Hindawi

Journal of Food Quality

Volume 2022, Article ID 4141914, 24 pages
https://doi.org/10.1155/2022/4141914

Review Article
Microbial and Parasitic Contamination of Vegetables in
Developing Countries and Their Food Safety Guidelines

Richard Osafo ,1 Gadafi Iddrisu Balali ,2,3 Papa Kofi Amissah-Reynolds,4

Francis Gyapong,5 Rockson Addy,4 Alberta Agyapong Nyarko,4 and Prince Wiafe6
1
School of Health and Life Science, University of the West of Scotland, Paisley, UK
2
Department of Theoretical and Applied Biology, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana
3
Department of Sciences, SDA College of Education, Agona-Ashanti, Ghana
4
Department of Biological Sciences Education, College of Agriculture Education,
Akenten Appiah-Menka University of Skills Training and Entrepreneurial Development, Mampong-Ashanti, Ghana
5
Department of Biochemistry, Cell and Molecular Biology, University of Ghana, Legon, Accra, Ghana
6
Department of Physiology, College of Health Science, University of Ghana, Korlebu Campus, Accra, Ghana

Correspondence should be addressed to Gadafi Iddrisu Balali; balaligadafi@gmail.com

Received 30 January 2022; Revised 12 July 2022; Accepted 1 September 2022; Published 27 September 2022

Academic Editor: Efstathios Giaouris

Copyright © 2022 Richard Osafo et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

The safety of humans is of paramount importance in the vegetable production chain. Evidence of microbial and parasitic
contamination of these products poses a great threat to consumers. This is an emerging issue the world is battling, and it is still in
the process of unravelling. However, one of the contributing factors responsible for the rapid spread of these pathogens to millions
of people among other factors is the distribution of food in our food systems. The purpose of this study was to draw the attention of
producers, retailers, consumers, and various stakeholders to the occurrence and potential hazard of these organisms, their
contamination origin, and food safety protocols. Among the food system, vegetables play a major role, and their consumption has
increased as they form a larger portion of daily diets. This urge for healthy diets coupled with changing dietary habits and human
population explosion has therefore accelerated their production. This has resulted in parasitic and microbial contamination
gaining grounds in salad vegetables, and as such, a wide range of microbes such as Escherichia coli O157: H7, Listeria mono-
cytogenes, Salmonella spp., Shigella, and Staphylococcus, and parasites such as Giardia lamblia, Entamoeba coli, Entamoeba
histolytica, Cystoisospora belli, Toxoplasma gondii, Trichuris trichiura, and Ascaris lumbricoides have been isolated from them.
Therefore, major routes for salad vegetable contamination and prevention methods have been pointed out in this review article.
The topic of protective countermeasures will also be covered here in this review. Notwithstanding, several control measures have
been reported to be effective and efficient in removing or eliminating pathogens, including treatment of irrigation water and
fertilizers, use of disinfectants like vinegar and saltwater, irradiation, ozone, and bacteriophages. Though consumption of
vegetables and salads is encouraged due to their nutritional advantage, appropriate systems should be put in place to ensure
their safety.

1. Introduction has expanded the mass production of fresh vegetables [2].

This was anticipated to increase vegetable consumption by
In recent years, there has been an upsurge in vegetable roughly 25% by 2020 [3]. Hence, the consumption of vege-
production and consumption throughout the whole world; tables globally has increased due to their relatively low cost,
this is said to be twice its initial production weight of 30 high nutritious value, and convenience in preparation.
million metric tons in 2018 [1]. In developing countries like Vegetables are either eaten raw or cooked, and are essential in
Ghana, the initiation of programmes such as the current human nutrition as a result of their nutrient composition such
“Planting for Food and Jobs” by the Government of Ghana as dietary fibre, minerals (like iron, calcium, zinc, magnesium,
2 Journal of Food Quality

and phosphorus), and vitamins (like vitamins B, C, and K) [4]. According to the World Health Organization, vegeta-
Furthermore, some of these vegetables are processed into bles constitute the majority (86%) of the total market street-
ready-to-eat salads prepared by combining two or more vended foods during its survey [9]. They are processed into
vegetables such as cucumber, tomatoes, pepper, cabbage, vegetable salads and served in restaurants, in canteens, and
carrots, spring onions, and radishes. They are usually sold by as street-vended foods [11]. A survey conducted in Ghana
street vendors and in canteens, restaurants, and grocery stores revealed that of the 15,000 street food vendors in the capital
as they are served with foods like “waakye,” fried rice, jollof region, about one-third of them sell foods that utilize
rice, and plain rice. Despite the numerous advantages veg- ready-to-eat vegetable salads (mainly lettuce and/or cab-
etable consumption contributes to our well-being, the practice bage) as accompaniments [12]. This result corroborates
can adversely affect our health given if food safety practices with other studies which investigated foods sold in can-
are not carefully followed. This is because vegetables present teens and restaurants [13]. Since vegetable salads and salad
numerous avenues for adherence and invasion of dangerous vegetables play a major role within the food system, their
microbes or parasites during cultivation, harvesting, pro- security has become a priority globally as they are faced
cessing, and marketing [5]. A consequence of vegetable with the risk of contamination [7]. The increased demand
contamination is the associated outbreaks (such as giardiasis, has exerted pressure on everyone from the producers to the
amebiasis, cyclosporiasis, and cryptosporidiosis) which have consumers to actively improve the safety of vegetable
been responsible for the higher rate of morbidity and mor- consumption [14]. Farmers in developing countries espe-
tality in various parts of developing countries [6]. While the cially in Africa who are usually into vegetable farming are
rate of vegetable and salad consumption is accelerating, there also faced with threats ranging from poor water quality and
is a tendency for increased microbial and parasitic contam- infertile soil to pest infestation, and hence the need for
ination leading to many other foodborne illnesses. However, more research into microbial and parasitic contamination
few reviews such as this have been conducted to integrate [15].
studies on this subject for proper surveillance and measures to
combat the incidence. Hence, the need to draw the attention
of producers, retailers, consumers, and various stakeholders 3. The State of Foodborne Illness Outbreak
to the epidemiology of microbes and parasites found in salad
vegetables and vegetable salads, their contamination origin, With a surge in the supply and consumption of vegetable
and food safety protocols in developing countries have ne- salads and salad vegetables in developing countries, there has
cessitated the conduct of this review. been an increasing threat of microbial contamination as a
result of the conditions under which they are been produced
2. Production, Distribution, and Consumption and sold due to poverty [17]. Street-vended food remains the
Trend of Vegetables and Vegetable Salads topmost source of foodborne sickness due to the high
prevalence of different microorganisms pointed out in
Globally, the agriculture sector from 1980 to 2004 expe- numerous research works [12]. In South African regions, for
rienced a surge in vegetable production by 94%, with instance, purchased and examined vegetables from the
population increase being a significant contributing factor streets of Gaborone and Botswana harboured a significant
[7]. Since that period, there has been a continuous surge in level of Bacillus cereus, and this suggests a threat of food-
production within the last eighteen years (2000 to 2018) borne illnesses [18]. Interestingly, around 1990, about 12%
from 682.43 to 1088.9 million metric tons though there of food-related diseases were specifically attributed to fruit
was a slight drop between 2017 and 2018 (Figure 1) [8]. and vegetable consumption [7]. This is not different in the
Among developing countries, interestingly, the produc- recent era (2018) where foodborne outbreaks in Ghana were
tion of vegetables is widely distributed in various conti- linked to the presence of Vibrio spp., Salmonella spp., and
nents including countries like India, Iran, Vietnam, other microbes in vegetables and salads [19]. In the sub-
Nigeria, Egypt, and Mexico, which form part of the top ten sequent year (2019), diarrhoeal diseases (many of which are
producers of vegetables in the world (Figure 2) [8]. Due to foodborne) were the second top cause of death in low-in-
this increase in the production, the consumption of veg- come countries (Figure 4) [8].
etables in recent years has also accelerated in different In Saudi Arabia, numerous outbreaks of foodborne
regions with Asian countries being the highest consumer, diseases have consistently been revealed. 31 foodborne
and then Europe, Northern America, Oceania, and Africa disease outbreaks representing 251 cases were accounted for
[1]. Additionally, the consumption rate of vegetables in 2006. From that report, a larger part (68.9%) of the af-
specifically in developing countries increased by 69% from fected individuals became ill after eating vegetables and
1961 to 2013 (Figure 3) [8]. However, due to a multitude of salads that were commercially made, and Salmonella species
factors, many people in South Asian developing countries was the highest pathogenic agent followed by Staphylococcus
such as India prefer to consume raw vegetables as com- aureus [20]. Likewise, foodborne disease outbreaks (typhoid
pared to fast foods [9]. In other African developing fever, food poisoning, meningitis, pneumonia, and gastro-
countries, vegetables such as cabbages, onions, tomatoes, enteritis) in India from 1980 to 2016 were linked to ready-to-
and lettuce are affordable, accessible, and readily available eat foods harbouring Staphylococcus aureus, Salmonella
in the markets; hence, their consumption have increased as species, Escherichia coli O157: H7, Yersinia enterocolitica,
compared to fruits [10]. and Listeria monocytogenes, with Salmonella species again
Journal of Food Quality 3

1200

1000

Production in million metric tons

800

600

400

200

0
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
2017
2018
Years
Figure 1: Volume (in million metric tonnes) of vegetables produced globally [8].

600

500

400
Million metric tons

300

200

100

0
China

India

USA

Vietnam

Nigeria

Egypt

Mexico

Russia

Spain
Turkey

Countries
Figure 2: 2019 top ten leading producers of vegetables [8].

being the most common cause [21]. The epidemiological and surveillance on listeriosis in Nigeria, research has shown
investigation also revealed the yearly prevalence of Salmo- its effect on pregnant women and infants [26]. South Africa
nella typhi to be much higher in developing countries like recently experienced severe outbreaks of listeriosis (820
Pakistan, India, and Vietnam, representing 451.7, 214.2, and cases) [27] and salmonellosis thought to be related to
21.3 cases, respectively, per 10000 individuals as opposed to vegetable consumption [28].
China (15.3 cases/100,000) [22]. A significant number of Furthermore, parasites have been shown to play a major
findings every year from Sri Lanka, Nepal, India, Maldives, role in the occurrence of foodborne illnesses. Foodborne
Pakistan, Bhutan, and Bangladesh have indicated shigellosis parasites are endoparasites comprising protozoans, trem-
as the most detrimental disease leading to high fatality and atodes (flatworms or flukes), nematodes (roundworms),
morbidity [22]. Concerning listeriosis, the disease initially and cestodes (tapeworms). Parasitic diseases have been
occurred periodically in Asia [23]; however, it is presently prevalent in tropical countries, but factors like climate
spreading widely across developing regions [24]. This pe- change, global warming, and globalization of food supply
riodic disease is typically linked to consuming foods like are extending them to other non-tropical regions. Ent-
milk and vegetables [25]. Though there are limited reports amoeba histolytica, which is responsible for amebiasis, was
4 Journal of Food Quality

45

40

35

30
Kilogram (kg)

25

20

15

10

0
1961
1963
1965
1967
1969
1971
1973
1975
1977
1979
1981
1983
1985
1987
1989
1991
1993
1995
1997
1999
2001
2003
2005
2007
2009
2011
2013
Year
Figure 3: Trend in vegetable consumption per capita in the least developed countries, 1961 to 2013 [8].

80

70
Death per thousand population

60

50

40

30

20

10

0
HIV/AIDS

Stroke

Malaria

Tuberculosis

Birth asphyxia and birth trauma

Lower respiratory infections

Diarrhoeal diseases

Ischaemic heart diseases

Preterm birth complications

Road injury

Cause of death
Figure 4: 2019 top ten leading causes of death in low-income countries [8].

reported to be the cause of illness among fifty million [29]. It is thought that vegetables washed in contaminated
patients and also resulted in a hundred thousand deaths in water are a major contributing factor to foodborne parasite
developing countries across South America, Africa, and the outbreaks [1]. Not only can these outbreaks be caused by
Indian sub-continent [25]. Furthermore, toxoplasmosis familiar foes but there are also recent cases of emerging
(caused by Toxoplasma gondii), one of the most common infections arising from contaminated vegetables. For in-
foodborne diseases, sickens thousands globally each year stance, in 1977, the first human case of cyclosporiasis was
Journal of Food Quality 5

reported [30]. Similarly, twenty states of the USA in 1990 presence of these microorganisms were also found when
and 2004 were affected by cyclosporiasis, and this was vegetables used for salad preparation and the salads itself
caused by a new member of the coccidian family, Cyclo- were analysed concurrently [51, 52].
spora cayetanensis [30]. Interestingly, these outbreaks were Contamination was reported in salads in some studies,
linked to lettuce, basil, and raspberry consumption [25]. It and the total bacterial count was found to be above the
is observed that the outbreak of foodborne illness has been national standard count of <5.0 log10 cfu/g [12, 53] as
overlooked or un-investigated, and will gain attention after stipulated by the Ghana standard authority [16]. In those
a major health incidence. Under such circumstances, investigations, the bacterial count was 5.13 log10 cfu/g [53]
identifying the risk factors and controlling the outbreak and 6.3 ± 0.78 log cfu/g [12], but a standard count was
will be impossible [31]. Therefore, instituting foodborne recorded in another study in Johannesburg [54]. Similarly,
disease observations would be essential as it will help to these pathogenic bacteria were found in an investigation in
generate data on the issue, determine the extent of con- Ghana [12]. One of the major contributing factors to several
tamination, and determine the kind of food to be con- microbial contaminations is the source of the vegetables
taminated in the future, and in other preventive measures used for salad preparation. Moreover, most street food
[25]. vendors purchase vegetables for salads from open-aired
markets and subject them to poor handling due to prefer-
4. Microbial Assessment of Salad Vegetables ential differences of buyers as well as improper washing
methods, thereby leaving some microbes at the point of
4.1. Vegetables. Table 1 displays evidence of different species consumption [55]. Hence, Penicillium spp., Staphylococcus
of microbes such as Escherichia coli O157: H7, Listeria aureus, Escherichia coli O157: H7, coagulase-positive
monocytogenes, and Salmonella spp. isolated from salad staphylococci, Cladosporium, and Salmonella spp. were
vegetables including lettuce, cabbage, and cucumbers. In observed in fresh-cut vegetables and ready-to-eat salads
2022, for instance, a study indicated the existence of mul- purchased from open-air markets [52, 56].
tidrug-resistant Listeria monocytogenes in fruits and vege-
tables in South Africa [24].
4.2.2. Vegetable Salads from Restaurants and Canteens.
Listeria spp. is a pathogen that causes listeriosis in animals
4.2. Vegetable Salads. Due to the growing need for work and
and humans. It is transmitted to susceptible individuals
humans’ busy schedules, most individuals in a bid to satisfy
when foods contaminated with manure from ruminants are
their nutritional requirements have resorted to the most
ingested [7]. Listeria has been isolated from vegetable salads,
convenient ways to access foods. They do not have enough
salad vegetables, and coleslaw restaurants, and this may
time to cook, and that paves way for the consumption of
present a threat to human health [57]. In this study, 95.8% of
already prepared foods which are usually served with ready-
the total 355 vegetable samples were contaminated with
to-eat vegetable salads. These are sold in open markets, in
Listeria spp. Out of the Listeria spp., 4.1% were Listeria
grocery stores, as street-vended foods, and in restaurants.
monocytogenes. In classifying the samples following the
Notwithstanding, an increased level of consumption is
infection rate, 4.7% of salad vegetables showed contami-
worth noting because these foods have been indicated as a
nation preceded by coleslaw (4.4%), with traditional vege-
source of several pathogenic infections with contamination
table salads being the lowest (1.7). Concerning the salad
originating from each point in the supply chain including
vegetables, cabbage (8.5%), lettuce (6.2%), and tomatoes
retailers, processors, and/or consumers.
(4.3%) were highly contaminated, with carrot and cucumber
being the least (2.2%) [57].
4.2.1. Vegetable Salads from Street Vendors and Open A comparable study in India indicated the presence of
Markets. The street food industry is known to satisfy the Listeria spp. in 73% of salads studied, while 20% of the
everyday food needs of a large number of inhabitants of samples harboured Yersinia spp. A higher range of bacterial
developing countries by serving different kinds of dishes that (106–108 cfu/gm) and mould (104–107 cfu/gm) counts were
are affordable and easily accessible [43]. The preparation of also observed in ready-to-eat salads. On the other hand,
these ready-to-eat street foods takes place either at home or fresh vegetables used to prepare the salads exhibited the
on the street, and is sold along the street; hence, their presence of Listeria, Yersinia, total bacteria, yeast, and
consumption requires no further processing [44]. These moulds. However, higher bacteria and mould counts in
foods are now popular in developing countries due to salads than in freshly washed vegetable ingredients denote
economic changes, population growth, and urbanization that cross-contamination into salads probably occurred
[44]. Consumption of street foods raised concern about during/after the preparation of salads [58].
potential food poisoning outbreaks due to improper han- Other important bacteria isolated from ready-to-eat
dling and unhygienic practices among street food vendors salads from restaurants are Clostridium difficile and Heli-
[45]. One of the most essential sources of pathogen con- cobacter pylori [59, 60]. The study reporting the presence of
tamination is vegetable salads which are commonly served Helicobacter pylori in both traditional and commercial
along with other foods [46]. This is because several mi- vegetable salads was the first research paper in a developing
croorganisms of public health concern have been identified country to make such a finding [60]. The prevalence rate of
in vegetable salads prepared in the streets [46–50]. The Helicobacter pylori in salads from these two sources was
6 Journal of Food Quality

Table 1: Microbes isolated from notable vegetables.

