Evaluation of environmental risk factors associated with survival of generic E. coli in organic integrated crop-livestock systems in California and Minnesota

Authors: CHEONG, SEJIN - University Of California, Davis; CHANDLER-KHAYD, CAROLYN - University Of California, Davis; WILLIAMS, SEQUOIA - University Of California, Davis; GAUDIN, AMELIE - University Of California, Davis; AMINABADI, PEIMAN - Collaborator; JAY-RUSSEL, MICHETE - Collaborator; EVANS, EMILY - University Of Minnesota; KLOSSNER, LEE - University Of Minnesota; PAGLIARI, PAULO - University Of Minnesota; Millner, Patricia

Submitted to: Frontiers in Sustainable Food Systems
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/27/2024
Publication Date: 12/11/2024
Citation: Cheong, S., Chandler-Khayd, C., Williams, S.R., Gaudin, A., Aminabadi, P., Jay-Russel, M.T., Evans, E., Klossner, L., Pagliari, P., Millner, P.D. 2024. Evaluation of environmental risk factors associated with survival of generic E. coli in organic integrated crop-livestock systems in California and Minnesota. Frontiers in Sustainable Food Systems. 8. Article e1464018. https://doi.org/10.3389/fsufs.2024.1464018.
DOI: https://doi.org/10.3389/fsufs.2024.1464018

Interpretive Summary: Potential risk of contamination by foodborne illness pathogens was investigated for certified organic fresh produce harvested from rotational cover crop fields grazed by livestock. A two-year study in California and Minnesota examined the presence of viable foodborne pathogens (E. coli O157, non-O157 Shiga toxin producing E. coli (STEC) and Listeria monocytogenes), in three treatments (fallow; cover crop with no grazing; and with grazing by small ruminants) on spinach (2021) and cucumber (2022). Random Forest (RF) analysis showed associations between meteorological and soil chemical characteristics and generic E. coli (gEc) presence in soil. Persistence of gEc, an indicator of fecal contamination in grazed soil, was evaluated using mixed effect zero-inflated negative binomial (ZINB) models, and meteorological factors identified from RF analyses. In 2022, soil contamination by non-O157 STEC increased (2.7%, 15/552) compared to 2021 (0%, 0/504) in both states; this tracked with increased prevalence of non-O157 STEC in post-grazed fecal samples from sheep in CA (41.7%, 5/12) and goats (42.5%, 17/40) in MN. These findings on food safety in livestock grazed, certified organic fresh produce production systems point to the need to consider: 1) meteorological conditions on sampling dates, and 2) cumulative effects of grazing on the 90- and 120-day wait periods between manuring by grazing and produce harvest.

Technical Abstract: Integrated crop-livestock systems (ICLS) may lead to the contamination of fresh produce with transfer of foodborne pathogens via from soil, as the contaminated with feces from grazing animals to fresh produce naturally harbor enteric foodborne pathogens. Over two years, organic ICLS field trials were conducted in California (CA) and Minnesota (MN) to examine the presence of viable foodborne pathogens (Escherichia coli O157, non-O157 Shiga toxin producing E. coli (STEC), and Listeria monocytogenes) across three treatments (fallow, ; cover crop without grazing, ; and cover crop with grazing by small ruminants) in on fresh produce (spinach in 2021 and cucumber in 2022) and in soils. A Random Forest (RF) analytical approach was used to determine potential associations between mMeteorological factors, and soil chemical characteristics were evaluated to identify potential associations with and the presence of generic E. coli (gEc) in the soil. using Random Forest (RF) analyses. The pPersistence of gEc was used as an indicator of fecal contamination in the grazed soil over time and was evaluated using mixed effect zero-inflated negative binomial (ZINB) models, considering top-ranked meteorological factors identified from RF analyses. Across the two-year time period, only one produce sample (cucumber) tested positive for non-O157 STEC (0.6%, 1/157) from the grazed soil in MN, with no detection of other foodborne pathogens in produce. Soil contamination by non-O157 STEC increased in 2022 (2.7%, 15/552) compared to 2021 (0%, 0/504) from both states, aligning with the increased prevalence of non-O157 STEC in post-grazed fecal samples from sheep in CA (41.7%, 5/12) and goats (42.5%, 17/40) in MN in 2022. The concentration Concentrations of gEc (Most Probable Number/100 g) in grazed soil returned to levels comparable to the non-grazed or fallow treatments within 87-147 days post-graze (DPG) over two years, with a significant decrease after 32 DPG predicted in by the final ZINB model. Interestingly, non-O157 STEC was detected in the soil even after the concentrations of gEc became lower on 115-147 DPG. Although the effects of meteorological factors and soil chemical characteristics were not as influential as the effects of treatment or sampling day (DPG) effects, ZINB analysis with identified meteorological factors in grazed soil suggested that regional differences in gEc counts were likely influenced by maximum air/soil temperatures on the sampling day. Further investigation is needed on the adoption of the NOP 90- and 120-day interval rules between manure application by grazing and harvest, considering a wider range of environmental factors across different regions and the potential cumulative effect of continuous ICLS in the same field.