Received: 30 August 2019 Revised: 1 December 2019 Accepted: 7 January 2020

DOI: 10.1111/1541-4337.12533

COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

Microbiological safety of ready-to-eat foods in low- and

middle-income countries: A comprehensive 10-year (2009 to 2018)
review

Oluwadamilola M. Makinde1 Kolawole I. Ayeni1 Michael Sulyok2 Rudolf Krska2,3

Rasheed A. Adeleke4 Chibundu N. Ezekiel1,2

1 Department of Microbiology, Babcock

Abstract
University, Ilishan Remo, Nigeria
2 Department of Agrobiotechnology
Ready-to-eat foods (RTEs) are foods consumed without any further processing. They
(IFA–Tulln), Institute of Bioanalytics and are widely consumed as choice meals especially by school-aged children and the fast-
Agro-Metabolomics, University of Natural paced working class in most low- and middle-income countries (LMICs), where they
Resources and Life Sciences Vienna (BOKU),
Tulln, Austria contribute substantially to the dietary intake. Depending on the type of processing
3 Institute
for Global Food Security, School of and packaging material, RTEs could be industrially or traditionally processed. Typi-
Biological Sciences, Queen’s University cally, RTE vendors are of low literacy level, as such, they lack knowledge about good
Belfast, Belfast, United Kingdom
hygiene and food handling practices. In addition, RTEs are often vended in outdoor
4 Department of Microbiology, North-West
University, Potchefstroom, South Africa
environments such that they are exposed to several contaminants of microbial origin.
Depending on the quantity and type of food contaminant, consumption of contami-
Correspondence nated RTEs may result in foodborne diseases and several other adverse health effects
Chibundu N. Ezekiel, Department of Micro-
biology, Babcock University, Ilishan Remo, in humans. This could constitute major hurdles to growth and development in LMICs.
121103, Ogun State, Nigeria. Therefore, this review focuses on providing comprehensive and recent occurrence and
Email: chaugez@gmail.com
impact data on the frequently encountered contaminants of microbial origin published
in LMICs within the last decade (2009 to 2018). We have also suggested viable food
safety solutions for preventing and controlling the food contamination and promoting
consumer health.

KEYWORDS
consumer protection, food safety, foodborne bacteria, mycotoxins, public health

1 I N T RO D U C T I O N 2013b; Mensah, Yeboah-Manu, Owusu-Darko, & Ablordey,

2002). RTEs can be processed from single or mixed raw
Ready-to-eat foods (RTEs) are foods consumed without any ingredients, such as cereals, fish, meat, nuts, and spices, into
further processing or preparations. They could be traditionally foods that may be liquid, semi-solid, or solid in consistency
or industrially processed, packaged, or unpackaged and are (Adebayo-Oyetoro et al., 2017; Ceyhun Sezgin & Sanher,
usually considered to comprise, mainly, the publicly vended 2016; Feglo & Sakyi, 2012). Based on the type of process-
foods consumed immediately or later (Cerna-Cortes et al., ing technique and packaging material, RTEs could range from
2015; FAO & WHO 2004; Von Holy & Makhoane, 2006). traditionally processed foods such as chaat in India (Agrawal,
Similar to other regions, RTEs are widely consumed in low- Gupta, & Varma, 2008), matoke in Uganda (Bardi et al.,
and middle-income countries (LMICs) due to ease of produc- 2014), and warankasi in Nigeria (Adeyeye, 2017) to industri-
tion, availability, affordability, and palatability (Al Mamun, ally processed foods such as bread, biscuits, canned sardine,
Rahman, & Turin, 2013a; Al Mamun, Rahman, & Turin, ice cream, and pizza. Depending on the type, RTEs can be

Compr Rev Food Sci Food Saf. 2020;1–30. wileyonlinelibrary.com/journal/crf3 © 2020 Institute of Food Technologists® 1
2 M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

consumed by different groups of people ranging from chil- The World Health Organization (WHO) of the United
dren to adults. For instance, kulikuli is mostly consumed by Nations reported that LMICs, particularly those in the African
children of school age as well as adults in Nigeria and Benin and South-East Asian sub-regions, suffer significantly from
(Adjou, Yehouenou, Sossou, Soumanou, & De Souza, 2012; the burden of FBD (Havelaar et al., 2015), sometimes result-
Ezekiel et al., 2013). In addition, RTEs are the preferred food ing to huge economic losses. To put this into proper per-
by individuals who are often very busy and have less time to spective, the World Bank estimates that the total productiv-
prepare meals while at work. ity loss associated with FBD in LMICs is about US$44.4
It is on record that many RTE vendors in LMICs often billion per year, whereas the annual cost of treating these
lack knowledge about good hygiene practices, which may diseases costs several billion dollars (Jaffee, Henson, Unn-
predispose the foods to microbial contamination (Al Mamun evehr, Grace, & Cassou, 2019). Obviously, FBD constitute a
et al., 2013a, 2013b; WHO, 2010). The situation is fur- major impediment to growth and development in the affected
ther complicated by the practice of vending RTEs in out- LMICs, because resources used in treating these preventable
door environments. Consequently, the foods are exposed diseases could be redistributed into building other sectors of
to aerosols, insects, and rodents, which serve as sources the economy (Alimi, 2016). In addition, FBD pose a threat to
of food contaminants (Fowoyo & Igbokwe, 2014; Mensah several of the Sustainable Development Goals of the United
et al., 2002). The microbial contaminants of RTEs include Nations in LMICs (FAO/WHO, 2018; Havelaar et al., 2015).
bacteria (for example, species of Bacillus, coagulase nega- Consequently, there is a need to intensify efforts to reduce
tive Staphylococci, Escherichia coli, Klebsiella pneumoniae, microbial contamination of RTEs across LMICs. One way to
Listeria monocytogenes, Pseudomonas spp., and Staphy- achieve this is to harness recent data (2009 to 2018) on micro-
lococcus aureus; Annan-Prah et al., 2011; Fadahunsi & bial contamination profiles of RTEs available in LMICs, with
Makinde, 2018; Felgo & Sakyi, 2012; Gdoura-Ben Amor a view to providing information on the most likely encoun-
et al., 2018; Kharel, Palni, & Tamang, 2016; Tambekar, tered microbial contaminants and suggest viable solutions for
Jaiswal, Dhanorkar, Gulhane, & Dudhane, 2009), fungi (for preventing and controlling the menace. Food contaminants of
example, diverse toxigenic species of Aspergillus, Alternaria, microbial origin are prioritized in this review owing to their
Fusarium, and Penicillium; Adjou et al., 2012; Oranusi & top-ranking on the list of foodborne hazards by the WHO
Nubi, 2016), parasites (for example, Ascaris lumbricoides (FAO/WHO, 2018).
and Toxoplasma gondii; Abd El-Razik, El Fadaly, Barakat, Thus, this comprehensive decade (2009 to 2018) review
& Abu Elnaga, 2014; Manyi, Idu, & Ogbonna, 2014), and focuses on (a) documenting the diversity of RTEs in LMICs;
viruses (for example, hepatitis A virus; Yongsi, 2018). Addi- (b) identifying the potential contamination sources; (c) X-
tionally, the contaminating bacteria and fungi may further raying the adequacy of detection methods applied to food
constitute increased public health risk by secreting toxic com- contaminants of microbial origin in the regions; (d) outlining
pounds such as cereulide (Ceuppens et al., 2011) and myco- the microbiologically related hazard groups and their health
toxins (IARC, 2015), respectively, at different stages dur- effects; and (e) proffering a cocktail of food safety solutions
ing food production. Nonmicrobial-related RTE contaminants that could be applied in LMICs for the enhancement of the
include heavy metals (for example, lead; Jalbani & Soy- RTE chain and promotion of consumer/public health. For
lak, 2015) and pesticide residues (for example, tetradifon; the purpose of this review, LMICs are considered to include
Skretteberg et al., 2015) mostly found in plant-based RTEs, as low-income and lower middle-income countries based on the
well as polyaromatic hydrocarbons from car fumes and other recent categorization by the World Bank for the 2020 fiscal
industrial sources (Proietti, Frazzoli, & Mantovani, 2014). year (World Bank, 2019).
Depending on the type and concentration of contaminant,
amount of food ingested by consumers, and health status of
the consumer, acute or chronic foodborne diseases (FBD) may 2 D I V E R S I T Y OF RT E s I N L M I C s
be result. On the other hand, continuous daily exposure to sin-
gle or mixtures of these food contaminants via consumption In different regions of LMICs, RTEs are adopted and accepted
of contaminated RTEs could produce a plethora of adverse as part of the cuisine of the people, thus giving them an
health effects. Observable effects may range from mild to identity and heritage, which are often passed across gener-
recurrent nausea, vomiting, and diarrhea (Ceuppens et al., ations (Kraig & Taylor, 2013). For example, uttapam pro-
2011) to severe complications such as cancers, neural tube cessed from rice and warankasi obtained from raw milk are
defects, and even human fatalities (Gibb et al., 2015; IARC, RTEs indigenous to the people of southern India and north-
2015; JECFA, 2017, 2018; Kamala et al., 2018; Wild & Gong, ern Nigeria, respectively (Iwuoha & Eke, 1996; Ray, Ghosh,
2010). Thus, improperly prepared RTEs in LMICs, where reg- Singh, & Mondal, 2016). Central to RTE processing are raw
ulations and monitoring for compliance are grossly inade- ingredients, which are mostly of plant (such as, grains, nuts,
quate, may constitute a huge risk to public health. and spices) and animal origin (such as, fish, meat, and milk).
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW … 3

