RESEARCH ARTICLE
Variation in the mineral element
concentration of Moringa oleifera Lam. and
M. stenopetala (Bak. f.) Cuf.: Role in human
nutrition
Diriba B Kumssa1,2,3, Edward JM Joy4, Scott D Young1, David W Odee5,6, E Louise Ander2,
Martin R Broadley1*
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1 School of Biosciences, University of Nottingham, Sutton Bonington, Loughborough, United Kingdom,
2 Centre for Environmental Geochemistry, British Geological Survey, Keyworth, Nottingham, United
Kingdom, 3 Crops For the Future, The University of Nottingham Malaysia Campus, Semenyih, Selangor,
Malaysia, 4 Faculty of Epidemiology and Population Health, London School of Hygiene & Tropical Medicine,
London, United Kingdom, 5 Kenya Forestry Research Institute, Nairobi, Kenya, 6 Centre for Ecology and
Hydrology, Bush Estate, Penicuik, Midlothian, United Kingdom
* martin.broadley@nottingham.ac.uk
Abstract
OPEN ACCESS
Citation: Kumssa DB, Joy EJM, Young SD, Odee
DW, Ander EL, Broadley MR (2017) Variation in the
mineral element concentration of Moringa oleifera
Lam. and M. stenopetala (Bak. f.) Cuf.: Role in
human nutrition. PLoS ONE 12(4): e0175503.
https://doi.org/10.1371/journal.pone.0175503
Editor: Jin-Tian Li, Sun Yat-Sen University, CHINA
Received: October 6, 2016
Background
Moringa oleifera (MO) and M. stenopetala (MS) (family Moringaceae; order Brassicales) are
multipurpose tree/shrub species. They thrive under marginal environmental conditions and
produce nutritious edible parts. The aim of this study was to determine the mineral composition of different parts of MO and MS growing in their natural environments and their potential
role in alleviating human mineral micronutrient deficiencies (MND) in sub-Saharan Africa.
Accepted: March 26, 2017
Published: April 7, 2017
Copyright: © 2017 Kumssa et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: Crops for the Future (http://www.
cropsforthefuture.org/) funded DBK’s studentship.
The funders had no role in study design, data
collection and analysis, decision to publish, or
preparation of the manuscript.
Competing interests: The authors have declared
that no competing interests exist.
Methods
Edible parts of MO (n = 146) and MS (n = 50), co-occurring cereals/vegetables and soils (n
= 95) underneath their canopy were sampled from localities in southern Ethiopia and Kenya.
The concentrations of seven mineral elements, namely, calcium (Ca), copper (Cu), iodine
(I), iron (Fe), magnesium (Mg), selenium (Se), and zinc (Zn) in edible parts and soils were
determined using inductively coupled plasma-mass spectrometry.
Results
In Ethiopian crops, MS leaves contained the highest median concentrations of all elements
except Cu and Zn, which were greater in Enset (a.k.a., false banana). In Kenya, Mo flowers
and MS leaves had the highest median Se concentration of 1.56 mg kg-1 and 3.96 mg kg-1,
respectively. The median concentration of Se in MS leaves was 7-fold, 10-fold, 23-fold, 117fold and 147-fold more than that in brassica leaves, amaranth leaves, baobab fruits, sorghum grain and maize grain, respectively. The median Se concentration was 78-fold and
98-fold greater in MO seeds than in sorghum and maize grain, respectively. There was a
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
strong relationship between soil total Se and potassium dihydrogen phosphate (KH2PO4)extractable Se, and Se concentration in the leaves of MO and MS.
Conclusion
This study confirms previous studies that Moringa is a good source of several of the measured mineral nutrients, and it includes the first wide assessment of Se and I concentrations
in edible parts of MO and MS grown in various localities. Increasing the consumption of MO
and MS, especially the leaves as a fresh vegetable or in powdered form, could reduce the
prevalence of MNDs, most notably Se deficiency.
Introduction
Human micronutrient deficiencies (MNDs) are widespread in sub-Saharan Africa [1–3].
There is increasing interest in the potential role of underutilised crops to address MNDs and
Moringa is one example [4]. Moringa is the sole genus of the flowering plant family Moringaceae, order Brassicales; [5]. It comprises 13 species of trees and shrubs (Table 1), namely, M.
arborea, M. borziana, M. concanensis, M. drouhardii, M. hildebrandtii, M. longituba, M. oleifera, M. ovalifolia, M. peregrine, M. pygmaea, M. rivae, M. ruspoliana, and M. stenopetala [6].
Nine of the 13 species in the genus Moringa are native to lowlands of eastern Africa (i.e.,
south-eastern Ethiopia, Kenya and Somalia), of which, eight are considered endemic [7, 8].
The Horn of Africa is considered to be the centre of diversity of Moringa genus, but Moringa
oleifera (MO) is the only species thought to originate outside Africa [8, 9]. Moringa oleifera
and M. stenopetala (MS) are the two cultivated and most studied species [4, 10–19].
Moringa oleifera (Fig 1) is indigenous to the Himalayan foothills of south India [20]. It has
been naturalized to tropical and sub-tropical Asia; Middle East; Africa; and America [8, 21–24].
This pantropical species is known by various names. In English, it is known as drumstick tree
due to the shape of its pods, never die tree due to its ability to thrive under marginal environmental conditions, and mother’s best friend due to its nutritious edible parts that help revive malnourished children [25]. It is known as Mlonge/ Mzunze/ Mjungu moto/ Mboga chungu/ Shingo
in Kenya [8]. Moringa stenopetala (Fig 1) is native to southern Ethiopia and northern Kenya [26,
27]. In southern Ethiopia, it is locally known as Haleko in Walayita and Konso languages.
Moringa oleifera and MS are fast growing multipurpose woody plants which grow in diverse
ecosystems [8, 21, 22, 28, 29], from very dry marginal lowland tropical climates to moist high
altitude regions. They shed their leaves during long dry seasons. Their tuberous roots enable
them to store water and withstand very long dry seasons. The MO tree can grow up to 5–15 m
in height, with a diameter at breast height up to 25 cm [8, 21, 22]. A mature MS tree is usually
larger in overall size and more drought tolerant than MO, with larger leaves, seeds and trunk.
However, MS is slower-growing compared to MO. In experiments conducted in the Sudan,
MS flowered after 2.5 years as compared to 11 months for MO [30].
Nutritional uses
Dietary diversification using underutilized crops/trees, such as Moringa spp. is one of the
many alternative strategies to fight MNDs [2, 3, 31–33]. However, data on nutritional contents
of such under-utilised vegetables and understanding of environmental/genetic variation in
trace elements concentration are limited. Ethnobotanical and biochemical studies carried out
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Table 1. Species in the Moringaceae family order Brassicales, current and synonymous binomial names, and species distribution [7].
Accepted binomial
name
Synonym
Distribution
NE-Kenya
Moringa arborea
Moringa borziana
Hyperanthera borziana
S-Somalia, E-Kenya
Moringa concanensis
Moringa concanensis
SE-Pakistan (Baluchistan, Sind), India (widespread), W-Bangladesh
S-Madagascar
Moringa drouhardii
Madagascar (extinct in the wild, but frequently planted)
Moringa hildebrandtii
Moringa longituba
Hyperanthera longituba
Moringa oleifera
Anoma moringa
NE-Kenya, SE-Ethiopia, Somalia
Indigenous to N-India, Nepal, E-Pakistan; and Introduced in Costa Rica, Australia (Queensland), trop.
