International Journal of Food Science and Technology 2023 1 Review Listeria monocytogenes at the food–human interface: A review of risk factors influencing transmission and consumer exposure in Africa Thulani Sibanda,1,2 Victor Ntuli,3 Swaleha Hudaa Neetoo,4 Ihab Habib,5,6 Patrick Murigu Kamau Njage,7 Angela Parry-Hanson Kunadu,8 Anthonia Helga Andoh,8 Ranil Coorey9 & Elna M. Buys1* 1 Department of Consumer and Food Sciences, University of Pretoria, Private Bag X20, Hatfield 0028, South Africa 2 Department of Applied Biology and Biochemistry, National University of Science and Technology, P. O. Box AC939, Bulawayo, Zimbabwe 3 Department of Food Science and Technology, School of Agriculture, University of Venda, P. Bag X5050, Thohoyandou 0950, Limpopo, South Africa 4 Department of Agriculture and Food Science, Faculty of Agriculture, University of Mauritius, Reduit 80837, Moka, Mauritius 5 Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine, United Arab Emirates University (UAEU), Al Ain P.O. Box 1555, United Arab Emirates 6 Department of Environmental Health, Food Hygiene and Control Discipline, High Institute of Public Health, Alexandria University, Alexandria 21526, Egypt 7 Research Group for Genomic Epidemiology, National Food Institute, Technical University of Denmark, Kemitorvet, Building 204, Kgs. Lyngby 2800, Denmark 8 Department of Nutrition and Food Science, University of Ghana, Legon P.O. Box LG134, Ghana 9 School of Molecular and Life Sciences, Curtin University, Bentley, Perth, Western Australia, Australia (Received 1 March 2023; Accepted in revised form 6 June 2023) Summary In African public health systems, Listeria monocytogenes is a pathogen of relatively low priority. Yet, the biggest listeriosis outbreak recorded to date occurred in Africa in 2018. This review highlights the factors that potentially impact L. monocytogenes transmission risks through African food value chains (FVCs). With the high rate of urbanisation, African FVCs have become spatially longer yet still informal. At the same time, dietary diversifications have resulted in increased consumption of processed ready-to-eat (RTE) meat, poultry, fishery and dairy products typically associated with a higher risk of L. monocytogenes con- sumer exposure. With frequent cold chain challenges, the potential of L. monocytogenes growth in contami- nated RTE foods can further amplify consumer exposure risks. Moreover, the high prevalence of untreated HIV infections, endemic anaemia, high fertility rate and a gradually increasing proportion of elderly per- sons expands the fraction of listeriosis-susceptible groups among African populations. With already warmer tropical conditions, the projected climate change-induced increases in ambient temperatures are likely to exacerbate listeriosis risks in Africa. As precautionary approaches, African countries should implement sys- tems for the detection and reporting of listeriosis cases and food safety regulations that provide L. monocytogenes standards and limits in high-risk RTE foods. Keywords Food safety, food value chains (FVCs), Listeria monocytogenes, ready-to-eat (RTE) foods, risk factors. middle-income countries (LMICs) contribute a sub- Introduction stantial share, accounting for 72% of global DALYs According to estimates of the World Health (Havelaar et al., 2015; Unnevehr, 2022). The African Organization (WHO) Foodborne Disease Burden continent contributes 43% of the global DALYs, Epidemiology Reference Group (FERG), foodborne making it the biggest contribution by a single region diseases are responsible for 600 million illnesses and of the WHO (Havelaar et al., 2015). Among bacte- 420 000 deaths per year resulting in 33 million rial foodborne diseases, listeriosis has a compara- Disability Adjusted Life Years (DALYs) (Havelaar tively lower incidence, varying from 0.1 to 1.3 cases et al., 2015). Of this global burden, low- and per 100 000 population per year around the world (de Noordhout et al., 2014). However, despite its *Correspondent: E-mail: elna.buys@up.ac.za low incidence, invasive listeriosis has a high fatality doi:10.1111/ijfs.16540  2023 The Authors. International Journal of Food Science & Technology published by John Wiley & Sons Ltd on behalf of Institute of Food, Science and Technology (IFSTTF). This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. 2 Listeria monocytogenes in Africa T. Sibanda et al. rate (Desai et al., 2019). It results in approximately Listeriosis incidence in Africa 10 DALYs per 100 000 population, making it the deadliest of all bacterial foodborne infections (Have- With much of the policy attention of African countries laar et al., 2015). focused on food security (availability and affordability) Notwithstanding the general trend of a higher bur- and the major public health challenges like malaria, den of foodborne diseases in Africa, the incidence of HIV/AIDS and tuberculosis, food safety-related chal- invasive listeriosis is contrastingly lower in Africa lenges tend to get less attention (Jaffee et al., 2020). compared to high-income regions of the world (de Compared to other foodborne illnesses like salmonel- Noordhout et al., 2014). From a total of 23 150 ill- losis, campylobacteriosis and E. coli gastroenteritis, lis- nesses and 5463 deaths globally attributed to invasive teriosis is generally an infrequent disease. Hence, it is listeriosis in 2010, the contribution of the African con- not a priority disease in African public health systems tinent was only 16% (de Noordhout et al., 2014). The and its incidence in Africa is not fully understood. In reasons for the disparity in the incidence of listeriosis general, unless a foodborne disease causes a major in contrast to other bacterial foodborne diseases on public health or economic impact, many small out- the continent have not been fully explored. Against a breaks and sporadic cases often go unreported and background of a historically ‘low’ incidence of the dis- unnoticed (Havelaar et al., 2015). Like many other ease, the biggest outbreak so far in the world was foodborne illnesses, there is no mandatory reporting of recorded in South Africa in 2017–2018, where a total listeriosis in African countries (Grace, 