Type of salad Reference
Microbes isolated
vegetable number
Escherichia coli O157:H7, Proteus spp., Enterobacter spp., Staphylococcus aureus, Salmonella spp.,
Lettuce Klebsiella spp., Listeria monocytogenes, Pseudomonas spp., Acinetobacter spp., Micrococcus spp., [32–35]
Bacillus, yeast, and moulds
Escherichia coli O157:H7, Pseudomonas spp., Erwinia spp., Salmonella spp., Listeria
Cabbage [33, 36, 37]
monocytogenes, Staphylococcus, and Enterococcus
Escherichia coli O157:H7, Erwinia spp., Staphylococcus aureus, Enterobacter spp., Citrobacter spp.,
Carrot Klebsiella spp., Lactobacillus spp., Pseudomonas spp., Vibrio spp., Proteus spp., Aspergillus spp., [33, 34, 36, 38]
Rhizopus spp., and Enterococcus
Escherichia coli O157:H7, Staphylococcus aureus, Enterobacter spp., Klebsiella spp., Lactobacillus
Cucumber [34, 36, 38]
spp., Pseudomonas spp., Vibrio spp., Aspergillus spp., and Shigella spp.
E. coli, Pseudomonas spp., Enterobacter spp., Staphylococcus spp., Streptococcus spp., and
Onion [36, 37, 39, 40]
Cryptosporidium spp.
Citrobacter spp., Enterobacter spp., Klebsiella spp., Lactobacillus spp., Pseudomonas spp.,
Tomatoes Staphylococcus spp., Vibrio spp., Aspergillus spp., Rhizopus spp., Penicillium spp., Shigella spp., [33, 38, 41, 42]
Escherichia coli O157:H7, Salmonella spp., Listeria spp., and Enterococcus
Italicized words indicate scientific names of microrganisms (Genus and Species).

significantly variable, wherein improperly cleaned leeks, toxin-producing E. coli pathotypes) have been identified in
lettuce, and traditional salads were the highly contaminated the vegetables [69]. In this study, vegetables were contami-
products. 9.56% of salad samples were found contaminated nated with E. coli strains, and less than half of the strains were
when the culture method was applied for isolation, while the classified as diarrhoea-causing E. coli pathotypes. 26.7% of
polymerase chain reaction (PCR) technique also revealed salad samples were contaminated with E. coli pathotypes, 15%
10.86% contamination. (two enterotoxigenic E. coli and one enteropathogenic E. coli)
Furthermore, a study conducted in Nigeria, which took from spinach salads, and 25% (three enterotoxigenic E. coli,
three months, revealed that salads from restaurants har- one enteropathogenic E. coli, and one Shiga toxin-producing
boured twelve nonhemolytic bacterial pathogens, including E. coli) isolated from mixed salad [69]. These vegetables could
Bacillus spp., Klebsiella oxytoca, and Escherichia coli O157: be a route for the emergence of bloody diarrhoea and he-
H7 [61]. The prevalence of microbial contamination in some molytic uremic syndrome which have been of high prevalence
vegetables from Tamale in Ghana [62] reflected in the salads in Africa, particularly in children and HIV patients, caused by
sold in that same area such that 73.3% and 76.7% of salad these E. coli pathotypes [70]. Apart from the above-men-
samples were contaminated with Salmonella spp. and Shi- tioned pathogens, P. aeruginosa, K. pneumoniae, Strepto-
gella spp., respectively [63]. coccus spp., and Bacillus cereus were also isolated from ready-
In and around several University campuses in developing to-eat salads offered with waakye on and across the University
countries, pathogens causing several foodborne illnesses have of Ghana campus, and from eating places around the campus.
been reported. Concerning E. coli and Salmonella, the ma- The majority of the vegetable salads harboured Bacillus cereus
jority (80%) of vegetable salads (Kachumbari) served in (93.3%) and Escherichia coli O157: H7 (96.7%), whereas
canteens around Egerton University, Kenya, contained an Staphylococcus aureus was absent [71]. This prevalence on our
average of 3.047 log10 cfu/g Escherichia coli O157: H7, while campuses suggests the need for various departments in charge
70% of the samples tested positive for Salmonella [64]. This of food safety to strengthen safety guidelines in order to
confirms the findings of a similar study wherein vegetable prevent foodborne illness among students.
salads (Kachumbari) harboured Escherichia coli O157: H7 but
not Salmonella. Additionally, sampled vegetable salads were
indicated as unsafe for consumption and hence detrimental to 4.2.3. Comparing Microbial Contamination of Vegetable
human health as a result of Campylobacter spp. and staph- Salads from Street Vendors and Restaurants/Cafeteria.
ylococci contamination [65]. In another study, Escherichia coli There has been a notion that foods purchased from res-
O157: H7 was found in over 80% of the product, but the taurants are much safer than those sold along the street.
topmost contamination was observed in street food salads However, microbial contamination has been reported in
(4.23 log10 cfu/g) [66]. Salads from a University campus in salad prepared in restaurants and canteens though on a
Bangladesh were also contaminated with Escherichia coli lower side than products from the street [72–75]. A study
O157: H7, Salmonella spp., and Staphylococcus spp. Monte found street market salads to contain a higher bacteria
Carlo simulation calculation on risk assessment showed that load than those from fast food markets [72]. The vege-
the risks of Staphylococcus spp., Salmonella spp., and E. coli tables used for the preparation of salad in the above study
infection yearly are 100% on average due to frequent salad however harboured a lower number of bacteria, some of
consumption in this region [67, 68]. Furthermore, different which include Staphylococcus aureus, Citrobacter freundii,
E. coli strains (enterotoxigenic, enteropathogenic, and Shiga and Neurospora crassa. However, Corynebacterium spp.
Journal of Food Quality 7

found in salad samples originated from street markets However, the underlying factors that warrant the reduction
[72]. Similarly, all fresh vegetable and ready-to-eat veg- and multiplication of pathogens should be further
etable salads purchased from restaurants in another study investigated.
were satisfactory regarding E. coli contamination, but
street-vended samples yielded unsatisfactory levels [73].
Then again, 32% of salad samples had Salmonella spp. and 4.2.5. Evidence of Antibiotic and Multidrug-Resistant Bac-
17% had helminth eggs and thermotolerant coliforms in teria from Vegetables Salads. Ingestion of vegetables and
street-vended and cafeteria salads in similar research [74]. salads contaminated with bacterial strains is associated with
Conversely, isolated Salmonella, Enterobacter aerogenes, several diseases and can even lead to death. It is therefore
Escherichia coli O157: H7, and Shigella spp. in another paramount to use antibiotics for proper treatment; however,
study were higher in salads from restaurants than in those there has been an evolution of resistance against these an-
from homes. Bacterial contamination reported was not tibiotics by most pathogenic bacteria, resulting in the loss of
surprising because the same vegetable salads analysed in drug effectiveness. In previous years, the resistance of
another experiment isolated 36 bacterial species [76]. The pathogenic microorganisms to multiple drugs was limited to
presence of Shigella spp. in the above study corroborates hospitals due to the frequent application of antimicrobial
another finding which detected Shigella spp. in tested agents. In the recent era, antimicrobial resistance is found in
salads before and after the enrichment [77]. The results other environments including food products like vegetables.
found in restaurants and home-made salads are consistent This situation is highly alarming, given that antimicrobial
with a lower state of hygienic practices of service workers, resistance can often spread via horizontal gene transfer [82].
quality of water, and processing of vegetables as well as Research in Nigeria revealed the existence of several bacterial
observance of other precautionary measures in the res- antibiotic resistances in different fast food industries, and
taurants than the homes where enhanced care is taken this has led to a spike in illness due to the consumption of
[75, 76]. Therefore, there is a need to improve food safety contaminated raw vegetables [83].
knowledge attitude and practices, and foods served in Salads made from these vegetables and sold in fast-food
restaurants and cafeterias where food products are con- industries harboured bacteria (25) of different species (6)
sidered to be highly safe. which were highly (>50%) resistant against eleven of the
twelve antibiotics tested. Among the antibiotics, the highest
resistance rates against Pseudomonas spp., Bacillus spp.,
4.2.4. Relationship between Microbial Prevalence in Vegetable Escherichia coli, Proteus spp., Enterobacter spp., and Aero-
Salads and Time. In developing countries, most individuals monas hydrophila were Augmentin (96%), Cotrimoxazole
usually consume foods such as “waakye” (rice and beans) (92%), and nitrofurantoin (88%), with streptomycin (44%)
and plain rice in the morning in order to increase their being the least [83], and this agrees with another study [72].
energy for work [78]. However, the prevalence of microbes Furthermore, Escherichia coli O157: H7 found in vegetable
has been reported to vary at different times in a day. In salads and salads vegetables were resistant to more than five
several investigations, the highest level of pathogen con- antibiotics, thus revealing the multidrug-resistant capacity
tamination in vegetable salads has been in the afternoon. of Escherichia coli O157: H7 [59, 69].
Moreover, a high load of bacteria was recorded in raw-mixed Apart from Escherichia coli O157: H7, two bacteria
vegetable salads obtained in Ghana for 15 days [11], and this species, Salmonella spp. and Staphylococcus aureus, found
was above the standard (Log10 3.0 cfu/g) given by the World in ready-to-eat vegetable salads showed a varied resistance
Health Organization (WHO) [79]. The bacteria identified rate (25.71% to 81.82%) against Chloramphenicol, Oflox-
comprised Streptococcus faecalis, Pseudomonas spp., Shigella acin, Dovid, Siprosan, gentamicin, Tarcvid, Ciproxin, and
spp., and Salmonella typhi. The rate of contamination was pefloxacin [84] with an overall multiple resistance rate of
higher in afternoon samples than samples taken in the 35.29%. Comparably, potential human pathogens, Staph-
morning [11], and this confirms the findings of a similar ylococcus aureus and Klebsiella aerogenes, from vegetable
investigation [49]. salads exhibited antibiotic resistance profiles at a range of
Other researchers [50, 61, 80] have added their finding 25.71% to 81.82% [85]. Whereas another study [86]
that vegetable salads sold in the afternoon have higher revealed the ability of Staphylococcus aureus to show 83%
contamination rate than those sold in the morning. Amala resistance against co-amoxiclav and 75% against penicillin.
and Agha [80] isolated Staphylococcus aureus (45%), Klebsiella aerogenes was fully (100%) ampicillin-resistant
Escherichia coli O157: H7 (36%), and Bacillus spp. (18%). In and against other antibiotics such as imipenem and
the study by Uwamere et al. [61], a substantial difference amoxicillin/clavulanic acid [86]. Other pathogens isolated
existed between morning and afternoon dishes in terms of from vegetable salads that showed multidrug resistance
the rate of bacterial contamination, but another investiga- were Listeria monocytogenes, Proteus vulgaris strain, Cit-
tion [50] had no significant difference although the after- robacter freundii, Bacillus thuringiensis strain, Staphylo-
noon bacteria load was higher. The two principal coccus aureus, and Serratia marcescens strain [57, 87].
contributing factors for bacterial growth associated with Specifically, Listeria monocytogenes were highly resistant to
fresh produce are storage temperature and pH. Hence, the ampicillin (92.9%), oxacillin (85.7%), gentamicin (21.4%),
low pH values and the short shelf life of morning salads and ciprofloxacin (14.3%). This resistance outcome of
could have been responsible for the low bacterial load [81]. microbes in this study indicated that microbes were
8 Journal of Food Quality

resistant to more than one antibiotic and that most of them Ancylostoma duodenale, and Ascaris lumbricoides), and
(64.3%) showed antimicrobial resistance against more than cestodes (Taenia spp., Moniezia spp., and Fasciola spp.) were
four antibiotics [57]. These results suggest that vegetables identified. About a third (32%) was contaminated with at
and salads may serve as a vehicle for bacteria that are least one parasite. Among the twelve genera of parasites
resistant to multiple antibiotics. recovered, Giardia lamblia, Entamoeba histolytica, and
Moniezia spp. were 6.7%, 6.4% and 4.2%, respectively. Other
5. Parasitic Contamination of Vegetables parasites found were Trichuris trichiura (3.8%) and Ent-
and Salads amoeba coli (3.5%), with the rest recording low prevalence
(<2%) [108].
5.1. Vegetables. Multiple types of research have assessed the Another report by Tefera et al. [109] revealed that 208 out
occurrences of parasites in vegetables worldwide and have of 360 vegetable salads and salad vegetables were infected
recovered several parasites such as Ascaris lumbricoides, with several strains of parasites, resulting in an overall
Entamoeba histolytica, and Giardia intestinalis [88–90]. This contamination rate of 57.8%. The prevalence rate of the salad
contamination is also evident in various parasitic isolates (16.8%) was greater than that of the vegetables. Concerning
from vegetable salads, as shown in Table 2. Many studies in the parasites, the prevalence is arranged in descending order:
Ethiopia, Ghana, and Iran also have consistently compared Strongyloides (21.9%), Toxocara spp. (14.7%), Cryptospo-
parasite prevalence in vegetables found in open-aired ridium spp. (12.8%), H. nana (8.3%), G. lamblia (7.5%),
markets and supermarkets where the former recorded a high A. lumbricoides (6.7%), E. histolytica/dispar (5.3%), Cyclo-
occurrence of human parasites [6, 104, 105]. The potential spora spp. (5.0%), and H. diminuta (1.4%). It was worthy to
cause is the unhygienic nature of the environment which note that samples obtained from open markets were more
serves as a medium for the growth, multiplication, and frequently contaminated (84.6%) than those purchased from
transfer of parasites [106]. However, in some developing grocery stores (15.4%) [109].
countries like Ghana, there are only a few available reports
highlighting parasitic contamination of fresh vegetables with
many of the studies centred on bacterial and chemical 6. Major Sources of Contamination
contamination.
6.1. On-farm Routes
5.2. Salads. A recent investigation into top causes of mor- 6.1.1. Irrigation Water Sources. (1) Wastewater: since ac-
bidity at the outpatient department by the Ghana Health cessibility to potable water for vegetable production is a big
service revealed intestinal worm infestation to be the 7th challenge among farmers, one other way to irrigate their
leading cause and has gradually increased from 2.1% to 3.6% produce is the reuse of wastewater [94]. This practice is
[107]. Based on these reports, it was suspected that con- rampant among farmers in developing countries where
sumption of street-vended salad may be contributing to the about 10% of the population is engaged in urban agri-
increasing prevalence of helminthiasis in Ghana. In Ashanti culture [110]. The wastewater comprises liquid wastes re-
Mampong, Ghana, field studies have reported risk to human leased from homes, farmlands, institutions, and
health as a result of parasitic contamination in salad veg- commercial and industrial companies which are usually
etables and ready-to-eat vegetable salads. In that work, combined with surface water, groundwater, and rainwater
parasite prevalence in the salad was the highest (66.0%), but [111]. However, wastewater that can be applied either in the
the individual vegetables had a greater number (16) of raw, or partially or fully treated state may harbour path-
species diversity than the salads (10) [2]. In the vegetables ogens, pesticides, toxins, organic particles, or inorganic
and salads, Ascaris lumbricoides and Giardia lamblia particles [111].
recorded varying levels of prevalence. While Ascaris lum- In South Africa, a high load of Escherichia coli O157: H7
bricoides was the highest (26.94%) succeeded by Giardia and Vibrio spp. were recovered from effluents of two
lamblia (19.93%) and Toxocara spp. (1.48%); in the vege- wastewater treatment facilities [112]. However, due to the
tables, Giardia lamblia was more prevalent (24.17%) in the costly and time-consuming nature of the treatment proce-
salad followed by Ascaris lumbricoides (19.17%) and Toxo- dure, only about 10% of wastewater is adequately treated in
plasma gondii (0.8%). Additionally, other parasites, namely, developing countries [113].
Fasciola spp., Moniezia, Toxocara spp., Trichuris trichiura, Unfortunately, insufficiently treated wastewater har-
and Entamoeba histolytica, were recovered from both veg- bours a high burden of pathogenic microbes [114]. One
etables and salads. litre of community sewage can harbour thousands of
The above study agrees with a similar finding in Ghana pathogens such as Entamoeba histolytica (4500), Salmo-
wherein Giardia lamblia in the salad was the also most nella spp. (7000), Shigella spp. (7000), and Ascaris lum-
prevalent but the overall prevalence of parasites in the salad bricoides (600) [115]. Therefore, the application of
was low (32.0%) [108]. In that report, out of 313 ready-to-eat wastewater during vegetable production should be criti-
vegetable salad samples analysed, 99 (32%) harboured more cally looked at by the necessary stakeholders as this raises
than one parasite. Twelve parasite species, including pro- public health concerns, especially where vegetables are
tozoa (Giardia lamblia, Entamoeba coli, Entamoeba histo- eaten uncooked or improperly cooked.
lytica, Cystoisospora belli, and Toxoplasma gondii), (2) Surface water, groundwater, and rainwater: surface
nematodes (Enterobius vermicularis, Trichuris trichiura, water bodies include rivers, streams, ponds, and dams.
Journal of Food Quality 9

Table 2: Parasites isolated from notable vegetables.