Africa, Java, Malesia, Jamaica, Lesser Antilles (St. Martin, St. Barts, Antigua, Saba, St. Eustatius,
St. Kitts, Montserrat, Guadeloupe, Martinique, St. Lucia, St. Vincent, Grenadines, Grenada,
Hyperanthera arborea
Barbados), Panama, Belize, Aruba, Bonaire, Curacao, Haiti, Dominican Republic, Bahamas, Cuba,
Hyperanthera decandra Nicaragua, Mexico, Venezuela, Brazil (c), Seychelles, Somalia, New Caledonia, Fiji, Christmas Isl.
Hyperanthera moringa (Austr.), Palau Isl. (Koror, Namoluk, Pohnpei), Society Isl. (Tahiti, Raiatea), Southern Marianas
(Saipan, Rota, Guam), Niue, Mauritius, Réunion, Rodrigues, Madagascar, Yemen, Oman, Cape
Hyperanthera
Verde Isl. (Santo Antao Isl., Sal Isl., Ilha de Maio, Ilha de Sao Tiago, Fogo Isl.), Ryukyu Isl.,
pterygosperma
Andamans, Nicobars, Myanmar [Burma], Vietnam, Bhutan, Sikkim, Sri Lanka, Laos, Philippines, USA
Moringa domestica
(Florida), U.S. Virgin Isl.
Moringa edulis
Guilandia moringa
Moringa erecta
Moringa moringa
Moringa nux-eben
Moringa octogona
Moringa parvifolia
Moringa polygona
Moringa pterygosperma
Moringa robusta
Moringa sylvestris
Moringa zeylanica
South Africa (Transvaal), Namibia, SW-Angola
Moringa ovalifolia
Moringa peregrina
Gymnocladus arabica
Hyperanthera aptera
Hyperanthera arborea
Hyperanthera
monodynama
Egypt (Eastern Desert, SE-Egypt), Israel (E-Israel: Rift Valley, SC-Israel: Judean Desert, S-Negev
Desert), Jordania (S-Jordania), Oman (Dhofar, Mascat & Oman), Saudi Arabia (C-Saudi Arabia,
N-Saudi Arabia, NW-Saudi Arabia: Hejaz, SW-Saudi Arabia: Asir), Sinai peninsula (Southern Sinai),
Yemen (Aden Desert, coastal Hadhramaut, NE-Yemen: Inner Hadhramaut, SW-Yemen, Tihama),
United Arab Emirates, N-Sudan, N-Ethiopia, Eritrea, Somalia, India
Hyperanthera peregrina
Hyperanthera
semidecandra
Moringa aptera
Moringa arabica
Moringa pygmaea
NE-Somalia
Moringa rivae subsp.
longisiliqua
S-Ethiopia
Moringa rivae subsp.
rivae
Hyperanthera rivae
S-Somalia, S-Ethiopia, Kenya
Moringa ruspoliana
Hyperanthera
ruspoliana
Somalia, SE-Ethiopia, NE-Kenya
Moringa stenopetala
Donaldsonia
stenopetala
Moringa streptocarpa
SW-Ethiopia, N-Kenya
https://doi.org/10.1371/journal.pone.0175503.t001
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Fig 1. M. oleifera tree intercropped with maize at Malindi, Kenya (a); M. stenopetala trees intercropped with
maize, southern Ethiopia (b); Husked M.oleifera seeds (c); husked M. stenopetala seeds (d); and kernel of M.
oleifera (e).
https://doi.org/10.1371/journal.pone.0175503.g001
in various countries where Moringa grow show that these species are multipurpose. They are
used for food, medicine, fodder, fencing, firewood, gum and as a coagulant to treat dirty water
[21, 23, 34–38]. The foliage, immature pods, seeds, and roots are used both as food and medicine. Young shoots are also cooked and eaten [23, 25]. Leaves are either cooked or consumed
raw as vegetables. Moringa leaves are used in a similar way as a cabbage and spinach thereby
nicknamed ‘cabbage tree’ [39]. As a food or forage source, Moringa spp. can supply a wide
range of essential macro and micro nutrients [4, 25, 40, 41]. The mean concentration of Ca,
Cu, Fe, Mg, and Zn in MO leaves collected from a garden in Jalisco State of Mexico were
16100, 9.6, 97.9, 2830 and 29.1 mg kg-1 dry weight (dw), respectively. Similarly, the concentrations of these elements in MS leaves were 12700, 9.1, 69.9, 3690 and 33.7 mg kg-1 dw, respectively [4]. A mean Se concentration of 0.877 mg kg-1 dw was reported in MO leaves grown at
six locations ranging from 0.455 mg kg-1 dw in Rwanda to 2.00 mg kg-1 dw in the Solomon
Islands [42]. However, systematic analysis of Se has not been conducted at multiple sites within
a country and concentrations of other elements such as iodine have not been reported.
Impact of environment on mineral element concentration in Moringa
edible parts
The mineral element concentrations in different edible parts of Moringa spp. are affected by
the environment in which they grow. For example, the effect of elevation and season on mineral micronutrient concentration of leaves and immature pods of MO and MS was studied in
Ethiopia [40]. Concentrations of Ca, Fe, and Zn in Moringa leaves grown in mid-altitude areas
during the rainy season were 24800, 578 and 24.3 mg kg-1 dw for MO and 14900, 700 and 24.7
mg kg-1 dw for MS, respectively. In low altitude areas, the Ca, Fe, and Zn concentration in MO
leaves during rainy season were 25700, 564 and 26 mg kg-1 dw, while in MS leaves, the concentrations were 24000, 581 and 28.1 mg kg-1 dw, respectively [40]. Other studies have compared
MO samples collected from various sites without specifying environmental variables. For
example, in their study on the mineral concentration of MO edible parts in two regions of
Nigeria, it was reported that Ca, Mg, Fe and Cu concentration in the leaves, pods and seeds
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
were higher in tissues collected from Sheda region than Kuje, Abuja [43]. Similarly, a study
conducted in the Punjab province of Pakistan indicated that the Ca, Mg, and Zn concentration
in the leaves and pods of MO varied significantly by region [44]. For example, the Ca concentration in MO leaves in Bahawalnagar and Sadiqabad were 22900 and 19000 mg kg-1 dw
respectively. A study conducted by Olson et al. [4] indicated variation in leaf elemental concentration between 12 Moringa species grown in a common garden experiment.
Study aims
To our knowledge, no studies have explored the association between plant tissue element concentration of Moringa spp., and the site-specific physico-chemical properties of the soil. Previous studies assessing the variation in the elemental concentration in edible parts of Moringa
spp. in various agro-ecological zones have typically been based on generic classifications, e.g.,
elevation [40]. Furthermore, there is some evidence that Moringa accumulates Se [42] but this
has not been widely confirmed in leaves or for other plant parts. Iodine concentrations have
not previously been reported in Moringa leaves. The objectives of this study were to:
• determine the multi-elemental concentration in the flowers, immature pods, leaves, and
seed kernels of MO and MS grown in different agro-ecological zones in Ethiopia and Kenya;
• explore the association between MO and MS edible parts mineral element concentration
and soil physico-chemical properties;
• assess the potential of consumption of MO and MS leaves in alleviating dietary micronutrient deficiencies in sub-Saharan Africa; and
• compare the mineral element concentrations in MS and MO edible parts with locally grown
cereal and vegetable crops.
Materials and methods
This study was conducted in southern Ethiopia and Kenya. Sample collections from localities
in southern Ethiopia were carried out in December 2014 and April 2015, and in July 2015
from localities in Kenya (Fig 2). Edible parts of MO and MS were sampled from plants that
were cultivated by Moringa growing households after receiving their consent. The study was
carried out on private/communal land with the owners’ permission, and it did not involve
endangered or protected species. The study received ethical approval from the University of
Nottingham, School of Biosciences Research Ethics Committee (SB REC), approval number:
SBREC140117A.
