Research progress on the mechanism of the impact of maternal childhood trauma on intergenerational transmission

LIU Juan; LIU Jian-Bo; KE Xiao-Yin

doi:10.7499/j.issn.1008-8830.2309147

PDF(517 KB)

Chinese Journal of Contemporary Pediatrics ›› 2024, Vol. 26 ›› Issue (2) : 207-212. DOI: 10.7499/j.issn.1008-8830.2309147

REVIEW

Research progress on the mechanism of the impact of maternal childhood trauma on intergenerational transmission

LIU Juan, LIU Jian-Bo, KE Xiao-Yin

Author information +

History +

Abstract

Childhood trauma refers to trauma experiences encountered during childhood and adolescence. Maternal childhood trauma experiences have a lasting impact on the next generation, affecting their physical and mental well-being. The mechanisms involved include the hypothalamic-pituitary-adrenal axis, inflammatory factors, brain structure and function, gene interactions, and parenting styles. This paper systematically reviews the mechanisms of the impact of maternal childhood trauma on intergenerational transmission, providing insights for the prevention of intergenerational transmission of childhood trauma.

Key words

Childhood trauma / Intergenerational transmission / Research progress

Cite this article

EndNote

Ris (Procite)

Bibtex

Download Citations

LIU Juan, LIU Jian-Bo, KE Xiao-Yin. Research progress on the mechanism of the impact of maternal childhood trauma on intergenerational transmission[J]. Chinese Journal of Contemporary Pediatrics. 2024, 26(2): 207-212 https://doi.org/10.7499/j.issn.1008-8830.2309147

