Antibiotic Administration Routes and Oral Exposure to Antibiotic Resistant Bacteria as Key Drivers for Gut Microbiota Disruption and Resistome in Poultry
Previous studies have identified oral administration of antibiotics and gut-impacting drugs as critical drivers for fecal antibiotic resistance (AR) and microbiome disruption in lab mice, but the practical implications of these findings have yet to be validated in hosts nurtured in conventional envi...
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Frontiers Media S.A.
2020-07-01
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Series: | Frontiers in Microbiology |
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Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.01319/full |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Yang Zhou Yang Zhou Yu Li Lu Zhang Lu Zhang Zuowei Wu Ying Huang Ying Huang He Yan He Yan Jiang Zhong Li-Ju Wang Hafiz M. Abdullah Hua H. Wang Hua H. Wang |
spellingShingle |
Yang Zhou Yang Zhou Yu Li Lu Zhang Lu Zhang Zuowei Wu Ying Huang Ying Huang He Yan He Yan Jiang Zhong Li-Ju Wang Hafiz M. Abdullah Hua H. Wang Hua H. Wang Antibiotic Administration Routes and Oral Exposure to Antibiotic Resistant Bacteria as Key Drivers for Gut Microbiota Disruption and Resistome in Poultry Frontiers in Microbiology antibiotic administration routes oral injection poultry resistome |
author_facet |
Yang Zhou Yang Zhou Yu Li Lu Zhang Lu Zhang Zuowei Wu Ying Huang Ying Huang He Yan He Yan Jiang Zhong Li-Ju Wang Hafiz M. Abdullah Hua H. Wang Hua H. Wang |
author_sort |
Yang Zhou |
title |
Antibiotic Administration Routes and Oral Exposure to Antibiotic Resistant Bacteria as Key Drivers for Gut Microbiota Disruption and Resistome in Poultry |
title_short |
Antibiotic Administration Routes and Oral Exposure to Antibiotic Resistant Bacteria as Key Drivers for Gut Microbiota Disruption and Resistome in Poultry |
title_full |
Antibiotic Administration Routes and Oral Exposure to Antibiotic Resistant Bacteria as Key Drivers for Gut Microbiota Disruption and Resistome in Poultry |
title_fullStr |
Antibiotic Administration Routes and Oral Exposure to Antibiotic Resistant Bacteria as Key Drivers for Gut Microbiota Disruption and Resistome in Poultry |
title_full_unstemmed |
Antibiotic Administration Routes and Oral Exposure to Antibiotic Resistant Bacteria as Key Drivers for Gut Microbiota Disruption and Resistome in Poultry |
title_sort |
antibiotic administration routes and oral exposure to antibiotic resistant bacteria as key drivers for gut microbiota disruption and resistome in poultry |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2020-07-01 |
description |
Previous studies have identified oral administration of antibiotics and gut-impacting drugs as critical drivers for fecal antibiotic resistance (AR) and microbiome disruption in lab mice, but the practical implications of these findings have yet to be validated in hosts nurtured in conventional environment. Using ampicillin (Amp) as a way to extrapolate the general effect of antibiotics, this project examined the impact of drug administration routes on fecal microbiota and resistome using poultry raised in a teaching farm. AR genes were found to be abundant in the feces of young Leghorn chicks without previous antibiotic treatment. In chickens seeded with blaCMY–2+Escherichia coli, 300 mg/kg body weight of Amp was orally administered for 5 days. This led to the fecal microbiota switching from Firmicutes occupied (95.60 ± 2.62%) and Lactobacillus rich, to being dominated by Proteobacteria (70.91 ± 28.93%), especially Escherichia/Shigella. However, when Amp was given via muscle injection, Firmicutes was mostly retained (i.e., from 83.6 ± 24.4% pre- to 90.4 ± 15.2% post-treatment). In control chickens without seeding with blaCMY–2+E. coli, oral Amp also led to the increase of Proteobacteria, dominated by Klebsiella and Escherichia/Shigella, and a reduction of Firmicutes. Specifically within Firmicutes, Enterococcus, Clostridium, etc. were enriched but Lactobacillus was diminished. The fecal resistome including Ampr genes was more abundant in chickens receiving oral Amp than those treated with muscle injection, but the difference was primarily within 1 log. The data illustrated that both drug administration routes and pre-existing gut microbiota have profound impacts on gut microbiome disruption when antibiotic treatment is given. In hosts nurtured in a conventional environment, drug administration route has the most evident impact on gut microbiota rather than the size of the targeted blaCMY–2+ gene pool, likely due to the pre-existing bacteria that are (i) less susceptible to Amp, and/or (ii) with Ampr- or multidrug resistance-encoding genes other than blaCMY–2+. These results demonstrated the critical interplay among drug administration routes, microbiota seeded through the gastrointestinal tract, AR, gut microbiota disruption, and the rise of common opportunistic pathogens in hosts. The potential implications in human and animal health are discussed. |
