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Maternal anxiety during pregnancy and newborn epigenome-wide DNA methylation

Molecular Psychiatry volume 26, pages 1832–1845 (2021)Cite this article

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Abstract

Maternal anxiety during pregnancy is associated with adverse foetal, neonatal, and child outcomes, but biological mechanisms remain unclear. Altered foetal DNA methylation (DNAm) has been proposed as a potential underlying mechanism. In the current study, we performed a meta-analysis to examine the associations between maternal anxiety, measured prospectively during pregnancy, and genome-wide DNAm from umbilical cord blood. Sixteen non-overlapping cohorts from 12 independent longitudinal studies of the Pregnancy And Childhood Epigenetics Consortium participated, resulting in a combined dataset of 7243 mother-child dyads. We examined prenatal anxiety in relation to genome-wide DNAm and differentially methylated regions. We observed no association between the general symptoms of anxiety during pregnancy or pregnancy-related anxiety, and DNAm at any of the CpG sites, after multiple-testing correction. Furthermore, we identify no differentially methylated regions associated with maternal anxiety. At the cohort-level, of the 21 associations observed in individual cohorts, none replicated consistently in the other cohorts. In conclusion, contrary to some previous studies proposing cord blood DNAm as a promising potential mechanism explaining the link between maternal anxiety during pregnancy and adverse outcomes in offspring, we found no consistent evidence for any robust associations between maternal anxiety and DNAm in cord blood. Larger studies and analysis of DNAm in other tissues may be needed to establish subtle or subgroup-specific associations between maternal anxiety and the foetal epigenome.

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Fig. 1: Manhattan and quantile-quantile plot showing meta-analytic associations between general anxiety during pregnancy and cord blood DNA methylation (within 15 cohorts, maximum N = 6686 mother-child dyads).
Fig. 2: Forest plot showing associations between general anxiety during pregnancy and cord blood DNA methylation for the most significant associations (p < 5 × 10−5), across all cohorts with available data.

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Data availability

Site-level meta-analytical results are publicly available (https://doi.org/10.5281/zenodo.4147817). For access to cohort-level data, requests can be sent directly to individual studies.

Code availability

Analytical codes can be requested from authors.

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Acknowledgements

Acknowledgements for each of the participating studies are listed in the Funding and Acknowledgements supplement.

Author information

Author notes

  1. These authors contributed equally: Sara Sammallahti, Andrea P. Cortes Hidalgo

  2. These authors contributed equally: Charlotte A. M. Cecil, Henning Tiemeier, Jari Lahti

Authors and Affiliations

  1. Erasmus MC, University Medical Center Rotterdam, Department of Adolescent and Child Psychiatry and Psychology, Rotterdam, The Netherlands

    Sara Sammallahti, Andrea P. Cortes Hidalgo, Rosa H. Mulder, Charlotte A. M. Cecil & Henning Tiemeier

  2. Erasmus MC, University Medical Center Rotterdam, Generation R Study Group, Rotterdam, The Netherlands

    Sara Sammallahti, Andrea P. Cortes Hidalgo, Rosa H. Mulder, Janine F. Felix, Charlotte A. M. Cecil & Henning Tiemeier

  3. Harvard T.H. Chan School of Public Health, Department of Social and Behavioral Science, Boston, MA, USA

    Sara Sammallahti & Henning Tiemeier

  4. University of Helsinki, Department of Psychology and Logopedics, Helsinki, Finland

    Sara Sammallahti, Samuli Tuominen, Anni Malmberg, Katri Räikkönen & Jari Lahti

  5. Leiden University, Institute of Education and Child Studies, Leiden, The Netherlands

    Rosa H. Mulder

  6. University of Cincinnati, College of Medicine, Department of Environmental Health, Cincinnati, OH, USA

    Kelly J. Brunst

  7. ISGlobal, Barcelona Institute for Global Health, Barcelona, Spain

    Silvia Alemany & Jordi Sunyer

  8. CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain

    Silvia Alemany & Jordi Sunyer

  9. Universitat Pompeu Fabra (UPF), Barcelona, Spain

    Silvia Alemany & Jordi Sunyer

  10. University of Bristol, MRC Integrative Epidemiology Unit, Population Health Sciences, Bristol Medical School, Bristol, UK

