Antibiotic exposure prevents acquisition of beneficial metabolic functions in the preterm infant gut microbiome
Abstract Background Aberrations in the preterm microbiome following antibiotic therapy have been reported in previous studies. The objective of this study was to probe potential underlying mechanisms between this observation and susceptibility to adverse prematurity-related outcomes. Results Metagen...
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| Format: | Article |
| Language: | English |
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BMC
2022-07-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-022-01300-4 |
| _version_ | 1828760100180852736 |
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| author | Yanping Xu Olivia Milburn Traci Beiersdorfer Lizhong Du Henry Akinbi David B. Haslam |
| author_facet | Yanping Xu Olivia Milburn Traci Beiersdorfer Lizhong Du Henry Akinbi David B. Haslam |
| author_sort | Yanping Xu |
| collection | DOAJ |
| description | Abstract Background Aberrations in the preterm microbiome following antibiotic therapy have been reported in previous studies. The objective of this study was to probe potential underlying mechanisms between this observation and susceptibility to adverse prematurity-related outcomes. Results Metagenomic shotgun sequencing was performed on 133 stool and 253 skin samples collected at 1 and 3 weeks of age from 68 infants born at <36 weeks postmenstrual age and birth weight <2000 g. After accounting for gestational age and maternal antibiotics, the distribution of organisms in all samples and the corresponding metabolic pathway abundance were compared between infants exposed to postnatal antibiotics and antibiotics-naïve infants. In antibiotic-naïve infants, gestational and postnatal age imparted similar trajectories on maturation of the microbial community and associated metabolic functional capacity, with postnatal age exerting greater contribution. Antibiotic exposure was associated with reversal in maturation trajectory from the first week to the third week of age (p< 0.001). Butyrate-producing genera, including Clostridium and Blautia, were significantly more abundant in antibiotic-naïve neonates at 3 weeks postnatal age. Correspondingly, metabolic pathways required for short-chain fatty acid synthesis were significantly increased in antibiotic-naïve infants, but not in antibiotic-exposed neonates, at 3 weeks after birth. Conclusions Early brief antibiotic exposure markedly disrupts developmental trajectory of the neonatal microbiome and its corresponding functional capacity. Our findings may provide a mechanistic explanation for the known associations between antibiotic use and adverse outcomes in preterm infants. Video Abstract |
| first_indexed | 2024-12-11T01:08:49Z |
| format | Article |
| id | doaj.art-7f48219bbd124f648f203244b26d896c |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-11T01:08:49Z |
| publishDate | 2022-07-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-7f48219bbd124f648f203244b26d896c2022-12-22T01:26:06ZengBMCMicrobiome2049-26182022-07-0110111510.1186/s40168-022-01300-4Antibiotic exposure prevents acquisition of beneficial metabolic functions in the preterm infant gut microbiomeYanping Xu0Olivia Milburn1Traci Beiersdorfer2Lizhong Du3Henry Akinbi4David B. Haslam5The Children’s Hospital, Zhejiang University School of MedicineDivision of Infectious Diseases, Cincinnati Children’s Hospital Medical CenterPerinatal Institute, CCHMCThe Children’s Hospital, Zhejiang University School of MedicinePerinatal Institute, CCHMCDivision of Infectious Diseases, Cincinnati Children’s Hospital Medical CenterAbstract Background Aberrations in the preterm microbiome following antibiotic therapy have been reported in previous studies. The objective of this study was to probe potential underlying mechanisms between this observation and susceptibility to adverse prematurity-related outcomes. Results Metagenomic shotgun sequencing was performed on 133 stool and 253 skin samples collected at 1 and 3 weeks of age from 68 infants born at <36 weeks postmenstrual age and birth weight <2000 g. After accounting for gestational age and maternal antibiotics, the distribution of organisms in all samples and the corresponding metabolic pathway abundance were compared between infants exposed to postnatal antibiotics and antibiotics-naïve infants. In antibiotic-naïve infants, gestational and postnatal age imparted similar trajectories on maturation of the microbial community and associated metabolic functional capacity, with postnatal age exerting greater contribution. Antibiotic exposure was associated with reversal in maturation trajectory from the first week to the third week of age (p< 0.001). Butyrate-producing genera, including Clostridium and Blautia, were significantly more abundant in antibiotic-naïve neonates at 3 weeks postnatal age. Correspondingly, metabolic pathways required for short-chain fatty acid synthesis were significantly increased in antibiotic-naïve infants, but not in antibiotic-exposed neonates, at 3 weeks after birth. Conclusions Early brief antibiotic exposure markedly disrupts developmental trajectory of the neonatal microbiome and its corresponding functional capacity. Our findings may provide a mechanistic explanation for the known associations between antibiotic use and adverse outcomes in preterm infants. Video Abstracthttps://doi.org/10.1186/s40168-022-01300-4AntibioticsMetagenomic shotgun sequencingMicrobiomeNeonatePreterm |
| spellingShingle | Yanping Xu Olivia Milburn Traci Beiersdorfer Lizhong Du Henry Akinbi David B. Haslam Antibiotic exposure prevents acquisition of beneficial metabolic functions in the preterm infant gut microbiome Microbiome Antibiotics Metagenomic shotgun sequencing Microbiome Neonate Preterm |
| title | Antibiotic exposure prevents acquisition of beneficial metabolic functions in the preterm infant gut microbiome |
| title_full | Antibiotic exposure prevents acquisition of beneficial metabolic functions in the preterm infant gut microbiome |
| title_fullStr | Antibiotic exposure prevents acquisition of beneficial metabolic functions in the preterm infant gut microbiome |
| title_full_unstemmed | Antibiotic exposure prevents acquisition of beneficial metabolic functions in the preterm infant gut microbiome |
| title_short | Antibiotic exposure prevents acquisition of beneficial metabolic functions in the preterm infant gut microbiome |
| title_sort | antibiotic exposure prevents acquisition of beneficial metabolic functions in the preterm infant gut microbiome |
| topic | Antibiotics Metagenomic shotgun sequencing Microbiome Neonate Preterm |
| url | https://doi.org/10.1186/s40168-022-01300-4 |
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