Microbiology of street food: understanding risks to improve safety

Abstract

Street foods play important socioeconomic and cultural roles and are popular worldwide. In addition to providing convenient and low-cost meals for urban populations, street food offers an essential source of income for vendors, especially women, and it can reflect traditional local culture, which is an important attraction for tourists. Despite these benefits, the microbiological safety of street food has become a worldwide concern because it is often prepared and sold under inadequate safety conditions, without legal control and sanitary surveillance. Consequently, high counts of fecal indicator bacteria and several foodborne pathogens have been detected in street foods. This review provides insight into the microbiology of street food, focus on the associated microbiological safety aspects and main pathogens, and the global status of this important economic activity. Furthermore, the need to apply molecular detection rather than traditional culture-based methods is discussed to better understand the actual risks of microbial infection associated with street foods. Recognition is always the first step toward addressing a problem.

Introduction

The World Health Organization (WHO) defines street foods as ready-to-eat foods and beverages prepared and/or sold by vendors and hawkers in streets and other public places. This definition includes fresh fruits and vegetables sold for immediate consumption outside authorized markets (WHO 1996, WHO 2010). In this sense, street foods are also sold in outdoor locations and enclosed markets, where people gather to shop or engage in recreational activities (Al Mamun and Turin 2016). Therefore, street food vendors can be found clustered around public locations such as schools, colleges, hospitals, bus and train stations, factories, offices, and amusement venues such as carnivals, fairs, and athletic events (Al Mamun and Turin 2016, Malhotra 2017).

Street food trade has historical roots and complex socioeconomic and cultural implications for many countries, including those that have lower incomes and industrialized nations. An estimated 10 million street vendors who sell goods to the public in temporary static structures or mobile stalls constitute ∼2% of metro populations (Malhotra 2017).

Despite their socioeconomic value, safety-related aspects should be considered, because street foods are often prepared and sold under inadequate conditions without legal control or sanitary surveillance, which can increase the risk of foodborne diseases (Abrahale et al. 2019). Although chemicals can poison food and cause such diseases, microbiological (mainly bacterial and viral) contamination is a major safety concern (WHO 2010, Gould et al. 2013, White et al. 2022). Therefore, this review summarizes current knowledge about the microbiology of street foods. Microbiological safety aspects, the main pathogens associated with street foods, and the global status of these important economic products are emphasized. The need to apply molecular detection, rather than traditional culture-based methods is discussed to better understand the actual microbial risk associated with street-vended foods.

We searched PubMed and Google Scholar to identify articles published mainly between January 2010 and June 2022, and a few classical references before this period. We included book chapters, research, and review articles, and restricted the search to full-text articles or abstracts published in English. The search was based on combinations of the keywords, “street food,” “street-vended food,” “microbiological safety,” “safety requirements,” “Campylobacter,” “enteric viruses,” “norovirus,” “hepatitis A virus,” “Staphylococcus,” “Listeria,” “Clostridium,” “Salmonella,” “Shigella,” “Escherichia,” “Enterobacteriaceae,” “vaccination,” and “food safety regulation.”

Street food and its social-economic and cultural role

Selling street food is a social, economic, and cultural phenomenon in an evolving world, especially in urban areas (Fellows and Hilmi 2012, Abrahale et al. 2019). Urbanization and changes in consumer habits, including travel, have increased the numbers of people who buy and consume foods prepared in public places (WHO 2019). Consequently, the amount of time spent cooking meals at home has considerably decreased (Abrahale et al. 2019). For example, the number of street-food stalls in India steadily increased from 920 000 to 1.2 million between 2008 and 2013, indicating that more people are opting to eat outside the home (Shenoy et al. 2022).

Street-vended food plays an important role in ensuring food and nutrition security for urban dwellers worldwide, particularly in lower-income countries where ∼2.5 billion people consume street food daily (Jaffee et al. 2019). The Food and Agriculture Organization (FAO) and WHO have found that the greatest factor in favor of street foods is that they can provide caloric and protein requirements at a cost of ∼$1 per capita (Malhotra 2017). Street food also accounts for >50% of the food intake in several sub-Saharan countries (Jaffee et al. 2019).

Street food plays important roles in providing easily accessible and low-cost meals for urban populations. It also offers essential income sources for those who do not work in formal economic sectors. Women with insufficient education, literacy, or skills in lower-income countries (Malhotra 2017, Jaffee et al. 2019) such as those in Africa can constitute >80% of the street vendor workforce. The level of education among street vendors in some of these countries is generally low, as >20% are illiterate (Bouafou et al. 2021).

Street food trade is an important segment of the food tourism industry that deserves attention. Street foods attract tourists, as they are convenient, relatively inexpensive, and offer unique flavors and experiences that can reflect traditional local cultures (WHO 2010, Khairuzzaman et al. 2014). Thus, street food contributes to the ability of tourists to enjoy authentic gastronomic experiences by linking food, venues, and tourism (Privitera 2014) and is thus one of the best ways to become immersed in the real culture of a community (Malhotra 2017). Therefore, using street food as an instrument for developing attractive regional images offers a clear benefit for creating and maintaining tourism (Privitera 2014).

Microbiological aspects of street food safety

The microbiological safety of street food is influenced by the quality of the raw material used to prepare foods for sale. Food can become contaminated with microbes throughout the production chain from processing, transport, storage, display, and preparation, to serving the food for consumption. The main problems are poor hygiene practices by food handlers, the absence of potable water, inadequate infrastructure, food storage at temperatures that favor microbial growth, exposure to domestic and other animals including rodents and insects, and air pollution (Amare et al. 2019, Abebe et al. 2020).

