Development of the preterm gut microbiome in twins at risk of necrotising enterocolitis and sepsis
The preterm gut microbiome is a complex dynamic community influenced by genetic and environmental factors and is implicated in the pathogenesis of necrotising enterocolitis (NEC) and sepsis. We aimed to explore the longitudinal development of the gut microbiome in preterm twins to determine how shar...
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| description | The preterm gut microbiome is a complex dynamic community influenced by genetic and environmental factors and is implicated in the pathogenesis of necrotising enterocolitis (NEC) and sepsis. We aimed to explore the longitudinal development of the gut microbiome in preterm twins to determine how shared environmental and genetic factors may influence temporal changes and compared this to the expressed breast milk (EBM) microbiome. Stool samples (n = 173) from 27 infants (12 twin pairs and 1 triplet set) and EBM (n = 18) from 4 mothers were collected longitudinally. All samples underwent PCR-DGGE (denaturing gradient gel electrophoresis) analysis and a selected subset underwent 454 pyrosequencing. Stool and EBM shared a core microbiome dominated by Enterobacteriaceae, Enterococcaceae, and Staphylococcaceae. The gut microbiome showed greater similarity between siblings compared to unrelated individuals. Pyrosequencing revealed a reduction in diversity and increasing dominance of Escherichia sp. preceding NEC that was not observed in the healthy twin. Antibiotic treatment had a substantial effect on the gut microbiome, reducing Escherichia sp. and increasing other Enterobacteriaceae. This study demonstrates related preterm twins share similar gut microbiome development, even within the complex environment of neonatal intensive care. This is likely a result of shared genetic and immunomodulatory factors as well as exposure to the same maternal microbiome during birth, skin contact and exposure to EBM. Environmental factors including antibiotic exposure and feeding are additional significant determinants of community structure, regardless of host genetics. |
| doi_str_mv | 10.1371/journal.pone.0073465 |
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We aimed to explore the longitudinal development of the gut microbiome in preterm twins to determine how shared environmental and genetic factors may influence temporal changes and compared this to the expressed breast milk (EBM) microbiome. Stool samples (n = 173) from 27 infants (12 twin pairs and 1 triplet set) and EBM (n = 18) from 4 mothers were collected longitudinally. All samples underwent PCR-DGGE (denaturing gradient gel electrophoresis) analysis and a selected subset underwent 454 pyrosequencing. Stool and EBM shared a core microbiome dominated by Enterobacteriaceae, Enterococcaceae, and Staphylococcaceae. The gut microbiome showed greater similarity between siblings compared to unrelated individuals. Pyrosequencing revealed a reduction in diversity and increasing dominance of Escherichia sp. preceding NEC that was not observed in the healthy twin. Antibiotic treatment had a substantial effect on the gut microbiome, reducing Escherichia sp. and increasing other Enterobacteriaceae. This study demonstrates related preterm twins share similar gut microbiome development, even within the complex environment of neonatal intensive care. This is likely a result of shared genetic and immunomodulatory factors as well as exposure to the same maternal microbiome during birth, skin contact and exposure to EBM. Environmental factors including antibiotic exposure and feeding are additional significant determinants of community structure, regardless of host genetics.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0073465</identifier><identifier>PMID: 24023682</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Antibiotics ; Babies ; Bacteria - growth & development ; Breast milk ; Breastfeeding & lactation ; Childbirth & labor ; Communities ; Community structure ; Demography ; Deoxyribonucleic acid ; Digestive system ; Disease ; DNA ; E coli ; Enterocolitis ; Enterocolitis, Necrotizing - microbiology ; Enterocolitis, Necrotizing - pathology ; Environmental changes ; Environmental factors ; Escherichia coli ; Exposure ; Feces - microbiology ; Female ; Gastroenterology ; Gastrointestinal diseases ; Gastrointestinal Tract - microbiology ; Gastrointestinal Tract - pathology ; Gel electrophoresis ; Genetic factors ; Genetics ; Hospitals ; Humans ; Immunomodulation ; Infant, Newborn ; Infants ; Infections ; Inflammatory bowel disease ; Intestinal microflora ; Life sciences ; Male ; Microbiota ; Milk ; Milk, Human - microbiology ; Multiple births ; Necrosis ; Neonates ; Newborn babies ; Pathogenesis ; Phylogenetics ; Premature Birth - microbiology ; Risk Factors ; Sepsis ; Sepsis - microbiology ; Sepsis - pathology ; Siblings ; Skin ; Twins</subject><ispartof>PloS one, 2013-08, Vol.8 (8), p.e73465</ispartof><rights>2013 Stewart et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Stewart et al 2013 Stewart et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-11eed5e983716bbc837b69d39e879fc107c344a5ad4e7096f2708b665d1a20903</citedby><cites>FETCH-LOGICAL-c526t-11eed5e983716bbc837b69d39e879fc107c344a5ad4e7096f2708b665d1a20903</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3758342/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3758342/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24023682$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Sanz, Yolanda</contributor><creatorcontrib>Stewart, Christopher