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Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes

Antimicrobial growth promoters (AGPs) are commonly used in broiler production. There is a huge societal concern around their use and their contribution to the proliferation of antimicrobial resistance (AMR) in food-producing animals and dissemination to humans or the environment. However, there is a...

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Autores principales: Paul, Shyam Sundar, Rama Rao, Savaram Venkata, Hegde, Nagendra, Williams, Nicola J., Chatterjee, Rudra Nath, Raju, Mantena Venkata Lakshmi Narasimha, Reddy, Godumagadda Narender, Kumar, Vikas, Phani Kumar, Prakki Santosh, Mallick, Sathi, Gargi, Madhuranjana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9244563/
https://www.ncbi.nlm.nih.gov/pubmed/35783415
http://dx.doi.org/10.3389/fmicb.2022.905050
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author Paul, Shyam Sundar
Rama Rao, Savaram Venkata
Hegde, Nagendra
Williams, Nicola J.
Chatterjee, Rudra Nath
Raju, Mantena Venkata Lakshmi Narasimha
Reddy, Godumagadda Narender
Kumar, Vikas
Phani Kumar, Prakki Santosh
Mallick, Sathi
Gargi, Madhuranjana
author_facet Paul, Shyam Sundar
Rama Rao, Savaram Venkata
Hegde, Nagendra
Williams, Nicola J.
Chatterjee, Rudra Nath
Raju, Mantena Venkata Lakshmi Narasimha
Reddy, Godumagadda Narender
Kumar, Vikas
Phani Kumar, Prakki Santosh
Mallick, Sathi
Gargi, Madhuranjana
author_sort Paul, Shyam Sundar
collection PubMed
description Antimicrobial growth promoters (AGPs) are commonly used in broiler production. There is a huge societal concern around their use and their contribution to the proliferation of antimicrobial resistance (AMR) in food-producing animals and dissemination to humans or the environment. However, there is a paucity of comprehensive experimental data on their impact on poultry production and the AMR resistome. Here, we investigated the effect of five antimicrobial growth promoters (virginiamycin, chlortetracycline, bacitracin methyl disalicylate, lincomycin, and tylosin) used in the commercial broiler production in the Indian subcontinent and in the different parts of the world for three consecutive production cycles on performance variables and also the impact on gut bacteria, bacteriophage, and resistome profile using culture-independent approaches. There was no significant effect of AGPs on the cumulative growth or feed efficiency parameters at the end of the production cycles and cumulative mortality rates were also similar across groups. Many antibiotic resistance genes (ARGs) were ubiquitous in the chicken gut irrespective of AGP supplementation. In total, 62 ARGs from 15 antimicrobial classes were detected. Supplementation of AGPs influenced the selection of several classes of ARGs; however, this was not correlated necessarily with genes relevant to the AGP drug class; some AGPs favored the selection of ARGs related to antimicrobials not structurally related to the AGP. AGPs did not impact the gut bacterial community structure, including alpha or beta diversity significantly, with only 16–20 operational taxonomic units (OTUs) of bacteria being altered significantly. However, several AGPs significantly reduced the population density of some of the potential pathogenic genera of bacteria, such as Escherichia coli. Chlortetracycline increased the abundance of Escherichia phage, whereas other AGPs did not influence the abundance of bacteriophage significantly. Considering the evidence that AGPs used in poultry production can select for resistance to more than one class of antimicrobial resistance, and the fact that their effect on performance is not significant, their use needs to be reduced and there is a need to monitor the spread of ARGs in broiler chicken farms.
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spelling pubmed-92445632022-07-01 Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes Paul, Shyam Sundar Rama Rao, Savaram Venkata Hegde, Nagendra Williams, Nicola J. Chatterjee, Rudra Nath Raju, Mantena Venkata Lakshmi Narasimha Reddy, Godumagadda Narender Kumar, Vikas Phani Kumar, Prakki Santosh Mallick, Sathi Gargi, Madhuranjana Front Microbiol Microbiology Antimicrobial growth promoters (AGPs) are commonly used in broiler production. There is a huge societal concern around their use and their contribution to the proliferation of antimicrobial resistance (AMR) in food-producing animals and dissemination to humans or the environment. However, there is a paucity of comprehensive experimental data on their impact on poultry production and the AMR resistome. Here, we investigated the effect of five antimicrobial growth promoters (virginiamycin, chlortetracycline, bacitracin methyl disalicylate, lincomycin, and tylosin) used in the commercial broiler production in the Indian subcontinent and in the different parts of the world for three consecutive production cycles on performance variables and also the impact on gut bacteria, bacteriophage, and resistome profile using culture-independent approaches. There was no significant effect of AGPs on the cumulative growth or feed efficiency parameters at the end of the production cycles and cumulative mortality rates were also similar across groups. Many antibiotic resistance genes (ARGs) were ubiquitous in the chicken gut irrespective of AGP supplementation. In total, 62 ARGs from 15 antimicrobial classes were detected. Supplementation of AGPs influenced the selection of several classes of ARGs; however, this was not correlated necessarily with genes relevant to the AGP drug class; some AGPs favored the selection of ARGs related to antimicrobials not structurally related to the AGP. AGPs did not impact the gut bacterial community structure, including alpha or beta diversity significantly, with only 16–20 operational taxonomic units (OTUs) of bacteria being altered significantly. However, several AGPs significantly reduced the population density of some of the potential pathogenic genera of bacteria, such as Escherichia coli. Chlortetracycline increased the abundance of Escherichia phage, whereas other AGPs did not influence the abundance of bacteriophage significantly. Considering the evidence that AGPs used in poultry production can select for resistance to more than one class of antimicrobial resistance, and the fact that their effect on performance is not significant, their use needs to be reduced and there is a need to monitor the spread of ARGs in broiler chicken farms. Frontiers Media S.A. 2022-06-16 /pmc/articles/PMC9244563/ /pubmed/35783415 http://dx.doi.org/10.3389/fmicb.2022.905050 Text en Copyright © 2022 Paul, Rama Rao, Hegde, Williams, Chatterjee, Raju, Reddy, Kumar, Phani Kumar, Mallick and Gargi. 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
Paul, Shyam Sundar
Rama Rao, Savaram Venkata
Hegde, Nagendra
Williams, Nicola J.
Chatterjee, Rudra Nath
Raju, Mantena Venkata Lakshmi Narasimha
Reddy, Godumagadda Narender
Kumar, Vikas
Phani Kumar, Prakki Santosh
Mallick, Sathi
Gargi, Madhuranjana
Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes
title Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes
title_full Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes
title_fullStr Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes
title_full_unstemmed Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes
title_short Effects of Dietary Antimicrobial Growth Promoters on Performance Parameters and Abundance and Diversity of Broiler Chicken Gut Microbiome and Selection of Antibiotic Resistance Genes
title_sort effects of dietary antimicrobial growth promoters on performance parameters and abundance and diversity of broiler chicken gut microbiome and selection of antibiotic resistance genes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9244563/
https://www.ncbi.nlm.nih.gov/pubmed/35783415
http://dx.doi.org/10.3389/fmicb.2022.905050
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