Cargando…

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

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 cou...

Descripción completa

Detalles Bibliográficos
Autores principales: Ferguson, Martine, Hsu, Chiun-Kang, Grim, Christopher, Kauffman, Michael, Jarvis, Karen, Pettengill, James B., Babu, Uma S., Harrison, Lisa M., Li, Baoguang, Hayford, Alice, Balan, Kannan V., Freeman, Josefina P., Rajashekara, Gireesh, Lipp, Erin K., Rozier, Ralph Scott, Zimeri, Anne Marie, Burall, Laurel S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10117993/
https://www.ncbi.nlm.nih.gov/pubmed/37089556
http://dx.doi.org/10.3389/fmicb.2023.1141043
_version_ 1785028712295563264
author Ferguson, Martine
Hsu, Chiun-Kang
Grim, Christopher
Kauffman, Michael
Jarvis, Karen
Pettengill, James B.
Babu, Uma S.
Harrison, Lisa M.
Li, Baoguang
Hayford, Alice
Balan, Kannan V.
Freeman, Josefina P.
Rajashekara, Gireesh
Lipp, Erin K.
Rozier, Ralph Scott
Zimeri, Anne Marie
Burall, Laurel S.
author_facet Ferguson, Martine
Hsu, Chiun-Kang
Grim, Christopher
Kauffman, Michael
Jarvis, Karen
Pettengill, James B.
Babu, Uma S.
Harrison, Lisa M.
Li, Baoguang
Hayford, Alice
Balan, Kannan V.
Freeman, Josefina P.
Rajashekara, Gireesh
Lipp, Erin K.
Rozier, Ralph Scott
Zimeri, Anne Marie
Burall, Laurel S.
author_sort Ferguson, Martine
collection PubMed
description 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.
format Online
Article
Text
id pubmed-10117993
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-101179932023-04-21 A longitudinal study to examine the influence of farming practices and environmental factors on pathogen prevalence using structural equation modeling Ferguson, Martine Hsu, Chiun-Kang Grim, Christopher Kauffman, Michael Jarvis, Karen Pettengill, James B. Babu, Uma S. Harrison, Lisa M. Li, Baoguang Hayford, Alice Balan, Kannan V. Freeman, Josefina P. Rajashekara, Gireesh Lipp, Erin K. Rozier, Ralph Scott Zimeri, Anne Marie Burall, Laurel S. Front Microbiol Microbiology 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. Frontiers Media S.A. 2023-04-06 /pmc/articles/PMC10117993/ /pubmed/37089556 http://dx.doi.org/10.3389/fmicb.2023.1141043 Text en Copyright © 2023 Ferguson, Hsu, Grim, Kauffman, Jarvis, Pettengill, Babu, Harrison, Li, Hayford, Balan, Freeman, Rajashekara, Lipp, Rozier, Zimeri and Burall. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ferguson, Martine
Hsu, Chiun-Kang
Grim, Christopher
Kauffman, Michael
Jarvis, Karen
Pettengill, James B.
Babu, Uma S.
Harrison, Lisa M.
Li, Baoguang
Hayford, Alice
Balan, Kannan V.
Freeman, Josefina P.
Rajashekara, Gireesh
Lipp, Erin K.
Rozier, Ralph Scott
Zimeri, Anne Marie
Burall, Laurel S.
A longitudinal study to examine the influence of farming practices and environmental factors on pathogen prevalence using structural equation modeling
title A longitudinal study to examine the influence of farming practices and environmental factors on pathogen prevalence using structural equation modeling
title_full A longitudinal study to examine the influence of farming practices and environmental factors on pathogen prevalence using structural equation modeling
title_fullStr A longitudinal study to examine the influence of farming practices and environmental factors on pathogen prevalence using structural equation modeling
title_full_unstemmed A longitudinal study to examine the influence of farming practices and environmental factors on pathogen prevalence using structural equation modeling
title_short A longitudinal study to examine the influence of farming practices and environmental factors on pathogen prevalence using structural equation modeling
title_sort longitudinal study to examine the influence of farming practices and environmental factors on pathogen prevalence using structural equation modeling
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10117993/
https://www.ncbi.nlm.nih.gov/pubmed/37089556
http://dx.doi.org/10.3389/fmicb.2023.1141043
work_keys_str_mv AT fergusonmartine alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT hsuchiunkang alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT grimchristopher alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT kauffmanmichael alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT jarviskaren alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT pettengilljamesb alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT babuumas alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT harrisonlisam alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT libaoguang alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT hayfordalice alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT balankannanv alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT freemanjosefinap alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT rajashekaragireesh alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT lipperink alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT rozierralphscott alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT zimeriannemarie alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT buralllaurels alongitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT fergusonmartine longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT hsuchiunkang longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT grimchristopher longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT kauffmanmichael longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT jarviskaren longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT pettengilljamesb longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT babuumas longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT harrisonlisam longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT libaoguang longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT hayfordalice longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT balankannanv longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT freemanjosefinap longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT rajashekaragireesh longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT lipperink longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT rozierralphscott longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT zimeriannemarie longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling
AT buralllaurels longitudinalstudytoexaminetheinfluenceoffarmingpracticesandenvironmentalfactorsonpathogenprevalenceusingstructuralequationmodeling