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Research Article

Maternal prenatal stress phenotypes associate with fetal neurodevelopment and birth outcomes

Kate Walsh, Clare A. McCormack, Rachel Webster, Anita Pinto, Seonjoo Lee, Tianshu Feng, H. Sloan Krakovsky, Sinclaire M. O’Grady, Benjamin Tycko, Frances A. Champagne, Elizabeth A. Werner, Grace Liu, and View ORCID ProfileCatherine Monk
PNAS November 26, 2019 116 (48) 23996-24005; first published October 14, 2019 https://doi.org/10.1073/pnas.1905890116
Kate Walsh
aFerkauf Graduate School of Psychology, Yeshiva University, The Bronx, NY 10461;bDepartment of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY 10032;
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Clare A. McCormack
cCenter for Science and Society, Columbia University, New York, NY 10027;
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Rachel Webster
dDepartment of Obstetrics and Gynecology, Columbia University Medical Center, New York, NY 10032;
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Anita Pinto
eData Science, Columbia University, New York, NY 10027;
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Seonjoo Lee
fDivision of Behavioral Medicine, New York State Psychiatric Institute, New York, NY 10032;gDepartment of Biostatistics (in Psychiatry), Mailman School of Public Health, Columbia University, New York, NY 10032;
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Tianshu Feng
gDepartment of Biostatistics (in Psychiatry), Mailman School of Public Health, Columbia University, New York, NY 10032;
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H. Sloan Krakovsky
dDepartment of Obstetrics and Gynecology, Columbia University Medical Center, New York, NY 10032;
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Sinclaire M. O’Grady
dDepartment of Obstetrics and Gynecology, Columbia University Medical Center, New York, NY 10032;
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Benjamin Tycko
hHackensack-Meridian Health Center for Discovery and Innovation, Nutley, NJ 07110;
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Frances A. Champagne
iDepartment of Psychiatry, Columbia University, New York, NY 10032;jDepartment of Psychology, University of Texas at Austin, Austin, TX 78712
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Elizabeth A. Werner
dDepartment of Obstetrics and Gynecology, Columbia University Medical Center, New York, NY 10032;iDepartment of Psychiatry, Columbia University, New York, NY 10032;
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Grace Liu
iDepartment of Psychiatry, Columbia University, New York, NY 10032;
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Catherine Monk
dDepartment of Obstetrics and Gynecology, Columbia University Medical Center, New York, NY 10032;fDivision of Behavioral Medicine, New York State Psychiatric Institute, New York, NY 10032;iDepartment of Psychiatry, Columbia University, New York, NY 10032;
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  • ORCID record for Catherine Monk
  • For correspondence: cem31@cumc.columbia.edu
  1. Edited by Bruce S. McEwen, Rockefeller University, New York, NY, and approved September 18, 2019 (received for review April 16, 2019)

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Significance

Despite decades of prenatal programming research showing that “the womb may be more important than the home” with respect to offspring health outcomes, no studies of which we are aware have considered multiple indicators of maternal stress to identify the types of maternal stress that most influence developing offspring. This study’s key contributions include the use of a data-driven procedure to specify types of maternal stress—psychological and subclinical physical health indicators—that predict offspring outcomes including sex at birth, risk of preterm birth, and fetal neurodevelopment. Social support is a key factor differentiating the stress groups and a malleable intervention target to improve offspring outcomes.

Abstract

Maternal prenatal stress influences offspring neurodevelopment and birth outcomes including the ratio of males to females born; however, there is limited understanding of what types of stress matter, and for whom. Using a data-driven approach with 27 variables from questionnaires, ambulatory diaries, and physical assessments collected early in the singleton pregnancies of 187 women, 3 latent profiles of maternal prenatal stress emerged that were differentially associated with sex at birth, birth outcomes, and fetal neurodevelopment. Most women (66.8%) were in the healthy group (HG); 17.1% were in the psychologically stressed group (PSYG), evidencing clinically meaningful elevations in perceived stress, depression, and anxiety; and 16% were in the physically stressed group (PHSG) with relatively higher ambulatory blood pressure and increased caloric intake. The population normative male:female secondary sex ratio (105:100) was lower in the PSYG (2:3) and PHSG (4:9), and higher in the HG (23:18), consistent with research showing diminished male births in maternal stress contexts. PHSG versus HG infants were born 1.5 wk earlier (P < 0.05) with 22% compared to 5% born preterm. PHSG versus HG fetuses had decreased fetal heart rate–movement coupling (P < 0.05), which may indicate slower central nervous system development, and PSYG versus PHSG fetuses had more birth complications, consistent with previous findings among offspring of women with psychiatric illness. Social support most strongly differentiated the HG, PSYG, and PHSG groups, and higher social support was associated with increased odds of male versus female births. Stress phenotypes in pregnant women are associated with male vulnerability and poor fetal outcomes.

  • prenatal stress
  • secondary sex ratio
  • social support
  • birth outcomes
  • neurodevelopment

Footnotes

  • ↵1To whom correspondence may be addressed. Email: cem31{at}cumc.columbia.edu.
  • Author contributions: B.T., F.A.C., and C.M. designed research; C.A.M., H.S.K., S.M.O., E.A.W., G.L., and C.M. performed research; K.W., A.P., S.L., and T.F. analyzed data; and K.W., C.A.M., R.W., and C.M. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • See Commentary on page 23877.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1905890116/-/DCSupplemental.

Published under the PNAS license.

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Maternal prenatal stress phenotypes associate with fetal neurodevelopment and birth outcomes
Kate Walsh, Clare A. McCormack, Rachel Webster, Anita Pinto, Seonjoo Lee, Tianshu Feng, H. Sloan Krakovsky, Sinclaire M. O’Grady, Benjamin Tycko, Frances A. Champagne, Elizabeth A. Werner, Grace Liu, Catherine Monk
Proceedings of the National Academy of Sciences Nov 2019, 116 (48) 23996-24005; DOI: 10.1073/pnas.1905890116

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Maternal prenatal stress phenotypes associate with fetal neurodevelopment and birth outcomes
Kate Walsh, Clare A. McCormack, Rachel Webster, Anita Pinto, Seonjoo Lee, Tianshu Feng, H. Sloan Krakovsky, Sinclaire M. O’Grady, Benjamin Tycko, Frances A. Champagne, Elizabeth A. Werner, Grace Liu, Catherine Monk
Proceedings of the National Academy of Sciences Nov 2019, 116 (48) 23996-24005; DOI: 10.1073/pnas.1905890116
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