2015). So far, of 1060 laboratory-confirmed cases, and 216 deaths only South Africa has classified listeriosis as a notifi- were reported (Thomas et al., 2020). The mismatch able condition, a consequence of the outbreak in 2018 between the historically low incidence and the occur- (Schutte et al., 2019). Moreover, the main clinical fea- rence of an outbreak of such magnitude in Africa is tures of invasive listeriosis, such as meningitis and likely a reflection of deficiencies in food safety systems meningoencephalitis that result from the invasion of and knowledge of risk factors influencing L. monocyto- the central nervous system, are also common features genes transmission dynamics in African food value chains of other bacterial pathogens such as Haemophilus influ- (FVCs). As countries undergo economic evolution and enzae, Streptococcus pneumoniae and Neisseria menin- move from low- to higher-income states, their food gitidis (Peltola et al., 2021). Since L. monocytogenes is safety systems also undergo a concomitant transforma- a less frequent cause, it is often excluded in the routine tion accompanied by diversification in diets and con- laboratory testing of cerebrospinal fluid (CSF) samples sumer food choices (Jaffee et al., 2020; de Bruin et al., when bacterial meningitis is suspected. In an extensive 2021). This food safety system transformation was review of the burden of meningitis in Africa, Pel- referred to by Jaffee et al. (2020) as a food safety life tola (2001) observed that about 10% of the aetiologies cycle in which nations move from the ‘traditional’ to the of bacterial meningitis were unconfirmed. Similarly, in ‘transitional’, ‘modernising’ and the ‘post-modern’ stages a recent study on childhood bacterial meningitis in as they transition from the low-income to middle- and Angola, only 64% of the bacterial causes were con- high-income stages of economic development respectively. firmed (Peltola et al., 2021). From these studies, it can In low-income countries, the spatially shorter value be surmised that the unconfirmed causes could poten- chains, and the predominantly traditional means of food tially be a result of the less commonly implicated path- production such as cooking close to the point of con- ogens like L. monocytogenes. sumption can understandably reduce L. monocytogenes So far, South Africa is the only country that has ran- transmission risks (Barrett et al., 2020). On the other domly reported cases of listeriosis over the years. hand, rising urbanisation in middle-income countries Through its National Institute for Communicable Dis- results in spatially elongated value chains and dietary eases (NICD) and National Health Laboratory Services diversifications towards the consumption of animal- (NHLS), it is probably the only country with laboratory source foods as well as processed ready-to-eat (RTE) diagnostic and surveillance capacity for the disease. foods (Barrett et al., 2020). Despite the nutritional bene- However, despite that, the country has not been able to fits of animal-source foods and the convenience of RTE provide any reliable listeriosis incidence data. In the foods, these dietary trends, unfortunately, result in a dis- absence of any reliable data, an inference of listeriosis proportionate amplification of L. monocytogenes con- incidence can only be made from the few studies so far sumer exposure risk (Jaffee et al., 2020; de Bruin reported in Africa. One retrospective review of neonatal et al., 2021). Thus, this review seeks to explore the dis- and central nervous system (CNS) infection records at tinctive characteristics of African FVCs and the poten- Tygerberg Hospital in Cape Town over the period tially attendant risks of L. monocytogenes transmission. 2006–2016, identified 51 sporadic cases with a preva- Furthermore, the review explores the possible risk factors lence of 0.04 cases per 1000 population (Oppel that can exacerbate listeriosis incidence in contemporary et al., 2018). In the 2017–2018 outbreak, the estimated African settings. prevalence was as high as 4–5 cases per 100 000 International Journal of Food Science and Technology 2023  2023 The Authors. International Journal of Food Science & Technology published by John Wiley & Sons Ltd on behalf of Institute of Food, Science and Technology (IFSTTF). Listeria monocytogenes in Africa T. Sibanda et al. 3 population in the most affected districts (Thomas Traditional FVCs are typically rural value chains of et al., 2020). In that outbreak, 50% of the cases were low-income countries. As foods are produced and con- pregnancy-associated, and the fatality rate was 27% sumed at home, these rural FVCs are spatially short (Thomas et al., 2020). Besides the data from South and the diversity in foods is limited, being dominated Africa, a meta-analysis of pregnancy-associated listerio- by staple grains and fewer processed animal products sis by Geteneh et al. (2022), identified a few studies from (Barrett et al., 2020). While poor hygiene and sanitary Nigeria, Senegal and Ethiopia. The pooled prevalence conditions and close interaction with farm animals in from these studies was 5.17% (Geteneh et al., 2022). these rural agri-food systems could increase the risk of L. monocytogenes contamination of foods and lead to a potential direct human exposure (Rodriguez et al., African FVCs and L. monocytogenes food safety 2021), the homecooking of food and absence of risks extended refrigerated storage of food, attenuates the L. monocytogenes risk by preventing undue multiplica- Overview of L. monocytogenes transmission pathway tion of the psychrotolerant organism to unsafe levels. The main source of L. monocytogenes contamination of In middle-income countries facing rapid urbanisa- foods is the farm environment. Its chronic colonisation tion, FVCs are in the transitional stage (Barrett of the gastrointestinal tracts of livestock species creates et al., 2019). These are spatially long value chains link- a reservoir for the spread of the organism into soil, ing the urban population to the rural agricultural pro- vegetation and surfaces and materials within the farm duction areas (Barrett et al., 2020). These FVCs are environment (Rodriguez et al., 2021). Thus, raw