Occurrence, characterization, and potential predictors of verotoxigenic Escherichia coli, Listeria monocytogenes, and Salmonella in surface water used for produce irrigation in the Lower Mainland of British Columbia, Canada

Abstract

Produce has become a major source of foodborne illness, and may become contaminated through surface water irrigation. The objectives of this study were to (i) determine the frequency of verotoxigenic E. coli (VTEC), Listeria monocytogenes, and Salmonella in surface waters used for irrigation in the Lower Mainland of British Columbia, (ii) assess the suitability of fecal coliforms and generic E. coli as hygiene indicators, and (iii) investigate the correlations of environmental factors with pathogen occurrence. Water samples were collected semi-monthly for 18 months from seven irrigation ditches across the Serpentine and Sumas watersheds. VTEC colonies on water filters were detected using a verotoxin colony immunoblot, and the presence of virulence genes vt1 and vt2 was ascertained via multiplex PCR. Detection of L. monocytogenes and Salmonella was completed using standard, Health Canada Compendium of Analytical Methods. Fecal coliforms and generic E. coli were enumerated by 3M™ Petrifilm™ and filtration methods, and meteorological and geographic data were collected from government records. VTEC, L. monocytogenes, and Salmonella were detected in 4.93%, 10.3%, and 2.69% of 223 samples, respectively. L. monocytogenes occurrence was greatest in the Serpentine watershed (χ2; p < 0.05), and was most common during the winter and fall (Fisher exact test; p < 0.05). Site dependence of VTEC and Salmonella occurrence was observed within watersheds (Fisher’s exact test; p < 0.10). Pathogen occurrence correlated with fecal coliform counts (r = 0.448), while VTEC occurrence also correlated with precipitation over the five days before sampling (r = 0.239). The density of upstream livestock correlated with VTEC (rs = 0.812), and L. monocytogenes (rs = 0.841) detection. These data show that foodborne pathogens are present in the waters used for irrigation in the Lower Mainland of British Columbia, but their frequency may depend on spatial and temporal factors.

Complex interactions between weather, and microbial and physiochemical water quality impact the likelihood of detecting foodborne pathogens in agricultural water

“…The identification of an association between year-day and microbial water quality suggests that microbial water quality varied seasonally, which is consistent with the findings of previous studies (Carter et al, 1987; Cooley et al, 2014; Falardeau et al, 2017; Gorski et al, 2011; Horman et al, 2004; Wilkes et al, 2009). For example, Falardeau et al (Falardeau et al, 2017) reported that L. monocytogenes was more prevalent in winter than summer in agricultural watersheds in British Colombia, Canada. Similarly, Cooley et al (Cooley et al, 2014) found that the likelihood of isolating L. monocytogenes from California surface water samples was significantly higher in winter and spring compared to summer and fall.…”

“…Similarly, Cooley et al (Cooley et al, 2014) found that the likelihood of isolating L. monocytogenes from California surface water samples was significantly higher in winter and spring compared to summer and fall. Falardeau et al (Falardeau et al, 2017) and Cooley et al (Cooley et al, 2014) attributed these seasonal trends in L. monocytogenes isolation to increased rainfall and lower temperatures in winter and spring compared to summer and fall. In our study, the likelihood of isolating L. monocytogenes in NY (i) was also associated with temperature, and (ii) decreased as air temperature increased from May to June and increased as air temperature decreased from July to September.…”

“…In our study, the likelihood of isolating L. monocytogenes in NY (i) was also associated with temperature, and (ii) decreased as air temperature increased from May to June and increased as air temperature decreased from July to September. However, year-day may also serve as a proxy for unmeasured factors that change seasonally and affect microbial water quality, including anthropogenic reductions in water flow (e.g., damming of irrigation ditches), which inhibit pathogen movement within watersheds (Falardeau et al, 2017). While we did not observe this type of activity, all of the sampled waterways are in agricultural areas and provide water to commercial operations.…”

“…Given the number of factors (e.g., bottom substrate, upstream land use) that differ between waterways and may affect water quality, it is not surprising that microbial water quality would vary between waterways. In fact, multiple studies have found associations between microbial water quality and upstream land use (Bradshaw et al, 2016; Brendel and Soupir, 2017; Dila et al, 2018; Falardeau et al, 2017; Lyautey et al, 2007; Pandey et al, 2012; Verhougstraete et al, 2015). For instance, Pandey et al (Pandey et al, 2012) tracked water quality at 46 sites in an Iowa watershed and found that E. coli levels were positively associated with the amount of cropland in Thiessen polygons around each site.…”

“…For instance, Pandey et al (Pandey et al, 2012) tracked water quality at 46 sites in an Iowa watershed and found that E. coli levels were positively associated with the amount of cropland in Thiessen polygons around each site. Associations between microbial water quality, and proximity to upstream livestock operations (Bond and Partyka, 2004; Lyautey et al, 2010; Wilkes et al, 2011), the number of septic systems in a watershed (Verhougstraete et al, 2015), and livestock and human population density (Dila et al, 2018; Falardeau et al, 2017) have also been reported. Post-hoc identification of factors that drive spatial variation in water quality is difficult and requires data that were not collected as part of the current study (e.g., on upstream activity and land use).…”