Type of salad Reference
Parasites isolated
vegetable number
Cryptosporidium spp., Microsporidia spp., Cyclospora spp., Ascaris spp., Toxocara spp., Giardia
spp., Hymenolepis nana, Ostertagia circumcincta, Cooperia spp., Fischoederius cobboldi, Fasciola
Lettuce [32, 91–97]
hepatica, Entamoeba histolytica, Giardia intestinalis, Entamoeba coli, Trichuris trichiura,
Balantidium coli, Hookworm, and Trichostrongylus spp.
Balantidium coli, Fischoederius cobboldi, Fasciola hepatica, Entamoeba histolytica,
Cabbage Diphyllobothrium, Ascaris lumbricoides, cryptosporidium spp., Giardia intestinalis, Strongyloides [92–95, 98, 99]
stercoralis, Giardia lamblia, Entamoeba coli, and Trichuris trichiura

Strongyloides stercoralis, Ascaris lumbricoides, Cryptosporidium spp., Entamoeba histolytica,

Carrot [6, 93, 95, 99]
Giardia lamblia, Entamoeba coli, Trichuris trichiura, and Cyclospora cayetanensis
Cucumber Fasciola hepatica, Entamoeba histolytica, and cryptosporidium spp. [92, 93]
Cryptosporidium spp., Microsporidia spp., Ascaris spp., Toxocara spp., Trichuris trichiura,
Green Onion [91, 97]
Hookworm eggs, and Taenia spp.
Giardia lamblia, Entamoeba histolytica, Strongyloides stercoralis, Trichuris trichiura, Ascaris
Onion [6, 98, 100]
lumbricoides, Cyclospora cayetanensis, Cryptosporidium parvum, and Hookworm ova
Cryptosporidium spp., Entamoeba histolytica, Giardia lamblia, Entamoeba coli, Trichuris trichiura,
Tomatoes Isospora belli, Cyclospora cayetanensis, Cryptosporidium parvum, Fasciolopsis buski, Hookworm [6, 33, 93, 95]
ova, and Taenia spp.
Ascaris spp., Trichuris trichiura, Hookworm eggs, Taenia spp., Taenia/Echinococcus, H. nana,
Radish Trichostrongylus spp., Giardia lamblia, Fasciola hepatica, Entamoeba coli, Blastocystis hominis, and [97, 101]
Dicrocoelium dendriticum
Ascaris lumbricoides, Giardia intestinalis, Entamoeba histolytica, Giardia lamblia, Entamoeba coli,
Spinach Trichuris trichiura, Entamoeba coli, Trichostrongylus spp., Toxocara spp., H. nana, Taenia spp., and [94, 95, 102]
Isospora spp.
Ascaris spp., Trichuris trichiura, Hookworm eggs, Taenia spp., Hymenolepsis nana, Trichostrongylus
Parsley spp., Entamoeba spp., Giardia lamblia, Trichostrongylus spp., Fasciola hepatica, Blastocystis [97, 103]
hominis, and Dicrocoelium dendriticum
Rocket Entamoeba histolytica, Entamoeba coli, Giardia lamblia, Cocci spp., and Balantidium coli [96]

Globally, surface water is the topmost and most extensively rainwater is an extremely useful and most convenient source
exploited water for irrigation but is highly open to patho- of water for domestic use and irrigation [121]. However, the
genic infestation as opposed to other water sources [116]. method of collection, that is, from rooftops or runoff on the
Contaminants such as heavy metals, and carcinogenic and ground which is then collected into containers or tanks, can
organic substances from rural, urban, and industrial facil- affect the quality of the water. For example, faeces from
ities can enter bodies of water. Furthermore, these water animals (such as bird’s faeces) and other debris as well as
sources can harbour several pathogenic microorganisms pathogens found in the soil such as Salmonella spp. may
such as Salmonella spp. and Listeria spp. [117]. These can be contaminate the harvested rainwater [121].
released into farmlands and produced during irrigation, (3) Prevalence of pathogens in irrigation water: water on
which therefore can affect the safety of food and consumers farmland coming from irrigation systems or rainfall can
[118]. serve as a potential vehicle for pathogen transmission onto
At a time when surface water bodies have dried up, fresh produce [122, 123]. These water sources are usually
groundwater is another alternative and inexpensive source contaminated with enteric microbes or parasites which come
of water for domestic and agricultural production. This is from faeces, sewage, soil, and other material introduced into
because the aquifers help to protect the water reserves during them [124]. Rainwater from rooftops has been reported to
drought [119]. Groundwater is usually suggested as water for harbour pathogenic bacteria like Salmonella spp., Aero-
irrigation of farm produce as compared to surface water, and monas spp., Listeria spp., Campylobacter spp., E.coli (faecal
this is due to the lower rate of contamination arising from indicator), and Legionella spp. [125]. This was confirmed by
the enclosed nature. Microbes like Clostridium spp., Sánchez et al. [126], who asserted that the presence of these
Staphylococcus, and E. coli were identified from borehole microorganisms is detrimental to the security and quality of
water in Kenya [120]. Since the occurrence of contamination vegetables which is not intensively treated before con-
in groundwater is usually minimal, they are relatively safe sumption. Twenty-three parasite species including eggs of
microbiologically for agricultural purposes [119]. Ascaris lumbricoides, Entamoeba histolytica, and Hymeno-
Research has elaborated that in rural regions especially lepis species, among others, were isolated from different
where there are few or no pipe-borne or boreholes, collected irrigation waters located in five African regions [127].
10 Journal of Food Quality

Several studies conducted in Morocco [128], Ghana [129], contamination. This is a result of the direct access farmers
and Ethiopia [94, 130] have demonstrated that irrigation have to soil such that some (93%) worked barefooted,
water could affect the safety of fresh vegetables due to the while others (86%) have direct hand contact with con-
high level of microbial and parasitic contamination. Thus, taminated soil, which leads to oral contamination during
the application of irrigation water contaminated with faecal hand-to-mouth events [66].
coliforms (CF), total coliform bacteria, Bacillus cereus, etc.
was also observed to be present in vegetable samples
[131, 132]. 6.1.2. The Entry of the Pathogen into the Soil and Produce via
Furthermore, lettuce is a significant vegetable and forms Manure. The recent increase in population in developing
a major part of vegetable salads. However, the application of countries has resulted in an upsurge in food production to
irrigation water containing helminth eggs and larvae on ensure food security. However, vegetable production
lettuce resulted in their contamination. The helminth eggs especially is facing many constraints like land pressure
identified included Ascaris lumbricoides, Trichuris trichiura, and low soil fertility [140]. Therefore, farmers have now
Hookworm, Enterobius vermicularis, Strongyloides larvae, intensified crop (vegetable) cultivation by introducing
and Taenia spp. [133]. Ascaris lumbricoides and Hookworm mineral and organic fertilizers to their crops in order to
were the most prevalent microbe in both irrigation water satisfy the increased demand by consumers. For centuries,
and lettuce samples [133]. Compared with the World Health the farmer has utilized animal manure of which the
Organization (WHO) standards, the faecal coliform and majority (60%) comes from poultry with the rest (40%)
helminth egg levels in irrigation water and lettuce samples from cattle, and this is practiced even frequently in
exceeded the recommended levels [133]. Levels of helminth present days [141]. However, the intense application of
eggs were substantially reduced after washing in that water manure from cattle, poultry, and other animal sources put
containing vinegar as compared to water without vinegar the soil, water, crops, and humans at risk of pathogen
[133]. Similarly, protozoan parasites (E. histolytica cysts, infection [142]. This is because several disease outbreaks
microsporidia spores, and Cryptosporidium oocysts) were have been linked to the consumption of vegetables that
identified in vegetable washing water and vegetable irriga- had been directly or indirectly contaminated with infected
tion water in a similar investigation [134]. In line with the animal manure [143]. The isolation of E. coli and faecal
above study, species of helminth eggs, Hymenolepis coliforms from sampled vegetables in three studies in-
diminuta, Ascaris lumbricoides, Strongyloides larvae, and dicates faecal pollution [2, 142, 144]. Furthermore, several
Fasciola hepatica, were also isolated from water and lettuce studies [136–138, 145] have also investigated how the type
samples [135]. of manure applied determines the extent of contamina-
Treatment of wastewater is one of the reported strategies tion. Some of these studies [136–138] revealed that the
to minimize the risk of microbial contamination. This is ability of a pathogen to survive was greater in vegetables
because research found microbes (like faecal coliform, co- grown with manure from poultry as opposed to manure
liform bacteria, and E. coli) and parasites (such as Ascaris from cattle, whereas another study [145] found an op-
lumbricoides and Strongyloides stercoralis) in wastewater posite result. Contaminated manure has been reported to
which was higher than that recorded on the vegetables affect the quality of soil, and this subsequently contam-
(lettuce, Amaranthus, and cabbages) [62]. Also, significantly inates the vegetables as pathogens found in soils reflected
higher bacteria counts were observed in surface water which in the vegetables [146]. Strongyloides stercoralis, Taenia,
subsequently contaminated salad vegetables (spinach, to- and Entamoeba spp. were observed in raw manure of
mato, green chilli, radish, and cabbage) than partially treated animal origin and vegetables [147]. Then also, fifteen
wastewater from sewage treatment plants [136]. However, different species of parasites, including nematode (9)
wastewater treatment could not eliminate pathogens as species were concurrently identified from the soil, irri-
Javanmard et al. [137] reported parasitic contamination of gation water, and vegetables produced, and these mi-
treated wastewater (53.8%) and vegetable (41.7%) samples crobes emanated from animals and humans. From the soil
irrigated with this water. Also, intestinal helminth ova samples were isolated Geo-helminth eggs, including
(Trichuris trichiura, Ascaris lumbricoides, and hookworms) Trichuris trichiura, Strongyloides, Ascaris lumbricoides,
were isolated from raw wastewater (83.3%) and treated Enterobius vermicularis, and hookworms [2]. This sug-
wastewater (68.2%), soil (68.6%), and vegetables (44.2%) in gests contamination from human faeces as a result of
the study area [137]. practices like open defecation among farmers and the use
Agricultural soil is highly susceptible to pathogenic of improperly composted manure. Similarly, the recovery
contaminations originating from irrigation water, animal of Toxocara spp. and Moniezia spp. from vegetables,
faeces, sewage, and effluents [138]. Then apart from the vegetable salads, and soils implicates the use of animal
naturally contained microbes in the soil, Klutse [139] faeces as sources of fertilizer [148]. When bovine faeces
reported that soils irrigated with wastewater have an was used as fertilizer, E coli was isolated from 17 samples
increased level of pathogenic microbes such as Staphy- (including 8 samples of soil and 9 samples of vegetables)
lococcus spp., Enterobacteriaceae, Clostridium spp., [148].
Pseudomonas spp., and Bacillus spp. However, it has also Interestingly, several pathogenic microbes tend to thrive
been pointed out that though irrigation water is more in the manure for a long-time, and this is due to specific
contaminated, the soil remained a major route for elements including physiochemical properties (pH of soil
Journal of Food Quality 11

and manure, moisture content, compost treatment tech- of contamination in washed vegetables was linked to the
niques, air circulation, soil type, and the degree of fertilizer medium (well and river water) in which the samples were
(manure) application) [149, 150]. E. coli O157: H7 and washed, wherein they were contaminated with several
Salmonella have been shown to live longer in farmyard parasites [160]. In the removal of pathogenic parasites,
manure under anaerobic conditions as well as in moist clay Alsubaie et al. [161] attributed running water from taps to
soil with a lower temperature [146, 151]. However, several perform a similar role to normal saline; therefore, the use of
methods such as composting, dry heating of pellets, and running taps and proper draining of the wash water should
alkaline stabilization, among others, are accessible for the also be encouraged instead.
treatment of manure before they are being applied. At a Normally, the water used for the washing procedure is
temperature of 55°C for 3 days, composting is usually suf- also utilized for salad preparation, and if the water is not
ficient to destroy bacteria, whereas pelleting is more clean, there can be contamination in the prepared salad.
favourable for the treatment of poultry manure [138]. Assessment of water quality and vegetable salads from a
restaurant in a study revealed a high level of coliform, faecal
coliform, Vibrio spp., and Salmonella spp. in both the water
6.1.3. Intruding Animals on Farms. Domestic or wild ani-
and salad samples. Salmonella spp. and Vibrio spp. were
mals moving into farmlands can result in vegetable con-
resistant to Cephalexin, Amoxicillin, and Cephradine [162].
tamination before harvest [152]. This is because several
The occurrence of coliforms in salads could be associated
outbreak investigations have been associated with free-
with cooks not engaging in enhanced sanitation, and the use
moving animals intruding into farms or cross-contamina-
of contaminated water to cleanse equipment like cutting or
tion originating from faeces of a neighbouring animal farm.
slicing machines resulting in cross-contamination. Most
Unfortunately, a lot of these wild and untamed animals
cooks also during salad preparation use their uncovered
harbour several parasites causing zoonotic diseases of hu-
hands, potentially transferring harmful pathogens into the
man importance [153]. Similarly, houseflies have been found
food. Similarly, the predominant population of coliforms,
to transfer E. coli O157: H7 in cattle [154] and spinach farms
Salmonella spp., Listeria monocytogenes, E. coli, and Bacillus
[155]. The contamination of tomatoes by Salmonella was
cereus, were found concurrently in prepared salads, worker’s
attributed to the movement of some of these animals such as
hands, and cooking equipment in a study [163]. This in-
mice and opossums onto production sites. It has been in-
dicates the probable transfer of microbes between prepa-
dicated that some bacteria such as Campylobacter spp. and
ration surroundings and ready-to-eat foods. However,
E. coli O157: H7 originating from these animals can spread
coliforms identified in vegetable salads are not surprising
in the agricultural environment [156]. In Ghana, the
because vegetable irrigation water, as well as manure utilized
identification of Toxocara spp., Giardia lamblia, and Mon-
as fertilizers, have been reported to harbour coliforms and
iezia spp. in farm soil and salad vegetables originating from
other enterobacteria [164].
droppings of dogs and ruminants is indicative of free-
Furthermore, improperly washed vegetables can result in
moving animals into production sites [2].
the contamination of vegetable salads, and this has been
noticed in several studies [156, 157]. Among these studies,
6.2. Off-Farming Routes Orozco et al. [156] noticed contamination variation between
vegetables that were cleaned with pure water, germicide, and
6.2.1. Impact of Washing Procedure and Hygienic Practices. vinegar as well as the uncleaned ones. Contamination of
Washing is one of the hygienic practices done to remove dirt, nematodes larvae was discovered in 82.5% of the uncleaned
bacteria, and parasites on vegetable surfaces. Washing of group. Additionally, 32.5%, 12.5%, and 0.5% of vegetables
vegetables is of utmost importance and therefore encour- cleaned with pure water, vinegar, and germicide, respec-
aged. The level of microbial and parasitic contamination tively, were also infested with nematodes. This showed that
usually depends on the quality of water used, together with the rate of parasite recurrence was significantly higher in
the kind of washing procedure performed. However, some of vegetables cleaned with pure water than in the germicide and
the vegetable sellers in some study areas use the same water vinegar groups. Washing with soap has also been indicated
in washing all vegetables [157]. This will lead to the transfer to have a lesser effect on the reduction of microbial and
of pathogens to uncontaminated ones if the water used is not parasitic contamination [165]. In that, the majority (43%) of
safe and the same wash water is repeatedly used. Most parasites and bacteria were identified in vegetables used with
vegetables washed before sales and displayed on tables had soap plus water, whereas those washed with pure water were
more geohelminths contamination than those that were not lesser (40.6%). Some isolated parasites and bacteria include
washed [158]. Conversely, another study reported more Giardia lamblia, Taenia spp., Enterobacter aerogenes, Tri-
parasites in unwashed produce before selling than in washed chocephalus spp., and Ascaris lumbricoides [165].
produce [159]. However, contamination in unwashed veg- In a one-year study, intestinal parasites (Entamoeba
etables in this study was facilitated by the environment in histolytica/dispar, Ascaris lumbricoides, Toxocara spp.,
which they were displayed. Most of them were on the floor, Hymenolepis nana, Dicrocoelium, Echinococcus, Fasciola,
and it is known that bacterial and viral contamination can Giardia lamblia, Entamoeba coli, and Trichostrongylus) were
take place on the floor together with flies that can act as a identified from unwashed (63.7%), traditionally washed
vector for several microorganisms like Toxoplasma gondii (49.1%), and standard washed vegetables (36.9%) [166].
and Cryptosporidium parvum [159]. Additionally, the source Comparing similar works in other developing countries, it
12 Journal of Food Quality

Table 3: Highlights on pathogens identified among various developing countries.