Typically, the choice of RTE ingredients is largely influenced ished products, thus constituting a health risk to the con-
by culture and belief, income, and socioeconomic status. For sumers (Alimi, 2016; Khairuzzaman, Chowdhury, Zaman, Al
example, in some parts of the Middle East and North Africa, Mamun, & Bari, 2014).
pork is considered as unacceptable; hence, it is replaced by
other meat source (such as mutton or beef) in RTEs (Benker-
roum, 2013). Despite the fact that RTEs are largely region spe-
3.2 Contaminated food process chains
cific, there is a high propensity to try out new types of foods Central to RTE preparation is water, which is usually applied
introduced from other parts of the world, mostly due to human in large proportions during several processing steps such as
migration. RTEs such as sharwama (Middle East) and samosa dilution, fermentation, milling, steeping, and washing of RTE
(Middle East and Asia) have become globally acceptable and ingredients. Thus, it is crucial that water utilized for the
are widely consumed especially in several LMICs (Privitera processing of RTEs is free from microbiological contami-
& Nesci, 2015). nants. This is often not the case in many LMICs, especially
Interestingly, RTE recipes and processing techniques are in resource scarce rural settings, where potable water is not
often similar across regions despite their diversity, although readily available (Ritchie & Roser, 2019; WHO, 2017). Con-
the RTE local names largely differ. For example, the grilling sequently, water from questionable sources such as wells,
or roasting technique commonly applied during meat pro- streams, and rivers (sometimes stored for long periods in
cessing into nyama choma in Kenya (Mwangi, den Hartog, unsterilized open containers) is routinely applied during the
Mwadime, van Staveren, & Foeken, 2002) is also applied processing of RTEs. Thus, the application of potentially con-
to process meat into suya in Nigeria (Obadina, Oyewole, & taminated water in RTE processing could predispose the
Ajisegiri, 2013). Similarly, fava beans are fried with other foods to pathogenic bacteria such as Campylobacter, E. coli,
ingredients to produce falafel in Egypt (El-Shenawy, El- Salmonella, Pseudomonas, and Vibrio. Consequently, con-
Shenawy, Mañes, & Soriano, 2011) and madlu’e in Syria sumers could be at risk of severe public health challenges
(Ceyhun Sezgin & Şanher, 2016). Table 1 shows the diver- (Rane, 2011).
sity of RTEs in some LMICs. Obviously, frying, roasting, and Quality of food packaging materials is another critical fac-
grilling are considered the prominent techniques employed in tor to consider in evaluating the role of contaminated food
the RTE processing across LMICs. process chains in RTE safety and consumer safety. In many
LMICs, the choice of food packaging material depends on the
type of RTE. Common packaging materials for locally pro-
3 POTENTI A L SO U RC E S O F cessed RTEs include prewashed but unsterilized plastic bot-
CONTAMINAT I O N O F RT E s tles for packaging of liquid RTEs such as fermented bever-
ages; polyethylene/nylon bags; or used paper (for example,
In LMICs, RTEs are processed and sold under unhygienic newspapers). The utilization of these kinds of low-quality
conditions such that the risk of exposure to food contaminants packaging materials may be direct source of pathogenic food-
is increased (Al Mamun et al., 2013a, 2013b; WHO, 2010). borne bacteria as well as fungal propagules; however, lim-
These conditions as well as other factors are discussed below. ited research data are available in this regard. Poor personal
hygiene during food processing is an additional predispos-
ing factor for RTE contamination during the process chain
3.1 Quality of ingredients (Fellows & Hilmi, 2011). This is often facilitated by the low
The use of high-quality ingredients is critical to ensuring the awareness level and poverty status of many of the local RTE
safety of RTEs. However, in LMICs, it is common practice processors in LMICs. Good personal hygiene is necessary
for vendors to purchase low-quality (often visibly bad) ingre- during actual food preparation as well as during food pack-
dients (such as cereals, legumes, spices, and vegetables) that aging in order to limit RTE contamination.
are prone to heavy contamination by bacteria, fungi, and their
toxins (Alimi, 2016) for RTE processing. Obvious reasons for
3.3 Unhygienic vending practices and
the utilization of low-quality ingredients include poverty (less
conditions
income to purchase high-quality ingredients); the need to gen-
erate more family income, which leads to purchase of large Poor post-food production handling by vendors plays a key
quantity of low-grade ingredients at low cost (often mixed role in RTE contamination (Fellows & Hilmi, 2011). RTE
with very small quantity of high quality ingredients) for RTE vendors often lack good hygiene practices. A common sce-
processing; and low awareness of the severity of FBD. To nario is vendors not washing their hands, the washing of hands
worsen the scenario, the low-quality ingredients are often not with nonpotable (contaminated and unsterilized) water, or
properly processed or are undercooked. Consequently, micro- use of potable water but without detergents or disinfectants
bial spores or their toxins may be carried over into the fin- before RTEs are packaged. For instance, it is common vendor
4 M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

TABLE 1 Diversity of traditionally processed ready-to-eat foods in low- and middle-income countries
Ready-to-eat
Region Country food Raw ingredients Processing technique References
Africa Egypt Falafel Ground chickpeas and/or fava Frying El-Shenawy et al., 2011
Ethiopia Injera and Wot Tef bread, beef, lamb, chicken, goat, Cooking Reda, Ketema, & Tsige,
lentils, or chickpeas, with spicy 2017
Berbere
Ghana Banku kenkey Cassava/plantain and yams Steaming/ boiling Rheinländer et al., 2008
Kenya Nyama choma Beef, veal, sheep, lamb, goat, and Grilling and steaming Mwangi et al., 2002
with Ugali maize/cassava dough
Morocco Merguez Lamb or beef, flour, and red pepper Baking Benkerroum, 2013
Nigeria Chin chin Wheat flour and eggs Frying Adebayo-Oyetoro et al.,
2017
Suya Spiced meat and onions Grilling Obadina et al., 2013
Akara Beans Frying Omemu & Aderoju,
2008
Moi-moi Beans, pepper, and onions Steamed/ boiled Nkere, Ibe, & Iroegbu,
2011
Tanzania Ndizi Kaanga Bananas or plantains Frying Sanches-Pereira et al.,
2017
Uganda Matoke Mashed plantain and groundnut Steaming/ boiling Bardi et al., 2014
sauce
Asia India Chaat Flour, yoghurt, onions, sev, Frying Agrawal et al., 2008
coriander, and spices
Pakoda Kodo millet, onions, green chillies, Frying Deshpande, Mohapatra,
and spices Tripathi, & Sadvatha,
2015
Pani puri Unleavened Indian bread fried crisp, Frying Fellows & Hilmi, 2011
tamarind, chili, potato, onion,
chickpeas, and various vegetables
Samosa Flour, potato, onion, spices, oil, and Frying Kharel et al., 2016
salt
Indonesia Nasi putih long-grain rice, chicken, pork, dog Cooked Neufingerl et al., 2016
meat, goat, or beef, coconut milk
Pakistan Pahata roll Beef or chicken, bread, onions, Frying Ceyhun Sezgin &
tomato, and raita Şanher, 2016
Philippines Siomai Squid, fish balls, chicken, and Frying Kraig & Taylor, 2013
dipping sauces
Taho Bean curd, syrup, and tapioca balls Canini, Bala, Maraginot,
& Mediana, 2013
Caribbean Haiti Mayi moulen Rice, beans, cornmeal mush, kidney Boiling, frying Ceyhun Sezgin &
with pikliz beans, coconut, and peppers with Şanher, 2016
spicy pickled carrots and cabbage
Middle East Palestine and Madlu’e Sweet cheese curds, rich biscuit in Frying Ceyhun Sezgin &
Syria Syrup, ground chickpeas, and/or Şanher, 2016
fava beans

practice to directly touch meat-based RTE (for example, suya) play the foods for sale in roadside make-shift sheds, which
with unwashed hands during the postproduction slicing pro- are sometimes situated close to dump sites or dirty stag-
cess. In addition, most vendors do not wear protective cov- nant roadside water. These serve as reservoirs to flies and
erings (for example, nylon gloves) before the packaging of other insects that are potential carriers of several bacte-
RTEs. rial pathogens (Lindh & Lehane, 2011). A study in Uganda
A major feature of RTE vending points in LMICs is revealed that 74.2% of vendors prepared food close to fly and
their characteristic dirty surroundings. Vendors openly dis- insect infested trash receptacles (Muyanja, Nayiga, Brenda, &
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW … 5

Nasinyama, 2011). Furthermore, improperly washed vending 2007). The ability of molecular techniques to accurately
utensils often contain leftover food particles suitable for pro- and rapidly detect pathogenic microorganisms known to
liferation of pathogenic microorganisms that could potentially cause FBD ensures source tracking and proper surveillance
cross-contaminate freshly prepared RTEs (Fellows & Hilmi, of RTEs (ECDC, 2013; Law et al., 2015). Consequently,
2011; Muyanja et al., 2011). In many LMICs, the unhygienic high-throughput molecular methods such as next-generation
vending condition is an easily controllable factor if regula- sequencing and whole genome sequencing (WGS) add cre-
tions targeting RTEs and their vending become existent and dence to inferences made from surveillance studies by high-
are enforced. lighting phylogenetic similarities among microorganisms.
WGS further provides information on the evolution of the
microorganisms as well as their genetic determinants that
could increase virulence and pathogenicity (Hazen et al.,
4 DETECTIO N O F 2013; Leekitcharoenphon, Nielsen, Kaas, Lund, & Aarestrup,
CONTAMINANTS OF 2014). Aside the application of WGS in surveillance stud-
MICROBIOLOGICA L ORIGIN I N ies, it is an invaluable approach during cases of outbreaks
RT E s because it gives a clearer picture of the possible source of
outbreaks and provides sufficient data on ways to prevent
Analytical techniques employed in the microbiological anal- the spread to other regions (Chin et al., 2011; Hendriksen
ysis of food typically include conventional (Mandal, Biswas, et al., 2011). A typical example is the application of WGS
Choi, & Pal, 2011) and molecular methods (Law, Ab Mutalib, in the 2010 cholera outbreak in Haiti, a LMIC. This tech-
Chan, & Lee, 2015). A combination of these techniques, often nique revealed the V. cholerae strain(s) responsible for the
referred to as “polyphasic approach,” is usually applicable outbreak may have been accidentally introduced from another
for high-throughput analysis of the food matrix (Randazzo, geographical location (Chin et al., 2011; Hendriksen et al.,
Scifo, Tomaselli, & Caggia, 2009). The application of con- 2011). Recently, molecular techniques including WGS have
ventional methods relies solely on the isolation of bacteria also been applied in other studies involving fermenters in tra-
on general purpose or selective media (for example, nutrient ditional foods and pathogens in vegetable samples of LMIC
agar, MacConkey agar, or eosin methylene blue) and of fungi origin (Adewumi, Oguntoyinbo, Keisam, Romi, & Jeyaram,
on mycological media (such as, malt extract agar) (Samson, 2013; Diaz et al., 2018; Ezekiel, Ayeni, et al., 2019; Igbinosa
Houbraken, Thrane, Frisvad, & Anderson, 2019). Microbial et al., 2018). These studies have mostly been conducted in
isolation is typically followed by preliminary identification collaboration with institutions in the North (Western world)
based on the assessment of morphological features including where facilities and expertise are readily available; thus, tech-
colony color, pigmentation, colony reverse color on selective nology and expertise transfer to LMICs are expected in the
media, microscopic characters, and reactions to a set of bio- future.
chemical tests (for example, catalase, coagulase, and indole In order to detect chemical contaminants of micro-
tests for bacteria) (Mandal et al., 2011). Majority of the stud- bial origin in RTEs, several techniques including enzyme-
ies on bacterial identification in RTEs in LMICs were solely linked immunosorbent assay (ELISA), high-performance liq-
based on conventional methods of microbe characterization uid chromatography (HPLC), and liquid chromatography–
(Table 2). The preferred application of conventional methods tandem mass spectrometry (LC/MS–MS) can be applied. In
in microbial characterization in many LMICs is multifactorial most LMICs, the ELISA method represents the most viable
including lack of molecular facilities, lack of expertise, inad- technique for detection of frequently encountered chemical
equate research funding for human capacity, and infrastruc- contaminants (for example, mycotoxins) in RTE foods. This
tural development. Although conventional methods are rel- is largely due to its low cost of analysis relative to high-end
atively cheaper compared to molecular methods, significant techniques such as the HPLC and LC–MS/MS. However, the
limitations such as laboriousness and low precision leading to ELISA technology has several limitations such as low sensi-
species misidentification make the conventional method inap- tivity and inability to simultaneously detect multiple myco-
propriate for microbial typing (Law et al., 2015; Mandal et al., toxins (Berthiller et al., 2013). In addition, ELISA kits are
2011; Zhao, Lin, Wang, & Oh, 2014). only readily available for the detection of single mycotoxins
In contrast, molecular methods offer a more sensitive and (for example, aflatoxin B1 , total aflatoxin, and ochratoxin A
accurate mode of microbial identification (EFSA, 2013). in foods). This constitutes a major hurdle to food safety espe-
These methods generally involve classifying pathogenic cially in most LMICs, where there is frequent co-occurrence
microorganisms based on genotypic traits as well as on genetic of multiple mycotoxins in dietary staples and RTE ingredi-
determinants known to increase their virulence and aid their ents (Abia et al., 2017; Oyedele et al., 2017; Sombie et al.,
adaptability to various food matrices (Hallin, Deplano, & 2018; Warth et al., 2012). Thus, high-end chromatography–
Struelens, 2012; Mandal et al., 2011; Van Belkum et al., based techniques (for example, HPLC and the more
TABLE 2 Bacterial contamination of ready-to-eat (RTE) foods in low- and middle-income countries (2009 to 2018)
6

