Effect of Single Dose of Antimicrobial Administration at Birth on Fecal Microbiota Development and Prevalence of Antimicrobial Resistance Genes in Piglets
Optimization of antimicrobial use in swine management systems requires full understanding of antimicrobial-induced changes on the developmental dynamics of gut microbiota and the prevalence of antimicrobial resistance genes (ARGs). The purpose of this study was to evaluate the impacts of early life...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-06-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.01414/full |
| _version_ | 1818062122055106560 |
|---|---|
| author | Mohamed Zeineldin Mohamed Zeineldin Mohamed Zeineldin Ameer Megahed Ameer Megahed Brandi Burton Benjamin Blair Brian Aldridge James F. Lowe |
| author_facet | Mohamed Zeineldin Mohamed Zeineldin Mohamed Zeineldin Ameer Megahed Ameer Megahed Brandi Burton Benjamin Blair Brian Aldridge James F. Lowe |
| author_sort | Mohamed Zeineldin |
| collection | DOAJ |
| description | Optimization of antimicrobial use in swine management systems requires full understanding of antimicrobial-induced changes on the developmental dynamics of gut microbiota and the prevalence of antimicrobial resistance genes (ARGs). The purpose of this study was to evaluate the impacts of early life antimicrobial intervention on fecal microbiota development, and prevalence of selected ARGs (ermB, tetO, tetW, tetC, sulI, sulII, and blaCTX–M) in neonatal piglets. A total of 48 litters were randomly allocated into one of six treatment groups soon after birth. Treatments were as follows: control (CONT), ceftiofur crystalline free acid (CCFA), ceftiofur hydrochloride (CHC), oxytetracycline (OTC), procaine penicillin G (PPG), and tulathromycin (TUL). Fecal swabs were collected from piglets at days 0 (prior to treatment), 5, 10, 15, and 20 post treatment. Sequencing analysis of the V3-V4 hypervariable region of the 16S rRNA gene and selected ARGs were performed using the Illumina Miseq platform. Our results showed that, while early life antimicrobial prophylaxis had no effect on individual weight gain, or mortality, it was associated with minor shifts in the composition of fecal microbiota and noticeable changes in the abundance of selected ARGs. Unifrac distance metrics revealed that the microbial communities of the piglets that received different treatments (CCFA, CHC, OTC, PPG, and TUL) did not cluster distinctly from CONT piglets. Compared to CONT group, PPG-treated piglets exhibited a significant increase in the relative abundance of ermB and tetW at day 20 of life. Tulathromycin treatment also resulted in a significant increase in the abundance of tetW at days 10 and 20, and ermB at day 20. Collectively, these results demonstrate that the shifts in fecal microbiota structure caused by perinatal antimicrobial intervention are modest and limited to particular groups of microbial taxa. However, early life PPG and TUL intervention could promote the selection of ARGs in herds. While additional investigations are required to explore the consistency of these findings across larger populations, these results could open the door to new perspectives on the utility of early life antimicrobial administration to healthy neonates in swine management systems. |
| first_indexed | 2024-12-10T13:59:11Z |
| format | Article |
| id | doaj.art-3776eccdb06840bbbe7b838739b96a9f |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-10T13:59:11Z |
| publishDate | 2019-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-3776eccdb06840bbbe7b838739b96a9f2022-12-22T01:45:50ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-06-011010.3389/fmicb.2019.01414449153Effect of Single Dose of Antimicrobial Administration at Birth on Fecal Microbiota Development and Prevalence of Antimicrobial Resistance Genes in PigletsMohamed Zeineldin0Mohamed Zeineldin1Mohamed Zeineldin2Ameer Megahed3Ameer Megahed4Brandi Burton5Benjamin Blair6Brian Aldridge7James F. Lowe8Integrated Food Animal Management Systems, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois at Urbana–Champaign, Champaign, IL, United StatesDepartment of Animal Medicine, College of Veterinary Medicine, Benha University, Benha, EgyptInfectious Genomic of One Health, Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana–Champaign, Champaign, IL, United StatesIntegrated Food Animal Management Systems, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois at Urbana–Champaign, Champaign, IL, United StatesDepartment of Animal Medicine, College of Veterinary Medicine, Benha University, Benha, EgyptIntegrated Food Animal Management Systems, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois at Urbana–Champaign, Champaign, IL, United StatesIntegrated Food Animal Management Systems, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois at Urbana–Champaign, Champaign, IL, United StatesIntegrated Food Animal Management Systems, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois at Urbana–Champaign, Champaign, IL, United StatesIntegrated Food Animal Management Systems, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois at Urbana–Champaign, Champaign, IL, United StatesOptimization of antimicrobial use in swine management systems requires full understanding of