Study sites
Edible parts of MO, MS, other food crops, and soil samples, were collected from localities in
southern Ethiopia and Kenya (Fig 2 and S1 Table). Site selection was conducted by the guidance of local agricultural development agents who knew about the localities and households
that cultivate Moringa trees. In addition, different sites with varying soil types were surveyed.
The altitude of the locations ranged from 13 m a.s.l. in Malindi, Kenya to 1700 m a.s.l. in
Hawassa, Ethiopia.
Plant multi-elemental analyses
Sample collection and preparation. A total of 196 Moringa plant edible parts with 3
samples per site for each tissue (i.e., flowers, leaves, immature pods, seeds and roots) were
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Fig 2. Sample collection localities in Ethiopia and Kenya, and grey scale altitudinal range for Ethiopia and Kenya. Country
boundaries shape files were downloaded from the Global Administrative Areas database (http://gadm.org/, Version 2, January 2012), and
digital elevation data were downloaded from http://www.diva-gis.org/Data. Map was created using ESRI ArcMap™ 10.3.1 software.
https://doi.org/10.1371/journal.pone.0175503.g002
collected from southern Ethiopia and Kenya (). The edible parts collected from MS were limited to leaves due to unavailability of other tissues during the sampling campaign. Cereal grains
and vegetable crops were also collected from some of the farmers’ fields that grew those crops
in combination with Moringa trees in Kenya. Similarly, various cereal and pulse grains were
acquired from households that took part in the survey from Ethiopia. Fresh Moringa leaves
were washed in the field by using either tap or bottled water. Fresh edible plant samples collected from Ethiopia were air dried and those from Kenya were oven-dried at 40–50˚C at Kenyan Forestry Research Institute (KEFRI) headquarters in Nairobi and transferred to the
University of Nottingham, UK, for further processing and chemical analyses. The dried edible
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
parts, and grains were milled using an ultra-centrifugal mill to pass through a 1 mm screen
(ZM 200, Retsch GmbH, Haan, Germany).
Nitric acid digestion of plant samples. Subsamples (c. 0.2 g) of the milled plant samples
were weighed in triplicate for nitric acid (HNO3) digestion and subsequent multi-elemental
analysis. Samples were mixed with 6 mL of HNO3 (PrimarPlus—Trace Analysis Grade (TAG),
Fisher Scientific, Loughborough, UK) in microwave digestion tubes and digested at 140˚C for
20 min (Multiwave PRO, Anton Paar, St. Albans, UK). After cooling, the samples were diluted
with 14 mL of Milli-Q water (MQW) (18.2 MO cm; Merck Millipore Milli-Q, Darmstadt, Germany) prior to multi-elemental analysis by inductively coupled plasma-mass spectrometry
(ICP-MS; iCAP-Q, Thermo-Scientific, Loughborough, UK) following a further 1-in-10 dilution with MQW.
TMAH-extractable plant Iodine (I). Iodine was extracted from 0.2 g milled plant material
in 5 mL of 5% tetramethylammonium hydroxide (TMAH) solution (25% w/w aq. Soln., Electronic Grade, 99.9999% [metal basis] Alfa Aesar, Ward Hill, MA, USA), with microwave heating
at 110˚C, for 20 min. The digested samples were diluted to 25 mL with MQW and centrifuged at
3000 rpm for 30 min (Heraeus Megafuge 40 Centrifuge, Thermo Scientific, Osterode am Harz,
Germany) in a single use 50 mL centrifuge tubes (SUCT) (Fisherbrand, Fisher Scientific, Pittsburgh, USA). Supernatant solutions were then filtered using a 0.22 μm syringe filter (SF) (Millex
PES, Merck Millipore Darmstadt, Germany) and transferred to sample tubes for ICP-MS analysis. Due to the high viscosity of the digestates from starchy seeds and grains which blocked the
ICP-MS auto sampler needle, plant iodine analyses were conducted on Moringa leaves only.
Soil multi-elemental analysis
Sample collection and preparation. Thirty-three and 62 soil samples were collected from
southern Ethiopia and Kenya, respectively (S2 Table). Each sample comprised soil pooled
from five locations underneath the canopy of a Moringa tree spp. Bulked samples were air
dried and sieved to pass through < 2 mm screen. A subsample of 30 g was taken to the University of Nottingham. From each sample, a 10 g subsample was Agate ball-milled (PM 400,
Retsch, Haan, Germany) for multi-elemental analyses.
Multi-acid digestion of soils. Triplicate finely ground soil samples (c. 0.2 g) were digested
for two days with 2.5 mL hydrofluoric acid (HF) (40% AR), 2 mL HNO3 (70% TAG), 1 mL
perchloric acid (HClO4) (70% AR) and 2.5 mL MQW in PFA tubes on a Teflon-coated graphite block digester (Model A3, Analysco Ltd, Chipping Norton, UK). On the third day, the hot
plate heating was turned off and 2.5 mL concentrated HNO3 (70% TAG) and MQW were
added and heated for 1 h at 50˚C. After cooling, the digestates were made up to 50 mL in plastic volumetric flasks. Multi-elemental analyses were undertaken by ICP-MS following a further
1-in-10 dilution.
Phosphate-extractable soil Se (Se-P). Duplicate soil samples (< 2 mm; c. 2 g) were
shaken in SUCT for 1 h on a rotary shaker with 20 mL of 0.016 M potassium dihydrogen phosphate (KH2PO4) [45]. The soil suspensions were centrifuged at 2200 rpm for 20 min and 10
mL of supernatant solution was filtered through a SF prior to Se-P analyses by ICP-MS.
TMAH-extractable soil iodine. Finely milled duplicate 2 g soil samples were mixed with
10 mL of 10% TMAH in a SUCT. The soil suspensions were heated in an oven at 70˚C (Memmert GmbH + Co, D 06061, Model 500, Schwabach, Germany) for 3 h and then centrifuged at
c. 3000 rpm for 20 min. The supernatant solution was diluted 1-in-10 with MQW prior to
analysis for iodine by ICP-MS.
Soil pH. The < 2 mm sieved soil was mixed with deionized water at a ratio of 5 g:12.5 mL
in SUCT and shaken for 30 min on a rotary shaker. The pH of the mixture was measured
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
using combined pH meter and electrode (HI-209 pH/mV pH Meter, Hanna Instruments Ltd.,
Leighton Buzzard, UK). Prior to taking the pH readings, the electrode was calibrated using
buffers at pH of 4.01 and 7.00. After each reading, the glass electrode was rinsed by deionized
water before measuring the pH of the next sample.
Analytical quality control
For analytical quality control, blanks, duplicates, internal standards and certified reference
materials were analysed in all instances of plant and soil analyses. The certified reference materials were tomato leaves (1573A), wheat flour (1567B), and Montana soil II (2711A) from the
National Institute of Standards and Technology, Gaithersburg, MD, USA (S3 and S4 Tables).
Raw data of the plant and soil sample analytical results is presented as supplementary tables
(S34–S39 Tables).
