ABSTRACT

Cross-contamination of raw food to other surfaces, hands, and foods is a serious issue in food service. With individuals eating more meals away from home, contracting a foodborne illness from a food service establishment is an increasing concern. However, most studies have concentrated on hands or food contact surfaces and neglected atypical and unusual surfaces (surfaces that are not typically identified as a source of cross-contamination) and venues. This review was conducted to identify atypically cross-contaminated surfaces and atypical venues where cross-contamination could occur that have not been examined thoroughly in the literature. Most surfaces that could be at risk for cross-contamination are frequently touched, are rarely cleaned and sanitized, and can support the persistence and/or growth of foodborne pathogens. These surfaces include menus, spice and condiment containers, aprons and coveralls, mobile devices and tablets, and money. Venues that are explored, such as temporary events, mobile vendors, and markets, are usually limited in space or infrastructure, have low compliance with proper hand washing, and provide the opportunity for raw and ready-to-eat foods to come into contact with one another. These factors create an environment in which cross-contamination can occur and potentially impact food safety. A more comprehensive cleaning and sanitizing regime encompassing these surfaces and venues could help mitigate cross-contamination. This review highlights key surfaces and venues that have the potential to be cross-contaminated and have been underestimated or not fully investigated. These knowledge gaps indicate where further work is needed to fully understand the role of these surfaces and venues in cross-contamination and how it can be prevented.

HIGHLIGHTS
  • The role of atypical surfaces in cross-contamination is underestimated.

  • Cross-contamination is not well characterized in atypical retail venues.

  • Proper cleaning, sanitizing, and hand washing lowers the risk of cross-contamination.

  • Further work on cross-contamination of atypical surfaces and venues is needed.

Foodborne disease constitutes a serious burden on public health, with annual estimates of >48 million illness cases in the United States and 600 million illness cases globally (76, 95). According to the U.S. Centers for Disease Control and Prevention, 61% of outbreaks associated with a single preparation location from 2009 to 2015 were linked to food consumed outside of the home (24). These outbreaks are a concern because individuals are spending up to 50% of their food budget on eating at food service establishments outside of the home (75). A variety of foodborne pathogens, such as Escherichia coli, Salmonella, Staphylococcus aureus, and Clostridium perfringens, have been linked to such outbreaks in the past, and these outbreaks highlight the myriad of ways food can become contaminated in a retail or food service environment (75, 88). Although many factors potentially contribute to pathogen contamination of food served outside the home, cross-contamination is one of the most thoroughly characterized (16, 46, 52, 87, 88).

Cross-contamination (transfer of microbes from a raw product to another surface or product) occurs in the food service industry in numerous ways (16, 24, 46, 52, 88). Traditionally, cross-contamination occurs between raw products and food contact surfaces, food handlers, and ready-to-eat (RTE) foods (14, 32, 47, 61, 70, 72, 73, 83). Cross-contamination can result in contamination of 13.8 to 81.8% of RTE products (38, 55). However, these traditional routes of contamination do not encompass all the potential surfaces that could become contaminated with a pathogen and present a danger to both employees and consumers.

Atypical cross-contaminated surfaces are surfaces that are not routinely associated with cross-contamination, such as menus, spice containers, and other surfaces not frequently in contact with food. These surfaces differ depending on location, restaurant, home, mobile food enterprise, and the type of food prepared. Although much speculation has been associated with atypical cross-contaminated surfaces, very little research has been conducted on the frequency and risk of cross-contamination associated with these surfaces. Some research has suggested that menus, currency, spice containers, and other atypical surfaces could be a concern for cross-contamination (25, 35, 81, 88), but the role these surfaces play in cross-contamination not well characterized. Little information is available on cross-contamination in atypical food service venues such as temporary events, mobile vendors, and retail markets. A hallmark of these atypical venues is a lack of space and infrastructure, which can lead to cross-contamination due to inadequate equipment or close quarters (68, 88, 94, 98). Foodborne illness outbreaks have been connected to these environments, and cross-contamination could be a factor in such outbreaks (88, 94, 98).

The purpose of this review was to identify and examine atypically cross-contaminated surfaces such as menus, monetary items, spice containers, cloth items, and screens and other technology in the retail food service environment and atypical food service settings such as mobile vendors, temporary events, and markets with RTE foods, where cross-contamination poses a significant concern. This review provides information on surfaces that are likely to be cross-contaminated in a retail setting but have not been thoroughly studied and possible routes of cross-contamination to these surfaces and reveals how cross-contamination occurs in unusual food service venues and on surfaces that may be more likely to be cross-contaminated, serving as a potential cause of foodborne illness.

Searches were conducted in Web of Science, National Center for Biotechnology Information, and Google Scholar databases with a variety of search terms combined with the term “cross-contamination” (Table 1). After scanning the abstracts, articles were eliminated from inclusion when the research design was flawed (i.e., the methods used were not appropriate for addressing the research goals) and when closer inspection revealed that the study did not provide information on atypical cross-contamination. This elimination process was repeated after reading the complete article. The 98 articles included in this review covered a variety of topics (e.g., microbial persistence on a diverse range of surfaces, food handling and food safety behaviors of food workers and consumers, and microbial transfer between surfaces) and methodologies (e.g., observational, survey-based, behavioral, and traditional benchtop microbial studies and studies that included surrogates and consumers) (22, 26, 43, 50, 83). Topics not included in this review were cleaning, sanitizing, and hand washing practices that were adopted by retail food service establishments during the COVID-19 pandemic and that may result in a decreased risk of cross-contamination. This exclusion was justified by the lack of data on the subject and the fact that COVID-19 is not currently thought to be transmitted through food.

TABLE 1

Search terms used in conjunction with “cross-contamination”

Search terms used in conjunction with “cross-contamination”
Search terms used in conjunction with “cross-contamination”

Cross-contamination has been previously studied on typical food contact surfaces, on the hands of consumers and employees, at conventional restaurants, and in homes (15, 83, 84), but limited information exists on cross-contamination of unusual or atypical surfaces or at atypical venues in the retail environment. Because of this research gap, many of the articles included in this review cover a variety of topics. Many cross-contamination studies were limited by the use of surrogates or tracers and of nonpathogenic microbes used in place of pathogenic microbes for safety reasons, especially when consumers are involved or other safety concerns may be present. Many of the applied studies in this review included surrogates or tracers for these reasons, even when consumers were not always actively involved in the study (25, 83, 89). However, results obtained from microbial surrogates and tracers can still be extremely useful when studying cross-contamination, and such studies have therefore been included in this review.

Atypical cross-contamination surfaces: menus

Although contamination of many nonfood contact surfaces has not been explored, menus have been targeted in previous studies. In these few studies, agreement has been reached that the material of the menu impacts the survival and persistence of foodborne microbes. Laminated menus support longer microbial contamination than do paper menus because of the absorbent properties of paper (35, 81, 88); on laminated menus survival was as long as 24 h for nonpathogenic E. coli and 72 h for Salmonella Typhimurium (81). Less available water means that gram-negative microbes in general would not be able to survive for as long on paper menu surfaces than on laminated surfaces, which do not absorb water (35). However, Salmonella can survive in low moisture environments (15), which could contribute to their persistence on a variety of low moisture surfaces, including menus. E. coli can survive for up to 25 days on plastic surfaces (66) but only 7 days on paper surfaces (41), supporting similar findings on menus (35, 81). Adenovirus can survive for 35 days on the plastic used to laminate menus (49). Studies on several foodborne viruses, such as hepatitis A virus, human rotavirus, and norovirus, have revealed that these viruses can survive for up to 60 days on both paper and plastic surfaces (28, 49). Because these microbes can survive on these surfaces, cross-contamination could occur between menus and hands. The longer the microbes are able to persist, the more likely it is that multiple consumers or employees could have their hands cross-contaminated and that more opportunities for cross-contamination in general could be created.

