Survival and persistence of indicator organisms and foodborne pathogens in spatially-separated integrated crop-livestock farm environments

Authors: GOODWYN, BRIAN - University Of Maryland Eastern Shore (UMES); Millner, Patricia; PUNCHIHEWAGE-DON, ANURADHA - University Of Maryland Eastern Shore (UMES); SCHWARZ, MELINDA - Eastern Shore Agricultural Research And Education; HASHEM, FAWZY - Eastern Shore Agricultural Research And Education; BOWERS, JOHN - Food And Drug Administration(FDA); BISWAS, DEBABRATA - University Of Maryland

Submitted to: Frontiers in Sustainable Food Systems
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/5/2023
Publication Date: N/A
Citation: N/A

Interpretive Summary: Certified organic producers are using an integrated crop-livestock farm (ICLF) management strategy to achieve production and income goals while building soil health through nutrient cycling of animal wastes to the soil for crop and fodder production, thereby sustaining overall system health. Proximity of on-farm animals to crop fields or application of raw or incompletely treated manure may increase the risk of foodborne illness contamination on fresh produce, but the extent of risk requires further analysis. This study focused on measuring survival of pathogenic (STEC) E. coli and the prevalence of associated virulence factor (VF) genes, Listeria monocytogenes, Salmonella, and indicator bacteria in manured soils and their transfer from soil to harvested produce from three organic (ICLF) farms on the Eastern Shore of Maryland. Manure/compost, soil, untreated produce, and water samples (n=428) were collected before and after manure or compost incorporation and monthly up to 180 days thereafter. Manure and compost samples were positive for L. monocytogenes [6.7% (1/15) and STEC/VF genes 66.7% (10/15)]. For soils amended with manure-based products, 29.1% (74/254) were positive for at least one of the tested pathogens, with 24.0% (61/254) attributable to STEC/VF-genes, 4.3% (11/254) to Listeria monocytogenes, and 0.8% (2/254) to Salmonella. All three pathogens were detected in soils directly after manure product incorporation, but with time their prevalence decreased, although they were still detected 90- and 120-days post-manure amendment application. Results revealed that 18.4% (26/141) of produce samples harvested were positive for at least one of the tested pathogens, and STEC were the most often detected pathogen. Produce harvested at 90- and 120-days after manure/compost incorporation was contaminated with at least one pathogen and fecal indicators. Results indicate that pathogens associated with contaminated manures or composts can persist after soil incorporation, and beyond the 90- and 120-day amendment to harvest time wait periods stipulated for the National Organic program and can transfer to produce. This information will be useful to scientists and policy makers.

Technical Abstract: Certified organic production prohibits the use of chemical fertilizers, but permits use of biological soil amendments of animal origin (BSAAOs). For production of fresh produce likely to be consumed uncooked, the United States Department of Agriculture National Organic Program (USDA-NOP) stipulates a 90-day wait period between BSAAO application and crop harvest for produce not in direct-contact with soil, to reduce concerns about potential for pathogen contamination from BSAAOs used for soil fertility. For fresh produce crops in direct contact with soil this wait period is 120-days. In this study, survival of Listeria monocytogenes, Salmonella, Shiga-toxin producing E. coli and associated virulence factor genes (STEC/VF-genes), and indicator bacteria in BSAAO-treated soils were analyzed along with their potential to transfer to produce harvested from three organic, integrated crop-livestock farms (ICLFs) on the Eastern shore of Maryland. A total of 428 manure/compost, soil, untreated produce, and water samples were collected before/after BSAAO incorporations and monthly until day 180. Samples were assessed for Listeria monocytogenes, Salmonella, and STEC/VF-genes, and for aerobic plate count (APC), generic Escherichia coli (gEC), and total coliform levels using standard methods and PCR. Overall, 18.4% (26/141) of produce samples were positive for at least one of the tested pathogens, with STEC/VF-genes most often detected. Harvested produce was contaminated with at least one pathogen and indicators 90- and 120-days post BSAAO incorporation. Salmonella was not highly prevalent in manure/composts, but 6.7% (1/15) and 66.7% (10/15) of manure/compost samples were positive for Listeria monocytogenes and STEC/VF genes, respectively. In soils amended with BSAAOs, 29.1% (74/254) were positive for at least one of the tested pathogens in this study. Similar to produce, STEC/VF-genes were detected the most at 24.0% (61/254), while Listeria monocytogenes and Salmonella were detected in 4.3% (11/254) and 0.8% (2/254) of soils, respectively. The three pathogens were detected in soils directly after BSAAO incorporation but were followed by reduced prevalence. However, pathogens were detected 90- and 120-days post-application of BSAAO. Results indicate that the pathogens associated with BSAAOs (as contaminated manures or composts) can persist after soil incorporation and transfer to produce.