foods dominated by informal wet markets, street vendors such as milk and meat can directly be contaminated and small-medium processors midstream between pro- with the pathogen at the farm and during slaughter ducers and consumers. Midstream processing increases (Rodriguez et al., 2021). Moreover, the use of animal the diversity of foods to include perishable fresh manure and contaminated irrigation water is an addi- animal-derived (poultry, beef, fish and dairy) and hor- tional route of pre-harvest contamination of field crops ticultural commodities requiring preservation and such as fruits and vegetables (Biswas et al., 2018; Gho- refrigeration (Reardon, 2015). The concentrated pur- lipour et al., 2020). Notwithstanding the possibility of chasing power of the urban population creates a contamination of raw foods, many human outbreaks demand for high-value processed, ready-to-cook and of listeriosis result from contaminated processed RTE RTE foods that save consumers food preparation time foods (Fagerlund et al., 2021). From its primary natu- (Barrett et al., 2019). Despite the benefits associated ral source on the farm, the pathogen is disseminated with diversified diets that bring about improved nutri- into food-processing environments through contami- tion, these transitional FVCs are unfortunately associ- nated raw foods. Subsequently, its ability to colonise ated with huge food safety challenges in African and persist in processing facilities often becomes a sec- middle-income countries (Waage et al., 2022). ondary source of post-process contamination of pro- Street-vended RTE foods are a common feature of cessed foods (Castro et al., 2018; Sun et al., 2021). the informal food market in African cities (Abrahale et al., 2019). In South Africa, about 30% of the urban population depends on street foods for their daily die- Characteristics of African FVCs and potential influence tary needs (Steyn et al., 2011). Typically, street foods on L. monocytogenes transmission and consumer exposure are prepared and sold by vendors on the street sides for immediate consumption. Their safety is compromised As African countries develop economically, their FVCs by inadvertent cross-contamination through poor han- also undergo transformations that have an impact on food dling practices and the unavailability of running water, safety (Waage et al., 2022). Propelled by rapid urbanisa- washing and disinfection facilities (Kok & Balkaran, tion and growing incomes, the value chains have changed 2014). Moreover, the extended storage of foods post- from traditional through transitional to modernising as preparation, the elevated ambient conditions of the African countries move from low-income to middle- and African tropical climate, and inadequate or lack of upper middle-income levels (Barrett et al., 2019). This evo- refrigeration are all factors that collectively increase the lution in food safety systems was referred to by Jaffee risk of bacterial growth once the food is contaminated et al. (2020) as a food safety life cycle. Given that most (Nkosi & Tabit, 2021; Oladipo-Adekeye & Tabit, 2021). African countries are in the LMIC (low- and middle- As economic development improves into upper income) bracket, their FVCs are predominantly in the tra- middle-income levels, FVCs become more modernised ditional and transitional stages. The characteristics of with formal agri-businesses and food-processing enter- these value chains and the possible attendant risks of L. prises and a dominant formal food retail sector (Jaffee monocytogenes transmission and consumer exposure et al., 2020). The implementation of good hygiene and (summarised in Table 1) are discussed in this section. food safety management systems in modernised systems  2023 The Authors. International Journal of Food Science & Technology published by John Wiley & Sons Ltd International Journal of Food Science and Technology 2023 on behalf of Institute of Food, Science and Technology (IFSTTF). 4 Listeria monocytogenes in Africa T. Sibanda et al. Table 1 Food value chain transformation stages in Africa and their potential influence on Listeria monocytogenes transmission and consumer exposure risk Food value Economic Potential L. monocytogenes transmission and chain stage development stage Characteristic consumer exposure risks Traditional Low-income • Spatially short rural agri-food systems • Low risk due to homecooking countries (46% of • Foods are prepared and consumed at home • Risk of direct human exposure through proximity African countries) • No processed or value-added foods to farm animals Transitional Lower middle- • Spatially longer urban value chains domi- • High transmission risk in informal wet markets, income countries nated by informal wet markets, street ven- street foods and artisanal processors (42% of African dors and artisanal processors serving • High risk of exposure through the consumption of countries) growing urban population animal-derived RTE foods. • Processed and value-added foods (including • High risk of exposure due to pathogen growth in RTE foods) contaminated RTE foods and inadequate cold • Diversity in foods includes animal and per- chains ishable foods requiring preservation and refrigeration) Modernising Upper middle- • Spatially long urban value chains domi- • Reduced risk due to implementation of GAP, income countries nated by large formal food producers, pro- GHP and HACCP in formal value chains. How- (12% of African cessors and retailers ever, the risk remains in informal markets and countries) • Investment in cold chains street foods • Informal food markets and street foods are still a significant part of the value chains GAP, good agricultural practices; GHP, good hygiene practices; HACCP, hazard analysis critical control point. Food value chain stages and character- istics compilation was based on the review of literature (Reardon, 2015; Barrett et al., 2020; Jaffee et al., 2020). significantly reduces food safety hazards (Jaffee et al., urban consumers has been increasing, while the share 2020). However, even with dominant modernised sys- of staple grains has been declining (Reardon, 2015). tems in upper middle-income countries, small shops and