Because menus are frequently handled by both employees and patrons of food service establishments, multiple opportunities exist for menus to be contaminated and serve as vectors for cross-contamination of either food or hands. Sirsat et al. (81) found that Salmonella and E. coli K-12 could effectively be transferred from inoculated menus, both laminated and nonlaminated, to fingerpads for up to 48 h, and up to 6 log CFU/cm2 was transferred from menus to fingertips after 6 h. Up to 4.5 to 5.5 log CFU/cm2 was transferred from fingerpads to menus, suggesting that cross-contamination can occur from hands to menus and from menus to hands (Table 2). Norovirus also was effectively transferred from hands to other hands or surfaces (5, 28, 91). In one study, a norovirus-inoculated fingerpad contaminated up to seven melamine surfaces touched sequentially, and the norovirus was easily transferred to uninoculated hands (5). Although hand washing for ≥15 s significantly reduces the amount of bacteria on hands and the amount that can be transferred (11, 44), best hygiene practices, such as proper hand washing, are not used regularly by food service employees or consumers (Table 3) (4, 20, 27, 83). Failure to comply with proper hand washing techniques and a lack of implementation of cleaning and sanitizing procedures can promote cross-contamination from hands to menus and vice versa.

TABLE 2

Studies that include atypical cross-contaminated surfaces

Studies that include atypical cross-contaminated surfaces
Studies that include atypical cross-contaminated surfaces
TABLE 3

Studies that include atypical food service venues

Studies that include atypical food service venues
Studies that include atypical food service venues

Menus are not often included in sampling protocols or cleaning regimens and are inspected only by sight or touch in some establishments (81). Combined with the low number of studies including menus, the level of contamination on and cross-contamination to and from menus has resulted in underestimation of the risk of cross-contamination associated with restaurant menus. Up to 87% of menus in monitoring studies harbored bacteria, including E. coli (which was not further serotyped) and S. aureus. The presence of both of these pathogens indicates poor hygienic practices (8, 19, 31, 81), suggesting that menus should be either cleaned and sanitized or periodically discarded as part of a restaurant's hygiene protocol. Laminated menus could easily be added to a restaurant's cleaning regimen and could be sanitized after each customer; paper menus cannot be cleaned as easily but do have a lower moisture content, which suggests that they could be used multiple times before being discarded. However, more studies are needed on the cleaning and sanitizing of laminated menus and on the harborage and persistence of pathogenic foodborne microbes on paper menus to determine the most effective practices for limiting cross-contamination.

Atypical cross-contamination surfaces: monetary items

In several studies, currency (both paper notes and metal coins) harbored bacteria, including foodborne pathogens (45, 48, 53, 64, 88). E. coli O157:H7 survived for 7 to 11 days from an inoculum of 102 to 103 CFU per coin, and Salmonella survived for 1 to 9 days on pennies, nickels, dimes, and quarters at 25°C from an inoculum of 10 to 102 CFU per coin (45). Although the levels of E. coli O157:H7 and Salmonella decreased over time, both bacteria have low infectious doses (i.e., <10 to <100 CFU) (24), so these microbes could contribute to foodborne illness even after being transferred from a coin to a hand or other surface, especially when transferred to a surface with more favorable growth conditions. Norovirus can survive on stainless steel for up to 7 days at room temperature (28). Viruses can survive on some metals, but copper, which is a component of several types of currency, has a viricidal effect on some foodborne viruses (91), although the extent of the effect is unclear. Khin et al. (48) isolated enterotoxigenic E. coli and Salmonella from currency notes in butcher shops and Vibrio spp. from currency obtained in fishmonger shops, indicating that currency can be cross-contaminated with microbes from both the food and the environment (Table 2) and that the reverse, contamination from currency to food, is also plausible.

Food service providers are aware of the risk of cross-contamination of food from currency, and certified food protection manager programs (65) and the U.S. Food and Drug Administration's Model Food Code highlight the need to wash hands or change gloves after handling money (84). The relative levels of bacteria and their persistence on currency have been reported (Table 2), but no direct research has been conducted on the potential for cross-contamination from currency to food. What has been documented is a lack of consistency among food handlers in compliance with good hygiene practices when handling money (37, 84, 88). Food workers in typical food service environments in general use best hand washing practices <50% of the time, providing opportunities for cross-contamination from currency to hands (16, 37, 84). In mobile or temporary food service operations, 31 to 70.3% of operators were noncompliant with hygiene standards, including hand washing and glove changing when handling money (Table 3) (22, 42, 54, 68). Not all cashiers are food handlers, and not all food handlers also handle currency, especially in more traditional food service settings, and this separation of duties should be considered when evaluating the potential for cross-contamination from currency to hands. These low rates of compliance with good hygiene practices when handling food and currency can create a situation in which cross-contamination can occur. Sanitization of currency itself is not a viable option, but cleaning and sanitizing the cash box and promoting hygienic practices in general are viable options and should be considered to reduce the risk of cross-contamination associated with currency, although the frequency of cleaning and sanitizing may vary depending on several factors such as the type of establishment and food served. Some businesses have transitioned to a cashless model, only accepting credit cards or other electronic forms of payment. Although we did not specifically address the use of credit cards and electronic forms of payment in this review, similar cleaning and sanitizing could be used with cards and electronic readers to process such payments.

Atypical cross-contamination surfaces: spice and condiment containers

Almost every food service establishment has spice containers or condiment bottles at the back or front of the house. With such a ubiquitous presence and frequency of use, it seems strange that very little work has been done on spice containers in the context of cross-contamination (25, 83, 89). When they have been studied with either a Salmonella surrogate or tracer microbe in consumer kitchens, spice containers were cross-contaminated >50% of the time (25, 83, 89). Such a high rate of cross-contamination indicates that spice containers could be a harborage site for pathogenic microbes. However, there is less agreement on the level of contamination present on spice containers following cross-contamination (Table 2). Sneed et al. (83) reported an average Lactobacillus casei (a nonpathogenic tracer bacterium) level of 0.59 log CFU/cm2, and the U.S. Department of Agriculture (89) reported much higher average levels of MS2 (a tracer bacteriophage), with potential cross-contamination of up to 9.1 log genome equivalent units. The use of different tracers (bacterial versus viral) could help explain some of the discrepancy in these results, but more work is needed to elucidate the levels of contamination present on spice containers after cross-contamination. Both of the tracer microbes studied, the gram-positive L. casei and the bacteriophage MS2, are hardier than the gram-negative pathogens usually associated with raw poultry and hamburger: Salmonella enterica and various pathogenic strains E. coli including E. coli O157:H7 and the “big six” E. coli (15, 83, 89). Other than these three studies, to our knowledge no studies have been conducted on spice and condiment containers as potential harborage sites for foodborne viruses. However, foodborne viruses can survive on a variety of materials, including those used for spice and condiment containers such as plastic, stainless steel, and glass, indicating that these sites could harbor foodborne viruses transferred by hands (5, 28, 49, 91).

Spice containers are used very differently in food service compared with a home kitchen. Often the number of spice and condiment containers available at the front of the house depends on the product being sold. Products prepared at temporary events or on the street (e.g., hot dogs) can have a multitude of condiments available to the consumer, making hand facilitated cross-contamination of these containers more likely to occur due to their frequency of use (42, 67, 96). Almost all restaurants and food service establishments have some condiments on tables at the front of the house (65), which leaves them vulnerable to cross-contamination from foods or human handling. Spice and condiment containers are handled frequently by multiple people before and after handling food items, which can be a risk factor for cross-contamination (42, 65, 67). The frequency of touch and the evidence that spice containers in the home can be cross-contaminated (25, 83) suggest that these containers are vulnerable to cross-contamination in retail environments and may not be fully recognized as a potential hazard. A potential solution could be to add periodic cleaning and sanitizing of spice and condiment containers to the hygiene practices of food service establishments. However, the most appropriate cleaning agents and techniques would likely differ depending on the container material and how those materials hold up to repeated cleaning and sanitizing.

