Maternal prenatal gut microbiota composition predicts child behaviour
Samantha L. Dawson,
Martin O'Hely,
Felice N. Jacka,
Anne-Louise Ponsonby,
Christos Symeonides,
Amy Loughman,
Fiona Collier,
Margarita Moreno-Betancur,
Peter Sly,
David Burgner,
Mimi L.K. Tang,
Richard Saffery,
Sarath Ranganathan,
Michael A. Conlon,
Leonard C Harrison,
Susanne Brix,
Karsten Kristiansen,
Peter Vuillermin
Affiliations
Samantha L. Dawson
Deakin University, IMPACT – the Institute for Mental and Physical Health and Clinical Translation, Barwon Health, Geelong, VIC, 3220, Australia; Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia
Martin O'Hely
Deakin University, IMPACT – the Institute for Mental and Physical Health and Clinical Translation, Barwon Health, Geelong, VIC, 3220, Australia; Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia
Felice N. Jacka
Deakin University, IMPACT – the Institute for Mental and Physical Health and Clinical Translation, Barwon Health, Geelong, VIC, 3220, Australia; Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; Black Dog Institute, NSW, Australia
Anne-Louise Ponsonby
The Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, Victoria 3052, Australia; The University of Melbourne, Parkville, Victoria 3052, Australia
Christos Symeonides
Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; The University of Melbourne, Parkville, Victoria 3052, Australia
Amy Loughman
Deakin University, IMPACT – the Institute for Mental and Physical Health and Clinical Translation, Barwon Health, Geelong, VIC, 3220, Australia
Fiona Collier
Deakin University, IMPACT – the Institute for Mental and Physical Health and Clinical Translation, Barwon Health, Geelong, VIC, 3220, Australia; Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; Barwon Health, Geelong, Victoria 3220, Australia
Margarita Moreno-Betancur
Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; The University of Melbourne, Parkville, Victoria 3052, Australia
Peter Sly
Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; University of Queensland, South Brisbane, Queensland 4101, Australia
David Burgner
Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; The University of Melbourne, Parkville, Victoria 3052, Australia; The Royal Children's Hospital, Parkville, Victoria 3052, Australia
Mimi L.K. Tang
Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; The University of Melbourne, Parkville, Victoria 3052, Australia; The Royal Children's Hospital, Parkville, Victoria 3052, Australia
Richard Saffery
Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; The University of Melbourne, Parkville, Victoria 3052, Australia
Sarath Ranganathan
Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; The University of Melbourne, Parkville, Victoria 3052, Australia; The Royal Children's Hospital, Parkville, Victoria 3052, Australia
Michael A. Conlon
CSIRO Health and Biosecurity, Adelaide, South Australia 5000, Australia
Leonard C Harrison
The University of Melbourne, Parkville, Victoria 3052, Australia; Walter and Eliza Hall Institute, Parkville, Victoria 3052, Australia
Susanne Brix
Technical University of Denmark, Department of Biotechnology and Biomedicine, DK-2800 Kgs. Lyngby, Denmark
Karsten Kristiansen
University of Copenhagen, Laboratory of Genomics and Molecular Biomedicine, Department of Biology, Universitetsparken 13, 2100 Copenhagen, Denmark
Peter Vuillermin
Deakin University, IMPACT – the Institute for Mental and Physical Health and Clinical Translation, Barwon Health, Geelong, VIC, 3220, Australia; Murdoch Children's Research Institute, Parkville, Victoria, 3052, Australia; Barwon Health, Geelong, Victoria 3220, Australia; Corresponding author at: iMPACT Deakin University & Barwon Health, Geelong 3220.
Background: Murine studies demonstrate that maternal prenatal gut microbiota influences brain development and behaviour of offspring. No human study has related maternal gut microbiota to behavioural outcomes during early life. This study aimed to evaluate relationships between the prenatal faecal microbiota, prenatal diet and childhood behaviour. Methods: A sub-cohort of 213 mothers and 215 children were selected from a longitudinal pre-birth cohort. Maternal prenatal exposure measures collected during the third trimester included the faecal microbiota (generated using 16S rRNA amplicon sequencing), and dietary intake. The behavioural outcome used the Childhood Behaviour Checklist at age two. Models were adjusted for prenatal diet, smoking, perceived stress, maternal age and sample batch. Findings: We found evidence that the alpha diversity of the maternal faecal microbiota during the third trimester of pregnancy predicts child internalising behaviour at two years of age (−2·74, (−4·71, −0·78), p = 0·01 (Wald test), R2=0·07). Taxa from butyrate-producing families, Lachnospiraceae and Ruminococcaceae, were more abundant in mothers of children with normative behaviour. A healthy prenatal diet indirectly related to decreased child internalising behaviours via higher alpha diversity of maternal faecal microbiota. Interpretation: These findings support animal studies showing that the composition of maternal prenatal gut microbiota is related to offspring brain development and behaviour. Our findings highlight the need to evaluate potential impacts of the prenatal gut microbiota on early life brain development. Funding: This study was funded by the National Health and Medical Research Council of Australia (1082307, 1147980), Murdoch Children's Research Institute, Barwon Health and Deakin University.
