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Reduction of Salmonella contamination on the surface of chicken skin using bacteriophage

BACKGROUND: Enteric infections caused by Salmonella spp. remain a major public health burden worldwide. Chickens are known to be a major reservoir for this zoonotic pathogen. The presence of Salmonella in poultry farms and abattoirs is associated with financial costs of treatment and a serious risk...

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Autores principales: Atterbury, Robert Joseph, Gigante, Adriano Marcelo, Rubio Lozano, María de la Salud, Méndez Medina, Ruben Danilo, Robinson, Gareth, Alloush, Habib, Barrow, Paul Andrew, Allen, Vivien Mary
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7346387/
https://www.ncbi.nlm.nih.gov/pubmed/32646515
http://dx.doi.org/10.1186/s12985-020-01368-0
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author Atterbury, Robert Joseph
Gigante, Adriano Marcelo
Rubio Lozano, María de la Salud
Méndez Medina, Ruben Danilo
Robinson, Gareth
Alloush, Habib
Barrow, Paul Andrew
Allen, Vivien Mary
author_facet Atterbury, Robert Joseph
Gigante, Adriano Marcelo
Rubio Lozano, María de la Salud
Méndez Medina, Ruben Danilo
Robinson, Gareth
Alloush, Habib
Barrow, Paul Andrew
Allen, Vivien Mary
author_sort Atterbury, Robert Joseph
collection PubMed
description BACKGROUND: Enteric infections caused by Salmonella spp. remain a major public health burden worldwide. Chickens are known to be a major reservoir for this zoonotic pathogen. The presence of Salmonella in poultry farms and abattoirs is associated with financial costs of treatment and a serious risk to human health. The use of bacteriophages as a biocontrol is one possible intervention by which Salmonella colonization of chickens could be reduced. In a prior study, phages Eϕ151 and Tϕ7 significantly reduced broiler chicken caecal colonization by S. Enteritidis and S. Typhimurium respectively. METHODS: Salmonella-free Ross broiler chickens were orally infected with S. Enteritidis P125109 or S. Typhimurium 4/74. After 7 days of infection, the animals were euthanased, and 25cm(2) sections of skin were collected. The skin samples were sprayed with a phage suspension of either Eϕ151 (S. Enteritidis), Tϕ7 phage suspension (S. Typhimurium) or SM buffer (Control). After incubation, the number of surviving Salmonellas was determined by direct plating and Most Probable Number (MPN). To determine the rate of reduction of Salmonella numbers on the skin surface, a bioluminescent S. Typhimurium DT104 strain was cultured, spread on sections of chicken breast skin, and after spraying with a Tϕ11 phage suspension, skin samples were monitored using photon counting for up to 24 h. RESULTS: The median levels of Salmonella reduction following phage treatment were 1.38 log(10) MPN (Enteritidis) and 1.83 log(10) MPN (Typhimurium) per skin section. Treatment reductions were significant when compared with Salmonella recovery from control skin sections treated with buffer (p < 0.0001). Additionally, significant reduction in light intensity was observed within 1 min of phage Tϕ11 spraying onto the skin contaminated with a bioluminescent Salmonella recombinant strain, compared with buffer-treated controls (p < 0.01), implying that some lysis of Salmonella was occurring on the skin surface. CONCLUSIONS: The results of this study suggest that phages may be used on the surface of chicken skin as biocontrol agents against Salmonella infected broiler chicken carcasses. The rate of bioluminescence reduction shown by the recombinant Salmonella strain used supported the hypothesis that at least some of the reduction observed was due to lysis occurred on the skin surface.
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spelling pubmed-73463872020-07-14 Reduction of Salmonella contamination on the surface of chicken skin using bacteriophage Atterbury, Robert Joseph Gigante, Adriano Marcelo Rubio Lozano, María de la Salud Méndez Medina, Ruben Danilo Robinson, Gareth Alloush, Habib Barrow, Paul Andrew Allen, Vivien Mary Virol J Research BACKGROUND: Enteric infections caused by Salmonella spp. remain a major public health burden worldwide. Chickens are known to be a major reservoir for this zoonotic pathogen. The presence of Salmonella in poultry farms and abattoirs is associated with financial costs of treatment and a serious risk to human health. The use of bacteriophages as a biocontrol is one possible intervention by which Salmonella colonization of chickens could be reduced. In a prior study, phages Eϕ151 and Tϕ7 significantly reduced broiler chicken caecal colonization by S. Enteritidis and S. Typhimurium respectively. METHODS: Salmonella-free Ross broiler chickens were orally infected with S. Enteritidis P125109 or S. Typhimurium 4/74. After 7 days of infection, the animals were euthanased, and 25cm(2) sections of skin were collected. The skin samples were sprayed with a phage suspension of either Eϕ151 (S. Enteritidis), Tϕ7 phage suspension (S. Typhimurium) or SM buffer (Control). After incubation, the number of surviving Salmonellas was determined by direct plating and Most Probable Number (MPN). To determine the rate of reduction of Salmonella numbers on the skin surface, a bioluminescent S. Typhimurium DT104 strain was cultured, spread on sections of chicken breast skin, and after spraying with a Tϕ11 phage suspension, skin samples were monitored using photon counting for up to 24 h. RESULTS: The median levels of Salmonella reduction following phage treatment were 1.38 log(10) MPN (Enteritidis) and 1.83 log(10) MPN (Typhimurium) per skin section. Treatment reductions were significant when compared with Salmonella recovery from control skin sections treated with buffer (p < 0.0001). Additionally, significant reduction in light intensity was observed within 1 min of phage Tϕ11 spraying onto the skin contaminated with a bioluminescent Salmonella recombinant strain, compared with buffer-treated controls (p < 0.01), implying that some lysis of Salmonella was occurring on the skin surface. CONCLUSIONS: The results of this study suggest that phages may be used on the surface of chicken skin as biocontrol agents against Salmonella infected broiler chicken carcasses. The rate of bioluminescence reduction shown by the recombinant Salmonella strain used supported the hypothesis that at least some of the reduction observed was due to lysis occurred on the skin surface. BioMed Central 2020-07-09 /pmc/articles/PMC7346387/ /pubmed/32646515 http://dx.doi.org/10.1186/s12985-020-01368-0 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Atterbury, Robert Joseph
Gigante, Adriano Marcelo
Rubio Lozano, María de la Salud
Méndez Medina, Ruben Danilo
Robinson, Gareth
Alloush, Habib
Barrow, Paul Andrew
Allen, Vivien Mary
Reduction of Salmonella contamination on the surface of chicken skin using bacteriophage
title Reduction of Salmonella contamination on the surface of chicken skin using bacteriophage
title_full Reduction of Salmonella contamination on the surface of chicken skin using bacteriophage
title_fullStr Reduction of Salmonella contamination on the surface of chicken skin using bacteriophage
title_full_unstemmed Reduction of Salmonella contamination on the surface of chicken skin using bacteriophage
title_short Reduction of Salmonella contamination on the surface of chicken skin using bacteriophage
title_sort reduction of salmonella contamination on the surface of chicken skin using bacteriophage
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7346387/
https://www.ncbi.nlm.nih.gov/pubmed/32646515
http://dx.doi.org/10.1186/s12985-020-01368-0
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