Atypical cross-contamination surfaces: cloth items

Clothing can become contaminated with bacteria and can transfer that bacteria to food products (Table 2) (87, 88). Several foodborne viruses have been found to persist on cloth for several hours; hepatitis A virus and norovirus survived on cloth for up to 90 days (1, 88). The risk of these pathogens being transferred to food and causing illness has been demonstrated in hospitals, food service establishments, and sporting events (6, 88). The transfer of microbes from skin to cloth and vice versa has been studied (57). The contamination of cloth is one reason that uniforms, coveralls, and aprons are important for ensuring food safety (15, 65). However, uniforms and aprons can also be vulnerable to contamination, especially when working with raw foods (Table 2). Although guidance on keeping cloth items clean and sanitized is available (65), Lues and Van Tonder (56) documented that 32% of food handlers' aprons had higher fecal coliform counts than considered advisable. Cleaning and sanitizing of cloth items are important food safety steps, even when separate uniforms and aprons are used.

Dish cloths and towels are used frequently as part of the cleaning and sanitizing procedures for food service operations (13, 36). These towels are used for numerous purposes, such as wiping tables and surfaces clean of water and food or drying employees' hands, and are used multiple times each day without cleaning between uses (13, 21, 36, 87). This heavy use can be concerning when a towel is employed to wipe up meat juice and then used for other purposes, potentially transferring pathogenic microbes picked up by the towel from meat juice to other kitchen surfaces, employees' hands, and food (13, 15, 36, 77). Salmonella and other foodborne microbes can form biofilms (21), and the ridges and nooks in a towel could create a harborage site. Educating employees on when to stop using a cloth towel or eliminating cloth towels in favor of disposable paper towels could help decrease the risk of cross-contaminating surfaces via cloth cleaning towels. Towels used in a home kitchen have been posited as a cause of cross-contamination in several studies (Table 2) (20, 21, 25, 73, 83). de Wit et al. (25) found that up to 74% of dishcloths were cross-contaminated with a Salmonella surrogate (E. coli K-12), and Sneed et al. (83) found that dish towels were a possible source of cross-contamination, with the towels harboring L. casei at up to 4.43 log CFU per towel. However, the L. casei could have come from another environmental source and not the inoculated meat and poultry used in the study. Outside of these kitchen studies, dish towels evaluated during outbreaks have been found to be contaminated (Table 2). For example, contaminated dish towels may have been responsible for an outbreak of Salmonella Enteritidis infection in a restaurant in the United Kingdom (77). The limited sampling of these surfaces contributes to the underestimation of microbial contamination of cloths.

Atypical cross-contamination surfaces: screens and technology

Smart phones, computer tablets, ATMs, and other electronic devices permeate the entire food safety system. Large and small food service providers have integrated technology into their daily operations. Restaurants are providing tablets for ordering and playing games at tables, and small vendors such as food trucks and farmers' market sellers are using tablets or swipe card accessories on mobile phones to provide consumers with more payment options and sometimes have ATMs on site (31, 33). Despite the increased presence of technology in the food service and retail sector, most information on contamination of technology related to food is performed in the home or in hospitals and other health care settings (2, 10, 12, 52, 92). Mobile devices and other technologies can harbor potentially harmful pathogenic bacteria such as S. aureus and E. coli (Table 2) (2, 10, 12, 30). Foodborne viruses also can persist on screens and other devices. Feline calicivirus, a surrogate for human norovirus, can survive for up 56 days on glass, which is often a component of screens and phones (91).

Bacterial species on participants' fingertips were also present on their phones (63). Food service employees and consumers frequently interact with technology provided by the venue and with their personal mobile devices (22, 31). These interactions can allow employees and consumers to transfer bacteria from their fingertips to the technology in the venue and cause cross-contamination from screens to food. Czarniecka-Skubina et al. (22) found that >30% of outdoor food vendors in Paris had personal mobile devices in their preparation areas, which could lead to cross-contamination of other food in the establishment (Tables 2 and 3).

Foodborne pathogens can persist on a variety surfaces, including glass, metal, and plastic (58, 78, 80). Listeria monocytogenes can survive for a least 24 h after drying and can form biofilms on glass, plastic, stainless steel, and rubber surfaces (78). Because covers for mobile devices are often made of plastic and the devices themselves can have metal and glass, L. monocytogenes and Salmonella could form biofilms (80, 82) in the niches and gaps in these devices. However, to our knowledge L. monocytogenes has not been linked to illness in a patient after handling a mobile device. The infectious dose of L. monocytogenes differs for healthy versus immunocompromised individuals, which also factors into the risk of infection from a mobile device or other technology. However, proper cleaning and sanitizing of these surfaces on at least a daily basis decreases microbial populations and reduces the likelihood of biofilm formation (51, 80). Proper cleaning of phones and other electronic devices could help decrease the likelihood of biofilm formation and the potential for cross-contamination. However, these devices are not always included in the cleaning and sanitizing procedure in food service environments (33, 65). Inclusion of on site technology such as ATMs and tablets to a restaurant's cleaning and sanitizing protocol may help mitigate cross-contamination from these sites to food and prevent biofilm formation.

All surfaces covered in this review are not routinely considered to be at risk for cross-contamination. However, they are frequently handled by employees or customers, making them vulnerable to hand-facilitated cross-contamination (31, 64, 81, 83, 88). Many of these surfaces, such as screens and menus, support the persistence or transfer of foodborne microbes or surrogates and tracers, indicating that these surfaces could become harborage sites of pathogenic microbes (Table 2) (2, 35). The impact of these surfaces on cross-contamination has not been well characterized because most studies have prioritized food contact surfaces, thus underestimating the role of these atypical surfaces. When spice containers were assessed during meal preparation studies, >50% of containers were cross-contaminated (25, 83), and menus transferred E. coli K-12 at up to 6 log CFU/cm2 to fingertips (81). These results indicate that these areas could substantially contribute to cross-contamination, but studies that have focused on these areas have mostly taken place in health care or consumer kitchen settings and not in retail or food service settings (2, 10, 25, 83). These technology surfaces are not routinely incorporated into cleaning and sanitizing protocols, which means they may facilitate cross-contamination to human hands and through human hands to food.

Atypical cross-contamination venues: mobile vendors

With more consumers on the go and focused on convenience, mobile food vendors are becoming more common globally. Mobile food vendors, such as street carts, stands, and food trucks, have different food safety challenges because their mobility makes their fundamental design different from that of brick-and-mortar businesses (67, 68, 90). These challenges are associated with limited space, limited access to potable water, fewer pieces of equipment, and the need to transport their business when necessary (Table 3). Traditional cross-contamination via a food contact surface or a worker's hands can occur in these situations because of the small working spaces and the tendency to reuse items (22, 54, 67). Atypical cross-contamination can also occur due to environmental exposure, a lack of storage space, and poor hygiene practices (9, 42, 67). However, the specific concerns differ by vendor type.

Street foods are often served out of carts or stands, which are usually small and wheeled with umbrellas or awnings, and sometimes a portion of the food preparation occurs in a secondary space. Many of these establishments do not have an ideal layout for food safety and can lack some equipment found in conventional food service establishments (3, 22, 67). Many stalls and carts will use the same cutlery and cutting boards to chop raw and RTE foods (Table 3) (3, 22, 54, 67), which is a proven risk factor for cross-contamination (52, 60). In developing countries in particular, the same cutlery and plates can be used by many customers without being properly washed (3, 67). In Shijiazhuang, People's Republic of China, 90% of street vendors prepared or touched food with bare hands while they were actively serving customers (54). Both of these conventional cross-contamination problems could be solved with improved education, regulation, and access to clean water for hand and tool washing (4, 11, 44). However, because of the mobile nature and lack of facilities associated with street food establishments, water for cleaning is not easily accessible (Table 3) (3, 67). The issue of water access could also explain why street food vendors in various studies did not wash their hands frequently (54, 68).

