Gestational Diabetes Is Uniquely Associated With Altered Early Seeding of the Infant Gut Microbiota

Gestational diabetes mellitus (GDM) is a worldwide public health problem affecting up to 27% of pregnancies with high predictive values for childhood obesity and inflammatory diseases. Compromised seeding of the infant gut microbiota is a risk factor for immunologic and metabolic diseases in the off...

Full description

Bibliographic Details
Main Authors: Taylor K. Soderborg, Charles M. Carpenter, Rachel C. Janssen, Tiffany L. Weir, Charles E. Robertson, Diana Ir, Bridget E. Young, Nancy F. Krebs, Teri L. Hernandez, Linda A. Barbour, Daniel N. Frank, Miranda Kroehl, Jacob E. Friedman
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-11-01
Series:Frontiers in Endocrinology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fendo.2020.603021/full
_version_ 1818351978576609280
author Taylor K. Soderborg
Charles M. Carpenter
Rachel C. Janssen
Tiffany L. Weir
Charles E. Robertson
Diana Ir
Bridget E. Young
Nancy F. Krebs
Teri L. Hernandez
Teri L. Hernandez
Linda A. Barbour
Linda A. Barbour
Daniel N. Frank
Miranda Kroehl
Jacob E. Friedman
Jacob E. Friedman
author_facet Taylor K. Soderborg
Charles M. Carpenter
Rachel C. Janssen
Tiffany L. Weir
Charles E. Robertson
Diana Ir
Bridget E. Young
Nancy F. Krebs
Teri L. Hernandez
Teri L. Hernandez
Linda A. Barbour
Linda A. Barbour
Daniel N. Frank
Miranda Kroehl
Jacob E. Friedman
Jacob E. Friedman
author_sort Taylor K. Soderborg
collection DOAJ
description Gestational diabetes mellitus (GDM) is a worldwide public health problem affecting up to 27% of pregnancies with high predictive values for childhood obesity and inflammatory diseases. Compromised seeding of the infant gut microbiota is a risk factor for immunologic and metabolic diseases in the offspring; however, how GDM along with maternal obesity interact to alter colonization remains unknown. We hypothesized that GDM individually and in combination with maternal overweight/obesity would alter gut microbial composition, diversity, and short-chain fatty acid (SCFA) levels in neonates. We investigated 46 full-term neonates born to normal-weight or overweight/obese mothers with and without GDM, accounting for confounders including cesarean delivery, lack of breastfeeding, and exposure to antibiotics. Gut microbiota in 2-week-old neonates born to mothers with GDM exhibited differences in abundance of 26 microbial taxa; 14 of which showed persistent differential abundance after adjusting for pre-pregnancy BMI. Key pioneering gut taxa, including potentially important taxa for establishing neonatal immunity, were reduced. Lactobacillus, Flavonifractor, Erysipelotrichaceae, and unspecified families in Gammaproteobacteria were significantly reduced in neonates from mothers with GDM. GDM was associated with an increase in microbes involved in suppressing early immune cell function (Phascolarctobacterium). No differences in infant stool SCFA levels by maternal phenotype were noted; however, significant correlations were found between microbial abundances and SCFA levels in neonates. Our results suggest that GDM alone and together with maternal overweight/obesity uniquely influences seeding of specific infant microbiota in patterns that set the stage for future risk of inflammatory and metabolic disease.
first_indexed 2024-12-13T18:46:20Z
format Article
id doaj.art-cc75e385ad1540c09e09def7844d653e
institution Directory Open Access Journal
issn 1664-2392
language English
last_indexed 2024-12-13T18:46:20Z
publishDate 2020-11-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Endocrinology
spelling doaj.art-cc75e385ad1540c09e09def7844d653e2022-12-21T23:35:04ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922020-11-011110.3389/fendo.2020.603021603021Gestational Diabetes Is Uniquely Associated With Altered Early Seeding of the Infant Gut MicrobiotaTaylor K. Soderborg0Charles M. Carpenter1Rachel C. Janssen2Tiffany L. Weir3Charles E. Robertson4Diana Ir5Bridget E. Young6Nancy F. Krebs7Teri L. Hernandez8Teri L. Hernandez9Linda A. Barbour10Linda A. Barbour11Daniel N. Frank12Miranda Kroehl13Jacob E. Friedman14Jacob E. Friedman15Department of Pediatrics, Section of Neonatology, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDivision of Biostatistics and Epidemiology, University of Colorado School of Public Health, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Pediatrics, Section of Neonatology, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Food Science and Human Nutrition, Colorado State University, Fort Collins, CO, United StatesDepartment of Medicine, Division of Infectious Disease, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Medicine, Division of Infectious Disease, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Pediatrics, Section of Nutrition, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Pediatrics, Section of Nutrition, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Medicine, Division of Endocrinology, Metabolism & Diabetes, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesCollege of Nursing, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Medicine, Division of