Data analyses
Research data compilation and management were carried out using Microsoft Excel and Access
2016 (Microsoft, Redmond, USA). Statistical analyses of the elemental concentration in edible
plant parts and the soils were conducted using IBM1 SPSS1 Statistics version 22 (IBM Corp.,
New York, USA). The Shapiro-Wilk test for normality of the distribution of the data and
Levene’s test for homogeneity of variance were run to select between parametric and nonparametric analyses of variance (ANOVA) (S5–S16 Tables). In addition, visual assessments of
the data distributions were made. Due to the small sample size at each locality, most of the plant
and soil elemental concentration data did not meet the assumptions of parametric ANOVA; logarithmic transformation did not improve the non-normal distribution and heteroscedasticity of
the elemental concentration data. Hence, Welch’s robust test for equality of means was applied
to test the variation in elemental concentration by locality. Spearman’s rank correlation analysis
was conducted using GenStat1 version 17 (VSN International, Hemel Hempstead, UK) to
assess the association between soil physico-chemical properties and Moringa leaves elemental
concentration, and relationships between elemental concentrations in edible parts of various
vegetables. Box plots of plant and soil elemental concentration and pH were drawn using Tableau1 Desktop Professional Edition version 10.0.0 (Tableau Software Inc., Seattle, Washington,
USA). Outliers were not included in the box plots. Plant edible parts with sample size < 3 per
locality were excluded from statistical analyses. For instance, there was only one MO and MS
sample at Baringo and Ramogi, respectively. These were not included in the data analyses.
Results
Plant edible parts and soil elemental concentration analytical results for calcium (Ca), copper
(Cu), iodine (I), iron (Fe), magnesium (Mg), selenium (Se), and zinc (Zn); and soil pH are
reported. The association between plant edible parts elemental concentration and soil properties, and variation in elemental concentration by location are also reported. Furthermore, comparisons are made among Moringa spp. edible parts, maize and sorghum grains, beans,
amaranth leaves, baobab fruit, brassica leaves, and enset (Ensete ventricosum a.k.a., false
banana), mineral element concentrations.
Moringa elemental concentration
The concentrations of mineral elements in Moringa leaves, immature pods, seeds and flowers
and variations by localities are presented below, and summarised in Figs 3—7, S17—S21
Tables and Table 2.
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Fig 3. Quartiles of elemental concentration (mg kg-1 dw) in M. oleifera leaves collected from Kenya
(Kibwezi, Malindi, Mbololo, Ramogi and Ukunda) localities. Median elemental concentration for each
locality is where the light and dark grey shading boxes meet. The horizontal broken lines depict the overall
median concentration for each element across localities.
https://doi.org/10.1371/journal.pone.0175503.g003
Moringa oleifera leaf elemental concentration. The overall mean concentrations of Ca,
Cu, I, Fe, Mg, Se and Zn in MO leaves were 18300, 6.92, 0.218, 202, 5390, 4.25 and 35.6 mg
kg-1 dw, respectively (S17 Table). Mineral element concentration of the MO leaves varied significantly (p < 0.05) between localities, except for Ca (Fig 3 and S27 Table). There was no systematic variation in the relative concentration at a given location for these elements, although
Kibwezi had the highest values of the trace elements (Cu, Se, Zn).
Moringa stenopetala leaf elemental concentration. The overall mean concentrations of
Ca, Cu, I, Fe, Mg, Se and Zn in MS leaves were 21100, 4.53, 0.07, 162, 6440, 1.66 and 22.2 mg
kg-1 dw, respectively (S18 Table). Mean Cu, I, Mg and Zn differed significantly between localities (p < 0.05), while Ca, Fe, and Se concentrations of MS leaves did not differ significantly
between localities (S28 Table). Moringa stenopetala leaves collected from Kenya (n = 5) had
higher median concentrations of mineral elements than those from Ethiopia (n = 36) except
Cu and Zn (Fig 4 and S18 Table). MS leaves from Hawassa, southern Ethiopia had significantly
(p < 0.05) higher concentration of Zn and lower Mg than those from Baringo Island, Kenya.
On the contrary, MS leaves collected from Baringo island contained significantly (p < 0.05)
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Fig 4. Quartiles of elemental concentration (mg kg-1 dw) in M. stenopetala leaves collected from
Ethiopia localities (Derashe, Hawassa and Konso), and Kenya locality (Baringo). Median elemental
concentration for each locality is where the light and dark grey shading boxes coincide. The horizontal broken
lines depict the overall median concentration for each element across localities.
https://doi.org/10.1371/journal.pone.0175503.g004
higher concentrations of Se and I than all samples from localities in Ethiopia. The concentration of Cu in MS leaves collected from Baringo island were significantly (p < 0.05) lower than
samples from Derashe, southern Ethiopia.
Moringa oleifera immature pods elemental concentration. The overall mean concentrations of Ca, Cu, Fe, Mg, Se and Zn in MO immature pods were 3600, 5.42, 65.4, 2860, 2.36 and
27.6 mg kg-1 dw, respectively (S19 Table). The distribution of MO immature pods elemental
concentration in comparison with the overall median value varied between the elements and
locations (Fig 5). For example, the median elemental concentration in the immature pods collected from Kibwezi were generally higher than the overall median concentration in Kenya.
The median Ca and Mg concentration in immature pods collected from Ramogi and Ukunda
were below the overall median concentration in Kenya. There were significant differences
(p < 0.05) in the Cu, Fe and Mg but not (p 0.05) Ca, Se and Zn mean concentrations of MO
immature pods collected from different localities (S30 Table).
Moringa oleifera seeds elemental concentration. The overall mean concentrations of Ca,
Cu, Fe, Mg, Se and Zn in MO seeds were 1310, 4.18, 49.2, 3080, 3.59 and 44.8 mg kg-1 dw,
respectively (S20 Table). Overall median elemental concentration in MO seeds varied between
the elements and locations (Fig 6). There was no significant difference (p 0.05) in the mean
elemental concentration of MO seeds collected from different localities (S31 Table).
Moringa oleifera flowers elemental concentration. The overall mean concentrations of
Ca, Cu, Fe, Mg, Se and Zn in MO flowers were 3650, 6.40, 253, 2830, 2.81 and 32.7 mg kg-1
dw, respectively (S21 Table). The distribution of MO flowers elemental concentration in
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Fig 5. Quartiles of elemental concentration (mg kg-1 dw) in M. oleifera immature pods collected from
Kenya localities. Median elemental concentration for each locality is where the light and dark grey shading
boxes coincide. The horizontal broken lines depict the overall median concentration for each element across
localities.
https://doi.org/10.1371/journal.pone.0175503.g005
comparison with the overall median value varied between elements and locations (Fig 7).
There were significant differences (p < 0.05) in the mean Ca, Cu, Fe, Mg and Se, but not Zn
concentrations of MO flowers collected from different localities (S32 Table).
Comparison of elemental concentration between crops
For comparison, elemental concentration of Moringa spp. edible parts and other vegetables,
fruits, and staple cereal crops are presented in Table 2. On a weight-for-weight basis, in Ethiopia, MS leaves contained the highest median concentrations of all elements except Cu and Zn.
Median concentrations of Cu and Zn were highest in enset and beans, respectively (Table 2).
In Kenya, on weight-for-weight basis, Moringa edible parts had the highest median Se concentration ranging from 1.56 mg kg-1 in MO flowers to 3.96 mg kg-1 in MS leaves. The median
concentration of Se in MS leaves was 7-fold, 10-fold, 23-fold, 117-fold and 147-fold more than
that in brassica leaves, amaranth leaves, baobab fruits, sorghum grain and maize grain, respectively. The median Se concentration in MO seeds was 78-fold and 98-fold greater than sorghum
and maize grain, respectively. Seeds of MO had the highest median Zn concentration while amaranth leaves contained comparable quantities of Zn with MO flowers and leaves. The median
Zn concentration in MO seeds was 2-fold greater than in maize and sorghum grain. (Table 2).
