Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood

Adversity exposures in the prenatal and postnatal period are associated with an increased risk for psychopathology, which can be perpetuated across generations. Nonhuman animal research highlights the gut microbiome as a putative biological mechanism underlying such generational risks. In a sample o...

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Main Authors: Querdasi, Francesca R., Enders, Craig, Karnani, Neerja, Broekman, Birit, Chong, Yap Seng, Gluckman, Peter D., Daniel, Lourdes Mary, Yap, Fabian, Eriksson, Johan G., Cai, Shirong, Chong, Mary Foong-Fong, Toh, Jia Ying, Godfrey, Keith, Meaney, Michael J., Callaghan, Bridget L.
Other Authors: Lee Kong Chian School of Medicine (LKCMedicine)
Format: Article
Language:English
Published: 2024
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Online Access:https://hdl.handle.net/10356/174264
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spelling sg-ntu-dr.10356-1742642024-03-31T15:40:05Z Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood Querdasi, Francesca R. Enders, Craig Karnani, Neerja Broekman, Birit Chong, Yap Seng Gluckman, Peter D. Daniel, Lourdes Mary Yap, Fabian Eriksson, Johan G. Cai, Shirong Chong, Mary Foong-Fong Toh, Jia Ying Godfrey, Keith Meaney, Michael J. Callaghan, Bridget L. Lee Kong Chian School of Medicine (LKCMedicine) KK Women’s and Children’s Hopsital Medicine, Health and Life Sciences Intergenerational transmission Early life adversity Adversity exposures in the prenatal and postnatal period are associated with an increased risk for psychopathology, which can be perpetuated across generations. Nonhuman animal research highlights the gut microbiome as a putative biological mechanism underlying such generational risks. In a sample of 450 mother-child dyads living in Singapore, we examined associations between three distinct adversity exposures experienced across two generations-maternal childhood maltreatment, maternal prenatal anxiety, and second-generation children's exposure to stressful life events-and the gut microbiome composition of second-generation children at 2 y of age. We found distinct differences in gut microbiome profiles linked to each adversity exposure, as well as some nonaffected microbiome features (e.g., beta diversity). Remarkably, some of the microbial taxa associated with concurrent and prospective child socioemotional functioning shared overlapping putative functions with those affected by adversity, suggesting that the intergenerational transmission of adversity may have a lasting impact on children's mental health via alterations to gut microbiome functions. Our findings open up a new avenue of research into the underlying mechanisms of intergenerational transmission of mental health risks and the potential of the gut microbiome as a target for intervention. Agency for Science, Technology and Research (A*STAR) Ministry of Health (MOH) National Medical Research Council (NMRC) National Research Foundation (NRF) Published version Funding was provided by the Singapore National Research Foundation under its Translational and Clinical Research Flagship Programme and administered by the Singapore Ministry of Health’s National Medical Research Council, Singapore–NMRC/TCR/004-NUS/2008; NMRC/TCR/012-NUHS/2014.Additional funding was provided by the Singapore Institute for Clinical Sciences, Agency for Science Technology and Research, the JPB Foundation (US) Toxic Stress Network (M.J.M.),and the UCLA Psychology Summer Research Fellowship (F.R.Q.). 2024-03-25T02:34:17Z 2024-03-25T02:34:17Z 2023 Journal Article Querdasi, F. R., Enders, C., Karnani, N., Broekman, B., Chong, Y. S., Gluckman, P. D., Daniel, L. M., Yap, F., Eriksson, J. G., Cai, S., Chong, M. F., Toh, J. Y., Godfrey, K., Meaney, M. J. & Callaghan, B. L. (2023). Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood. Proceedings of the National Academy of Sciences, 120(30), e2213768120-. https://dx.doi.org/10.1073/pnas.2213768120 0027-8424 https://hdl.handle.net/10356/174264 10.1073/pnas.2213768120 37463211 2-s2.0-85165508006 30 120 e2213768120 en NMRC/TCR/004-NUS/2008 NMRC/TCR/012-NUHS/2014 Proceedings of the National Academy of Sciences © 2023 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution- NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Medicine, Health and Life Sciences
Intergenerational transmission
Early life adversity
spellingShingle Medicine, Health and Life Sciences
Intergenerational transmission
Early life adversity
Querdasi, Francesca R.
Enders, Craig
Karnani, Neerja
Broekman, Birit
Chong, Yap Seng
Gluckman, Peter D.
Daniel, Lourdes Mary
Yap, Fabian
Eriksson, Johan G.
Cai, Shirong
Chong, Mary Foong-Fong
Toh, Jia Ying
Godfrey, Keith
Meaney, Michael J.
Callaghan, Bridget L.
Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood
description Adversity exposures in the prenatal and postnatal period are associated with an increased risk for psychopathology, which can be perpetuated across generations. Nonhuman animal research highlights the gut microbiome as a putative biological mechanism underlying such generational risks. In a sample of 450 mother-child dyads living in Singapore, we examined associations between three distinct adversity exposures experienced across two generations-maternal childhood maltreatment, maternal prenatal anxiety, and second-generation children's exposure to stressful life events-and the gut microbiome composition of second-generation children at 2 y of age. We found distinct differences in gut microbiome profiles linked to each adversity exposure, as well as some nonaffected microbiome features (e.g., beta diversity). Remarkably, some of the microbial taxa associated with concurrent and prospective child socioemotional functioning shared overlapping putative functions with those affected by adversity, suggesting that the intergenerational transmission of adversity may have a lasting impact on children's mental health via alterations to gut microbiome functions. Our findings open up a new avenue of research into the underlying mechanisms of intergenerational transmission of mental health risks and the potential of the gut microbiome as a target for intervention.
author2 Lee Kong Chian School of Medicine (LKCMedicine)
author_facet Lee Kong Chian School of Medicine (LKCMedicine)
Querdasi, Francesca R.
Enders, Craig
Karnani, Neerja
Broekman, Birit
Chong, Yap Seng
Gluckman, Peter D.
Daniel, Lourdes Mary
Yap, Fabian
Eriksson, Johan G.
Cai, Shirong
Chong, Mary Foong-Fong
Toh, Jia Ying
Godfrey, Keith
Meaney, Michael J.
Callaghan, Bridget L.
format Article
author Querdasi, Francesca R.
Enders, Craig
Karnani, Neerja
Broekman, Birit
Chong, Yap Seng
Gluckman, Peter D.
Daniel, Lourdes Mary
Yap, Fabian
Eriksson, Johan G.
Cai, Shirong
Chong, Mary Foong-Fong
Toh, Jia Ying
Godfrey, Keith
Meaney, Michael J.
Callaghan, Bridget L.
author_sort Querdasi, Francesca R.
title Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood
title_short Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood
title_full Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood
title_fullStr Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood
title_full_unstemmed Multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood
title_sort multigenerational adversity impacts on human gut microbiome composition and socioemotional functioning in early childhood
publishDate 2024
url https://hdl.handle.net/10356/174264
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