topic |
antibiotic administration routes oral injection poultry resistome |
url |
https://www.frontiersin.org/article/10.3389/fmicb.2020.01319/full |
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doaj-f9fd9cb759e948fb985ca1c35335d3292020-11-25T03:36:32ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-07-011110.3389/fmicb.2020.01319528224Antibiotic Administration Routes and Oral Exposure to Antibiotic Resistant Bacteria as Key Drivers for Gut Microbiota Disruption and Resistome in PoultryYang Zhou0Yang Zhou1Yu Li2Lu Zhang3Lu Zhang4Zuowei Wu5Ying Huang6Ying Huang7He Yan8He Yan9Jiang Zhong10Li-Ju Wang11Hafiz M. Abdullah12Hua H. Wang13Hua H. Wang14Department of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesDepartment of Microbiology, School of Life Sciences, Fudan University, Shanghai, ChinaDepartment of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesDepartment of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesCollege of Food Science and Engineering of Technology, Guangzhou, ChinaCollege of Veterinary Preventive Medicine, Iowa State University, Ames, IA, United StatesDepartment of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesCollege of Food Science, Fujian Agriculture and Forestry University, Fuzhou, ChinaDepartment of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesCollege of Food Science and Engineering of Technology, Guangzhou, ChinaDepartment of Microbiology, School of Life Sciences, Fudan University, Shanghai, ChinaDepartment of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesDepartment of Animal Science Poultry Facility, OARDC, Wooster, OH, United StatesDepartment of Food Science and Technology, The Ohio State University, Columbus, OH, United StatesDepartment of Microbiology, The Ohio State University, Columbus, OH, United StatesPrevious studies have identified oral administration of antibiotics and gut-impacting drugs as critical drivers for fecal antibiotic resistance (AR) and microbiome disruption in lab mice, but the practical implications of these findings have yet to be validated in hosts nurtured in conventional environment. Using ampicillin (Amp) as a way to extrapolate the general effect of antibiotics, this project examined the impact of drug administration routes on fecal microbiota and resistome using poultry raised in a teaching farm. AR genes were found to be abundant in the feces of young Leghorn chicks without previous antibiotic treatment. In chickens seeded with blaCMY–2+Escherichia coli, 300 mg/kg body weight of Amp was orally administered for 5 days. This led to the fecal microbiota switching from Firmicutes occupied (95.60 ± 2.62%) and Lactobacillus rich, to being dominated by Proteobacteria (70.91 ± 28.93%), especially Escherichia/Shigella. However, when Amp was given via muscle injection, Firmicutes was mostly retained (i.e., from 83.6 ± 24.4% pre- to 90.4 ± 15.2% post-treatment). In control chickens without seeding with blaCMY–2+E. coli, oral Amp also led to the increase of Proteobacteria, dominated by Klebsiella and Escherichia/Shigella, and a reduction of Firmicutes. Specifically within Firmicutes, Enterococcus, Clostridium, etc. were enriched but Lactobacillus was diminished. The fecal resistome including Ampr genes was more abundant in chickens receiving oral Amp than those treated with muscle injection, but the difference was primarily within 1 log. The data illustrated that both drug administration routes and pre-existing gut microbiota have profound impacts on gut microbiome disruption when antibiotic treatment is given. In hosts nurtured in a conventional environment, drug administration route has the most evident impact on gut microbiota rather than the size of the targeted blaCMY–2+ gene pool, likely due to the pre-existing bacteria that are (i) less susceptible to Amp, and/or (ii) with Ampr- or multidrug resistance-encoding genes other than blaCMY–2+. These results demonstrated the critical interplay among drug administration routes, microbiota seeded through the gastrointestinal tract, AR, gut microbiota disruption, and the rise of common opportunistic pathogens in hosts. The potential implications in human and animal health are discussed.https://www.frontiersin.org/article/10.3389/fmicb.2020.01319/fullantibioticadministration routesoralinjectionpoultryresistome |