anthelmintics, a proportion o f the
administered drug is excreted either in the faeces or urine, often in largely unmetabolised
form (Strong and Wall, 1990). Concern has been expressed by many researchers about the
impact o f excreted anthelmintics on insects o f the dung community and the potential effects
on dung degradation and nutrient recycling (Herd et al., 1993; Strong et al., 1996).
The success of controlled release systems in the control o f PGE in ruminants in
developing countries will depend upon the demonstration o f cost effectiveness. The
176
anthelmintic compound will have to be released and be effective at a time when the
susceptible population o f target parasites is present. In many tropical and subtropical regions
however, the actual patterns o f infection have yet to be elucidated. Until it is known when
effective levels o f the anthelmintics should be delivered to the host, the true value o f such
treatment in these environments cannot be fully recognized or evaluated. Moreover, although
controlled release systems should prove to be among the most significant improvements in
the control o f helminth parasites, they will not necessarily preclude the need for conventional
administration o f anthelmintics. As the epidemiology and transmission patterns are being
clarified, control programmes can incorporate the use o f boluses at one time o f the year with
conventional dosing at other times. In cases where grazing on contaminated pastures
following conventional single-dose therapy would result in immediate reinfection, the bolus
approach would be preferable. But if continual exposure to infection is not likely, the cost
o f a bolus may not justify its use (Zimmerman and Hoberg, 1988; Waruiru et a l., 1997).
177
- C h a p te r 9-
OVERWINTERING RESIDUAL GRASS INFECTIVITY IN PASTURES
PREVIOUSLY GRAZED BY DUDDINGTONIA FLAGRANS FED CALVES
9.1 Introduction
Field studies conducted in Denmark on the control o f gastrointestinal nematodes of
cattle have demonstrated that feeding of calves during the first two months of the grazing
season with the microfungus, D.flagrans grown on barley grain reduced herbage infectivity
and subsequently ingestion o f trichostrongylid larvae, mainly O. ostertagi, later in the season
(Wolstrup et al., 1994). An experiment conducted in 1993, showed that the strategic feeding
o f first season calves with D. flagrans over the first three months o f the grazing season was
able to prevent severe clinical trichostrongylosis in the late summer. These results also
demonstrated that larval populations o f Ostertagia and Cooperia were significantly reduced
on the pasture grazed by fungus-treated calves. In comparison, numbers of Nematodirus
larvae seemed less affected (Nansen et al., 1995).
The present investigation, conducted in 1994 was designed to determine the
overwintering residual grass infectivity in a pasture previously grazed by D.flagrans treated
and untreated calves.
9.2.1 Study area
The experiment was conducted at the field station o f the Royal Veterinary and
Agricultural University, 20 km West of Copenhagen, Denmark, on a permanent low-lying
pasture known to have a mixed parasite fauna o f the following genera: Ostertagia, Cooperia,
Nemaiodirus , Strongyloides and Trichuris. This pasture was grazed by two experimental
groups o f calves the previous year and group 1 calves had been fed fungal material (D.
flagrans grown on barley grain) once daily over a three-month period starting from turnout
(25th May 1993). The fungal-barley amount given corresponded to 200 g dry weight per
animal per day, and the approximate number o f chlamydospores was 106 per g fungal-barley
(d. w ). The control, group 2 calves received barley grains only, in the same amount as group
1 , over the same period.
9 .2 .2 Experimental design
Ten parasite-naive male Jersey calves, 6 months old were used. On May 2nd 1994
the animals were divided into two comparable groups, A and B, on the basis of body weight.
The average weight in group A was 188.4 ± 10.7 kg, and in group B, 1 8 8 .0 ± 2 2 .9 kg. The
total area available to the experiment was 2 .2 4 hectares and was divided by a fence into two
comparable plots, experimental plot B and control plot A, which had been grazed by group
1 and 2 calves o f the previous experiment, respectively. In the present study, these plots
were allocated to groups B and A calves which were set-stocked for 4 weeks, before being
housed for 3 weeks prior to slaughter on week (wk) 7 post-turnout. Herbage samples were
collected weekly, for the first 4 weeks, while faecal samples were obtained at weekly
intervals until termination o f the study. The calves were weighed on three occasions, at
turnout (week 1), at week 4 and during termination o f the experiment (wk 7).
9 .2.3 Herbage larval counts
Three grass samples were collected randomly from each o f the two plots weekly, for
the first 4 weeks. Each grass sample consisted of 300-500 g o f grass collected by hand
179
following a W-shaped route across each plot. Grass in close proximity to dung pats was
avoided. Third-stage (L,) trichostrongylid infective larvae were isolated by a technique
established by Jorgensen (1975) and Mwegoha and Jorgensen (1977), and subsequently (for
detailed description of the methods see Appendix 9.1) enumerated.
9 .2 .4 Faecal egg counts
Numbers o f trichostrongylid eggs per gram (epg) of faeces were determined using a
modified McMaster technique (Henriksen and Aagaard, 1976) (Appendix 9.2). From each
o f the two groups of calves three faecal cultures were established to determine the nematodes
at genus level. Each faecal culture comprised o f a bulk sample o f 2 gram o f faeces from each
animal. Four grams o f vermiculite and eight ml o f water were added to the (for more details
see Appendix 9.3) faeces (Henriksen and Korsholm, 1983). After incubation at 20-22 °C for
14 days, larvae were harvested by a modified Baermann technique (Jorgensen and Madsen,
1982).
9.2.5 Post mortem worm counts
At post mortem, the abomasum and the proximal four metres of the small intestines
were eviscerated and examined according to the procedures described by Gronvold et al.
(1989) and Satrija and Nansen (1993). Larvae and adult parasites were enumerated and
identified to genus level (MAFF, 1986).
9.3 Results
9.3.1 Herbage larval counts
The mean larval counts for the two plots remained very low especially in the first two
180
weeks o f sampling and were comparable throughout the sampling period (Fig. 9.1). Cooperia
spp. dominated numerically over Ostertagia spp. Lj, while, Nematodirus spp. L3 counts of
the two plots were comparable throughout the study period.
9 .3 .2 Faecal egg counts
The two groups o f calves started shedding eggs after week 2 post turnout and mean
faecal egg counts between the groups were roughly comparable (Fig. 9.2). There was a
predominance o f strongylid-type eggs ( Ostertagia spp., Cooperia spp.) and in addition, eggs
of Nematodirus spp. were encountered but in very small numbers in both groups o f calves.
Trichuris spp. eggs were also recovered on a few occasions.
9 .3 .3 Faecal cultures
Larvae recovered from faecal cultures set from pooled faeces of the two groups of
calves were comparable throughout the experimental period as shown in Fig. 9.3. However,
recovery o f larvae on the last day o f sampling was lower in group A compared to group B
cultures. There was a predominance o f Cooperia spp. over Ostertagia spp. in both groups
of calves over the entire sampling period, while, Nematodirus spp. larvae did not appear in
the faecal cultures, presumably because they require a longer period o f time to permit
hatching o f eggs and larval development.
9.3.4 Post mortem worm counts
Trichostrongylid species of Ostertagia, Cooperia and Nematodirus were found in the
alimentary tract o f slaughtered calves. Table 9.1 shows that the intestinal worm Cooperia
spp. was the predominant parasite in the gastrointestinal tract o f the two groups o f calves.
181
80
Weeks
— Plot A Plot B
F ig . 9 . 1 : H e rb a g e t r ic h o s t r o n g y lid la rv a l c o u n ts
o n th e p lo ts p r e v io u s ly g ra z e d b y ca lve s
fe d w ith n e m a to d e -tra p p in g fu n g u s
D . fla g r a n s ( p lo t B ) a n d b y c a lv e s
n o t o ffe r e d a n y n e m a to d e -tra p p in g
fu n g u s ( p lo t A )
182
Faecal egg counts (epg)
Group A Group B
F ig . 9 . 2 : Mean t r ic h o s t r o n g y lid faecal e g g c o u n ts

