Veterinary World, EISSN: 2231-0916
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RESEARCH ARTICLE
Open Access
Fungal food spoilage of supermarkets’ displayed fruits
Iman Saleh and Roda Al-Thani
Department of Biological and Environmental Sciences, College of Arts and Sciences, Qatar University, P.O. Box 2713,
Doha, Qatar.
Corresponding author: Iman Saleh, e-mail: imanesaleh@qu.edu.qa
Co-author: RA: ralthani@qu.edu.qa
Received: 08-07-2019, Accepted: 22-10-2019, Published online: 29-11-2019
doi: www.doi.org/10.14202/vetworld.2019.1877-1883 How to cite this article: Saleh I, Al-Thani R (2019) Fungal food
spoilage of supermarkets’ displayed fruits, Veterinary World, 12(11):1877-1883.
Abstract
Background and Aim: Post-harvest fungal infection of fruits and vegetables is mainly caused by fungal pathogens that
can be harmful to both human and animals as they produce mycotoxins, post-harvest diseases in fruits and vegetables are
a serious problem that results in the loss of a large percentage of crops reaching 50% in some fruits. This study aims at
screening the post-purchasing shelf-life of four highly consumed fruits and vegetables and at identifying the fungal strains
behind their spoilage in Qatar.
Materials and Methods: Fruits and vegetables were collected from the market to study their post-purchasing shelf-life and
to identify the fungal types involved in samples rotting. Factors that affect samples’ shelf-life were also analyzed.
Results: A total of 73 fungal isolates were isolated and identified, with the highest percentage of Penicillium (21.9%)
followed by Rhizopus (17.8%). Interestingly, many mycotoxins producing and diseases inducing fungi were identified in
this study; this includes Rhizopus, Aspergillus, Penicillium, Alternaria, Fusarium, Cladosporium, Botrytis, Geotrichum,
and Colletotrichum. Statistical analysis shows that different fruits have significantly different shelf-life and different
predispositions for spoilage. In many cases, a strong relationship was shown between the fungal types isolated and the
country of origin of the fruit. Finally, the price of the commodity did not have a significant effect on its contamination level
nor did the market from which the sample was purchased. This indicates that the fruit displaying methods in Qatar do not
affect their contamination level.
Conclusion: The study is among the first reports about fungal types involved in fruits and vegetables rotting in Qatar and it
highlights the strong link between spoiling fungi and their country of origin.
Keywords: country of origin, fungi, post-harvest, shelf-life, spoilage.
Introduction
Microbiological food safety is a major economic
and public health concern nowadays. According to
the WHO, one in every 10 people become ill from
consuming contaminated food each year, a trend that
results in the death of 420,000 individuals annually
WHO [1]. Food contaminants consist of physical
agents, including pieces of metals or plastic, that enter
food during the packaging stage of manufacture, as
well as other chemical agents including heavy metals,
pesticides, and, most importantly, microbes [2,3].
Fruits are a major source of nutrients for humans
and animals, but it has been reported that, globally, around
45% of harvested fruits and vegetables are wasted every
year due to spoilage caused by contaminated growth
environments, inappropriate harvesting conditions,
unsafe handling and storage processes, and incorrect
methods of display [3]. Even though freshly harvested
vegetables and fruits are unavoidably contaminated with
Copyright: Saleh and Al-Thani. Open Access. This article is
distributed under the terms of the Creative Commons Attribution
4.0 International License (http://creativecommons.org/licenses/
by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit
to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made.
The Creative Commons Public Domain Dedication waiver (http://
creativecommons.org/publicdomain/zero/1.0/) applies to the data
made available in this article, unless otherwise stated.
Veterinary World, EISSN: 2231-0916
a variety of bacteria, fungi and other microorganisms.
However, molds in general and mycotoxin producers in
particular are the main cause of spoilage, especially in
products that are refrigerated in open boxes [4-6].
Microorganisms, including bacteria and fungi,
cause considerable economic losses by spoiling not
only harvested fruits and vegetables but also crops in
their fields. The identification of such spoilage microorganisms is a crucial step toward controlling them.
Some pathogenic strains specific to fruits are pathogenic to humans as well, especially those that produce
toxins [5,7]. The metabolites of many such microorganisms are heat stable, which suggests that they
remain in the food after heat processing and continue
to cause toxicity. Once mycotoxins are formed, it is
difficult to manage their quantities as they are stable
under storage conditions and particularly insensitive
to physical and chemical treatments. Therefore, the
best way to limit mycotoxin exposure is to stop them
from forming in the first place [6,8,9].