Soil pH and elemental concentrations
Ninety percent of the soil samples from Ethiopia and 97% of those from Kenya had pH >7
(S37 Table). The soil pH at the three localities in Ethiopia ranged from 6.12 in Hawassa to
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Fig 6. Quartiles of elemental concentrations in M. oleifera seeds (mg kg-1 dw) collected from Kenya
localities. Median elemental concentration for each locality is where the light and dark grey shading boxes
coincide. The horizontal broken lines depict the overall median concentration for each element across
localities.
https://doi.org/10.1371/journal.pone.0175503.g006
8.67 in Derashe, with overall mean and median of 7.84 and 7.98, respectively. In Kenya, soil
pH ranged from 6.63 in Mbololo to 8.65 in Malindi with overall mean and median of 7.88
and 7.85, respectively (Fig 8, Table 3 and S22 Table). Welch’s robust test of equality of means
showed that the soil pH varied significantly between localities (p < 0.05) (S33 Table). Similarly, Welch’s robust tests of equality of mean soil elemental concentrations showed that
there was significant difference (p < 0.05) between soils collected from various localities (S33
Table). Descriptive statistics of the soil physico-chemical properties across all localities in
Ethiopia and Kenya are summarized in Table 3. Soil samples from Baringo, Kibwezi and
Ramogi localities were the three with highest median phosphate-extractable Se concentration. Total Se concentration was highest in soils from Baringo, Hawassa and Ramogi. With
respect to total soil iodine, Ramogi, Kibwezi and Mbololo soil samples had the highest concentrations. Total Zn concentration in soil samples from Hawassa were 2-fold, 4-fold and
3-fold more than the median Zn concentration from soils in Ethiopia, Kenya and overall
median Zn concentrations.
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Fig 7. Quartiles of elemental concentrations (mg kg-1 dw) in M. oleifera flowers collected from Kenya localities.
Median elemental concentration for each locality is where the light and dark grey shading boxes coincide. The horizontal
broken lines depict the overall median concentration for each element across localities.
https://doi.org/10.1371/journal.pone.0175503.g007
Relationships between MO edible parts and other vegetables
The association between elemental concentrations of the edible parts of MO are presented in
S40 Table. Calcium concentration in MO flowers showed highly significant (p < 0.01) positive
correlation with the Ca, Cu, Mg, and Se concentration in MO immature pods. Contrary to
this, the Cu concentration in MO flowers had a significant (p < 0.01) negative correlation with
the Ca in the seeds and leaves. The Se in the MO flower was highly significantly (p < 0.01) correlated with the Se in leaves and immature pods. The association between the elemental concentrations in MO edible parts and other vegetables cultivated on the same location are
presented in S41–S43 Tables. The Fe concentration in MO leaves showed significant
(p < 0.05) positive correlation with the Fe, and negative correlation with the Se concentration
in amaranth leaves (S41 Table). Calcium concentration in MO leaves showed significant
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Table 2. Median elemental concentrations in cereals, vegetables, fruits and seeds grown in various parts of Ethiopia and Kenya, and the number
of samples (n).
Crop
Median concentration (mg kg-1 dw)
n
Ca
Cu
I
Fe
Mg
Se
Zn
Ethiopia
MS leaves
36
19400
117
6070
1.12
21.0
Maize grain
17
55.1
0.943
4.71
0.093
28.2
918
0.182
20.4
Enset
5
2,190
1.30
71.3
260
0.060
34.2
Sorghum grain
8
176
1.74
51.5
1350
0.097
16.1
Beans
4
1500
9.41
88.5
1760
0.150
24.9
Amaranth leaves
6
26700
6.88
339
12900
0.399
33.9
Baobab fruits
4
2660
7.63
9.40
1180
0.169
11.9
Brassica leaves
4
32000
9.25
104
7880
0.597
17.4
Maize grain
9
51.2
2.80
16.5
912
0.027
21.5
MO flowers
33
3420
6.25
4.73
2610
1.56
31.7
MO immature pods
25
3060
5.05
62.6
2610
1.99
27.8
MO leaves
56
16700
6.83
160
5400
2.73
33.3
MO seeds
32
1250
4.02
49.8
3100
2.64
46.0
MS leaves
5
22500
3.07
Sorghum grain
6
103
6.24
Kenya
0.201
0.231
190
7210
3.96
15.7
33.7
1220
0.034
22.6
https://doi.org/10.1371/journal.pone.0175503.t002
(p < 0.01) negative correlation with the Ca, Cu, and Mg concentration in brassica leaves (S42
Table). Similarly, Ca concentration in amaranth leaves showed a significant (p < 0.01) negative
correlation with the Ca, Cu, and Mg concentrations in brassica leaves (S43 Table).
Relationships between Moringa leaves elemental concentration and soil
properties
The concentration of Cu in MO leaves was significantly (p < 0.05) positively associated with
total soil Cu and Fe concentrations. Similarly, MO leaf Fe concentration also showed a statistically significant (p < 0.05) positive correlation with soil Fe, Se and Zn. Selenium concentration
in MO leaves showed a stronger significant (p < 0.05) positive correlation with phosphate
extractable (Se-P) soil Se than the total soil Se (S23 and S24 Tables). The Ca and Zn concentration in MO leaves showed no statistically significant (p 0.05) correlation with any of the
reported soil properties.
Moringa stenopetala leaf Fe concentration was significantly (p < 0.05) positively correlated
with soil Mg, Se and Se-P. Similarly, MS leaves Mg concentration showed a statistically significant (p <0.05) negative correlation with soil Zn concentration. The Se content of MS leaves
indicated a strong and significant positive correlation with the soil Se-P (S25 and S26 Tables).
However, the Ca, Cu and I concentration of MS leaves did not show significant (p 0.05) correlation with any of the soil properties.
Discussion
Elemental concentration in edible parts of Moringa spp.
This study is the first comprehensive analysis of Se concentrations in different edible parts of
MO and MS grown in various localities. Four previous studies reported Se concentrations in
MO leaves, from Niger (27.1 mg kg-1 dw) [46], Solomon Islands (2 mg kg-1 dw) [42], South
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Fig 8. Quartiles of soil elemental concentration (mg kg-1 dw) and pH collected from southern Ethiopia
(Derashe, Hawassa and Konso), and Kenya (Baringo, Kibwezi, Malindi, Mbololo, Ramogi and Ukunda)
localities. Median elemental concentration for each locality is where the light and dark grey shading boxes
coincide. The horizontal broken lines depict the overall median of each property across localities. Total soil
elemental concentrations except for Se-P, which is KH2PO4-extractable fraction.
https://doi.org/10.1371/journal.pone.0175503.g008
Africa (363 mg kg-1 dw) [41], and Mexico, Lombardia (0.096 mg kg-1 dw) and San Pedro (1.07
mg kg-1 dw) [47]. Our MO leaf Se concentration (mean = 4.25 and median = 2.73 mg kg-1 dw)
is consistent with results from Solomon Islands and Mexico, but differ markedly from the
South African data. The results of the analyses from Niger were based on two samples. Taking
this into account, and the fact that a MO leaf sample (L-MO-29-MBO) from Mbololo, Kenya,
had a mean Se concentration of 21.2 mg kg-1 dw from triplicate analyses (S34 Table), the findings from Niger were reasonably consistent with ours. Our attempt to verify the very high
reported concentrations from the South Africa study by contacting the authors was not successful. Iodine concentrations in MO and MS leaves or other parts have not been reported previously to our knowledge.