Atypical cross-contamination can also be an issue with street food. In one street food study, 72% of vendors did not wash their hands between handling food and handling money (22), a finding consistent with those of other studies (54, 68). Because money is a potential vector for foodborne pathogens, this practice could result in foodborne illness through cross-contamination (Table 2) (45, 88). Vendors do not always wear aprons or coveralls, which can lead to cross-contamination from cloth to hands or cloth to food (54). The minimal protection offered by the stalls and carts exposes much of the food to the environment, including dirt, dust, animals, and other unhygienic factors (Table 3) (3, 9, 67, 88). Little information is available about cleaning and sanitizing practices used for the outer cart or stall in street food operations; without cleaning and sanitizing, umbrellas, awnings, or the cart itself could become contaminated. Salmonella, Listeria, E. coli, and norovirus can survive on both cloth and metal for up to several days (1, 23, 87, 88). Even with proper sanitation, the exposure of the food to the environment could allow contact with dirt or insects (3, 9, 67, 88). Both fruit flies and common house flies can be vectors for foodborne pathogens and can transfer these bacteria to food and food contact surfaces (Table 3) (9, 88). Street food vendors could address some of these problems by using more disposable items, using carts and stalls with a more hygienic design to minimize potential cross-contamination and contact with the environment, storing raw items below cooked ones, and providing covers or splash guards around open bins or food products. However, carts with a hygienic design may not be feasible in developing countries or in low-income areas, and more accessible and sustainable alternatives to prevent cross-contamination are needed.

Unlike street food vendors, food trucks are mostly enclosed, have a small restaurant-style kitchen, and contain more appliances and tools (42, 68, 90). These additional features make food trucks less vulnerable to some of the risk factors associated with street foods, such as a lack of water for washing dishes and hands. However, food trucks still have a small workspace, and the potential for employee errors such as improper use of utensils and tools, improper food handling, inadequate hygienic practices, unhygienic money handling practices, and incorrect uniform or apron use can still cause cross-contamination, similar to that for street foods (Table 3) (22, 42, 54, 68, 90). Flies around or inside a food truck can also cause problems (9, 68).

Because most food sold from food trucks is prepared on site or possibly at a commissary location, the cleanliness of the clothes and hands of food handlers is the most important way of avoiding cross-contamination (22, 42, 54, 67, 68). In several studies, aprons or uniforms were not worn or were unclean, allowing microbes on the cloth to contact the food and facilitating cross-contamination (Tables 2 and 3) (22, 54, 68). Guidance on proper apron and uniform usage is routinely provided to food service establishments, which makes employee education on apron and uniform practices a primary avenue to address this particular cross-contamination risk. However, the most effective way to change food safety behaviors are controversial (16, 89, 96) and are not covered in this review. Many food trucks provide a variety of spice and condiment containers for consumers, and contamination of these containers could cause cross-contamination of the food being served (Table 3). Isoni Auad et al. (42) found that food trucks that provided more sauces or condiments had a higher percentage of coliform and S. aureus contamination than did food trucks with fewer containers available. Condiment containers could be the source of additional S. aureus contamination due to increased handling of items in the food truck by employees and patrons. More frequent hand washing by both employees and consumers and the inclusion of these containers into a cleaning and sanitizing procedure would likely reduce cross-contamination associated with spice and condiment containers.

Atypical cross-contamination venues: temporary events

Like mobile vendors, temporary events have also been linked to foodborne illness cases and several outbreaks (18, 94). Temporary events such as festivals, community picnics, fairs, and tailgate parties (Table 1) often bring a community together and sometimes involve volunteers or people untrained in food safety, and food for the event is often prepared in temporary structures or spaces (18, 34, 59, 85, 94, 96, 97). These factors can promote an unsafe food handling environment that can result in the cross-contamination of foods and eventually foodborne illnesses (Table 3).

Because food is often prepared at temporary events by people who are untrained in food safety practices, unsafe food handling and cleaning and sanitizing practices are relatively common (59, 79, 96, 97). Shumaker et al. (79) found that 91.5% of temporary food service establishments were out of compliance with one risk factor for foodborne illness and 14.3% were identified as having practices that could lead to cross-contamination (Table 3). Low rates of hand washing compliance, when reported, were found across most studies (59, 79, 97). However, because some of these events (e.g., tailgate parties and barbeques) are consumer driven, hand washing information is often not available. Education campaigns can be an important component for ensuring that food is prepared safely at temporary events (79, 85, 86, 96). In one such campaign in which researchers provided educational materials and a meat thermometer to individuals cooking at tailgate parties, 56% of participants in the study used the food thermometer (96), indicating that education campaigns can change behavior in these settings. In a more general sense, the spaces where these temporary events occur could also provide cleaning and sanitizing stations or supplies to help increase compliance with proper hygiene procedures.

Even when an event occurs every year, such as a state fair, the temporary nature of the structures in which food is prepared can create cross-contamination risks. Limited space and the temporary nature of the venue have been specifically cited as part of the problem with temporary food service events (34, 59, 85). Because of the limited space, atypical surfaces such as spice containers may be in closer proximity to raw food products or contaminated surfaces and thus become cross-contaminated (Table 2). Cleaning and sanitizing practices were also associated with errors, such as sanitizers prepared incorrectly or poor cleaning techniques (i.e., sanitizing without cleaning, sanitizing before cleaning, and cleaning without sanitizing) (34, 59, 79, 97). Hygiene is especially important when livestock are part of the event, as at county and state fairs, due to the presence of zoonotic pathogens associated with these animals (18). State and county fairs have been implicated in previous foodborne illness outbreaks, especially those caused by pathogenic E. coli infections, and foodborne pathogens have been isolated from samples collected at county fairs (7, 18, 94), indicating that appropriate hand washing facilities and proper sanitation of both the animal areas and the food vendors are vital for preventing illness in these situations.

Atypical cross-contamination venues: markets with RTE goods

Other venues where cross-contamination can occur and that are often overlooked are markets with RTE goods. Even when all products sold at these markets are not considered RTE, raw products can be stored near RTE foods or foods often consumed raw in a market or within a consumer's bag or cart as occurs at farmers' markets and grocery stores (39, 40, 93, 98). The number of farmers' markets increased by >300% from 2000 to 2016 to >8,000 in the United States (98). Grocery stores are increasing production of a larger number of RTE meals and foods to satisfy customer demand for convenient ready-made meals, and 20% of customers leave the store with at least one RTE food service-style meal (74).

Farmers' markets contain a variety of goods, both raw and RTE, that regularly change with the seasons (69, 98). Many such goods sold at farmers; markets, such as leafy greens, vegetables, and fruits, have been consistently found to be contaminated with pathogens such as L. monocytogenes, E. coli, and Salmonella (69, 98). These goods must be stored and displayed in containers or on tables provided by the farmer or retailer. Because the products are in direct contact with the containers or tables, they can become contaminated by pathogens when only one food product is contaminated (39, 71, 98). Cleaning and sanitizing practices vary between markets, and in two studies 82.2% of farmers' markets did not use sanitizers on food contact surfaces or did not use other hygienic practices (39, 98). Guidance documents are available to farmers' markets and should be reviewed by the organizers and vendors for cleaning and sanitizing recommendations to help reduce the risk of cross-contamination.

Vendors are frequently observed handling food with bare hands and performing multiple tasks without washing hands (Table 3) (39, 98). Compliance with best hand washing practices in general are low; in one review hand washing compliance was only 4% across multiple studies (98). In other studies, compliance levels differed, with some as low as 0% for other hand washing factors (e.g., presence of hand sanitizer and hand washing stations close to vendors) (39, 71, 98). Handling food after handling money without proper hand washing could be a risk factor for cross-contamination (Table 2) (48, 53, 64). Farmers' markets are usually outdoors or in a semicovered location, which exposes the products and surfaces to the environment (Table 3). Some farmers' markets allow animals and leave food in the open, exposing them to dust and insects, which could cause cross-contamination (9, 39, 62, 98). Some farmers' markets do provide hand washing stations (39, 62, 71, 98), but the continued used of improper hand washing techniques and low compliance indicate that more can be done with the location of these stations or hand washing education for vendors in general. To protect RTE food from environmental contamination, food shields and other protective cases or wrappings also could be used by vendors.