    Nancy S. McBride, Paul Yousefi, Doretta Caramaschi, Maria C. Magnus, Deborah A. Lawlor, Caroline L. Relton, Gemma C. Sharp, Lotte C. Houtepen & Thorkild I. A. Sørensen

  11. Icahn School of Medicine at Mount Sinai, Department of Environmental Medicine and Public Health, New York, NY, USA

    Jonathan A. Heiss & Elena Colicino

  12. Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Nia McRae & Robert O. Wright

  13. Centre for Fertility and Health, Norwegian Institute of Public Health, Oslo, Norway

    Christian M. Page, Maria C. Magnus & Siri E. Håberg

  14. Oslo Centre for Biostatistics and Epidemiology, Oslo University Hospital, Oslo, Norway

    Christian M. Page

  15. Westat, Durham, NC, USA

    Jianping Jin

  16. INSERM UMR-S 1136, EPAR, Saint-Antoine Medical School, Paris, France

    Giancarlo Pesce, Nour Baïz & Isabella Annesi-Maesano

  17. Sorbonne Université, Epidemiology of Allergic and Respiratory Diseases Department (EPAR), Pierre Louis Institute of Epidemiology and Public Health (IPLESP), Paris, France

    Giancarlo Pesce, Nour Baïz & Isabella Annesi-Maesano

  18. Harvard Medical School, Department of Population Medicine, Harvard Pilgrim Health Care Institute, Boston, MA, USA

    Sheryl L. Rifas-Shiman & Marie-France Hivert

  19. University of Cape Town, Department of Psychiatry and Mental Health, Cape Town, South Africa

    Nastassja Koen & Dan J. Stein

  20. South African Medical Research Council (SAMRC) Unit on Risk and Resilience in Mental Disorders, Cape Town, South Africa

    Nastassja Koen & Dan J. Stein

  21. University of Cape Town, Neuroscience Institute, Cape Town, South Africa

    Nastassja Koen & Dan J. Stein

  22. Beckman Research Institute of City of Hope, Department of Population Sciences, Duarte, CA, USA

    Charleen D. Adams

  23. Columbia University, Department of Epidemiology, New York City, NY, USA

    Andrew Ratanatharathorn

  24. Harvard T.H. Chan School of Public Health, Department of Epidemiology, Boston, MA, USA

    Andrew Ratanatharathorn

  25. Max-Planck-Institute of Psychiatry, Department of Translational Research in Psychiatry, Munich, Germany

    Darina Czamara

  26. Columbia University Mailman School of Public Health, Precision Environmental Health Lab, New York, NY, USA

    Andrea A. Baccarelli

  27. University of California, Division of Environmental Health Sciences, School of Public Health, Berkeley, CA, USA

    Andres Cardenas

  28. Brigham and Women’s Hospital, Channing Division of Network Medicine, Boston, MA, USA

    Dawn L. DeMeo

  29. Harvard Medical School, Boston, MA, USA

    Dawn L. DeMeo

  30. Erasmus MC, University Medical Center Rotterdam, Department of Pediatrics, Rotterdam, The Netherlands

    Janine F. Felix

  31. Erasmus University Rotterdam, Department of Psychology, Education, and Child Studies, Rotterdam, The Netherlands

    Marinus H. van IJzendoorn

  32. University of Cambridge, School of Clinical Medicine, Cambridge, UK

    Marinus H. van IJzendoorn

  33. Leiden University, Leiden Institute for Brain and Cognition, Leiden, The Netherlands

    Marian J. Bakermans-Kranenburg

  34. Vrije Universiteit Amsterdam, Clinical Child & Family Studies, Amsterdam, The Netherlands

    Marian J. Bakermans-Kranenburg

  35. Finnish Institute for Health and Welfare, Helsinki, Finland

    Eero Kajantie

  36. Oulu University Hospital and University of Oulu, PEDEGO Research Unit, MRC Oulu, Oulu, Finland

    Eero Kajantie

  37. Children’s Hospital, Helsinki University Hospital and University of Helsinki, Helsinki, Finland

    Eero Kajantie

  38. Norwegian University of Science and Technology, Department of Clinical and Molecular Medicine, Trondheim, Norway

    Eero Kajantie

  39. IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain

    Jordi Sunyer

  40. University of Southern Denmark, Institute of Clinical Research and Department of Gynaecology and Obstetrics, Odense, Denmark