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Table 3. Descriptive statistics of soil pH, and elemental concentrations by locality.
Locality
Statistic
Baringo
n
Concentration (mg kg-1 dw)
Ca
Derashe
Hawassa
Kibwezi
Konso
Malindi
Mbololo
Ramogi
Ukunda
Ethiopia
Kenya
Total
Cu
I
Fe
Mg
Se
Se-P
Zn
pH
5
5
5
5
5
5
5
5
5
Mean
38400
23.7
0.923
66200
15000
0.550
0.027
97.7
7.88
Median
52000
31.1
1.06
67000
19500
0.664
0.035
92.9
7.96
12
12
12
12
12
12
12
12
12
Mean
28400
33.4
0.851
69200
13700
0.255
0.006
88.0
8.40
Median
30600
31.2
0.748
74900
14800
0.222
0.006
90.7
8.48
9
9
9
9
9
9
9
9
9
Mean
15800
13.0
1.13
35400
4800
0.599
0.011
260
7.43
Median
14100
8.62
0.941
32900
3800
0.622
0.010
229
7.66
14
14
14
14
14
14
14
14
14
Mean
14200
24.0
1.72
33000
4020
0.362
0.024
54.0
7.88
Median
12800
21.7
1.41
29300
3260
0.366
0.023
51.5
7.89
12
12
12
12
12
12
12
12
12
Mean
18700
26.2
0.771
56000
7120
0.239
0.004
85.725
7.595
Median
21800
35.0
0.676
63100
6100
0.204
0.005
83.1
7.59
11
11
11
11
11
11
11
11
11
Mean
7290
4.72
0.955
12200
566
0.179
0.019
39.9
8.40
Median
4000
5.63
0.768
14500
591
0.177
0.018
45.4
8.44
n
n
n
n
n
16
16
16
16
16
16
16
16
16
Mean
13400
10.3
1.43
22300
3210
0.241
0.020
39.8
7.53
Median
12900
9.38
1.30
21300
3260
0.203
0.018
39.7
7.50
8
8
8
8
8
8
8
8
8
Mean
3550
35.5
3.24
68900
2210
0.550
0.018
87.8
7.81
Median
3670
21.3
2.81
53600
2020
0.529
0.019
81.6
7.81
7
7
7
7
7
7
7
7
7
Mean
12900
7.55
1.00
7690
715.3
0.155
0.014
92.3
7.94
Median
14600
7.07
0.923
8040
839
0.169
0.013
102
7.83
33
33
33
33
33
33
33
33
33
Mean
21400
25.2
0.898
55200
8870
0.343
0.007
134
7.84
Median
22300
30.7
0.773
51200
6700
0.281
0.006
101
7.98
61
61
61
61
61
61
61
61
61
Mean
13200
16.5
1.56
31000
3470
0.313
0.020
60.2
7.88
Median
11800
11.3
1.20
23500
2300
0.239
0.018
53.5
7.85
94
94
94
94
94
94
94
94
94
Mean
16100
19.6
1.33
39500
5360
0.324
0.016
86.1
7.87
Median
13700
13.0
0.972
29700
3130
0.240
0.015
66.0
7.88
n
n
n
n
n
n
https://doi.org/10.1371/journal.pone.0175503.t003
Table 4 summarises 11 previous studies of MO leaf elemental concentrations alongside data
from the present study. Allowing for differences in analytical method and likely inter-study
variation in leaf maturity there are many broad similarities. For example, the mean Ca concentration in MO leaves in the present study is the fourth lowest following MO leaf samples collected from Kuje, Nigeria [43], Hawassa, Ethiopia [48] and Jalisco state, Mexico [4], while the
mean Zn concentration is the second highest following MO leaves collected from Thailand
[49]. Similarly, mean elemental concentrations in MS leaves collected from Ethiopia and
Kenya in the current study indicated inconsistent variation when compared with previous
studies. For instance, the mean concentration of Ca in MS leaves of 21 g kg-1 dw in the present
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Table 4. Comparison of reported mineral element concentrations in MO leaf, sources, number of observation (n) and locations. The concentration
values in the first row in bold are the result from current study.
Ca
Cu
I
Fe
Mg
Se
Zn
Source
n
Location
-1
mean (mg kg dw)
18300
6.92
0.218
202
5370
4.25
35.6 Current study
56 Various localities, Kenya
16000
9.6
__
97.9
2800
__
29.1 [4]
23 Mexico, Jalisco State
25800
9.44
__
591
5520
__
24.7 [40] †
6 Hawassa, Ethiopia
26200
9.58
__
561
5550
__
25.2 [40]†
6 Arbaminch, Ethiopia
36500
8.25
__
490
5000
363
31 [41]
20000
7
__
___
3700
2.0
31 [42]
3463
44
__
41
725
__
__ [43]
2 Kuje, Abuja, Nigeria
38270
43.6
__
78.8
806
__
__ [43]
2 Sheda, Abuja, Nigeria
22900
9.5
__
205
100
__
25.9 [44]
2 Bahawalnager, Pakistan
19000
11.2
__
397
98.2
__
20.9 [44]
2 Sadiqabad, Pakistan
26400
7.3
__
573
109
__
34.1 [44]
2 Chenabnager, Pakistan
24000
8.85
__
226
4340
27.1
< 5 [46]
2 Zinger, Niger
20200
10.3
__
194
3230
0.096
10 [47]
5 Lombardia, Mexico
26200
4.1
__
70.7
3400
1.07
16 [47]
5 San Pedro, Mexico
12900
17.7
__
391
1800
__
28.2 [48]
Hawassa, Ethiopia
__
7.6
18400
†
Limpopo, South Africa
Honaiara, Solomon Islands
__
82.2
__
__
92.8 [49]
5 Thailand
__
173
5630
__
24.8 [50]
Chad
27400
12.2
__
417
4900
__
30.9 [50]
Sahrawi camps, Algeria
21500
6.6
__
119
5340
__
21.8 [50]
Haiti
†
Values were averaged
https://doi.org/10.1371/journal.pone.0175503.t004
study is comparable with that reported from Ethiopia [40] (19.8 g kg-1 dw), and greater than
the 12.7 g kg-1 dw reported from Mexico [4]. However, the Fe concentration (162 mg kg-1 dw)
in the present study is far lower than that reported from Ethiopia (666 mg kg-1 dw) [40].
Mean elemental concentrations in MS leaves collected from Ethiopia and Kenya in the current study indicated inconsistent variation when compared with previous studies. For
instance, the mean concentration of Ca in MS leaves of 21 g kg-1 dw in the present study is
comparable with that reported from Ethiopia [40] (19.8 g kg-1 dw), and greater than the 12.7 g
kg-1 dw reported from Mexico [4]. However, the Fe concentration (162 mg kg-1 dw) in the
present study is far lower than that reported from Ethiopia (666 mg kg-1 dw) [40].