Although grocery stores are the main venues where consumers purchase food, very little is known about cross-contamination in this setting. Thus, we designated grocery stores as an atypical venue for cross-contamination. Grocery stores sell a variety of products with differing risks of cross-contamination. Consumers usually place multiple products into a single shopping cart, increasing the risk of cross-contamination of other foods, the cart, or the consumer's hands (17, 27). The outside of retail poultry packaging can be contaminated with Salmonella and Campylobacter spp., and packaging can leak, creating the potential for cross-contamination (17, 27, 40). Donelan et al. (26) found that produce was the food most often directly touched by raw poultry in a shopping cart, but dry goods and refrigerated goods also were frequently touched. Because produce is often eaten raw or after minimal processing, cross-contamination of produce could result in more serious consequences, such as foodborne illness, than cross-contamination of products such as rice that will be cooked before consumption (93). The shopping cart is also at risk for cross-contamination because raw products and contaminated hands come into direct contact with the cart (Table 3) (27). In one study, carts were touched directly after handling poultry 85% of the time (30), which may result in cross-contamination from the poultry packaging or customers' hands.

The checkout area has surfaces that could become cross-contaminated, including the conveyor belt at the checkout counter and the bags used to transport groceries (17, 55). Pathogens in leaky packages and on the packaging exterior could transfer to grocery bags, especially reusable bags (Table 3) (17, 40). Reusable grocery bags can support the growth of bacteria from meat fluids when held in a car trunk for 2 h (93); thus, when these bags are used again for other foods, cross-contamination may occur. Cross-contamination from packaging can also occur on the conveyor belt or touch screens at the checkout area, and screens have been identified as potential harborage sites for microbes (31, 78).

Mobile vendors, temporary events, and markets with RTE foods all have different features but do have some commonalities that can increase the risk of cross-contamination of foods and surfaces. All of these atypical venues have constrained space and/or limited equipment (22, 42, 79). These restrictions mean that foods and surfaces are more likely to be contaminated with pathogenic microbes from raw food or the environment. In many of these venues, such as street food carts and some farmers' markets, direct access to hand washing facilities is limited (Table 3) (22, 39, 67, 98). Without this access, microbes can be transferred from contaminated hands to RTE or minimally processed foods, money, technology, and spice and condiment containers (18, 25, 31, 45, 48). Food trucks and grocery stores, which usually provide hand washing or hand sanitizing materials, also must deal with cross-contaminated surfaces because of low hand washing compliance and consumer handling of raw products or lack of cleaning of highly touched surfaces, such as spice containers (Table 3) (17, 26, 42, 68). This issue is especially concerning for grocery stores where contaminated grocery carts or checkout screens expose more people to highly touched possibly contaminated surfaces (17, 26). Unclear or variable cleaning and sanitizing practices add to the issue of cross-contamination by potentially allowing microbes to persist on a surface, especially surfaces that are not often part of a cleaning protocol. More uniform and widespread use of proper cleaning and sanitizing procedures would help mitigate the risk of cross-contamination of human hands, surfaces, and foods.

This review of atypical surfaces involved in and venues vulnerable to cross-contamination is not comprehensive because almost any surface or venue could be implicated in an atypical instance of cross-contamination. Instead, this review highlights the most likely surfaces and venues where cross-contamination has been underestimated or underreported in the retail environment, with some support in the literature. Because of the general lack of information on these topics, a variety of studies were included in this review but only after their methodology and design were assessed by the authors and determined to appropriately address the research question of each study. This variability among the few studies highlights the need for further research on these surfaces and venues to validate or confirm previous cross-contamination findings on atypical surfaces or in atypical venues. Few articles were found on food trucks and stalls in the United States, farmers' markets or grocery stores outside the United States, and the general role of uncommon surfaces in cross-contamination and temporary events. These data gaps mean that the conclusions presented here may not be universally applicable, based on the current information and publications available. The effect of changes to hygiene protocols for combating cross-contamination that have been instituted in response to the COVID-19 pandemic were not explored here. More frequent cleaning and sanitization of surfaces and increases in hand washing adopted during the COVID-19 pandemic could help decrease the likelihood of cross-contamination at retail food establishments in general. However, few data on this topic are available, and whether these practices will continue after the COVID-19 restrictions and awareness cease is unclear.

Cross-contamination is an issue of concern in retail food service establishments and typically occurs between raw foods and hands or RTE foods. However, cross-contamination research has mainly focused on food contact surfaces and has neglected other surfaces that could become contaminated and in turn could cross-contaminate foods (24, 46, 52, 88). This review included several atypical surfaces and venues that are not often discussed in connection with cross-contamination and whose impact on cross-contamination may be underestimated (Tables 2 and 3). By targeting these uncommon cross-contamination circumstances, we identified surfaces and venues that are often overlooked when assessing cross-contamination risk and the contribution of these surfaces and venues to cross-contamination in general. Overall, the surfaces identified in this review were touched frequently, often not part of a cleaning and sanitizing protocol, and were known to harbor foodborne pathogens in a food service setting. These atypical venues all have smaller operating spaces than are available at a conventional restaurant, have generally limited access to hand washing facilities or low hand washing compliance, and possess surfaces handled by consumers that could become cross-contaminated. Because these scenarios are not often reported, several data gaps in the cross-contamination literature were identified, including but not limited to the role of menus, technology devices, and spice and condiment containers in cross-contamination and cross-contamination that occurs at temporary events, food trucks, and farmers' markets globally. More studies on these topics are needed to gain a more complete understanding of how these surfaces and venues factor into cross-contamination within food service and retail establishments, how foodborne illnesses are associated with food consumed outside the home, and how to properly clean and sanitize surfaces to reduce the risk of cross-contamination and of developing a foodborne illness.