fro m e x p e rim e n ta l (g ro u p B) a n d c o n tro l
( g r o u p A ) c a lv e s g ra z e d on p lo ts p r e v io u s ly
g ra z e d b y c a lv e s fed w ith th e n e m a to d e -tra p p in g
fu n g u s D . f la q r a n s ( p lo t B) a n d b y c a lv e s
n o t o ffe r e d a n y n e m a to d e -tra p p in g fu n g u s
( p lo t A )
183
Infective larvae per 10 g of faeces ('000)
F ig . 9 . 3 : N u m b e r o f t r ic h o s t r o g y lid la rv a e h a rv e s te d
fro m fae ca l c u lt u r e s o f e x p e rim e n ta l ( g r o u p B )
a nd c o n tr o l ( g r o u p A ) c a lv e s fro m 3 0 th May
(w e e k 4) to 2 0 th Ju n e (w e e k 7) 1994
184
The average abomasal larval and adult worm counts o f Ostertagia spp. were markedly similar
in the two groups. In the small intestine, markedly large numbers o f Cooperia spp. relative
to Nematodirus spp. were recovered. The average total number o f parasites was relatively
higher in group A compared to group B calves. In both groups of calves, there were apparent
individual variations in worm recovery as shown in Table 9.1.
9.3.5 Body weight
The increase in body weight within the two groups was similar throughout the
experimental period as shown in Table 9.2. At the end o f the experiment, the average weight
of the experimental group B was relatively lower (206.0 ± 13.1 kg) compared to 208.2 ± 19.9
for the control group A calves.
9.4 Discussion
Overwintered population of infective larvae (L3) which survive on the pasture from
the preceding grazing season provide the source o f infection for calves turned out in spring.
The rate at which this population o f L3 has decreased will determine the extent o f the
infestation initially available to the calves (Rose, 1970). In the present observations, the rate
o f decrease of the larval population on the experimental pasture was similar in both plots A
and B in that by early May, the herbage infestation was at low level. Thus, when calves were
turned out, they were subjected to light herbage infestation and their faecal egg counts during
early summer were comparatively low.
The present observations confirm the impression gained from previous field
experiments that the large numbers o f eggs passed by infected calves later in the grazing
season (September and October) do not contribute significantly to the herbage infestation
18 5
Table 9.1 Mean worm counts o f two groups o f calves at necropsy on 22nd o f June 1994. Five animals were slaughtered from each
group of calves. The experimental group (B) o f calves grazed on a plot previously grazed by calves fed with the nematode
trapping fungus D. flagrans. The control group (A) o f calves grazed on a plot previously grazed by calves not offered
any nematode-trapping fungus
Abomasum Small intestines
Ostertasia spp . Cooperia spp. Nemaiodirus spp.
Group or calves Animal Larvae Adults Total Larvae3 Adults Adults Total
No.
Controls 17 176 760 936 186 14420 80 14686
(A) 516 274 700 974 244 4590 90 4924
524 242 10 252 4 20 0 24
518 100 2150 2250 9 12640 550 13199
186
559 177 0 177 777 7450 770 8997

Mean 194 724 918 244 7824 298 8366
(s.e) (30) (392) (372) (142) (2629) (153) (2694)
Experimental 530 117 510 627 5 810 30 845
(B) 533 20 2090 2110 31 800 60 891
514 24 0 24 49 8380 1310 9739
515 49 1740 1789 218 2520 410 3148
307 151 70 221 0 130 0 130
Mean 72 882 954 61 2528 362 2951
(s.e) (26) (434) (421) (40) (1516) (248) (1771)
“Larvae = Larvae not differentiated to species level

Table 9.2: The average ( ± S.D) increase in body weight (kg) o f experimental (group B) and control (group A) calves from 2nd May
(week 0) to 22nd June (week 7)
Group No. of Mean initial Mean interim Mean final Mean gain Mean daily gain
animals weight (kg) weight (kg) Weight (kg) (kg) (g d a y 1)
(Week 0) (week 3) (week 7)
A 5 1 8 8 .0 ± 2 2 .9 193 .4 ± 2 2 .1 2 0 8 .2 ± 1 9 .9 2 0 .2 ± 5 .8 388.5 ± 110.8