The mean concentration of Ca (3,600 mg kg-1 dw) in the immature pods of MO in the
current study was higher than that reported from Ethiopia (2,740 mg kg-1 dw) [40] and Pakistan (2,740 mg kg-1 dw) [44]. However, the Fe concentration (65.4 mg kg-1 dw) in the MO
immature pods in this study was much lower than that reported from Ethiopia (510 mg kg-1
dw) [40] and Pakistan (510 mg kg-1 dw) [44]. The Cu, Mg and Zn concentrations in the
immature pods of MO reported from Ethiopia [40] are comparable to our findings. However, the concentration of Cu in the immature pods of MO reported from Pakistan (26.6 mg
kg-1 dw) [44] was higher than the results in this study (5.42 mg kg-1 dw). Elemental concentration in MO seed kernel in the present study showed inconsistent variation as compared to
previous studies in two regions of Nigeria [43]. For example, the mean concentration of Cu
(4.2 mg kg-1 dw) and Fe (49.2 mg kg-1 dw) in MO seed kernel in the present study is lower
than the MO seed kernel samples collected from Sheda region of Nigeria with Cu and Fe
concentration of 34.2 mg kg-1 dw and 118.5 mg kg-1 dw, respectively. Calcium concentration
of 1310 mg kg-1 dw in the present study is higher than the concentration of Ca (1029 mg kg-
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
1
) in MO seed kernel collected from Kuje region of Nigeria [43]. The variation in elemental
concentration in immature pods and seeds of MO this study and others can be attributed to
the variation in environment in which MO grew, intra-specific variation in the MO, the variation in maturity levels of immature pods, and the difference in analytical method pursued.
There are no studies we are aware of that report the elemental concentrations in the flowers
of Moringa species.
Variation in Moringa spp. element concentration
Variation in the elemental concentrations of the different edible parts of MO and MS can be
due to the impact of the environment/management, the effect of intra- and inter-specific
genetic variation [4], and the interactions between the genetics and environment [40]. The
seeds and/or planting materials sources of the Moringa trees from which the edible parts were
sampled were not traceable and so this discussion is limited to environment/management factors. Samples were collected from trees that were grown and managed by households in various localities of Ethiopia and Kenya. Different households pursue various tree management
regimes, such as, lone trees, hedgerow, woodlot, pollarding, lopping, watering, fertilizing,
intercropping, etc. For example, some households place household wastes and manure that
can supply nutrients to the trees and some may water their plants during dry season. Stages of
growth, for instance, of the leaves at the time of surveying varies due to variation in management regime, and climate and soil type may all contribute further to variation of the elemental
concentration in the edible parts.
The positive correlation between some of the Moringa edible parts elemental concentration
and soil chemical properties indicate the significance of the soil environment in which the
plants grow besides the inherent genetic ability of these species to absorb and translocate mineral elements to edible parts. In addition, it is not only the quantity of the mineral element
available in the soil which impacts on the Moringa spp. edible parts elemental concentration
but also the chemical form in which the element exists in the soil [51]. The stronger positive
correlation of Moringa leaves Se concentration with KH2PO4 extractable soil Se than the total
soil Se was an indication of the association between Moringa edible parts and phyto-available
soil elemental concentration.
Moringa spp. role in human Se nutrition
Selenium deficiencies are widespread in sub-Saharan Africa [3, 33]. For instance, based on
2009 food supply data from the Food and Agriculture Organization, national level Se deficiency risks in Ethiopia and Kenya were estimated to be 35.5% and 58.3%, respectively [33].
Based on seven day dietary recall survey conducted in the year 2010–2011, Joy, Kumssa et al.,
[3] estimated that 81% of Malawian households had insufficient Se to meet dietary requirements. Similarly, in northwest Ethiopia, Gonder town, a cross-sectional study on school children (n = 100) using blood serum concentration of mineral nutrients reported 62% of the
children were deficient in Se [52]. Gashu et al. [53] reported Se deficiency risk in school children in the Amhara region of Ethiopia to be 58% (n = 349).
Moringa spp. edible parts contain high concentrations of Se and the leaves have similar
levels of the 6 other reported mineral elements to other leafy vegetables grown in the same
localities. Table 5 summarizes the Recommended Daily Allowances (RDA) for an adult male
of Ca, Cu, I, Fe, Mg, Se and Zn, concentrations of these mineral elements in MO and MS
leaves collected from various localities of Ethiopia and Kenya, and percentage of RDA fulfilled by consuming 100 g of fresh Moringa leaves per day. The RDA is a daily nutrient intake
level that fulfils the nutrient requirements of ~ 98% of the healthy individuals in an age- and
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Table 5. Recommended Daily Allowance (RDA) [54] for 19–70 yrs. old adult males (mg capita-1 d-1), median elemental concentration in 100 g fresh
Moringa leaves (mg) from Kenya and Ethiopia and percentage of RDA fulfilled by consuming 100 g fresh Moringa leaves.
Ca
Cu
I
Fe
Mg
Se
Zn
RDA
1000
0.9
0.15
18
MO Kenya
334
0.137
0.004
3.18
320
0.055
8
108
0.055
% of RDA fulfilled
33
15
3
18
34
100
0.665
8
MS Ethiopia
387
0.094
0.002
2.34
121
0.022
0.419
% of RDA fulfilled
39
10
1
13
38
41
5
MS Kenya
450
0.061
0.005
3.80
144
0.079
0.314
% of RDA fulfilled
45
7
3
21
45
144
4
https://doi.org/10.1371/journal.pone.0175503.t005
sex-specific population [54]. Moringa oleifera grown without Se fertilizer can provide 100%
of the RDA of a healthy adult man which is comparable with Se obtained from a similar
quantity of carrots biofortified with 1 kg ha-1 of Se fertilizer [55], and maize biofortified with
5 g of Se ha-1 at the level of the Malawian population maize consumption [56]. A daily consumption of 100 g fresh leaves of MS grown in Ethiopia can fulfil 41% of the Se RDA, while
MS grown in Kenya can provide 144% of the Se RDA for a healthy adult man. Consumption
of fresh leaves or leaf powders of MO and MS, for example, can help at least to reduce the
many MNDs and alleviate Se deficiency if interventions target vulnerable populations living
in localities where these Moringa species grow vigorously. Besides, Moringa leaf powders can
be stored for use during the dry season and transported and traded with areas where Moringa
is not cultivated to fight against MNDs. In areas where rain fed agriculture is practiced, other
vegetables, for example, Brassica can be used to diversify sources of dietary mineral elements
and Moringa leaf powders can be stored and used when they are needed most during the dry
season.
Conclusion
In addition to the high selenium concentration, Moringa spp. leaves are rich in proteins and
β-carotene [4, 50], possess anti-oxidant properties [17], contain low concentrations of antinutrients [57–60], may be used in treating ailments [18, 61], the seeds are used as water
coagulant [62], and they grow under marginal environmental conditions providing much
needed ecological services (for example, shade, wind break, etc.). Moringa oleifera is naturalized while MS is indigenous to Kenya and Ethiopia. Where these species grow, the population have indigenous knowledge of their multiple uses including the high nutritive values
[63]. Nonetheless, the utilization of these species as food is limited to specific localities and
communities [8], they are neglected in terms of research and development, and the trees
can be classed as underutilized crops [64, 65]. Agricultural and health extension work to
popularise the production and consumption of MO and MS may be a useful strategy to
complement efforts to alleviate dietary MNDs through dietary diversification, and use of
Moringa leaf powders to fortify meals in the dry season when other leafy green vegetables
are not available. In addition, variations in mineral micronutrient concentrations suggest
that breeding efforts to increase the nutritional value of Moringa foliage may be successful.
However, research is also required to determine the bioavailability of nutrients from Moringa edible parts. The Moringaceae belongs to the same order (Brassicales) as Brassicaceae
[5] which are known to be Se accumulators [66, 67]. Hence further studies on the Se concentrations in edible portions of the other Moringa species are important to understand and
exploit the potential of the family in the fight against human Se undernutrition.
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
Supporting information
S1 Table. Number of Moringa edible part samples collected from Ethiopia and Kenya by
locality and species. MO, M. oleifera, MS, M. stenopetala.
(PDF)
S2 Table. Number of soil samples (n) collected from the different localities in Ethiopia and
Kenya.