1.
Abad,
F. X.,
Pinto
R. M.,
and
Bosch
A.
1995
.
Survival of enteric viruses on environmental fomites
.
Appl. Environ. Microbiol
.
60
:
3704
3710
.
2.
Akinyemi,
K.,
Atapu
A.,
Adetona
O.,
and
Coker
A.
2009
.
The potential role of mobile phones in the spread of bacterial infections
.
J. Infect. Dev. Ctries
.
3
:
628
632
.
3.
Alimi,
B. A.
2016
.
Risk factors in street food practices in developing countries: a review
.
Food Sci. Hum. Wellness
5
:
141
148
.
4.
Anderson,
J. B.,
Shuster
T. A.,
Hansen
K. E.,
Levy
A. S.,
and
Volk
A.
2004
.
A camera's view of consumer food-handling behaviors
.
J. Am. Diet. Assoc
.
104
:
186
191
.
5.
Barker,
J.,
Vipond
I. B.,
and
Bloomfield
S. F.
2004
.
Effects of cleaning and disinfection in reducing the spread of norovirus contamination via environmental surfaces
.
J. Hosp. Infect
.
58
:
42
49
.
6.
Becker,
K. M.,
Moe
C. L.,
Southwick
K. L.,
and
MacCormack
J. N.
2000
.
Transmission of Norwalk virus during football game
.
N. Engl. J. Med
.
343
:
1223
1227
.
7.
Bender,
J. B.,
Shulman
S. A.,
and
Animals in Public Contact Subcommittee of the National Association of State Public Health Veterinarians
.
2004
.
Reports of zoonotic disease outbreaks associated with animal exhibits and availability of recommendations for preventing zoonotic disease transmission from animals to people in such settings
.
J. Am. Vet. Med. Assoc
.
224
:
1105
1109
.
8.
Bilici,
S.,
Mortas
H.,
Köse
S.,
Varli
S. N.,
and
Ayhan
B.
2017
.
Are restaurant menus vectors of bacterial cross-contamination? A pilot study in Turkey
.
Br. Food J
.
119
:
401
410
.
9.
Black,
E. P.,
Hinrichs
G. J.,
Barcay
S. J.,
and
Gardner
D. B.
2018
.
Fruit flies as potential vectors of foodborne illness
.
J. Food Prot
.
81
:
509
514
.
10.
Borer,
A.,
Gilad
J.,
Smolyakov
R.,
Eskira
S.,
Peled
N.,
Porat
N.,
Hyam
E.,
Trefler
R.,
Riesenberg
K.,
and
Schlaeffer
F.
2005
.
Cell phones and Acinetobacter transmission
.
Emerg. Infect. Dis
.
11
:
1160
1161
.
11.
Boyce,
J. M.,
and
Pittet
D.
2002
.
Guideline for hand hygiene in health-care settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force
.
Am. J. Infect. Control
30
:
S1
S46
.
12.
Braddy,
C.,
and
Blair
J.
2005
.
Colonization of personal digital assistants used in a health care setting
.
Am. J. Infect. Control
33
:
230
232
.
13.
Brown,
L. G.,
Khargonekar
S.,
Bushnell
L.,
and
Environmental Health Specialists Network Working Group.
2013
.
Frequency of inadequate chicken cross-contamination prevention and cooking practices in restaurants
.
J. Food Prot
.
76
:
2141
2145
.
14.
Byrd-Bredbenner,
C.,
Berning
J.,
Martin-Biggers
J.,
and
Quick
V.
2013
.
Food safety in home kitchens: a synthesis of the literature
.
Int. J. Environ. Res. Public Health
10
:
4060
4085
.
15.
Carrasco,
E.,
Morales-Rueda
A.,
and
García-Gimeno
R. M.
2012
.
Cross-contamination and recontamination by Salmonella in foods: a review
.
Food Res. Int
.
45
:
545
556
.
16.
Chapman,
B.,
Eversley
T.,
Fillion
K.,
MacLaurin
T.,
and
Powell
D.
2010
.
Assessment of food safety practices of food service food handlers (risk assessment data): testing a communication intervention (evaluation of tools)
.
J. Food Prot
.
73
:
1101
1107
.
17.
Chen,
F. C.,
Godwin
S.,
Chambers
D.,
Chambers
E.,
Cates
S.,
Stone
R.,
and
Donelan
A.
2018
.
Contamination by meat juice when shopping for packages of raw poultry
.
J. Food Prot
.
81
:
835
841
.
18.
Cho,
S.,
Bender
J. B.,
Diez-Gonzalez
F.,
Fossler
C. P.,
Hedberg
C. W.,
Kaneene
J. B.,
Ruegg
P. L.,
Warnick
L. D.,
and
Wells
S. J.
2006
.
Prevalence and characterization of Escherichia coli O157 isolates from Minnesota dairy farms and county fairs
.
J. Food Prot
.
69
:
252
259
.
19.
Choi,
J.,
Almanza
B.,
Nelson
D.,
Neal
J.,
and
Sirsat
S.
2014
.
A strategic cleaning assessment program: menu cleanliness at restaurants
.
J. Environ. Health
76
:
18
24
.
20.
Cogan,
T. A.,
Bloomfield
S. F.,
and
Humphrey
T. J.
1999
.
The effectiveness of hygiene procedures for prevention of cross-contamination from chicken carcases [sic] in the domestic kitchen
.
Lett. Appl. Microbiol
.
29
:
354
358
.
21.
Cogan,
T. A.,
Slader
J.,
Bloomfield
S. F.,
and
Humphrey
T. J.
2002
.
Achieving hygiene in the domestic kitchen: the effectiveness of commonly used cleaning procedures
.
J. Appl. Microbiol
.
92
:
885
892
.
22.
Czarniecka-Skubina,
E.,
Trafiałek
J.,
Wiatrowski
M.,
and
Głuchowski
A.
2018
.
An evaluation of the hygiene practices of European street food vendors and a preliminary estimation of food safety for consumers, conducted in Paris
.
J. Food Prot
.
81
:
1614
1621
.
23.
Dantas,
S. T. A.,
Rossi
B. F.,
Bonsaglia
E. C. R.,
Castilho
I. G.,
Hernandes
R. T.,
Fernandes
A.,
and
Rall
V. L. M.
2018
.
Cross-contamination and biofilm formation by Salmonella enterica serovar Enteritidis on various cutting boards
.
Foodborne Pathog. Dis
.
15
:
81
85
.
24.
Dewey-Mattia,
D.,
Manikonda
K.,
Hall
A. J.,
Wise
M. E.,
and
Crowe
S. J.
2018
.
Surveillance for foodborne disease outbreaks—United States, 2009–2015
.
Morb. Mortal. Wkly. Rep. Surveill. Summ
.
67
(10)
:
1
11
.
25.
de Wit,
J. C.,
Broekhuizen
G.,
and
Kampelmacher
E. H.
1979
.
Cross-contamination during the preparation of frozen chickens in the kitchen
.
J. Hyg. (Lond.)
83
:
27
32
.
26.
Donelan,
A. K.,
Chambers
D. H.,
Chambers
E.,
Godwin
S. L.,
and
Cates
S. C.
2016
.
Consumer poultry handling behavior in the grocery store and in-home storage
.
J. Food Prot
.
79
:
582
588
.
27.
Doring,
L.,
Duong
M.,
Goodson
L.,
Kirchner
M.,
Shelley
L.,
Goulter
R.,
Thomas
E.,
Cates
S.,
Bernstein
C.,
Jaykus
L.-A.,
and
Chapman
B.
2018
.
Investigating handwashing practices of consumers during meal preparation: an observational approach, P2-32
.
Abstr. Annu. Meet. IAFP 2018.
International Association for Food Protection
,
Des Moines, IA.
28.
D'Souza,
D. H.,
Sair
A.,
Williams
K.,
Papafragkou
E.,
Jean
J.,
Moore
C.,
and
Jaykus
L.-A.
2006
.
Persistence of caliciviruses on environmental surfaces and their transfer to food
.
Int. J. Food Microbiol
.
108
:
84
91
.
29.
Duong,
M.,
Shumaker
E. T.,
Cates
S. C.,
Shelley
L.,
Goodson
L.,
Bernstein
C.,
Lavallee
A.,
Kirchner
M.,
Goulter
R.,
Jaykus
L.-A.,
and
Chapman
B.
2020
.
An observational study of thermometer use by consumers when preparing ground turkey patties
.
J. Food Prot
.
83
:
1167
1174
.
30.
Egert,
M.,
Späth
K.,
Weik
K.,
Kunzelmann
H.,
Horn
C.,
Kohl
M.,
and
Blessing
F.
2015
.
Bacteria on smartphone touchscreens in a German university setting and evaluation of two popular cleaning methods using commercially available cleaning products
.
Folia Microbiol (Praha)
60
:
159
164
.
31.
Elsergany,
M.,
Moussa
M.,
Ahsan
A.,
Khalfan
A.,
and
Eissa
A.
2015
.
Exploratory study of bacterial contamination of different surfaces in four shopping malls in Sharjah, UAE
.
J. Environ. Occup. Sci
.
4
:
101
105
.
32.
Evans,
E. W.,
and
Redmond
E. C.
2018
.