187
B 5 1 8 8 .0 ± 1 0 .6 1 9 0 .2 ± 9 .8 2 0 6 .0 ± 1 3 .1 1 7 .6 ± 7 .3 3 3 8 .4 ± 1 4 0 .4
(Rose. 1970). However, outbreaks o f early-season trichostrongylosis in calves were reported
by Nansen et al. (1989) in Denmark. It was hypothesized that the preceding extremely dry
summer followed by a hard (very cold) winter had indirectly retarded the degradation of
dung pats and thereby favoured the overwintering of the larval populations in the dung
reservoirs (Nansen et al., 1989).
In an earlier (1993) experiment where grazing calves were fed fungal material during
the first three months o f the season, a clear effect o f the treatment was demonstrated as larval
populations o f Ostertagia spp. and Cooperia spp. were significantly reduced on the pasture
grazed by fungus-treated calves (Nansen et al . , 1995). In the present study (1994 experiment)
the parasitological parameters (herbage, faecal egg counts) for the two groups of calves and
their respective grazing plots were roughly comparable, indicating that there were no
differences in pasture infectivity between plot B previously grazed by calves fed nematode
trapping D. flagrans and plot A previously grazed by calves not fed nematode-trapping
fungus. This showed that the treatment effect o f D. flagrans was eventually lost later in the
grazing season as tracer calves in plot B had strikingly comparable worm burdens as control
calves in plot A, even though there were apparent individual variations in worm recovery
within the groups. Body weight gains within the two groups o f calves remained relatively
similar throughout the experimental period. It is reasonable to speculate that the number of
overwintering larvae were most likely influenced by the level o f pasture contamination the
previous season and weather conditions during winter rather than the effect of nematode
trapping fungus D. flagrans. The present results demonstrated that the effectiveness of D.
flagrans in destroying parasitic nematodes o f cattle in dung pats was limited only to the early
grazing season. Thus, further studies are indicated to elucidate the effect o f the fungus when
fed for the entire normal grazing season or while administered in controlled release devices.
188
- C h a p t e r 10-
THE INFLUENCE OF EGG COUNTS AND FUNGAL DOSE LEVELS ON THE
NEMATODE-TRAPPING CAPABILITY OF DUDDINGTONIA FLAGRANS
AGAINST FREE-LIVING STAGES OF GASTROINTESTINAL NEMATODES OF
CATTLE
10.1 Introduction
The control of nematodes in cattle and other domestic animals is presently based on
anthelmintic treatments and grazing management. However, the threats o f development of
anthelmintic resistance, concerns about chemical residues in livestock products and possible
ecotoxicity o f excreted drugs causes anxiety (Herd et al., 1993; Strong et al., 1996). This
has stimulated attempts to develop alternative methods for worm control, including biological
control o f free-living stages o f strongylid nematodes of ruminants by using nematode-trapping
microfungi (Grenvold et a l ., 1993a; Waller and Larsen, 1993; Waller and Faedo, 1996).
Recent investigations successfully demontrated that feeding of calves during the first months
of the grazing season with D.flagrans grown on barley grain reduced herbage infectivity and
a reduced acquisition of Ostertagia spp. and Cooperia spp. later in the season (Larsen et al.,
1995a; Nansen et al., 1995).
The nematode-destroying effect of a fungus may both be determined by the capacity
of the nematode larvae to induce traps in the fungus and later to become effectively ensnared
in these. In an earlier in-vitro experiment (Nansen et al., 1988) with a closely related fungus,
A. oligospora, it was shown that trap induction was in all cases dependent on the presence
of living nematodes, and all categories of nematodes, parasitic as well as free-living, were
able to stimulate trap morphogenesis. However, there seems to be a correlation between the
189
locomotive behaviour and the ability to induce traps, e.g. the rapidly moving intestinal
trichostrongylids o f cattle and sheep were potent trap inducers, while the slow-moving D.
viviparus had a poor capability in this respect (Nansen et al., 1988).
One important objective o f the on-going research on nematophagous fungi as an
adjunct to conventional anthelmintic treatment for the control o f parasitic gastroenteritis in
cattle, is to determine the effect o f D. flagrans against the various important nematode
species and to evaluate the impact of different fungal dose levels. The present experiment
was specifically designed to quantify the effects o f varying fungal concentrations of D.
flagrans on free-living stages of H. placei, T. axei, C. oncophora and O. radiatum o f cattle
in faecal cultures and, to define the minimum amounts o f fungal material needed for a
significant reduction o f the number o f larvae o f the individual species. In general,
irrespective o f species o f nematode, it may be anticipated that the extent of trap formation,
and hence nematode-killing potential o f D. flagrans , may be enhanced at higher nematode
larval densities. Therefore, the effect o f increasing doses o f nematode eggs admixed to the
faecal cultures, was examined as well.
10.2 M aterials and methods
10.2.1 Parasite material
Faeces, containing eggs o f H. placei, T. axei, C. oncophora and O. radiatum, were
obtained from calves experimentally infected with monocultures of these parasites. Faeces,
without eggs, were obtained from two uninfected calves. These animals were originally
parasite-free, and were kept in experimental housing facilities (National Veterinary
Laboratory, Copenhagen, Denmark) where parasite transmission was not possible.
190
10.2.2 Fungal material
A D. flagrans (C13) isolate previously selected by Larsen et al. (1991; 1992), was
used. The fungus was cultivated on barley grains as described by Gronvold et al. (1993b).
One-litre Ehrlenmeyer flasks containing 200 g barley grains plus 200 ml tapwater were
autoclaved and subsequently inoculated with agar pieces from a stock culture of D. flagrans
grown on 1:10 diluted corn meal agar (Difco). After incubation for 6 weeks at 24°C the
fungal material was washed off the grains by thorough shaking and mixing with sterile water.
The material was poured successively through a kitchen sieve, a layer o f fine gauze, and
finally a 3fyi nylon net. Fungal material in the suspension contained less than 5% conidia,
the rest were chlamydospores. The concentration o f fungal units in the suspension was
determined by using a haemocytometer and were added at the desired concentration in small
volumes (1ml) o f fluid to standard 10 g faecal cultures. Fungal concentrations used were 0
(controls), 1000, 5000 and 25000 units g 1 faeces.
Faeces were collected from the calves to avoid any contamination with soil
nematodes. After thorough mixing, the number o f parasite eggs gram 1 o f faeces (epg) was
determined by a modified McMaster method (Henriksen and Aagaard, 1976). For each
nematode species other than T. axei, faecal portions with three to four epg levels were made
using nematode free faeces as a diluting medium. These were low (40-50 epg), medium (200-
280 epg), high (600-680 epg) and very high (1288-4800 epg), respectively.
10.2.4 Faecal culture assay
Faecal cultures (10 g faecal material mixed with 4 g vermiculite, plus 8 ml tap water for
191
control, and 7 ml H20 plus 1 ml fungal material for the fungal treated cultures) were set
according to a procedure described by Henriksen and Korsholm (1983). Five replicate
cultures at each fungal concentration were set for each epg level per parasite species and
incubated for 14 days in darkness, and under constant temperature (25°C) and 95% relative
humidity. After incubation, the larvae were harvested using a modified Baermann technique
(Jorgensen and Madsen, 1982), and the number o f third stage larvae (L3) determined. After
14 days incubation only L, larvae harvested were recoverable. At low and medium epg levels
all harvested L3 were counted, while at high and very high epg levels subsamples were
counted under a stereo microscope.
10.2.5 Trapping efficacy and statistical analysis
The trapping efficacy of D. flagrans was expressed as the percentage reduction in
numbers of larvae recovered from fungal treated relative to numbers in fungal free cultures
and was calculated thus: [(N in controls- N in fungal treated cultures)/N in controls] x 100,
where N represents the mean number of infective larvae in fungus free and fungus treated
replicates, respectively. The data for L3recoveries did not meet assumptions of normality and
equality of treatment variance necessary for valid statistical analysis, using parametric
methods. Consequently, the one-tailed Mann-Whitney U test (Siegel, 1956) (non parametric
analogue of the unpaired t-test) was used to test the differences between median larval counts
between the fungal treated and fungal free cultures (ultimately reported in terms of
percentage efficacy).
192
10.3 R e s u lts
The influence o f the inoculation level o f D. flagrans on the number o f infective
nematode L, recovered from faecal cultures per epg level is shown in Tables 10.1 to 10.4b.
In the control cultures, recovery o f LjOf H. placei and 0 . radiatum (batch A and B) was
significantly (P < 0 .0 5 ) higher at low epg level compared to the high and very high epg levels
and, overall yield o f L3 ranged from 16.7% (C. oncophora, batch A) to 95.5% ( O. radiatum,
batch A). Recovery o f L3 o f all four nematodes decreased significantly (P < 0 .0 5 ) at each epg
level with increasing fungal spore concentration. At each level o f fungal spore concentration,
percent recovery of larvae decreased significantly (P < 0 .0 5 ) for each increase in epg level.
As shown in Table 10.3a, there were no significant differences (P > 0 .0 5 ) in percent larval
recovery between the high and very high epg levels at 1000, 5000 and 25000 fungal spore
concentrations. At the 1000 and 5000 fungal spore concentrations, the range o f percent
reduction of larvae at the medium epg level for the 4 species was 53.5% for O. radiatum,
78.8% for C. oncophora, 80.4% for T. axei and 83.8% for H. placei.
The percent yields o f larvae from faecal cultures of the 4 species are presented in
Figs. 10.1 to 10.4b. In the control cultures o f H. placei and O. radiatum (batch B), percent
yields decreased with each increase in epg level. However, there was much variability in
percent yields for other species, especially C. oncophora (Figs. 10.3a and 10.3b). For the
fungus inoculated cultures in all species, there were definite reductions o f percent yield ot
larvae for each fungal spore concentration and at each epg level. At low and medium epg
levels, average percent reductions for all nematode species at 1000 and 5000 fungal spore
concentrations were 52.2% and 71.9%, respectively. At high epg levels, percent yields were
significantly (P < 0 .0 5 ) reduced for H. placei, C. oncophora and O. radiatum. However,
percent reductions were generally lower for O. radiatum compared to the other 2 species.
TJNJV.' « •- /■»* NAIROBI?

193
T a b le 1 0 .1 : M e a n n u m b e r o f in fe c tiv e H. p la cei la rv a e (L ,) re c o v e r e d f ro m lO g o f c a ttle f a e c e s m ix e d w ith 1 0 0 0 ,
5000 and 25000 D. flagrans chlamydospores per gram of faeces
Mean ± S.D larval counts (% reduction)

*Epg levels 0 (Controls) ‘ ‘ 1000 5000 25000
50 a376.6 ± 17.2 •*219.6 ± 16.0 (41.7) b166.4 ± 15.4 (55.8) b75.4 ± 12.7 (79.9)
200 a594.8 ± 23.0 b136.2 ± 13.6 (77.1) b56.4 ± 8.7 (90.5) b28.6 ± 4.2 (95.2)
680 a1300.4 ± 130.2 b147.8 ± 21.3 ( 88. 6) b62.0 ± 6.2 (95.2) b23.0 ± 4.7 (98.2)
‘Faecal egg counts g "1 faeces. **Clamydospore units g '1 faeces. Larval counts in the same row differ significantly (P < 0 .0 5 ).
194
Table 10.2: Mean number of infective T. axei larvae (Lj) recovered from lOg of cattle faeces mixed with 1000,
5000 and 25000 D. flagrans chlamydospores per gram o f faeces
■ ............- ■ —