    Ellen A. Nohr

  41. University of Copenhagen, Faculty of Health and Medical Sciences, Department of Public Health, Copenhagen, Denmark

    Thorkild I. A. Sørensen

  42. University of Copenhagen, Faculty of Medical and Health Sciences, Novo Nordisk Foundation Center for Basic Metabolic Research, Copenhagen, Denmark

    Thorkild I. A. Sørensen

  43. National Institute of Public Health, Center for Nutrition and Health Research, Cuernavaca, Mor, Mexico

    Martha M. Téllez-Rojo

  44. Bradford Institute for Health Research, Bradford Teaching Hospitals, NHS Foundation Trust, Bradford, UK

    John Wright

  45. Massachusetts General Hospital, Diabetes Unit, Boston, MA, USA

    Marie-France Hivert

  46. Icahn School of Medicine at Mount Sinai, Environmental Medicine & Public Health, Institute for Exposomic Research, New York, NY, USA

    Rosalind J. Wright

  47. University of Cape Town, Department of Paediatrics and Child Health, Cape Town, South Africa

    Heather J. Zar

  48. South African Medical Research Council (SAMRC) Unit on Child and Adolescent Health, Cape Town, Cape Town, South Africa

    Heather J. Zar

  49. Epidemiology Branch, National Institute of Environmental Health Sciences, National Institutes of Health, Department of Health and Human Services, Research Triangle Park, NC, USA

    Stephanie J. London

  50. Erasmus MC, University Medical Center Rotterdam, Department of Epidemiology, Rotterdam, The Netherlands

    Charlotte A. M. Cecil

  51. Leiden University Medical Center, Molecular Epidemiology, Department of Biomedical Data Sciences, Leiden, The Netherlands

    Charlotte A. M. Cecil

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  1. Sara Sammallahti
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  2. Andrea P. Cortes Hidalgo
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  3. Samuli Tuominen
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  4. Anni Malmberg
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  5. Rosa H. Mulder
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  6. Kelly J. Brunst
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  7. Silvia Alemany
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  8. Nancy S. McBride
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  9. Paul Yousefi
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  10. Jonathan A. Heiss
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  11. Nia McRae
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  12. Christian M. Page
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  13. Jianping Jin
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  14. Giancarlo Pesce
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  15. Doretta Caramaschi
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  16. Sheryl L. Rifas-Shiman
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  18. Charleen D. Adams
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  19. Maria C. Magnus
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  20. Nour Baïz
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  21. Andrew Ratanatharathorn
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  22. Darina Czamara
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  23. Siri E. Håberg
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  24. Elena Colicino
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  25. Andrea A. Baccarelli
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  26. Andres Cardenas
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  27. Dawn L. DeMeo
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  28. Deborah A. Lawlor
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  29. Caroline L. Relton
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  30. Janine F. Felix
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  31. Marinus H. van IJzendoorn
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  32. Marian J. Bakermans-Kranenburg
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  33. Eero Kajantie
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  34. Katri Räikkönen
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  35. Jordi Sunyer
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  36. Gemma C. Sharp
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  37. Lotte C. Houtepen
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  38. Ellen A. Nohr
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  39. Thorkild I. A. Sørensen
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  40. Martha M. Téllez-Rojo
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  41. Robert O. Wright
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Corresponding author

Correspondence to Henning Tiemeier.

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DJS received research grants and/or consultancy honoraria from Lundbeck and Sun; the other authors confirm they have no financial relationships with commercial interests to disclose. Funding for each of the participating studies is listed in the Funding and Acknowledgements supplement. There was no editorial direction or censorship from the sponsors.

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Sammallahti, S., Cortes Hidalgo, A.P., Tuominen, S. et al. Maternal anxiety during pregnancy and newborn epigenome-wide DNA methylation. Mol Psychiatry 26, 1832–1845 (2021). https://doi.org/10.1038/s41380-020-00976-0

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