Behavioral observation and microbiological analysis of older adult consumers' cross-contamination practices in a model domestic kitchen
.
J. Food Prot
.
81
:
569
581
.
33.
Filloon,
W.
2017
.
Why tablets on restaurant tables are here to stay
.
34.
Franklyn,
S.,
and
Badrie
N.
2015
.
Vendor hygienic practices and consumer perception of food safety during the carnival festival on the island of Tobago, West Indies
.
Int. J. Consum. Stud
.
39
:
145
154
.
35.
Gámez,
M. N.,
Lombar
M. M.,
Carcedo
I.,
Lopez
M. A.,
and
Álava
J. I.
2016
.
Pathogen persistence in restaurant menus: comparison between materials
.
J. Food Microbiol. Saf. Hyg.
1
(1)
.
36.
Gilbert,
R. J.
1969
.
Cross-contamination by cooked-meat slicing machines and cleaning cloths
.
J. Hyg. (Lond.)
6
:
249
254
.
37.
Green,
L. R.,
Selman
C. A.,
Radke
V.,
Ripley
D.,
Mack
J. C.,
Reimann
D. W.,
Stigger
T.,
Motsinger
M.,
and
Bushnell
L.
2006
.
Food worker hand washing practices: an observation study
.
J. Food Prot
.
69
:
2417
2423
.
38.
Guyard-Nicodème,
M.,
Tresse
O.,
Houard
E.,
Jugiau
F.,
Courtillon
C.,
El Manaa
K.,
Laisney
M. J.,
and
Chemaly
M.
2013
.
Characterization of Campylobacter spp. transferred from naturally contaminated chicken legs to cooked chicken slices via a cutting board
.
Int. J. Food Microbiol
.
164
:
7
14
.
39.
Harrison,
J. A.,
Gaskin
J. W.,
Harrison
M. A.,
Cannon
J. L.,
Boyer
R. R.,
and
Zehnder
G. W.
2013
.
Survey of food safety practices on small to medium-sized farms and in farmers markets
.
J. Food Prot
.
76
:
1989
1993
.
40.
Harrison,
W. A.,
Griffith
C. J.,
Tennant
D.,
and
Peters
A. C.
2001
.
Incidence of Campylobacter and Salmonella isolated from retail chicken and associated packaging in South Wales
.
Lett. Appl. Microbiol
.
33
:
450
454
.
41.
Hübner,
N.-O.,
Hübner
C.,
Kramer
A.,
and
Assadian
O.
2011
.
Survival of bacterial pathogens on paper and bacterial retrieval from paper to hands: preliminary results
.
Am. J. Nurs
.
111
:
30
34
.
42.
Isoni Auad,
L.,
Cortez Ginani
V.,
dos Santos Leandro
E.,
Stedefeldt
E.,
Habu
S.,
Yoshio Nakano
E.,
Costa Santos Nunes
A.,
and
Puppin Zandonadi
R.
2019
.
Food trucks: assessment of an evaluation instrument designed for the prevention of foodborne diseases
.
Nutrients
11
.
43.
Jensen,
D. A.,
Friedrich
L. M.,
Harris
L. J.,
Danyluk
M. D.,
and
Schaffner
D. W.
2013
.
Quantifying transfer rates of Salmonella and Escherichia coli O157:H7 between fresh-cut produce and common kitchen surfaces
.
J. Food Prot
.
76
:
1530
1538
.
44.
Jensen,
D. A.,
Macinga
D. R.,
Shumaker
D. J.,
Bellino
R.,
Arbogast
J. W.,
and
Schaffner
D. W.
2017
.
Quantifying the effects of water temperature, soap volume, lather time, and antimicrobial soap as variables in the removal of Escherichia coli ATCC 11229 from hands
.
J. Food Prot
.
80
:
1022
1031
.
45.
Jiang,
X.,
and
Doyle
M. P.
1999
.
Fate of Escherichia coli O157:H7 and Salmonella Enteritidis on currency
.
J. Food Prot
.
62
:
805
807
.
46.
Kang,
C. R.,
Bang
J. H.,
and
Cho
S.-I.
2019
.
Campylobacter jejuni foodborne infection associated with cross-contamination: outbreak in Seoul in 2017
.
J. Infect. Chemother
.
51
:
21
27
.
47.
Kendall,
P. A.,
Elsbernd
A.,
Sinclair
K.,
Schroeder
M.,
Chen
G.,
Bergmann
V.,
Hillers
V. N.,
and
Medeiros
L. C.
2004
.
Observation versus self-report: validation of a consumer food behavior questionnaire
.
J. Food Prot
.
67
:
2578
2586
.
48.
Khin,
N. O.,
Phyu
P. W.,
Aung
M. H.,
and
Aye
T.
1989
.
Contamination of currency notes with enteric bacterial pathogens
.
J. Diarrhoeal Dis. Res
.
7
(3–4)
:
92
94
.
49.
Koopmans,
M.,
and
Duizer
E.
2004
.
Foodborne viruses: an emerging problem
.
Int. J. Food Microbiol
.
90
:
23
41
.
50.
Kosa,
K. M.,
Cates
S. C.,
Bradley
S.,
Chambers
E.,
and
Godwin
S.
2015
.
Consumer-reported handling of raw poultry products at home: results from a national survey
.
J. Food Prot
.
78
:
180
186
.
51.
Krysinski,
E.,
Brown
L.,
and
Marchisello
T.
1992
.
Effect of cleaners and sanitizers on Listeria monocytogenes attached to product contact surfaces
.
J. Food Prot
.
55
:
246
251
.
52.
Lahou,
E.,
Jacxsens
L.,
Daelman
J.,
Van Landeghem
F.,
and
Uyttendaele
M.
2012
.
Microbiological performance of a food safety management system in a food service operation
.
J. Food Prot
.
75
:
706
716
.
53.
Lamichhane,
J.,
Adhikary
S.,
Gautam
P.,
Maharjan
R.,
and
Dhakal
B.
2009
.
Risk of handling paper currency in circulation chances of potential bacterial transmittance
.
Nepal J. Sci. Technol
.
10
:
161
166
.
54.
Liu,
Z.,
Zhang
G.,
and
Zhang
X.
2014
.
Urban street foods in Shijiazhuang city, China: current status, safety practices and risk mitigating strategies
.
Food Control
41
:
212
218
.
55.
Luber,
P.,
Brynestad
S.,
Topsch
D.,
Scherer
K.,
and
Bartelt
E.
2006
.
Quantification of Campylobacter species cross-contamination during handling of contaminated fresh chicken parts in kitchens
.
Appl. Environ. Microbiol
.
72
:
66
70
.
56.
Lues,
J. F. R.,
and
Van Tonder
I.
2007
.
The occurrence of indicator bacteria on hands and aprons of food handlers in the delicatessen sections of a retail group
.
Food Control
18
:
326
332
.
57.
Mackintosh,
C. A.,
and
Hoffman
P. N.
1984
.
An extended model for the transfer of micro-organisms via the hands: differences between organisms and the effect of alcohol disinfection
.
Epidemiol. Infect
.
92
:
345
355
.
58.
Mafu,
A. A.,
Plumety
C.,
Deschênes
L.,
and
Goulet
J.
2011
.
Adhesion of pathogenic bacteria to food contact surfaces: influence of pH of culture
.
Int. J. Microbiol.
2011
.
59.
Mancini,
R.,
Murray
L.,
Chapman
B. J.,
and
Powell
D. A.
2012
.
Investigating the potential benefits of on-site food safety training for Folklorama, a temporary food service event
.
J. Food Prot
.
75
:
1829
1834
.
60.
Mazengia,
E.,
Fisk
C.,
Liao
G.,
Huang
H.,
and
Meschke
J.
2015
.
Direct observational study of the risk of cross-contamination during raw poultry handling: practices in private homes
.
Food Prot. Trends
35
:
8
23
.
61.
Mazengia,
E.,
Samadpour
M.,
Hill
H. W.,
Greeson
K.,
Tenney
K.,
Liao
G.,
Huang
X.,
and
Meschke
J. S.
2014
.
Prevalence, concentrations, and antibiotic sensitivities of Salmonella serovars in poultry from retail establishments in Seattle, Washington
.
J. Food Prot
.
77
:
885
893
.
62.
McIntyre,
L.,
Karden
L.,
Shyng
S.,
and
Allen
K.
2014
.
Survey of observed vendor foodhandling practices at farmers' markets in British Columbia, Canada
.
Food Prot. Trends
34
:
397
408
.
63.
Meadow,
J. F.,
Altrichter
A. E.,
and
Green
J. L.
2014
.
Mobile phones carry the personal microbiome of their owners
.
PeerJ
2
:
e447
.
64.
Michaels,
B.
2002
.
Handling money and serving ready-to-eat food
.
Food Serv. Technol
.
2
:
1
3
.
65.
National Restaurant Association.
2017
.
ServSafe manager book, 7th ed
.
Pearson
,
London
.
66.
Neely,
A. N.
2000
.
A survey of gram-negative bacteria survival on hospital fabrics and plastics
.
J. Burn Care Rehab
.
21
:
523
527
.
67.
Nicolas,
B.,
Razack
B. A.,
Yollande
I.,
Aly
S.,
Tidiane