Region/ Potential source of

Country RTE food contamination Pathogen Prevalence %(n/ N) Analytical technique References
Africa
Burkina Faso Grilled chicken Poor hygiene practices E. coli 27.45 (28/102)* Conventional and Somda et al., 2018
Polymerase Chain
Reaction (PCR)

Cameroon Cooked pork Poor hygiene and E. coli 54.4 (6/11)* Conventional Yannick, Rawlings, &
sanitary practices K. pneumoniae 72.7 (8/11)* Emmanuela, 2013
S. aureus, 81.8 (9/11)*
Salmonella 45.4 (5/11)*
Proteus vulgaris 27 (3/11)*
Shigella spp. 9 (1/11)*
Cote d’Ivoire Cooked kebabs Poor hygiene practices C. perfringens 13 (81/222)** Conventional Kouassi, Dadie,
C. difficile 20.5 (27/222)** Nanga, Dje, &
C. sporogenes 21.2 (91/222)** Loukou, 2011
Democratic Bush meat Poor hygiene and Salmonella sp. 56.25 (9/16)* Conventional Makelele et al., 2015
Republic Smoked fish handling practices S. aureus 93.75 (15/16)*
of Congo Salmonella sp. 50 (9/18)*
S. aureus 33.3 (6/18)*
Egypt Shawarma Poor hygienic Listeria species 24 (138/576)* Conventional El-Shenawy et al.,
conditions L. monocytogenes 57 (328/576)* 2011
L. innocua 39 (225/576)*
Egypt Sliced luncheon meat Poor hygiene and food MRSA 37.5 (30/80)* Conventional PCR- El Bayomi et al., 2016
and chicken nuggets handling Restriction Fragment
Length Polymorphism
(RFLP)
Egypt Burger sandwiches Listeria species 60 (6/10)* Conventional Zaghloul et al., 2014
Egypt Shawarma with salads C. jejuni 31.8 (22/69)** Conventional and Elbehiry et al., 2017
S. enterica 13.04 (9/69)** MALDI-TOF
A. baumannii 8.69 (6/69)**
Ethiopia Ambasha Poor hygienic E. coli 19 (4/21)*** Conventional Eromo et al., 2016
conditions Proteus spp. 28.5 (2/7)***
Klebsiella spp. 14.3 (1/7)***
Citrobacter spp. 33.3 (3/9)***
Ethiopia Sambusa Poor hygienic S. aureus 56.2 (9/16)** Conventional Derbew et al., 2013,
Bombolino conditions E. coli 37.5 (6/16)** Conventional Derbew et al., 2013,
Macaroni S. aureus 66.7 (9/12)** Conventional Derbew, Sahle, &
E. coli 50 (6/12)** Endris, 2013
S. aureus 58.3 (7/12)**
E. coli 75 (9/12)**
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

(Continues)
TABLE 2 (Continued)
Region/ Potential source of
Country RTE food contamination Pathogen Prevalence %(n/ N) Analytical technique References
Ghana Ice-kenkey and Macaroni Poor food handling Bacillus sp. 5.9 (8/135)** Conventional Felgo & Sakyi, 2012
Poor food handling CoNS 7.4 (10/135)** Conventional Felgo & Sakyi, 2012
Klebsiella sp. Enterobacter sp. 0.7 (1/135)**
E. coli 0.7 (1/135)**
S. aureus 0.7 (1/135)**
Aeromonas sp. 1.5 (2/135)**
Bacillus sp. 3.0 (4/135)**
CoNS 3.0 (4/135)**
Klebsiella sp. Enterobacter sp. 4.4 (6/135)**
S. aureus 5.9 (8/135)**
Aeromonas sp. 0.7 (1/135)**
0.7 (1/135)**
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

4.4 (6/135)**
Ghana Fried rice Poor hygiene practices E. cloacae, E. coli, K. pneumoniae, NA (NA) Conventional Yeboah-Manu, Kpeli,
and S. aureus Akyeh, & Bimi,
2010
Madagascar RTE pork Poor hygiene practices Salmonella spp. 5.0 (9/178)* Conventional and Cardinale et al., 2015
serology
Nigeria Wara, Kununzaki, Poor hygienic P. aeruginosa, P. putida, and P. NA (NA) Conventional Fadahunsi & Makinde,
Smoked fish, and conditions mendocina 2018
Meat-pie
Nigeria Suya Poor hygienic E. coli, Staphylococcus spp., NA (NA) Conventional Adio, Ovuoraini, &
conditions Pseudomonas spp., C. septicum, Olubunmi, 2014
Micrococcus spp., and B. alvei
Nigeria Locally processed fruit Poor quality water Enterococcus spp., E. coli, Bacillus NA (NA) Conventional Agwa, Ossai-Chidi, &
juice sp., and Staphylococcus sp. Ezeani, 2014
Nigeria Boiled rice and beans Poor food handling E. coli 100 (5/5)* Conventional Bukar et al., 2009
Bread E. coli 40 (2/5)* Bukar et al., 2009
Zobo drink E. coli 20 (1/5)* Bukar et al., 2009,
S. typhi 20 (1/5)* Bukar et al., 2009
Nigeria Akara and fried potato Poor food handling S. aureus and E. coli NA (NA) Conventional Madueke, Awe, &
practices Jonah, 2014
Fried yam Poor food handling K. pneumoniae NA (NA) Conventional Madueke et al., 2014
practices
Nigeria Cooked meat Poor hygiene and Salmonella spp. 18 (9/50)* Conventional and PCR Smith et al., 2012
sanitation practice
(Continues)
7
 8

TABLE 2 (Continued)
Region/ Potential source of
Country RTE food contamination Pathogen Prevalence %(n/ N) Analytical technique References
Nigeria Meat pie Poor food handling Bacillus spp. 85.0 (153/180)* Conventional Obande, Umeh, Azua,
practices S. aureus 38.9 (70/180)* Chuku, & Adikwu,
Klebsiella spp. 18.9 (34/180)* 2018
Proteus spp. 17.8 (32/180)*
E. coli 10.0 (18/180)*
Shigella spp. 5.0 (9/180)*
Citrobacter 5.0 (9/180)*
Nigeria Egg roll B. atrophaeus and B. NA (NA) 16S rDNA sequencing Aruwa & Ogunlade,
amyloliquefaciens 2016
Meat pie B. thuringiensis and B. subtilis NA (NA) 16S rDNA sequencing Aruwa & Ogunlade,
2016
Buns B. licheniformis NA (NA) 16S rDNA sequencing Aruwa & Ogunlade,
2016
Kenya Street vended meat Poor hygiene practices S. aureus 66.7 (6/9)* Conventional and PCR Gitahi, Wangoh, &
Njage, 2012
Rwanda Boiled beef, grilled Poor hygiene practices Salmonella 11.7 (35/300)* Conventional Niyonzima et al., 2017
chicken, grilled goat
meat, grilled rabbit,
and fried pork
Sudan Um-Jinger Poor hygiene practices Bacillus spp. 70.0 (42/60)* Conventional Abdallah & Mustafa,
S. aureus 68.3 (41/60)* 2010
E. coli 6.6 (4/60)*
Salmonella spp. 5 (3/60)*
Proteus spp. 8.3 (5/60)*
Sudan Shawarma Poor food handling E. coli NA (NA) Conventional Elfaki & Elhakim,
S. aureus 2011
Salmonella
Tanzania Raw juice Poor hygiene practices E. coli 63.3 (19/30)* Conventional Nonga et al., 2015
Tunisia Cooked poultry meat B. cereus 32.7 (18/55)* Conventional, PCR, and Gdoura-Ben Amor
Pulsed-Field Gel et al., 2018
Electrophoresis
(PFGE)
pastries B. cereus 46.2 (37/80)* Conventional, PCR, and Gdoura-Ben Amor
PFGE et al., 2018
Asia
Bangladesh Sweets and dairy Poor hygiene and V. cholerae NA (NA) Conventional Mrityunjoy et al., 2013
products sanitation practice
(Continues)
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …
TABLE 2 (Continued)
Region/ Potential source of
Country RTE food contamination Pathogen Prevalence %(n/ N) Analytical technique References
Bangladesh Chotpoti Poor hygiene Acinetobacter 66 (71/108)* Conventional Hassan et al., 2016
E. coli 3 (3/108)*
Klebsiella spp. 54 (58/108)*
Proteus spp. 0.9 (1/108)*
Bangladesh Chatpati Poor hygiene practices Cronobacter sakazakii 100 (3/3)* Conventional Tabashsum et al., 2013
Listeria spp. 33.3 (1/3)*
Salmonella spp. 66.7 (2/3)*
Yersinia spp. 100 (3/3)*
Bangladesh Jhalmuri Poor food handling Coliform bacteria 59.1 (13/22)* Conventional Al Mamun et al.,
practices 2013a
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

