Prenatal Stress, Mood, and Gray Matter Volume in Young Adulthood
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
MOP125892
CIHR - Canada
PubMed
29425268
PubMed Central
PMC6373666
DOI
10.1093/cercor/bhy030
PII: 4841691
Knihovny.cz E-zdroje
- MeSH
- afekt fyziologie MeSH
- dospělí MeSH
- lidé MeSH
- magnetická rezonanční tomografie MeSH
- mladý dospělý MeSH
- mozek patologie MeSH
- pohlavní dimorfismus MeSH
- psychický stres patologie psychologie MeSH
- šedá hmota patologie MeSH
- těhotenství MeSH
- zpožděný efekt prenatální expozice patologie psychologie MeSH
- Check Tag
- dospělí MeSH
- lidé MeSH
- mladý dospělý MeSH
- mužské pohlaví MeSH
- těhotenství MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
This study aimed to determine whether prenatal stress, measured by the number of stressful life events during the first 20 weeks of pregnancy, might relate to mood dysregulation and altered brain structure in young adulthood. Participants included 93 young adults from a community-based birth cohort from the Czech Republic. Information on prenatal stress exposure was collected from their mothers in 1990-1992. Magnetic resonance imaging (MRI) and mood-related data were collected from the young adults in 2015. MRI analyses focused on overall gray matter (GM) volume and GM volume of cortical regions previously associated with major depression. Higher prenatal stress predicted more mood dysregulation, lower overall GM volume, and lower GM volume in mid-dorsolateral frontal cortex, anterior cingulate cortex, and precuneus in young adulthood. We observed no prenatal stress by sex interactions for any of the relations. We conclude that prenatal stress is an important risk factor that relates to worse mood states and altered brain structure in young adulthood irrespective of sex. Our results point to the importance and long-lasting effects of prenatal programming and suggest that offspring of mothers who went through substantial stress during pregnancy might benefit from early intervention that would reduce the odds of mental illness in later life.
Child Mind Institute New York NY USA
Department of Neurology St Anne's University Hospital and Faculty of medicine MU Brno Czech Republic
Departments of Psychology and Psychiatry University of Toronto Toronto ON Canada
Research Centre for Toxic Compounds in the Environment Faculty of Science MU Brno Czech Republic
Zobrazit více v PubMed
Bangasser DA, Valentino RJ.. 2014. Sex differences in stress-related psychiatric disorders: neurobiological perspectives. Front Neuroendocrinol. 35(3):303–319. PubMed PMC
Bock J, Rether K, Gröger N, Xie L, Braun K.. 2014. Perinatal programming of emotional brain circuits: an integrative view from systems to molecules. Front Neurosci. 8:11. PubMed PMC
Bock J, Wainstock T, Braun K, Segal M.. 2015. Stress in utero: prenatal programming of brain plasticity and cognition. Biol Psychiatry. 78(5). 10.1016/j.biopsych.2015.02.036. PubMed DOI
Brand SR, Engel SM, Canfield RL, Yehuda R.. 2006. The effect of maternal PTSD following in utero trauma exposure on behavior and temperament in the 9-month-old infant. Ann N Y Acad Sci. 1071:454–458. PubMed
Brown AS, van Os J, Driessens C, Hoek HW, Susser ES.. 2000. Further evidence of relation between prenatal famine and major affective disorder. Am. Psychiatry. 157(2):190–195. PubMed
Buss C, Davis EP, Muftuler LT, Head K, Sandman CA.. 2010. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9 year old children. Psychoneuroendocrinology. 35(1):141–153. PubMed PMC
Buss C, Davis EP, Class QA, Gierczak M, Pattillo C, Glynn LM, Sandman CA. 2009. Maturation of the human fetal startle response: Evidence for sex-specific maturation of the human fetus. Early Hum Dev. 85:633–638. PubMed PMC