‘Epg levels 0 (Controls) “ 1000 5000 25000
50 a162.0 ± 8.8 b76.6 ± 14.1 (52.7) b47.2 ± 14.0 (70.8) b29.2 ± 7.8 (81.9)
236 al 189.4 ± 20.0 b3 5 1.0 ± 147.0 (70.5) b114.2 ± 26.3 (90.4) b6 1 .6 ± 16.3 (94.8)
‘Faecal egg counts g'1 faeces. Clamydospore units g '1 faeces. Larval counts in the same row differ significantly (P < 0 .0 5 ).
Table 10.3a: Mean number o f infective C. oncophora larvae (L,) recovered from lOg o f cattle faeces mixed with 1000,
5000 and 25000 D. flagrans chlamydospores per gram of faeces (Batch A)

*Epg levels 0 (Controls) ” 1000 5000 25000
40 a66.6 ± 25.8 b26.8 ± 1 1 . 9 (59.8) b17.2 ± 6.2 (74.2) b10.2 ± 6.9 (84.7)
280 a468.0 ± 92.3 b155.8 ± 47.5 (66.7) b35.2 ± 12.9 (92.5) b22.0 ± 5.5 (95.2)
1640 “3525.0 ± 653.5 b234.8 ± 64.3 (93.3) b43.8 ± 22.2 (95.2) b9.8 ± 5.3 (99.9)
4800 “7967.2 ± 908.2 b376.0 ± 116.5 (95.3) b60.6 ± 45.8 (99.2) b7.2 ± 1.3 (99.9)
195
’Faecal egg counts g '1 faeces. Clamydospore units g '1 faeces. Larval counts in the same row differ significantly (p < 0 .0 5 ).
Table 10.3b: Mean number o f infective C. oncophora larvae (L 3) recovered from lOg o f cattle faeces mixed with 1000,
5000 and 25000 D. flagrans chlamydospores per gram of faeces (Batch B)

*Epg levels 0 (controls) ” 1000 5000 25000
40 “109.2 ± 6.7 b53.2 ± 6.3 (51.3) b33.2 ± 4.5 (69.6) b16.8 ± 2.8 (84.6)
240 “940.0 ± 44.6 b324.4 ± 1 1 . 5 (65.5) b91.0 ± 6.6 (90.3) b59.0 ± 3.8 (95.2)
620 “2805.6 ± 1 2 6 .6 b240.4 ± 7.8 (91.4) bl 12.0 ± 6.3 (96.0) b3 1.2 ± 3 . (98.9)
’Faecal egg counts g '1 faeces. Clamydospore units g '1 faeces. Larval counts in the same row differ significantly (p < 0 .0 5 ).
T a b le 1 0 .4 a : M e a n n u m b e r o f in fe c tiv e O. radiatum la rv a e (L 3) r e c o v e r e d f r o m lO g o f c a ttle f a e c e s m ix e d w ith 1 0 0 0 ,
5000 and 25000 D. flagrans chlamydospores per gram o f faeces (Batch A)

‘Epg levels 0 (Controls) ‘*1000 5000 25000
50 a477.4 ± 3 3 .1 b351.4 ± 35.8 (26.4) b244.6 ± 48.4 (48.8) b199.6 ± 6.3 (58.2)
250 *1125.0 ± 162.2 b689.0 ± 29.6 (38.7) b476.2 ± 80.1 (57.7) b390.6 ± 70.9 (65.3)
644 “3820.0 ± 74.2 b1916.6 ± 56.4 (49.8) b1304.8 ± 68.4 (65.9) b881.0 ± 104.7 (76.9)
1288 *4510.0 ± 353.7 b1752.6 ± 43.9 (61.1) b978.4 ± 46.1 (78.3) b317.4 ± 46.6 (92.9)
‘Faecal egg counts g '1 faeces. Clamydospore units g '1 faeces. Larval counts in the same row differ significantly (p < 0 .0 5 ).
Table 10.4b: Mean number o f infective O. radiatum larvae (Lj) recovered from lOg o f cattle faeces mixed with 1000,
5000 and 25000 D. flagrans chlamydospores per gram o f faeces (Batch B)
Mean ± S .D larval counts (% reduction)

*Epg levels 0 (Controls) “ 1000 5000 25000
40 *190.0 ± 11.2 b136.2 ± 12.7 (28.3) b93.2 ± 8.2 (50.9) b61.6 ± 5.1 (67.6)
230 *656.6 ± 29.3 b341.8 ± 12.9 (47.9) b199.2 ± 10.8 (69.7) b30.6 ± 4.4 (86.1)
600 *1270.8 ± 121.3 b349.0 ± 6.4 (72.5) b13.2 ± 4.5 (89.4) b53.8 ± 3.7 (95.8)
‘Faecal egg counts g '1 faeces. Clamydospore units g '1 faeces. Larval counts in the same row differ significantly (p < 0 .0 5 ).
Y ie ld (% o f EPG)
ro -P* O) oo
o o o o o
Control
Fungal units/g of faeces (EPG)
1,000
5,000
25,000
F ig . 1 0 .1 : E ffe c ts o f D. fla g ra n s on the re c o v e ry

o f IN. placei in fe c tiv e la rva e
197
Y ie ld (% o f EPG)
Control
1,000
5,000
25,000
□ 50
EPG
F ig . 1 0 .2 : E ffe c ts o f D. fla q ra n s on th e re c o v e ry
o f T_. axei in fe c tiv e larva e
198
Y ie ld (% o f EPG)
—*■ f\3 G) Ol
O O O O O O
Control
1,000
5,000
25,000
-.3 a : " ■arvC

aeV^ ya ,c h A,
199
Y ie ld (% o f EPG)
Control
1,000
5,000
25,000
F ig . 1 0 .3 b : E ffe c ts o f D^. fla g ra n s on the re c o v e ry

o f C. o n c h o p h o ra in fe c tiv e la rv a e (b a tc h B)
200
Y ie ld (% o f EPG)
ro 03 -t* cn
o o o o o o
F ig . 1 0 .4 a : E ffe c ts o f D_. fla g r a n s on th e re c o v e ry

