Maternal anxiety, depression and stress affects offspring gut microbiome diversity and bifidobacterial abundances

Jeffrey D Galley; Lauren Mashburn-Warren; Lexie C Blalock; Christian L Lauber; Judith E Carroll; Kharah M Ross; Calvin Hobel; Mary Coussons-Read; Christine Dunkel Schetter; Tamar L Gur

doi:10.1016/j.bbi.2022.10.005

Maternal anxiety, depression and stress affects offspring gut microbiome diversity and bifidobacterial abundances

Brain Behav Immun. 2023 Jan:107:253-264. doi: 10.1016/j.bbi.2022.10.005. Epub 2022 Oct 12.

Affiliations

¹ Department of Psychiatry and Behavioral Health, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Institute for Behavioral Medicine Research, The Ohio State University Wexner Medical Center, Columbus, OH, USA.
² Institute for Genomic Medicine, Nationwide Children's Hospital, Columbus, OH, USA.
³ Institute for Genomic Medicine, Nationwide Children's Hospital, Columbus, OH, USA; Department of Pediatrics, The Ohio State University Wexner Medical Center, Columbus, OH, USA.
⁴ Cousins Center for Psychoneuroimmunology, Semel Institute for Neuroscience and Human Behavior, Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California, Los Angeles, CA, USA.
⁵ Center for Social Sciences, Athabasca University, Athabasca, Alberta, Canada.
⁶ Cedars-Sinai Medical Centre, Los Angeles, CA, USA.
⁷ Department of Psychology, The University of Colorado, Colorado Springs, CO, USA.
⁸ Department of Psychology, University of California, Los Angeles, Los Angeles, CA, USA.
⁹ Department of Psychiatry and Behavioral Health, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Institute for Behavioral Medicine Research, The Ohio State University Wexner Medical Center, Columbus, OH, USA; Department of Neuroscience, The Ohio State University, Columbus, OH, USA; Obstetrics and Gynecology, The Ohio State University Wexner Medical Center, Columbus, OH, USA. Electronic address: tamar.gur@osumc.edu.

PMID: 36240906
DOI: 10.1016/j.bbi.2022.10.005

Abstract

Uncovering mechanisms underlying fetal programming during pregnancy is of critical importance. Atypical neurodevelopment during the pre- and immediate postnatal period has been associated with long-term adverse health outcomes, including mood disorders and aberrant cognitive ability in offspring. Maternal factors that have been implicated in anomalous offspring development include maternal inflammation and tress, anxiety, and depression. One potential mechanism through which these factors perturb normal offspring postnatal development is through microbiome disruption. The mother is a primary source of early postnatal microbiome seeding for the offspring, and the transference of a healthy microbiome is key in normal neurodevelopment. Since psychological stress, mood disorders, and inflammation have all been implicated in altering maternal microbiome community structure, passing on aberrant microbial communities to the offspring that may then affect developmental outcomes. Therefore, we examined how maternal stress, anxiety and depression assessed with standardized instruments, and maternal inflammatory cytokine levels in the pre- and postnatal period are associated with the offspring microbiome within the first 13 months of life, utilizing full length 16S sequencing on infant stool samples, that allowed for species-level resolution. Results revealed that infants of mothers who reported higher anxiety and perceived stress had reduced alpha diversity. Additionally, the relative taxonomic quantitative abundances of Bifidobacterium dentium and other species that have been associated with either modulation of the gut-brain axis, or other beneficial health outcomes, were reduced in the offspring of mothers with higher anxiety, perceived stress, and depression. We also found associations between bifidobacteria and prenatal maternal pro-inflammatory cytokines IL-6, IL-8, and IL-10. In summary, specific microbial taxa involved in maintaining proper brain and immune function are lower in offspring born to mothers with anxiety, depression, or stress, providing strong evidence for a mechanism by which maternal factors may affect offspring health through microbiota dysregulation.

Keywords: Anxiety; Bifidobacteria; Depression; Gut microbiota; Prenatal stress.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Female
Humans
Mothers*

Grants and funding

R01 HD073491/HD/NICHD NIH HHS/United States