Buss C, Davis EP, Shahbaba B, Pruessner JC, Head K, Sandman CA.. 2012. Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proc Natl Acad Sci USA. 109:E1312–9. PubMed PMC
Cavanna AE, Trimble MR.. 2006. The precuneus: a review of its functional anatomy and behavioral correlates. Brain. 129:564–583. PubMed
Clifton VL. 2010. Review: Sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 31(Suppl):S33–S39. PubMed
Cohen RA, Grieve S, Hoth KF, Paul RH, Sweet L, Tate D, Gunstad J, Stroud L, McCaffery J, Hitsman B, et al. . 2006. Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol Psychiatry. 59(10):975–982. PubMed
Constantinof A, Moisiadis VG, Matthews SG.. 2016. Programming of stress pathways: a transgenerational perspective. J Steroid Biochem Mol Biol. 160:175–180. PubMed
Dipietro JA, Novak MF, Costigan KA, Atella LD, Reusing SP.. 2006. Maternal psychological distress during pregnancy in relation to child development at age two. Child Dev. 77:573–587. PubMed
Drevets WC, Price JL, Furey ML.. 2008. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct. 213(1–2):93–118. PubMed PMC
Engel SM, Berkowitz GS, Wolff MS, Yehuda R.. 2005. Psychological trauma associated with the World Trade Center attacks and its effect on pregnancy outcome. Paediatr Perinat Epidemiol. 19:334–41. PubMed
Fischl B, Dale AM.. 2000. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A. 97(20):11050–11055. PubMed PMC
Fisher J, Cabral de Mello M, Patel V, Rahman A, Tran T, Holton S, Holmes W.. 2012. Prevalence and determinants of common perinatal mental disorders in women in low- and lowermiddle income countries: a systematic review. Bull World Health Organ. 90:139G–49G. PubMed PMC
Frodl T, Reinhold E, Koutsouleris N, Reiser M, Meisenzahl EM.. 2010. Interaction of childhood stress with hippocampus and prefrontal cortex volume reduction in major depression. J Psychiatr Res. 44(13):799–807. PubMed
Gilman SE, Cherkerzian S, Buka SL, Hahn J, Hornig M, Goldstein JM.. 2016. Prental immune programming of the sex -dependent risk for major depression. Transl Psychiatry. 6(5):e822 10.1038/tp.2016.91. PubMed DOI PMC
Gilmore JH, Schmitt JE, Knickmeyer RC, Smith JK, Lin W, Styner M, Gerig G, Neale MC.. 2010. Genetic and environmental contributions to neonatal brain structure: a twin study. Hum Brain Mapp. 31(8):1174–1182. PubMed PMC
Golding J. 1989. European Longitudinal Study of Pregnancy and Childhood (ELSPAC). Paediatr Perinat Epidemiol. 3(4):460–469. PubMed
Goldstein JM, Handa RJ, Tobet SA.. 2014. Disruption of fetal hormonal programming (prenatal stress) implicates shared risk for sex differences in depression and cardiovascular disease. Front Neuroendocrinol. 35(1):140–158. PubMed PMC
Janssen AB, Kertes DA, McNamara GI, Braithwaite EC, Creeth HD, Glover VI, John RM.. 2016. A role for the placenta in programming role for the placenta in programming maternal mood and childhood behavioural disorders. J Neuroendocrinol. 28(8). 10.1111/jne.12373. PubMed DOI PMC
Jensen SKG, Dickie EW, Schwartz DH, Evans JC, Dumontheil I, Paus T, Barker ED.. 2015. Effect of early adversity and childhood internalizing symptoms on brain structure in young men. JAMA Pediatr. 169(10):938–946. PubMed PMC
Kertes DA, Kamin HS, Hughes DA, Rodney NC, Bhatt S, Mulligan CJ.. 2016. Prenatal maternal stress predicts methylation of genes regulating the hypothalamic-pituitary-adrenocortical system in mothers and newborns in the Democratic Republic of Congo. Child Dev. 87:61–72. PubMed PMC
Kelly PA, Viding E, Wallace GL, Schaer M, De Brito SA, Robustelli B, McCrory EJ.. 2013. Cortical thickness, surface area, and gyrification abnormalities in children exposed to maltreatment: neural markers of vulnerability? Biol Psychiatry. 74(11):845–852. PubMed
