There are very few food types that have not been reported as sources of VTEC illness, including both foods of animal and plant origin. The diversity of foods reported as vehicles of infection in foodborne VTEC outbreaks is presented in Table 4. However, though the range of foods reported as vehicles of VTEC are diverse, a much smaller range of foods can be identified which account for the majority of outbreaks.
Foods Associated with VTEC illness
The following discussion is based on analysis of 733 incidents of foodborne VTEC, with an identified food vehicle, reported in Canada (n=189) and internationally (United States n=392, United Kingdom n=63, Japan n=18, France n=10, Sweden n=9, etc.) from 1982 to 2018 (Supplement 2*). A summary of the data set divided by food type is presented in Table 5. This data set is heavily weighted to North America, with 79.3% of reports from the United States or Canada. This is a result of the two largest national summaries of reports available being the Centers for Disease Control National Outbreak reporting System, which has data from 1998 onwards, and the series Foodborne and Waterborne Disease in Canada (Health and Welfare Canada), which provides reports for foodborne VTEC from 1982 to 1995. VTEC O157 were involved in 86.3% of foodborne VTEC incidents identified worldwide, and 13.7% involved other VTEC serotypes or serotype was not specified (Supplement 2*). This dominance of VTEC O157 may partially reflect bias in laboratory and investigatory methods, as foodborne incidents of non-O157 have been reported with increasing frequency since the beginning of the 21st century (Figure 3).
Internationally, foods of animal origin accounted for the largest proportion of incidents (65.5%), followed by foods of plant origin (18.7%) and complex foods (where no specific ingredient was identified) 15.8%. The ingredients most commonly identified as vehicles for VTEC were beef (40.5%), raw milk dairy products (9.8%), leafy greens (9.7%) and unspecified meats (5.9%). In Canada, the ingredients most commonly identified as vehicles for VTEC were beef (62.4%), raw milk dairy products (8.5%), unspecified meats (6.3%) and pork (4.8%). However, when considered in terms of the number of cases of foodborne illness, foods of plant origin appear considerably more significant. Internationally, 57.5% of cases of foodborne VTEC illness were associated with foods of plant origin, and in Canada 22.0%. Internationally, the greatest number of illness was associated with sprouts (40.4%), with leafy greens (8.7%), fruits and berries (5.0%), and vegetables (2.6%). In Canada, leafy greens (7.1%), vegetables (7.8%), and fruits and berries (5.5%) have contributed a disproportionate number of cases of illness per outbreak.
The association of specific foods with VTEC illness can be understood with reference to the ecology of the pathogen. E. coli, including VTEC, achieves maximal replication rates in a warm, wet, nutrient rich environment, as exemplified by the gastrointestinal tract of mammalian or avian hosts. However, VTEC can colonise a wide range of animal hosts and can persist for prolonged periods under environmental conditions inhibitory to their replication; as such, VTEC and other E. coli, are ubiquitous environmental organisms (Jang et al., 2017; Persad and LeJeune 2014). Consequently, there is a sporadic occurrence of outbreaks associated with foods, which are unlikely to be contaminated with VTEC and are not conducive to VTEC replication, such as flour (Crowe et al., 2017) or nuts (US CDC, 2011; Davidson et al., 2015).
The high association of VTEC exposure with food of animal origin, particularly beef and dairy, arises from the potential for animals to serve as hosts for VTEC (Ekong et al., 2015; Farrokh et al., 2013). This creates a significantly greater likelihood of initial contamination during harvesting (i.e., slaughter and milking). The relative association of VTEC with different meat animals, based on outbreak data, will be determined by the potential for specific host species to be colonised by VTEC strains which cause BD and HUS, as these are more likely to be reported, for example carriage of these types of strains appears more common in cattle than in swine (Ercoli et al., 2015). However, recent outbreaks of VTEC O157 in the province of Alberta linked to pork products indicate this may be an emerging area of concern (Honish et al., 2017; Alberta Health Services, 2018).
Historical reported rates of VTEC prevalence on raw meats in Canada are significantly higher than contemporary rates. A study published in 1990, reported VTEC frequency in ground beef of 36.4% (25 g n=225) and 10.6% in ground pork (25 g n=235) (Read et al., 1990). A study published a decade later reported isolation of VTEC from 30% of raw boneless beef samples (25 g n=120) (Atalla et al., 2000). While more recently, FoodNet testing of retail ground beef from 2014-2017 reported VTEC in 2% of 1,458 samples (25 g), and 6.1% (25 g n=98) in ground pork (Table 6). Similarly, over the last two decades the frequency of VTEC in raw ground beef precursor material has fallen significantly from 30% in 2000 to 1.82% (325-350 g) in 2012, a trend correlated with significant changes in hygiene and decontamination practices at Canadian beef slaughter plants (Pollari et al., 2017).