High ambient temperatures impact the amount of microbial contamination in street foods. Total aerobic bacterial counts in ready-to-eat street food samples are maximal during the summer in Quetta, Pakistan, when the average ambient temperature reaches 37°C (Raza et al. 2021). The authors concluded that an increased abundance of houseflies could also help to explain why microbial contamination is maximal during the summer.

Enteric pathogens in untreated sewage used to fertilize soils or in water to irrigate crops can contaminate raw materials. Such pathogens can multiply exponentially, particularly if used to prepare street food under unhygienic conditions. Some street foods worldwide have high microbial counts and harbor several foodborne pathogens (Birgen et al. 2020, Budiarso et al. 2021, Ferrari et al. 2021, Salamandane et al. 2021).

However, regardless of the sanitary conditions in the environment, microbiologically safe food can be prepared on the street if appropriate food-handling measures are implemented. For example, food cooked to 70°C and served piping hot poses little or no risk of transmitting foodborne pathogens (WHO 2010).

The microbiological safety of street foods is important to consider especially because of the risk of serious infections in children, pregnant women, and elderly, as well as immunocompromised persons. Foodborne diseases cause 2.2 million deaths annually in lower-income countries and 1.9 million of these are children; thus, the microbial contamination of food is more critical in such countries (Loukieh et al. 2018).

Foodborne pathogens and diseases

Among the main problems associated with the consumption of street food, foodborne diseases comprise a substantial preventable public health problem with a major impact on health and economy (Allison et al. 2021). The incidence of toxins and microbes that cause lethal foodborne illnesses is high in lower-income countries. Infection and other illnesses are caused by ingesting foods contaminated with pathogens, and by toxins produced by such pathogens. The main bacterial pathogens that cause foodborne diseases are the Salmonella, Shigella, Escherichia genera that belong to the Enterobacteriaceae family, as well as species such as Staphylococcus aureus, Clostridium perfringens, Listeria monocytogenes, and Campylobacter jejuni (Hemalata and Virupakshaiah 2016, Abebe et al. 2020, Gohan et al. 2021).

Although bacteria are generally responsible for the most severe foodborne diseases, viruses cause the most infections worldwide (Bosch et al. 2018). Several human enteroviruses, such as norovirus (NoV) and hepatitis A virus (HAV) are transmitted by the fecal-oral route and are predominant causes of foodborne diseases. However, they are rarely diagnosed because appropriate analytical and diagnostic tools for these viruses are not widely available, especially in low-income countries (WHO and FAO 2008, Anonymous 2017, Bosch et al. 2018).

The United States Food and Drug Administration (FDA) have highlighted six highly infectious pathogens that cause severe illness and can easily be transmitted by food workers. These six foodborne pathogens are known as the “Big 6″, and include NoV, HAV, Salmonella typhi, Shigella spp., Shiga toxin-producing Escherichia coli and nontyphoidal Salmonella (FDA 2020).

This review aimed to clarify the roles of the “Big 6″ along with S. aureus, L. monocytogenes, Clostridium spp., Campylobacter spp., and viruses as important health hazards associated with street food consumption.

Microbiology of street food

Enterobacteriaceae

The Enterobacteriaceae family of Gram-negative bacteria includes Salmonella spp., E. coli, and Shigella spp. (Addis and Sisay 2015, Al-Seghayer and Al-Sarraj 2021).

Salmonella spp. are rod-shaped, non-spore-forming, facultative anaerobes, and some species cause mild-to-severe infections such as salmonellosis. Salmonella is disseminated via the fecal-oral route and can be transmitted through person-to-person contact, direct contact with other animals, or contaminated food and water. Contaminated unpasteurized milk, cheese, eggs, and poultry are responsible for 94% of all Salmonella infections. The incubation period is 12‒36 hours and the symptoms are usually gastrointestinal, including vomiting, abdominal cramps, nausea, and bloody diarrhea with mucus. Most symptoms resolve within 2‒3 days but they can be more severe among elderly persons and young children (Addis and Sisay 2015, Al-Seghayer and Al-Sarraj 2021).

Escherichia coli are rod-shaped, motile, facultatively anaerobic, and nonspore-forming bacteria. Some of its pathotypes cause enterohemorrhagic (EHEC), enterotoxigenic (ETEC), enteropathogenic (EPEC), enteroinvasive (EIEC), and enteroaggregative (EAEC) diseases, but all of these pathotypes cause intestinal symptoms in humans. However, their modes of transmission differ; they target intestinal cells, and symptoms are based on types of virulence factors and toxins (Kim et al. 2020). The incubation period vary from 72 to 120 hours. Diarrhea with abdominal cramps can become grossly bloody within a few days, and bacteremia and toxemia can occasionally develop (Clements et al. 2012, Addis and Sisay 2015, Al-Seghayer and Al Sarraj 2021).

Shigella spp. are rod-shaped, nonmotile, nonspore-forming, facultative anaerobes that cause shigellosis. Shigella infections arise via direct person-to-person transmission or contaminated water and food. Ingested Shigella spp. attach to intestinal cell walls, multiply, and produce enterotoxins and serotype toxin 1 that cause watery or bloody diarrhea. Shigella infection manifests as high fever, vomiting, abdominal pain, and tenesmus (Addis and Sisay 2015). The genus Shigella has four serotypes (A–D), of which Shigella sonnei (serotype D) causes a mild illness that can be limited to watery diarrhea, whereas Shigella flexneri (serotype B) and Shigella dysenteriae (serotype A) can cause dysentery that presents as bloody mucoid diarrhea (McCrickard et al. 2018).