Different spoilage-causing microorganisms have
different nutrients requirements. Due to the variable
composition of fruits and vegetables, it is important
to determine the microbial hazards for each product
separately. In Qatar, the country imports over 90% of
its consumed food. Food security as one of the major
challenges of the modern world is mentioned as one
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of the pillars of Qatar’s National Vision 2030, which
places great importance on fungal contamination control. Products of great concern include cucumbers
and tomatoes, which are produced in large amounts
in Qatar and are among the most highly consumed
vegetables in the Middle East, as well as oranges and
strawberries, which are used in great quantities for the
production of fresh juices. Therefore, it is of significant concern to understand the spoiling agents behind
their shelf-life termination [10,11].
In this study, samples of cucumber, tomato,
strawberry, and orange were tested to determine their
shelf life and to identify spoiling agents, if found.
Factors that affect the rate of fungal spoilage in the
purchased samples were also analyzed.
Materials and Methods
Ethical approval
This study did not involve the use of live animals, and hence, ethical approval was not required.
Sample collection
Samples were collected during four trips which
took place between September 2017 and November
2017. All trips occurred on Saturday and samples
were collected between 10.00 am and 12.00 pm from
three large supermarkets in Qatar. At each market, a
sample was collected per available type of cucumber,
tomato, orange, and strawberry. Samples were handled aseptically, kept in sterile bags with a breathable
patch 44 cm×20.5 cm (Sun bag, transparent, SIGMAALDRICH, Montreal, QC), and were assigned serial
numbers. All necessary data regarding each sample
were collected including the product’s country of origin, its type, and the price per kg. Samples were kept
in the sterile bags and at a storage temperature approximating that of the supermarket until transferred to the
laboratory the next day.
Sample processing
The sample collection was kept individually in a
sterile and empty Petri dish with a sample number identifier. All samples were incubated at 25°C and observed
twice a day to determine when each would rot. When
a sample began to exhibit fungal hyphae growth, it
was removed from the incubator, at which point, the
observer noted the day as the end of the home shelf-life
of that particular sample. Hyphae were subsequently
collected using a sterilized needle and subcultures on
potato dextrose agar (PDA) [12]. The number of spoiling spots on each sample was counted as a measure of
contamination level. If more than spoiling spot color
and shape appear, each spot’s hyphae were cultured
separately. Rotten fruits were discarded in hazardous
waste and the inoculated PDA plates were separately
incubated at 25°C. The process continued for 10 days,
after which time, the experiment was completed.
Identification of isolated fungi
After 1 week of incubation, fungal isolates were identified using colonies and cell
Veterinary World, EISSN: 2231-0916
morphological features such as the thallus growth
pattern, pigmentation, conidiophore, and conidial
morphology [13]. Isolated fungi were identified using
cotton blue in lactophenol stain. A drop of the stain
was placed on a clean slide and a portion of the mycelia was placed on the stain using a sterilized needle
and forceps. A coverslip was then placed on the wet
mount and the slide was examined by a light microscope at various magnifications. The morphology
and characteristics of the conidia and conidiophores
were then used to classify the different types of fungus according to the standard taxonomic system [5].
Data were entered into the excel datasheet, pictures
were taken of the fungi on the PDA agar, and pictures
of each isolate under the microscope showing conidia
and conidiophores were taken.
Statistical analysis
Data were analyzed using SPSS statistical software, version 24 (IBM Corp., NY, USA). Chi-square
test and ANOVA were applied against an acceptance
limit of p<0.05. Chi-square was used to determine if
there were significant differences in the detection of
spoiling among the four samples type, the three collection markets, the eight countries of origin, and the
two levels of the countries’ economic conditions and
commodity price.
Results
Fungal isolates
Out of the 90 samples, 51 (56.7%) showed fungal growth within the experiment timeline (10 days).
Various types of fungus were isolated from different
fruits. Table-1 shows the number of various fungal
types isolated from each kind of fruit. A total of 73
fungal isolates were collected and identified, with the
highest percentage of Penicillium (21.9%) followed
by Rhizopus (17.8%). Different mycotoxins producing fungi were isolated in the study.
Samples contamination rates
Chi-square test was used to detect the factors
that significantly affect fruit spoilage: Sample type,
the market from which the samples were purchased,
and the sample’s country of origin. Our results show
that 100% of the collected strawberry samples became
rotten within the 10 day experimental timeframe followed by 81.25% of the cucumber samples. On the
other hand, 60% of the tomato samples became rotten
during the experiment, while only 20% of the oranges
showed fungal growth within the same time period.
The results of the Chi-square test indicate that the fungal-driven spoiling rates of the various fruits are significantly different (p=0<0.01).
