Epigenome-wide meta-analysis of prenatal maternal stressful life events and newborn DNA methylation.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
10 Mar 2023
10 Mar 2023
Historique:
received:
28
07
2022
accepted:
21
02
2023
revised:
08
02
2023
entrez:
10
3
2023
pubmed:
11
3
2023
medline:
11
3
2023
Statut:
aheadofprint
Résumé
Prenatal maternal stressful life events are associated with adverse neurodevelopmental outcomes in offspring. Biological mechanisms underlying these associations are largely unknown, but DNA methylation likely plays a role. This meta-analysis included twelve non-overlapping cohorts from ten independent longitudinal studies (N = 5,496) within the international Pregnancy and Childhood Epigenetics consortium to examine maternal stressful life events during pregnancy and DNA methylation in cord blood. Children whose mothers reported higher levels of cumulative maternal stressful life events during pregnancy exhibited differential methylation of cg26579032 in ALKBH3. Stressor-specific domains of conflict with family/friends, abuse (physical, sexual, and emotional), and death of a close friend/relative were also associated with differential methylation of CpGs in APTX, MyD88, and both UHRF1 and SDCCAG8, respectively; these genes are implicated in neurodegeneration, immune and cellular functions, regulation of global methylation levels, metabolism, and schizophrenia risk. Thus, differences in DNA methylation at these loci may provide novel insights into potential mechanisms of neurodevelopment in offspring.
Identifiants
pubmed: 36899042
doi: 10.1038/s41380-023-02010-5
pii: 10.1038/s41380-023-02010-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Medical Research Council
ID : G9815508
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_PC_15018
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_PC_19009
Pays : United Kingdom
Organisme : NICHD NIH HHS
ID : R21 HD085849
Pays : United States
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Lautarescu A, Craig MC, Glover V. Prenatal stress: effects on fetal and child brain development. Int Rev Neurobiol. 2020;150:17–40.
pubmed: 32204831
doi: 10.1016/bs.irn.2019.11.002
Coussons-Read ME. Effects of prenatal stress on pregnancy and human development: mechanisms and pathways. Obstet Med. 2013;6:52–7.
pubmed: 27757157
pmcid: 5052760
doi: 10.1177/1753495x12473751
Orr ST, James SA, Casper R. Psychosocial stressors and low birth weight. J Dev Behav Pediatr. 1992;13:343–7.
pubmed: 1401118
doi: 10.1097/00004703-199210010-00005
Ruiz R, Fullerton J. The measurement of stress in pregnancy. Nurs Health Sci. 1999;1:19–25.
pubmed: 10894648
doi: 10.1046/j.1442-2018.1999.00004.x
March of Dimes. Stress and Pregnancy. 2023; at https://www.marchofdimes.org/find-support/topics/pregnancy/stress-and-pregnancy .
Brunst KJ, Zhang L, Zhang X, Baccarelli AA, Bloomquist T, Wright RJ. Associations between maternal lifetime stress and placental mitochondrial DNA mutations in an urban multiethnic cohort. Biol Psychiatry. 2021;89:570–8.
pubmed: 33229036
doi: 10.1016/j.biopsych.2020.09.013
Glover V, O’Donnell KJ, O’Connor TG, Fisher J. Prenatal maternal stress, fetal programming, and mechanisms underlying later psychopathology—A global perspective. Dev Psychopathol. 2018;30:843–54.
pubmed: 30068411
doi: 10.1017/S095457941800038X
Van den Bergh BRH, van den Heuvel MI, Lahti M, Braeken M, de Rooij SR, Entringer S, et al. Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neurosci Biobehav Rev. 2017;117:26–64.
pubmed: 28757456
doi: 10.1016/j.neubiorev.2017.07.003
Araji S, Griffin A, Dixon L, Spencer S-K, Peavie C, Wallace K. An overview of maternal anxiety during pregnancy and the post-partum period. J Ment Health Clin Psychol. 2020;4:47–56.