Ferrari et al. (2021) analysed street food in Brazil and showed Salmonella spp. in 6.3% (n = 4) of the samples, 1 of hot dogs and 3 of savoury snacks. All savory snacks contaminated with Salmonella spp. were fried, suggesting that they had been cross-contaminated, or re-contaminated after frying. The absence of Salmonella spp. in 25 g of food was employed in this study as the microbiological limit.

Raw chicken portions were highly contaminated with Salmonella spp., which were also found in cooked chicken, food contact surfaces, and equipment such as knives and storage containers in Nairobi, Kenya (Birgen et al. 2020).

A microbiological analysis classified 121 (37.81%) of 320 ready-to-eat street food samples in Quetta, Pakistan as unacceptable for consumption due to high total counts of aerobic bacteria. Approximately 49 (40%) of 121 of food samples that were not suitable for human consumption were contaminated with Salmonella spp., of which 34 (69.39%) and 15 (30.61%) were S. enteritidis and S. typhimurium, respectively. Both species were extremely resistant to amoxicillin, all S. enteritidis isolates were resistant to erythromycin and chloramphenicol, and S. typhimurium isolates were resistant to erythromycin (Raza et al. 2021).

Escherichia coli was found in all analyzed samples savory snacks, hot dogs, coconut water, barbecued meat on skewers, and boiled corn, with savory snacks harboring the most counts (1.15 × 10⁵ colony forming units [CFU] g⁻¹) (Ferrari et al. 2021). Brazilian legislation states that the limit for E. coli counts in these foods is <10² CFU g⁻¹.

Salamandane et al. (2021) analysed 83 ready-to-eat street food sold in Maputo, Mozambique, and in traditional hot foods, 63% of the samples were classified as unsatisfactory due to contamination with E. coli (>2.8 log CFU g⁻¹). Considering total coliforms as a hygiene indicator, this ratio increased to 76.7% (>2 log CFU g⁻¹). Furthermore, 62.5% and 75% of sandwich samples, respectively, containing >2.5 and > 3 log CFU g⁻¹ of E. coli, were classified as unsatisfactory, and 80% of ready-to-eat salad samples contaminated with > 2.4 log CFU g⁻¹ of E. coli and >3.4 log CFU g⁻¹ of coliforms were classified by both indicators as unsatisfactory. Despite the high counts of total coliforms and E. coli, all samples were negative for Salmonella and L. monocytogenes.

An analysis in Yogyakarta City, Indonesia revealed that all of 30 street food samples were contaminated with coliforms, most of which exceeded the threshold limit set by the National Agency of Drug and Food Control (BPOM). Furthermore, coliforms and enteric pathogens in snack foods included E. coli (16.6%), Yersinia enterocolitica (13.3%), and Shigella spp. (3.3%) (Budiarso et al. 2021).

In Quito, Ecuador, 22.6% of ready-to-eat street foods were positive for total thermotolerant coliforms resistant to cefotaxime. The clonal groups ST410, ST131, and ST744 were recognized as epidemic and showed that harmful commensal E. coli could be directly acquired from specific types of food (Zurita et al. 2020). These foods might also play significant roles in the dissemination of antimicrobial resistance (Economou and Gousia 2015).

Clostridium

Within the genus Clostridium, C. botulinum and C. perfringens are important from a public health standpoint in terms of foodborne diseases.

Clostridium botulinum is a Gram-positive, anaerobic, spore-forming bacillus that produces highly potent neurotoxins that cause botulism in humans. This toxin blocks the release of acetylcholine at neuromuscular junctions, resulting in flaccid paralysis. Respiratory failure can develop if botulism is not treated promptly and appropriately. The incubation period is 12‒36 hours. The most prevalent symptoms are vomiting, dry mouth, thirst, constipation, ocular paresis, and difficulty with breathing, speaking, and swallowing (Addis and Sisay 2015, Pernu et al. 2020).

Clostridium perfringens is a Gram-positive, anaerobic, spore-forming bacillus that produces a type A enterotoxin that is directly involved in food poisoning. This toxin causes excessive accumulation of fluid in the intestinal lumen. The incubation period is 8‒24 hours, and the main symptoms are acute abdominal pain, vomiting, and diarrhea, which are usually self-limiting (Addis and Sisay 2015, Gohan et al. 2021).

Meat and poultry contaminated with C. perfringens are particularly important causes of foodborne outbreaks. C. perfringens has been detected in 5.06% of cooked beef sold on streets in the Ivory Coast (2.32% and 7.17% in kidney and flesh samples, respectively). The prevalence of C. perfringens in cooked beef was the highest and lowest in Abobo (12%) and Yopougon (1.85%), respectively (Kouassi et al. 2014).

Listeria monocytogenes

Listeria monocytogenes is a Gram-positive, ubiquitous bacterium that can survive the harsh acidic or saline conditions and low temperatures that are usually applied in food processing for microbial control. Consequently, L. monocytogenes is difficult to manage as it can persist for long periods in food-processing environments and cross-contaminate food products (Gray et al. 2021). The ability to withstand food-processing environments is probably linked to resistance against common cleaning and sanitation strategies, a high adaptive capacity against physical control methods, and the ability to form biofilms on various surfaces (Carpentier and Cerf 2011, EFSA BIOHAZ Panel et al. 2018).

Despite being relatively rare compared with other bacterial foodborne diseases, listeriosis is among the most serious foodborne infections of humans due high mortality rates (20%‒30%) among at-risk immunocompromised and elderly persons, pregnant women, and neonates. Clinical manifestations include febrile gastroenteritis, which can lead to severe complications, including sepsis and meningitis. Serious perinatal infections can lead to abortion, stillborn fetuses, generalized infections, sepsis, and neonatal meningitis (Lopez-Valladares et al. 2018).