Effect of displaying market on fruit spoilage
Samples were collected from three large supermarkets in Doha. A Chi-square test demonstrated no
significant difference among the different markets in
terms of the number of samples showing fungal spoilage within 10 days (p=0.87>0.05), which implies that
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contamination is country of origin related and not
induced in market.
Veterinary World, EISSN: 2231-0916
*Mucor was isolated from cucumber sample, Colletotrichum was isolated from orange sample, Geotrichum candidum was collected from a tomato sample
1
0
1
4
6
4
4
3
5
16
1
2
5
2
10
Cucumber
Orange
Strawberry
Tomato
Total
2
0
8
3
13
Cladosporium
Aspergillus
Rhizopus
Penicillium
0
0
5
2
7
4
1
0
5
10
5
0
0
0
5
1
1
0
4
6
16
30
14
30
90
Effect of fruits country of origin on fruit spoilage
Fruit type
Table-1: The number of various fungal types isolated from each kind of fruit.
Botrytis
Alternaria
Fusarium
Others*
Number of collected samples
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When testing for the effect of the country of origin on commodities’ fungal spoilage, the Chi-square
p-value obtained was 0.02 (p<0.05); however, the
Chi-square assumptions in this case were not valid
(10 cells have expected count <5%). Chi-square test
results of the comparison of the number of samples
showing fungal growth among samples originated
from different countries suggest that the country of
origin has an effect on the contamination of commodities, although significance could not be proven,
as more samples were needed to reach an adequate
level of statistical power. The effect of the country of
origin can be observed when analyzing the results;
for example, samples imported from the Netherlands
were highly contaminated with Penicillium when
compared to samples from other countries. On the
other hand, Penicillium is known to be more common
in citrus fruits. However, the data in Table-1 do not
demonstrate a significant difference between the number of Penicillium isolated from oranges and those
isolated from the rest of the fruits, which might link
Penicillium to the country of origin.
The data indicate also high concentrations of
Cladosporium in samples originating specifically
from Morocco. Interestingly, a total of 16 samples
of cucumber were collected from Iran (six samples),
Qatar (six samples), and Lebanon (four samples). Out
of the six locale samples, five were contaminated with
Fusarium, suggesting that most Fusarium isolates are
local in origin. Finally, it is worth mentioning that the
rate of occurrence of Aspergillus and Rhizopus is particularly high in samples originated from the USA.
However, this high rate might be more related to the
fruits’ nature than to the country of origin, as those
two fungal types were linked to strawberry infections
knowing that most of these fruit samples were of
American origin (data not shown).
Effect of the country of origin’s economy on fruit
spoilage
The various countries of origin of the samples
were divided into countries categorized as having a
developing economy and those with a developed economy (as based on the Department of Economic and
Social Affairs of the United Nations Secretariat). Chisquare test was again applied to determine whether a
countries’ economic classification affected the fungal
contamination frequency of their fruits. Although the
test returned a non-significant p=0.081 and >0.05,
Table-2 indicates that 49% of the samples originating
from developing economy countries were contaminated, while 67.6% of samples from developed economy countries showed fungal growth within 10 days.
The statistical results are likely to be biased by the
fact that different fruits were exported from specific
countries; for example, strawberries are more prone
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to spoilage than other fruits and, due to the nature of
their skin, tend to be produced in developed nations.
Effect of price of commodity on spoilage rate
The collected fruit samples ranged in price from
items that were on promotion, to very expensive fruit
types. Therefore, it is important to interrogate the
effect of the price of fruit on their home shelf-life to
understand if, in the market, low price reflects the
microbiological condition of the commodity or if it
is a reflection of the taste and/or probable variation in
the nutritional value. The average price per commodity was calculated by SPSS, as shown in Table-3.
High and low price categories were created by
considering fruits whose price was above or below the
Table-2: Number of samples originated from countries of
different economy and their contamination frequency.
Contamination
Economy
Total
Developed
Developing
12
25
37
27
26
53
No
Yes
Total
39
51
90
Table-3: Descriptive statistics of the prices QAR/kg of
different fruit types.
Sample type
Mean
n
Standard deviation
Cucumber
Orange
Strawberry
Tomato
Total
8.20
8.85
63.02
16.31
19.65
16
30
14
30
90
4.38
5.46
18.30
6.81
20.96
average for their category respectively. Chi-square test
was computed to assess the effect of price category
on spoilage rate. Chi-square results are for cucumber
(p=0.267>0.05), orange (p=0.232>0.05), and tomato
(p=0.296>0.05) indicate a non-significant effect. The
test could not be conducted on strawberries because all
samples were contaminated. In the three categories of
fruits tested, the data did not provide evidence that more
expensive fruits are less contaminated or last longer.