O. C. A.,
Philippe
N. A.,
De Souza
C.,
and
Sababénédjo
T. A.
2007
.
Street-vended foods improvement: contamination mechanisms and application of food safety objective strategy: critical review
.
Pak. J. Nutr
.
6
:
1
10
.
68.
Okumus,
B.,
Sönmez
S.,
Moore
S.,
Auvil
D. P.,
and
Parks
G. D.
2019
.
Exploring safety of food truck products in a developed country
.
Int. J. Hosp. Manag
.
81
:
150
158
.
69.
Pan,
F.,
Li
X.,
Carabez
J.,
Ragosta
G.,
Fernandez
K. L.,
Wang
E.,
Thiptara
A.,
Antaki
E.,
and
Atwill
E. R.
2015
.
Cross-sectional survey of indicator and pathogenic bacteria on vegetables sold from Asian vendors at farmers' markets in northern California
.
J. Food Prot
.
78
:
602
608
.
70.
Phang,
H. S.,
and
Bruhn
C. M.
2011
.
Burger preparation: what consumers say and do in the home
.
J. Food Prot
.
74
:
1708
1716
.
71.
Pollard,
S.,
Boyer
R.,
Chapman
B.,
di Stefano
J.,
Archibald
T.,
Ponder
M. A.,
and
Rideout
S.
2016
.
Identification of risky food safety practices at southwest Virginia farmers' markets
.
Food Prot. Trends
36
:
168
175
.
72.
Redmond,
E. C.,
and
Griffith
C. J.
2003
.
Consumer food handling in the home: a review of food safety studies
.
J. Food Prot
.
66
:
130
161
.
73.
Redmond,
E. C.,
Griffith
C. J.,
Slader
J.,
and
Humphrey
T. J.
2004
.
Microbiological and observational analysis of cross contamination risks during domestic food preparation
.
Br. Food J
.
106
:
581
597
.
74.
Robertson,
L. A.,
Boyer
R. R.,
Chapman
B. J.,
Eifert
J. D.,
and
Franz
N. K.
2013
.
Educational needs assessment and practices of grocery store food handlers through survey and observational data collection
.
Food Control
34
:
707
713
.
75.
Saksena,
M. J.,
Okrent
A. M.,
Anekwe
T. D.,
Cho
C.,
Dicken
C.,
Effland
A.,
Elitzak
H.,
Guthrie
J.,
Hamrick
K. S.,
Hyman
J.,
Jo
Y.,
Lin
B.-H.,
Mancino
L.,
McLaughlin
P. W.,
Rahkovsky
I.,
Ralston
K.,
Smith
T. A.,
Stewart
H.,
Todd
J.,
and
Tuttle
C.
2018
.
America's eating habits: food away from home. Economic information bulletin 196
.
U.S. Department of Agriculture
,
Economic Research Service,
Washington, DC
.
76.
Scallan,
E.,
Hoekstra
R. M.,
Angulo
F. J.,
Tauxe
R. V.,
Widdowson
M. A.,
Roy
S. L.,
Jones
J. L.,
and
Griffin
P. M.
2011
.
Foodborne illness acquired in the United States—major pathogens
.
Emerg. Infect. Dis
.
17
:
7
15
.
77.
Severi,
E.,
Booth
L.,
Johnson
S.,
Cleary
P.,
Rimington
M.,
Saunders
D.,
Cockcroft
P.,
and
Ihekweazu
C.
2012
.
Large outbreak of Salmonella Enteritidis PT8 in Portsmouth, UK, associated with a restaurant
.
Epidemiol. Infect
.
140
:
1748
1756
.
78.
Sheth,
I.,
Li
F.,
Hur
M.,
Laasri
A.,
DeJesus
A. J.,
Kwon
H. J.,
Macarisin
D.,
Hammack
T.,
Jinneman
K.,
and
Chen
Y.
2018
.
Comparison of three enrichment schemes for the detection of low levels of desiccation-stressed Listeria spp. from select environmental surfaces
.
Food Control
84
:
493
498
.
79.
Shumaker,
E. T.,
Doherty
I.,
Sifleet
S.,
Chapman
B.,
Pierce
A.,
Ham
M.,
and
Kowalcyk
B.
2019
.
Risk factors for foodborne illness in temporary eating establishments in North Carolina
.
Food Prot. Trends
39
:
218
224
.
80.
Sinde,
E.,
and
Carballo
J.
2000
.
Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluorethylene: the influence of free energy and the effect of commercial sanitizers
.
Food Microbiol
.
17
:
439
447
.
81.
Sirsat,
S. A.,
Choi
J.-K. K.,
Almanza
B. A.,
and
Neal
J. A.
2013
.
Persistence of Salmonella and E. coli on the surface of restaurant menus
.
J. Environ. Health
75
:
8
14
.
82.
Smoot,
M. L.,
and
Pierson
M. D.
1998
.
Effect of environmental stress on the ability of Listeria monocytogenes Scott A to attach to food contact surfaces
.
J. Food Prot
.
61
:
1293
1298
.
83.
Sneed,
J.,
Phebus
R.,
Duncan-Goldsmith
D.,
Milke
D.,
Sauer
K.,
Roberts
K. R.,
and
Johnson
D.
2015
.
Consumer food handling practices lead to cross-contamination
.
Food Prot. Trends
35
:
36
46
.
84.
Strohbehn,
C.,
Sneed
J.,
Paez
P.,
and
Meyer
J.
2008
.
Hand washing frequencies and procedures used in retail food services
.
J. Food Prot
.
71
:
1641
1650
.
85.
Summers,
D. K.,
and
Fritz
J. H.
1978
.
Environmental health surveillance at the 1976 Festival of American Folklife
.
J. Food Prot
.
41
:
660
666
.
86.
Todd,
E. C. D.,
Greig
J. D.,
Bartleson
C. A.,
and
Michaels
B. S.
2007
.
Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 2. Description of outbreaks by size, severity, and settings
.
J. Food Prot
.
70
:
1975
1993
.
87.
Todd,
E. C. D.,
Greig
J. D.,
Bartleson
C. A.,
and
Michaels
B. S.
2007
.
Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 3. Factors contributing to outbreaks and description of outbreak categories
.
J. Food Prot
.
70
:
2199
2217
.
88.
Todd,
E. C. D.,
Greig
J. D.,
Bartleson
C. A.,
and
Michaels
B. S.
2009
.
Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 6. Transmission and survival of pathogens in the food processing and preparation environment
.
J. Food Prot
.
72
:
202
219
.
89.
U.S. Department of Agriculture, Food Safety and Inspection Service.
2018
.
Food safety consumer research project: meal preparation experiment related to thermometer use
.
U.S. Department of Agriculture
,
Food Safety and Inspection Service, Washington, DC
.
90.
Vanschaik,
B.,
and
Tuttle
J. L.
2014
.
Mobile food trucks: California EHS-Net study on risk factors and inspection challenges
.
J. Environ. Health
76
:
36
38
.
91.
Vasickova,
P.,
and
Kovarcik
K.
2013
.
Natural persistence of food- and waterborne viruses
,
p.
179
204
.
In
Cook
N.
(ed.),
Viruses in food and water: risks, surveillance and control, 1st ed
.
Woodhead Publishing
,
Cambridge
.
92.
White,
S.,
Topping
A.,
Humphreys
P.,
Rout
S.,
and
Williamson
H.
2012
.
The cross-contamination potential of mobile telephones
.
J. Res. Nurs
.
17
:
582
595
.
93.
Williams,
D. L.,
Gerba
C. P.,
Maxwell
S.,
and
Sinclair
R. G.
2011
.
Assessment of the potential for cross-contamination of food products by reusable shopping bags
.
Food Prot. Trends
31
:
508
513
.
94.
Wilson,
E.
2015
.
Foodborne illness and seasonality related to mobile food sources at festivals and group gatherings in the state of Georgia
.
J. Environ. Health
77
:
8
11
.
95.
World Health Organization.
2015
.
WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007–2015
.
World Health Organization
,
Geneva
.
96.
Yavelak,
M.,
Cope
S.,
Hochstein
J.,
and
Chapman
B.
2018
.
Assessing the usage of food thermometers at American University football tailgates
.
Food Prot. Trends
38
:
8
17
.
97.
Yavelak,
M.,
Luchansky
J.,
Porto-Fett
A.,
Hochstein
J.,
Campbell
J.,
Hanson
D.,
Warren
C.,
Schollenberger
A.,
and
Chapman
B.
2019
.
Assessing consumer food safety knowledge and practice at temporary events
.
Meat Muscle Biol
.
2
:
166
167
.
98.
Young,
I.,
Thaivalappil
A.,
Reimer
D.,
and
Greig
J.
2017
.
Food safety at farmers' markets: a knowledge synthesis of published research
.
J. Food Prot
.
80
:
2033
2047
.
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