Oxygenation and intestinal perfusion and its association with perturbations of the early life gut microbiota composition of children with congenital heart disease

BackgroundEarly life gut microbiota is known to shape the immune system and has a crucial role in immune homeostasis. Only little is known about composition and dynamics of the intestinal microbiota in infants with congenital heart disease (CHD) and potential influencing factors.MethodsWe evaluated...

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Main Authors: Hanna Renk, Ulrich Schoppmeier, Jennifer Müller, Vanessa Kuger, Felix Neunhoeffer, Christian Gille, Silke Peter
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1468842/full
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author Hanna Renk
Hanna Renk
Hanna Renk
Ulrich Schoppmeier
Jennifer Müller
Vanessa Kuger
Felix Neunhoeffer
Christian Gille
Silke Peter
Silke Peter
author_facet Hanna Renk
Hanna Renk
Hanna Renk
Ulrich Schoppmeier
Jennifer Müller
Vanessa Kuger
Felix Neunhoeffer
Christian Gille
Silke Peter
Silke Peter
author_sort Hanna Renk
collection DOAJ
description BackgroundEarly life gut microbiota is known to shape the immune system and has a crucial role in immune homeostasis. Only little is known about composition and dynamics of the intestinal microbiota in infants with congenital heart disease (CHD) and potential influencing factors.MethodsWe evaluated the intestinal microbial composition of neonates with CHD (n = 13) compared to healthy controls (HC, n = 30). Fecal samples were analyzed by shotgun metagenomics. Different approaches of statistical modeling were applied to assess the impact of influencing factors on variation in species composition. Unsupervised hierarchical clustering of the microbial composition of neonates with CHD was used to detect associations of distinct clusters with intestinal tissue oxygenation and perfusion parameters, obtained by the “oxygen to see” (O2C) method.ResultsOverall, neonates with CHD showed an intestinal core microbiota dominated by the genera Enterococcus (27%) and Staphylococcus (20%). Furthermore, a lower abundance of the genera Bacteroides (8% vs. 14%), Parabacteroides (1% vs. 3%), Bifidobacterium (4% vs. 12%), and Escherichia (8% vs. 23%) was observed in CHD compared to HCs. CHD patients that were born by vaginal delivery showed a lower fraction of the genera Bacteroides (15% vs. 21%) and Bifidobacterium (7% vs. 22%) compared to HCs and in those born by cesarean section, these genera were not found at all. In infants with CHD, we found a significant impact of oxygen saturation (SpO2) on relative abundances of the intestinal core microbiota by multivariate analysis of variance (F[8,2] = 24.9, p = 0.04). Statistical modeling suggested a large proportional shift from a microbiota dominated by the genus Streptococcus (50%) in conditions with low SpO2 towards the genus Enterococcus (61%) in conditions with high SpO2. We identified three distinct compositional microbial clusters, corresponding neonates differed significantly in intestinal blood flow and global gut perfusion.ConclusionEarly life differences in gut microbiota of CHD neonates versus HCs are possibly linked to oxygen levels. Delivery method may affect microbiota stability. However, further studies are needed to assess the effect of potential interventions including probiotics or fecal transplants on early life microbiota perturbations in neonates with CHD.
