Maternal steroids during pregnancy and their associations with exposure to lifetime stressful life events, prenatal stress appraisal and psychological functioning.

Androgens Corticosteroids Depression Estrogens Lifetime stress Perceived stress Pregnancy Sex steroids

Journal

Psychoneuroendocrinology
ISSN: 1873-3360
Titre abrégé: Psychoneuroendocrinology
Pays: England
ID NLM: 7612148

Informations de publication

Date de publication:
12 2023
Historique:
received: 01 02 2023
revised: 19 09 2023
accepted: 20 09 2023
medline: 10 11 2023
pubmed: 1 10 2023
entrez: 30 9 2023
Statut: ppublish

Résumé

During pregnancy, steroids enable physiological adaptations in response to many factors, including maternal stress or psychological functioning. While stress and psychological dysfunction can have endocrine-disrupting effects beyond cortisol disruption, associations between prenatal maternal stress or related psychological dysfunction and the broader steroid milieu remain understudied. To assess associations between independent and joint maternal stress and psychological functioning measures and steroid profiles in pregnancy (22-40 gestational weeks) in the Programming of Intergenerational Stress Mechanisms (PRISM) birth cohort (n = 334). Serum metabolomics detected 42 steroids and their metabolites, which were grouped into five classes (pregnenolone, androgens, estrogens, progestin, and corticosteroids). The Perceived Stress Scale, Life Stressor Checklist-Revised, and Edinburgh Postnatal Depression Scale indexed lifetime traumatic/non-traumatic stressors, global prenatal stress appraisal, and depressive symptoms during pregnancy, respectively. Exposures were categorized as high-low using the corresponding 3rd quartiles. We assessed associations between both individual and joint stress exposures with steroid classes using linear mixed effect models and with individual steroids using linear regressions. We also examined fetal sex-specific effects. High prenatal perceived stress was independently associated with lower levels of androgens and estrogens in the overall sample [β (95%CI): androgens: -0.13 (-0.25;-0.01); estrogens: -0.16 (-0.31;-0.01)], particularly among women carrying males [androgens: -0.22 (-0.39;-0.05); estrogens: -0.28 (-0.50;-0.07)]. Results on estrogens were consistent when considering joint exposure to both greater lifetime stressors and higher prenatal perceived stress. We also found a single testosterone metabolite-5alpha-androstan-3alpha,17alpha-diol disulfate-negatively associated with both individual high perceived stress and joint exposure to high lifetime stressors and high perceived stress among women carrying males. Increased maternal perceived stress experienced in pregnancy was independently associated with lower maternal androgen and estrogen levels during pregnancy in the overall sample, particularly among women carrying males. Results on estrogens were consistent when we considered the joint exposure of increased lifetime stressors and higher prenatal perceived stress.

Sections du résumé

BACKGROUND
During pregnancy, steroids enable physiological adaptations in response to many factors, including maternal stress or psychological functioning. While stress and psychological dysfunction can have endocrine-disrupting effects beyond cortisol disruption, associations between prenatal maternal stress or related psychological dysfunction and the broader steroid milieu remain understudied.
AIM
To assess associations between independent and joint maternal stress and psychological functioning measures and steroid profiles in pregnancy (22-40 gestational weeks) in the Programming of Intergenerational Stress Mechanisms (PRISM) birth cohort (n = 334).
METHODS
Serum metabolomics detected 42 steroids and their metabolites, which were grouped into five classes (pregnenolone, androgens, estrogens, progestin, and corticosteroids). The Perceived Stress Scale, Life Stressor Checklist-Revised, and Edinburgh Postnatal Depression Scale indexed lifetime traumatic/non-traumatic stressors, global prenatal stress appraisal, and depressive symptoms during pregnancy, respectively. Exposures were categorized as high-low using the corresponding 3rd quartiles. We assessed associations between both individual and joint stress exposures with steroid classes using linear mixed effect models and with individual steroids using linear regressions. We also examined fetal sex-specific effects.
RESULTS
High prenatal perceived stress was independently associated with lower levels of androgens and estrogens in the overall sample [β (95%CI): androgens: -0.13 (-0.25;-0.01); estrogens: -0.16 (-0.31;-0.01)], particularly among women carrying males [androgens: -0.22 (-0.39;-0.05); estrogens: -0.28 (-0.50;-0.07)]. Results on estrogens were consistent when considering joint exposure to both greater lifetime stressors and higher prenatal perceived stress. We also found a single testosterone metabolite-5alpha-androstan-3alpha,17alpha-diol disulfate-negatively associated with both individual high perceived stress and joint exposure to high lifetime stressors and high perceived stress among women carrying males.
CONCLUSIONS
Increased maternal perceived stress experienced in pregnancy was independently associated with lower maternal androgen and estrogen levels during pregnancy in the overall sample, particularly among women carrying males. Results on estrogens were consistent when we considered the joint exposure of increased lifetime stressors and higher prenatal perceived stress.

Identifiants

pubmed: 37776732
pii: S0306-4530(23)00373-6
doi: 10.1016/j.psyneuen.2023.106395
pii:
doi:

Substances chimiques

Testosterone 3XMK78S47O
Hydrocortisone WI4X0X7BPJ
Estrogens 0

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

106395

Subventions

Organisme : NIEHS NIH HHS
ID : R01 ES032242
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL095606
Pays : United States
Organisme : NIH HHS
ID : UG3 OD023337
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL114396
Pays : United States
Organisme : NIEHS NIH HHS
ID : P30 ES023515
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001433
Pays : United States
Organisme : NIEHS NIH HHS
ID : U2C ES026555
Pays : United States
Organisme : NIEHS NIH HHS
ID : R00 ES032029
Pays : United States

Informations de copyright

Copyright © 2023 Elsevier Ltd. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Auteurs

Elena Colicino (E)

Department of Environmental Medicine and Public Health, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Institute for Exposomic Research, Icahn School of Medicine at Mount Sinai, New York, NY, USA. Electronic address: elena.colicino@mssm.edu.

Whitney Cowell (W)

Departments of Pediatrics and Population Health, NYU Grossman School of Medicine, New York, NY, USA.

Nicolo Foppa Pedretti (NF)

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

Anu Joshi (A)

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

Lauren Petrick (L)

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

Megan Niedzwiecki (M)

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

Robert O Wright (RO)

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

Rosalind J Wright (RJ)

Department of Environmental Medicine and Public Health, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Institute for Exposomic Research, Icahn School of Medicine at Mount Sinai, New York, NY, USA; Kravis Children's Hospital, Department of Pediatrics, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

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Classifications MeSH