The frequency of dairy contamination with VTEC is significantly higher than beef, with a 2014 US study finding verotoxin genes in 13.1% of 100 ml samples of bulk raw cow milk (Sonnier et al., 2018). The origin of these pathogens as with other milk microbiota is the surface of the udder (Oliver et al., 2005). However, the probability of VTEC contamination at milking is offset by routine thermal processing, which prevents consumer exposure. Of 97 incidents of foodborne VTEC involving dairy products identified internationally, 72 (74%) involved dairy products specifically identified as raw milk products. In Canada, 89% of incidents involving dairy products identified raw milk products as the exposure vehicle (Table 5). From this, it can be presumed that without routine pasteurisation the association of dairy with VTEC outbreaks would be much higher.
In comparison, surveys of VTEC frequency on leafy greens indicate that it is much less likely to be contaminated with these pathogens. A US survey from 2009 to 2015 reported that the prevalence of VTEC O157 and non-O157 VTEC in 14,183 samples of leafy greens (iceberg lettuce, romaine lettuce, spinach) was 0.01% and 0.07%, respectively (Zhang et al., 2018). CFIA testing of fresh and fresh-cut ready to eat (RTE) fruits and vegetables (n=37,718) did not identify VTEC O157 in any surveys from 2013 to 2018 (Table 7). Thus, the association of VTEC with these products does not reflect a high probability of contamination, instead the popularity of these products, and practice of consuming them raw are probably the major factors making these foods a prominent vehicle of VTEC illness.
From these observations it can be concluded that foods derived from ruminants, such as beef and dairy, will continue to have a relatively high likelihood of VTEC contamination at harvest, but the likelihood of illness can be moderated by decontamination prior to consumption. Since VTEC contamination of leafy greens and, fruits and berries is dependent on relatively rare pre-harvest contamination from diverse origins, opportunities to prevent pre-harvest contamination may be limited and costly. It should be expected that, without the introduction of effective and routine decontamination treatment prior to consumption, these products will remain a significant source of VTEC illness.
Food Preparation Practices Associated with VTEC Illness
As discussed, in the previous section, foods of animal and plant origin may both become contaminated with VTEC. Foods of animal origin, particularly from cattle and other ruminants, have a higher probability of being contaminated with VTEC, as the animals may be hosts, or raised or transported with hosts. The probability of contamination of foods of plant origin is much lower, but as noted in Foods Associated with VTEC Illness outbreaks can involve a disproportionate number of illnesses.
The key risk factor related to food preparation in all food types is consumption of raw or undercooked food. In the case of foods which are typically heat treated, such as fresh meats (cooking) or dairy (pasteurisation), investigations have commonly found evidence of the consumption of undercooked, raw, or ready to eat products (Beutin and Martin, 2012; Cowden et al., 2001; Michino et al., 1999). Therefore, it is important for consumers to be aware of how their food is manufactured and the associated risks, for example raw milk cheeses and needle tenderized meats. Similarly, illnesses associated with contaminated flour were linked to consumption of uncooked dough (Morton et al., 2017). The importance of the consumption of raw or RTE products to the scale of outbreaks is illustrated by the dominance of such food vehicles in the largest foodborne VTEC outbreaks reported internationally (Table 8) and in Canada (Table 9). Therefore, it is important that food be prepared in a hygienic manner to prevent contamination and be cooked according to the recommended guidelines (Safe Cooking Temperatures).
It is commonly recommended that fresh fruits, vegetables and leafy greens, whether whole, fresh cut or prepackaged, should always be washed prior to preparation and consumption (CDC, 2018). However, although washing may remove visible soil, reducing the level of contamination, it is not a process that can ensure safety.
Levels of VTEC in Outbreak-Associated Foods
Quantification of VTEC in outbreak food vehicles is not regularly reported and what data is available is primarily for VTEC O157. A table summarising twelve reports of VTEC contamination levels in outbreak associated foods is provided (Table 10). Reported levels range from tens of CFU per g to below 1 MPN per 100 g. What is apparent from this data is that outbreaks can result from foods contaminated with VTEC at levels below 1 cell per 25 g. As 25 g is the analytical unit most commonly recommended for foods other than raw ground beef (RGB) and RGB precursor, it is clear that robust sampling plans are required to ensure detection of VTEC in foods at levels that can potentially cause outbreaks.
The following features describe the relationship between food types and outbreaks of VTEC illness:
- The range of foods implicated in outbreaks of VTEC illness are very diverse including, meats, dairy, vegetables, fruits, nuts, seafood, wheat flour etc.
- Based on the number of reports of foodborne outbreaks of VTEC illness related to specific food types, the most common sources of VTEC exposure are meat (particularly beef), dairy (particularly raw milk products) and leafy greens.
- Though less likely to be a cause of outbreaks than foods of animal origin, more cases of illness are associated with foods of plant origin.
- Consumption of raw or ready-to-eat foods increases the probability of VTEC illness.
- The levels of VTEC in outbreak associated foods are variable, with contamination levels ranging from tens of CFU per g to below 1 MPN per 100 g.