Endocrinology, Metabolism & Diabetes, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Obstetrics and Gynecology, Division of Maternal Fetal Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Medicine, Division of Infectious Disease, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDivision of Biostatistics and Epidemiology, University of Colorado School of Public Health, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Pediatrics, Section of Neonatology, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Medicine, Division of Endocrinology, Metabolism & Diabetes, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesGestational diabetes mellitus (GDM) is a worldwide public health problem affecting up to 27% of pregnancies with high predictive values for childhood obesity and inflammatory diseases. Compromised seeding of the infant gut microbiota is a risk factor for immunologic and metabolic diseases in the offspring; however, how GDM along with maternal obesity interact to alter colonization remains unknown. We hypothesized that GDM individually and in combination with maternal overweight/obesity would alter gut microbial composition, diversity, and short-chain fatty acid (SCFA) levels in neonates. We investigated 46 full-term neonates born to normal-weight or overweight/obese mothers with and without GDM, accounting for confounders including cesarean delivery, lack of breastfeeding, and exposure to antibiotics. Gut microbiota in 2-week-old neonates born to mothers with GDM exhibited differences in abundance of 26 microbial taxa; 14 of which showed persistent differential abundance after adjusting for pre-pregnancy BMI. Key pioneering gut taxa, including potentially important taxa for establishing neonatal immunity, were reduced. Lactobacillus, Flavonifractor, Erysipelotrichaceae, and unspecified families in Gammaproteobacteria were significantly reduced in neonates from mothers with GDM. GDM was associated with an increase in microbes involved in suppressing early immune cell function (Phascolarctobacterium). No differences in infant stool SCFA levels by maternal phenotype were noted; however, significant correlations were found between microbial abundances and SCFA levels in neonates. Our results suggest that GDM alone and together with maternal overweight/obesity uniquely influences seeding of specific infant microbiota in patterns that set the stage for future risk of inflammatory and metabolic disease.https://www.frontiersin.org/articles/10.3389/fendo.2020.603021/fullgestational diabetesmaternal obesitymicrobiotaexcess gestational weight gaininfantshort-chain fatty acids
spellingShingle Taylor K. Soderborg
Charles M. Carpenter
Rachel C. Janssen
Tiffany L. Weir
Charles E. Robertson
Diana Ir
Bridget E. Young
Nancy F. Krebs
Teri L. Hernandez
Teri L. Hernandez
Linda A. Barbour
Linda A. Barbour
Daniel N. Frank
Miranda Kroehl
Jacob E. Friedman
Jacob E. Friedman
Gestational Diabetes Is Uniquely Associated With Altered Early Seeding of the Infant Gut Microbiota
Frontiers in Endocrinology
gestational diabetes
maternal obesity
microbiota
excess gestational weight gain
infant
short-chain fatty acids
title Gestational Diabetes Is Uniquely Associated With Altered Early Seeding of the Infant Gut Microbiota
title_full Gestational Diabetes Is Uniquely Associated With Altered Early Seeding of the Infant Gut Microbiota
title_fullStr Gestational Diabetes Is Uniquely Associated With Altered Early Seeding of the Infant Gut Microbiota
title_full_unstemmed Gestational Diabetes Is Uniquely Associated With Altered Early Seeding of the Infant Gut Microbiota
title_short Gestational Diabetes Is Uniquely Associated With Altered Early Seeding of the Infant Gut Microbiota
title_sort gestational diabetes is uniquely associated with altered early seeding of the infant gut microbiota
topic gestational diabetes
maternal obesity
microbiota
excess gestational weight gain
infant
short-chain fatty acids
url https://www.frontiersin.org/articles/10.3389/fendo.2020.603021/full
work_keys_str_mv AT taylorksoderborg gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT charlesmcarpenter gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT rachelcjanssen gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT tiffanylweir gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT charleserobertson gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT dianair gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT bridgeteyoung gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT nancyfkrebs gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT terilhernandez gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT terilhernandez gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT lindaabarbour gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT lindaabarbour gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT danielnfrank gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT mirandakroehl gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT jacobefriedman gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota
AT jacobefriedman gestationaldiabetesisuniquelyassociatedwithalteredearlyseedingoftheinfantgutmicrobiota