Cargando…

Gender-specific associations of pregnancy-related anxiety with placental epigenetic patterning of glucocorticoid response genes and preschooler’s emotional symptoms and hyperactivity

BACKGROUD: We have recently reported that maternal prenatal pregnancy-related anxiety predicts preschoolers’ emotional and behavioral development in a gender-dependent manner. This study aims to test for this gender-specific effect in a different cohort and investigate whether the gender difference...

Descripción completa

Detalles Bibliográficos
Autores principales: Liu, Hui, Liu, Yuwei, Huang, Kun, Yan, Shuangqin, Hao, Jiahu, Zhu, Peng, Tao, Fangbiao, Shao, Shanshan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8555194/
https://www.ncbi.nlm.nih.gov/pubmed/34715840
http://dx.doi.org/10.1186/s12887-021-02938-z
_version_ 1784591928498585600
author Liu, Hui
Liu, Yuwei
Huang, Kun
Yan, Shuangqin
Hao, Jiahu
Zhu, Peng
Tao, Fangbiao
Shao, Shanshan
author_facet Liu, Hui
Liu, Yuwei
Huang, Kun
Yan, Shuangqin
Hao, Jiahu
Zhu, Peng
Tao, Fangbiao
Shao, Shanshan
author_sort Liu, Hui
collection PubMed
description BACKGROUD: We have recently reported that maternal prenatal pregnancy-related anxiety predicts preschoolers’ emotional and behavioral development in a gender-dependent manner. This study aims to test for this gender-specific effect in a different cohort and investigate whether the gender difference was specific to placental methylation of genes regulating glucocorticoids. METHODS: A total of 2405 mother–child pairs from the Ma’anshan Birth Cohort Study were included in present study. The maternal pregnancy-related anxiety symptoms were evaluated with the Pregnancy-Related Anxiety Questionnaire in the third trimester of pregnancy. Child neurobehavior was assessed with the Strengths and Difficulties Questionnaire at 4 years old. Placental methylation of FKBP5, NR3C1 and HSD11B2 genes was quantified using the MethylTarget approach in 439 pregnant women. After exploratory factor analysis, the associations between methylation factor scores and pregnancy-related anxiety and child neurobehavior were examined using logistic regression analysis. RESULTS: After controlling for confounding factors, pregnancy-related anxiety in the third trimester of pregnancy increased the risk of hyperactivity only in boys and emotional symptoms only in girls. Decreased scores of the factor characterized by FKBP5 methylation were associated with maternal pregnancy-related anxiety only in boys. Furthermore, increased scores of the factors characterized by NR3C1 and HSD11B2 methylation were associated with hyperactivity (NR3C1: adjusted OR = 1.80, 95%CI = 1.15–2.83) and emotional symptoms (HSD11B2: adjusted OR = 0.53, 95%CI = 0.29–0.97; NR3C1: adjusted OR = 1.64, 95%CI = 1.03–2.59) only in boys. However, the scores of the factor characterized by FKBP5, NR3C1 and HSD11B2 did not mediate the relationship between maternal pregnancy-related anxiety and preschoolers’ emotional symptoms and hyperactivity. CONCLUSIONS: Our results suggested that pregnancy-related anxiety in the third trimester of pregnancy predicted preschoolers’ emotional symptoms and hyperactivity in a gender-dependent manner. Although we did not find the mediation role of the placental methylation of genes regulating glucocorticoids, we found it was associated with both maternal pregnancy-related anxiety and preschoolers’ emotional symptoms and hyperactivity in a gender-dependent manner. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12887-021-02938-z.
format Online
Article
Text
id pubmed-8555194
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-85551942021-10-29 Gender-specific associations of pregnancy-related anxiety with placental epigenetic patterning of glucocorticoid response genes and preschooler’s emotional symptoms and hyperactivity Liu, Hui Liu, Yuwei Huang, Kun Yan, Shuangqin Hao, Jiahu Zhu, Peng Tao, Fangbiao Shao, Shanshan BMC Pediatr Research BACKGROUD: We have recently reported that maternal prenatal pregnancy-related anxiety predicts preschoolers’ emotional and behavioral development in a gender-dependent manner. This study aims to test for this gender-specific effect in a different cohort and investigate whether the gender difference was specific to placental methylation of genes regulating glucocorticoids. METHODS: A total of 2405 mother–child pairs from the Ma’anshan Birth Cohort Study were included in present study. The maternal pregnancy-related anxiety symptoms were evaluated with the Pregnancy-Related Anxiety Questionnaire in the third trimester of pregnancy. Child neurobehavior was assessed with the Strengths and Difficulties Questionnaire at 4 years old. Placental methylation of FKBP5, NR3C1 and HSD11B2 genes was quantified using the MethylTarget