o f 0 . ra d ia tu m in fe c tiv e la rv a e (b a tc h A )
201
Y ie ld (% o f EPG)
IO -P* O) CD o
o o o o o o
Control
1,000
5,000
25,000
It
□ 50
I D 0
EPG
-*• O) N>
ro cn
CD O
CD
F ig . 1 0 .4 b : E ffe c ts o f fla q r a n s on th e r e c o v e r y
o f 0 . ra d ia tu m in fe c tiv e la rv a e (b a tc h B )
202
10.4 D is c u s s io n
There was appreciable variability in the recovery of L3 as depicted by the control
cultures o f most species. Recovery o f L3decreased with each increase of epg level for H.
placei and O. radiatum (batch B), while no consistency was detected in die cultures o f other
species. The recorded variability may be attributed to biotic and/or abiotic factors in cultural
medium or other uncontrolled sources of experimental error. The present results have shown
that chlamydospores o f the predacious fungus D. flagrans, when added to cattle faeces,
resulted in a significant reduction o f Lj of H. placei , T. axei, C. oticophora and O. radiatum.
Moreover, the trapping effect in faecal cultures was shown to depend on the fungal
concentration and the number of eggs gram 1 o f faeces (epg levels). Several studies to
quantify the efficiency o f different concentrations o f conidia on nematode-destroying capacity
have been conducted (Gronvold, et al. 1985; Bird and Herd, 1995). Gronvold et al. (1985),
who worked with A. oligospora on cattle nematode C. oncophora, found that larval numbers
in faecal culture were not significantly reduced until approximately 250 conidia g '1 faeces
were used and ten times that number were required to reduce larval numbers by more than
99%. Subsequent field studies by the same research workers (Gronvold, et al. 1988) showed
that a concentration of 2000 A. oligospora conidia g 1 faeces resulted in a significant lowering
of herbage larval infectivity during the grazing season. Other, as yet unpublished
observations referred to by Hashmi and Connan (1989), indicated that substantial reductions
in larval numbers can result from the addition o f 20-50 A. oligospora conidia g ] to either
cattle or sheep faeces. The present studies show that the 1000 and 5000 fungal spore
concentrations (at all epg levels) gave significant reduction (73%) o f the number o f parasite
larvae in the faecal cultures. Further experiments using different chlamydospore densities per
egg to determine the minimal number of fungal units to obtain the desired reduction (i.e 75-
203
80 %) in the larval population is warranted.
The efficacy o f nematode capture by D. flagrans was dependent on the faecal egg
count and thus the number o f larvae obtained from cultures, as percent yield of L, decreased
with each increase o f epg level. This was as reported for A. oligospora that increasing
numbers of nematode-trapping hyphal nets were produced with increasing numbers o f 0.
ostertagi larvae (Gronvold, 1989). In the present study, no significant species variation in
entrapment was detected at the various fungal and/or epg levels, respectively, as all species
were readily entrapped as earlier reported by Nansen et al. (1988) and Waller and Faedo
(1993). The design of the experiment allowed exposure o f all the three free-living stages (L,,
Lj and Lj) to D. flagrans , but it was not possible to determine whether a certain stage
experienced a greater predation. Under natural conditions, 2 or more nematode species co
exist in a host and it seems they can be destroyed readily by the fungus in the dung pats as
predacious fungi trap and digest nematodes to a large extent independently of their species
or genus position (Drechsler, 1941). The investigated strain o f D. flagrans forms capturing
traps in response to soil organisms, especially nematodes, in their environment. It may
therefore be expected that not only the parasitic nematode larvae already present, but also
soil nematodes invading the dung pats, may be responsible for the induction o f capturing
traps and thereby enhance the entrapment o f parasitic nematodes. It may also be anticipated
that free-living nematodes in the dung have an indirect influence on eventual fungal predation
on animal parasitic nematodes in the dung, e.g . through their role as baits and disseminators
of fungi (Linford, 1937).
As illustrated by C. oncophora, percent larval recoveries from 1000 to 25000 fungal
concentrations were not significantly different between the high and very high epg levels.
This indicates that the epg threshold which is needed for a significant reduction o f L3 in
204
faecal cultures would be much lower. Indeed, at the medium epg level, the range o f percent
reduction o f L3 at 5000 fungal spore concentration was >60% for all the 4 nematode
species. Under normal circumstances, worm egg counts in naturally infected cattle are on
average < 3 0 0 as the medium epg levels used in the present study. Thus, as entrapment of
>60% was noted, the fungi can be o f value in the field if given orally to cattle and entrap
the free-living stages in dung pats, with subsequent reduction o f pasture infectivity and
economic losses attributable to G1 nematode parasitism. In Australia, worm control in sheep
was improved over the standard (wormkill) program for fungal controlled-release devices
with efficacy o f at least 75% and duration o f at least 60 days (Barnes et al., 1995).
In the present study, percent yield at low epg level and at 1000 and 5000
chlamydospores g '1 faeces was markedly higher than at higher and very high epg levels.
Working with cyathostomes o f horses. Bird and Herd (1995) argued that there appeared to
be a threshold below which the number of spores per egg failed to effect sufficient mortality
as low mean egg counts may fail to produce enough larvae to effectively induce traps, thus
explaining the marked difference in percent yield between low and high epg levels for the
nematode species examined. Further experiments should be undertaken to determine the
minimum number o f larvae required to induce trap formation and subsequent capture of
parasitic nematodes in faecal cultures.
205
-Chapter 11-
GENERAL DISCUSSION
The main objective o f this thesis was to determine the seasonal prevalence, intensity
and importance o f GI nematodes in dairy cattle in Kiambu District, central Kenya. Other
objectives were to evaluate the efficacy o f a sustained release anthelmintic bolus in
controlling GI nematode parasitism in naturally infected grazing yearlings, and to quantify
the nematode-trapping effects of the fungus D. flagrans on free-living larval stages o f the
four main GI nematodes o f cattle in the tropics.
In an effort to achieve the above objectives, a number o f studies ( 8) were conducted
as summarized herebelow:
Results in chapters 3, 5, and 6 demonstrate a generally high prevalence o f GI
nematode infections o f cattle in the study area, even outside the two rainy seasons. However,
the degree o f infection or the level o f helminth-egg load was generally low to moderate in
most cases; the infections therefore being subclinical (Soulsby, 1965). Subclinical or
economic parasitism is the level of infection that prevents the host from reaching its genetic
potential in the production of meat, milk or other measureable criteria (Craig, 1988).
Economic parasitism is widespread, seasonal and often affected by other factors including
quality and abundance o f feed, stocking rate, age, sex, breed or acquired resistance.
Compared to clinical parasitism, economic parasitism is the most difficult to assess because
of the many factors that may be involved. One common way of assessing economic
parasitism is by administration of an anthelmintic to cattle and then, after a predetermined
period of time, comparing weight gains between treated and untreated animals (see Chapter
8). This is a valid method o f determining anthelmintic effects, but it may not always assess
206
the true effects o f parasitism (Craig, 1988).
A survey o f gastrointestinal parasites (GIP) o f cattle (Chapter 3) showed that
strongylosis (due mainly to H. p la c ei ) was the most prevalent GIP, followed by liver fluke,
coccidial and tapeworm infections. The seasonal, management system, and age o f the animals
influenced occurence and intensity o f infection. A higher intensity of strongylid eggs was
found in the wet season compared to the dry season (P < 0 .0 5 ). The age-specific intensity was
in the following order: yearlings had the highest egg counts, followed by calves and adult
cattle.
The strongylid egg counts followed the negative binomial pattern of distribution at
each sampling, which suggests highly overdispersed worm burdens. Thus, by eliminating
"wormy" individuals o f the herd (i.e by selective anthelmintic treatment), effective control
of parasite transmission can be achieved (Sreter et al., 1994).
An outbreak o f haemonchosis caused by H. placei which occurred in weaner calves
in late June 1992 is reported in Chapter 4. Post mortem examination of an animal which died
during the outbreak confirmed H. placei as the primary pathogen. The number o f other
nematode species found was very small.
Seven nematode genera were found during an abattoir survey (Chapter 5 ), with the
predominant genus being Haemonchus while the genus Strongyloides was the least
predominant. Other genera present were Cooperia, Trichostrongylus, Oesophagostomum,
Nematodirus and Trichuris in that order o f prevalence.
As reported by Gatongi (1984), all the genera found during this study appeared to be
equally influenced by prevailing weather conditions (Chapter 6) and there was no indication
that a particular genus was more favoured or more adversely affected by a particular season
than others.
207
It is important to note that the digestion o f the abomasal mucosae o f slaughtered cattle
did not reveal any significant numbers o f immature (histotropic) H. placei worms in the
digesta. Hypobiosis is now widely recognized as a form of adaptation, whereby the parasite
arrests at a particular stage in the host when environmental conditions are adverse for its
free-living development, for example, in winter in Europe or in the dry season in parts of
Africa (Benitez-Usher et al., 1984; Gatongi, 1995). Benitez-Usher et al. (1984) emphasized
that in areas with weather conditions favourable for development of stages, the faculty of
hypobiosis was discarded by the parasites (Gupta et al., 1987). Accordingly, it is significant
that H. placei encountered in the present study showed no hypobiosis.
In Chapter 7, observations were made on the abundance and survival o f H. placei,
Cooperia spp., T. axei and 0. radiatum infective larvae fron cattle faecal pats exposed at
various times of the year (July 1995 to June 1996) in the study area. Rainfall rather than
temperature played the major role in the development and survival of the larvae on pasture
during the study period. These results show that the hatching o f the eggs and the
development o f the larvae can take place at any time of the year, and suggest that similar
results would be obtained in other tropical regions provided the rainfall throughout the year
was sufficient to allow development o f eggs to infective larvae (L3). Similar observations
were made elsewhere under tropical conditions (Okon and Akinpelu, 1982; Fabiyi et al.,
1988; Banks et al., 1990; Barger et al., 1994). It can be deduced that L, would be expected
to have died off on pasture after 12 to 16 weeks of resting the pasture. Thus, it is suggested
that safe pasture can be produced by spelling contaminated pasture for a minimum of 3
months (Ndamukong and Ngone, 1996).
Results presented in Chapter 8 demontrated that subclinical infection by GI nematodes
has adverse effects on weight gains in calves. MSRT bolus administered to weaner calves
208
?rior to their turnout onto pasture produced adequate control of nematode infection dominated
oy H. placei. Benefit o f the bolus was reflected in the improvement o f liveweight gain and
a reduction o f infectivity o f herbage with larvae, faecal egg counts, post mortem worm
counts o f tracer calves that grazed on the pasture where treated animals were maintained, and
post mortem worm counts o f principal (treated) calves slaughtered at termination o f the trial.
In this experiment, average liveweight gain benefit was 69.2 kg per animal over the
experimental period. This is the most important parameter in production efficiency (Block
et al., 1985). The weight gain is achieved with a single treatment without a concomitant
increase in the amount o f herbage available or the size o f the grazing area. The MSRT bolus
also has an advantage over conventional helminth-prophylactic programmes in areas where
land and/or labour are scarce or expensive, which either involves treatment of calves and a
subsequent move to a safe pasture or strategic anthelmintic treatment. Both systems require
extra labour, land, and money (Jones and Bliss, 1983).
Albendazole, one o f the more recently developed benzimidazole anthelmintics was
used as a single drench in group T-3 calves and as two dosings, 14 days apart for group T-4
calves. Faecal egg counts were significantly reduced in both groups T-3 and T-4, 2 weeks
after single treatment (Fig. 8.2) and the gradual increase in egg counts recorded in group T-3
may be attributed to reinfection. With the second treatment (group T-4) faecal egg output was
significantly reduced up to July. This prolonged effect of two treatments with albendazole
indicates that the deposition o f eggs in the early rainy season is very important for buildup
of pasture infectivity. Treatment during this period must be regarded as strategic as they
resulted in a relatively reduced buildup o f pasture contamination followed by a favorable
production response (weight gains). Not until the next rainy season (short rains) did the epg
counts reach the levels o f the other groups (i.e. T -l and T-3).
209
This study offers good indications for the use o f few effective strategic treatments in
the control o f cattle nematode infections. However, this benefit can be enhanced under
practical field conditions when anthelmintic treatment is combined with grazing management,
like placing animals on relatively clean pastures (Block et al., 1985). This unfortunately is
difficult to practice in Kenya, particularly in areas where animals graze on communal land.
However, other approaches like zero grazing in certain periods of the year may be
considered as adjunct control strategies (Nansen, 1991). The anthelmintic activity o f plants
like papaya latex (Carica papaya Linn) against gastrointestinal nematodes o f cattle should be
investigated as it has been found to be effective against intestinal nematodes of monogastric
animals (Satrija et al., 1994) and against H. contortus in sheep (Murdiati and Beriajaya,
1997).
An attempt was made in Chaper 9 to determine the overwintering residual grass