Dunkel Schetter C, Tanner L. Anxiety, depression and stress in pregnancy: implications for mothers, children, research, and practice. Curr Opin Psychiatry. 2012;25:141–8.
pubmed: 22262028
pmcid: 4447112
doi: 10.1097/YCO.0b013e3283503680
Dunkel Schetter C, Glynn L. Stress in pregnancy: Empirical evidence and theoretical issues to guide interdisciplinary research. In: Contrada RJ, Baum A, editors. The handbook of stress science: biology, psychology, and health. Springer Publishing; 2011;321–47.
Hobel CJ, Goldstein AMY, Barrett ES. Psychosocial stress and pregnancy outcome. Clin Obstet Gynecol. 2008;51:333–48.
pubmed: 18463464
doi: 10.1097/GRF.0b013e31816f2709
Wadhwa PD, Entringer S, Buss C, Lu MC. The contribution of maternal stress to preterm birth: issues and considerations. Clin Perinatol. 2011;38:351–84.
pubmed: 21890014
pmcid: 3179976
doi: 10.1016/j.clp.2011.06.007
Rosa MJ, Nentin F, Bosquet Enlow M, Hacker MR, Pollas N, Coull B, et al. Sex-specific associations between prenatal negative life events and birth outcomes. Stress. 2019;22:647–53.
pubmed: 31057018
pmcid: 6776698
doi: 10.1080/10253890.2019.1608944
van Meel ER, Saharan G, Jaddoe VWV, de Jongste JC, Reiss IKM, Tiemeier H, et al. Parental psychological distress during pregnancy and the risk of childhood lower lung function and asthma: a population-based prospective cohort study. Thorax. 2020;75:1074–81.
pubmed: 33046570
doi: 10.1136/thoraxjnl-2019-214099
Brunst KJ, Rosa MJ, Jara C, Lipton LR, Lee A, Coull BA, et al. Impact of maternal lifetime interpersonal trauma on childrenʼs asthma. Psychosom Med. 2017;79:91–100.
pubmed: 27359172
pmcid: 5182122
doi: 10.1097/PSY.0000000000000354
Lee A, Mathilda Chiu YH, Rosa MJ, Jara C, Wright RO, Coull BA, et al. Prenatal and postnatal stress and asthma in children: temporal- and sex-specific associations. J Allergy Clin Immunol. 2016;138:740–7.
pubmed: 26953156
pmcid: 5011027
doi: 10.1016/j.jaci.2016.01.014
Lee AG, Chiu YM, Rosa MJ, Cohen S, Coull BA, Wright RO, et al. Association of prenatal and early childhood stress with reduced lung function in 7-year-olds. Ann Allergy Asthma Immunol. 2017;119:153–9.
pubmed: 28668548
pmcid: 5554462
doi: 10.1016/j.anai.2017.05.025
Lahti M, Savolainen K, Tuovinen S, Pesonen A-K, Lahti J, Heinonen K, et al. Maternal depressive symptoms during and after pregnancy and psychiatric problems in children. J Am Acad Child Adolesc Psychiatry. 2017;56:30–9.
pubmed: 27993226
doi: 10.1016/j.jaac.2016.10.007
Herba CM, Glover V, Ramchandani PG, Rondon MB. Maternal depression and mental health in early childhood: an examination of underlying mechanisms in low-income and middle-income countries. Lancet Psychiatry. 2016;3:983–92.
pubmed: 27650772
doi: 10.1016/S2215-0366(16)30148-1
Tarabulsy GM, Pearson J, Vaillancourt-Morel M-P, Bussières E-L, Madigan S, Lemelin J-P, et al. Meta-analytic findings of the relation between maternal prenatal stress and anxiety and child cognitive outcome. J Dev Behav Pediatr. 2014;35:38–43.
pubmed: 24345757
doi: 10.1097/DBP.0000000000000003
Pearson RM, Bornstein MH, Cordero M, Scerif G, Mahedy L, Evans J, et al. Maternal perinatal mental health and offspring academic achievement at age 16: the mediating role of childhood executive function. J Child Psychol Psychiatry. 2015;57:491–501.
pubmed: 26616637
pmcid: 4789117
doi: 10.1111/jcpp.12483
Mennes M, Bergh BVD, Lagae L, Stiers P. Developmental brain alterations in 17 year old boys are related to antenatal maternal anxiety. Clin Neurophysiol. 2009;120:1116–22.