Chotpoti Poor food handling Coliform bacteria 29.4 (5/17)* Conventional Al Mamun et al.,
practices 2013a
Indonesia RTE noodle with chicken Poor hygiene Coliform bacteria NA (NA) Conventional Adolf & Azis, 2012
and S. aureus
India Fruit juice Poor water quality, E. coli 40 (31/77)** Conventional Tambekar et al., 2009
unhygienic Pseudomonas spp. 25 (19/77)**
conditions Salmonella spp. 16 (12/77)**
Klebsiella spp. 3 (2/77)**
India RTE foods Poor hygiene practices E. coli 74 (37/50)* Conventional, RFLP Biswas et al., 2010
India Chowmein Poor hygiene practices B. cereus, E. coli, Salmonella, and NA (NA) Conventional Chauhan, Uniyal, &
Shigella Rawat, 2015
India Ice cream Poor hygiene and Y. intermedia 5 (1/20)* Conventional and PCR Divya & Varadaraj,
sanitary practices 2011
Pani puri Y. intermedia 4 (2/20)* Conventional and PCR Divya & Varadaraj,
2011
Bread sandwiches Y. enterolitica 5 (1/20)* Conventional and PCR Divya & Varadaraj,
2011
India Chutney B. cereus (Biotype 6) 38.46 (5/13)** Conventional Hafeez, Iqbal, &
B. cereus (Biotype 5) 23.07 (3/13)** Ahmad, 2012
Mutton tikka B. cereus (Biotype 3) 29.63 (8/27)** Conventional Hafeez et al., 2012
B. cereus (Biotype 4) 25.93 (7/27)**
India Bread chop and Samosa Poor hygiene practices Bacillus and Staphylococcus NA (NA) Conventional and Kharel et al., 2016
Serology
(Continues)
9
 10

TABLE 2 (Continued)
Region/ Potential source of
Country RTE food contamination Pathogen Prevalence %(n/ N) Analytical technique References
India Dairy products Poor food handling MRSA NA (NA) Conventional, Manukumar &
practices MALDI–TOF, and Umesha, 2017
PCR
Nepal Fried rice Poor hygiene practices B. cereus 23.8 (5/21)** Conventional Ankita et al., 2012
S. aureus 19 (4/21)**
S. typhi 9.5 (2/21)**
Nepal Chicken momo, samosa Poor hygiene and poor Staphylococcus and Salmonella NA (NA) Conventional Bohara, 2018
food handling
practices
Nepal Puri Poor hygiene and poor S. aureus 55.5 (20/36)** Conventional Khadka, Adhikari, Rai,
food handling E. coli 5.5 (2/36)** Ghimire, & Parajuli,
practices B. cereus 27.7 (10/36)** 2018
Citrobacter spp. 11 (4/36)**
Pakistan Pasteurized juice Poor hygiene practices E. coli, Salmonella, NA (NA) Conventional Batool et al., 2013
Staphylococcus, and Pseudomonas
India Panipuri Poor hygiene practices E. coli 6.25 (5/80)* Conventional Kiranmai, Siva
Klebsiella spp. 2.5 (2/80)* Kamesh, Divija, &
Sara, 2016
Philippines Hot grilled pork, hot Poor hygiene practices E. coli, S. aureus, B. cereus, and NA (NA) PCR-based detection Manguiat & Fang,
grilled chicken Salmonella kits 2013
Vietnam Grilled pork meat Poor hygiene practices S. aureus 21.8 (7/32)* Conventional and RFLP Huong et al., 2009
Ice cream S. aureus 25 (3/12)* Conventional and RFLP Huong et al., 2009
Fermented meat S. aureus 13.8 (4/29)* Conventional and RFLP Huong et al., 2009
Note. Abbreviations: n, number of pathogen; N, number of samples/isolates/particular species; NA, not available; A. baumannii, Acinetobacter baumannii; B. cereus, Bacillus cereus; B. alvei, Bacillus alvei; C. difficile, Clostridium
difficile; C. perfringens, Clostridium perfringens; C. sporongenes, Clostridium sporongenes; C. septicum, Clostridium septicum: CoNS, coagulase negative staphylococci; E. coli, Escherichia coli; E. cloacae, Enterobacter cloacae;
K. pneumonia, Klebsiella pneumonia; MRSA, Methicillin-resistant S. aureus; P. aeruginosa, Pseudomonas aeruginosa; P. putida, Pseudomonas putida; P. mendocina, Pseudomonas mendocina; S. aureus, Staphylococcus aureus;
Y. intermedia, Yersinia intermedia; Y. enterolitica, Yersinia enterolitica.
* Number of samples
**
Number of isolates
***
Number of a particular species
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW … 11

sensitive LC/MS–MS) are applied to give a more precise Africa) (Somda et al., 2018). Similarly, Pseudomonas was
result and accurately quantify the concentration levels of mul- detected in street-vended juice in Pakistan, (Batool, Tahir,
tiple mycotoxins in several foods (Berthiller et al., 2018; Rauf, & Kalsoom, 2013), whereas in Bangladesh (Asia)
Malachova, Sulyok, Beltran, Berthiller, & Krska, 2014). The and Ethiopia, Klebsiella was found to contaminate chotpoti
application of these high-end techniques represents the gold and ambasha, respectively (Eromo, Tassew, Daka, & Kibru,
standards for detection of multiple mycotoxins in food. How- 2016; Hassan et al., 2016).
ever, these techniques are expensive and there is lack of skilled
expertise in most LMICs, which makes routine application 5.2 Gram-positive bacteria
impracticable.
Notable foodborne pathogens within this group (such as,
Bacillus, Listeria, and Staphylococcus) are able to tolerate
harsh food storage and processing conditions such as low tem-
5 PAT H O G E N I C BAC T E R I A I N
perature, low moisture content, and high acidity and salinity
RTEs FROM L MI C s
(De Noordhout et al., 2014; Kadariya, Smith, & Thapaliya,
The ability of pathogenic bacteria to proliferate in RTEs 2014; Stecchini, Del Torre, & Polese, 2013; Swarminathan
depends on several intrinsic (for example, nutrient compo- & Smidt, 2007). These capabilities make them a major con-
sition) and extrinsic (for example, environmental tempera- cern to food safety. Some species (such as, Listeria mono-
ture) factors (Smith & Fratamico, 2005). Upon consumption cytogenes) are opportunistic in nature and can cause high
of contaminated foods, pathogenic bacteria can cause a wide mortality rates among infants, older adults, and immunocom-
range of adverse health effects including gastrointestinal- promised individuals (Guillet et al., 2010; Nyenje, Green, &
related diseases, thus constituting a huge health risk to con- Ndip, 2012). There have been several reports on contamina-
sumers. The development of adverse health effects is, how- tion of RTEs by Gram-positive bacteria especially Bacillus
ever, dependent on several factors including, but not limited species, Listeria species, and Staphylococcus aureus across
to, number of pathogenic bacteria present in the food, age, and LMICs (Table 2). Staphylococcus aureus was detected in
grilled pork meat, ice cream, and fermented meat in Vietnam
level of immunity of the consumer. In this section, we have
(Asia) (Huong et al., 2009), whereas Bacillus species were
clustered the diverse bacteria reported in RTEs across LMICs
recovered from Um-Jinger in Sudan (North Africa) (Abdal-
into two broad groups: Gram-negative and Gram-positive.
lah & Mustafa, 2010). In Nepal (Asia) and India, S. aureus
were also recovered from fried rice and samosa, respec-
5.1 Gram-negative bacteria tively (Ankita, Prasad, & Umesh, 2012; Kharel et al., 2016).
This group of bacterial species can be found in a wide range In addition, Tabashsum et al. (2013) and Zaghloul et al.
of habitats including the gastrointestinal tract of humans and (2014) reported Listeria in pitha and burger sandwiches from
animals. They contribute significantly to the FBD burden in Bangladesh and Egypt (North Africa), respectively. In another
LMICs (Kirk et al., 2015a, 2015b). Of major concern to food study in the Democratic Republic of Congo, S. aureus was
safety is the ability of some members, for example, Vibrio recovered from bush meat (Makelele et al., 2015). Diverse
cholerae and Salmonella spp., to transfer and/or acquire species of Bacillus, including B. cereus, were also detected
virulent genes thereby leading to the proliferation of highly in several RTEs including meat pie, buns, and jollof rice from
virulent strains (Alcaine et al., 2005; Seitz & Blokesch, Nigeria (Aruwa & Ogunlade, 2016). Similarly, in Tunisia, B.
2013). Consequently, the presence of these strains in food cereus contaminated cooked poultry meat and pastry products
could render it unsafe for human consumption and obviously (Gdoura-Ben Amor et al., 2018).
threaten the health of the consumers. Diverse Gram-negative
bacteria have been reported to contaminate RTEs across
LMICs (Table 2). Among these, E. coli, Klebsiella species, 6 BAC T E R I A L TOX I N S I N RT E s
Salmonella, and Pseudomonas were commonly reported. FROM LMICs
Abdallah and Mustafa (2010) and Bukar, Uba, and Oyeyi
(2009) detected Salmonella in street-vended juice in Sudan Beyond the mere presence of pathogenic bacteria in RTEs,
(North Africa) and in zobo from Nigeria (West Africa), bacteria sometimes secrete potent toxins that could pose addi-
respectively. In addition, Biswas, Parvez, Shafiquzzaman, tional health risks to the food consumers. Of particular impor-
Nahar, and Rahman (2010) and Yannick, Rawlings, & tance are cereulide, botulinum toxin, and staphylococcal exo-
Emmanuela (2013) reported the presence of E. coli in toxins discussed hereafter. Generally, there are sparse data
RTE meat from Bangladesh (Asia) and Cameroon (Central on the detection of bacterial toxins in RTEs from LMICs in
Africa), respectively, whereas diarrheagenic E. coli strains the decade under study. Obvious reasons include (a) lack of
were recovered from grilled chicken in Burkina Faso (West trained personnel and equipment for detection of bacterial
12 M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

