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Oral Administration of a Phage Cocktail to Reduce Salmonella Colonization in Broiler Gastrointestinal Tract—A Pilot Study

SIMPLE SUMMARY: Salmonella contamination in the poultry supply chain is a global public concern and can lead to a serious foodborne illness; thus, effective control measures are needed. Here, we focused on the application of phage treatment to control Salmonella during the pre-harvest step of poultr...

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Autores principales: Pelyuntha, Wattana, Yafa, Ananya, Ngasaman, Ruttayaporn, Yingkajorn, Mingkwan, Chukiatsiri, Kridda, Champoochana, Nidanut, Vongkamjan, Kitiya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9686501/
https://www.ncbi.nlm.nih.gov/pubmed/36428315
http://dx.doi.org/10.3390/ani12223087
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author Pelyuntha, Wattana
Yafa, Ananya
Ngasaman, Ruttayaporn
Yingkajorn, Mingkwan
Chukiatsiri, Kridda
Champoochana, Nidanut
Vongkamjan, Kitiya
author_facet Pelyuntha, Wattana
Yafa, Ananya
Ngasaman, Ruttayaporn
Yingkajorn, Mingkwan
Chukiatsiri, Kridda
Champoochana, Nidanut
Vongkamjan, Kitiya
author_sort Pelyuntha, Wattana
collection PubMed
description SIMPLE SUMMARY: Salmonella contamination in the poultry supply chain is a global public concern and can lead to a serious foodborne illness; thus, effective control measures are needed. Here, we focused on the application of phage treatment to control Salmonella during the pre-harvest step of poultry meat production. Salmonella reduction was monitored in broilers on a commercial farm. Phage treatment has been proposed as a potential alternative biocontrol agent for agricultural purposes due to its specificity and safety, whereby it will only target bacterial hosts without harmful effects on human and animal health. Phages not only provide benefits for reducing the number of pathogens, but they are also easy to apply or deliver to a wide range of animals. In this study, phages and a phage cocktail were developed to provide an effective method for reducing Salmonella colonization in the gastrointestinal tract of broilers to improve food safety from farm to fork. ABSTRACT: Salmonella contamination in poultry meat products can lead to serious foodborne illness and economic loss from product recalls. It is crucial to control Salmonella contamination in poultry from farm to fork. Bacteriophages (phages) are viruses of bacteria that offer several advantages, especially their specificity to target bacteria. In our study, three Salmonella phages (vB_SenS_KP001, vB_SenS_KP005, and vB_SenS_WP110) recovered from a broiler farm and wastewater treatment stations showed high lysis ability ranging from 85.7 to 96.4% on over 56 serovars of Salmonella derived from several sources, including livestock and a broiler farm environment. A three-phage cocktail reduced S. Enteritidis and S. Typhimurium, in vitro by 3.9 ± 0.0 and 3.9 ± 0.2 log units at a multiplicity of infection (MOI) of 10(3) and 3.8 ± 0.4 and 4.1 ± 0.2 log units at MOI of 10(4) after 6 h post-phage treatment. A developed phage cocktail did not cause phage resistance in Salmonella during phage treatments for three passages. Phages could survive under simulated chicken gastrointestinal conditions in the presence of gastric acid for 2 h (100.0 ± 0.0% survivability), bile salt for 1 h (98.1 ± 1.0% survivability), and intestinal fluid for 4 h (100 ± 0.0% survivability). Each phage was in the phage cocktail at a concentration of up to 9.0 log PFU/mL. These did not cause any cytotoxicity to human fibroblast cells or Caco-2 cells as indicated by the percent of cell viability, which remained nearly 100% as compared with the control during 72 h of co-culture. The phage cocktail was given to broilers raised in commercial conditions at a 9 log PFU/dose for five doses, while naturally occurring Salmonella cells colonized in the gastrointestinal tract of broilers were significantly reduced as suggested by a considerably lower Salmonella prevalence from over 70 to 0% prevalence after four days of phage treatment. Our findings suggest that a phage cocktail is an effective biocontrol agent to reduce Salmonella present in the guts of broilers, which can be applied to improve food safety in broiler production.
