Factors Influencing the Persistence of Salmonella Infantis in Broiler Litter During Composting and Stabilization Processes and Following Soil Incorporation

Broiler litter (BL), a by-product of broiler meat production, is frequently contaminated with Salmonella and other zoonotic pathogens. To ensure the safety of crop production chains and limit pathogen spread in the environment, a pre-treatment is desired before further agricultural utilization. The...

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Main Authors: Ran Avidov, Vempalli Sudharsan Varma, Ibrahim Saadi, Aviva Hanan, Avishai Lublin, Shlomo Sela Saldinger, Yona Chen, Yael Laor
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-04-01
Series:Frontiers in Sustainable Food Systems
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fsufs.2021.645721/full
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author Ran Avidov
Ran Avidov
Vempalli Sudharsan Varma
Ibrahim Saadi
Aviva Hanan
Avishai Lublin
Shlomo Sela Saldinger
Yona Chen
Yael Laor
spellingShingle Ran Avidov
Ran Avidov
Vempalli Sudharsan Varma
Ibrahim Saadi
Aviva Hanan
Avishai Lublin
Shlomo Sela Saldinger
Yona Chen
Yael Laor
Factors Influencing the Persistence of Salmonella Infantis in Broiler Litter During Composting and Stabilization Processes and Following Soil Incorporation
Frontiers in Sustainable Food Systems
poultry litter
poultry manure
antagonistic microorganisms
thermal inactivation
pathogen elimination
zoonotic microorganisms
author_facet Ran Avidov
Ran Avidov
Vempalli Sudharsan Varma
Ibrahim Saadi
Aviva Hanan
Avishai Lublin
Shlomo Sela Saldinger
Yona Chen
Yael Laor
author_sort Ran Avidov
title Factors Influencing the Persistence of Salmonella Infantis in Broiler Litter During Composting and Stabilization Processes and Following Soil Incorporation
title_short Factors Influencing the Persistence of Salmonella Infantis in Broiler Litter During Composting and Stabilization Processes and Following Soil Incorporation
title_full Factors Influencing the Persistence of Salmonella Infantis in Broiler Litter During Composting and Stabilization Processes and Following Soil Incorporation
title_fullStr Factors Influencing the Persistence of Salmonella Infantis in Broiler Litter During Composting and Stabilization Processes and Following Soil Incorporation
title_full_unstemmed Factors Influencing the Persistence of Salmonella Infantis in Broiler Litter During Composting and Stabilization Processes and Following Soil Incorporation
title_sort factors influencing the persistence of salmonella infantis in broiler litter during composting and stabilization processes and following soil incorporation
publisher Frontiers Media S.A.
series Frontiers in Sustainable Food Systems
issn 2571-581X
publishDate 2021-04-01
description Broiler litter (BL), a by-product of broiler meat production, is frequently contaminated with Salmonella and other zoonotic pathogens. To ensure the safety of crop production chains and limit pathogen spread in the environment, a pre-treatment is desired before further agricultural utilization. The objective of this study was to characterize the effect of physico-chemical properties on Salmonella persistence in BL during composting and stabilization and following soil incorporation, toward optimization of the inactivation process. Thirty-six combinations of temperature (30, 40, 50, and 60°C), water content (40, 55, and 70%; w/w), and initial pH (6, 7, and 8.5) were employed in static lab vessels to study the persistence of Salmonella enterica serovar Infantis (S. Infantis; a multidrug-resistant strain) during incubation of artificially-inoculated BL. The effect of aeration was investigated in a composting simulator, with controlled heating and flow conditions. Temperature was found to be the main factor significantly influencing Salmonella decay rates, while water content and initial pH had a secondary level of influence with significant effects mainly at 30 and 40°C. Controlled simulations showed faster decay of Salmonella under anaerobic conditions at mesophilic temperatures (<45°C) and no effect of NH3 emissions. Re-wetting the BL at mesophilic temperatures resulted in Salmonella burst, and led to a higher tolerance of the pathogen at increased temperatures. Based on the decay rates measured under all temperature, water content, and pH conditions, it was estimated that the time required to achieve a 7 log10 reduction in Salmonella concentration, ranges between 13.7–27.2, 6.5–15.6, 1.2–4.7, and 1.3–1.5 days for 30, 40, 50, and 60°C, respectively. Inactivation of BL indigenous microbial population by autoclaving or addition of antibiotics to which the S. Infantis is resistant, resulted in augmentation of Salmonella multiplication. This suggests the presence of microbial antagonists in the BL, which inhibit the growth of the pathogen. Finally, Salmonella persisted over 90 days at 30°C in a Vertisol soil amended with inoculated BL, presumably due to reduced antagonistic activity compared to the BL alone. These findings are valuable for risk assessments and the formulation of guidelines for safe utilization of BL in agriculture.