infectivity in a pasture previously grazed by D. flagrans fed calves using tracer calves over
a period o f 7 weeks. Parasitological parameters were generally comparable indicating that
there were no differences in pasture infectivity between the plot (B) previously grazed by
calves fed the fungus D. flagrans and the plot (A) previously grazed by calves not fed the
microfungus. Body weight gains within the two groups of calves remained relatively similar
throughout the experimental period and on slaughter, tracer calves in plot B had comparable
worm burdens as control calves in plot A.
The effects of different fungal concentrations and faecal epg levels on nematode-
trapping ability o f D. flagrans against the four predominant genera of cattle nematodes in the
tropics are discussed in Chapter 10. Results show that the nematode-trapping capacity of D.
flagrans was dependent on the fungal concentration and number of eggs in the faecal
cultures. Thus, percent reduction increased with corresponding increase in fungal
concentration and epg levels in all the four genera o f nematodes examined.
210
11.1 C o n clu sio n s
The following observations and conclusions were made from this study:
a) That GI nematode infections are major constraints to the health o f young dairy cattle
of the study area.
b) Moisture, which is influenced by rainfall, was the major epidemiological factor
affecting the development and survival of the strongylid nematode larvae, and
the prevalence and intensity o f infection with nematode parasites.
c) Hypobiosis does not seem to play any important role in the epidemiology o f H. placei
as adult worms persisted in the host throughout the year and there was no indication
o f inhibition o f EL4.
d) That control o f established subclinical nematode infections is indicated, this can
be accomplished using sustained release boluses where economically justifiable.
e) That strategic application of conventional (drenches) anthelmintics could be o f value
in the farming systems studied. Three strategic treatments of young cattle may be
attempted before (mid-March) and after (July) the long rains, and before the short
rains (mid-October).
f) That the trapping efficiency o f D. flagrans against H. placei , T. axei, C. oncophora
and O. radiatum increased with the corresponding increase in fungal concentration
and epg levels.
211
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Zarlenga, D .S ., Stringfellow, F ., Nobery, M. and Lichtenfels, J.R. (1994). Cloning and
characterization o f ribosomal RNA genes from three species o f Haemonchus
(Nematode: Trichostrongloidea) and identification o f PCR primers for rapid
differentiation. Exp. Parasitol., 78: 28-36.
Zimmerman, G.L. and Hoberg, E.P. (1988). Controlled release devices for the delivery of
Anthelmintics in cattle. Parasitol. Today, 4: 55-56.
281
APPENDICES
Appendix 3.1 The recovery and identification of gastrointestinal
nematodes post mortem
3.1.1 Recovery o f nematodes from the abomasum
: Immediately after removing the alimentary tract from the body cavity, the abomasum
was ligated twice just below the pylorus and at the omasal-abomasal junction. It was
separated from the small intestine and omasum by cutting the portion between the two
ligatures by means of a knife. This was done immediately after slaughter.
: The abomasum was placed in a bucket and opened along the greater curvature and the
contents washed out.
: The abomasum was rinsed 3-5 times with water with special attention being paid
between folds and mucous membranes.
The abomasum was put in a small plastic bag with proper identification number until
processing in the laboratory.
• The contents o f the abomasum were adjusted to 10 litres by tapwater.
Using a ladle the contents were carefully mixed until all food materials, mucus and
water were thoroughly mixed.
: Quickly a subsample of 1 litre (10%) was recovered.
The subsample was processed through a 200 /xm sieve which retains adult nematode
parasites.
The residue on the sieve was rinsed with a jet o f tap water and the volume made up
to 200 ml and put in a plastic container.
282
10-15 ml o f concentrated Lugol’s iodine solution was added into the contents to
preserve retained parasites until identification and enumeration.
The sample was adjusted to 300ml and was constantly stirred by the use o f a magnetic
stirrer.
30 ml (10% o f the total volume) o f the sample was poured into one or more small
petri dishes with ruled bottom. Using a stereo microscope at X 12-16 magnification,
all the worms in the sub-sample were counted. Further sub-samples were taken until
10% o f the total volume was examined.
Mature males and females were picked and put into small plastic cup with glycerol
ethanol.
Mature male worms were identified to species level if possible, using light
microscope at a magnification o f 40-400 according to MAFF (1986).
1.2 Processing of the abomasal mucosa by pepsin/HCl digestion
The entire abomasal mucosa was removed by scraping with a knife.
For every 100 g o f mucosa a preheated (37°C) 500 ml o f digestion fluid was added
into a plastic bag, and blended in the stomacher at 39°C for 30 minutes.
The larvae were being isolated from the fluid by straining them through a 37 p.m
sieve.
All the materials on top o f the sieve were transferred by rinsing with tap water into
a beaker; the total volume was made up to 30 ml.
The larvae were stained using 2-3 ml of iodine solution; and then counted in a petri
dish under a stereo microscope 30-40 X magnification.
283
3.1.2.1 Chemicals and equipm ent
A: D igestive fluid
Water 1,000 ml
HC1, I N (86 ml cone. HC1 + 914 ml water) 150 ml
Pepsin (1: 3,000) 8 g
(The solution was stable for one day when kept at 37°C ).
B: Stomacher 3,500 (thermo model)
C: Strainer 37 /im aperture
D: Iodine solution
Potassium iodide (KI) 250 g
Iodine crystals 50 g
Water 500 ml
3.1.3 Recovery o f nematodes from the small intestines
: The small intestine was ligated below the pyloric pore and between small and large
intestine, and removed from the gastrointestinal tract.
: The small intestine was freed from the mesentery by use of a pair o f scissors or by
stripping and divided into 3 equal parts which were processed separately.
: Each part was transferred into a plastic tray, then opened along the entire length and
washed carefully.
: The contents were adjusted to 10 litres by tap water, and a sub-sample o f 1 litre was
washed through 53 /xm sieve to retain adult parasites as well as larval stages.
: O nly the first 3 metres o f the front part was digested following the ordinary digestion
procedure as described for the abomasal mucosa.
The procedure for staining and counting was the same as previous described for
w orm s o f the abomasum.
284
3.1.4 Recovery of nematodes from the large intestine
: The colon was ligated twice at the point where it joins the caecum.
: It was separated from the caecum by cutting with a pair of scissors inbetween the
two ligatures.
: The two organs were processed separately.
: For both of them, the contents were washed into a bucket and adjusted to10 litres by
tap water.
: A sub-sample o f 1 litre was passed through a coarse mesh sieve (500 pm) and any
worms retained were picked and put into small plastic bottles with glycerol ethanol
until use.
: Mature male worms were identified to species level if possible using a light
microscope at a magnification o f 40-400 according to MAFF (1986).
Reference : MAFF (1986).
Appendix 6.1 The serum pepsinogen test
6.1.1 Principle
The principle o f the test is that the sample of serum is acidified to pH 2.0, thus
activating the inactive zymogen, pepsinogen, to the active proteolytic enzyme pepsin. The
activated pepsin is then allowed to react with the protein substrate (serum albumine) and the
enzyme concentration is calculated in international units (I.U: p mols tyrosine released 1000
ml serum m inute1 at 37°C). The tyrosine (a phenolic compound) liberated from the protein
substrate by the pepsin is estimated by the blue colour which is formed when it react with
285
F o lin -C io c a lte u ’s r e a g e n t.
6.1.2 Procedure
: To 0.25 ml o f serum were added 1.25 ml o f 0 .6 N hydrochloric acid and mixed well.
: The mixture was incubated at 3 7 °C for 3 hrs.
: The reaction was then stopped by adding 1 ml of 10%trichloroacetic acid.
: A parallel control was prepared for each test by precipitating the mixture as above
without incubation.
: The tubes were allowed to stand for 10 min and, then centrifuged (at 2,000 r.p.m.)
for 10 min.
: The tubes were allowed to stand for another 10 min.
: The supernatant (1ml) was placed in a clean test tube and made alkaline with 2 ml of
0.5 N sodium hydroxide and 0.5 ml o f freshly diluted (1 in 3) Folin and Ciocalteu s
reagent was added and mixed well.
: Colours o f test and control were read within 20 min. at 560 ml and tyrosine-like
products estimated by reference to standard tyrosine (0.2 u mole) and blank (water)
treated similarly.
Reference : Ross et al. (1967).
Appendix 9.1 Technique for recovery of gastrointestinal nematode larvae
from herbage
286
9.1.1 Procedure fo r collecting herbage samples
: Three small samples of grass per plot/paddock were collected following a "W" shaped
route. The sampler walked along the route and after every ten steps he/she stopped
and a small wisp o f grass was picked to the right, to the left and in front o f the picker
and put into a plastic bag.
: Areas o f heavy faecal contamination and soil collection were avoided.
: The grass was collected by hand and sampling was undertaken at the same time o f the
day (9-10 am) in order to avoid diurnal variations in pasture infectivity.
: The grass collection o f approximately 300-600 g was placed in a plastic bag.
: In the laboratory, the collected samples were weighed to get the wet weight.
9.1.2 Isolation o f debris and larvae form herbage
: The sample was then soaked overnight in a bucket containing 10 litres o f tap water.
: The sample was placed in a concrete mixer machine and 2 drops o f teepol (0.02%
teepol) was added to loosen the larvae from grass blades.
: The water with the herbage was agitated for 5 minutes to further loosen the larvae.
: Subsequently the washings were filtered through a 70 x 70 cm piece o f nylon mesh
(25-30 mm apertures) cloth placed in the conical support. The nylon mesh cloth was
used to retain debris and larvae.
: The herbage was caught in a metal grid above the cloth, it was removed, squeezed
and put in a cheese cloth bag and dried so as to get the dry weight.
: Support for the nylon mesh cloth was a 40 cm ring-stand fitted with a conical shaped
30 cm deep bag made o f plastic fly screen material.
: Occasionally, the flow rate through the nylon mesh was increased by clearing the
287
mesh with a water jet. The debris collected on the mesh was washed down the sides
and concentrated at the bottom.
A 16 cm diameter filter o f the nylon mesh was inserted between the cylindrical part
and the funnel o f the sieving cylinder. The mesh with the debris was then everted and
the debris washed off into the sieving cylinder.
The water was allowed to drain; when necessary sanction pump was attached to the
stem o f the funnel.
The filter with debris and larvae was removed and the debris rinsed with water into
a beaker where the total volume o f the sample was made up to 60 ml.
1.3 Isolation o f larvae from debris
The mixture o f debris and larvae in water was heated to 39 °C in an incubator.
For each sample to be processed, 60 ml o f warm debris, 3% agar without bile at a
temperature o f 38°C were mixed and kept at 38-40°C in a water bath until used.
A 20 x 35 cm piece o f gauze or non-woven lysine (J. Cloth, Johnson and Johnson,
Slough, Great Britain) was fixed in the tray by a fine mist o f water.
Equal volumes o f agar and debris at 38°C were poured into the tray containing the
cloth to form a layer o f even thickness.
15 to 30 min later the gauze with the solid agar slab was lifted out o f the tray, kept
in a vertical position and wound into a roll.
The agar roll was placed in a glass column containing water at 38°C . The roll was
kept in position by means of a small wooden rod (swab stick) and a clothes-peg. The
tray was rinsed and the rinsing fluid poured into the column.
Following incubation at 38°C for 18-20hrs, approximately, 10 ml o f fluid were drawn
288
off into a conical centrifuge tube and centrifuged at 2000 r.p.m. for 2 minutes.
: The supernatant was siphoned o ff leaving approximately 0.2 ml o f water containing
the final sediment.
9 .1 .4 Staining and microscopic examination
: One drop o f iodine solution was added to the sediment in the centrifuge tube.
: After a minimum o f one hour the sediment was transferred to a glass slide and a drop
of thiosulphate solution was mixed with it. The parasitic larvae will retain the brown
colour much longer than the soil nematodes due to the double cuticle they have which
is not in soil nematodes. This facilitates the identification and counting o f L, under
the microscope.
: This preparation was examined after a few minutes under a cover glass at a low
power magnification.
: The larvae were identified using keys found in a standard laboratory manual (MAFF,
1986).
The counting was recorded and expressed as number o f L3 kg'1 dried herbage 1=
count X 1,000/weight o f dry herbage (in grammes)].
Reference: Jorgensen (1975); Mwegoha and Jorgensen (1977); MAFF (1986).
Appendix 9.2 Modified McMaster technique
9-2.1 Procedure
289
4 g o f faeces were weighed out in plastic cup with accuracy o f 0.1 g.
Tap water was added in a proportion of 1.0 g faecal: 14.0 ml o f water.
The contents were stirred up with a wooden spatula, and left for about 30 min. The
stirring was repeated after 30 min. to breakup the faeces.
The suspension was poured through a piece o f gauze (cheese cloth) placed over
another plastic cup, and immediately, 10 ml was transferred into a labelled centrifuge
tube.
The tubes were centrifuged for 7 min, at 1200 rpm (X g).
The supernatant was sucked off by a water suction pump and flotation medium (sugar
and salt solution) was added to the sediment up 4 .0 ml.
The sample was stirred by pasture pipette or by a test tube shaker and while stirring
a subsample was taken and one chamber was filled.
The remaining sample was mixed well again and a second subsample taken and put
into the second counting chamber.
The counting chamber was allowed to stand for 5 minutes so that the eggs get enough
time to float.
The two subsamples in the two chambers were examined under a light microscope at
4 X 10 or 10 X 10 magnification.
All nematode eggs were counted within the engraved area o f both chambers.
Egg counts o f the two chambers were added together and multiplied by 20 to get eggs
per g o f faeces (epg).
290
9.2.2 Flotation fluid fo r the Method
Salt/sugar solution
Sodium chloride (Kitchen salt) 400 g