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spelling doaj-art-cff07506195d4ba6b8ddaa1f7ef8f9f42025-08-20T02:59:03ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.14688421468842Oxygenation and intestinal perfusion and its association with perturbations of the early life gut microbiota composition of children with congenital heart diseaseHanna Renk0Hanna Renk1Hanna Renk2Ulrich Schoppmeier3Jennifer Müller4Vanessa Kuger5Felix Neunhoeffer6Christian Gille7Silke Peter8Silke Peter9Department of Neuropediatrics, Developmental Neurology and Social Pediatrics, University Children’s Hospital Tübingen, Tübingen, GermanyGerman Centre for Infection Research (DZIF), Partner Site Tübingen, Tübingen, GermanyDepartment of Pediatric Cardiology, Pulmonology and Pediatric Intensive Care Medicine, University Children’s Hospital Tübingen, Tübingen, GermanyInstitute of Medical Microbiology and Hygiene, University of Tübingen, Tübingen, GermanyNGS Competence Center Tübingen (NCCT), University of Tübingen, Tübingen, GermanyDepartment of Pediatric Cardiology, Pulmonology and Pediatric Intensive Care Medicine, University Children’s Hospital Tübingen, Tübingen, GermanyDepartment of Pediatric Cardiology, Pulmonology and Pediatric Intensive Care Medicine, University Children’s Hospital Tübingen, Tübingen, GermanyDepartment of Neonatology, Heidelberg University Children’s Hospital, Heidelberg, GermanyGerman Centre for Infection Research (DZIF), Partner Site Tübingen, Tübingen, GermanyInstitute of Medical Microbiology and Hygiene, University of Tübingen, Tübingen, GermanyBackgroundEarly life gut microbiota is known to shape the immune system and has a crucial role in immune homeostasis. Only little is known about composition and dynamics of the intestinal microbiota in infants with congenital heart disease (CHD) and potential influencing factors.MethodsWe evaluated the intestinal microbial composition of neonates with CHD (n = 13) compared to healthy controls (HC, n = 30). Fecal samples were analyzed by shotgun metagenomics. Different approaches of statistical modeling were applied to assess the impact of influencing factors on variation in species composition. Unsupervised hierarchical clustering of the microbial composition of neonates with CHD was used to detect associations of distinct clusters with intestinal tissue oxygenation and perfusion parameters, obtained by the “oxygen to see” (O2C) method.ResultsOverall, neonates with CHD showed an intestinal core microbiota dominated by the genera Enterococcus (27%) and Staphylococcus (20%). Furthermore, a lower abundance of the genera Bacteroides (8% vs. 14%), Parabacteroides (1% vs. 3%), Bifidobacterium (4% vs. 12%), and Escherichia (8% vs. 23%) was observed in CHD compared to HCs. CHD patients that were born by vaginal delivery showed a lower fraction of the genera Bacteroides (15% vs. 21%) and Bifidobacterium (7% vs. 22%) compared to HCs and in those born by cesarean section, these genera were not found at all. In infants with CHD, we found a significant impact of oxygen saturation (SpO2) on relative abundances of the intestinal core microbiota by multivariate analysis of variance (F[8,2] = 24.9, p = 0.04). Statistical modeling suggested a large proportional shift from a microbiota dominated by the genus Streptococcus (50%) in conditions with low SpO2 towards the genus Enterococcus (61%) in conditions with high SpO2. We identified three distinct compositional microbial clusters, corresponding neonates differed significantly in intestinal blood flow and global gut perfusion.ConclusionEarly life differences in gut microbiota of CHD neonates versus HCs are possibly linked to oxygen levels. Delivery method may affect microbiota stability. However, further studies are needed to assess the effect of potential interventions including probiotics or fecal transplants on early life microbiota perturbations in neonates with CHD.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1468842/fullcongenital heart diseaseintestinal microbiotanext-generation sequencingoxygen to seeO2Coxygenation
spellingShingle Hanna Renk
Hanna Renk
Hanna Renk
Ulrich Schoppmeier
Jennifer Müller
Vanessa Kuger
Felix Neunhoeffer
Christian Gille
Silke Peter
Silke Peter
Oxygenation and intestinal perfusion and its association with perturbations of the early life gut microbiota composition of children with congenital heart disease
Frontiers in Microbiology
congenital heart disease
intestinal microbiota
next-generation sequencing
oxygen to see
O2C
oxygenation
title Oxygenation and intestinal perfusion and its association with perturbations of the early life gut microbiota composition of children with congenital heart disease
title_full Oxygenation and intestinal perfusion and its association with perturbations of the early life gut microbiota composition of children with congenital heart disease
title_fullStr Oxygenation and intestinal perfusion and its association with perturbations of the early life gut microbiota composition of children with congenital heart disease
title_full_unstemmed Oxygenation and intestinal perfusion and its association with perturbations of the early life gut microbiota composition of children with congenital heart disease
title_short Oxygenation and intestinal perfusion and its association with perturbations of the early life gut microbiota composition of children with congenital heart disease
title_sort oxygenation and intestinal perfusion and its association with perturbations of the early life gut microbiota composition of children with congenital heart disease
topic congenital heart disease
intestinal microbiota
next-generation sequencing
oxygen to see
O2C
oxygenation
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1468842/full
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