Ready-to-eat meat, seafood products, unpasteurized milk, and other dairy products are typically associated with L. monocytogenes. However, fruits and vegetables, plant-derived foods, frozen foods, and sandwiches have also been implicated in outbreaks (Desai et al. 2019), indicating that various foods support L. monocytogenes growth and can contribute to the burden of listeriosis.

Listeria spp. have been identified in 24% of 576 samples of ready-to-eat street-vended foods including sandwiches and traditional dishes sold in Egypt (El-Shenawy et al. 2011); L. monocytogenes and L. innocua were isolated in 57% and 39% of positive samples, respectively. Most samples contaminated with L. monocytogenes had high levels of total viable bacterial counts (>10⁴ CFU g⁻¹). Nyenje et al. (2012) evaluated the microbiological quality of 252 ready-to-eat foods sold in Alice, South Africa, including vegetables, potatoes, rice, pies, beef and chicken stew. High levels of total aerobic count were detected in all the samples analyzed, and a high occurrence of Listeria spp. was recorded in pies (33%) and chicken stew (28%).

Two pulsed field gel electrophoresis (PFGE) types (serotypes 1/2a and 4b) of L. monocytogenes have been detected in 20% of hotdog and hamburgers samples from 10 street-vending trailers in the Porto region, Portugal. Two L. monocytogenes clones were detected in different samples/trailers, suggesting cross-contamination or a common source of contamination (Campos et al. 2015).

Listeria monocytogenes isolates from 6% of 261 samples of ready-to-eat salads sold on the streets in Turkey were resistant to erythromycin (23%) and cephalothin (20%) (Gurler et al. 2015). Listeria monocytogenes has been detected in 15% of 96 samples of ready-to-eat meat sold on the streets of Windhoek, Namibia (Shiningeni et al. 2019) and in 7.5% of 400 ready-to-eat artisanal foods in Chile, all of which also harbored the virulence genes hlyA, prfA, and inlA (Bustamante et al. 20,20).

The overall prevalence of L. monocytogenes was 0.13% in samples of various ready-to-eat foods collected over a period of two years from 28 large retailers and 148 canteens in northern Italy (Castrica et al. 2021). The authors detected L. monocytogenes particularly among multi-ingredient preparations comprising cooked and uncooked food or only raw ingredients (0.54% of 554 evaluated samples).

A global systematic review revealed that the pooled prevalence of L. monocytogenes in ready-to-eat chicken products is 22%, followed by various uncategorized, ready-to-eat foods (21%) and that the pooled prevalences of antibiotic resistance to penicillin and cephalosporin are respectively, 80% and 47% (Mpundu et al. 2021).

Coagulase positive staphylococci

The genus Staphylococcus comprises spherical, nonsporulating, nonmotile facultatively anaerobic, Gram-, and catalase-positive bacteria. Staphylococcus spp. are ubiquitous in air, dust, sewage, water, environmental surfaces, humans, and other animals (Hennekinne et al. 2012).

Staphylococcus spp. are classified as coagulase-producing (CPS) or noncoagulase-producing (CNS) strains, and the main CPS species is S. aureus (Hennekinne et al. 2012).

Some CPS strains (mainly S. aureus and occasionally other species), while growing in foods, produce enterotoxins that can lead to staphylococcal food poisoning. This is typically characterized by severe nausea and vomiting within 2‒8 hours of consuming contaminated food. Notably, the cooking process destroys S. aureus, but is insufficient to inactivate its heat-stable enterotoxins (Schelin et al. 2011).

Although enterotoxigenic potential is not a relevant feature among CNS bacteria, some strains express staphylococcal enterotoxin genes and other virulence factors (Ünal and Çinar 2012). Although CNS play important roles in the fermentation of meat- and milk-based products, high counts in other types of foods have been associated with ineffective hygienic-sanitary conditions (Janssens et al. 2013).

Staphylococcus aureus is among the normal microbiota of the skin and in the upper respiratory tracts of healthy humans and it can be transmitted to various types of food, mostly via asymptomatic handlers. Another frequent source of S. aureus is unpasteurized milk from dairy animals with mastitis. Food contamination with enterotoxigenic CPS is usually caused by either inadequate food handling or unpasteurized milk from cows with staphylococcal mastitis (Hennekinne et al. 2012).

Staphylococcal food poisoning is a common foodborne disease worldwide. It might involve foods that provide a suitable medium for S. aureus growth such as unpasteurized milk cheese, especially when handmade, as well as meat- or meat-based products, poultry, salads, and cream-filled pastries (Hennekinne et al. 2012).

Street foods can become contaminated by staphylococci in raw materials and/or poor hygiene practices during processing, cooking, or distribution. Street foods are generally associated with conditions that favor staphylococcal growth and enterotoxin production, such as nutritional content and permissive temperatures during storage (Bennett et al. 2013). Ingesting street foods containing sufficient amounts of enterotoxins can be poisonous.

Outbreaks of Staphylococcal food poisoning after consuming street food are probably underreported, not only because it is a short-term and self-limiting illness but also because it is difficult to identify the food responsible for carrying the enterotoxin, especially when only a few people are affected.

Coagulase-positive staphylococci were undetectable in samples from hotdogs and hamburgers sold at trailers on the streets of the Porto region of Portugal, even though 44% of those from food-handlers were positive for CPS (Campos et al. 2015). Poor hygiene practices have been identified in Uberaba, Brazil, where 47% of street food vendor hands were contaminated with high levels of CPS (Souza et al. 2015). In addition, S. aureus has been detected in 52% of ready-to-eat meat samples sold on the streets of Windhoek, Namibia (Shiningeni et al. 2019).