Water 1000 ml
Sugar 500 g
Specific gravity 1.280
Dissolve the salt in water (saturated solution). Add the sugar to the saturated salt solution.
Stir until the sugar is dissolved.
Reference : Henriksen and Aagard (1976).
Appendix 9.3 Techniques for faecal culture
9.3.1 Procedure
• Faeces, 10 g were mixed with demineralized water (8 mis) until a suitable soft
consistency was attained.
: Vermiculite, 4 g, was added to the faeces suspension and thorough stirred until an
ideal moist/porous consistency was attained.
The culture was transferred to vessel B (Fig. 11), which was thereafter covered by
the double layer of gauze (c). To fix the gauze, and complete the culture chamber (L)
the ring A was pressed down in reversed position until the cut lines o f A and B are
level.
: The culture chamber (L) was incubated in the moist box fastened in apposition 1-2
cm above the filter paper as indicated in Fig. 11.
: After incubation for 14 days at room temperature, the culture chamber was
transferred for baermanisation to the conical glass vessel (H), which was filled with
291
tap water (20-25 °C). The holder (J) ensures the correct position o f the chamber and
further move makes room for a pipette (K) to be passed besides the chamber to the
bottom of the vessel.
The aggregate was left for 24 hrs. at room temperature, during which period the
larvae will have migrated through the meshes of the gauze and settled at the bottom
of the glass vessel. For collecting the larvae, 0 .2 -0 .4 ml of the deposit was pipetted
off and put into a test tube.
2-3 drops o f iodine solution was added to the deposit in the test tube.
After a minimum o f one hour the deposit was transferred to a glass slide and a drop
of thiosulphate solution was mixed with it. Parasitic larvae retained the brown colour
due to double cuticle they have. This facilitates the identification and counting o f L3
under the microscope.
The deposit was examined under 10 X 10 magnification.
Steps 8 and 9 were repeated until 100 larvae were identified. The counts for each
species provided an estimate o f the composition (%) o f the parasite population in the
host.
■3.2 Equipment
Culture chamber was made from a disposable polystyrene cup. The cup was divided
into two parts o f equal height (A and B) by horizontal cut (See Fig. 28). Four to five
perforations having been made in the bottom o f the lower part (B) by means of an 18
G needle. Circular gauze (C), 10 cm in diameter.
Moisture box with cover, made from an ordinary plastic box o f suitable volume (D).
A sheet o f filter paper soaked in water (E) was spread on the bottom, and a plate (F)
292
with circular holes fitting the culture chamber or, alternatively, rings (G) made from the
middle third o f disposable polystyrene cups, identical to those which the culture chambers
were made, were placed upon the filter paper.
: vermiculite
: conical glass vessel (H)
Reference : Henriksen and Korsholm (1983).
UNIVFP*-» v o f Na
293
FIG. 11 Schematic representation o f the equipments and the technique
294