Kempton MJ, Salvador Z, Munafò MR, Geddes JR, Simmons A, Frangou S, Williams SC.. 2011. Structural neuroimaging studies in major depressive disorder: meta-analysis and comparison with bipolar disorder. Arch Gen Psychiatry. 68(7):675–690. PubMed
Kingsbury M, Weeks M, MacKinnon N, Evans J, Mahedy L, Dykxhoorn J, Colman I.. 2016. Stressful life events during pregnancy and offspring depression: evidence from a prospective cohort study. J Am Acad Child Adolesc Psychiatry. 55(8):709–716. PubMed
Kinney DK, Munir KM, Crowley DJ, Miller AM.. 2008. Prenatal stress and risk for autism. Neurosci Biobehav Rev. 32:1519–1532. PubMed PMC
Ko JY, Farr SL, Dietz PM, Robbins CL.. 2012. Depression and treatment among US pregnant and nonpregnant women of reproductive age, 2005–2009. J Womens Health (Larchmt). 21:830–836. PubMed PMC
Li G, Nie J, Wang L, Shi F, Lin W, Gilmore JH, Shen D.. 2013. Mapping region-specific longitudinal cortical surface expansion from birth to 2 years of age. Cereb Cortex. 23(11):2724–2733. PubMed PMC
Li Y, Gonzalez P, Zhang L.. 2012. Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: mechanisms and possible interventions. Prog Neurobiol. 98(2):145–165. PubMed PMC
Lussier SJ, Stevens HE.. 2016. Delays in GABAergic interneuron development and behavioral inhibition after prenatal stress. Dev Neurobiol. 76:1078–1091. PubMed PMC
Mairesse J, Lesage J, Breton C, Bréant B, Hahn T, Darnaudéry M, Dickson SL, Seckl J, Blondeau B, Vieau D, et al. . 2007. Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endocrinol Metab. 292:E1526–E1533. PubMed
Maniam J, Antoniadis C, Morris MJ.. 2014. Early-life stress, HPA axis adaptation, and mechanisms contributing to later health outcomes. Front Endocrinol (Lausanne). 5–73. PubMed PMC
Mapayi B, Makanjuola RO, Mosaku SK, Adewuya OA, Afolabi O, Aloba OO, Akinsulore A.. 2013. Impact of intimate partner violence on anxiety and depression amongst women in Ile-Ife, Nigeria. Arch Womens Ment Health. 16:11–8. PubMed
Maselko J, Sikander S, Bhalotra S, Bangash O, Ganga N, Mukherjee S, Egger H, Franz L, Bibi A, Liaqat R, et al. . 2015. Effect of an early perinatal depression intervention on long-term child development outcomes: follow-up of the Thinking Healthy Programme randomised controlled trial. Lancet Psychiatry. 2:609–617. PubMed
McNair DM, Lorr M, Droppleman LF.. 1971. Manual for the Profile of Mood States. San Diego, CA: Educational and Industrial Testing Service.
Nathanielsz PW, Berghorn KA, Derks JB, Giussani DA, Docherty C, Unno N, Davenport A, Kutzlers M, Koenen S, Visser GH, et al. . 2003. Life before birth: Effects of cortisol on future cardiovascular and metabolic function. Acta Paediatr. 92:766–772. PubMed
O’Donnell KJ, Bugge Jensen A, Freeman L, Khalife N, O’Connor TG, Glover V.. 2012. Maternal prenatal anxiety and downregulation of placental 11β-HSD2. Psychoneuroendocrinology. 37:818–826. PubMed
Paus T. 2001. Primate anterior cingulate cortex: where motor control, drive, and cognition interface. Nature Reviews Neuroscience. 2:417–424. PubMed
Piler P, Kandrnal V, Kukla L, Andrýsková L, Švancara J, Jarkovský J, Dušek L, Pikhart H, Bobák M, Klánová J.. 2016. Cohort profile: European Longitudinal Study of Pregnancy and Childhood (ELSPAC) in the Czech Republic. International Journal of Epidemiology. 10.1093/ije/dyw091. PubMed DOI PMC
Pryce R, Aubert Y, Maier C, Pearce PC, Fuchs E.. 2011. The developmental impact of prenatal stress, prenatal dexamethasone and postnatal social stress on physiology, behaviour, and neuroanatomy of primate offspring: studies in rhesus macaque and common marmoset. Psychopharmacology. 214(1):33–53. PubMed PMC
Rakic P. 1995. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 18(9):383–388. PubMed
Rubin LP. 2016. Maternal and pediatric health and disease: integrating biopsychosocial models and epigenetics. Pediatr Res. 79:127–135. PubMed