toxins in RTEs and (b) possible biased interest of food micro- implicated in S. aureus contamination include cakes, dairy
biologists toward viable bacteria than on their toxins. products, flour-based products, meat pie fillings, salads, and
sandwiches (Argudin et al., 2010). El Bayomi et al. (2016)
reported the incidence of S. aureus in RTE chicken prod-
6.1 Botulinum toxin ucts in Egypt, but did not report the production of staphy-
The botulinum toxin is a potent neurotoxin produced by toxi- lococcal exotoxin by the bacterial isolates or its presence in
genic strains of Clostridium botulinum (Popoff, 2013). Inges- the RTE. However, Huong et al. (2009) reported that 40%
tion of botulinum toxin through consumption of RTEs may (n = 45) of S. aureus recovered from RTEs in Vietnam were
result in botulism, a neuroparalytic disease that could be fatal enterotoxigenic.
in humans (Johnson & Montecucco, 2018). The presence of
the botulinum toxin gene (BoNt/A) was reported in 4% of
toxigenic strains of Clostridium species isolated from RTEs 7 F UNGAL CONTAM INATIO N OF
in Nigeria (Chukwu et al., 2016). However, no study has RTEs F RO M LM ICs
reported the presence of the toxin in RTEs in LMICs within
the period under review. Fungal contamination of RTEs is commonplace in LMICs due
to vendor practice of displaying the foods openly in markets,
6.2 Cereulide such that they are exposed to fungal spores. Diverse fungal
genera contaminate food materials, but the frequently occur-
Cereulide is an emetic exotoxin from certain Bacillus cereus ring ones in RTEs include Aspergillus, Fusarium, Mucor,
strains. It is highly stable at extreme temperature and pH, with Penicillium, and Rhizopus. Aspergillus and Fusarium were
report on stability at 121 ◦ C for 2 hr and over the pH range reported to contaminate retailed kulikuli (peanut cake) and
of 2 to 11, which makes it very difficult to inactivate dur- salads from Benin Republic, Togo, and Nigeria (Adjou et al.,
ing food processing (Ceuppens et al., 2011; Rajkovic, Uyt- 2012; Adjrah et al., 2013; Ezekiel et al., 2011). Similarly,
tendaele, & Debevere, 2005). Additionally, cereulide is par- Aspergillus and Penicillium were reported in street-vended
ticularly toxic to infants, sometimes causing acute toxicity doughnut, egg roll, and meat pie from Nigeria (Oranusi
(Shiota et al., 2010). Cereulide is able to contaminate a range & Braide, 2012). In India, Mucor and Rhizopus contam-
of RTEs such as improperly cooked and stored rice, pasta, inated street-vended rice-based bhelpuri (Das, Nagananda,
eggs, milk, and meat (Ceuppens, Boon, & Uyttendaele, 2013). Bhattacharya, & Bhardwaj, 2010). Although diverse fungal
To worsen the scenario, this toxin sometimes co-occurs with propagules can be recovered in RTEs, these viable fungi pose
other potent fungal toxins in RTEs. Such co-occurrence may far less public health menace compared to the occurrence of
lead to additive and/or synergistic effects that could possi- their toxic secondary metabolites (mycotoxins) liberated into
bly compound the health risk to consumers upon ingestion the foods.
(Beisl et al., 2019). Recently, one LC–MS/MS-based study
reported the presence of cereulide (mean: 37 𝜇g/kg) in all
50 RTE maize fufu from Cameroon, with 20% and 100% co-
7.1 Mycotoxins in RTE ingredients
occurrence of aflatoxins and deoxynivalenol, respectively, in Several RTEs in LMICs are mostly cereal and nut based.
addition to other mycotoxins (Abia et al., 2017). These ingredients are known to be prone to toxigenic fun-
gal contamination. Mycotoxigenic fungal species within the
Aspergillus, Fusarium, Penicillium, and Alternaria genera
6.3 Staphylococcal exotoxins
can proliferate and produce toxic metabolites in the crops
The staphylococcal exotoxin is a heat stable super-antigenic under favorable climatic conditions and poor pre- and posthar-
toxin (SAgs) produced predominantly by coagulase positive vest practices, similar to those prevalent in tropical and
and a few coagulase negative Staphylococci (Even, Leroy, & subtropical regions where many LMICs are situated (Bankole,
Charlier, 2010; Zell et al., 2008). Staphylococcal exotoxins Schollenburger, & Drochner, 2006; Bhat & Vasanthi, 2003;
are responsible for food poisoning and toxic shock syndrome IARC, 2015). The major mycotoxins of food safety impor-
often characterized by vomiting, especially in immunocom- tance include aflatoxins (AFs), fumonisins (FUM), ochratoxin
promised individuals (Argudin, Mendoza, & Rodicio, 2010; A (OTA), citrinin, deoxynivalenol (DON), and zearalenone
Hennekinne, De Buyser, & Dragacci, 2012; Hu et al., 2007; (ZEN).
Pinchuk, Beswick, & Reyes, 2010; Schelin et al., 2011). Recent data on mycotoxin occurrence in raw grains from
Staphylococcal food poisoning can be traced to poor han- Africa and Asia allude to the severity of the mycotoxin
dling of foods by handlers carrying enterotoxigenic S. aureus menace in these regions (Ayalew, Hoffmann, Lindahl, &
in their hands or noses, which may contaminate food prod- Ezekiel, 2016; Ezekiel et al., 2018; Misihairabgwi, Ezekiel,
ucts during packaging (Argudin et al., 2010). RTEs commonly Sulyok, Shephard, & Krska, 2019; Pereira, Fernandes, &
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW … 13

Cunha, 2014). Of particular importance are AFs, FUM, and beauvericin and OTA in peanut cake from Nigeria (Ezekiel,
DON, which appear to occur more frequently at high levels Sulyok, et al., 2012); DON, patulin, and ZEN in maize
in raw grains. Typical examples are the very high levels of fufu from Cameroon (Abia et al., 2017); and OTA in garba
AFs in groundnuts from Nigeria (max: 2,076 𝜇g/kg) and from Cote d’Ivoire (West Africa) (Anoman, Koffi, Aboua,
Sierra Leone (max: 5,729 𝜇g/kg) (Oyedele et al., 2017; & Koussemon, 2018). In some other RTEs, several other
Sombie et al., 2018), and in maize from Tanzania (max: mycotoxins, aflatoxins excluded, have also been reported
1,081 𝜇g/kg) and Somalia (max: 1,407 𝜇g/kg) (Kamala (sometimes in co-occurrence). These include DON in fried
et al., 2015; Probst, Bandyopadhyay, & Cotty, 2014). To maize and popcorn from Indonesia (Asia) (Setyabudi, Nury-
worsen the scenario, several mycotoxins often co-occur in ono, Wedhastri, Mayer, & Razzazi-Fazeli, 2012), OTA in
RTE ingredients from LMICs. For example, AFs, FUM, and garri from Nigeria (Makun et al., 2013), OTA in biscuits and
DON have been reported to simultaneously occur in maize bread from Pakistan (Majeed, Khaneghah, Kadmic, Khanf, &
from Burkina Faso, Cameroon, Mozambique, and Nigeria Shariatig, 2017), and DON, FUM, T-2 toxin and ZEN in garri
(Abia et al., 2013; Adetunji et al., 2014; Warth et al., 2012), from Nigeria (Chilaka, De Boevre, Atanda, & De Saeger,
whereas AFs and OTA co-occurred in rice from Pakistan 2018). A major concern is that many of the RTEs contained
(Majeed, Iqbal, Asi, & Iqbal, 2013). mycotoxin levels higher than maximum limits stipulated by
the Codex Alimentarius and the European Union.

7.2 Mycotoxins in RTEs

Processing techniques (such as grain washing, fermentation, 8 PARAS ITES IN RTEs F RO M
dilution, and heat treatment) routinely applied during RTE LMICs
production may influence mycotoxin levels in the finished
product (Ezekiel, Ayeni, et al., 2019; Ezekiel, Sulyok, et al., In addition to the contamination of RTEs by bacteria, fungi,
2019; Karlovsky et al., 2016; Okeke et al., 2015, 2018). and their toxic metabolites, parasites can also contaminate
Nonetheless, mycotoxins in ingredients are commonly car- RTEs (Ayeni, Ofem, Duru, Oyedele, & Ezekiel, 2019; Manyi
ried over to the final product albeit in varying concentrations et al., 2014). Parasitic contamination is usually common in
depending on the toxin levels in the starting raw material meat-based RTEs. The major contamination sources include
(Ezekiel et al., 2015; Ezekiel, Ayeni, et al., 2019; Matumba the improperly cooked or roasted meat, contaminated water
et al., 2014; Okeke et al., 2015). Mycotoxin carry-over is typ- applied to wash the meats, and the slaughter environments.
ical, particularly in resource scarce rural settings, where local Although not much studies have been conducted in this
food processors commonly apply low-quality grains in the regard, possibly due to perceived less severity of parasitic
production of RTEs because high-quality grains are often sold infections in humans, it is important to always determine the
for household income (Ayalew et al., 2016; Misihairabgwi presence of all potential hazards in foods. This will ensure
et al., 2019). Consequently, human consumption of mycotoxin consumers are protected and they can have confidence in the
contaminated RTEs could constitute health hazards and some safety of the foods.
of which could include, but are not limited to, cancers, gas- Only two reports were found for the presence of parasites
trointestinal barrier alterations, immunosuppression, growth in RTEs in LMICs in the decade under review (Table 4).
faltering, and nephrotoxicity (IARC, 2015). Toxoplasma gondii was reported in barbeque chicken, mutton
Details of mycotoxin contamination levels in RTEs across kebab, and sausages from Egypt (Abd El-Razik et al., 2014),
LMICs in the decade under review are highlighted in Table 3. whereas Ascaris lumbricoides, Entamoeba histolytica, Giar-
Aflatoxins appear to be the most frequently studied mycotox- dia lamblia, and Taenia sp. were found in roasted meat (suya)
ins in RTEs in LMICs, possibly due to their categorization in Nigeria (Manyi et al., 2014). Suffice to say that contrary to
as the most toxic and carcinogenic of all mycotoxins (IARC, the perceived less severity of parasitic infections in humans,
1993). Obviously, massive contamination levels in this these infections can be deadly especially when parasites
group of foods widely consumed by all age groups have been migrate to unwanted body organs or cause perforations of
reported in literature. Concentration ranges of the most potent intestinal walls leading to severe complications (Tardieux
carcinogenic mycotoxin, aflatoxins, have reached 2,820 and & Menard, 2008). In addition, the combined risk of acute
3,328 𝜇g/kg in peanut cake (kulikuli) and roasted peanuts bacterial infection, chronic mycotoxin exposure, and parasitic
from Nigeria and Sierra Leone, respectively (Ezekiel, Sulyok, infections in affected humans cannot be underestimated.
Warth, Odebode, & Krska, 2012; Sombie et al., 2018). In Perhaps one major possible effect of such combined risk
addition, other mycotoxins have been reported to co-occur may be a contribution to malnutrition and growth faltering
with aflatoxins in RTEs from several countries. These include in children due to alterations of intestinal/gut integrity by
OTA in peanut cake from Benin (Adjou et al., 2012; Ediage, mycotoxins, low assimilation of essential nutrients within the
Mavungu, Monbaliu, Van Peteghem, & De Saeger, 2011); body system as a result of the parasites feeding on required
 14