Processed foods include low-value foods that are informal markets continue to be major suppliers of food ready-to-cook and high-value foods that are ready to for a significant portion of low-income consumers (Hoff- eat (Snyder et al., 2015; de Brauw & Herskowitz, 2021). mann et al., 2019). Thus, both formal and informal FVCs Along with an increase in the consumption of pro- co-exist and intersect as the formal retail food sector is cessed foods, is also an increase in the consumption of frequently a major supply source for the informal sector animal-derived foods, such as meat, fish and dairy (Gbadegesin et al., 2020). For instance, in South Africa products among the growing urban population (Rear- and several other southern African countries, processed don, 2015). While the consumption of animal-derived deli-meat products sourced from formal retailers are foods may be considered beneficial for human nutri- ingredients for preparing street-vended RTE foods tion, such foods are incidentally the most frequently (Ryan, 2019). Furthermore, the enforcement of quality implicated in foodborne disease outbreaks (EFSA & and safety standards in formal retailers often results in ECDC, 2017; Ricci et al., 2018). In addition to dietary rejected foods finding their way into the informal mar- changes, urbanisation and income growth are also kets where they are sold at discounted prices to poorer accompanied by an increased tendency of consuming urban households (Hoffmann et al., 2019). In such situa- foods away from home. As has been observed by stud- tions, the public health risks of L. monocytogenes trans- ies in South Africa and Nigeria, a great share of the mission can be aggravated by potential cross- food service providers in the rapidly growing African contamination and improper storage conditions that cities are formal restaurants, and informal street food encourage pathogen growth. vendors that serve RTE foods (Blick et al., 2018; Hoff- mann et al., 2019; de Brauw & Herskowitz, 2021). A wide variety of RTE foods of animal origin is found Risk factors exacerbating L. monocytogenes in different regions of the continent (Adeyeye, 2017; consumer exposure and infections in African Nemo et al., 2017; Matle et al., 2019; Gichure et al., settings 2020; Makinde et al., 2020; Adeyeye & Ashaolu, 2022). Owing to their high moisture content and neutral pH, Consumption of high-risk RTE foods meat, fish and dairy-based products are most at risk of As African countries urbanise and average incomes L. monocytogenes growth during storage (Gerard grow, the dietary share of processed foods among et al., 2018; Taylor et al., 2019). Indeed, previous risk International Journal of Food Science and Technology 2023  2023 The Authors. International Journal of Food Science & Technology published by John Wiley & Sons Ltd on behalf of Institute of Food, Science and Technology (IFSTTF). Listeria monocytogenes in Africa T. Sibanda et al. 5 profiling has identified meat-based products as the et al., 2008; Ndahi et al., 2014; Akanbi & Usoh, 2016; highest-risk category of RTE foods, followed by dairy, Usman et al., 2016). In South Africa, prevalence rates fish and fruits and vegetables (FDA & FSIS, 2003; of 4.3–14% were reported in RTE meat products, Batz et al., 2014; WHO & FAO, 2022). Many of these sandwiches and salads (Christison et al., 2008; Matle RTE meat products, such as nyirinyiri, suya, koche, et al., 2019). and smoked fish are traditional African products now produced for the urban informal food market by arti- Cold chain challenges and L. monocytogenes growth sanal and small-scale processors (Table 2). However, potential others such as vienna sausages and frankfurters are exotic cooked or smoked meat products that are pro- Inadequate cold chains are responsible for huge food duced by large formal processors and consumed widely losses in developing countries (IIR, 2020). Inadequate across the continent (Christison et al., 2008). refrigeration equipment and chronic electricity supply In the last few decades, the per capita consumption challenges can make the sustenance of cold chains dif- of such high-risk foods has dramatically increased in ficult in many African countries (IIR, 2020). Gener- Africa. A survey of food consumption changes in ally, the most common and easily discernible effect of South Africa between 1999 and 2012 showed that the an inadequate cold chain is the food quality deteriora- consumption of chilled ready meals and frozen pro- tion that results from the growth of spoilage organ- cessed foods increased by 50–100% (Ronquest-Ross isms. Normally, a high level of organisms in the range et al., 2015). In South Africa, most of the processed of 106–108 CFU g1 is required before sensory quality RTE meat products emanate from formal food pro- deterioration becomes evident (Poghossian duction systems as factory-packaged or retail-sliced et al., 2019). Yet, unlike the spoilage problem, the and re-packaged products (Matle et al., 2019). They food safety risks arising from cold chain failures may are also important ingredients in the preparation of not be easily detectable as the growth of pathogens street-vended foods. For example, polony, viennas and may not produce any discernible sensory effects. More- frankfurters are used in the production of kota, a over, foodborne infections frequently result from the street-vended sandwich that is widely consumed by consumption of relatively lower levels of microbes South African urban populations (Steyn et al., 2011). than are required for spoilage. In more than 90% of Although there are no systematic surveillance studies listeriosis cases, the identified RTE foods frequently on the occurrence and contamination levels of contain at least 2000 CFU g1 of the pathogen (Ricci L. monocytogenes among RTE foods sold in African et al., 2018). Worse still, the concept of food safety cities, a few random reports have been recorded. among African consumers is often misconstrued with Prevalence rates of 4% in processed meat products negative sensorial perceptions of foods such as smell. (suya, balangu, kilishi, dambun nama), 14% in Thus, temperature-abused leftover RTE foods can be street-vended soy wara (a soft cheese), and 