Epidemiology, Gastrointestinal Parasite Infections, Dairy Cattle, Kiambu District, Kenya Denmark

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v\ EPIDEM IOLOGY AND CONTROL O F GASTROINTESTINAL PARASITE

INFECTIONS OF DAIRY CATTLE IN KIAMBU DISTRICT, KENYA A ND IN

DENM ARK W ITH EMPHASIS ON PARASITIC GASTROENTERITIS //

ROBERT MAINA W ARUIRU, BVM (Nairobi), M .Sc. (Cornell, USA)

Doctor o f Philosophy in Veterinary Parasitology

of the University of Nairobi

Departm ent of Veterinary Pathology and Microbiology,

Faculty o f Veterinary Medicine

University of Nairobi, Kenya

Prof. W.K. Munyua, B .V .Sc., M .Sc., Dip.A.t.H.. Ph.D.

Prof. J.M. Gathuma, M .Sc., Ph.D.

Faculty o f Veterinary Medicine (Kabete Campus), University o f Nairobi, P. O. Box

29053 Nairobi, Kenya

Prof. Peter Nansen, DVM ., Dr. Vet. Sci., Ph.D.

Danish Centre fo r Experimental Parasitology, Department o f Veterinary

Microbiology, Royal Veterinary and Agricultural University, Bulowsvej, DK-1870

TITLE AND AUTHOR .................................................................................................................. j

LIST OF TABLES ...........................................................................................................................xiii

LIST OF F IG U R E S .................................................................... xviii

LIST OF A P P E N D IC E S .............................................................. xxiii

ACKNOWLEDGEMENTS ...................................................................................................... xxiv

ABSTRACT ..................................................................................................................................... xxvii

CHAPTER 1 GENERAL IN T R O D U C T IO N ............................................................... I

CHAPTER 2 LITERATURE REVIEW ..................................................................... II

2 .1 Farm ing systems and livestock populations

2.1.1 Farming sy stem s....................................................................................... 12

2 .1 .2 Population dynamics .............................................................................. 16

2 .1.3 Offtake estimates by en te r p r ise ........................................................... 17

2.2 Epidemiology o f helminth infections of

rum inants in the tropics .................................................................... 20

2.2.1 Epidemiology o f nematodoses in K e n y a ............................................. 22

2 .2 .2 Bovine parasitic g a stro en teritis........................................................ 23

2.2.2.1 Aetiology, mode of transmissionand species sp ectru m ................... 23

TABLE OF CONTENTS (continued)

2 .2 .2 .2 Nematode life c y c l e s .............................................................................. 24

2 .2 .2 .3 Parasitic development and tissue changes

caused by strongylid nem atodes........................................................... 27

2.2 .2 .3 .1 Haemonchus spp S . ................................................................................. 27

2 .2 .2 .3 .4 Oesophagostomum radiatum ............................................................... 30

2 .2 .2 .4 Factors influencing ep id em io lo g y ...................................................... 32

2 .2 .2 .4 .1 .1 Climate and weather .............................................................................. 32

2 .2 .2 .4 .1 .1 .1 Bionomics of free-living s t a g e s ............................................................ 33

2 .2 .2 .4 .1 .1 .2 Seasonal patterns of in fe c tio n .............................................................. 34

2 .2 .2 .4 .1 .1 .3 Livestock production systems and

2 .2 .2 .4 .2 Intrinsic factors ........................................................................................ 38

2 .2 .2 .4 .2 .2 Host age, sex, acquired resistance and

2 .2 .2 .4 .2 .3 Arrested larval developm en t.................................................................. 42

2 . 2 .2 .4 .2 .4 Concurrent in fection s.............................................................................. 44

TABLE OF CONTENTS (continued)

2 .2.2.5 Pathophysiology and clinical effects of

nem atode in f e c t io n s .............................................................................. 45

2 .2 .2 .5 .1 .1 Decreased feed intake ......................................................................... 45

2 .2 .2 .5 .1 .2 Gut motility, digestion and absorption.............................................. 46

2 .2 .2 .5 .1 .3 Protein and energy m eta b o lism .......................................................... 47

2 .2 .2 .5 .1 .4 Mineral metabolism ............................................................................ 47

2 .2 .2 .5 .1 .5 Water and electrolyte balance .......................................................... 48

2 .2 .2 .5 .2 Clinical effects ..................................................................................... 49

2 .2 .2 .6 Impact o f nematodosis on livestock

2 .2 .2 .7 Diagnosis of parasitic gastroenteritis ........................................... 52

2 .2 . 2 .7.1 Clinical d ia g n o s is .................................................................................. 52

2 .2 . 2 .7 . 2.1 Faecal egg counts ................................................................................ 53

2 .2 .2 .7 .2 .1 .1 Factors affecting egg counts ............................................................. 54