Risk factors associated with the prevalence of Listeria monocytogenes in manured soils on certified organic farms in four regions of the United States

Authors: KHAYD, CAROLYN - University Of California, Davis; DI FRANCESCO, JULIETTE - University Of California, Davis; BARON, JEROME - University Of California, Davis; DE MELO RAMOS, THAIS - University Of California, Davis; AMINABADI, PEIMAN - University Of California, Davis; JAY-RUSSEL, MICHELE - University Of California, Davis; HAGHANI, VIKTORIA - University Of California, Davis; Millner, Patricia; PAGLIARI, PAULO - University Of Minnesota; HUTCHINSON, MARL - University Of Maryland Eastern Shore (UMES); KENNY, ANNETTE - University Of Maryland Eastern Shore (UMES); HASHEM, FAWZY - University Of Maryland Eastern Shore (UMES); MARTÍNEZ-LÓPEZ, BEATRIZ - University Of California, Davis; BIHN, ELIZABETH - Cornell University; CLEMENTS, DONNA - Cornell University; SHADE, JESSICA - The Organic Center; SCILIGO, AMBER - The Organic Center

Submitted to: Frontiers in Sustainable Food Systems
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/25/2023
Publication Date: 9/12/2023
Citation: Khayd, C.C., Di Francesco, J., Baron, J.N., De Melo Ramos, T., Aminabadi, P., Jay-Russel, M.T., Haghani, V., Millner, P.D., Pagliari, P., Hutchinson, M., Kenny, A., Hashem, F., Martínez-López, B., Bihn, E.A., Clements, D.P., Shade, J.R., Sciligo, A.R. 2023. Risk factors associated with the prevalence of Listeria monocytogenes in manured soils on certified organic farms in four regions of the United States. Frontiers in Sustainable Food Systems. 7:1222192. https://doi.org/10.3389/fsufs.2023.1222192.
DOI: https://doi.org/10.3389/fsufs.2023.1222192

Interpretive Summary: Use of raw (untreated), aged, or incompletely composted (non-thermophilic) manure when used on farms to maintain or improve soil fertility increases the risk of contamination of fresh produce by foodborne illness pathogens. For USDA certified organic farms [National Organic Program (NOP], 90- or 120-day intervals between application of untreated manure and crop harvest is required. The longer time interval applies to edible produce that directly contacts soil. In this multi-regional study, the effects of environmental and management factors on survival of Listeria monocytogenes in soil and their transfer to the fresh produce were examined. Manure, soil, and irrigation water samples collected from 19 farms in 4 USA regions (9 CA, 4 ME, 5 MN, and 1 MD) during the 2017-2018 growing seasons were cultured for L. monocytogenes up to180 days post-manure application. Farm management practices (previous use with livestock, presence of feces, season of manure application), soil characteristics increased the odds of detecting positive samples. This is the first study to examine L. monocytogenes contamination risk factors associated with untreated manure amended soil on organic farms in four regions of the US. The findings of this study highlight that factors beyond time intervals are associated with the presence of L. monocytogenes in soil. While sampling time was significantly associated with L. monocytogenes contamination, multiple environmental (weather, soil characteristics), management (land use, domestic animals, manure application season), and microbiological (generic E. coli, other foodborne pathogens) factors also were associated with the presence of L. monocytogenes in the soil. This emphasizes the need to further examine risk factors beyond time intervals, and incorporate those variables into regulations for the use of untreated manure on organic fresh produce fields.

Technical Abstract: Biological soil amendments, including raw or untreated manure, are currently used to improve soil fertility, especially in organic operations that are prohibited from using conventional fertilizers and other soil amendments. However, the addition of untreated manure may pose a contamination risk to the soil and growing produce as it may contain microorganisms of public health significance, including Listeria monocytogenes. Organic growers follow the United States Department of Agriculture (USDA) National Organic Program regulations for use of raw manure, which stipulate harvest should commence no earlier than 90 or 120 days post application, depending on the level of contact the edible portion of the produce has with the soil. To inform the establishment of such time-intervals, this study aimed to explore the farm-level predictors of L. monocytogenes prevalence in untreated manure amended soils on USDA-certified organic farms in the United States. A longitudinal, multi-regional study was conducted on 19 farms in four states (California, Minnesota, Maine, and Maryland) over two growing seasons (2017 and 2018). Untreated manure, soil, irrigation water, and produce samples were collected and cultured for L. monocytogenes. Mixed effect logistic regression was used to investigate risk factors associated with L. monocytogenes prevalence in soil. Results showed that multiple factors influenced the odds of a positive sample, including temporal (year, sampling day) and weather (precipitation, temperature, soil moisture) variables, microbiological characteristics (concentration of generic E. coli in soil, presence of L. monocytogenes and other pathogens in manure), and other factors associated with field usage, farm management practices, and soil composition. This study highlights the complexity of L. monocytogenes prevalence in soil and contributes science-based metrics that may be used when determining risk-mitigation strategies for pathogen contamination.