25% in consumed if the sensorial properties are deemed smoked fish have been reported in Nigeria (Salihu acceptable (Odeyemi et al., 2019). Table 2 Ready-to-eat (RTE) meat, fish and dairy foods with potential for Listeria monocytogenes transmission risk as they are produced and sold in African urban areas RTE food category Product examples Product Description Country References Meat Nyirinyiri Deep-fried fresh meat Kenya Gichure et al. (2020) Koche Deep-fried beef or camel meat Kenya Werikhe et al. (2019) Mutura Blood sausage made from goat or cow-cleaned Kenya Karoki et al. (2018) intestines stuffed with cooked small pieces of meat and formed into long coils Suya Grilled meat West Africa Adeyeye & Ashaolu (2022) Kilishi Smoked spiced meat Nigeria Ndife et al. (2022) Polony Comminuted and cooked meat stuffed into large South Africa Cluff et al. (2017) tubular nylon casings Fish Smoked fish Hot smoked fish West and East Africa Adeyeye & Oyewole (2016) Dairy Omashikwa Buttermilk Namibia Bille et al. (2007) Wara and Soy wara Curdled cow and soy milk products Nigeria Akanbi & Usoh (2016) Warankasi Soft white cheese made from goat or cow milk Nigeria Adeyeye (2017) Amasi Fermented cow milk South Africa Maleke et al. (2021)  2023 The Authors. International Journal of Food Science & Technology published by John Wiley & Sons Ltd International Journal of Food Science and Technology 2023 on behalf of Institute of Food, Science and Technology (IFSTTF). 6 Listeria monocytogenes in Africa T. Sibanda et al. In RTE foods (whose physicochemical properties per- practices of informal food vendors (Letuka et al., mit growth), the cold growth ability of L. monocyto- 2021; Nkosi & Tabit, 2021; Azanaw et al., 2022). A genes is an important food safety and public health risk. survey of street food vendors in Johannesburg, South As a psychrotroph, L. monocytogenes is intrinsically Africa found that at least 60% of them did not know adapted to growth under low-temperature conditions the correct temperature for the hot and cold storage of (Saldivar et al., 2018). Besides the inherent growth abil- RTE foods (Oladipo-Adekeye & Tabit, 2021). In ity, any fluctuations in temperature brought about by Kenya, a similar survey found that foods requiring cold chain breaks can accelerate the multiplication in refrigeration are frequently kept at ambient tempera- contaminated foods. Thus, foods with initially low tures by almost 80% of street vendors (Mwove levels of the pathogen can exceed the safety threshold in et al., 2020). Moreover, many vendors keep leftover relatively short periods. Experimental models in RTE foods for sale on the following day, sometimes without food matrices have shown that the growth rate of the any form of preservation (Mwove et al., 2020). With organism doubles as temperature increases from 4°C to all these challenges, the possibility of L. monocytogenes 8°C and from 8°C to 12°C (Kataoka et al., 2017; Ziegler contamination and growth presents a palpable con- et al., 2019). As the manufacturing processes for most sumer exposure risk. RTE products involve some listericidal heating steps, In addition to the safety hazards emanating from L. monocytogenes contamination levels in the products informal food vendors, the consumer stage of the FVC at the point of release from the processor are usually presents additional challenges that could amplify low (frequently <10 CFU g1) (Angelidis & Koutsou- L. monocytogenes exposure risk. In Europe, quantita- manis, 2006). Dose–response models and epidemiologi- tive modelling has shown that one-third of listeriosis cal data have shown that such low cell numbers cases are due to pathogen growth in the consumer (including a single cell) if ingested in food, have a low phase of the value chain (Ricci et al., 2018). A survey probability of listeriosis (Pouillot et al., 2015; Ricci of microbial hazards awareness among consumers of et al., 2018; Sampedro et al., 2022). However, the street-vended RTE foods in Johannesburg, South growth ability of the pathogen in refrigerated RTE Africa showed that although the majority of con- foods amplifies the human exposure risk (Ricci sumers were aware of foodborne diseases and some et al., 2018). Using risk assessment models, the overall pathogens, over 70% of the consumers had never impact of in-food growth was estimated to contribute heard about L. monocytogenes (Asiegbu et al., 2016). up to 37% of the risk of human invasive listeriosis In addition, a survey on consumer food safety perspec- (Ricci et al., 2018). Moreover, the handling of RTE tives in Ghana, Guinea, Kenya, Tanzania, Nigeria and foods along the value chain (e.g. retail-level slicing and Cameroon found that 67% of the consumers rely re-packaging), further amplifies the consumer exposure mainly on sensory properties such as smell, taste and risk. Risk assessment models estimate that retail-level appearance as criteria for safe food consumption contamination causes a two- to four-fold risk amplifica- (Odeyemi et al., 2019; Isanovic et al., 2023). With the tion compared to factory-prepackaged products (Ricci habit of using sensory characteristics as indicators of et al., 2018). In many Southern African cities, RTE pro- food safety, African consumers could unwittingly be cessed meats and cheeses are a common part of the local exposed to an increased risk of L. monocytogenes street food culture, especially as ingredients for street- infections given the rampant practices of storing RTE prepared sandwiches (von Holy & Makhoane, 2006). foods under growth-permitting conditions for long Such high-risk RTE food products are often purchased periods. from formal retail chains each day and can be kept for long hours unrefrigerated as the food preparation goes Populations at risk on during the day (von Holy & Makhoane, 2006). The growth potential of the pathogen in such foods can Susceptibility to invasive listeriosis varies among undoubtedly be a major public health challenge. human populations. Many people are frequently exposed to L. monocytogenes through the ingestion of contaminated foods without showing any symptoms of Food safety knowledge and practices of informal vendors invasive disease (WHO & FAO, 2022). Variability