Early life exposure of infants to benzylpenicillin and gentamicin is associated with a persistent amplification of the gut resistome

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dc.contributor.authorPatangia, Dhratien
dc.contributor.authorGrimaud, Ghjuvanen
dc.contributor.authorO’Shea, Carol-Anneen
dc.contributor.authorRyan, C. A.en
dc.contributor.authorDempsey, Eugene M.en
dc.contributor.authorStanton, Catherineen
dc.contributor.authorRoss, R. Paulen
dc.contributor.funderSeventh Framework Programmeen
dc.contributor.funderScience Foundation Irelanden
dc.contributor.funderDepartment of Agriculture, Food and the Marine, Irelanden
dc.date.accessioned2024-03-21T15:16:38Z
dc.date.available2024-03-21T15:16:38Z
dc.date.issued2024en
dc.description.abstractBackground Infant gut microbiota is highly malleable, but the long-term longitudinal impact of antibiotic exposure in early life, together with the mode of delivery on infant gut microbiota and resistome, is not extensively studied. Methods Two hundred and eight samples from 45 infants collected from birth until 2 years of age over five time points (week 1, 4, 8, 24, year 2) were analysed. Based on shotgun metagenomics, the gut microbial composition and resistome profile were compared in the early life of infants divided into three groups: vaginal delivery/no-antibiotic in the first 4 days of life, C-section/no-antibiotic in the first 4 days of life, and C-section/antibiotic exposed in first 4 days of life. Gentamycin and benzylpenicillin were the most commonly administered antibiotics during this cohort’s first week of life. Results Newborn gut microbial composition differed in all three groups, with higher diversity and stable composition seen at 2 years of age, compared to week 1. An increase in microbial diversity from week 1 to week 4 only in the C-section/antibiotic-exposed group reflects the effect of antibiotic use in the first 4 days of life, with a gradual increase thereafter. Overall, a relative abundance of Actinobacteria and Bacteroides was significantly higher in vaginal delivery/no-antibiotic while Proteobacteria was higher in C-section/antibiotic-exposed infants. Strains from species belonging to Bifidobacterium and Bacteroidetes were generally persistent colonisers, with Bifidobacterium breve and Bifidobacterium bifidum species being the major persistent colonisers in all three groups. Bacteroides persistence was dominant in the vaginal delivery/no-antibiotic group, with species Bacteroides ovatus and Phocaeicola vulgatus found to be persistent colonisers in the no-antibiotic groups. Most strains carrying antibiotic-resistance genes belonged to phyla Proteobacteria and Firmicutes, with the C-section/antibiotic-exposed group presenting a higher frequency of antibiotic-resistance genes (ARGs). Conclusion These data show that antibiotic exposure has an immediate and persistent effect on the gut microbiome in early life. As such, the two antibiotics used in the study selected for strains (mainly Proteobacteria) which were multiple drug-resistant (MDR), presumably a reflection of their evolutionary lineage of historical exposures—leading to what can be an extensive and diverse resistome.en
dc.description.sponsorshipDepartment of Agriculture, Food and the Marine, Ireland (INFANTMET)en
dc.description.statusPeer revieweden
dc.description.versionPublished Versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.citationPatangia, D.V., Grimaud, G., O’Shea, C.-A., Ryan, C.A., Dempsey, E., Stanton, C. and Ross, R.P. (2024) ‘Early life exposure of infants to benzylpenicillin and gentamicin is associated with a persistent amplification of the gut resistome’, Microbiome, 12(19), (20pp). doi: 10.1186/s40168-023-01732-6en
dc.identifier.doi10.1186/s40168-023-01732-6en
dc.identifier.endpage20en
dc.identifier.issued19en
dc.identifier.journaltitleMicrobiomeen
dc.identifier.startpage1en
dc.identifier.urihttps://hdl.handle.net/10468/15692
dc.identifier.volume12en
dc.language.isoenen
dc.publisherBioMed Central Ltden
dc.relation.projectinfo:eu-repo/grantAgreement/EC/FP7::SP1::KBBE/613979/EU/Microbiome Influence on Energy balance and Brain Development-Function Put into Action to Tackle Diet-related Diseases and Behavior./MYNEWGUTen
dc.relation.projectinfo:eu-repo/grantAgreement/EC/HE::ERC::HORIZON-ERC/101054719/EU/Bacteriocins from interbacterial warfare as antibiotic alternative/BACtheWINNERen
dc.rights© The Author(s) 2024. Open Access This 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.en
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/en
dc.subjectInfant guten
dc.subjectGut microbiotaen
dc.subjectShotgun metagenomicsen
dc.subjectResistome profileen
dc.subjectStrain persistenceen
dc.titleEarly life exposure of infants to benzylpenicillin and gentamicin is associated with a persistent amplification of the gut resistomeen
dc.typeArticle (peer-reviewed)en
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