Integrated crop-livestock farming systems influence the incidence of <i>Salmonella</i>, <i>Listeria monocytogenes</i>, Shiga toxin-producing <i>Escherichia coli</i>, and indicator bacteria on fresh produce

Abstract

Concerns remain about foodborne pathogen contamination risks to integrated crop-livestock farm (ICLF) fresh produce due to farm animal proximity to crop fields and use of biological soil amendments of animal origin (BSAAO). This study aimed to evaluate the extent of microbial contamination in Maryland's Eastern Shore ICLFs and compare results with those from corresponding samples from crop-only farms (COFs), farmers' markets, and supermarkets. Altogether, 1,782 soil, animal reservoir, water, and produce samples from ICLFs, COFs, farmers' markets, and supermarkets were analyzed following standard methods. Total aerobic bacterial counts and generic <i>Escherichia coli</i> were enumerated using petrifilms, whereas <i>Salmonella, Listeria monocytogenes</i> (<i>L. monocytogenes</i>), and Shiga toxin-producing <i>E. coli</i> (STEC) and virulence factors (VFs) were detected by culturing and PCR confirmation. ICLF soil health parameters were evaluated pre- and post-BSAAO incorporation. Animal pen samples and BSAAOs, which generally improved ICLF soil health parameters, harbored more pathogens and generic <i>E. coli</i>. Samples of ICLF produce (0.39%, 1.95%, and 13.62%) and soils (2.04%, 2.72%, and 20.86%) had higher <i>Salmonella</i>, <i>L. monocytogenes</i>, and STEC/VF-gene prevalence than COF produce (0.00%, 0.00%, and 5.33%) and soils (1.33%, 0.00%, and 20.00%), respectively. Pathogen contamination was relatively low in retail environments where <i>Salmonella</i> and <i>L. monocytogenes</i> were each isolated from one farmers' market produce, whereas STEC/VF-genes were found in one supermarket produce. Overall, the most frequent <i>Salmonella</i> serovars were Bareilly and Newport, whereas the highest detected STEC serovars and VF-genes were O103 and <i>stx</i>2. Produce contamination in ICLFs and farmers' markets was greater than that of traditional counterparts, indicating the importance of continued research/education regarding produce safety for producers and consumers.IMPORTANCEShifts in consumer demand have led to notable increases in integrated crop-livestock farms (ICLFs), which are major contributors to popular farmers' markets. However, production practices in these settings, like manure-based soil amendments and the lack of food safety regulation enforcement, have raised concerns regarding potential foodborne illness cases and outbreaks. This study provides valuable information on the prevalence and comparison of three major foodborne bacterial pathogens and indicator microorganisms in ICLF, crop-only farm (COF), farmers' market, and supermarket environments. <i>Salmonella</i>, <i>Listeria monocytogenes</i>, and Shiga toxin-producing <i>E. coli</i> were detected more frequently in ICLF and farmers' market samples compared with COF and supermarket samples, respectively. However, at least one pathogen was detected in each setting. Findings from this study highlight that, regardless of studied settings, the contamination risks associated with fresh produce production on the Maryland Eastern Shore will contribute to developing food safety standards in various produce production environments.