in and consumers susceptibility is influenced by an individual’s CD4+ It is widely acknowledged that the food safety hazard T-cell-mediated immunity (WHO & FAO, 2022). Preg- awareness and handling practices among African nant women and their newborns (<28 days), elderly informal food vendors are poor (Mwove et al., 2020; persons, individuals with untreated HIV infections, Letuka et al., 2021; Oladipo-Adekeye & Tabit, 2021; cancer patients, organ transplant patients and immu- Azanaw et al., 2022). As was observed in Kenya, Ethi- nosuppressed patients are known to be among the sus- opia and South Africa, inadequate food safety knowl- ceptible subpopulations (WHO & FAO, 2022). Due to edge is a determining factor in the poor handling the decreased efficacy of cell-mediated immunity, HIV International Journal of Food Science and Technology 2023  2023 The Authors. International Journal of Food Science & Technology published by John Wiley & Sons Ltd on behalf of Institute of Food, Science and Technology (IFSTTF). Listeria monocytogenes in Africa T. Sibanda et al. 7 infection is an important risk factor for the incidence associated with a high risk of mortality in cases of and severity of invasive listeriosis (Thomas et al., invasive listeriosis (Scobie et al., 2019). 2020). With about 25.6 million people living with HIV, sub-Saharan Africa accounts for two-thirds of the Regional food trade and globalisation global burden of HIV/AIDS (UNAIDS, 2022). Although a significant portion of this HIV-infected Global and regional trade in raw and processed food population is on antiretroviral therapy, an estimated products is a significant part of African economies 22% are not on treatment (UNAIDS, 2022). More- (Zamani et al., 2021). Currently, most of the trade in over, about 8% of people on antiretroviral therapy do the typical vehicle foods for L. monocytogenes trans- not have successful viral suppression (UNAIDS, 2022). mission (meat, dairy and fishery) is in the form of With such a disproportionately high number of indi- imports into Africa, with limited intra-Africa trade viduals with untreated HIV infections, the risk of inva- (Zamani et al., 2021). For instance, in 2018, West Afri- sive L. monocytogenes infections is a major concern can countries imported about 484 million tonnes of for Africa. Using a dose–response model, Pouillot poultry meat and milk products from the EU and et al. (2015) estimated the probability of developing North America, while South Africa imported 30% of invasive listeriosis from ingesting a single cell of its chicken meat requirements, mostly from Brazil L. monocytogenes to be 100-fold higher for HIV- (Makgopa, 2020; Zamani et al., 2021). Although intra- infected individuals than the general non-susceptible Africa trade is not as prominent as food imports, the population. Epidemiological data from the 2017–2018 more industrialised countries like South Africa export South African listeriosis outbreak demonstrated the both raw and processed meat products to neighbour- impact of HIV infection as a risk factor in African set- ing countries within the Southern African Develop- tings, with a disproportionately higher number of cases ment Community (SADC) region (Makgopa, 2020). observed among HIV-infected persons (Thomas South African companies and retail chains supply the et al., 2020). Along with the high HIV infection rates, bulk of the processed food products sold in countries the fertility rate is likely to be another major risk fac- such as Botswana, Namibia, Zambia and Zimbabwe tor in pregnancy-associated listeriosis. The estimated (das Nair & Chisoro, 2016). The public health impacts probability of developing invasive listeriosis in preg- of the regional trade were directly evident at the height nancy is 1000-fold higher than the general non- of the listeriosis outbreak in 2018. Up to 15 countries susceptible population (Pouillot et al., 2015). Com- (Angola, Botswana, Democratic Republic of Congo, pared to other regions, sub-Saharan Africa has the Ghana, Lesotho, Madagascar, Malawi, Mauritius, highest female fertility rates in the world (Atake & Mozambique, Namibia, Nigeria, eSwatini, Uganda, Ali, 2019). In the 2017–2018 South African outbreak, Zambia and Zimbabwe) were affected by recalls of the 50% of the total cases were pregnancy-related, the contaminated polony (Olanya et al., 2019). With such majority (87%) of which occurred in neonates wide distribution networks of processed RTE foods, (Thomas et al., 2020). Moreover, a retrospective study the African urban food systems pose a potential risk of pregnancy-associated listeriosis cases in South to epidemic listeriosis outbreaks. Africa found that HIV seropositivity and anaemia were additional risk factors (Iiyambo et al., 2022). Iron Climate change effects deficiency anaemia is an endemic problem in sub- Saharan Africa with prevalence rates of up to 60% in At the current rate of global warming, annual average some worst affected countries (Kassebaum and GBD surface temperatures are predicted to increase by up to 2013 Anemia Collaborators, 2016). It is a known risk 5°C by the end of the century (IPCC, 2021). The envi- factor in human susceptibility to invasive bacterial ronmental effects of climate change have significant infections (Abuga et al., 2023). impacts on the epidemiology of foodborne diseases Another major listeriosis risk factor that is likely to (Anas et al., 2021). Several studies have provided evi- have a big influence on Africa is population ageing. In dence for a strong correlation between ambient tem- general, old age (>65 years) has been known to be perature conditions and the incidence of infection by associated with a high risk of mortality in cases of foodborne pathogens such as Salmonella, Vibrio cho- invasive listeriosis (Scobie et al., 2019). At the current lerae and Campylobacter (Reyburn et al., 2011; Jiang rate, the global proportion of older people is projected et al., 2015; Kuhn et al., 2020; Morgado et al., 2021). to increase (Rudnicka et al., 2020). With the rise in As for L. monocytogenes, evidence from the listeriosis ageing, a concomitant increase in the incidence of surveillance in the EU from 2008 to 2016 showed a multi-morbidities has also been observed (Chang seasonal pattern of cases with higher peaks during the et al., 2019). Many of these conditions such as cardio- warmer summer months (EFSA & ECDC, 2017). At vascular disease, liver disease and haematological the current rate, the African continent is predicted to malignancy have been known to be co-morbidities record average temperature increases of 3.5–5.6°C by  2023 The Authors. International Journal of Food Science & Technology published by John Wiley & Sons Ltd International Journal of Food Science and Technology 2023 on behalf of Institute of Food, Science and Technology (IFSTTF). 