antimicrobial-induced changes on the developmental dynamics of gut microbiota and the prevalence of antimicrobial resistance genes (ARGs). The purpose of this study was to evaluate the impacts of early life antimicrobial intervention on fecal microbiota development, and prevalence of selected ARGs (ermB, tetO, tetW, tetC, sulI, sulII, and blaCTX–M) in neonatal piglets. A total of 48 litters were randomly allocated into one of six treatment groups soon after birth. Treatments were as follows: control (CONT), ceftiofur crystalline free acid (CCFA), ceftiofur hydrochloride (CHC), oxytetracycline (OTC), procaine penicillin G (PPG), and tulathromycin (TUL). Fecal swabs were collected from piglets at days 0 (prior to treatment), 5, 10, 15, and 20 post treatment. Sequencing analysis of the V3-V4 hypervariable region of the 16S rRNA gene and selected ARGs were performed using the Illumina Miseq platform. Our results showed that, while early life antimicrobial prophylaxis had no effect on individual weight gain, or mortality, it was associated with minor shifts in the composition of fecal microbiota and noticeable changes in the abundance of selected ARGs. Unifrac distance metrics revealed that the microbial communities of the piglets that received different treatments (CCFA, CHC, OTC, PPG, and TUL) did not cluster distinctly from CONT piglets. Compared to CONT group, PPG-treated piglets exhibited a significant increase in the relative abundance of ermB and tetW at day 20 of life. Tulathromycin treatment also resulted in a significant increase in the abundance of tetW at days 10 and 20, and ermB at day 20. Collectively, these results demonstrate that the shifts in fecal microbiota structure caused by perinatal antimicrobial intervention are modest and limited to particular groups of microbial taxa. However, early life PPG and TUL intervention could promote the selection of ARGs in herds. While additional investigations are required to explore the consistency of these findings across larger populations, these results could open the door to new perspectives on the utility of early life antimicrobial administration to healthy neonates in swine management systems.https://www.frontiersin.org/article/10.3389/fmicb.2019.01414/fullantimicrobialmicrobiotaneonatal pigletsresistance genesfecal |
| spellingShingle | Mohamed Zeineldin Mohamed Zeineldin Mohamed Zeineldin Ameer Megahed Ameer Megahed Brandi Burton Benjamin Blair Brian Aldridge James F. Lowe Effect of Single Dose of Antimicrobial Administration at Birth on Fecal Microbiota Development and Prevalence of Antimicrobial Resistance Genes in Piglets Frontiers in Microbiology antimicrobial microbiota neonatal piglets resistance genes fecal |
| title | Effect of Single Dose of Antimicrobial Administration at Birth on Fecal Microbiota Development and Prevalence of Antimicrobial Resistance Genes in Piglets |
| title_full | Effect of Single Dose of Antimicrobial Administration at Birth on Fecal Microbiota Development and Prevalence of Antimicrobial Resistance Genes in Piglets |
| title_fullStr | Effect of Single Dose of Antimicrobial Administration at Birth on Fecal Microbiota Development and Prevalence of Antimicrobial Resistance Genes in Piglets |
| title_full_unstemmed | Effect of Single Dose of Antimicrobial Administration at Birth on Fecal Microbiota Development and Prevalence of Antimicrobial Resistance Genes in Piglets |
| title_short | Effect of Single Dose of Antimicrobial Administration at Birth on Fecal Microbiota Development and Prevalence of Antimicrobial Resistance Genes in Piglets |
| title_sort | effect of single dose of antimicrobial administration at birth on fecal microbiota development and prevalence of antimicrobial resistance genes in piglets |
| topic | antimicrobial microbiota neonatal piglets resistance genes fecal |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.01414/full |
| work_keys_str_mv | AT mohamedzeineldin effectofsingledoseofantimicrobialadministrationatbirthonfecalmicrobiotadevelopmentandprevalenceofantimicrobialresistancegenesinpiglets AT mohamedzeineldin effectofsingledoseofantimicrobialadministrationatbirthonfecalmicrobiotadevelopmentandprevalenceofantimicrobialresistancegenesinpiglets AT mohamedzeineldin effectofsingledoseofantimicrobialadministrationatbirthonfecalmicrobiotadevelopmentandprevalenceofantimicrobialresistancegenesinpiglets AT ameermegahed effectofsingledoseofantimicrobialadministrationatbirthonfecalmicrobiotadevelopmentandprevalenceofantimicrobialresistancegenesinpiglets AT ameermegahed effectofsingledoseofantimicrobialadministrationatbirthonfecalmicrobiotadevelopmentandprevalenceofantimicrobialresistancegenesinpiglets AT brandiburton effectofsingledoseofantimicrobialadministrationatbirthonfecalmicrobiotadevelopmentandprevalenceofantimicrobialresistancegenesinpiglets AT benjaminblair effectofsingledoseofantimicrobialadministrationatbirthonfecalmicrobiotadevelopmentandprevalenceofantimicrobialresistancegenesinpiglets AT brianaldridge effectofsingledoseofantimicrobialadministrationatbirthonfecalmicrobiotadevelopmentandprevalenceofantimicrobialresistancegenesinpiglets AT jamesflowe effectofsingledoseofantimicrobialadministrationatbirthonfecalmicrobiotadevelopmentandprevalenceofantimicrobialresistancegenesinpiglets |