pubmed: 19433367
doi: 10.1016/j.clinph.2009.04.003
Bergh BRHVD, Mennes M, Oosterlaan J, Stevens V, Stiers P, Marcoen A, et al. High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neurosci Biobehav Rev. 2005;29:259–69.
pubmed: 15811497
doi: 10.1016/j.neubiorev.2004.10.010
Davis EP, Hankin BL, Glynn LM, Head K, Kim DJ, Sandman CA. Prenatal maternal stress, child cortical thickness, and adolescent depressive symptoms. Child Development. 2019;91:e432–50.
Buss C, Davis EP, Muftuler LT, Head K, Sandman CA. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9-year-old children. Psychoneuroendocrinology. 2010;35:141–53.
pubmed: 19674845
pmcid: 2795128
doi: 10.1016/j.psyneuen.2009.07.010
Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, et al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry. 2008;65:146.
pubmed: 18250252
doi: 10.1001/archgenpsychiatry.2007.20
Cao-Lei L, de Rooij SR, King S, Matthews SG, Metz GAS, Roseboom TJ, et al. Prenatal stress and epigenetics. Neurosci Biobehav Rev. 2020;117:198–210.
pubmed: 28528960
doi: 10.1016/j.neubiorev.2017.05.016
Dadds MR, Moul C, Hawes DJ, Mendoza Diaz A, Brennan J. Individual differences in childhood behavior disorders associated with epigenetic modulation of the cortisol receptor gene. Child Dev. 2015;86:1311–20.
pubmed: 26152664
doi: 10.1111/cdev.12391
Heinrich A, Buchmann AF, Zohsel K, Dukal H, Frank J, Treutlein J, et al. Alterations of glucocorticoid receptor gene methylation in externalizing disorders during childhood and adolescence. Behav Genet. 2015;45:529–36.
pubmed: 25894927
doi: 10.1007/s10519-015-9721-y
Radtke KM, Ruf M, Gunter HM, Dohrmann K, Schauer M, Meyer A, et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl Psychiatry. 2011;1:e21–e21.
pubmed: 22832523
pmcid: 3309516
doi: 10.1038/tp.2011.21
Brunst KJ, Tignor N, Just A, Liu Z, Lin X, Hacker MR, et al. Cumulative lifetime maternal stress and epigenome-wide placental DNA methylation in the PRISM cohort. Epigenetics. 2018;13:665–81.
pubmed: 30001177
pmcid: 6291301
doi: 10.1080/15592294.2018.1497387
Rijlaarsdam J, Pappa I, Walton E, Bakermans-Kranenburg MJ, Mileva-Seitz VR, Rippe RCA, et al. An epigenome-wide association meta-analysis of prenatal maternal stress in neonates: a model approach for replication. Epigenetics. 2016;11:140–9.
pubmed: 26889969
pmcid: 4846102
doi: 10.1080/15592294.2016.1145329
Polinski KJ, Putnick DL, Robinson SL, Schliep KC, Silver RM, Guan W, et al. Periconception and prenatal exposure to maternal perceived stress and cord blood DNA methylation. Epigenet Insights. 2022;15:25168657221082045.
pubmed: 35237744
pmcid: 8882928
doi: 10.1177/25168657221082045
Lund RJ, Kyläniemi M, Pettersson N, Kaukonen R, Konki M, Scheinin NM, et al. Placental DNA methylation marks are associated with maternal depressive symptoms during early pregnancy. Neurobiol Stress. 2021;15:100374.
pubmed: 34401410
pmcid: 8353413
doi: 10.1016/j.ynstr.2021.100374
Tesfaye M, Chatterjee S, Zeng X, Joseph P, Tekola-Ayele F. Impact of depression and stress on placental DNA methylation in ethnically diverse pregnant women. Epigenomics. 2021;13:1485–96.
pubmed: 34585950
pmcid: 8503803
doi: 10.2217/epi-2021-0192
Bakulski KM, Halladay A, Hu VW, Mill J, Fallin MD. Epigenetic research in neuropsychiatric disorders: the “tissue issue”. Curr Behav Neurosci Rep. 2016;3:264–74.