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spelling pubmed-96865012022-11-25 Oral Administration of a Phage Cocktail to Reduce Salmonella Colonization in Broiler Gastrointestinal Tract—A Pilot Study Pelyuntha, Wattana Yafa, Ananya Ngasaman, Ruttayaporn Yingkajorn, Mingkwan Chukiatsiri, Kridda Champoochana, Nidanut Vongkamjan, Kitiya Animals (Basel) Article SIMPLE SUMMARY: Salmonella contamination in the poultry supply chain is a global public concern and can lead to a serious foodborne illness; thus, effective control measures are needed. Here, we focused on the application of phage treatment to control Salmonella during the pre-harvest step of poultry meat production. Salmonella reduction was monitored in broilers on a commercial farm. Phage treatment has been proposed as a potential alternative biocontrol agent for agricultural purposes due to its specificity and safety, whereby it will only target bacterial hosts without harmful effects on human and animal health. Phages not only provide benefits for reducing the number of pathogens, but they are also easy to apply or deliver to a wide range of animals. In this study, phages and a phage cocktail were developed to provide an effective method for reducing Salmonella colonization in the gastrointestinal tract of broilers to improve food safety from farm to fork. ABSTRACT: Salmonella contamination in poultry meat products can lead to serious foodborne illness and economic loss from product recalls. It is crucial to control Salmonella contamination in poultry from farm to fork. Bacteriophages (phages) are viruses of bacteria that offer several advantages, especially their specificity to target bacteria. In our study, three Salmonella phages (vB_SenS_KP001, vB_SenS_KP005, and vB_SenS_WP110) recovered from a broiler farm and wastewater treatment stations showed high lysis ability ranging from 85.7 to 96.4% on over 56 serovars of Salmonella derived from several sources, including livestock and a broiler farm environment. A three-phage cocktail reduced S. Enteritidis and S. Typhimurium, in vitro by 3.9 ± 0.0 and 3.9 ± 0.2 log units at a multiplicity of infection (MOI) of 10(3) and 3.8 ± 0.4 and 4.1 ± 0.2 log units at MOI of 10(4) after 6 h post-phage treatment. A developed phage cocktail did not cause phage resistance in Salmonella during phage treatments for three passages. Phages could survive under simulated chicken gastrointestinal conditions in the presence of gastric acid for 2 h (100.0 ± 0.0% survivability), bile salt for 1 h (98.1 ± 1.0% survivability), and intestinal fluid for 4 h (100 ± 0.0% survivability). Each phage was in the phage cocktail at a concentration of up to 9.0 log PFU/mL. These did not cause any cytotoxicity to human fibroblast cells or Caco-2 cells as indicated by the percent of cell viability, which remained nearly 100% as compared with the control during 72 h of co-culture. The phage cocktail was given to broilers raised in commercial conditions at a 9 log PFU/dose for five doses, while naturally occurring Salmonella cells colonized in the gastrointestinal tract of broilers were significantly reduced as suggested by a considerably lower Salmonella prevalence from over 70 to 0% prevalence after four days of phage treatment. Our findings suggest that a phage cocktail is an effective biocontrol agent to reduce Salmonella present in the guts of broilers, which can be applied to improve food safety in broiler production. MDPI 2022-11-09 /pmc/articles/PMC9686501/ /pubmed/36428315 http://dx.doi.org/10.3390/ani12223087 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Pelyuntha, Wattana
Yafa, Ananya
Ngasaman, Ruttayaporn
Yingkajorn, Mingkwan
Chukiatsiri, Kridda
Champoochana, Nidanut
Vongkamjan, Kitiya
Oral Administration of a Phage Cocktail to Reduce Salmonella Colonization in Broiler Gastrointestinal Tract—A Pilot Study
title Oral Administration of a Phage Cocktail to Reduce Salmonella Colonization in Broiler Gastrointestinal Tract—A Pilot Study
title_full Oral Administration of a Phage Cocktail to Reduce Salmonella Colonization in Broiler Gastrointestinal Tract—A Pilot Study
title_fullStr Oral Administration of a Phage Cocktail to Reduce Salmonella Colonization in Broiler Gastrointestinal Tract—A Pilot Study
title_full_unstemmed Oral Administration of a Phage Cocktail to Reduce Salmonella Colonization in Broiler Gastrointestinal Tract—A Pilot Study
title_short Oral Administration of a Phage Cocktail to Reduce Salmonella Colonization in Broiler Gastrointestinal Tract—A Pilot Study
title_sort oral administration of a phage cocktail to reduce salmonella colonization in broiler gastrointestinal tract—a pilot study
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9686501/
https://www.ncbi.nlm.nih.gov/pubmed/36428315
http://dx.doi.org/10.3390/ani12223087
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