TABLE 3 Mycotoxins in ready-to-eat foods from low-and middle-income countries (2009 to 2018)
Region/Country Ready-to-eat food aN bN
p (%) LOD(𝝁g/kg) LOQ(𝝁g/kg) Mycotoxins Mean(𝝁g/kg) Range(𝝁g/kg) Analytical method References
Africa
Benin Kuli kuli 45 ND NA NA AFB1 ND 25.5 to 455 ELISA & LC–MS/MS Adjou et al., 2012
ND NA NA AFB2 ND 33.9 to 491 ELISA & LC–MS/MS Adjou et al., 2012
ND NA NA AFG1 ND 0.41 to 100 ELISA & LC–MS/MS Adjou et al., 2012
ND NA NA AFG2 ND 22.0 to 87.7 ELISA & LC–MS/MS Adjou et al., 2012
ND NA NA OTA ND 0.3 to 2.0 ELISA & LC–MS/MS Adjou et al., 2012
Benin Peanut cake 15 14 (93) 2 6 AFB1 ND <LOQ to 282 LC/MS–MS Ediage et al., 2011
4 (27) 1 4 AFB2 ND <LOQ to 31.0 LC/MS–MS Ediage et al., 2011
10 (67) 1 3 AFG1 ND <LOQ to 79.0 LC/MS–MS Ediage et al., 2011
15 (100) 0 1 AFG2 ND 6.0 to 96.0 LC/MS–MS Ediage et al., 2011
5 (33) 0.1 0.3 OTA ND <LOQ to 2.0 LC/MS–MS Ediage et al., 2011
Cameroon Maize fufu 50 12 (24) 0.15 0.5 AFB1 0.9 ND to 1.8 LC–MS/MS Abia et al., 2017
50 (100) 3.2 10 FB1 151 48.0 to 709 LC–MS/MS Abia et al., 2017
50 (100) 0.8 2.6 DON 23 14.0 to 55.0 LC–MS/MS Abia et al., 2017
15 (30) 5 17 PAT 105 12.0 to 890 LC–MS/MS Abia et al., 2017
50 (100) 0.1 0.3 ZEN 49 5.0 to 150 LC–MS/MS Abia et al., 2017
Cote d’ Ivore Garba 300 170 (57) 0.00564 0.0188 AFB1 3.44 0.02 to 35.8 HPLC Anoman et al., 2018
70 (23) 0.00151 0.0050 AFB2 1.90 0.10 to 24.0 HPLC Anoman et al., 2018
140 (47) 0.00136 0.0045 AFG1 8.07 0.56 to 69.3 HPLC Anoman et al., 2018
120 (40) 0.00143 0.0047 AFG2 0.56 0.04 to 13.3 HPLC Anoman et al., 2018
190 (63) 0.0500 0.20 OTA 0.42 0.06 to 1.83 HPLC Anoman et al., 2018
Egypt Corn based snack 25 10 (40) NA 0.5 AFB1 3.85 0.59 to 15.8 HPLC Amin, Abo-Ghalia,
& Hamed, 2010
1 (4) NA 0.5 AFB2 1.98 1.98 HPLC Amin et al., 2010
Egypt Hard cheese 50 19 (38) 50 ng/kg NA AFM1 132 51.6 to 182 ELISA Amer & Ibrahim,
2010
Soft cheese 50 20 (40) 50 ng/kg NA AFM1 70.6 52.0 to 87.6 ELISA Amer & Ibrahim,
2010
Processed cheese 50 11 (22) 50 ng/kg NA AFM1 52.5 51.8 to 54.0 ELISA Amer & Ibrahim,
2010
Egypt Fresh kariesh cheese 25 8 (32) NA NA AFM1 3.6 1.95 to 6.11 Immuno affinity column Awad, Amer,
with flurometric assay Mansour, &
Ismail, 2014
(Continues)
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …
TABLE 3 (Continued)
Region/Country Ready-to-eat food aN bN
p (%) LOD(𝝁g/kg) LOQ(𝝁g/kg) Mycotoxins Mean(𝝁g/kg) Range(𝝁g/kg) Analytical method References
Damietta cheese 25 12 (48) NA NA AFM1 6.7 1.54 to 14.7 Immuno affinity column Awad, Amer,
with flurometric assay Mansour, &
Ismail, 2014
Ghana Ice-kenkey ND ND NA NA AFB1 ND 7.01 to 20.5 HPLC Atter, Ofori,
Anyebuno,
Amoo-Gyasi, &
Amoa-Awua,
2015
ND ND NA NA AFB2 ND 0.51 to 1.63 HPLC Atter et al., 2015
ND ND NA NA AFG1 ND 0.0 to 0.47 HPLC Atter et al., 2015
Kenya Roasted coated 101 ND NA NA AFs 56.5 0.0 to 382 ELISA Nyirahakizimana
Peanut et al., 2013
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

Roasted de-coated 49 ND NA NA AFs 19.9 0.0 to 201 ELISA Nyirahakizimana

peanut et al., 2013
Kenya Peanut butter 12 12 (100) NA NA AFs ND ND VICAM AflaTest Filbert & Brown,
immunoaffinity 2012
fluorometric method
Malawi Locally processed 14 14 (100) NA 0.5 AFB1 ND 13.2 to 40.6 Immuno-affinity Matumba et al., 2014
peanut butter column and reversed
phase liquid
chromatography
14 14 (100) NA 0.2 AFB2 ND 1.7 to 7.2 Immuno-affinity Matumba et al., 2014
column and reversed
phase liquid
chromatography
De-skinned roasted 15 11 (73) NA 0.5 AFB1 ND 0.1 to 12.3 Immuno-affinity Matumba et al., 2014
groundnut column and reversed
phase liquid
chromatography
15 10 (67) NA 0.2 AFB2 ND 0.2 to 1.8 Immuno-affinity Matumba et al., 2014
column and reversed
phase liquid
chromatography
Nigeria Corn based snack 3 3 (100) NA NA AFB1 14 6.0 to 30.0 Thin Layer Ezekiel, Kayode,
Chromatography Fapohunda,
(TLC) Olorunfemi, &
Kponi, 2012
(Continues)
15
TABLE 3 (Continued)
16

Region/Country Ready-to-eat food aN bN

p (%) LOD(𝝁g/kg) LOQ(𝝁g/kg) Mycotoxins Mean(𝝁g/kg) Range(𝝁g/kg) Analytical method References
AFB2 8.0 ND TLC Ezekiel, Kayode,
et al., 2012
AFG1 6.0 ND TLC Ezekiel, Kayode,
et al., 2012
Groundnut based 12 9 (75) NA NA AFB1 8.5 0.0 to 12.5 TLC Ezekiel, Kayode,
snack et al., 2012
AFB2 9.0 0.0 to 9.0 TLC Ezekiel, Kayode,
et al., 2012
AFG1 15.8 0.0 to 31.3 TLC Ezekiel, Kayode,
et al., 2012
Nut-based snack 5 1 (20) NA NA AFB1 6.0 ND TLC Ezekiel, Kayode,
et al., 2012
Wheat-based snack 5 4 (80) NA NA AFB1 17.8 0.0 to 50.0 TLC Ezekiel, Kayode,
et al., 2012
AFG1 13 ND TLC Ezekiel, Kayode,
et al., 2012
Nigeria Peanut cake 29 29 (100) 2.0 NA AFB1 ND ND to 2820 LC/ESI–MS/MS Ezekiel, Sulyok,
et al., 2012
29 (100) 0.02 NA BEAU ND ND LC/ESI–MS/MS
4 (14) 4.0 NA OTA ND ND LC/ESI–MS/MS
Nigeria Kokoro 16 8 (50) NA NA AFB1 ND 0.75 to 7.25 ELISA Onifade, Adesokan,
& Adebayo-Tayo,
2014
Nigeria Roasted groundnut 22 21 (96) 2 NA AFB1 14.1 1.3 to 59.1 High-Performance Afolabi et al., 2015
Thin Layer
Chromatography
(HPTLC)
18 (82) 2 NA tAF 23.9 1.3 to 134 HPTLC Afolabi et al., 2015
Nigeria Roasted cashew nut 27 ND NA NA AF ND 0.1 to 6.8 ELISA Adetunji, Alika,
Awa, Atanda, &
Mwanza, 2018
Nigeria Roasted groundnut 10 6 (60) NA NA tAF ND 1.20 to >20.0 ELISA Ubwa et al., 2014
Roasted cashew nut 10 2 (20) NA NA tAF ND 0.10 to 0.40 ELISA Ubwa et al., 2014
Nigeria Garri 18 18 (100) 0.001 NA OTA 7.63 3.28 to 22.7 HPLC Makun et al., 2013
Nigeria Garri 24 9 (38) 14.5 29.0 DON 57 35.0 to 99.0 LC–MS/MS Chilaka et al., 2018
6 (25) 15.0 30.0 FB1 60 45.0 to 80.0 LC–MS/MS Chilaka et al., 2018
5 (21) 10.5 21.1 FB2 40 29.0 to 65.0 LC–MS/MS Chilaka et al., 2018
3 (13) 4.5 9.1 T-2 19 17.0 to 22.0 LC–MS/MS Chilaka et al., 2018
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

(Continues)
TABLE 3 (Continued)
a b
Region/Country Ready-to-eat food N Np (%) LOD(𝝁g/kg) LOQ(𝝁g/kg) Mycotoxins Mean(𝝁g/kg) Range(𝝁g/kg) Analytical method References
4 (17) 3.6 7.2 ZEN 14 11.0 to 17.0 LC–MS/MS Chilaka et al., 2018
Nigeria Aadun 5 5 (100) NA NA AFB1 ND 3.4 to 12.8 HPLC Jonathan et al., 2015
NA NA AFB2 ND 2.8 to 3.2 HPLC Jonathan et al., 2015
AFG1 ND 1.7 to 3 HPLC Jonathan et al., 2015
NA NA AFG2 ND 1.6 to 3.2 HPLC Jonathan et al., 2015
Nigeria Sausage roll 4 4 (100) NA NA AFB1 ND 1.08 to 1.88 HPLC/MS Jonathan, Okoawo,
& Asemoloye,
2016
NA NA AFB2 ND 0.99 to 1.98 HPLC/MS Jonathan et al., 2016
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