8 Listeria monocytogenes in Africa T. Sibanda et al. the end of the century (Almazroui et al., 2020). On the areas can lead to an increased risk of foodborne dis- other hand, precipitation predictions indicate spatial ease outbreaks. Burr et al. (1978) observed a strong variations across the continent where the Northern association between water restriction times and rates and Southern regions are projected to get drier while of childhood diarrhoea. Similarly, evidence from the Central, East and West African regions are pro- around Africa has shown that higher precipitation and jected to have an increasing precipitation trend flooding events are associated with a high risk of food- (Almazroui et al., 2020). borne diseases (Horn et al., 2018; Cisse, 2019). An increasing trend in ambient temperatures will likely put a strain on cooling systems that could cause Listeria monocytogenes food safety standards in temperature fluctuations and enhance L. monocyto- Africa genes multiplication risks in contaminated foods (Hell- berg & Chu, 2016). For instance, Christison et al. Microbiological safety standards can provide a regula- (2008) found that core temperatures of RTE foods in tory guide that assures consumer protection against retail delicatessens in South Africa were ranging from food safety hazards. A survey on microbiological stan- 10 to 16°C instead of the recommended range of 4– dards conducted as part of this review showed that 8°C due to warm ambient conditions. Additionally, only a few African countries have any form of stan- elevated ambient temperatures could affect the expres- dards on L. monocytogenes in their food safety legisla- sion of virulence genes in the pathogen within the tion (Table 3). Among these countries, the specified environment and the potential spread of hyper-virulent standards vary in terms of the allowable limits and the strains (Bruno Jr & Freitag, 2010; Levy et al., 2016). type of foods covered by the respective regulations As an environmental saprophyte, L. monocytogenes (Table 3). Whereas some countries have requirements normally exists in an avirulent state in which virulence for the absence of L. monocytogenes in one or five genes are repressed at temperatures of 30°C and below samples of 25 g of raw and RTE products, others have (Sibanda & Buys, 2022). Elevated temperatures at limits of 100–1000 CFU g1 (Table 3). Moreover, the 37°C serve as a stimulus for the activation of virulence food products listed in the respective regulations also gene expression (Sibanda & Buys, 2022). In the nor- vary with the focus seemingly on raw fishery, beef and mal infection cycle of L. monocytogenes, the activation poultry products. The focus on raw animal and fishery of virulence gene expression occurs inside the host as products is probably a reflection of efforts by African the organism switches from the avirulent to the viru- countries to meet the export safety requirements to lent state. Constitutive expression of virulence genes overseas markets (World Bank, 2022). Indeed, many within the environment observed in some mutants LMICs successfully export safe food but are unable to has been associated with hyper-virulence (Bruno Jr & implement sustainable food safety systems that work Freitag, 2010). for domestic settings dominated by informal markets Based on overall predictions of precipitation trends and food vendors (Waage et al., 2022). In view of the for the African continent, the frequency and intensity projected rise in the proportion of susceptible popula- of extreme weather (drought and floods) are likely to tion groups and consumption of high-risk RTE foods, worsen (Almazroui et al., 2020). Although there is cur- it will be prudent for African countries to develop rently limited data showing a correlation between domestic standards and regulations for the protection drought and foodborne diseases, several factors sug- of consumers. gest a possible increase in the risk of human exposure In countries with a higher level of formal food pro- to foodborne pathogens (Levy et al., 2016). These duction like South Africa, the implementation of regu- include the concentration of faecal contamination in lated standards would provide a significant level of water sources and greater dependence on non-potable consumer protection against potential outbreaks as the sources of water for cleaning food-processing equip- food business operator is an essential stage of ensuring ment and domestic use in times of drought (Levy the safety of RTE products before release to the mar- et al., 2016; Chersich et al., 2018). A study by Wang ket. Already, global guidelines for risk-based regula- et al. (2022) in African LMICs observed that mild and tions for L. monocytogenes in RTE foods are available severe drought was associated with a 5% increase in (CAC, 2009). However, data on the physicochemical the risk of diarrhoea. Likewise, Iwu et al. (2022) profiles of African RTE foods, the growth potential of observed high levels of L. monocytogenes contamina- the pathogen in the respective foods, the amount and tion in irrigation water from semi-arid regions of frequency of consumption of the foods, the virulence South Africa and an increased risk of human exposure potential of strains found in the African food environ- through unintentional and intentional ingestion of ment and susceptibility profiles of African populations such water. are necessary to understand the relative risks to Afri- In addition, drought-induced restrictions in potable can consumers. In the aftermath of the 2017–2018 out- water supplies, particularly