topic poultry litter
poultry manure
antagonistic microorganisms
thermal inactivation
pathogen elimination
zoonotic microorganisms
url https://www.frontiersin.org/articles/10.3389/fsufs.2021.645721/full
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spelling doaj-b7b1b71ee8ed4b07ac7dc8c4b14bcdcb2021-04-20T06:23:41ZengFrontiers Media S.A.Frontiers in Sustainable Food Systems2571-581X2021-04-01510.3389/fsufs.2021.645721645721Factors Influencing the Persistence of Salmonella Infantis in Broiler Litter During Composting and Stabilization Processes and Following Soil IncorporationRan Avidov0Ran Avidov1Vempalli Sudharsan Varma2Ibrahim Saadi3Aviva Hanan4Avishai Lublin5Shlomo Sela Saldinger6Yona Chen7Yael Laor8Institute of Soil, Water and Environmental Sciences, Newe Ya'ar Research Center, Agricultural Research Organization - Volcani Institute, Ramat Yishay, IsraelFaculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Jerusalem, IsraelInstitute of Soil, Water and Environmental Sciences, Newe Ya'ar Research Center, Agricultural Research Organization - Volcani Institute, Ramat Yishay, IsraelInstitute of Soil, Water and Environmental Sciences, Newe Ya'ar Research Center, Agricultural Research Organization - Volcani Institute, Ramat Yishay, IsraelInstitute of Soil, Water and Environmental Sciences, Newe Ya'ar Research Center, Agricultural Research Organization - Volcani Institute, Ramat Yishay, IsraelDivision of Avian Diseases, Kimron Veterinary Institute, Bet Dagan, IsraelInstitute of Postharvest and Food Sciences, Agricultural Research Organization - Volcani Institute, Rishon LeZion, IsraelFaculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Jerusalem, IsraelInstitute of Soil, Water and Environmental Sciences, Newe Ya'ar Research Center, Agricultural Research Organization - Volcani Institute, Ramat Yishay, IsraelBroiler litter (BL), a by-product of broiler meat production, is frequently contaminated with Salmonella and other zoonotic pathogens. To ensure the safety of crop production chains and limit pathogen spread in the environment, a pre-treatment is desired before further agricultural utilization. The objective of this study was to characterize the effect of physico-chemical properties on Salmonella persistence in BL during composting and stabilization and following soil incorporation, toward optimization of the inactivation process. Thirty-six combinations of temperature (30, 40, 50, and 60°C), water content (40, 55, and 70%; w/w), and initial pH (6, 7, and 8.5) were employed in static lab vessels to study the persistence of Salmonella enterica serovar Infantis (S. Infantis; a multidrug-resistant strain) during incubation of artificially-inoculated BL. The effect of aeration was investigated in a composting simulator, with controlled heating and flow conditions. Temperature was found to be the main factor significantly influencing Salmonella decay rates, while water content and initial pH had a secondary level of influence with significant effects mainly at 30 and 40°C. Controlled simulations showed faster decay of Salmonella under anaerobic conditions at mesophilic temperatures (<45°C) and no effect of NH3 emissions. Re-wetting the BL at mesophilic temperatures resulted in Salmonella burst, and led to a higher tolerance of the pathogen at increased temperatures. Based on the decay rates measured under all temperature, water content, and pH conditions, it was estimated that the time required to achieve a 7 log10 reduction in Salmonella concentration, ranges between 13.7–27.2, 6.5–15.6, 1.2–4.7, and 1.3–1.5 days for 30, 40, 50, and 60°C, respectively. Inactivation of BL indigenous microbial population by autoclaving or addition of antibiotics to which the S. Infantis is resistant, resulted in augmentation of Salmonella multiplication. This suggests the presence of microbial antagonists in the BL, which inhibit the growth of the pathogen. Finally, Salmonella persisted over 90 days at 30°C in a Vertisol soil amended with inoculated BL, presumably due to reduced antagonistic activity compared to the BL alone. These findings are valuable for risk assessments and the formulation of guidelines for safe utilization of BL in agriculture.https://www.frontiersin.org/articles/10.3389/fsufs.2021.645721/fullpoultry litterpoultry manureantagonistic microorganismsthermal inactivationpathogen eliminationzoonotic microorganisms