Instead, price variation may be a product of the quality
of the commodity, rather than its home shelf-life.
Number of fungal types per sample
Some fruits were found to be contaminated with
more than one, but no more than three, types of fungi
at once. Data were summarized in a boxplot and the
results indicate that strawberry samples contain the
greatest variety of fungi of all the fruits. This range
of contamination is due to the nature of the skin of
this fruit, which contains pouches that fungal spores
get stuck within. It should be noted that strawberries
were primarily contaminated with black molds, whose
spores can easily be transmitted by air. The cucumbers
data demonstrate the existence of some outliers, but
its median is at one fungal type per sample, whereas
tomatoes showed high specificity in terms of fungal
types and oranges did not have enough contaminated
samples to be included (Figure-1).
The P-P plot of the number of fungal types
indicates that the number of fungal types per fruit
sample follows a normal distribution (data not shown).
SPSS was, therefore, used to perform an ANOVA test
to compare the mean numbers of contaminant kinds
Figure-1: Box plot of the number of fungal contaminants by sample type.
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per sample type. The results (p<0.01) suggest that
fruits do significantly vary in the number of fungal
types they carry. Post hoc tests show that the main significant differences in the number of fungi are between
cucumbers and oranges, oranges and strawberries,
tomatoes and oranges, and tomatoes and strawberries.
Contamination level of various fruit samples
The level of contamination across different fruits
was assessed based on the number of spots shown on
each sample at the beginning of the rotting process.
Because each spot represents a spore, their number
reflects the level of contamination. The levels were
described as follows:
1. Undetectable contamination level: Zero spots
(within 10 days)
2. Low contamination level: 1-4 spots
3. Moderate contamination level: 5-10 spots
4. Heavy contamination level: Sample fully covered
with fungus
5. Detected by swab: Contamination was not visible,
but proven by swab culture.
Figure-2 summarizes the contamination levels of
each of the fruits. Strawberries exhibited the highest
levels of fungi per fruit; again, this may result from
the characteristics of its skin. Oranges exhibited a
high level of contamination across 13.3% of samples, whereas more than half of the cucumber samples
(56.25%) showed no hyphae growth by the end of the
10 days at all. However, the visibly bad condition of
the fruit motivated us to take a swab culture from them
on PDA, all of which demonstrated the growth of various fungi types. Finally, it is worth mentioning that
60% of the tomato samples were contaminated but
that most of those (53.3%) exhibited only a low spread
of contaminations per fruit, which can be explained by
the smooth, thick nature of the tomatoes’ skin.
The home shelf-life of various fruits
The time taken by a fruit sample to rot will vary
from 1 to more than 10 days. Based on the rotting
speed, samples were divided as follows:
1. Speed 1 samples: Very short home shelf-life,
rotten between 1 and 3 days
Figure-2: The percentage of various fruits that have undetected, low, moderate, heavy, and swab detected contamination
levels.
Figure-3: Percentages of various fruits that have very short, short, moderate, and long home shelf-life.
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2. Speed 2 samples: Short home shelf-life, rotten between 4 and 6 days
3. Speed 3 samples: Moderate home shelf-life,
rotten between 7 and 10 days
4. Speed 4 samples: Long home shelf-life, the
samples did not rot within the experiment time.
Strawberries experienced the shortest home shelflife, with all samples rotting within 3 days. This period
was followed shortly by cucumbers, of which 87.5%
of the samples were in a bad condition within 10 days.
About 40% of the tomato samples and 80% of the
orange samples remained in a good and appealing condition during the 10 days of the experiment (Figure-3).
Discussion
Fungi have always been a public health concern.
In 1992, a study conducted in Australia on packaged
cheddar cheese showed that mold infections were
tough to control as they were isolated from different
equipment in the cheese factory, fungi were also isolated from the air, curd, and whey. The most common
fungi isolated from the packaged cheese samples were
Cladosporium followed by Penicillium, which are
our most commonly isolated fungi [14]. Similarly, in
2001, Weidenborner determined the major source of
contamination for pine nuts as Cladosporium. A total
of 31 different species were isolated in the study, of
which 16 were potentially toxigenic [15].
Recent studies regarding fungal contamination
are conducted all over the world. A total of 117 isolates
of fungi were recovered from nuts and dried fruits in the
Washington D.C. area, including potential toxigenic
Aspergillus, Penicillium, Alternaria, and Fusarium
species. Similarly, the most common isolated fungi
type identified in a study by Tournas et al. [16] was
Aspergillus, while the most common mold in walnuts
was identified as Penicillium. In Brazil, a 2007 study
investigating toxigenic fungi on dried fruits identified
Aspergillus niger as the most common species from
a sample of 117 [17]. Both studies imply an affinity
between Aspergillus and dried fruits.