The contamination of handmade coalho cheese samples with S. aureus has been associated with contaminated milk, re-contamination after pasteurization, and inadequate storage and handling (Andrade et al. 2019). Furthermore, CPS have been detected in ∼25% of ready-to-eat street food samples sold in Maputo, Mozambique (Salamandane et al. 2021).

Campylobacter

The genus Campylobacter comprises microaerophilic, nonspore-forming, curved, slender Gram-negative rods, 0.5‒5-μm long, and have a characteristic corkscrew-like motion (Silva et al. 2011, Facciolà et al. 2017, Igwaran and Okoh 2019). When at least two of these cells come into contact, they form an “S” shape or the “V” shape of a gullwing (Silva et al. 2011).

Campylobacter is the most common bacterial cause of human gastroenteritis worldwide (Corcionivoschi and Gundogdu 2021). Campylobacter infects ∼1.5 million persons annually in the USA (US Centers for Disease Control and Prevention [CDC] 2019a). Globally, pathogenic Campylobacter species infect >400 million people annually (Igwaran and Okoh 2019, Corcionivoschi and Gundogdu 2021). In general, >80% of human isolates are C. jejuni, and C. coli accounts for most of the remainder (Fontanot et al. 2014, Igwaran and Okoh 2019). That C. jejuni is resistant to multiple antibiotics is a matter of particular concern (Corcionivoschi and Gundogdu 2021).

Campylobacteriosis is characterized by diarrhea (often bloody in high-resource countries rather than the watery diarrhea that occurs mostly in young children living in low-resource areas), fever and abdominal pains, but nausea and vomiting can also occur. Most people infected with Campylobacter completely recover within one week. However, serious postinfectious sequelae, such as neuromuscular paralysis due to Guillain-Barré syndrome can arise. Campylobacter can occasionally spread into the bloodstream of immunocompromised individuals and cause life-threatening infection (CDC 2019a, Corcionivoschi and Gundogdu 2021).

Campylobacter spp. are commensal microorganisms that colonize the intestinal tract of warm-blooded animals and frequently infect all avian species that are suitable for human consumption. Thus, the main route of campylobacteriosis transmission in humans is through the consumption of undercooked poultry meat (Facciolà et al. 2017, CDC 2019a). In fact, 60%‒80% of global campylobacteriosis is caused by ingested contaminated poultry meat and its products (Igwaran and Okoh 2019).

Campylobacter is also transmitted by drinking untreated water and raw milk, as well as fruits and vegetables that are contaminated via contact with soil or water containing feces from cows, birds, and other animals (Carrillo et al. 2017, Facciolà et al. 2017, CDC 2019a). Therefore, eating raw fruits and vegetables is inherently risky when not treated to inactivate pathogens before consumption (Mohammadpour et al. 2018; Bozkurt et al. 2021). Indeed, in the USA, for example, the consumption of fresh fruits and vegetables has increased in recent years, and concomitantly, the number of outbreaks caused by microbial pathogens associated with these fresh products has also increased (Carstens et al. 2019).

A low infective dose (≤100 cells) of Campylobacter has been linked to human infections (Igwaran and Okoh 2019). Therefore, ingesting anything that has touched raw or undercooked poultry contaminated with Campylobacter can cause campylobacteriosis. Even a single drop of juice from raw chicken can contain sufficient bacteria to cause infection. Thus, infections can arise when kitchen utensils used to cut and prepare raw chicken are not washed before being applied to prepare raw fruits and vegetables (Facciolà et al. 2017, CDC 2019a).

Considering that improper food handling and poor hygiene practices are prevalent among street food handlers, street foods should be an important source of Campylobacter contamination. However, surprisingly there are only a few studies on the occurrence of Campylobacter in street food in the last decade. We speculated that one reason for this is that Campylobacter species are fastidious and difficult to culture (Corcionivoschi and Gundogdu 2021). Recovery of these bacteria from food samples is challenging because they grow slowly and competing organisms must be suppressed during isolation (Carrillo et al. 2017).

Most studies exploring the bacterial contamination of street food have used culture-based methods to recover and identify foodborne pathogens. Nevertheless, there is evidence that molecular methods are more effective in detecting Campylobacter than conventional methods, as molecular methods also allow detection of cells that are viable but cannot be grown on agar media due to starvation and physical stress (Chai et al. 2007, Fontanot et al. 2014).

Campylobacter was not detected by traditional culture techniques in samples of ready-to-eat street-vended pork meat sold on the streets of Antananarivo, Madagascar (Cardinale et al. 2015). A C. jejuni contamination rate of 0.5% has been identified in raw fish samples from Morogoro Municipality, Tanzania (Nonga et al. 2015). In contrast, high C. jejuni counts were detected on the hands of street food vendors, and work surfaces (knife, food contact surface, storage container), as well as raw and cooked chicken sold on the streets of Nairobi County, Kenya (Birgen et al. 2020). Contamination with C. jejuni was the highest in raw portions of chicken products and in cooked chicken samples (range: 8.95 ± 0.94 to 4.66 ± 2.67 log CFU g⁻¹, respectively). Counts on storage containers, work surfaces, and hands, and between knives and cooked chicken did not significantly differ. This was attributed to cross-contamination, especially via hands and unsanitary conditions at vending sites.