J</creatorcontrib><creatorcontrib>Marrs, Emma C L</creatorcontrib><creatorcontrib>Nelson, Andrew</creatorcontrib><creatorcontrib>Lanyon, Clare</creatorcontrib><creatorcontrib>Perry, John D</creatorcontrib><creatorcontrib>Embleton, Nicholas D</creatorcontrib><creatorcontrib>Cummings, Stephen P</creatorcontrib><creatorcontrib>Berrington, Janet E</creatorcontrib><title>Development of the preterm gut microbiome in twins at risk of necrotising enterocolitis and sepsis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The preterm gut microbiome is a complex dynamic community influenced by genetic and environmental factors and is implicated in the pathogenesis of necrotising enterocolitis (NEC) and sepsis. 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Antibiotic treatment had a substantial effect on the gut microbiome, reducing Escherichia sp. and increasing other Enterobacteriaceae. This study demonstrates related preterm twins share similar gut microbiome development, even within the complex environment of neonatal intensive care. This is likely a result of shared genetic and immunomodulatory factors as well as exposure to the same maternal microbiome during birth, skin contact and exposure to EBM. Environmental factors including antibiotic exposure and feeding are additional significant determinants of community structure, regardless of host genetics.</description><subject>Antibiotics</subject><subject>Babies</subject><subject>Bacteria - growth & development</subject><subject>Breast milk</subject><subject>Breastfeeding & lactation</subject><subject>Childbirth & labor</subject><subject>Communities</subject><subject>Community structure</subject><subject>Demography</subject><subject>Deoxyribonucleic acid</subject><subject>Digestive system</subject><subject>Disease</subject><subject>DNA</subject><subject>E coli</subject><subject>Enterocolitis</subject><subject>Enterocolitis, Necrotizing - microbiology</subject><subject>Enterocolitis, Necrotizing - pathology</subject><subject>Environmental changes</subject><subject>Environmental factors</subject><subject>Escherichia coli</subject><subject>Exposure</subject><subject>Feces - microbiology</subject><subject>Female</subject><subject>Gastroenterology</subject><subject>Gastrointestinal diseases</subject><subject>Gastrointestinal Tract - 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We aimed to explore the longitudinal development of the gut microbiome in preterm twins to determine how shared environmental and genetic factors may influence temporal changes and compared this to the expressed breast milk (EBM) microbiome. Stool samples (n = 173) from 27 infants (12 twin pairs and 1 triplet set) and EBM (n = 18) from 4 mothers were collected longitudinally. All samples underwent PCR-DGGE (denaturing gradient gel electrophoresis) analysis and a selected subset underwent 454 pyrosequencing. Stool and EBM shared a core microbiome dominated by Enterobacteriaceae, Enterococcaceae, and Staphylococcaceae. The gut microbiome showed greater similarity between siblings compared to unrelated individuals. Pyrosequencing revealed a reduction in diversity and increasing dominance of Escherichia sp. preceding NEC that was not observed in the healthy twin. Antibiotic treatment had a substantial effect on the gut microbiome, reducing Escherichia sp. and increasing other Enterobacteriaceae. This study demonstrates related preterm twins share similar gut microbiome development, even within the complex environment of neonatal intensive care. This is likely a result of shared genetic and immunomodulatory factors as well as exposure to the same maternal microbiome during birth, skin contact and exposure to EBM. Environmental factors including antibiotic exposure and feeding are additional significant determinants of community structure, regardless of host genetics.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24023682</pmid><doi>10.1371/journal.pone.0073465</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Antibiotics Babies Bacteria - growth & development Breast milk Breastfeeding & lactation Childbirth & labor Communities Community structure Demography Deoxyribonucleic acid Digestive system Disease DNA E coli Enterocolitis Enterocolitis, Necrotizing - microbiology Enterocolitis, Necrotizing - pathology Environmental changes Environmental factors Escherichia coli Exposure Feces - microbiology Female Gastroenterology Gastrointestinal diseases Gastrointestinal Tract - microbiology Gastrointestinal Tract - pathology Gel electrophoresis Genetic factors Genetics Hospitals Humans Immunomodulation Infant, Newborn Infants Infections Inflammatory bowel disease Intestinal microflora Life sciences Male Microbiota Milk Milk, Human - microbiology Multiple births Necrosis Neonates Newborn babies Pathogenesis Phylogenetics Premature Birth - microbiology Risk Factors Sepsis Sepsis - microbiology Sepsis - pathology Siblings Skin Twins |
| title | Development of the preterm gut microbiome in twins at risk of necrotising enterocolitis and sepsis |
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