Similarly, a study of grapes conducted in Lebanon
identified a high level of contamination with various
strains of Aspergillus section Nigri. In addition, tests
of ochratoxin A (OTA) levels indicated low-level contamination of the isolates in 57.4% of cases which,
again, illustrates the risk to human health posed by the
toxins produced by Aspergillus species, the third most
isolated species in the present study [13].
Aflatoxin and OTA producing fungi are also of
major concern in cocoa production. During the chocolate production process but, in particular, during the
fermentation of the cocoa beans, molds contamination
is common [18]. In a study conducted in Brazil, in
2014, out of 356 chocolate samples tested, 303 (85.1%)
showed traces of OTA. Although the detected toxin
levels were within acceptable ranges, chocolate-based
products are widely consumed, especially by children, and the accumulative effect of low-level OTA
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consumption may cause severe health problems in
vulnerable populations, making the control of toxin-producing fungi of major importance [19].
While the orange samples considered in the present study displayed the highest level of contamination
with Penicillium, the previous study conducted on
sweet oranges in Nigeria found isolates of A. niger to
be the most numerous (27.5%) followed by Rhizopus
(22.5%) and Aspergillus flavus (17.5%) [20]. In close
consistency with our results, the second and third most
common spoiling agents of our study were isolated
in Uyo metropolis, Nigeria, from samples of cucumbers, carrots, cabbages, and onions. Approximately
one-third or 37.5% of the Nigerian samples showed
contamination with Rhizopus stolonifer and with
Aspergillus fumigatus, while A. niger was found only
in cucumber and onion samples, which constituted
25% of the overall number of samples [21]. Eight of
our 11 Botrytis isolates were isolated from the strawberry sample, which is consistent with a study conducted in Virginia USA on strawberries, which later
revealed that the most abundant fungi among the fruit
were Botrytis and Cladosporium [22].
In the Gulf region, studies conducted on fungal
contamination levels are few. A study conducted in
Bahrain on 17 types of imported spices showed that
black pepper and red chili have the highest fungal
contamination. The most encountered fungal type
was Aspergillus, which was isolated from four types
of spices followed by Penicillium, which was isolated from two types. Cladosporium, Rhizopus, and
Trichoderma were also frequently isolated [23]. In
Saudi Arabia, 520 samples of date Rutab were tested
for microbial spoilage. The two main spoilage-causing agents were Penicillium and Cladosporium [24].
Despite the various sample types, the results of the
two studies are in harmony with our results.
This study illustrates the high level of fungi present
in the food products that are consumed daily. However,
there are many steps to take that can help avoid human
exposure to such microorganisms and conserve
imported fruits and vegetables for longer periods of
time. Among the required steps are the implementation
of programs such as hazard analysis and critical control
point (HACCP) in places where food is processed and
produced. Programs such as HACCP help to establish
the critical control points used to monitor food quality continuously and they help to provide appropriate
training to food handlers at all food production stages.
Although such measures are costly, they are necessary
to ensure appropriate food quality control [25,26].
Conclusion
Food spoilage monitoring and spoiling agents’
identification is crucial steps in food management
programs. Food security is a global concern in both
developed and developing countries. The world population has increased from 1.5 to 6.9 billion between
1900 and 2000. This booming comes with an increase
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in food demand. Fresh fruits and vegetables microbial
spoilage causes huge economic losses every year in
Qatar and all around the world. Development of spoilage control methods requires first a good knowledge
of existing spoiling agents in each country and about
the factors that control their growth. It is clear in this
analysis that the displaying practices and the prices of
the commodities are not food spoilage affecting factors in Qatar, rather fresh produces country of origin
and locally produced crops require further attention.
9.
10.
11.
Authors’ Contributions
IS and RA conceived and designed the experiments and wrote the manuscript. IS performed the
experiments. Both authors read and approved the final
manuscript.
12.
13.
Acknowledgments
The authors wish to thank Dr. Mohammed AbuDieyeh at the Biological and Environmental Sciences
Department at Qatar University for his assistance in
identifying some of the isolated species and Mr. Ahmad
Hawi for his valuable input in the statistical analysis.
This study was partially funded by Biological and
Environmental Science Department of Qatar University.
14.
15.
16.
17.
Competing Interests
The authors declare that they have no competing
interests.
18.
Publisher’s Note
Veterinary World remains neutral with regard
to jurisdictional claims in published institutional
affiliation.
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