Reference
Country Salad ingredients Microbes/parasites identified
number
Africa
Shigella, Escherichia coli O157:H7, Bacillus spp., and
Ghana Cabbage, tomato, onion, and lettuce [63]
Salmonella spp.
Lettuce, cabbage, onion, cucumber, and Escherichia coli O157:H7, Staphylococcus aureus, Klebsiella
Ghana [48]
tomato spp., and Bacillus spp.
Salmonella typhi, Shigella spp., S. faecalis, and Pseudomonas
Ghana Raw mixed vegetable salads [11]
spp.
Bacillus spp., Klebsiella spp., Aeromonas spp., Escherichia
Ghana Salad (leaves and fresh vegetables) [53]
coli O157:H7, and Citrobacter spp.
Ghana Salad (leaves and fresh vegetables) Salmonella spp. and Helminth eggs [74]
Giardia lamblia, Entamoeba coli, Entamoeba histolytica,
Cystoisospora belli, and Toxoplasma gondii, Trichuris
Cucumber, carrot, onions, tomatoes, and
Ghana trichiura, Ascaris lumbricoides, Enterobius vermicularis, [108]
cabbage
Ancylostoma duodenale, Taenia spp., Moniezia spp., and
Fasciola spp.
Giardia lamblia, Ascaris lumbricoides, Moniezia spp.,
Entamoeba coli, Toxocara spp., Taenia spp., Fasciola
Ghana Cabbage, lettuce, carrot, and green pepper [2]
hepatica, Enterobius vermicularis, Trichuris trichiura, and
Toxoplasma gondii
Nigeria Vegetable salad Listeria monocytogenes [57]
Mucor spp., A. fumigatus, Aspergillus niger, Neurospora
Nigeria Carrot, lettuce, cabbage, and cucumber crassa, Proteus vulgaris, Staphylococcus aureus, and [72]
Pseudomonas
Escherichia coli O157:H7, Staphylococcus aureus, Salmonella
Nigeria Vegetable salads [84]
spp.
Bacillus spp., Pseudomonas spp., E. coli, Proteus spp.,
Nigeria Ready-to-eat vegetable salads [83]
Enterobacter spp., and Aeromonas hydrophila
Aeromonas spp., Serratia species, Pseudomonas spp.,
Corynebacterium, Klebsiella spp., Escherichia coli,
Nigeria Fresh vegetable salads [47]
Lactobacillus, Staphylococcus, Aspergillus spp., and Rhizopus
spp.
Nigeria Vegetable salads Enterobacter spp. and Streptococcus spp. [46]
Serratia spp., Citrobacter spp., Proteus spp., Staphylococcus
Nigeria Cabbage, lettuce, carrot, and cream [87]
spp., and Bacillus spp.
Acinetobacter spp., Bacillus spp., Pseudomonas aeruginosa,
Proteus mirabilis, Staphylococcus epidermis, Micrococcus
Nigeria Vegetable salads luteus, Enterobacter aerogenes, Serratia marcescens, [61]
Klebsiella pneumoniae, Klebsiella oxytoca, and Citrobacter
freundii
Ethiopia Vegetable salads Salmonella spp. and Escherichia coli O157:H7 [50]
Ivory Coast Tomatoes, onion, cucumber, and lettuce E coli, Enterobacteriaceae, and Salmonella [75]
Kachumbari (dhania, onions, tomatoes, and
Kenya Salmonella spp. and Escherichia coli O157:H7 [64]
chilli)
Onion, lettuce, carrot, tomatoes, cabbage, Escherichia coli O157:H7, Campylobacter spp., and
Kenya [65]
chilli, coriander, and green capsicum Staphylococcus spp.
Cucumber, carrot, onions, tomatoes, cabbage,
Egypt Shigella, Salmonella, and Staphylococcus aureus [167]
and parsley
Arugula, coriander, parsley, celery dill, lettuce,
Egypt Escherichia coli O157:H7 and Salmonella [73]
cucumber, tomato, green pepper, and mint
Asia
Pakistan Lettuce, tomato, onion, cucumber, and carrot Escherichia coli O157:H7 [69]
Escherichia coli O157:H7, Shigella spp., Citrobacter spp.,
Pakistan Vegetable salads Pantoea spp., Bacillus species, Klebsiella spp., Enterobacter [86]
spp., and Pseudomonas aeruginosa
Cladosporium spp., Penicillium spp., Alternaria, Escherichia
Lettuce, coleslaw, cucumber, carrot, and
Iran coli O157:H7, Salmonella spp., Geotrichum, Trityracium, and [56]
tomato
Aspergillus
Iran Vegetable salads Helicobacter pylori [60]
Journal of Food Quality 13

Table 3: Continued.
Reference
Country Salad ingredients Microbes/parasites identified
number
Lettuce, cabbage, tomato, cucumber, and
Iran Escherichia coli O157:H7 [59]
carrot
Yeast, Staphylococcus aureus, Escherichia coli O157:H7, and
Iran Vegetable salads [68]
parasitic eggs
Iran Lettuce Shigella spp. [77]
Yeast, mould, E coli O157:H7, Salmonella, and
Iran Mixed fresh cut vegetable salads [52]
Staphylococcus aureus
India Ready-to-eat green vegetable salads Listeria spp. and Yersinia spp. [58]
Saudi Tabbouleh, Fattoush, Hummus, Mutabbel, and Escherichia coli O157:H7, Shigella spp., Salmonella spp., and
[76]
Arabia Caesar E. aerogenes
Pseudomonas spp., Bacillus cereus, Acinetobacter, Serratia
Saudi Tabbouleh, Fattoush, Hummus, Mutabbel, and marcescens. Klebsiella spp., Enterobacter spp., Kluyvera
[168]
Arabia Caesar cryocrescens, Enterobacter spp., Pantoea spp., and
Escherichia coli O157:H7
Bangladesh Cucumber, tomato, and carrot E coli, Staphylococcus spp., and Salmonella spp. [67]
Latin America and the Caribbean
Mexico Vegetable salad samples Salmonella [169]
Lettuce, tomato, onion, cucumber, carrot,
Mexico spinach, mushrooms, watercress, wheat E coli, faecal coliform, and diarrhoeagenic E coli pathotypes [170]
sprouts, and radish
Lettuce, carrot, cabbage, spinach, collard green,
Brazil Staphylococcus aureus and Salmonella [171]
and watercress
Kale, cabbage, lettuce, onion, parsley, chicory,
Brazil spinach, arugula, watercress, carrot, collard Listeria monocytogenes and Salmonella [172, 173]
green, and escarole
Cabbage, kale, lettuce, spinach, parsley, and
Brazil Cronobacter spp. [174]
collard green
Balantidium coli, Giardia spp., Ascaris lumbricoides,
Brazil Lettuce [175]
Entamoeba spp., and Strongyloides stercoralis
Chile Vegetable salads Listeria monocytogenes [176]
Italicized words indicates scientific names of microrganisms (Genus and Species).

was found that the contamination rates in the above research contamination can enter humans. Pathogenic microor-
are higher than the findings from other countries (Table 3), like ganisms could be transferred from contaminated soil or
Libya [88], Egypt [90], and Nigeria [177]. In Kenya, however, produced in workers’ hands. In other instances, workers
parasitic contamination of unwashed vegetables increased harbouring infectious microbes could transfer them to
significantly (75.9%) as compared to the reduced level of produce [181]. Then also, harvesting knives can serve as
contamination observed in washed vegetables [178]. In con- contamination vectors during cross-contamination of mi-
formity with this research [166], soil-transmitted helminth crobes from infected soil to vegetables. For example,
infestation in standard washed vegetables (1.2%) and in tra- trimming and coring of lettuces after harvest can lead to
ditionally washed vegetables (3.2%) was also indicated by plant contamination [182]. Moreover, the environment
Nawas et al. [162]. In contrast, Fallah et al. [179] isolated in- where these vegetables are handled including machinery for
testinal parasites in unwashed (32.6%), traditionally washed processing could also be an important route of vegetable
(1.3%), and standard washed (0%) vegetables in Shahrekord, contamination [183].
Iran. Despite the findings of these investigations, Salavati et al. In an observational study, vegetables were displayed
[166] explained that standard washing procedures cannot on unhygienic sacks, and unsold ones were stored in
utterly eliminate the parasite from the vegetables. It should be uncontrolled states in the market or backyard of homes,
noted that the identification of parasites in standard washed resulting in bacterial and parasitic contamination of these
vegetables is probably because disinfectant solutions are ca- vegetables [184]. Six bacteria species were isolated in the
pable of completely killing worm eggs, cysts, and larvae, but the previous study, with Staphylococcus aureus being the
remaining dead agents in the corresponding vegetables are still highest, while Serratia marcescens was the least. Fur-
detectable via light microscopy [166, 180]. thermore, ten parasitic protozoans and helminths were
discovered, with Balantidium coli being frequently de-
tected and found in all samples together with Entamoeba
6.2.2. Processing. Manipulation of vegetables after harvest is spp. Interestingly, lettuce (25.4%) recorded the greatest
a major concern in the farm-to-fork chain. During pro- level of infestation, with the lowest being green pepper
cessing, there are several ways through which pathogenic (8.5%) [184].
14 Journal of Food Quality

6.2.3. Storage and Distribution. Several risk factors are as- Furthermore, the temperature of cars and the cooling period
sociated with the presence of enteric pathogens on vege- tend to proliferate pathogens when fresh vegetables are
tables during storage. Some of which include relative transported by consumers [193]. At home, undertaking food
humidity, gaseous composition of the atmosphere, storage hygiene practices like hand-washing before handling fresh
temperature, and the presence of nutrients, bacteria, or produce is important [188]. Kitchen sink, sponges, and
antimicrobial compounds [185, 186]. Hence, at the point of dishrags are another substantial and familiar reserve for
storage, an intervention to reduce the multiplication and pathogenic microorganism [188]. Therefore, the number one
activity of human pathogens on the products is by storing point of call should be educating retailers on excellent food
them at an appropriate refrigerated temperature. This is safety practices together with consumers on how to handle
because depending on the temperature range, the shelf life and process vegetable and vegetable salads in other to
and survival of microbes on the surface of vegetables can protect produce from contamination.
extend Listeria monocytogenes, for instance, multiply slowly
at temperatures above 3.8°C [187]. 7. Food Safety Guidelines
At home, cross-contamination is expected to occur if
domestic refrigerated vegetables are stored together with other 7.1. Strategies of Minimizing Microbial and Parasitic
foods that have been contaminated. In developing countries, Contamination. Whole vegetable and vegetable product
consumers usually store vegetables in all-purpose refrigerators contamination occurs at any point from planting to con-
together with other foods that have varying temperature sumption. Unfortunately, there have been no potent anti-
ranges due to financial constraints [188]. However, if they are microbial treatments to efficiently eliminate pathogenic
not routinely cleaned, they may serve as a source of harmful microbes and parasites [14]. However, the extent of con-
organisms. Furthermore, the spread of bacteria and mould is tamination is usually linked to the environmental conditions
also predicated on refrigeration units located in warehouses; under which the produce is grown and produced. Therefore,
therefore, routine disinfection of air filters and refrigeration programs such as “Good Agricultural Practices (GAP) and
systems is required [189]. If contamination takes place in the an in-plant food safety program such as Hazard Analysis and
storage area, the whole facility should be cleaned and dis- Critical Control Point (HACCP)” at the preharvest level are
infected to reduce any potential pathogens [190]. major techniques to minimize threats to food safety [194].
Julien-Javaux et al. [181] and Gil et al. [190], from a food
safety standpoint, suggested key factors that should influ-
6.2.4. Retail Food Services and Consumer Handling. The ence the choice of cultivation sites at the preharvest level.
foodservice industry receives the majority (60%) of fresh- Factors that should be considered include the closeness of
cut produce, while the remaining (40%) goes into the retail the farm site to livestock farms or industrial facilities, prior
market. A significant cause of foodborne diseases has been land use, and landscape as a potential for water and soil
attributed to contamination by food service workers during runoff [195]. Another important factor is the establishment
outbreak studies [191]. This is thought to be a result of the of sanitary facilities that are positioned away from the
frequency with which workers have an unguarded hold on production environment coupled with producers’ education
fresh produce during preparation and distribution in food on proper hygiene is essential to avoid cross-contamination
service and retail facilities [163, 192]. Higher bacterial of pathogens onto produce [190, 195]. Then again, the safety
contamination was observed in takeout vegetable salads of irrigation water is necessary to prevent contamination of
kept in packages than in those prepared and served at the produce, soil, and working equipment and machinery that
restaurant, suggesting potential cross-contamination should be maintained in sanitized condition [190, 195].
[163, 192]. Those studies recorded a high prevalence of However, plants cultivated close to the soil from which we
Gram-negative and positive bacteria in salads, and this was get fresh vegetables consumed raw should not be irrigated
in correlation with bacteria found on cooking utensils, with sewage or untreated water. This is because it could be a
cutting boards, and serving spoons [163, 192]. Further- route through which Escherichia coli O157: H7 enters the
more, most vendors do not take precautions during veg- fruit via the leaves [196]. The use of either manual or me-
etable salad preparation as consumers reported the chanical harvest during processing together with containers
occurrence of food poisoning after consumption [11]. Since for collecting produce should be done in a way to reduce the
these places do not utilize techniques designed to kill risk of potential contamination coming from soil, workers,
microorganisms, the occurrence of microbes in fresh water, or machine surfaces [190, 195].
produces is expected to be influenced by the hygienic During the postharvest period, good handling practices
conditions of food workers. Hence, retailers should have a during processing are critical. Processing tends to facilitate
defined procedure to examine and accept only fresh pro- the growth of pathogens when there is an alteration of
duce that attains the ideal standard. vegetable colour, nutrients, and water loss as a result of
Apart from the contamination originating from retailers mechanical injury, and hence the need for proper treatment
in retail joints, consumers also play a major role in the [172]. This indicates the importance of a well-controlled
contamination of vegetables. During sales, consumers de- layout across every production point. At this stage, one must
liberate on buying fresh vegetables by touching them, and consider several interventions consisting of physical,
this process could lead to cross-contamination if the buyer is chemical, and biological treatments that minimize con-
contaminated as a result of poor hygienic practices [184]. tamination, prolong life span, and enhance product quality
Journal of Food Quality 15

