Early-life prophylactic antibiotic treatment disturbs the stability of the gut microbiota and increases susceptibility to H9N2 AIV in chicks
Abstract Background Antibiotics are widely used for prophylactic therapy and for improving the growth performance of chicken. The problem of bacterial drug resistance caused by antibiotic abuse has previously attracted extensive attention; however, the influence of early-day use of prophylactic anti...
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| Format: | Article |
| Language: | English |
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BMC
2023-07-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-023-01609-8 |
| _version_ | 1797769399551131648 |
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| author | Xianghui Liang Zhipeng Zhang Hai Wang Xingbang Lu Wen Li Haoran Lu Ayan Roy Xuejuan Shen David M. Irwin Yongyi Shen |
| author_facet | Xianghui Liang Zhipeng Zhang Hai Wang Xingbang Lu Wen Li Haoran Lu Ayan Roy Xuejuan Shen David M. Irwin Yongyi Shen |
| author_sort | Xianghui Liang |
| collection | DOAJ |
| description | Abstract Background Antibiotics are widely used for prophylactic therapy and for improving the growth performance of chicken. The problem of bacterial drug resistance caused by antibiotic abuse has previously attracted extensive attention; however, the influence of early-day use of prophylactic antibiotics on the gut microflora and on the disease resistance ability in chicks has not been explored. Here, we comprehensively evaluate the growth performance, gut microbial dynamics, level of antibiotic resistance genes (ARGs) in the gut microbial community, and resistance to H9N2 avian influenza virus (AIV) in chickens following long-term and short-term early-day prophylactic antibiotic treatment. Results Unexpectedly, long-term prophylactic enrofloxacin treatment slowed the growth rate of chickens, whereas short-term antibiotics treatments were found to increase the growth rate, but these changes were not statistically significant. Strikingly, expansions of Escherichia-Shigella populations were observed in early-life prophylactic antibiotics-treated groups of chickens, which is in contrast to the general perception that antibiotics should control their pathogenicity in chicks. The gut microbiota composition of chickens treated long term with antibiotics or received early-day antibiotics treatment tend to be more dramatically disturbed compared to the gut microbiome of chickens treated with antibiotics for a short term at a later date, especially after H9N2 AIV infection. Conclusions Our data provide evidence that early-day and long-term antibiotic treatments have a more adverse effect on the intestinal microbiome of chickens, compared to short-term late age antibiotic treatment. Furthermore, our metagenomic data reveal that both long-term and short-term antibiotic treatment increase the relative abundance of ARGs. Our findings highlight the adverse effects of prophylactic antibiotic treatment and provide a theoretical basis for the cautious administration of antibiotics in food-producing animal management. Video Abstract |
| first_indexed | 2024-03-12T21:08:29Z |
| format | Article |
| id | doaj.art-e131595f5564446aa3bb396f204d539c |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-12T21:08:29Z |
| publishDate | 2023-07-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-e131595f5564446aa3bb396f204d539c2023-07-30T11:20:31ZengBMCMicrobiome2049-26182023-07-0111111410.1186/s40168-023-01609-8Early-life prophylactic antibiotic treatment disturbs the stability of the gut microbiota and increases susceptibility to H9N2 AIV in chicksXianghui Liang0Zhipeng Zhang1Hai Wang2Xingbang Lu3Wen Li4Haoran Lu5Ayan Roy6Xuejuan Shen7David M. Irwin8Yongyi Shen9Guangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Animal Disease Control and Prevention, Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural UniversityGuangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Animal Disease Control and Prevention, Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural UniversityGuangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Animal Disease Control and Prevention, Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural UniversityGuangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Animal Disease Control and Prevention, Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural UniversityGuangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Animal Disease Control and Prevention, Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural UniversitySchool of Mathematics, Sun Yat-Sen UniversityMailman School of Public Health, Columbia UniversityGuangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Animal Disease Control and Prevention, Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural UniversityDepartment of Laboratory Medicine and Pathobiology, University of TorontoGuangdong Laboratory for Lingnan Modern Agriculture, State Key Laboratory for Animal Disease Control and Prevention, Center for Emerging and Zoonotic Diseases, College of Veterinary Medicine, South China Agricultural UniversityAbstract Background Antibiotics are widely used for prophylactic therapy and for improving the growth performance of chicken. The problem of bacterial drug resistance caused by antibiotic abuse has previously attracted extensive attention; however, the influence of early-day use of prophylactic antibiotics on the gut microflora and on the disease resistance ability in chicks has not been explored. Here, we comprehensively evaluate the growth performance, gut microbial dynamics, level of antibiotic resistance genes (ARGs) in the gut microbial community, and resistance to H9N2 avian influenza virus (AIV) in chickens following long-term and short-term early-day prophylactic antibiotic treatment. Results Unexpectedly, long-term prophylactic enrofloxacin treatment slowed the growth rate of chickens, whereas short-term antibiotics treatments were found to increase the growth rate, but these changes were not statistically significant. Strikingly, expansions of Escherichia-Shigella populations were observed in early-life prophylactic antibiotics-treated groups of chickens, which is in contrast to the general perception that antibiotics should control their pathogenicity in chicks. The gut microbiota composition of chickens treated long term with antibiotics or received early-day antibiotics treatment tend to be more dramatically disturbed compared to the gut microbiome of chickens treated with antibiotics for a short term at a later date, especially after H9N2 AIV infection. Conclusions Our data provide evidence that early-day and long-term antibiotic treatments have a more adverse effect on the intestinal microbiome of chickens, compared to short-term late age antibiotic treatment. Furthermore, our metagenomic data reveal that both long-term and short-term antibiotic treatment increase the relative abundance of ARGs. Our findings highlight the adverse effects of prophylactic antibiotic treatment and provide a theoretical basis for the cautious administration of antibiotics in food-producing animal management. Video Abstracthttps://doi.org/10.1186/s40168-023-01609-8Prophylactic antibioticChickenGut microbiotaH9N2 influenza virusDisease resistanceAntibiotic resistance genes |
| spellingShingle | Xianghui Liang Zhipeng Zhang Hai Wang Xingbang Lu Wen Li Haoran Lu Ayan Roy Xuejuan Shen David M. Irwin Yongyi Shen Early-life prophylactic antibiotic treatment disturbs the stability of the gut microbiota and increases susceptibility to H9N2 AIV in chicks Microbiome Prophylactic antibiotic Chicken Gut microbiota H9N2 influenza virus Disease resistance Antibiotic resistance genes |
| title | Early-life prophylactic antibiotic treatment disturbs the stability of the gut microbiota and increases susceptibility to H9N2 AIV in chicks |
| title_full | Early-life prophylactic antibiotic treatment disturbs the stability of the gut microbiota and increases susceptibility to H9N2 AIV in chicks |
| title_fullStr | Early-life prophylactic antibiotic treatment disturbs the stability of the gut microbiota and increases susceptibility to H9N2 AIV in chicks |
| title_full_unstemmed | Early-life prophylactic antibiotic treatment disturbs the stability of the gut microbiota and increases susceptibility to H9N2 AIV in chicks |
| title_short | Early-life prophylactic antibiotic treatment disturbs the stability of the gut microbiota and increases susceptibility to H9N2 AIV in chicks |
| title_sort | early life prophylactic antibiotic treatment disturbs the stability of the gut microbiota and increases susceptibility to h9n2 aiv in chicks |
| topic | Prophylactic antibiotic Chicken Gut microbiota H9N2 influenza virus Disease resistance Antibiotic resistance genes |
| url | https://doi.org/10.1186/s40168-023-01609-8 |
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