NA NA AFG1 ND 0.92 to 1.23 HPLC/MS Jonathan et al., 2016

NA NA AFG2 ND 0.91 to 1.73 HPLC/MS Jonathan et al., 2016
Sierra Leone Roasted peanut 50 8 (16) 0.24 0.79 AFB1 178 0.62 to 1,387 LC–MS/MS Sombie et al., 2018
3 (6) 0.4 1.3 AFB2 96.4 6.49 to 271 LC–MS/MS Sombie et al., 2018
12 (24) 0.32 1.1 AFG1 281 0.34 to 3,328 LC–MS/MS Sombie et al., 2018
2 (4) 0.8 2.6 AFG2 378 14.7 to 742 LC–MS/MS Sombie et al., 2018
2 (4) 0.4 1.3 AFM1 34 1.22 to 66.8 LC–MS/MS Sombie et al., 2018
Sudan Peanut butter 43 28 (65) 1.5 NA AFB1 223 73.9 to 534 HPLC Elzupir, Salih,
Suliman, Adam,
& Elhussein, 2011
42 (98) 0.09 NA AFB2 3.2 0.18 to 23.9 HPLC Elzupir et al., 2011
43 (100) 0.8 NA AFG1 137 26.5 to 401 HPLC Elzupir et al., 2011
4 (9) 0.4 NA AFG2 18.5 8.60 to 30.1 HPLC Elzupir et al., 2011
43 (100) NA NA tAF 287 26.6 to 853 HPLC Elzupir et al., 2011
Zambia Peanut butter 109 100 (92) NA NA AFs 18.9 1.75 to 147 CD–ELISA Banda, Likwa,
Bwembya, Banda,
& Mbewe, 2018
Zimbabwe Peanut butter 11 10 (91) NA NA AFB1 51 3.7 to 191 HPLC Mupunga, Lebelo,
Mngqawa,
Rheeder, &
Katerere, 2014
(Continues)
17
 18

TABLE 3 (Continued)
Region/Country Ready-to-eat food aN bN
p (%) LOD(𝝁g/kg) LOQ(𝝁g/kg) Mycotoxins Mean(𝝁g/kg) Range(𝝁g/kg) Analytical method References
4 (36) NA NA AFB2 ND 6.2 to 25.7 HPLC Mupunga et al., 2014
5 (45) NA NA AFG1 ND 9.3 to 47.1 HPLC Mupunga et al., 2014
1 (9) NA NA AFG2 ND 0 to 8.8 HPLC Mupunga et al., 2014
10 (91) NA NA tAF 75.7 6.1 to 247 HPLC Mupunga et al., 2014
Asia
India Chilgoza pine nuts 58 11 (19) NA NA AFB1 0.91 0.73 to 1.64 TLC & HPLC Sharma, Gupta, &
Sharma, 2013
13 (22) NA NA AFB2 1.01 0.70 to 2.26 TLC & HPLC Sharma et al., 2013
India Jam 40 20 (50) NA NA AFB1 ND 1.52 to 183 HPLC Nair, Ghadevaru,
Manimehali, &
Athmaselvi, 2015
Indonesia Popcorn 7 7 (100) 20 NA DON 127 59.9 to 202 HPLC–UV Setyabudi, Nuryono,
Wedhastri,
Mayerm, &
Fazeli, 2012
Fried maize 9 9 (100) 20 NA DON 155 67.1 to 348 HPLC–UV Setyabudi et al.,
2012
Pakistan Biscuit 10 3 (20) 0.01 0.02 to 0.05 tAF ND 0.04 to 2.28 RP–HPLC Mushtaq, Sultana,
Anwar, Khan, &
Ashrafuzzaman,
2012
Bread slice 3 1 (33) 0.01 0.02 to 0.05 tAF ND 0.1 to 0.26 RP–HPLC Mushtaq et al., 2012
Pakistan Biscuit 5 2 (40) NA NA OTA 23.9 ND to 360 LC Majeed et al., 2017
Bread 5 3 (60) NA NA OTA 1.96 ND to 4.66 LC Majeed et al., 2017
The Caribbean
Haiti Peanut butter 18 16 (89) NA NA AFs ND ND VICAM AflaTest Filbert & Brown,
immunoaffinity 2012
fluorometric method
Abbreviations: NA, not applicable; ND, no data; LOD, limit of detection; LOQ, limit of quantification; AFB1 , aflatoxin B1 ; AFB2 , aflatoxin B2 ; AFG1 , aflatoxin G1 ; AFG2 , aflatoxin G2 , AF, aflatoxins; tAF, total aflatoxin,
AFM1 , aflatoxin M1 , OTA, ochratoxin; FUM, fumonisin; DON, deoxynivalenol; PAT, patulin; ZEN, zearalenone; TLC, thin layer chromatography; LC–MS/MS, liquid chromatography–tandem mass spectrometry; HPLC, high-
performance liquid chromatography, ELISA, enzyme linked immunosorbent assay; LC/ESI–MS/MS, liquid chromatography/electrospray ionization–tandem mass spectrometric; RP-HPLC, reverse-phase high-performance liquid
chromatography.
a Number of samples
b Number of positive samples
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW … 19

TABLE 4 Parasites reported in ready-to-eat (RTE) foods in low- and middle-income countries (2009 to 2018)
Potential source of
Region Country RTE food contamination Parasite Analytical method References
Africa Egypt Barbeque chicken Insufficient cooking Toxoplasma gondii PCR Abd El-Razik et al., 2014
Mutton kebab Insufficient cooking T. gondii PCR Abd El-Razik et al., 2014
Sausage Insufficient cooking T. gondii PCR Abd El-Razik et al., 2014
Nigeria Suya Lack of potable water Ascaris lumbricoides, Microscopy Manyi et al., 2014
for processing Entamoeba histolytica,
Taenia sp., and Giardia
lamblia

nutrients for child growth, and gastroenteropathy from severe tion very difficult, and variability of methods applied for dif-
foodborne bacterial infections in the gut; this postulation ferent food matrices (Koopmans, & Duizer, 2004; Maunula,
needs verification. Furthermore, it is pertinent to mention & von Bonsdorff, 2016). Nevertheless, several reports on
that compared to bacterial and fungal identification, parasites human exposure to foodborne viruses in some LMICs via
can be characterized with less sophisticated techniques (such detection of these viruses in biological samples, for example,
as light microscopy; Cheesbrough, 1998). Thus, more reports stool (Ayukekbong et al., 2011; Kumar, Basu, Vashishtha, &
on this foodborne hazard are expected in the future from Choudhury, 2016; Mans, 2019; Mattison, Sebunya, Shukla,
LMICs where access to high-end molecular equipment (such Noliwe, & Bidawid, 2010; Mukherjee et al., 2010; Omore
as polymerase chain reaction and sequencers) may not be et al., 2019) and blood (Chadha, Lole, Bora, & Arankalle,
fully available. 2009; Teshale et al., 2010), suggest that humans are frequently
exposed to foodborne viruses in LMICs.
Currently, norovirus and rotavirus rank among the leading
9 VIRU S ES I N RT E s F RO M L MICs cause of diarrheal-related deaths in humans particularly chil-
dren in LMICs (Kirk et al., 2015a, 2015b; Lopman, Steele,
Notable foodborne viruses include hepatitis A and E, Kirkwood, & Parashar, 2016; Mans, 2019; Parashar et al.,
norovirus, and rotavirus (FAO/WHO, 2008; Maunula, & von 2009; Taneja & Malik, 2012). It is important to mention that
Bonsdorff, 2016; Stals, Baert, Van Coillie, & Uyttendaele, rotavirus vaccines are now available and have been included
2012). These viruses are well equipped with machineries to in the national immunization programs in some LMICs (Patel,
withstand environmental stressors in food matrices. These Glass, Desai, Tate, & Parashar, 2012; Shah, Tate, Mwenda,
stressors include extreme pH, harsh food processing and stor- Steele, & Parashar, 2017). Furthermore, administration of
age conditions (such as heat, freezing, and exposure to organic these vaccines in humans has yielded some positive results
acids), and persistence in food contact surfaces (for exam- as revealed in a few studies that reported reduction in human
ple, stainless steel) (Hewitt & Greening, 2004; Koopmans, exposure to rotavirus in some LMICs (Armah et al., 2016;
& Duizer, 2004; Lamhoujeb, Fliss, Ngazoa, & Jean, 2009). Bar-Zeev et al., 2015; Schwartz et al., 2019). Notwithstand-
Unlike pathogenic bacteria, fungi, and parasites, foodborne ing, rotavirus vaccines are not yet widely available in some
viruses are obligate intracellular parasites, thus are incapable LMICs (Motayo, Faneye, & Adeniji, 2018; Sindhu, Babji,
of replicating in an inert environment like food matrices & Ganesan, 2017). Contrary to the case of rotavirus, devel-
(Koopmans, & Duizer, 2004). Thus, the viral load at the opment of norovirus vaccines is still ongoing (Hallowell,
point of contamination is unlikely to increase (Koopmans, Parashar, & Hall, 2018; Riddle, Chen, Kirkwood, & MacLen-
& Duizer, 2004; Newell et al., 2010). Nonetheless, low viral nan, 2018), and thus a licensed norovirus vaccine is currently
doses are required to cause an infection (Maunula, & von unavailable (Huys, Grau, & Karst, 2020). Taken together,
Bonsdorff, 2016), as such, viruses are a major concern to food indications are that these two viruses and other foodborne
safety. viruses could continually pose a threat to RTE consumers in
Regarding the occurrence of viruses in RTEs from LMICs LMICs. Consequently, in the interim, it is pertinent that in
in the decade under review, we found only one report on the addition to screening for the presence of bacteria, fungi, and
presence of hepatitis A virus in flour- and/or meat-based meal parasites in RTEs, food surveillance studies in LMICs should
from Cameroon (Table 5; Yongsi, 2018). Obvious reasons include the detection of viruses. This will provide data for rel-
for this paucity of data could be the lack of skilled exper- evant government agencies and policy makers to enact poli-
tise required for the detection of viruses in RTEs in LMICs, cies and drive regulations concerning foodborne viruses in
low amount of viruses present in foods, which makes detec- RTEs.
20 M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

TABLE 5 Virus reported in ready-to-eat (RTE) foods in low- and middle-income countries (2009 to 2018)
Potential source
Region Country RTE food of contamination Virus Analytical method References
Africa Cameroon Flour and meat based Poor hygiene Hepatitis A virus Direct flocculation Yongsi, 2018
practices and NASBA
NASBA, nucleic acid sequence-based amplification