A meta-analysis revealed that the overall estimated prevalence of Campylobacter in fresh vegetables and fruits from various geographical areas and origins, including ready-to-eat street foods, is 0.53%. Interestingly, the results of this meta-analysis demonstrated that the highest prevalence of Campylobacter were detected when molecular techniques were employed (Mohammadpour et al. 2018). Thus, these authors concluded that the lower rates of isolation were probably due to problems associated with the growth and recovery of microorganisms. In line with this notion, Chai et al. (2007) state that the lack of appropriate methods for recovering Campylobacter from produce samples could explain part of the reported low incidence of this bacterium in vegetables.

Viruses

Human enteric viruses are extremely widespread causes of foodborne diseases. The numbers of foodborne illness outbreaks caused by viruses have steadily increased over the past few years in industrialized countries to the point where they have superseded bacteria as the most common cause of such outbreaks and pose a serious threat to global health (Bosch et al. 2018).

Human enteric viruses represent functional, rather than taxonomic groups (Gibson et al. 2019). Thus, viruses belonging to different genera and families are considered human foodborne agents, including NoV (Caliciviridae), HAV (Picornaviridae), hepatitis E virus (HEV) (Hepeviridae), rotaviruses (Reoviridae), enteroviruses (e.g. Poliovirus and Coxsackievirus) (Picornaviridae), adenoviruses (Adenoviridae), and astroviruses (Astroviridae). From an epidemiological perspective, NoV and HAV are the most significant foodborne viruses (WHO and FAO 2008, Vasickova et al. 2010, Gibson et al. 2019, O'Shea et al. 2019).

Despite increasing knowledge about the role of viruses as widespread causes of foodborne illnesses, the literature currently provides an unrealistic appraisal of their importance as hazards associated with street food. We could not find any reports on the detection of viruses in street food. However, this does not mean that a problem does not exist. Considering that many street food vendors overlook the importance of the safety of food that they prepare and sell (Azanza et al. 2019), street food contamination by human enteric viruses can be a very real and serious problem.

This problem must be addressed, particularly in lower-to-middle-income countries where street food is mainly prepared and sold without appropriate hygienic measures (Raza et al. 2021). This is due to factors such as inadequate knowledge about food safety and practices (Birgen et al. 2020), the absence of toilets, and clean running water for washing hands and utensils (Malhotra 2017, Azanza et al. 2019). Epidemiological evidence indicates that the consumption of ready-to-eat foods contaminated by infected food handlers is a major risk factor for foodborne viral outbreaks (Butot et al. 2009, Bosch et al. 2018). Furthermore, policies and regulations for safe street food trade are very weak and poorly enforced in most lower-income countries, and nonexistent in some others (Alimi 2016).

In addition, the absence of information regarding the association of viruses with street food is not surprising, due to difficulties in the detection and quantitation of infectious virus particles in food matrices (Anonymous 2017, Bosch et al. 2018). That infections caused by foodborne viruses have only recently started to be routinely surveilled in some industrialized countries is notable (Bosch et al. 2018).

For instance, the numbers of foodborne viral disease outbreaks since 1998 have significantly increased in the USA (Gould et al. 2013, White et al. 2022). Rather than a true increase in the number of foodborne virus outbreaks, this was likely caused by increased capacity to diagnose NoV (leading cause of foodborne illnesses) in state health department laboratories and improved strategies for collecting specimens for diagnostic tests. Thus, the number of outbreaks of unknown etiology decreased proportionately as the number of viral etiology outbreaks increased (Gould et al. 2013). The association between viruses and foodborne illnesses is likely to increase as current methods of detecting viruses improve and novel detection strategies are developed (Bosch et al. 2018).

However, even in high-income countries, outbreak investigations are costly and require time, resources, and commitments from competing priorities. Thus, most jurisdictions prioritize investigations associated with pathogens that might cause more severe illnesses. Thus, in the USA, most jurisdictions prioritize investigations associated with pathogens that may cause more severe illness and consequently may intentionally deprioritize NoV outbreaks (White et al. 2022). Challenges for outbreak investigations are significantly more pronounced in lower-income countries, and this can help explain the divergent data regarding the association of NoV with foodborne disease outbreaks between high-income countries and lower-to-middle-income countries. The results of surveillance in the USA from 2009 to 2018 showed that NoV caused 47% of outbreaks with a single confirmed or suspected etiology (White et al. 2022), whereas it accounted for only 2.5% of outbreaks with identified etiological agents between 2000 and 2018 in Brazil (Finger et al. 2019).

The lack of data on foodborne viral infections associated with street food might also be associated with the fact that most of these infections, such as those caused by NoV, either do not lead to clinically obvious diseases or lead to gastroenteritis, which is usually an acute and self-limiting disease. Therefore, because most infected individuals do not consult a medical practitioner; most infections have not been reported or followed up (Vasickova et al. 2010).

Laboratory analyses of street-food samples for microbiological purposes have traditionally relied solely on bacterial cultures. Consequently, many authors have documented high levels of total coliforms in some street food samples in addition to pathogenic bacteria such as Salmonella spp. (Birgen et al. 2020, Ferrari et al. 2021), S. aureus (Shiningeni et al. 2019), C. perfringens (Kouassi et al. 2014), and Campylobacter spp. (Birgen et al. 2020), as already discussed here. However, published findings of foodborne disease outbreaks indicate that reliance solely on routine bacterial culture is inadequate for monitoring the microbiological quality of street food (Gould et al. 2013, White et al. 2022). The presence or absence of bacterial faecal indicators in food such as E. coli, has proven to be unreliable to indicate presence of enteric viruses, since various studies have shown that some foodborne viruses are more resistant than vegetative bacteria (Bosch et al. 2018).