in densely populated urban break, the subject of mandatory L. monocytogenes International Journal of Food Science and Technology 2023  2023 The Authors. International Journal of Food Science & Technology published by John Wiley & Sons Ltd on behalf of Institute of Food, Science and Technology (IFSTTF). Listeria monocytogenes in Africa T. Sibanda et al. 9 Table 3 Standards and limits for Listeria monocytogenes in foods as specified in the regulations of some African countries Countries with standards for L. monocytogenes Listed Foods Limits Regulation† Djibouti Meat and fishery products <100 CFU g1 Official Journal of the Republic of Djibouti (Arrête n°2000-0728/PR/ MAEM) Egypt Pasteurised cream, whipped cream, Absent in five samples of 1 g of Food and Agricultural Import fermented cream, butter, cheese, product Regulations and Standards of Egypt powdered milk, dietetic food intended for high-risk groups, frozen raw crustaceans and coleslaw Kenya Meat products Absent in a 25 g sample Kenya Standard (DKS 2830: 2018) Madagascar Seafood and aquaculture products Absent in five 25 g samples Ministry of Agriculture and Fisheries of <100 CFU g1 before the end of the Madagascar (ARRETE No 6235/2009) product shelf-life Mauritania RTE aquatic food products Absent in five 25 g samples Arrête conjoint no. 2905 <100 CFU g1 before the end of the product shelf-life Mauritius Infant formula, dairy products, cheese and Absent in 1 g samples of infant Mauritius Food Regulations (GN 173 of other RTE food products formula and dairy products 1999) Absent in 25 g samples of cheese <1000 CFU g1 in other RTE products Morocco Meat, poultry and fishery products Absent in five 25 g samples Microbiological Standards for Food of Animal Origin, Morocco (MO1814) Seychelles Fishery products Absent in five 25 g samples taken Export of Fishery Products (Sanitary) before the product left the Regulations (2010) of Seychelles establishment Saint Helena RTE fishery products Absent from five 25 g samples taken Fish and Fish Products Regulations before the product left the (2011) of St Helena establishment Tunisia RTE processed bovine, poultry and Absent in five 25 g samples before the Journal Officiel de la Republique lagomorph meat products products have left the establishment Tunisienne (2013) <100 CFU g1 in products before the end of shelf-life Uganda Fishery products <1000 CFU g1 The Uganda Gazette, The Fish (Quality Assurance) Rules, 2008 United Republic Raw or cooked red meat sausages Absent from 25 g samples of the Tanzania Bureau of Standards (AFDC of Tanzania product 22 (5279) P3) †Regulations are available from the FAOLEX database (http://www.fao.org/faolex/en/). standards for processed RTE meat products was diseases, yet it has the highest fatality rate. In Africa, debated among authorities and industry stakeholders. listeriosis is not given much attention in public health Based on submissions from representatives of food systems. In the absence of systems for identifying and manufacturers and the food retail sector, the adoption reporting cases, the incidence of the disease is hard to of the Codex 100 CFU g1 L. monocytogenes limit for establish. However, the occurrence of the greatest out- RTE meat products appeared to be a common agree- break in history in South Africa in 2018 is an indica- ment (CGCSA, 2018). Ultimately, the role of govern- tion of the potential public health dangers of ignoring ments and public health institutions in controlling and the disease in Africa. With the transformation of value regulating the informal food sector and effective con- chains and diet diversification brought about by the sumer risk education will be crucial in preventing big rapid urbanisation of many African countries, several outbreaks in future. risk factors create opportunities for L. monocytogenes transmission and consumer exposure. The increased consumption of high-risk RTE meat, fishery and dairy Conclusions and future directions foods, cold chain challenges that increase the potential On a global level, the incidence of invasive listeriosis is for pathogen multiplication, a high proportion of comparatively lower than other bacterial foodborne listeriosis-susceptible subpopulations, inadequate consumer  2023 The Authors. International Journal of Food Science & Technology published by John Wiley & Sons Ltd International Journal of Food Science and Technology 2023 on behalf of Institute of Food, Science and Technology (IFSTTF). 10 Listeria monocytogenes in Africa T. Sibanda et al. food safety knowledge and climate change effects are Ethical approval all risk factors that could potentially exacerbate con- sumer exposure and listeriosis outbreaks in African Ethics approval was not required for this research. settings. As a precautionary approach, it will be neces- sary for African countries to implement systems for the detection and reporting of listeriosis cases. This Peer review could be done systematically through the laboratory The peer review history for this article is available diagnosis of meningitis and maternal infections, espe- at https://www.webofscience.com/api/gateway/wos/peer- cially where the common bacterial causes are excluded. review/10.1111/ijfs.16540. Furthermore, such laboratory-based surveillance should be enhanced by genomic surveillance tech- niques like whole-genome sequencing that improve the Data availability statement efficiency of outbreak detection and epidemiological Data sharing not applicable - no new data generated identification of implicated RTE foods. In addition, food safety regulations that include L. monocytogenes standards and limits in high-risk RTE foods will be References necessary to provide a layer of consumer protection. Abrahale, K., Sousa, S., Albuquerque, G., Padra~o, P. & Lunet, N. In light of the wide diversity of potentially high-risk (2019). Street food research worldwide: a scoping review. Journal African RTE products, a risk profiling of these foods of Human Nutrition and Dietetics, 32, 152–174. with regards to the ability to support L. monocyto- Abuga, K.M., Nairz, M., MacLennan, C.A. & Atkinson, S.H. genes growth under the commonly used temperature– (2023). 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