Table 4: Food safety legislation in some developing countries (Nigeria, South Africa, Ghana, Ethiopia, and Ivory Coast) [215].
Ministries, departments, and agencies involved in
enforcement and monitoring (MDAs not in any particular
Country Legislation
order concerning the enforcement of food laws for each
country. Mandates and functions overlap)
Counterfeit and Fake Drugs and Unwholesome Processed
Federal Ministry of Health
Food Decree (Act No. 25 of 1999)
National Agency for Food and Drug Administration and
Food and Drug Agency
Control (Amendment) Decree 1999 (No. 19 of 1999)
Food and Drugs (Amendment) Decree 1999 (No. 21 of 1999) Food and Drug Administration and Control (NAFDAC)
Nigeria National Agency for Food and Drug Administration and
Standards Organization of Nigeria (SON)
Control Decree 1993 (No. 15 of 1993)
Public Health Ordinance Cap 164 of 1958 National Codex Committee
The Standards Organisation of Nigeria Decree, No. 56 of 1971 Standards Organization of Nigeria (SON)
The Animal Disease Control Decree, No. 10 of 1988
Federal Ministry of Agriculture
The Marketing of Breast Milk substitute Decree, No. 41 of 1990
Regulations relating to the labelling of alcoholic beverages (No.
Ministry of Health
109 of 2005)
Regulations governing general hygiene requirements for food
Ministry of Health
premises and the transport of food of 12 July 2002
Agreement between the European Community and the
Republic of South Africa on trade in spirits - November 2002 Dept. of Health and SABS
Meat Safety Act, 2000
Foodstuffs, cosmetics and Disinfectant, Act No. 54 of 1972 Dept. of Agriculture
Health Act No. 63 of 1977 Ministry of Health
South
Standards Act No. 29 of 1993 SABS
Africa
Food, Drugs and Disinfectant, Act No. 13 of 1929 Dept. of Trade and Industry
Trade Metrology Act No. 77 of 1973 Dept. of Trade and Industry
Regulations on Food Establish & Export/Import Customs and Excise Division
The International Health Regulations Act, 1974 (Act 28 of
Ministry of Health
1974)
The Medicines and Related Substances Act, 1965 (Act 101 of
1965) Wine and Spirits Control Act
Ministry of Health
Regulations governing general hygiene requirements for food
premises and the transport of food (G. N. No. R.918 of 1999)
Food and Drugs Law (P.N.D.C.L. 305B, 1992) Food and Drugs Board
Standards Decree (N.R.C.D. 173, 1973) Ghana Standards Board
General Labelling Rules, 1992 (L.I. No. 1541, 1992) Food and Drugs Board
Ghana
Ghana Standards Board Certification Mark Rule, LI 662,1970 Ghana Standards Board
Pest and Plant Disease Act 307, 1965 (L.I. No. 1541, 1992) Plant Protection and Regulatory Services
Pesticides Act 528, 1997 Ministries of Health, Food and Agriculture and Trade
Quality and Standards Authority of Ethiopia Establishment
Proclamation (No. 102/1998) Emergency Food Security
Ethiopia Emergency food security reserve administration
Reserve Administration Establishment Council of Ministers
Regulations (No. 67/2000)
Decree No. 86–454 establishing the power of the government to
Ivory
the municipalities and to the city of Abidjan on veterinary Ministries of Finance, Rural Development
Coast
public hygiene measures

as well as its safety during processing vegetables into veg- chlorine-based compounds, ozone, electrolyzed water, or-
etable salads [197, 198]. Physical decontamination tech- ganic acids, modified atmosphere packaging, refrigeration,
niques involving irradiation, ultraviolet (UV), and high and atmospheric cold plasma discharges or plasma-activated
pressure have been used to deactivate microbes and para- water have been employed in intervention in recent times
sites. Studies have revealed UV’s efficacy to destroy and/or [202, 203]. Washing is an important process that removes
slow down the development of microorganisms, and in- dirt and soil, reduces microbial load, and prevents cross-
crease shelf life, quality, and nutritional benefit of food contamination to some extent; however, the addition of
products [199]. The application of biological treatments such sanitizers such as chlorine has facilitated the action [204].
as bacteriocins, bacteriophages, or protective cultures has Chlorine is the most commonly used sanitizer in washing
also been reported [198]. The use of bacteriophages in recent procedures due to its inexpensiveness and effectiveness
years has gained ground to suppress microbes present in against several pathogens. Notwithstanding, pathogen sen-
carrots and tomatoes [200, 201]. High doses of chlorine, sitivity varies; Listeria monocytogenes have higher resistance
16 Journal of Food Quality

against chlorine than E. coli O157: H7 and Salmonella spp. partially attributed to changes in increased dietary habits
[205]. It has also been reported that it is detrimental to leading, to increased patronage of foods sold outside homes
human health; hence, other alternatives such as chlorine of which vegetable and vegetable products form a greater
dioxide, electrolyzed water, hydroxide peroxide, and ozone part. Microbes are found everywhere, but vegetables have
have been employed [70, 196]. The efficacy of ozone to demonstrated their higher susceptibility to being con-
eliminate microbes has been reported to be higher than taminated with these microbes. As such, almost any ready-
treatments that make use of chlorine and organic acid [206]. to-eat vegetable and salads have been infested with mi-
Additionally, it helps to improve the sensory qualities of crobes originating from the field of cultivation, produce
produce such as lettuce [206]. Increased ozone concentra- processing, handling, or storage. This has accelerated the
tion in the atmosphere is harmful to human health; outbreak of several foodborne diseases. Since there is an
therefore, more research is needed regarding the efficient use increased need for healthy and quality products, it is es-
of ozone treatment [207]. sential and possible to minimize pathogens in vegetable and
vegetable salads by utilizing various methods. At the
preharvest level, the first step is to educate farmers on the
7.2. Biochemical and Molecular Methods for Isolating, Iden- threat posed by using contaminated water, fertilizers, hu-
tifying, and Characterizing Pathogens. Applying robust man faeces, and untreated fertilizers. Therefore, treatment
techniques to identify, count, and characterize microor- of sources of irrigation water and organic fertilizers should
ganisms is a major step toward understanding the risk as- be done to reduce microbe contamination at the highest
sociated with microbial and parasitic contamination as well level. Then also individuals involved in the production
as further mitigating measures to ensure food safety. Di- continuum from cultivation to consumption comprising
agnostic techniques employed in molecular biology and farmers, packers, and carriers should be trained on hygienic
microbiology such as ELISA, magnetic immunity isolation customs for contamination to reduce. During the pro-
(IMS), polymerase chain reaction (PCR), microarrays, and cessing and handling of vegetables and vegetable salads at
biochip technologies have been extensively proven to be the postharvest stage, issues regarding workers’ hygiene
reliable in the said action [208]. PCR analysis including and health, proper washing and disinfection procedures
conventional, real-time, and more digital droplet PCR is (making use of vinegar and salt but avoiding the utilization
used to detect microbial load and harmful pathogens in of one cycle of water to prevent cross-contamination), and
vegetables including Listeria monocytogenes, Salmonella equipment (use of smooth contact surfaces) should be
enterica, and pathogenic Escherichia coli [209]. Other bio- addressed. This is because some retailers and consumers
chemical techniques like liquid chromatography-mass in developing countries like Ghana do not wash vegetables
spectrometry (LC-MS), gas chromatography-mass spec- with disinfectants. Hence, these operations should be
trometry (GC-MS), and Raman spectroscopy have been undertaken in a way that will guarantee the safety of
utilized for bacterial, virus, pesticide, and pathogen detec- products for consumption. Governmental stakeholders
tion, quality, and freshness assessment in vegetables and should have detectable limits always associated with
other food products to ensure their safety [210, 211]. pathogens’ infectious doses, particularly in developing
Additionally, technological advancements in recent countries. To this end, various stakeholders should put in
years have paved for the emergence of newer isolation place various systems to survey when, where, how, and
detection techniques such as digital droplet PCR (ddPCR) what preventive measures to take when there is con-
[212], whole-genome sequencing (WGS) [213], and next- tamination to address the issue of when and where it is
generation sequencing (NGS) [214]. These technologies essential to give attention to the “five major risks asso-
make it possible to detect pathogens at a lower rate in ciated with vegetable production proposed by the Euro-
vegetables, and they are more precise. Harnessing healthy pean Commission. This comprises environmental and
vegetable consumption is a necessity and can only be wildlife factors, irrigation water, usage of fertilizers and
attained when these technologies are integrated into the pesticides, hygiene of workers, equipment, and contact
various production and inspection chain of vegetable pro- levels” [216].
duction chain.
Data Availability
7.3. Food Safety Legislations. Developing countries are now
working harder to develop working systems to achieve good All data used for the study have been included in the article.
food safety standards; these countries include South Africa,
Nigeria, and Ghana. The table below shows the good safety Conflicts of Interest
guidelines adopted in these countries. Specifically, Table 4
presents food safety legislation in Nigeria, South Africa, and The authors declare that they have no conflicts of interest.
Ghana.
Acknowledgments
8. Conclusion
The authors are grateful to Nick Poulton, a graduate fellow at
Several studies have pointed out the increased production the laboratory of Host-Pathogen Biology, University, the
and consumption of vegetables in today’s world. This can be USA, for his input and comments.
Journal of Food Quality 17

References [16] Ghana Standard Authority (GSA), Local Reference Stan-

dards, vol. 7006, pp. 1–4, 2003.
[1] G. I. Balali, D. D. Yar, V. G. Afua Dela, and P. Adjei-Kusi, [17] B. Keraita, R. Abaidoo, I. Beernaerts et al., “Safe Re-use
“Microbial contamination, an increasing threat to the practices in wastewater-irrigated urban vegetable farming in
consumption of fresh fruits and vegetables in today’s world,” Ghana,” Journal of Agriculture, Food Systems, and Com-
International Journal of Microbiology, vol. 2020, Article ID munity Development, vol. 2, no. 4, pp. 147–158, 2012.
3029295, 13 pages, 2020. [18] G. Y. Murindamombe, E. K. Collison, S. F. Mpuchane, and
[2] P. K. Amissah-Reynolds, D. D. Yar, I. Gyamerah, B. A. Gashe, “Presence of Bacillus cereus in street foods in
O. Y. Apenteng, and S. Sakyi, “Fresh vegetables and ready-to- Gaborone, Botswana,” Journal of Food Protection, vol. 68,
eat salads: sources of parasitic zoonoses in mampong- no. 2, pp. 342–346, 2005.
ashanti, Ghana,” European Journal of Nutrition & Food [19] A. Septembre-Malaterre, F. Remize, and P. Poucheret,
Safety, vol. 12, no. 2, pp. 47–55, 2020. “Fruits and vegetables, as a source of nutritional compounds
[3] J. Harrington, “Water for agriculture: global change and and phytochemicals: changes in bioactive compounds
geographic perspectives on research challenges for the fu- during lactic fermentation,” Food Research International,
ture,” Journal of Contemporary Water Research & Education, vol. 104, pp. 86–99, 2018.
vol. 142, no. 1, pp. 36–41, 2009. [20] A. S. Al-Goblan and S. Jahan, “Surveillance for foodborne
[4] E. M. Yahia, P. Garcı́a-Solı́s, and M. E. MaldonadoCelis, illness outbreaks in qassim, Saudi Arabia, 2006,” Foodborne
“Contribution of fruits and vegetables to human nutrition Pathogens and Disease, vol. 7, no. 12, pp. 1559–1562, 2010.
and health,” in Postharvest Physiology and Biochemistry of [21] J. Manitz, T. Kneib, M. Schlather, D. Helbing, and
Fruits and Vegetables, pp. 19–45, Elsevier, Amsterdam, D. Brockmann, “Origin detection during food-borne disease
Netherlands, 2018. outbreaks - a case study of the 2011 EHEC/HUS outbreak in
[5] K. Takeuchi, A. N. Hassan, and J. F. Frank, “Penetration of Germany,” PLoS Currents, vol. 6, 2014.
Escherichia coli O157:H7 into lettuce as influenced by [22] R. L. Ochiai, C. J. Acosta, M. C. Danovaro-Holliday et al., “A
modified atmosphere and temperature,” Journal of Food study of typhoid fever in five Asian countries: disease burden
Protection, vol. 64, no. 11, pp. 1820–1823, 2001. and implications for controls,” Bulletin of the World Health
[6] K. O. Duedu, E. A. Yarnie, P. B. Tetteh-Quarcoo, S. K. Attah, Organization, vol. 86, no. 4, pp. 260–268, 2008.
E. S. Donkor, and P. F. Ayeh-Kumi, “A comparative survey [23] L. Yi, P. Zeng, K. Y. Wong, K. F. Chan, S. Chen, and S. Chen,
of the prevalence of human parasites found in fresh vege- “Controlling Listeria monocytogenes in ready-to-eat leafy
tables sold in supermarkets and open-aired markets in greens by amphipathic α-helix peptide zp80 and its anti-
Accra, Ghana,” BMC Research Notes, vol. 7, no. 1, 2014. microbial mechanisms,” Lebensmittel-Wissenschaft und
[7] V. Kumar and S. K. Mritunjay, “Fresh farm produce as a -Technologie, vol. 152, Article ID 112412, 2021.
source of pathogens: a review,” Research Journal of Envi- [24] A. J. Kayode and A. I. Okoh, “Incidence and genetic diversity
of multi-drug resistant Listeria monocytogenes isolates re-
ronmental Toxicology, vol. 9, no. 2, pp. 59–70, 2015.
covered from fruits and vegetables in the Eastern Cape
[8] Food and Agriculture Organization of the United Nations,
Province, South Africa,” International Journal of Food Mi-
Food and Agriculture Organization of the UN: Global Pro-
crobiology, vol. 363, Article ID 109513, 2022.
duction of Vegetables in 2017, FAO, Rome, Italy, 2017.
[25] S. Khare, A. Tonk, and A. Rawat, “Foodborne diseases
[9] S. K. Mritunjay and V. Kumar, “A study on prevalence of
outbreak in India: a review,” International Journal of Food
microbial contamination on the surface of raw salad vege-
Sciences & Nutrition, vol. 3, no. 3, pp. 9-10, 2018.
tables,” 3 Biotech, vol. 7, no. 1, pp. 13–19, 2017.
[26] M. A. C. Ikeh, S. K. C. Obi, D. N. Ezeasor, I. M. Ezeonu, and
[10] B. E. Acheampong, Assessment of Food Hygiene Practices by
A. N. Moneke, “Incidence and pathogenicity profile of
Street Food Vendors and Microbial Quality of Selected Foods
Listeria spp . isolated from food and environmental samples
Sold, A Study at Dunkwa-On-On, Upper Denkyira East in Nsukka, Nigeria,” African Journal of Biotechnology, vol. 9,
Municipality of the Central Region, Kwame Nkrumah Uni- no. 30, pp. 4776–4782, 2010.
versity of Science and Technology, Kumasi, Ghana, 2015. [27] C. D. Kaptchouang Tchatchouang, J. Fri, M. De Santi et al.,
[11] E. Ameko, S. Achio, and S. Alhassan, “Microbial safety of raw “Listeriosis outbreak in South Africa: a comparative analysis
mixed-vegetable salad sold as an accompaniment to street with previously reported cases worldwide,” Microorganisms,
vended cooked rice in Accra, Ghana,” African Journal of vol. 363, Article ID 109513, 2020.
Biotechnology, vol. 11, no. 50, pp. 11078–11085, 2012. [28] A. J. Niehaus, T. Apalata, Y. M. Coovadia, A. M. Smith, and
[12] P. Mensah, D. Yeboah-manu, K. Owusu-Darko, and P. Moodley, “An outbreak of foodborne Salmonellosis in
A. Ablordey, “Street foods in Accra, Ghana: how safe are rural KwaZulu-Natal, South Africa,” Foodborne pathogens
they,” Bulletin of WHO, vol. 80, pp. 546–554, 2002. and disease, vol. 8, no. 6, pp. 693–697, 2011.
[13] P. Amoah, P. Drechsel, M. Henseler, and R. C. Abaidoo, [29] R. A. M. de Barros, A. C. Torrecilhas, M. A. M. Marciano
“Irrigated urban vegetable production in Ghana: microbi- et al., “Toxoplasmosis in human and animals around the
ological contamination in farms and markets and associated world. Diagnosis and perspectives in the one health ap-
consumer risk groups,” Journal of Water and Health, vol. 5, proach,” Acta Tropica, vol. 231, Article ID 106432, 2022.
no. 3, pp. 455–466, 2007. [30] A. Hadjilouka and D. Tsaltas, “Cyclospora cayeta-
[14] J. W. Buck, R. R. Walcott, and L. R. Beuchat, “Recent trends nensis—major outbreaks from ready to eat fresh fruits and
in microbiological safety of fruits and vegetables,” Plant vegetables,” Foods, vol. 9, no. 11, p. 1703, 2020.
Health Progress, vol. 4, no. 1, p. 25, 2003. [31] A. K. Bhunia, “Foodborne diseases and food safety in India,”
[15] I. D. Amoah, Helminth Infection Risk Associated with the Use Foodborne Microbial Pathogens, Food Science Text Series,
of Wastewater in Urban Agriculture in Kumasi, Ghana, Springer, Berlin, Germany, 2018.
Master’s thesis, Kwame Nkrumah University of Science and [32] A. I. Al-Hindi, A. A. Elmanama, and S. Khalaf, “Prevalence
Technology, Kumasi, Ghana, 2014. of intestinal parasites and microbial contamination in
18 Journal of Food Quality