(PDF)
S3 Table. Descriptive statistics on elemental concentration (mg kg-1) of plant Certified
Reference Materials (CRM).
(PDF)
S4 Table. Descriptive statistics on elemental concentration (mg kg-1) of soil Certified Reference Materials (CRM) (2711A).
(PDF)
S5 Table. Shapiro-Wilk test of normality of the distribution of soil elemental concentration by locality.
(PDF)
S6 Table. Levene’s test of homogeneity of variances of soil elemental concentration based
on mean and median. D.f. 1 is the degree of freedom of the numerator, and d.f. 2 is the degree
of freedom of the denominator.
(PDF)
S7 Table. Test of normality of the distribution of MO leaves elemental concentration by
locality in Kenya.
(PDF)
S8 Table. Levene’s test of homogeneity of variances of MO leaves elemental concentration
by localities in Kenya based on mean and median. D.f. 1 is the degree of freedom of the
numerator, and d.f. 2 is the degree of freedom of the denominator.
(PDF)
S9 Table. Test of normality of the distribution of MS leaves elemental concentration by
locality.
(PDF)
S10 Table. Levene’s test of homogeneity of variances of MS leaves elemental concentration
by localities based on mean and median. D.f. 1 is the degree of freedom of the numerator,
and d.f. 2 is the degree of freedom of the denominator.
(PDF)
S11 Table. Test of normality of the distribution of MO immature pods elemental concentration by locality.
(PDF)
S12 Table. Levene’s test of homogeneity of variances of MO immature pods elemental concentration by localities.
(PDF)
S13 Table. Test of normality of the distribution of MO seeds elemental concentration by
locality.
(PDF)
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
S14 Table. Levene’s test of homogeneity of variances of MO seeds elemental concentration
by localities.
(PDF)
S15 Table. Test of normality of the distribution of MO flowers elemental concentration by
locality.
(PDF)
S16 Table. Levene’s test of homogeneity of variances of MO flowers elemental concentration by localities.
(PDF)
S17 Table. Descriptive statistics of MO leaves elemental concentration (mg kg-1) by locality.
(PDF)
S18 Table. Descriptive statistics for MS leaves elemental concentration (mg kg-1) by locality.
(PDF)
S19 Table. Descriptive statistics for MO immature pods elemental concentration (mg kg1) by locality.
(PDF)
S20 Table. Descriptive statistics for MO seeds elemental concentration (mg kg-1) by locality.
(PDF)
S21 Table. Descriptive statistics for MO flowers elemental concentration (mg kg-1) by
locality.
(PDF)
S22 Table. Descriptive statistics for soil elemental concentration (mg kg-1) and pH by
locality.
(PDF)
S23 Table. Spearman’s rank correlation (N = 56, d.f. = 54) between the elemental concentration of MO leaves and soil properties.
(PDF)
S24 Table. The t probabilities for the Spearman’s rank correlation between the elemental
concentration of MO leaves and soil properties. Significant correlations are in bold.
(PDF)
S25 Table. Spearman’s rank correlation (N = 32, d.f. = 30) between the elemental concentration of MS leaves and soil properties.
(PDF)
S26 Table. The t probabilities for the Spearman’s rank correlation between the elemental
concentration of MS leaves and soil properties. Significant correlations are in bold.
(PDF)
S27 Table. Welch’s robust test of equality of mean elemental concentrations in MO leaves
across localities in Kenya. d.f. 1 (degrees of freedom of the numerator), d.f. 2 (degrees of freedom of the denominator), and the p probability value.
(PDF)
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
S28 Table. Welch’s robust test of equality of mean elemental concentrations in MS leaves
across localities. d.f. 1 (degrees of freedom of the numerator), d.f. 2 (degrees of freedom of the
denominator), and the p (probability value).
(PDF)
S29 Table. Welch’s robust test of equality of mean elemental concentrations in MO and
MS leaves. d.f. 1 (degrees of freedom of the numerator), d.f. 2 (degrees of freedom of the
denominator), and the p (probability value).
(PDF)
S30 Table. Welch’s robust test of equality of mean elemental concentrations in MO immature pods across localities. d.f. 1 (degrees of freedom of the numerator), d.f. 2 (degrees of freedom of the denominator), and the p (probability value).
(PDF)
S31 Table. Welch’s robust test of equality of mean elemental concentrations in MO seeds
across localities. d.f. 1 (degrees of freedom of the numerator), d.f. 2 (degrees of freedom of the
denominator), and the p (probability value).
(PDF)
S32 Table. Welch’s robust test of equality of mean elemental concentrations in MO flowers
across localities. d.f. 1 (degrees of freedom of the numerator), d.f. 2 (degrees of freedom of the
denominator), and the p (probability value).
(PDF)
S33 Table. Welch’s robust tests of equality of mean soil elemental concentrations across
localities. d.f. 1 (degrees of freedom of the numerator), d.f. 2 (degrees of freedom of the
denominator), and the p (probability value).
(PDF)
S34 Table. Raw data on MO and MS edible parts elemental concentration (mg kg-1), and
sample details.
(PDF)
S35 Table. Raw data on MO and MS leaves iodine concentration (mg kg-1) and sample
details.
(PDF)
S36 Table. Raw data on elemental concentrations (mg kg-1) in various crops and sample
details. ND = not detectable.
(PDF)
S37 Table. Raw data on soil elemental concentration (mg kg-1) and pH, and sample details.
(PDF)
S38 Table. Raw data on soil iodine concentration (mg kg-1) and sample details.
(PDF)
S39 Table. Raw data on phosphate-extractable soil selenium (Se-P) concentration (mg kg1) and sample details.
(PDF)
S40 Table. Correlation between elemental concentrations of MO edible parts (flower,
immature pod, leaf and seed). The figures below the yellow diagonal are correlation coefficients and those above the diagonal are p values. Correlation is significant at the 0.01 level
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Mineral element concentration of M. oleifera and M. stenopetala: Role in human nutrition
(2-tailed). Correlation is significant at the 0.05 level (2-tailed). N = 18
(PDF)
S41 Table. Correlation between the elemental composition of MO and amaranth leaves.
Correlation is significant at the 0.05 level (2-tailed). N = 6.
(PDF)
S42 Table. Correlation between the elemental composition of MO and brassica (BO)
leaves. Correlation is significant at the 0.05 level (2-tailed). N = 4.
(PDF)
S43 Table. Correlation between the elemental composition of MO and brassica (BO)
leaves. Correlation is significant at the 0.05 level (2-tailed). N = 3.
(PDF)
Acknowledgments
We are grateful to Charles Oduor, James Gitu and Mishek Kiarie of the Kenyan Forestry
Research Institute for their assistance during sample collection from various locations in
Kenya, and Asmelash Dagne for assistance during sample collection in Ethiopia. Dr Vazquez
Reina Saul helped in multi-elemental analyses of MS leaves collected from Hawassa, Ethiopia.
Author Contributions
Conceptualization: DBK EJMJ SDY ELA DWO MRB.
Data curation: DBK EJMJ.
Formal analysis: DBK EJMJ.
Funding acquisition: MRB ELA SDY.
Investigation: DBK EJMJ SDY.
Methodology: DBK MRB SDY ELA EJMJ DWO.
Project administration: DBK EJMJ DWO ELA SDY MRB.
Resources: ELA SDY DWO.
Supervision: MRB SDY ELA.
Validation: DBK.
Visualization: DBK.
Writing – original draft: DBK.
Writing – review & editing: DBK MRB SDY ELA EJMJ DWO.
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Diriba Kumssa