Landscape, Water Quality, and Weather Factors Associated With an Increased Likelihood of Foodborne Pathogen Contamination of New York Streams Used to Source Water for Produce Production.

Daniel Weller,Martin Wiedmann,Alexandra Belias,Hyatt Green,Sherry Roof

doi:10.3389/fsufs.2019.00124

Abstract

There is a need for science-based tools to (i) help manage microbial produce safety hazards associated with preharvest surface water use, and (ii) facilitate comanagement of agroecosystems for competing stakeholder aims. To develop these tools an improved understanding of foodborne pathogen ecology in freshwater systems is needed. The purpose of this study was to identify (i) sources of potential food safety hazards, and (ii) combinations of factors associated with an increased likelihood of pathogen contamination of agricultural water Sixty-eight streams were sampled between April and October 2018 (196 samples). At each sampling event separate 10-L grab samples (GS) were collected and tested for Listeria, Salmonella, and the stx and eaeA genes. A 1-L GS was also collected and used for Escherichia coli enumeration and detection of four host-associated fecal source-tracking markers (FST). Regression analysis was used to identify individual factors that were significantly associated with pathogen detection. We found that eaeA-stx codetection [Odds Ratio (OR) = 4.2; 95% Confidence Interval (CI) = 1.3, 13.4] and Salmonella isolation (OR = 1.8; CI = 0.9, 3.5) were strongly associated with detection of ruminant and human FST markers, respectively, while Listeria spp. (excluding Listeria monocytogenes) was negatively associated with log10 E. coli levels (OR = 0.50; CI = 0.26, 0.96). L. monocytogenes isolation was not associated with the detection of any fecal indicators. This observation supports the current understanding that, unlike enteric pathogens, Listeria is not fecally-associated and instead originates from other environmental sources. Separately, conditional inference trees were used to identify scenarios associated with an elevated or reduced risk of pathogen contamination. Interestingly, while the likelihood of isolating L. monocytogenes appears to be driven by complex interactions between environmental factors, the likelihood of Salmonella isolation and eaeA-stx codetection were driven by physicochemical water quality (e.g., dissolved oxygen) and temperature, respectively. Overall, these models identify environmental conditions associated with an enhanced risk of pathogen presence in agricultural water (e.g., rain events were associated with L. monocytogenes isolation from samples collected downstream of dairy farms; P = 0.002). The information presented here will enable growers to comanage their operations to mitigate the produce safety risks associated with preharvest surface water use.

Highlights

Over the last two decades, the occurrence of multiple foodborne disease outbreaks linked to contamination of preharvest produce by wildlife (Cody et al, 1999; Jay et al, 2007; Kangas et al, 2008; Laidler et al, 2013; Kwan et al, 2014) or surface water have highlighted the role of wildlife and surface water as on-farm sources of foodborne pathogens
Using a diversity of data types and advanced geographic analyses this study identified combinations of environmental conditions associated with an increased likelihood of pathogen presence in agricultural water
This study provides data that will enable growers to better manage the food safety risks associated with preharvest surface water use

Summary

Introduction

Over the last two decades, the occurrence of multiple foodborne disease outbreaks linked to contamination of preharvest produce by wildlife (Cody et al, 1999; Jay et al, 2007; Kangas et al, 2008; Laidler et al, 2013; Kwan et al, 2014) or surface water (e.g., during irrigation; Gelting et al, 2011, 2015; Mody et al, 2011; Lundqvist et al, 2013; FDA, 2019) have highlighted the role of wildlife and surface water as on-farm sources of foodborne pathogens. As part of the traceback investigation during a 2006 Escherichia coli outbreak linked to bagged spinach, the outbreak strain was isolated from both feral pig feces and preharvest water from the implicated farm (Jay et al, 2007) Following this outbreak, growers reported increased pressure to adopt practices to prevent wildlife intrusion into produce fields, including through the removal of on-farm, non-crop vegetation (e.g., forest and wetland cover, hedgerows; Beretti and Stuart, 2008; Karp et al, 2015; Baur et al, 2016). Additional research on the association between upstream landscape structure and foodborne pathogen contamination of preharvest surface water sources is needed to (i) develop effective strategies for comanaging agricultural watersheds for multiple stakeholder aims (e.g., preventing wildlife intrusion, water quality), and (ii) reduce the unintended consequences of on-farm food safety practices (e.g., removal of non-crop vegetation). One aim of the present study is to characterize the association between upstream landscape structure and foodborne pathogen detection

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