common edible vegetables used in Gaza Governorate, Pal- [48] G. A. Pesewu, J. N. Y. K. Agyei, K. I. Gyimah et al., “Bac-
estine,” Journal of Food Safety and Hygiene, vol. 2, no. 1–2, teriological assessment of the quality of raw-mixed vegetable
pp. 21–25, 2016. salads prepared and sold by street food vendors in korle-
[33] M. Avazpour, M. R. Nejad, F. Seifipour, and J. Abdi, “As- gonno, accra metropolis, Ghana,” Journal of Health Science,
sessment of the microbiological safety of salad vegetables vol. 2, pp. 560–566, 2014.
from different Restaurants in Ilam,” Journal of Paramedical [49] A. Adu-Gyamfi and J. Nketsia-Tabiri, “Microbiological
Sciences, vol. 4, no. 2, pp. 111–115, 2013. studies of macaroni and vegetable salads in waakye, a local
[34] A. M. Itohan, O. Peters, and I. Kolo, “Short communication: street food,” Ghana Journal of Science, vol. 47, pp. 3–9, 2007.
bacterial contaminants of salad vegetables in abuja munic- [50] F. K. Kechero, K. Baye, A. T. Tefera, and T. S. Tessema,
ipal area council, Nigeria,” Malaysian Journal of Microbi- “Bacteriological quality of commonly consumed fruit juices
ology, vol. 7, no. 2, pp. 111–114, 2011. and vegetable salads sold in some fruit juice houses in Addis
[35] B. Guchi and M. Ashenafi, “Microbial load, prevalence and Ababa, Ethiopia,” Journal of Food Safety, vol. 39, no. 1,
antibiograms of Salmonella and Shigella in lettuce and green pp. 1–9, 2018.
peppers,” Ethiopian Journal of Health Sciences, vol. 20, no. 1, [51] P. Viswanathan and R. Kaur, “Prevalence and growth of
pp. 41–48, 2010. pathogens on salad vegetables, fruits and sprouts,” Inter-
[36] B. C. Adebayo-Tayo, N. N. Odu, C. U. Esen, and national Journal of Hygiene and Environmental Health,
I. O. A. Okonko, “Microorganisms associated with spoilage vol. 203, no. 3, pp. 205–213, 2001.
of stored vegetables in uyo metropolis, akwa ibom state, [52] M. B. H. Najafi and M. Bahreini, “Microbiological quality of
Nigeria,” Nature and Science, vol. 10, no. 3, pp. 1036-1037, mixed fresh-cut vegetable salads and mixed ready-to-eat
2012. fresh herbs in mashhad, Iran,” International Conference on
[37] M. O. Ekong, T. J. Ebob, and I. C. Ukwuoma, “Bacterio- Nutrition and Food Sciences IPCBEE, vol. 39, 2012.
logical quality of fresh salad vegetables sold in calabar road [53] P. Feglo and K. Sakyi, “Bacterial contamination of street
and marian markets, calabar, cross river state, Nigeria,” vending food in Kumasi, Ghana,” Journal of Medicine and
South Asian Journal of Research in Microbiology, vol. 4, no. 3, Biomedical Sciences, vol. 1, no. 1, pp. 1–8, 2012.
[54] D. K. Olukoya, S. B. Bakare, and O. Abayomi, “Letters to the
pp. 1–9, 2019.
[38] M. Nipa, R. Mazumdar, S. Islam, H. R. Bhuiyan, and A. Iqbal, editor,” Journal of Tropical Pediatrics, vol. 37, no. 5,
pp. 266–268, 1991.
“Prevalence of multi drug resistant bacteria on raw salad
[55] M. A. Halablab, I. H. Sheet, and H. M. Holail, “Microbio-
vegetables sold in major markets of chittagong city, Ban-
logical quality of raw vegetables grown in Bekaa Valley,
gladesh,” Middle-East Journal of Scientific Research, vol. 10,
Lebanon,” American Journal of Food Technology, vol. 6, no. 2,
no. 1, pp. 70–77, 2011.
pp. 129–139, 2011.
[39] A. O. Eni, I. A. Oluwawemitan, and O. S. Solomon, “Mi-
[56] M. Z. Jeddi, M. Yunesian, M. E. haghi Gorji, N. Noori,
crobial quality of fruits and vegetables sold in Sango,” Af-
M. R. Pourmand, and G. R. J. Khaniki, “Microbial evaluation
rican Journal of Food Science, vol. 4, pp. 291–296, 2010.
of fresh, minimally-processed vegetables and bagged sprouts
[40] S. Ranjbar-Bahadori, A. Mostoophi, and B. Shemshadi,
from chain supermarkets,” Journal of Health, Population and
“Study on Cryptosporidium contamination in vegetable
Nutrition, vol. 32, no. 3, pp. 391–399, 2014.
farms around Tehran,” Tropical Biomedicine, vol. 30, no. 2, [57] I. I. Ieren, M. Bello, and J. K. P. Kwaga, “Occurrence and
pp. 193–198, 2013. antibiotic resistance profile of Listeria monocytogenes in
[41] A. H. Hosseinvand, S. Sohrabvand, and A. mortazavian, salad vegetables and vegetable salads sold in Zaria, Nigeria,”
“Assessment of the microbiological safety of some spices and African Journal of Food Science, vol. 7, no. 9, pp. 334–338,
raw vegetables in Tehran caterings,” Arvand Journal of 2013.
Health and Medical Sciences, vol. 1, no. 2, 2016. [58] K. Pingulkar Anu Kamat Dilip Bongirw, A. Kamat, and
[42] F. Rahman and R. Noor, “Prevalence of pathogenic bacteria D. Bongirwar, “Microbiological quality of fresh leafy vege-
in common salad vegetables of Dhaka metropolis,” Ban- tables, salad components and ready-to-eat salads: an evi-
gladesh Journal of Botany, vol. 41, no. 2, pp. 159–162, 2013. dence of inhibition of Listeria monocytogenes in tomatoes,”
[43] J. B. Rosales Chavez, M. Bruening, P. Ohri-Vachaspati, International Journal of Food Sciences & Nutrition, vol. 52,
R. E. Lee, M. Jehn, and M. John, “Street food stand avail- no. 1, pp. 15–23, 2001.
ability, density, and distribution across income levels in [59] H. Kouchakkhani, P. Dehghan, M. h. Moosavy, and
Mexico City,” International Journal of Environmental Re- B. Sarmadi, “Occurrence, molecular detection and antibiotic
search and Public Health, vol. 18, no. 8, p. 3953, 2021. resistance profile of Escherichia coli O157: h7 isolated from
[44] B. A. Alimi, “Risk factors in street food practices in devel- ready-To-eat vegetable salads in Iran,” Pharmaceutical Sci-
oping countries: a review,” Food Science and Human ences, vol. 22, no. 3, pp. 195–202, 2016.
Wellness, vol. 5, no. 3, pp. 141–148, 2016. [60] S. Atapoor, F. Safarpoor Dehkordi, and E. Rahimi, “De-
[45] A. Rakha, M. Fatima, Y. Bano et al., “Safety and quality tection of Helicobacter pylori in various types of vegetables
perspective of street vended foods in developing countries,” and salads,” Jundishapur Journal of Microbiology, vol. 7,
Food Control, vol. 138, Article ID 109001, 2022. no. 5, pp. e10013–e10014, 2014.
[46] H. Mepba, S. Achinewhu, S. Aso, and C. Wachukwu, [61] O. O. Uwamere, O. O. Nosa, A. T. Wakil, U. Frances,
“Microbiological quality of selected street foods in Port O. N. Eseosa, and I. O. Nicholas, “Bacteriological quality of
Harcourt, Nigeria,” Journal of Food Safety, vol. 27, no. 2, vegetable salads sold at restaurants within okada town, edo
pp. 208–218, 2007. state, Nigeria,” IOSR Journal of Pharmacy and Biological
[47] O. A. Adeyemi, B. M. Fejukui, and O. O. Adeyemi, “Mi- Sciences, vol. 5, no. 2, pp. 87–90, 2013.
crobial contamination of fresh vegetable salads from food [62] S. J. Cobbina, M. C. Kotochi, J. K. Korese, and M. O. Akrong,
vendors in oyo metropolis,” Nigerian Journal of Pure and “Microbial contamination in vegetables at the farm gate due
Applied Sciences, vol. 32, no. 1, 2019. to irrigation with wastewater in the Tamale metropolis of
Journal of Food Quality 19

northern Ghana,” Journal of Environmental Protection, vegetable salads in Riyadh, Saudi Arabia,” Journal of Me-
vol. 4, no. 7, pp. 676–682, 2013. dicinal Plants Research, vol. 5, no. 3, pp. 444–451, 2011.
[63] G. Abakari, S. J. Cobbina, and E. Yeleliere, “Microbial quality [77] S. Tahmasebi Tehrani, N. Harzandi, and L. Jabalameli,
of ready-to-eat vegetable salads vended in the central “Molecular detection of Shigella spp. contamination in
business district of Tamale, Ghana,” International Journal of ready-to-eat salad samples in west of tehran,” International
Flow Control, vol. 5, no. 1, pp. 3–9, 2018. Journal of Enteric Pathogens, vol. 6, no. 2, pp. 41–44, 2018.
[64] S. K. Kibitok and J. M. Ndoku, “Journal of food safety and [78] R. Annan, N. Agyapong, C. Apprey, and R. Aryeetey,
hygiene evaluation of microbial contamination of consumed “Review of Ghana’s food environment: drivers of availability,
fruits and vegetable salad (kachumbari) around Egerton barriers to healthy food access, and impact of interventions
university, Kenya,” Journal of Food Safety and Hygiene, and policies,” African Journal of Food, Agriculture, Nutrition
vol. 2, no. 1, pp. 3–6, 2016. and Development, vol. 22, no. 2, pp. 19658–19701, 2022.
[65] K. M. Mbae, M. K. Ndwiga, and F. G. Kiruki, “Microbio- [79] World Health Organization (WHO), WHO’s First-Ever
logical quality of kachumbari, a raw vegetable salad popu- Global Estimates of Foodborne Diseases Find Children under
larly served alongside roast meat in Kenya,” Journal of Food 5 Account for Almost One-Third of Deaths, WHO, Geneva,
Quality, vol. 2018, Article ID 8539029, 7 pages, 2018. Switzerland, 2019.
[66] P. A. Agyei and J. Ensink, “Wastewater use in urban agri- [80] A. S. Enoch and A. I. Christiana, “Bacterial burden of
culture: an exposure and risk assessment in Accra, Ghana,” vegetables salad sold in some fast food centers in port
Journal of Science and Technology, vol. 36, no. 1, pp. 7–14, harcourt, rivers state, Nigeria,” Journal of Advances in Mi-
2016. crobiology, vol. 13, no. 2, pp. 1–10, 2018.
[67] M. I. Younus, A. Sabuj, Z. Haque et al., “Microbial risk [81] J. B. James and T. Ngarmsak, Processing of Fresh-Cut Tropical
assessment of ready-to-eat mixed vegetable salads from Fruits and Vegetables: A Technical Guide, FAO, Rome, Italy,
different restaurants of Bangladesh agricultural university 2011.
campus,” Journal of Advanced Veterinary and Animal Re- [82] R. J. Olson, A. Shalapyonok, and H. M. Sosik, “An automated
search, vol. 7, no. 1, pp. 34–41, 2020. submersible flow cytometer for analyzing pico- and nano-
[68] T. Shahryari, A. A. Ramazan, A. Gholami, and A. Zolfaghari, phytoplankton: FlowCytobot,” Deep-Sea Research Part I
“Bacterial contamination of salads and vegetables offered in Oceanographic Research Papers, vol. 50, no. 2, pp. 301–315,
restaurants and fast food in Birjand city in 2015,” Journal of
2003.
Birgand University of Medical Sciences, vol. 25, no. 2,
[83] E. A. Adebayo, O. N. Majolagbe, I. O. Ola, and
pp. 167–171, 2015.
M. A. Ogundiran, “Antibiotic resistance pattern of isolated
[69] M. S. Shah, M. Eppinger, S. Ahmed, A. A. Shah, A. Hameed,
bacterial from salads,” Journal of Research in Biology, vol. 2,
and F. Hasan, “Multidrug-resistant diarrheagenic E. coli
no. 2, pp. 136–142, 2012.
pathotypes are associated with ready-to-eat salad and veg-
[84] M. D. Wogu and I. Iwezeua, “Microbial quality of ready-to-
etables in Pakistan,” J Korean Soc Appl Biol Chem, vol. 58,
eat salad sold in,” International Journal of Science and
no. 2, pp. 267–273, 2015.
Technology, vol. 2, no. 2, pp. 26–38, 2013.
[70] U. De Corato, “Improving the shelf-life and quality of fresh
[85] S. Udo, I. Andy, A. Umo, and M. Ekpo, “Potential human
and minimally-processed fruits and vegetables for a modern
pathogens (bacteria) and their antibiogram in ready–to–eat
food industry: a comprehensive critical review from the
traditional technologies into the most promising advance- salads sold in calabar,” The Internet Journal of Tropical
ments,” Critical Reviews in Food Science and Nutrition, Medicine, vol. 5, no. 2, 2009.
vol. 60, no. 6, pp. 940–975, 2019. [86] S. Ilyas, M. U. Qamar, M. H. Rasool, N. Abdulhaq, and
[71] D. Yeboah-Man, G. Kpeli, M. Akyeh, and L. Bimi, “Bacte- Z. Nawaz, “Multidrug-resistant pathogens isolated from
riological quality of ready-to-eat foods sold on and around ready-to-eat salads available at a local market in Pakistan,”
university of Ghana campus,” Research Journal of Micro- British Food Journal, vol. 118, no. 8, pp. 2068–2075, 2016.
biology, vol. 5, no. 2, pp. 130–136, 2010. [87] E. J. Okafor-Elenwo and O. S. Imade, “Ready-to-eat vege-
[72] R. E. Uzeh, F. A. Alade, and M. Bankole, “The microbial table salads served in Nigerian restaurants: a potential source
quality of pre-packed mixed vegetable salad in some retail of multidrug-resistant bacteria,” Journal of Applied Micro-
outlets in Lagos, Nigeria,” African Journal of Food Science, biology, vol. 129, no. 5, pp. 1402–1409, 2020.
vol. 3, no. 9, pp. 270–272, 2009. [88] A. K. Abougrain, M. H. Nahaisi, N. S. Madi, M. M. Saied, and
[73] A. F. Abaza, “Bacteriological assessment of some vegetables K. S. Ghenghesh, “Parasitological contamination in salad
and ready-to-eat salads in Alexandria, Egypt,” Journal of the vegetables in Tripoli-Libya,” Food Control, vol. 21, no. 5,
Egyptian Public Health Association, vol. 92, no. 3, pp. 177– pp. 760–762, 2010.
187, 2017. [89] A. Daryani, G. H. Ettehad, M. Sharif, L. Ghorbani, and
[74] J. Fung, B. Keraita, F. Konradsen, C. Moe, and M. Akple, H. Ziaei, “Prevalence of intestinal parasites in vegetables
“Microbiological quality of urban-vended salad and its as- consumed in Ardabil, Iran,” Food Control, vol. 19, no. 8,
sociation with gastrointestinal diseases in Kumasi, Ghana,” pp. 790–794, 2008.
International Journal of Food Safety, Nutrition and Public [90] A. Hassan, H. Farouk, and R. Abdul-Ghani, “Parasitological
Health, vol. 4, no. 2/3/4, p. 152, 2011. contamination of freshly eaten vegetables collected from
[75] E. Toe, A. Dadié, E. Dako, and G. Loukou, “Bacteriological local markets in Alexandria, Egypt: a preliminary study,”
quality and risk factors for contamination of raw mixed Food Control, vol. 26, no. 2, pp. 500–503, 2012.
vegetable salads served in collective catering in abidjan (ivory [91] D. El-Said Said, “Detection of parasites in commonly con-
Coast),” Advances in Microbiology, vol. 7, no. 06, sumed raw vegetables,” Alexandria Journal of Medicine,
pp. 405–419, 2017. vol. 48, no. 4, pp. 345–352, 2012.
[76] M. Khiyami, N. Al-Faris, B. Busaeed, and H. Sher, “Food- [92] Z. Khurseed and T. Majeed, “Prevalence of parasitic con-
borne pathogen contamination in minimally processed tamination in leafy raw vegetable consumed in lahore,
20 Journal of Food Quality