approach in 439 pregnant women. After exploratory factor analysis, the associations between methylation factor scores and pregnancy-related anxiety and child neurobehavior were examined using logistic regression analysis. RESULTS: After controlling for confounding factors, pregnancy-related anxiety in the third trimester of pregnancy increased the risk of hyperactivity only in boys and emotional symptoms only in girls. Decreased scores of the factor characterized by FKBP5 methylation were associated with maternal pregnancy-related anxiety only in boys. Furthermore, increased scores of the factors characterized by NR3C1 and HSD11B2 methylation were associated with hyperactivity (NR3C1: adjusted OR = 1.80, 95%CI = 1.15–2.83) and emotional symptoms (HSD11B2: adjusted OR = 0.53, 95%CI = 0.29–0.97; NR3C1: adjusted OR = 1.64, 95%CI = 1.03–2.59) only in boys. However, the scores of the factor characterized by FKBP5, NR3C1 and HSD11B2 did not mediate the relationship between maternal pregnancy-related anxiety and preschoolers’ emotional symptoms and hyperactivity. CONCLUSIONS: Our results suggested that pregnancy-related anxiety in the third trimester of pregnancy predicted preschoolers’ emotional symptoms and hyperactivity in a gender-dependent manner. Although we did not find the mediation role of the placental methylation of genes regulating glucocorticoids, we found it was associated with both maternal pregnancy-related anxiety and preschoolers’ emotional symptoms and hyperactivity in a gender-dependent manner. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12887-021-02938-z. BioMed Central 2021-10-29 /pmc/articles/PMC8555194/ /pubmed/34715840 http://dx.doi.org/10.1186/s12887-021-02938-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Liu, Hui
Liu, Yuwei
Huang, Kun
Yan, Shuangqin
Hao, Jiahu
Zhu, Peng
Tao, Fangbiao
Shao, Shanshan
Gender-specific associations of pregnancy-related anxiety with placental epigenetic patterning of glucocorticoid response genes and preschooler’s emotional symptoms and hyperactivity
title Gender-specific associations of pregnancy-related anxiety with placental epigenetic patterning of glucocorticoid response genes and preschooler’s emotional symptoms and hyperactivity
title_full Gender-specific associations of pregnancy-related anxiety with placental epigenetic patterning of glucocorticoid response genes and preschooler’s emotional symptoms and hyperactivity
title_fullStr Gender-specific associations of pregnancy-related anxiety with placental epigenetic patterning of glucocorticoid response genes and preschooler’s emotional symptoms and hyperactivity
title_full_unstemmed Gender-specific associations of pregnancy-related anxiety with placental epigenetic patterning of glucocorticoid response genes and preschooler’s emotional symptoms and hyperactivity
title_short Gender-specific associations of pregnancy-related anxiety with placental epigenetic patterning of glucocorticoid response genes and preschooler’s emotional symptoms and hyperactivity
title_sort gender-specific associations of pregnancy-related anxiety with placental epigenetic patterning of glucocorticoid response genes and preschooler’s emotional symptoms and hyperactivity
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8555194/
https://www.ncbi.nlm.nih.gov/pubmed/34715840
http://dx.doi.org/10.1186/s12887-021-02938-z
work_keys_str_mv AT liuhui genderspecificassociationsofpregnancyrelatedanxietywithplacentalepigeneticpatterningofglucocorticoidresponsegenesandpreschoolersemotionalsymptomsandhyperactivity
AT liuyuwei genderspecificassociationsofpregnancyrelatedanxietywithplacentalepigeneticpatterningofglucocorticoidresponsegenesandpreschoolersemotionalsymptomsandhyperactivity
AT huangkun genderspecificassociationsofpregnancyrelatedanxietywithplacentalepigeneticpatterningofglucocorticoidresponsegenesandpreschoolersemotionalsymptomsandhyperactivity
AT yanshuangqin genderspecificassociationsofpregnancyrelatedanxietywithplacentalepigeneticpatterningofglucocorticoidresponsegenesandpreschoolersemotionalsymptomsandhyperactivity
AT haojiahu genderspecificassociationsofpregnancyrelatedanxietywithplacentalepigeneticpatterningofglucocorticoidresponsegenesandpreschoolersemotionalsymptomsandhyperactivity
AT zhupeng genderspecificassociationsofpregnancyrelatedanxietywithplacentalepigeneticpatterningofglucocorticoidresponsegenesandpreschoolersemotionalsymptomsandhyperactivity
AT taofangbiao genderspecificassociationsofpregnancyrelatedanxietywithplacentalepigeneticpatterningofglucocorticoidresponsegenesandpreschoolersemotionalsymptomsandhyperactivity
AT shaoshanshan genderspecificassociationsofpregnancyrelatedanxietywithplacentalepigeneticpatterningofglucocorticoidresponsegenesandpreschoolersemotionalsymptomsandhyperactivity