pubmed: 28093577
pmcid: 5235359
doi: 10.1007/s40473-016-0083-4
Felix JF, Joubert BR, Baccarelli AA, Sharp GC, Almqvist C, Annesi-Maesano I, et al. Cohort profile: pregnancy and childhood epigenetics (PACE) consortium. Int J Epidemiol. 2018;47:22–3u.
pubmed: 29025028
doi: 10.1093/ije/dyx190
Croft J, Heron J, Teufel C, Cannon M, Wolke D, Thompson A, et al. Association of trauma type, age of exposure, and frequency in childhood and adolescence with psychotic experiences in early adulthood. JAMA Psychiatry. 2019;76:79–86.
pubmed: 30477014
doi: 10.1001/jamapsychiatry.2018.3155
Miller-Lewis LR, Searle AK, Sawyer MG, Baghurst PA, Hedley D. Resource factors for mental health resilience in early childhood: an analysis with multiple methodologies. Child Adolesc Psychiatry Ment Health. 2013;7:6.
pubmed: 23432929
pmcid: 3598384
doi: 10.1186/1753-2000-7-6
Cortes Hidalgo AP, Tiemeier H, Metcalf SA, Monninger M, Meyer-Lindenberg A, Aggensteiner PM, et al. No robust evidence for an interaction between early-life adversity and protective factors on global and regional brain volumes. Dev Cogn Neurosci. 2022;58:101166.
pubmed: 36327649
pmcid: 9636055
doi: 10.1016/j.dcn.2022.101166
Chen YA, Lemire M, Choufani S, Butcher DT, Grafodatskaya D, Zanke BW, et al. Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray. Epigenetics. 2013;8:203–9.
pubmed: 23314698
pmcid: 3592906
doi: 10.4161/epi.23470
McCartney DL, Walker RM, Morris SW, McIntosh AM, Porteous DJ, Evans KL. Identification of polymorphic and off-target probe binding sites on the Illumina Infinium MethylationEPIC BeadChip. Genom Data. 2016;9:22–4.
pubmed: 27330998
pmcid: 4909830
doi: 10.1016/j.gdata.2016.05.012
Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinforma. 2012;13:86.
doi: 10.1186/1471-2105-13-86
Gervin K, Salas LA, Bakulski KM, van Zelm MC, Koestler DC, Wiencke JK, et al. Systematic evaluation and validation of reference and library selection methods for deconvolution of cord blood DNA methylation data. Clin Epigenetics. 2019;11:125.
pubmed: 31455416
pmcid: 6712867
doi: 10.1186/s13148-019-0717-y
Venables WN, Ripley BD. Modern Applied Statistics with S, 4th ed. Springer: New York; 2002. https://www.stats.ox.ac.uk/pub/MASS4/ .
Min JL, Hemani G, Davey Smith G, Relton C, Suderman M. Meffil: efficient normalization and analysis of very large DNA methylation datasets. Bioinformatics. 2018;34:3983–89.
Willer CJ, Li Y, Abecasis GR. METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics. 2010;26:2190–1.
pubmed: 20616382
pmcid: 2922887
doi: 10.1093/bioinformatics/btq340
Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.
pubmed: 12111919
doi: 10.1002/sim.1186
Saffari A, Silver MJ, Zavattari P, Moi L, Columbano A, Meaburn EL, et al. Estimation of a significance threshold for epigenome-wide association studies. Genet Epidemiol. 2017;42:20–33.
pubmed: 29034560
pmcid: 5813244
doi: 10.1002/gepi.22086
Peters TJ, Buckley MJ, Statham AL, Pidsley R, Samaras K, V Lord R, et al. De novo identification of differentially methylated regions in the human genome. Epigenetics Chromatin. 2015;8:6.
pubmed: 25972926
pmcid: 4429355
doi: 10.1186/1756-8935-8-6
Sammallahti S, Cortes Hidalgo AP, Tuominen S, Malmberg A, Mulder RH, Brunst KJ. et al. Maternal anxiety during pregnancy and newborn epigenome-wide DNA methylation. Mol Psychiatry. 2021;26:1832–45.