10 FOOD SA FET Y SOLUTIONS 2013). Furthermore, there should be increased awareness on

AND FUTURE P E RSP E CT IV ES public health issues surrounding contaminated foods by edu-
cating food processors, vendors, and consumers on effec-
The search for interventions geared toward ensuring the safety tive food handling, good personal hygiene, good handling,
of foods, RTEs inclusive, globally has been marked with suc- and processing practices. The advocacy and awareness efforts
cesses as well as challenging efforts (FAO/WHO, 2018). Nev- should also target policy makers and high-level government
ertheless, to make RTEs safe for consumers in LMICs, there is officials and should focus on their commitments and roles to
a need to adopt a holistic approach, which involves interven- providing those they govern and protect with basic amenities
ing in the areas highlighted below. Major factors to consider to enhance food safety and protect consumer health.
in proposing interventions for mitigating foodborne hazards
in LMICs include the feasibility of the interventions consid-
10.2 Effective surveillance and monitoring of
ering the low-income status of greater population in the coun-
foodborne pathogens in RTEs
tries, sanitation and environmental conditions in the countries,
and low awareness of the food safety issue as it affects human Surveillance and monitoring exercises aimed at identifying
health among processors, vendors, and consumers of RTEs. foodborne hazards are major steps toward the prevention and
control FBD. Such program, if effectively executed, could
bridge some enlightenment gaps among food vendors and pro-
10.1 Integration of control approaches cessors depending on the food sampling points. Thus, it is
There is a need to focus interventions at the entire value chain, imperative that regulatory officials effectively monitor RTEs
beginning from farm to fork. For example, a set of good pre- for the presence of pathogenic microorganisms and their tox-
and postharvest practices has been suggested to reduce myco- ins before they are allowed in the market. However, monitor-
toxin contamination of cereals and nuts that serve as RTE ing at the local market in remote area may be a heinous task.
ingredients (Bandyopadhyay et al., 2016; Ezekiel et al., 2018). One approach to tackle this problem is to increase food safety
These practices include crop rotation, irrigation in areas of awareness and education; that is, mainstream food safety
drought, timely harvesting, proper drying to safe moisture courses into the educational curriculum at the basic (primary)
levels, sorting out the visibly discolored, infected and dam- and high school (secondary) levels.
aged grains, and storage in appropriate conditions to avoid The quality of techniques applied during the surveillance
moisture rise and insect infestation. In addition, good trans- studies is also crucial for proper risk assessment. Investments
port systems are essential to ensure the safety of grains moved focused on building cutting-edge infrastructures in LMICs
within the different parts of the LMICs (Grace, 2015). To for proper monitoring of RTEs should be prioritized. Such
be specific, in many LMICs there are lack of good road net- advanced infrastructures will gradually erode the application
works connecting grain producing communities to municipal of conventional techniques (such as, culture-based microbial
cities. The vehicles utilized for transport of the grains are also isolations and thin-layer chromatography for toxin detection).
of low quality (often uncleaned). These factors need atten- Rapid techniques involving immunoassays and nucleic acid-
tion in order to reduce RTE contamination. In addition, it has based methods for foodborne pathogen detection (Lee et al.,
been suggested that oxygenated tanks may be used to trans- 2015) and liquid chromatography–mass spectrometric meth-
port fresh fish alive to the point of sale (Grace, 2017). Access ods for microbial toxin analysis (Berthiller et al., 2017) should
to portable water sources is also crucial to ensuring food be adopted to enable accurate and high-throughput analysis.
safety especially in rural communities where the low-income
households and food processors reside. Proper RTE storage
10.3 Building food safety expertise for
facilities (for example, cold temperature) could also be use-
monitoring and control of food contaminants in
ful to keep pathogenic microorganisms away (Kunadu, Ofosu,
LMICs
Aboagye, & Tano-Debrah, 2016). In addition, bacteriophages
could be used as biocontrol agents against notorious psy- It is crucial to invest in training researchers and food reg-
chrophilic foodborne pathogens such as Listeria spp. (Chibeu, ulatory officers on modern technologies to detect microbial
M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW … 21

contaminants in RTEs in order to ensure proper surveillance RTE retail points, and definition of acceptable standards for
and source tracking. This can be achieved through collabo- RTEs (for example, water quality standards, standard packag-
rations between relevant government agencies and research ing materials, and vending sites/locations).
institutions in LMICs, as well as between food safety experts
in LMICs and those in the economically developed world 10.5 Protection of consumer rights
(Europe and North America). Forms of collaborations may
include staff and student exchange for technology trans- Consumer demand for RTEs is high in LMICs; hence, con-
fer, short training programs/fellowships, collaborative fund- sumers should be made aware of what to look out for in
ing/grant acquisition for establishment of functional food these foods and insist on details of processed RTEs to be pro-
safety centers equipped with state-of-the-art equipment in vided. These will afford consumers the opportunity to make
LMICs, as well as donation of equipment to LMICs. Coun- informed decisions on their choices of RTEs, thereby tak-
try governments are also urged to prioritize food safety and ing the first steps toward safeguarding their health. Consumer
thus invest in cutting-edge infrastructure and human capacity enlightenment can be achieved through various means such
building for effective prevention and control of FBD as well as soapboxes, the media, internet platforms (where available),
as consumer protection. and workshops. Education via the media and internet plat-
Building expertise for food safety should also be viewed forms could be useful tools for consumers in the urban and
on the scope of the value chain. Consequently, farmers, suburban areas owing to wider coverage and ability to trans-
food handlers, processors, and vendors should be educated mit information to several people in a relatively short period
on food safety regulations and standards. For example, they (Jabbar, Baker, & Fadiga, 2010). However, in rural commu-
could be encouraged to form cooperative and industrial soci- nities where media and internet facilities maybe unavailable,
eties geared toward acquiring relevant skills and training to trainings involving major community stakeholders, for exam-
ensure good agricultural and processing practices, which may ple, community heads and chiefs and local households, could
positively influence food safety (Kumar, Parappurathu, & be organized to disseminate such crucial information. Beyond
Jee, 2013). In addition, there should be requisite infrastruc- being aware about the safety of RTEs, the government via
tures and good welfare packages to enable all relevant stake- relevant agencies in LMICs should enact and sustain poli-
holders carry out effective monitoring and control of food cies to protect consumer rights. In addition, in cases of food
contaminants. fraud, consumers should be properly compensated, and strict
penalties should be meted out to the defaulting food processor
and/or vendor.
10.4 Regulations: Setting and enforcement
Any need for regulations regarding RTEs (on-shelf and off- 11 CONC LU SI ON
shelf) in LMICs? Would this impact negatively on food secu-
rity? If it would, do we then prioritize food safety over food This comprehensive review paper has presented robust data
availability? The obvious answer should be YES! These are on the spectra of RTEs in LMICs, sources of microbial con-
the obvious set of questions bugging the minds of food safety tamination of RTEs in the regions, techniques for detecting
regulators in LMICs and militating against the establishment the microbial contaminants as well as the occurrences of var-
of regulations targeting RTEs, especially the locally produced ious RTE contaminants of microbial origin. The paper has
ones. Taking a look at food production in some LMICs, it is shown that RTEs are important food sources for a large set
observable that most LMICs conveniently produce in large of the populations in LMICs due to the food diversity and
quantities the raw ingredients (for example, cereals, nuts, and ease of acquisition. However, these foods constitute a high-
tubers) for RTEs. Obviously, the major problem with estab- risk set of foods due to poor personal hygiene of proces-
lishing regulations is not the availability of these foods, but sors, poverty, lack of insights and knowledge into the adverse
how to ensure their safety. Thus, it is crucial to ensure the health effects that could arise from consumption of contami-
microbiological safety of these foods, which will help sustain nated foods, and nonexistent or inadequately enforced regula-
food security. Consequently, there should be strict regulations tions. To tackle the challenge, we proposed a set of integrated
guiding the production and sale of RTE ingredients and their and feasible food safety solutions and future perspectives tai-
finished products in countries where regulations are nonexis- lored for LMICs in order to ensure safety of RTEs and protec-
tent. Where food regulations do exist, appropriate measures tion of public health. These include, but not limited to, adop-
must be in place to enforce them. The regulations should tion of good agricultural, good processing and handling prac-
cover all aspects of food safety and include the quality of tices, effective surveillance and monitoring along the RTE
ingredients, strict personal hygiene standards for RTE vendors chain, establishment and enforcement of regulations, capac-
(including routine health checks and certification from recom- ity building of food safety experts, and enlightenment of the
mended health facilities), periodic inspection standards for all public (RTE processors, vendors, consumers, and government
22 M ICROBIOLOGICAL SAFETY OF READY-TO-EAT FOODS IN LOW …

officials) on the following: dangers of consuming contam- culture-dependent molecular methods for the determination of bacte-
inated foods, strategies to avoid food contamination and rial community of iru, a fermented Parkia biglobosa seeds. Frontiers
enhance food safety, and their obligations to ensure the foods in Microbiology, 3, 1–9
Adeyeye, S. A. O. (2017). “A preliminary study on the quality and
they consume are safe.
safety of street vended warankasi (a Nigerian soft white cheese) from
Ibadan, Oyo state, Nigeria”. British Food Journal, 119(2), 322–330.
AU THOR CONT RI B UT I O NS Adio, H. I., Ovuoraini, E. H., & Olubunmi, A. E. (2014). Microbial qual-
ity of ready to eat barbecue meat (suya) sold on the streets of Lagos
Conception of idea: C.N.E. Design of review outline: O.M.M. State. International Journal of Advances in Pharmacy, Biology and
and C.N.E. Drafting and reviewing of study outline: O.M.M., Chemistry, 3(4), 973–982.
K.I.A., R.A.A., and C.N.E. Sourcing literature: O.M.M. and Adjou, E. S., Yehouenou, B., Sossou, C. M., Soumanou, M. M., &
K.I.A. Data compilation and preparation of tables: O.M.M., De Souza, C. A. (2012). Occurrence of mycotoxins and associ-
K.I.A., and C.N.E. Interpretation of data, preparation, and ated mycoflora in peanut cake product (kulikuli) marketed in Benin.
fine-tuning of draft manuscript: O.M.M., K.I.A., M.S., R.K., African Journal of Biotechnology, 11(78), 14354–14360.
Adjrah, Y., Soncy, K., Anani, K., Blewussi, K., Karou, D. S., Ameyapoh,
R.A.A., and C.N.E.
Y., … Gbeassor, M. (2013). Socio-economic profile of street food
vendors and microbiological quality of ready-to-eat salads in Lomé.
CONFLICT OF IN T E RE ST International Food Research Journal, 20(1), 65–70.
Adolf, J. N. P., & Azis, B. S. (2012). Microbiological status of vari-
The authors declare no conflict of interest. ous foods served in elementary school based on social economic sta-
tus differences in Karawaci Region, Tangerang District – Indonesia.
ORC ID International Food Research Journal, 19(1), 65–70.
Afolabi, C. G., Ezekiel, C. N., Kehinde, I. A., Olaolu, A. W., & Ogun-
Michael Sulyok https://orcid.org/0000-0002-3302-0732 sanya, O. M. (2015). Contamination of groundnut in South-western
Chibundu N. Ezekiel Nigeria by aflatoxigenic fungi and aflatoxins in relation to process-
https://orcid.org/0000-0002-2113-2948 ing. Journal of Phytopathology, 163, 279–286.
Agrawal, A., Gupta, R., & Varma, K. (2008). High trans fatty acid content
in common Indian fast foods. Nutrition & Food Science, 38(6), 564–
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