Pakistan,” Journal of Natural and Applied Sciences Pakistan, [107] GHS, “The health sector in ghana facts and figures 2017
vol. 1, no. 2, pp. 167–173, 2019. foreword,” The Health Sector in Ghana Facts and Figures,
[93] J. Rahman, A. Islam Talukder, F. Hossain, S. Mahomud, vol. 2, 2017.
M. Atikul Islam, and S. Shamsuzzoha, “Detection of Cryp- [108] P. K. Amissah-Reynolds, D. D. Yar, V. Aboagye, I. Monney,
tosporidium oocyts in commonly consumed fresh salad F. Nuamah, and E. A. Ndego, “Parasitic contamination in
vegetables,” American Journal of Microbiological Research, ready-to-eat salads in the accra metropolis, Ghana,” South
vol. 2, no. 6, pp. 224–226, 2014. Asian Journal of Parasitology, vol. 3, no. 4, pp. 1–11, 2020.
[94] G. Benti and F. Gemechu, “Parasitic contamination on [109] T. Tefera, K. R. Tysnes, K. S. Utaaker, and L. J. Robertson,
vegetables irrigated with Awash River in selected farms, “Parasite contamination of berries: risk, occurrence, and
Eastern Showa, Ethiopia,” Journal of Parasitology and Vector approaches for mitigation,” Food and Waterborne Parasi-
Biology, vol. 5, no. 7, pp. 103–109, 2014. tology, vol. 10, pp. 23–38, 2018.
[95] A. E. Adeleke, T. T. Sodiya, and A. A. Hassan, “Parasitic [110] I. D. Amoah, A. Abubakari, T. A. Stenström, R. C. Abaidoo,
contamination of some vegetables sold at two major markets and R. Seidu, “Contribution of wastewater irrigation to soil-
in jos,” The University of Sindh, vol. 2, no. 3, pp. 1–9, 2018. transmitted helminths infection among vegetable farmers in
[96] L. O. Elmajdoub, M. A. Omar, S. Mohammed, F. Al-Aboudy kumasi, Ghana,” PLoS Neglected Tropical Diseases, vol. 10,
AboSheba, and S. Elzwawi, “Prevalence of parasitic con- no. 12, 2016.
tamination of leafy green vegetables in Misurata, Libya,” [111] FAO, On-farm Practices for the Safe Use of Wastewater in an
Russian Journal of Parasitologu, vol. 40, no. 2, pp. 197–204, Urban and Peri-Urban Horticulture-A Training Handbook
2017. for Farmers Field Schools, FAO, Rome, Italy, 2012.
[97] A. Rostami, M. Ebrahimi, S. Mehravar, V. Fallah Omrani, [112] M. A. Adefisoye and A. I. Okoh, “Ecological and public
S. Fallahi, and H. Behniafar, “Contamination of commonly health implications of the discharge of multidrug-resistant
consumed raw vegetables with soil-transmitted helminth bacteria and physicochemical contaminants from treated
eggs in Mazandaran province, northern Iran,” International wastewater effluents in the Eastern Cape, South Africa,”
Journal of Food Microbiology, vol. 225, pp. 54–58, 2016. Water (Switzerland), vol. 9, no. 8, p. 562, 2017.
[98] B. Sunil, D. R. Thomas, C. Latha, and H. Shameem, “As- [113] M. Uyttendaele, L. A. Jaykus, P. Amoah et al., “Microbial
sessment of parasitic contamination of raw vegetables in hazards in irrigation water: standards, Norms, and testing to
Mannuthy, Kerala state, India,” Veterinary World, vol. 7, manage use of water in fresh produce primary production,”
Comprehensive Reviews in Food Science and Food Safety,
no. 4, pp. 253–256, 2014.
vol. 14, no. 4, pp. 336–356, 2015.
[99] P. U. Umeanaeto and O. F. Nwofor, “Parasite contamination
[114] M. Steele and J. Odumeru, “Irrigation water as source of
of edible vegetables sold in onitsha markets,” The Bioscientist,
foodborne pathogens on fruit and vegetables,” Journal of
vol. 4, pp. 21–31, 2016.
Food Protection, vol. 67, no. 12, pp. 2839–2849, 2004.
[100] O. S. Omowaye and P. A. Audu, “Incidence and detection of
[115] R. G. Feachem, D. J. Bradley, H. Garelick, and D. D. Mara,
parasitic infections by cyst and ova on fruits and vegetables
Sanitation and Disease: Health Aspects of Excreta and
from different major markets in Kogi, Nigeria,” Journal of
Wastewater Management, pp. 23–43, John Wiley & Sons,
Applied and Natural Science, vol. 4, no. 1, pp. 42–46, 2012.
Hoboken, NJ, USA, 1983.
[101] S. Nazemi, M. Raei, M. Amiri, and R. Chaman, “Parasitic
[116] A. Allende and J. Monaghan, “Irrigation water quality for
contamination of raw vegetables in shahroud, semnan,”
leafy crops: a perspective of risks and potential solutions,”
Zahedan Journal of Research in Medical Sciences, vol. 14, International Journal of Environmental Research and Public
no. 8, pp. 84–86, 2012. Health, vol. 12, no. 7, pp. 7457–7477, 2015.
[102] A. Endale, B. Tafa, D. Bekele, and F. Tesfaye, “Detection of [117] E. Páll, M. Niculae, T. Kiss, C. D. Şandru, and M. Spı̂nu,
medically important parasites in fruits and vegetables col- “Human impact on the microbiological water quality of the
lected from local markets in Dire Dawa, Eastern Ethiopia,” rivers,” Journal of Medical Microbiology, vol. 62, no. 11,
Global Journal of Medical Research, vol. 18, no. 1, 2018. pp. 1635–1640, 2013.
[103] S. A. Alshareef, A. M. Abdulsalam, R. A. Alghanaei, [118] M. P. Combarro, M. Gonzalez, M. Araujo, A. C. Amezaga,
E. S. Salim, and M. Chibani, “Parasitic contamination of raw R. A. Sueiro, and M. J. Garrido, “Listeria species incidence
vegetables sampled from different farm locations in Brack and characterisation in A river receiving town sewage from
Al-Shati, Libya,” Journal of Pure and Applied Sciences, vol. 18, A sewage treatment plant,” Water Science and Technology,
no. 4, pp. 210–214, 2019. vol. 35, no. 11–12, pp. 201–204, 1997.
[104] G. Alemu, M. Mama, D. Misker, and D. Haftu, “Parasitic [119] S. Siebert, J. Burke, J. M. Faures et al., “Groundwater use for
contamination of vegetables marketed in Arba Minch town, irrigation - a global inventory,” Hydrology and Earth System
southern Ethiopia,” BMC Infectious Diseases, vol. 19, no. 1, Sciences, vol. 14, no. 10, pp. 1863–1880, 2010.
pp. 410–417, 2019. [120] A. E. Onyango, M. W. Okoth, C. N. Kunyanga, and
[105] A. C. Rodrigues, M. D. C. Silva, R. Â. S. Pereira, and B. O. Aliwa, “Microbiological quality and contamination
L. C. Pinto, “Prevalence of contamination by intestinal level of water sources in isiolo county in Kenya,” Journal of
parasites in vegetables (Lactuca sativaL. andCoriandrum Environmental and Public Health, vol. 2018, Article ID
sativumL.) sold in markets in Belém, northern Brazil,” 2139867, 10 pages, 2018.
Journal of the Science of Food and Agriculture, vol. 100, no. 7, [121] M. Jongman and L. Korsten, “Irrigation water quality and
pp. 2859–2865, 2020. microbial safety of leafy greens in different vegetable pro-
[106] A. Taghipour, E. Javanmard, A. Haghighi, H. Mirjalali, and duction systems: a review,” Food Reviews International,
M. R. Zali, “The occurrence of Cryptosporidium sp., and eggs vol. 34, no. 4, pp. 308–328, 2018.
of soil-transmitted helminths in market vegetables in the [122] D. Faour-Klingbeil, E. C. D. Todd, and V. Kuri, “Microbi-
north of Iran,” Gastroenterology and Hepatology from Bed to ological quality of ready-to-eat fresh vegetables and their link
Bench, vol. 12, no. 4, pp. 364–369, 2019. to food safety environment and handling practices in
Journal of Food Quality 21

restaurants,” LWT—Food Science and Technology, vol. 74, Gastroenterology and Hepatology from Bed to Bench, vol. 11,
pp. 224–233, 2016. no. 4, pp. 352–358, 2018.
[123] D. Faour-Klingbeil, M. Murtada, V. Kuri, and E. C. D. Todd, [138] O. O. Alegbeleye, I. Singleton, and A. S. Sant’Ana, “Sources
“Understanding the routes of contamination of ready-to-eat and contamination routes of microbial pathogens to fresh
vegetables in the Middle East,” Food Control, vol. 62, produce during field cultivation: a review,” Food Microbi-
pp. 125–133, 2016. ology, vol. 73, pp. 177–208, 2018.
[124] A. Rajwar, P. Srivastava, and M. Sahgal, “Microbiology of [139] C. K. Klutse, M. Sc. Thesis Submitted to the Department Of
fresh produce: route of contamination, detection methods, Theoretical And Applied, Kwame Nkrumah University of
and remedy,” Critical Reviews in Food Science and Nutrition, Science and Technology, Kumasi, Ghana, 2009.
vol. 56, no. 14, pp. 2383–2390, 2016. [140] P. Drechsel and S. Dongus, “Dynamics and sustainability of
[125] W. Ahmed, T. Gardner, and S. Toze, “Microbiological urban agriculture: examples from sub-Saharan Africa,”
quality of roof-harvested rainwater and health risks: a re- Sustainability Science, vol. 5, no. 1, pp. 69–78, 2010.
view,” Journal of Environmental Quality, vol. 40, pp. 13–21, [141] M. Delgado, C. Rodrı́guez, J. V. Martı́n, R. Miralles de
2011. Imperial, and F. Alonso, “Environmental assay on the effect
[126] A. S. Sánchez, E. Cohim, and R. A. Kalid, “A review on of poultry manure application on soil organisms in agro-
physicochemical and microbiological contamination of roof- ecosystems,” Science of the Total Environment, vol. 416,
harvested rainwater in urban areas,” Sustainability of Water pp. 532–535, 2012.
Quality and Ecology, vol. 6, pp. 119–137, 2015. [142] S. C. Atidégla, J. Huat, E. K. Agbossou, H. Saint-Macary, and
[127] A. Zacharia, A. H. Outwater, B. Ngasala, and R. Van Deun, R. Glèlè Kakai, “Vegetable contamination by the fecal
“Pathogenic parasites in raw and treated wastewater in bacteria of poultry manure: case study of gardening sites in
Africa: a Review,” Resources and Environment, vol. 8, no. 5, southern Benin,” International Journal of Food Science,
pp. 232–240, 2018. vol. 2016, Article ID 4767453, 8 pages, 2016.
[128] S. Idrissa, D. Belghyti, K. Kharrim, and C. Yoro, “Parasitic [143] O. A. Ijabadeniyi, L. K. Debusho, M. Vanderlinde, and
contamination of the mint and turnip irrigated by untreated E. M. Buys, “Irrigation water as a potential preharvest source
wastewater in sidi yahia gharb (Morocco),” Balwois, Ohrid, of bacterial contamination of vegetables,” Journal of Food
Republic of Macedonia, 2010. Safety, vol. 31, no. 4, pp. 452–461, 2011.
[129] K. Abass, J. K. Ganle, and E. Adaborna, “Coliform con- [144] T. Garcia-Armisen and P. Servais, “Respective contributions
tamination of peri-urban grown vegetables and potential of point and non-point sources of E. coli and enterococci in a
public health risks: evidence from kumasi, Ghana,” Journal large urbanized watershed (the Seine river, France),” Journal
of Community Health, vol. 41, no. 2, pp. 392–397, 2016. of Environmental Management, vol. 82, no. 4, pp. 512–518,
[130] G. Alamnie, A. Kebede, and S. Menkir, “Microbiological 2007.
quality of leafy vegetables irrigated with wastewater in harar [145] M. Islam, M. P. Doyle, S. C. Phatak, P. Millner, and X. Jiang,
town vegetable farm, eastern Ethiopia,” Food Science and “Survival of Escherichia coli O157: H7 in soil and on carrots
Quality Management, vol. 79, pp. 1–8, 2018. and onions grown in fields treated with contaminated ma-
[131] L. Adetunde, I. Sackey, D. DombirI, and Z. Mariama, nure composts or irrigation water,” Food Microbiology,
“Potential links between irrigation water microbiological vol. 22, no. 1, pp. 63–70, 2005.
quality and fresh vegetables quality in upper east region of [146] J. P. Brooks, A. Adeli, M. R. Mclaughlin, and D. M. Miles,
Ghana subsistence farming,” Annual Research & Review in “The effect of poultry manure application rate and AlCl3
Biology, vol. 6, no. 6, pp. 347–354, 2015. treatment on bacterial fecal indicators in runoff,” Journal of
[132] M. C Kayombo and A. W Mayo, “Assessment of microbial Water and Health, vol. 10, no. 4, pp. 619–628, 2012.
quality of vegetables irrigated with polluted waters in dar es [147] Z. Tomass and D. Kidane, “Parasitological contamination of
salaam city, Tanzania,” Environment and Ecology Research, wastewater irrigated and raw manure fertilized vegetables in
vol. 6, no. 4, pp. 229–239, 2018. mekelle city and its suburb, tigray, Ethiopia,” Momona
[133] D. Woldetsadik, P. Drechsel, B. Keraita, F. Itanna, B. Erko, Ethiopian Journal of Science, vol. 4, no. 1, p. 77, 2012.
and H. Gebrekidan, “Microbiological quality of lettuce [148] J. Khandaghi, V. Razavilar, and A. Barzgari, “Isolation of
(Lactuca sativa) irrigated with wastewater in Addis Ababa, Escherichia coli O157:H7 from manure fertilized farms and
Ethiopia and effect of green salads washing methods,” In- raw vegetables grown on it, in Tabriz city in Iran,” African
ternational Journal of Flow Control, vol. 4, no. 1, p. 3, 2017. Journal of Microbiology Research, vol. 4, no. 9, pp. 891–895,
[134] M. A. Gad, A. A. Ashour, M. I. Soliman, F. E. R. Saleh, 2010.
A. Z. Al-Herrawy, and A. H. Nigm, “Article info,” Egyptian [149] S. C. Ingham, J. A. Losinski, M. P. Andrews et al.,
Journal of Aquatic Biology & Fisheries, vol. 24, no. 2, “Escherichia coli contamination of vegetables grown in soils
pp. 451–468, 2020. fertilized with noncomposted bovine manure: garden-scale
[135] P. Amoah, P. Drechsel, and R. C. Abaidoo, “Irrigated urban studies,” Applied and Environmental Microbiology, vol. 70,
vegetable production in Ghana: sources of pathogen con- no. 11, pp. 6420–6427, 2004.
tamination and health risk elimination,” Irrigation and [150] J. L. Wood, Examination of Microbiological Quality of In-
Drainage, vol. 54, no. S1, pp. 49–61, 2005. Field Leafy Vegetables and Identification of On-Farm Generic
[136] P. K. Rai and B. D. Tripathi, “Microbial contamination in Escherichia coli Transmission Dynamics, University of British
vegetables due to irrigation with partially treated municipal Columbia, Endowment Lands, Canada, 2013.
wastewater in a tropical city,” International Journal of En- [151] A. V. Semenov, L. Van Overbeek, A. J. Termorshuizen, and
vironmental Health Research, vol. 17, no. 5, pp. 389–395, A. H. C. Van Bruggen, “Influence of aerobic and anaerobic
2007. conditions on survival of Escherichia coli O157:H7 and
[137] E. Javanmard, H. Mirjalali, M. Niyyati et al., “Small-scale risk Salmonella enterica serovar Typhimurium in Luria-Bertani
assessment of transmission of parasites from the wastewater broth, farm-yard manure and slurry,” Journal of Environ-
treatment plant to downstream vegetable farms,” mental Management, vol. 92, no. 3, pp. 780–787, 2011.
22 Journal of Food Quality