The environmental stability of viral particles is crucial for the persistence and transmission of enteric viruses to new hosts. One of the most important factors affecting their survival is a viral envelope. Nonenveloped viruses, including most of those that cause foodborne diseases, are more resistant to drying or desiccation and therefore spread more easily than enveloped viruses (which are less stable in the environment). In contrast to some enveloped viruses that remain infectious for a few hours to days, foodborne enteric viruses can survive for several weeks to months on various surfaces (Vasickova et al. 2010).

Human enteric viruses are also resistant to a wide range of popular food processing, preservation, and storage methods (Gibson et al. 2019). For instance, frozen berries, including blackberries, raspberries, strawberries and blueberries, have been implicated in several foodborne illness outbreaks. In such cases, the hazard of concern has been viral, since freezing maintains viral infectivity (WHO and FAO 2008, Bozkurt et al. 2021). Enteric viruses in freeze-dried blueberries can also resist inactivation by dry heating at 100°C for 20 min (Butot et al. 2009). Foodborne viruses can survive beyond the shelf life of fresh produce, and in shellfish enteric viruses are known to persist for several weeks or months (Bosch et al. 2018).

Therefore, the chain of enteric viral infections is difficult to analyze. In addition to the environmental resistance of viral particles, enteric viruses are shed in high numbers in the feces and/or vomitus of infected individuals (Gibson et al. 2019). Viruses can be shed for up to two weeks postrecovery (O'Shea et al. 2019). This means that a food handler who returns to work after acute symptoms of an enteric virus infection have subsided, but before the infectious period has ended, poses a risk of contaminating food products during preparation (Hardstaff et al. 2018). Furthermore, infected asymptomatic persons can spread enteroviruses (O'Shea et al. 2019), although they tend to shed fewer viruses than those who are symptomatic (Hardstaff et al. 2018). For example, HAV can be transmitted by asymptomatic people via feces for up to 2 weeks before and 2 weeks after symptoms appear (Fleetwood 2021).

Unlike bacteria, viruses are obligate intracellular parasites that do not replicate outside their host cells and low numbers are frequently found in contaminated foods. However, enteric viruses are generally highly infectious (Bozkurt et al. 2021). For example, current estimates suggest that the NoV infective dose (number of NoV particles required to cause detectable infection), might be 1‒10 (Bosch et al. 2018). Thus, although the viral load is frequently low in contaminated foods, it could pose a significant public health risk (Gibson et al. 2019). In addition, the finding of enteric virus particles in the hands of food handlers indicates easy transfer among utensils, work surfaces, and foods (Hardstaff et al. 2018).

Guidance documents

Guidelines specific for street-vended foods have not been fully established worldwide. The Codex Alimentarius normative guidelines, which could assist governments in developing standards consistent with international norms, do not specifically cover traditional markets (defined as spaces for purchasing fresh food for home preparation or food prepared on the street). However, the Codex has developed four regional documents that include codes of practice and guidelines for managing safety risks in street foods. These normative codes were developed in 1995 for the Latin America and the Caribbean (LAC) region (revised in 2001 by the Codex Regional Coordinating Committee for LAC: Codex Alimentarius 2001), 1997 for the African region (Codex Alimentarius 1997), 2013 for the Near East region (Codex Alimentarius 2013), and 2017 for the Asian region (Codex Alimentarius 2017), and have been extensively compared (DeWaal et al. 2022).

All regional guidelines provide important standards that can be used to improve the safety of street vendors and other foods sold in traditional markets. However, given the different approaches among the regional guidelines, global standardization for managing food safety in traditional markets should be considered by international organizations such as the Codex, WHO, and FAO to assist national, regional, state, and local governments (DeWaal et al. 2022).

Vaccination as a strategy for foodborne diseases control

Traditional tactics such as improving basic sanitation, supplying safe drinking water, proper hygiene, and educational programs for food handlers are crucially important in reducing the transmission of foodborne pathogens. However, they might be insufficient to guarantee the microbiological safety of street-vended foods (Deng 2015, Seo et al. 2020, Shenoy et al. 2022). Indeed, sanitation programmes are harder to implement broadly and take longer to achieve modest improvements (Deng 2015).

A study of street food vendors in India revealed that although most of them were familiar with the terms, “food hygiene” and “foodborne illness,” less than one-third of them had acceptable food preparation practices, mainly attributable to an indifferent attitude towards food safety (Shenoy et al. 2022). Therefore, a high prevalence of general awareness of hygiene and food safety principles among food handlers does not guarantee that such principles will be implemented during food preparation.

Considering this, effort has been directed towards supplementing traditional approaches to reduce the health and economic impact of foodborne pathogens (Deng 2015). Vaccines might an effective and practical preventive approach against some common viral and bacterial foodborne pathogens, particularly in resource-limited countries or regions where the implementation of sanitation systems and the supply of safe drinking water are not quickly achievable (Seo et al. 2020). Vaccination is popular because cost-effective results are immediate and immunity is rapidly build in populations (Deng 2015).

The development of effective vaccines targeting enteric pathogens is challenging due to many factors (Seo et al. 2020). These include genetic and antigenic heterogeneity among strains (many genotypes, serotypes, or pathotypes), the absence of suitable animal models to verify vaccine efficacy, and the absence of suitable or cost-effective cell culture systems to attenuate viral pathogens such as human Calicivirus. Superficial knowledge about pathogen virulence or disease mechanisms (such as those of nontyphoidal Salmonella or Campylobacter), short-lived protective immunity, and inability to achieve satisfied efficacy among some populations (such as young children in endemic regions) are also factors. In addition, multiple pathogens in individual patients during enteric infection complicates the effectiveness of vaccination. This limitation might be addressed by developing vaccine combinations targeting at least two enteric pathogens and in silico predictions combining computational biology and protein modeling.

