Frontiers in Microbiology (Apr 2023)

A longitudinal study to examine the influence of farming practices and environmental factors on pathogen prevalence using structural equation modeling

  • Martine Ferguson,
  • Chiun-Kang Hsu,
  • Christopher Grim,
  • Michael Kauffman,
  • Karen Jarvis,
  • James B. Pettengill,
  • Uma S. Babu,
  • Lisa M. Harrison,
  • Baoguang Li,
  • Alice Hayford,
  • Kannan V. Balan,
  • Josefina P. Freeman,
  • Gireesh Rajashekara,
  • Erin K. Lipp,
  • Ralph Scott Rozier,
  • Anne Marie Zimeri,
  • Laurel S. Burall

DOI
https://doi.org/10.3389/fmicb.2023.1141043
Journal volume & issue
Vol. 14

Abstract

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The contamination of fresh produce with foodborne pathogens has been an on-going concern with outbreaks linked to these commodities. Evaluation of farm practices, such as use of manure, irrigation water source, and other factors that could influence pathogen prevalence in the farming environment could lead to improved mitigation strategies to reduce the potential for contamination events. Soil, water, manure, and compost were sampled from farms in Ohio and Georgia to identify the prevalence of Salmonella, Listeria monocytogenes (Lm), Campylobacter, and Shiga-toxin-producing Escherichia coli (STEC), as well as Arcobacter, an emerging human pathogen. This study investigated agricultural practices to determine which influenced pathogen prevalence, i.e., the percent positive samples. These efforts identified a low prevalence of Salmonella, STEC, and Campylobacter in soil and water (< 10%), preventing statistical modeling of these pathogens. However, Lm and Arcobacter were found in soil (13 and 7%, respectively), manure (49 and 32%, respectively), and water samples (18 and 39%, respectively) at a comparatively higher prevalence, suggesting different dynamics are involved in their survival in the farm environment. Lm and Arcobacter prevalence data, soil chemical characteristics, as well as farm practices and weather, were analyzed using structural equation modeling to identify which factors play a role, directly or indirectly, on the prevalence of these pathogens. These analyses identified an association between pathogen prevalence and weather, as well as biological soil amendments of animal origin. Increasing air temperature increased Arcobacter and decreased Lm. Lm prevalence was found to be inversely correlated with the use of surface water for irrigation, despite a high Lm prevalence in surface water suggesting other factors may play a role. Furthermore, Lm prevalence increased when the microbiome’s Simpson’s Diversity Index decreased, which occurred as soil fertility increased, leading to an indirect positive effect for soil fertility on Lm prevalence. These results suggest that pathogen, environment, and farm management practices, in addition to produce commodities, all need to be considered when developing mitigation strategies. The prevalence of Arcobacter and Lm versus the other pathogens suggests that multiple mitigation strategies may need to be employed to control these pathogens.

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