Sandman CA, Buss C, Head K, Davis EP.. 2015. Fetal exposure to maternal depressive symptoms is associated with cortical thickness in late childhood. Biol Psychiatry. 77:324–334. PubMed PMC
Sandman CA, Davis EP, Buss C, Glynn LM.. 2012. Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus. Neuroendocrinology. 95:7–21. PubMed PMC
Sawyer A, Ayers S, Smith H.. 2010. Pre- and postnatal psychological wellbeing in Africa: a systematic review. J Affect Disord. 123:17–29. PubMed
Scheinost D, Sinha R, Cross SN, Kwon HS, Sze G, Constable RT, Ment LR.. 2017. Does prenatal stress alter the developing connectome? Pediatric Research. 81:214–226. PubMed PMC
Scheinost D, Kwon SH, Lacadie C, Sze G, Sinha R., Constable RT, Ment LR.. 2016. Prenatal stress alters amygdala functional connectivity in preterm neonates. Neuroimage Clin. 12:381–388. PubMed PMC
Seckl JR. 1998. Physiologic programming of the fetus. Clin Perinatol. 25(4):939–962. PubMed
Seckl JR, Cleasby M, Nyirenda MJ.. 2000. Glucocorticoids, 11betahydroxysteroid dehydrogenase, and fetal programming. Kidney Int. 57(4):1412–1417. PubMed
Selemon LD, Ceritoglu C, Ratnanather JT, Wang L, Harms MP, Aldridge K, Begović A, Csernansky JG, Miller MI, Rakic P.. 2013. Distinct abnormalities of the primate prefrontal cortex caused by ionizing radiation in early or midgestation. J Comp Neurol. 521(5):1040–1053. PubMed PMC
Stiles J, Jernigan TL.. 2010. The basics of brain development. Neuropsychol Rev. 20(4):327–348. PubMed PMC
Stroud LR, Papandonatos GD, Parade SH, Salisbury AL, Phipps MG, Lester BM, Padbury JF, Marsit CJ.. 2016. Prenatal major depressive disorder, placenta glucocorticoid and serotonergic signalling, and infant cortisol response. Psychosom Med. 78(9):979–990. PubMed PMC
Teicher MH, Andersen SL, Polcari A, Anderson CM, Navalta CP, Kim DM.. 2003. The neurobiological consequences of early stress and childhood maltreatment. Neurosci Biobehav Rev. 27:33–44. PubMed
Tomoda A, Sheu YS, Rabi K, Suzuki H, Navalta CP, Polcari A, Teicher MH.. 2011. Exposure to parental verbal abuse is associated with increased gray matter volume in superior temporal gyrus. Neuroimage. 54:S280–S286. PubMed PMC
Van Os J, Jones P, Lewis G, Wadsworth M, Murray R.. 1997. Developmental precursors of affective illness in a general population birth cohort. Arch Gen Psychiatry. 54(7):625–631. PubMed
Vythilingam M, Heim C, Newport J, Miller AH, Anderson E, Bronen R, Brummer M, Staib L, Vermetten E, Charney DS, et al. . 2002. Childhood trauma associated with smaller hippocampal volume in women with major depression. Am J Psychiatry. 159(12):2072–2080. PubMed PMC
Watson JB, Mednick SA, Huttunen M, Wang X.. 1999. Prenatal teratogens and the development of adult mental illness. Dev Psychopathol. 11(3):457–466. PubMed
Welberg LA, Seckl JR.. 2001. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol. 13(2):113–128. PubMed
Wierenga LM, Langen M, Oranje B, Durston S.. 2014. Unique developmental trajectories of cortical thickness and surface area. Neuroimage. 87:120–126. PubMed
Yonkers KA, Wisner KL, Stewart DE, Oberlander TF, Dell DL, Stotland N, Ramin S, Chaudron L, Lockwood C.. 2009. The management of depression during pregnancy: a report from the American Psychiatric Association and the American College of Obstetricians and Gynecologists. Gen Hosp Psychiatry. 31:403–413. PubMed PMC
Socioeconomic and cognitive roots of trait anxiety in young adults
Prenatal stress and its association with amygdala-related structural covariance patterns in youth
Lifelong impact of extreme stress on the human brain: Holocaust survivors study
Assessing Stress in Pregnancy and Postpartum: Comparing Measures
Perinatal stress and human hippocampal volume: Findings from typically developing young adults