However, vaccines are commercially available only for HAV (Fleetwood 2021) and S. typhi (Seo et al. 2020) among the “Big 6″ foodborne pathogens that cause severe illness and are transmitted by food workers.

The vaccination of high-risk populations can prevent foodborne infections. The WHO considers food handlers as a risk group for HAV (Shenoy et al. 2022), because only a single food handler with HAV is needed transmit the virus to many people, thus creating a substantial economic burden on the public health system (Fleetwood 2021). Because people infected with HAV are most contagious before they become symptomatic, and because children and immunocompromised people can remain contagious for up to 6 months, mandating symptomatic workers in food services to remain home is insufficient (Fleetwood 2021). Thus, vaccinating food handlers is considered an important step in preventing HAV transmission to susceptible individuals (Shenoy et al. 2022).

The current body of evidence about the topic should be a wake-up call for policymakers in low- and middle-income countries with high and intermediate endemicity to make vaccination against HAV mandatory for food handlers and not rely merely on standard interventions such as investigation, education, appropriate sanitation, and hygiene (Shenoy et al. 2022).

India is of particular interest because it is currently transitioning from high to intermediate HAV endemicity due to rapid socioeconomic development in some areas. Consequently, a growing proportion of the population is no longer exposed during childhood when the infection is usually asymptomatic and provides lifelong protection against the disease. Consequently, adolescents, and young adults (who constitute the majority of food handlers) are presently more susceptible than in the past, HAV infection is more severe, and the number of outbreaks has increased compared with before (Agrawal et al. 2019). Therefore, vaccinating food handlers in India could prevent HAV infection as well as its complications and transmission. The Indian Medical Association (IMA) and Association of Physicians of India (API) recommend HAV vaccination for food handlers (Shenoy et al. 2021).

The value of immunization for food handlers has also been proven in high-income countries such as the USA. Several HAV outbreaks in St. Louis, MO, USA led to the implementation of mandatory HAV vaccinations by food handlers. Subsequently, the rate of HAV infections dropped from 3 to 1 per 100 000 population. The Alabama Department of Public Health, Immunization Division, recommended statewide HAV vaccination during 2019 for all food workers in response to a local outbreak (Shenoy et al. 2021). However, mandatory HAV vaccination for food service workers is only ethically justifiable based on scientific evidence of transmission from workers to consumers in high-income countries (Fleetwood 2021). The endemicity of HAV infection is associated with hygiene status and sanitary infrastructure; hence all high-income countries have very low endemicity (Suwantika et al. 2013). Thus, transmission from food handlers to customers is rare with practice of good food hygiene (Fleetwood 2021).

Few vaccines against foodborne bacterial pathogens have been licensed. The heterogeneity of the serogroups or pathotypes, as well as difficulties with identifying appropriate antigens to target enterotoxins remains a key challenge. However, several vaccine candidates are under investigation, including live attenuated or killed whole-bacterial cells, glycoconjugates or bioconjugates, and bacterial polysaccharide- and protein-based subunits (Seo et al. 2020). Most are in the preclinical stage, but a few vaccine candidates have undergone phase I, II, or even phase III trials.

Only two typhoid vaccines against foodborne bacterial pathogens are commercially available. They help to prevent typhoid fever caused by S. typhi that is common in many regions of the world, including parts of East and Southeast Asia, Africa, the Caribbean, and Central and South America. One each of these vaccines is based on killed, and live attenuated bacterial cells. Although not recommended as a routine procedure and despite being unable to provide 100% protection, typhoid vaccination is recommended for those traveling to endemic areas, people in close contact with typhoid carriers, and laboratory workers who work with S. typhi (CDC 2019b).

Concluding remarks

Recent socioeconomic changes in an evolving world have driven significant growth in street food sales. Urbanization and population growth are associated with difficulty in finding employment in the formal sector, particularly in lower- income countries, and this is predicted to continue. Consequently, the street food sector will likely expand as it provides a livelihood for numerous workers/families and offers business opportunities, making it a significant part of the urban food supply chain.

Despite their popularity and social, economic, and cultural implications, street food vending activities are mostly outside government regulations, and street foods can be vehicles for several foodborne pathogens, which remain a threat to public health. The microbiological quality of street foods is poor in various countries, particularly those with low incomes, where high levels of contamination by pathogenic and/or fecal indicator bacteria are often detected. A finding of particular concern is antibiotic resistance among pathogenic foodborne bacteria isolated from street foods. Such foods might play a significant role in the spread of antimicrobial resistance.

Microbiological safety is primarily analyzed using culture-based methods that focus on the isolation and quantitation of bacteria such as the the Enterobacteriaceae family, specifically Escherichia and Salmonella genera, and Staphylococcus species. Thus, the prevalence of microorganisms that are detected in street food using molecular techniques is probably underestimated. This is true for all human enteric viruses, but also for some fastidious bacteria such as Campylobacter spp. Therefore, the application of reliable and standardized molecular techniques to detect such microorganisms in street foods has become increasingly important.

The supply of potable water, sanitation systems, personal hygiene, training programs to improve knowledge of basic food safety measures, and good food handling practices should be stimulated and implemented to improve the microbiological quality of street foods. Vaccinating food handlers against common viral and bacterial foodborne pathogens is recommended when available.

Conflict of interest

None declared.

Author contributions

Anderson Assunção Andrade (Conceptualization, Formal analysis, Supervision, Writing – original draft, Writing – review & editing), Aline Dias Paiva (Conceptualization, Formal analysis, Writing – original draft, Writing – review & editing), and Alessandra Barbosa Ferreira Machado (Conceptualization, Formal analysis, Writing – original draft, Writing – review & editing)

References