Rakyan VK, Down TA, Balding DJ, Beck S. Epigenome-wide association studies for common human diseases. Nat Rev Genet. 2011;12:529–41.
pubmed: 21747404
pmcid: 3508712
doi: 10.1038/nrg3000
van Dongen J, Nivard MG, Willemsen G, Hottenga J-J, Helmer Q, Dolan CV, et al. Genetic and environmental influences interact with age and sex in shaping the human methylome. Nat Commun. 2016;7:11115.
pubmed: 27051996
pmcid: 4820961
doi: 10.1038/ncomms11115
Hannon E, Knox O, Sugden K, Burrage J, Wong CCY, Belsky DW, et al. Characterizing genetic and environmental influences on variable DNA methylation using monozygotic and dizygotic twins. PLOS Genet. 2018;14:e1007544.
pubmed: 30091980
pmcid: 6084815
doi: 10.1371/journal.pgen.1007544
Min JL, Hemani G, Hannon E, Dekkers KF, Castillo-Fernandez J, Luijk R, et al. Genomic and phenotypic insights from an atlas of genetic effects on DNA methylation. Nat Genet. 2021;53:1311–21.
pubmed: 34493871
pmcid: 7612069
doi: 10.1038/s41588-021-00923-x
Edgar RD, Jones MJ, Meaney MJ, Turecki G, Kobor MS. BECon: a tool for interpreting DNA methylation findings from blood in the context of brain. Transl Psychiatry. 2017;7:e1187.
pubmed: 28763057
pmcid: 5611738
doi: 10.1038/tp.2017.171
Ruiz-Arenas C, Hernandez-Ferrer C, Vives-Usano M, Mari S, Quintela I, Mason D. et al. Identification of autosomal cis expression quantitative trait methylation (cis eQTMs) in children’s blood. eLife. 2022;11:e65310.
Ramesh V, Bayam E, Cernilogar FM, Bonapace IM, Schulze M, Riemenschneider MJ, et al. Loss of Uhrf1 in neural stem cells leads to activation of retroviral elements and delayed neurodegeneration. Genes Dev. 2016;30:2199–212.
pubmed: 27798843
pmcid: 5088568
doi: 10.1101/gad.284992.116
Schroeder P, Rivalan M, Zaqout S, Kruger C, Schuler J, Long M, et al. Abnormal brain structure and behavior in MyD88-deficient mice. Brain Behav Immun. 2021;91:181–93.
pubmed: 33002631
doi: 10.1016/j.bbi.2020.09.024
Li G, Forero MG, Wentzell JS, Durmus I, Wolf R, Anthoney NC. et al. A Toll-receptor map underlies structural brain plasticity. eLife. 2020;9:e52743.
Harrison JS, Cornett EM, Goldfarb D, DaRosa PA, Li ZM, Yan F. et al. Hemi-methylated DNA regulates DNA methylation inheritance through allosteric activation of H3 ubiquitylation by UHRF1. eLife. 2016;5:e17101.
Watanabe K, Stringer S, Frei O, Umicevic Mirkov M, de Leeuw C, Polderman TJC, et al. A global overview of pleiotropy and genetic architecture in complex traits. Nat Genet. 2019;51:1339–48.
pubmed: 31427789
doi: 10.1038/s41588-019-0481-0
Hoffman GE, Ma Y, Montgomery KS, Bendl J, Jaiswal MK, Kozlenkov A, et al. Sex differences in the human brain transcriptome of cases with schizophrenia. Biol Psychiatry. 2022;91:92–101.
pubmed: 34154796
doi: 10.1016/j.biopsych.2021.03.020
Flynn M, Whitton L, Donohoe G, Morrison CG, Morris DW. Altered gene regulation as a candidate mechanism by which ciliopathy gene SDCCAG8 contributes to schizophrenia and cognitive function. Hum Mol Genet. 2020;29:407–17.
pubmed: 31868218
doi: 10.1093/hmg/ddz292
Hamshere ML, Walters JT, Smith R, Richards AL, Green E, Grozeva D, et al. Genome-wide significant associations in schizophrenia to ITIH3/4, CACNA1C and SDCCAG8, and extensive replication of associations reported by the schizophrenia PGC. Mol Psychiatry. 2013;18:708–12.
pubmed: 22614287
doi: 10.1038/mp.2012.67
Monk C, Lugo-Candelas C, Trumpff C. Prenatal developmental origins of future psychopathology: mechanisms and pathways. Ann Rev Clin Psychol. 2019;15:317–44.
Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010;11:373–84.
pubmed: 20404851
doi: 10.1038/ni.1863
Lee Y, Choi I, Kim J, Kim K. DNA damage to human genetic disorders with neurodevelopmental defects. J Genet Med. 2016;13:1–13.
doi: 10.5734/JGM.2016.13.1.1
Qi T, Wu Y, Zeng J, Zhang F, Xue A, Jiang L. et al. Identifying gene targets for brain-related traits using transcriptomic and methylomic data from blood. Nat Commun. 2018;9:2282.
Joseph RM. Neuronatin gene: Imprinted and misfolded: Studies in Lafora disease, diabetes and cancer may implicate NNAT-aggregates as a common downstream participant in neuronal loss. Genomics. 2014;103:183–8.
pubmed: 24345642
doi: 10.1016/j.ygeno.2013.12.001
Dunn EC, Soare TW, Zhu Y, Simpkin AJ, Suderman MJ, Klengel T, et al. Sensitive periods for the effect of childhood adversity on DNA methylation: results from a prospective, longitudinal study. Biol Psychiatry. 2019;85:838–49.
pubmed: 30905381
pmcid: 6552666
doi: 10.1016/j.biopsych.2018.12.023
Liu J, Cerutti J, Lussier AA, Zhu Y, Smith BJ, Smith A et al. Socioeconomic changes predict genome-wide DNA methylation in childhood. Hum Mol Genet. 2022;32:709–19.
Lussier AA, Zhu Y, Smith BJ, Simpkin AJ, Smith A, Suderman MJ, et al. Updates to data versions and analytic methods influence the reproducibility of results from epigenome-wide association studies. Epigenetics. 2022;17:1373–88.
pubmed: 35156895
pmcid: 9601563
doi: 10.1080/15592294.2022.2028072
Merid SK, Novoloaca A, Sharp GC, Kupers LK, Kho AT, Roy R, et al. Epigenome-wide meta-analysis of blood DNA methylation in newborns and children identifies numerous loci related to gestational age. Genome Med. 2020;12:25.
pubmed: 32114984
pmcid: 7050134
doi: 10.1186/s13073-020-0716-9
Reese SE, Xu CJ, den Dekker HT, Lee MK, Sikdar S, Ruiz-Arenas C, et al. Epigenome-wide meta-analysis of DNA methylation and childhood asthma. J Allergy Clin Immunol. 2019;143:2062–74.
pubmed: 30579849
doi: 10.1016/j.jaci.2018.11.043
Maccani JZJ, Koestler DC, Lester B, Houseman EA, Armstrong DA, Kelsey KT, et al. Placental DNA methylation related to both infant toenail mercury and adverse neurobehavioral outcomes. Environ Health Perspect. 2015;123:723–9.
pubmed: 25748564
pmcid: 4492267
doi: 10.1289/ehp.1408561
Lee KWK, Richmond R, Hu P, French L, Shin J, Bourdon C, et al. Prenatal exposure to maternal cigarette smoking and dna methylation: epigenome-wide association in a discovery sample of adolescents and replication in an independent cohort at birth through 17 years of age. Environ Health Perspect. 2015;123:193–9.
pubmed: 25325234
doi: 10.1289/ehp.1408614
Ghazi T, Naidoo P, Naidoo RN, Chuturgoon AA. Prenatal air pollution exposure and placental dna methylation changes: implications on fetal development and future disease susceptibility. Cells. 2021;10:3025.
pubmed: 34831248
pmcid: 8616150
doi: 10.3390/cells10113025
Alves AC, Cecatti JG, Souza RT. Resilience and stress during pregnancy: a comprehensive multidimensional approach in maternal and perinatal health. Sci World J. 2021;2021:9512854.
doi: 10.1155/2021/9512854