[152] E. A. Alum, S. M. O. C. Urom, and C. M. A. Ben, “Mi- and their relation with season and washing procedures,”
crobiological contamination of food: the mechanisms, im- Journal of Food Quality and Hazards Control, vol. 4, no. 2,
pacts and prevention,” International Journal of Scientific & pp. 37–41, 2017.
Technology Research, vol. 5, no. 3, pp. 65–78, 2016. [167] M. F. Saddik, M. R. El-Sherbeeny, and F. L. Bryan, “Mi-
[153] S. Altizer, R. Bartel, and B. A. Han, “Animal migration and crobiological profiles of Egyptian raw vegetables and salads,”
infectious disease risk,” Science, vol. 331, no. 6015, Journal of Food Protection, vol. 48, no. 10, pp. 883–886, 1985.
pp. 296–302, 2011. [168] M. A. Khiyami, M. M. Shehata, and N. A. Al-Faris, “Isolation
[154] M. J. Alam and L. Zurek, “Association of Escherichia and identification of bacterial pathogens in minimally
coliO157:H7 with houseflies on a cattle farm,” Applied and processed vegetable salads in some Saudi restaurants using
Environmental Microbiology, vol. 70, no. 12, pp. 7578–7580, DNA sequencing,” Journal of Food Agriculture and Envi-
2004. ronment, vol. 9, no. 3–4, pp. 94–100, 2011.
[155] J. L. Talley, A. C. Wayadande, L. P. Wasala et al., “Association [169] H. Bautista-De León, C. A. Gómez-Aldapa, E. Rangel-
of Escherichia coli O157:H7 with filth flies (Muscidae and Vargas, E. Vázquez-Barrios, and J. Castro-Rosas, “Frequency
Calliphoridae) captured in leafy greens fields and experi- of indicator bacteria, Salmonella and diarrhoeagenic
mental transmission of E. coli O157:H7 to spinach leaves by Escherichia coli pathotypes on ready-to-eat cooked vegetable
house flies (diptera: muscidae),” Journal of Food Protection, salads from Mexican restaurants,” Letters in Applied Mi-
vol. 72, no. 7, pp. 1547–1552, 2009. crobiology, vol. 56, no. 6, pp. 414–420, 2013.
[156] L. Orozco R, M. H. Iturriaga, M. L. Tamplin et al., “Animal [170] J. Castro-Rosas, J. F. Cerna-Cortés, E. Méndez-Reyes,
and environmental impact on the presence and distribution D. Lopez-Hernandez, C. A. Gómez-Aldapa, and T. Estrada-
of Salmonella and Escherichia coli in hydroponic tomato Garcia, “Presence of faecal coliforms, Escherichia coli and
greenhouses,” Journal of Food Protection, vol. 71, no. 4, diarrheagenic E. coli pathotypes in ready-to-eat salads, from
pp. 676–683, 2008. an area where crops are irrigated with untreated sewage
[157] I. A. Simon-Oke, O. J. Afolabi, and O. P. Obasola, “Parasitic water,” International Journal of Food Microbiology, vol. 156,
contamination of fruits and vegetables sold at Akure me- no. 2, pp. 176–180, 2012.
tropolis, Ondo State, Nigeria,” Researcher, vol. 6, no. 12, [171] M. R. G. d. Cruz, Y. J. BdS. Leite, JdL. Marques et al.,
2014. “Microbiological quality of minimally processed vegetables
[158] H. G. Bishop and A. Z. Yohanna, “of vegetables with geo-
commercialized in brasilia, df, Brazil,” Food Science and
helminths: prevalence, intensity and roles of hygiene prac-
Technology, vol. 39, no. 2, pp. 498–503, 2019.
tices in samaru-zaria, Nigeria (geohelminthic contamination
[172] M. A. d. Oliveira, V. Maciel de Souza, A. M. Morato Ber-
of vegetables),” International Jjournal of Academic and
gamini, and E. C. P. De Martinis, “Microbiological quality of
Applied Research (IJAAR), vol. 2, no. 7, pp. 8–13, 2018.
ready-to-eat minimally processed vegetables consumed in
[159] B. G. Meerburg, H. M. Vermeer, and A. Kijlstra, “Con-
Brazil,” Food Control, vol. 22, no. 8, pp. 1400–1403, 2011.
trolling risks of pathogen transmission by flies on organic pig
[173] A. S. Sant’ Ana, M. Landgraf, M. T. Destro, and
farms A review,” Outlook on Agriculture, vol. 36, no. 3,
B. D. G. M. Franco, “Prevalence and counts of Salmonella
pp. 193–197, 2007.
spp. in minimally processed vegetables in São Paulo, Brazil,”
[160] T. Tefera, A. Biruksew, Z. Mekonnen, and T. Eshetu,
Food Microbiology, vol. 28, no. 6, pp. 1235–1237, 2011.
“Parasitic contamination of fruits and vegetables collected
[174] L. Vasconcellos, C. T. Carvalho, R. O. Tavares et al., “Iso-
from selected local markets of jimma town, southwest
Ethiopia,” International Scholarly Research Notices, vol. 2014, lation, molecular and phenotypic characterization of Cro-
Article ID 382715, 7 pages, 2014. nobacter spp . in ready-to-eat salads and foods from Japanese
[161] A. S. R. Alsubaie, A. Al-Mekhlafi, L. A. Al-Shibani, S. M. Al- cuisine commercialized in Brazil,” Food Research Interna-
Eryani, and A. A. Azazy, “Hygienic assessment of pathogenic tional, vol. 107, pp. 353–359, 2018.
contamination in raw vegetables in local markets: an im- [175] T. M. A. Vidigal and E. E. C. Landivar, “Presence of parasitic
plication for public health,” International Research Journal of structures in lettuces served in self-service restaurants of São
Microbiology, vol. 5, no. 2, pp. 16–21, 2014. Miguel do Oeste, Santa Catarina State, Brazil,” Acta Scien-
[162] T. Nawas, R. Mazumdar, S. Das et al., “Microbiological tiarum. Biological Sciences, vol. 40, pp. 35027–35035, 2018.
quality and antibiogram of E. coli, Salmonella and Vibrio of [176] A. M. Cordano, C. Jacquet, and C. Jacquet, “Listeria mon-
salad and water from restaurants of chittagong,” Journal of ocytogenes isolated from vegetable salads sold at super-
Environmental Science and Natural Resources, vol. 5, no. 1, markets in Santiago, Chile: prevalence and strain
pp. 159–166, 2012. characterization,” International Journal of Food Microbiol-
[163] C. A. Christison, D. Lindsay, and A. von Holy, “Microbi- ogy, vol. 132, no. 2–3, pp. 176–179, 2009.
ological survey of ready-to-eat foods and associated prep- [177] N. B. Adamu, J. Y. Adamu, and D. Mohammed, “Prevalence
aration surfaces in retail delicatessens, Johannesburg, South of helminth parasites found on vegetables sold in Maiduguri,
Africa,” Food Control, vol. 19, no. 7, pp. 727–733, 2008. Northeastern Nigeria,” Food Control, vol. 25, no. 1,
[164] J. V. Gagliardi and J. S. Karns, “Leaching of Escherichia coli pp. 23–26, 2012.
O157: H7 in diverse soils under various agricultural man- [178] R. M. Nyarango, P. A. Aloo, E. W. Kabiru, and
agement practices,” Applied and Environmental Microbiol- B. O. Nyanchongi, “The risk of pathogenic intestinal parasite
ogy, vol. 66, no. 3, pp. 877–883, 2000. infections in Kisii Municipality, Kenya,” BMC Public Health,
[165] A. Ashrafi Hafez, A. A. Hafez, E. Asadolahi et al., “Study on vol. 8, no. 1, pp. 237–246, 2008.
the parasitic and microbial contamination of vegetables, and [179] A. A. Fallah, K. Pirali-Kheirabadi, F. Shirvani, and S. S. Saei-
the effect of washing procedures on their elimination in ilam Dehkordi, “Prevalence of parasitic contamination in vege-
city,” Journal of Paramedical Sciences, vol. 4, no. 4, 2008. tables used for raw consumption in Shahrekord, Iran: in-
[166] Z. Salavati, A. A. Chalehchaleh, and F. Rezaei, “Parasitic fluence of season and washing procedure,” Food Control,
infections in raw vegetables of Kermanshah, Western Iran vol. 25, no. 2, pp. 617–620, 2012.
Journal of Food Quality 23

[180] M. A. Eraky, S. M. Rashed, M. E. S. Nasr, A. M. S. El- [195] CAC, General Principles of Food Hygiene, Codex Ali-
Hamshary, and A. Salah El-Ghannam, “Parasitic contami- mentarius Comission, Rome, Italy, 2003.
nation of commonly consumed fresh leafy vegetables in [196] A. Meireles, E. Giaouris, and M. Simões, “Alternative dis-
Benha, Egypt,” Journal of Parasitology Research, vol. 2014, infection methods to chlorine for use in the fresh-cut in-
Article ID 613960, 7 pages, 2014. dustry,” Food Research International, vol. 82, pp. 71–85, 2016.
[181] F. Julien-Javaux, C. Gerard, M. Campagnoli, and S. Zuber, [197] I. Castro-Ibáñez, M. I. Gil, and A. Allende, “Ready-to-eat
“Strategies for the safety management of fresh produce from vegetables: current problems and potential solutions to re-
farm to fork,” Current Opinion in Food Science, vol. 27, duce microbial risk in the production chain,” LWT - Food
pp. 145–152, 2019. Science and Technology, vol. 85, pp. 284–292, 2017.
[182] Y. Yang, Y. Luo, P. Millner, E. Turner, and H. Feng, “As- [198] A. M. Sikin, C. Zoellner, and S. S. H. Rizvi, “Current in-
sessment of Escherichia coli O157:H7 transference from soil tervention strategies for the microbial safety of sprouts,”
to iceberg lettuce via a contaminated field coring harvesting Journal of Food Protection, vol. 76, no. 12, pp. 2099–2123,
knife,” International Journal of Food Microbiology, vol. 153, 2013.
no. 3, pp. 345–350, 2012. [199] E. O. Gogo, A. M. Opiyo, K. Hassenberg, C. Ulrichs, and
[183] B. Machado-Moreira, K. Richards, F. Brennan, F. Abram, S. Huyskens-Keil, “Postharvest UV-C treatment for
and C. M. Burgess, “Microbial contamination of fresh extending shelf life and improving nutritional quality of
produce: what, where, and how?” Comprehensive Reviews in African indigenous leafy vegetables,” Postharvest Biology and
Food Science and Food Safety, vol. 18, no. 6, pp. 1727–1750, Technology, vol. 129, pp. 107–117, 2017.
2019. [200] T. Abuladze, M. Li, M. Y. Menetrez, T. Dean, A. Senecal, and
[184] J. F. T. K. Akoachere, B. F. Tatsinkou, and J. M. Nkengfack, A. Sulakvelidze, “Bacteriophages reduce experimental con-
“Bacterial and parasitic contaminants of salad vegetables tamination of hard surfaces, tomato, spinach, broccoli, and
sold in markets in Fako Division, Cameroon and evaluation ground beef by Escherichia coli O157:H7,” Applied and
of hygiene and handling practices of vendors,” BMC Re- Environmental Microbiology, vol. 74, no. 20, pp. 6230–6238,
search Notes, vol. 11, no. 1, pp. 100–107, 2018. 2008.
[185] N. Garg, J. J. Churey, and D. F. Splittstoesser, “Microflora of [201] A. Vaidya, S. Ravindranath, and U. S. Annapure, “Bacte-
fresh cut vegetables stored at refrigerated and abuse tem- riophages for pre- and post-contamination biocontrol of
peratures,” Journal of Food Science & Technology, vol. 30, artificial Escherichia coli contamination in carrots,” Leb-
no. 5, pp. 385-386, 1993. ensmittel-Wissenschaft und -Technologie, vol. 97, pp. 193–
[186] D. Zagory, “Effects of post-processing handling and pack- 197, 2018.
aging on microbial populations,” Postharvest Biology and [202] F. Judée, S. Simon, C. Bailly, and T. Dufour, “Plasma-acti-
Technology, vol. 15, no. 3, pp. 313–321, 1999. vation of tap water using DBD for agronomy applications:
[187] L. A. Rodriguez-Romo and A. E. Yousef, “Microbial stress identification and quantification of long lifetime chemical
adaptation and safety of produce,” in Microbiology of Fruits species and production/consumption mechanisms,” Water
and Vegetables, Taylor Francis Group, Abingdon-on- Research, vol. 133, pp. 47–59, 2018.
Thames, Oxfordshire United Kingdom, 2005. [203] P. Puligundla, J. W. Kim, and C. Mok, “Effects of Non-
[188] WHO, “Food and agricultural organization of the united thermal plasma treatment on decontamination and
Nations/world health organization,” Microbiological Haz- sprouting of radish (raphanus sativus L.) seeds,” Food and
ards in Fresh Leafy Vegetables and Herbs, WHO, Geneva, Bioprocess Technology, vol. 10, no. 6, pp. 1093–1102, 2017.
Switzerland, 2008. [204] M. I. Gil, M. V. Selma, F. López-Gálvez, and A. Allende,
[189] J. James, “Overview of microbial hazards in fresh fruit and “Fresh-cut product sanitation and wash water disinfection:
vegetables operations,” in Microbial Hazard Identification in problems and solutions,” International Journal of Food
Fresh Fruit and Vegetables, Wiley, Hoboken, NJ, USA, 2005. Microbiology, vol. 134, no. 1–2, pp. 37–45, 2009.
[190] M. I. Gil, M. V. Selma, T. Suslow, L. Jacxsens, [205] L. R. Beuchat and J. H. Ryu, “Produce handling and pro-
M. Uyttendaele, and A. Allende, “Pre- and postharvest cessing practices,” Emerging Infectious Diseases, vol. 3, no. 4,
preventive measures and intervention strategies to control pp. 459–465, 1997.
microbial food safety hazards of fresh leafy vegetables,” [206] H. Ölmez and M. Y. Akbas, “Optimization of ozone treat-
Critical Reviews in Food Science and Nutrition, vol. 55, no. 4, ment of fresh-cut green leaf lettuce,” Journal of Food En-
pp. 453–468, 2015. gineering, vol. 90, no. 4, pp. 487–494, 2009.
[191] (National Advisory Committee on Microbiological Criteria [207] L. Carletti et al., “Use of ozone in sanitation and storage of
for Foods) NACMCF, “Microbiological safety evaluations fresh fruits and vegetables,” Journal of Food Agriculture and
and recommendations on fresh produce,” Food Control, Environment, vol. 11, no. 3–4, pp. 585–589, 2013.
vol. 10, no. 2, pp. 117–143, 1999. [208] M. Nemati, A. Hamidi, S. Maleki Dizaj, V. Javaherzadeh, and
[192] N. Achiwa, M. Katayose, K. Yoshida, S. Kusakari, and F. Lotfipour, “An overview on novel microbial determina-
K. Abe, “Viable bacterial counts on fresh-cut salads and tion methods in pharmaceutical and food quality control,”
bactericidal effect of electrolyzed acidic water,” Food Pres- Advanced Pharmaceutical Bulletin, vol. 6, no. 3, pp. 301–308,
ervation Science, vol. 30, no. 4, pp. 185–190, 2004. 2016.
[193] T. Hofer, B. Gardner, and T. Ford, “Fresh produce safety in [209] E. Badosa, N. Chico, M. Pla, D. Parés, and E. Montesinos,
retail operations,” in Microbial Hazard Identification in “Evaluation of ISO enrichment real-time PCR methods with
Fresh Fruits and Vegetables, pp. 245–259, Wiley, Hoboken, internal amplification control for detection of Listeria
NJ, USA, 2006. monocytogenes and Salmonella enterica in fresh fruit and
[194] P. V. Mahajan, O. J. Caleb, M. I. Gil et al., “Quality and safety vegetables,” Letters in Applied Microbiology, vol. 49, no. 1,
of fresh horticultural commodities: recent advances and pp. 105–111, 2009.
future perspectives,” Food Packaging and Shelf Life, vol. 14, [210] G. Holmes, D. Fletcher, and P. Reutemann, “An application
pp. 2–11, 2017. of data mining to fruit and vegetable sample identification
24 Journal of Food Quality

using gas Chromatography-Mass Spectrometry,” in Pro-

ceedings of the 6th Biennial Meeting of the International
Environmental Modelling and Software Society, pp. 1577–
1584, Brussels, Belgium, 2012.
[211] J. Qin, M. S. Kim, K. Chao et al., “Advances in Raman
spectroscopy and imaging techniques for quality and safety
inspection of horticultural products,” Postharvest Biology
and Technology, vol. 149, pp. 101–117, 2019.
[212] D. Cristiano, M. Peruzy, M. Aponte et al., “Comparison of
droplet digital PCR vs. real-time PCR for Yersinia enter-
ocolitica detection in vegetables,” International Journal of
Food Microbiology, vol. 354, Article ID 109321, 2021.
[213] S. Araújo, M. Tacão, R. Baraúna et al., “Genome analysis of
two multidrug-resistant Escherichia coli O8: H9-ST48 strains
isolated from lettuce,” Gene, vol. 785, Article ID 145603,
2021.
[214] E. Manthou, G. Coeuret, S. Chaillou, G. J. E. Nychas, and
G.-J. E. Nychas, “Metagenetic characterization of bacterial
communities associated with ready-to-eat leafy vegetables
and study of temperature effect on their composition during
storage,” Food Research International, vol. 158, 2022.
[215] WHO, “National food safety systems in Africa—a situation
analysis,” in FAO/WHO Regional Conference of Food Safety
for Africa, Geneva, Switzerland, October 2005.
[216] A. Allende, P. Truchado, R. Lindqvist, and L. Jacxsens,
“Quantitative microbial exposure modelling as a tool to
evaluate the impact of contamination level of surface irri-
gation water and seasonality on fecal hygiene indicator E. coli
in leafy green production,” Food Microbiology, vol. 75,
pp. 82–89, 2018.