References

1 Gilgoff R, Singh L, Koita K, et al. Adverse childhood experiences, outcomes, and interventions[J]. Pediatr Clin North Am, 2020, 67(2): 259-273. PMID: 32122559. DOI: 10.1016/j.pcl.2019.12.001.
2 Lu D, Wang W, Qiu X, et al. The prevalence of confirmed childhood trauma and its' impact on psychotic-like experiences in a sample of Chinese adolescents[J]. Psychiatry Res, 2020, 287: 112897. PMID: 32203750. DOI: 10.1016/j.psychres.2020.112897.
3 Kessler RC, McLaughlin KA, Green JG, et al. Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys[J]. Br J Psychiatry, 2010, 197(5): 378-385. PMID: 21037215. PMCID: PMC2966503. DOI: 10.1192/bjp.bp.110.080499.
4 Giano Z, Wheeler DL, Hubach RD. The frequencies and disparities of adverse childhood experiences in the U.S[J]. BMC Public Health, 2020, 20(1): 1327. PMID: 32907569. PMCID: PMC7488299. DOI: 10.1186/s12889-020-09411-z.
5 Bellis MA, Hughes K, Ford K, et al. Life course health consequences and associated annual costs of adverse childhood experiences across Europe and North America: a systematic review and meta-analysis[J]. Lancet Public Health, 2019, 4(10): e517-e528. PMID: 31492648. PMCID: PMC7098477. DOI: 10.1016/S2468-2667(19)30145-8.
6 Kang NR, Kwack YS, Song JK, et al. The impact of maternal adverse childhood experiences on offspring's internalizing and externalizing problems[J]. Psychiatry Investig, 2021, 18(11): 1050-1057. PMID: 34710961. PMCID: PMC8600217. DOI: 10.30773/pi.2021.0343.
7 Moon DS, Bong SJ, Kim BN, et al. Association between maternal adverse childhood experiences and attention-deficit/hyperactivity disorder in the offspring: the mediating role of antepartum health risks[J]. Soa Chongsonyon Chongsin Uihak, 2021, 32(1): 28-34. PMID: 33424239. PMCID: PMC7788667. DOI: 10.5765/jkacap.200041.
8 Ishikawa K, Azuma N, Ohka M. Intergenerational transmission of maternal adverse childhood experiences on next generation's development: a mini-review[J]. Front Psychol, 2022, 13: 852467. PMID: 35645853. PMCID: PMC9131025. DOI: 10.3389/fpsyg.2022.852467.
9 Adgent MA, Elsayed-Ali O, Gebretsadik T, et al. Maternal childhood and lifetime traumatic life events and infant bronchiolitis[J]. Paediatr Perinat Epidemiol, 2019, 33(4): 262-270. PMID: 31206733. PMCID: PMC6660418. DOI: 10.1111/ppe.12559.
10 Leonard SA, Petito LC, Rehkopf DH, et al. Maternal history of child abuse and obesity risk in offspring: mediation by weight in pregnancy[J]. Child Obes, 2017, 13(4): 259-266. PMID: 28440693. PMCID: PMC5549809. DOI: 10.1089/chi.2017.0019.
11 Tomfohr-Madsen LM, Bayrampour H, Tough S. Maternal history of childhood abuse and risk of asthma and allergy in 2-year-old children[J]. Psychosom Med, 2016, 78(9): 1031-1042. PMID: 27763990. DOI: 10.1097/PSY.0000000000000419.
12 Tsigos C, Chrousos GP. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress[J]. J Psychosom Res, 2002, 53(4): 865-871. PMID: 12377295. DOI: 10.1016/s0022-3999(02)00429-4.
13 Cattaneo A, Riva MA. Stress-induced mechanisms in mental illness: a role for glucocorticoid signalling[J]. J Steroid Biochem Mol Biol, 2016, 160: 169-174. PMID: 26241031. DOI: 10.1016/j.jsbmb.2015.07.021.
14 Lu S, Gao W, Huang M, et al. In search of the HPA axis activity in unipolar depression patients with childhood trauma: combined cortisol awakening response and dexamethasone suppression test[J]. J Psychiatr Res, 2016, 78: 24-30. PMID: 27049575. DOI: 10.1016/j.jpsychires.2016.03.009
15 Stephens JE, Kessler CL, Buss C, et al. Early and current life adversity: past and present influences on maternal diurnal cortisol rhythms during pregnancy[J]. Dev Psychobiol, 2021, 63(2): 305-319. PMID: 32572946. DOI: 10.1002/dev.22000.
16 Epstein CM, Houfek JF, Rice MJ, et al. Integrative review of early life adversity and cortisol regulation in pregnancy[J]. J Obstet Gynecol Neonatal Nurs, 2021, 50(3): 242-255. PMID: 33524324. PMCID: PMC8113070. DOI: 10.1016/j.jogn.2020.12.006.
17 Steine IM, LeWinn KZ, Lisha N, et al. Maternal exposure to childhood traumatic events, but not multi-domain psychosocial stressors, predict placental corticotrophin releasing hormone across pregnancy[J]. Soc Sci Med, 2020, 266: 113461. PMID: 33126094. PMCID: PMC9380779. DOI: 10.1016/j.socscimed.2020.113461.
18 Graham AM, Rasmussen JM, Entringer S, et al. Maternal cortisol concentrations during pregnancy and sex-specific associations with neonatal amygdala connectivity and emerging internalizing behaviors[J]. Biol Psychiatry, 2019, 85(2): 172-181. PMID: 30122286. PMCID: PMC6632079. DOI: 10.1016/j.biopsych.2018.06.023.
19 Sandman CA, Curran MM, Davis EP, et al. Cortical thinning and neuropsychiatric outcomes in children exposed to prenatal adversity: a role for placental CRH?[J]. Am J Psychiatry, 2018, 175(5): 471-479. PMID: 29495899. PMCID: PMC5930042. DOI: 10.1176/appi.ajp.2017.16121433.
20 Slopen N, Roberts AL, LeWinn KZ, et al. Maternal experiences of trauma and hair cortisol in early childhood in a prospective cohort[J]. Psychoneuroendocrinology, 2018, 98: 168-176. PMID: 30170311. DOI: 10.1016/j.psyneuen.2018.08.027.
21 Broeks CW, Molenaar N, Brouwer M, et al. Intergenerational impact of childhood trauma on hair cortisol concentrations in mothers and their young infants[J]. Compr Psychoneuroendocrinol, 2023, 14: 100167. PMID: 36819463. PMCID: PMC9930158. DOI: 10.1016/j.cpnec.2023.100167.
22 Duffy KA, Sammel MD, Johnson RL, et al. Maternal adverse childhood experiences impact fetal adrenal volume in a sex-specific manner[J]. Biol Sex Differ, 2023, 14(1): 7. PMID: 36803442. PMCID: PMC9936707. DOI: 10.1186/s13293-023-00492-0.
23 Yuan N, Chen Y, Xia Y, et al. Inflammation-related biomarkers in major psychiatric disorders: a cross-disorder assessment of reproducibility and specificity in 43 meta-analyses[J]. Transl Psychiatry, 2019, 9(1): 233. PMID: 31534116. PMCID: PMC6751188. DOI: 10.1038/s41398-019-0570-y.
24 Brown M, Worrell C, Pariante CM. Inflammation and early life stress: an updated review of childhood trauma and inflammatory markers in adulthood[J]. Pharmacol Biochem Behav, 2021, 211: 173291. PMID: 34695507. DOI: 10.1016/j.pbb.2021.173291.
25 Nusslock R, Miller GE. Early-life adversity and physical and emotional health across the lifespan: a neuroimmune network hypothesis[J]. Biol Psychiatry, 2016, 80(1): 23-32. PMID: 26166230. PMCID: PMC4670279. DOI: 10.1016/j.biopsych.2015.05.017.
26 Baumeister D, Akhtar R, Ciufolini S, et al. Childhood trauma and adulthood inflammation: a meta-analysis of peripheral C-reactive protein, interleukin-6 and tumour necrosis factor-α[J]. Mol Psychiatry, 2016, 21(5): 642-649. PMID: 26033244. PMCID: PMC4564950. DOI: 10.1038/mp.2015.67.
27 Huffhines L, Jackson Y, McGuire A, et al. The intergenerational interplay of adversity on salivary inflammation in young children and caregivers[J]. Psychoneuroendocrinology, 2021, 128: 105222. PMID: 33878600. PMCID: PMC8131264. DOI: 10.1016/j.psyneuen.2021.105222.
28 Kwon HK, Choi GB, Huh JR. Maternal inflammation and its ramifications on fetal neurodevelopment[J]. Trends Immunol, 2022, 43(3): 230-244. PMID: 35131181. PMCID: PMC9005201. DOI: 10.1016/j.it.2022.01.007.
29 Han VX, Patel S, Jones HF, et al. Maternal immune activation and neuroinflammation in human neurodevelopmental disorders[J]. Nat Rev Neurol, 2021, 17(9): 564-579. PMID: 34341569. DOI: 10.1038/s41582-021-00530-8.
30 Urakubo A, Jarskog LF, Lieberman JA, et al. Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain[J]. Schizophr Res, 2001, 47(1): 27-36. PMID: 11163542. DOI: 10.1016/s0920-9964(00)00032-3.
31 Pribiag H, Stellwagen D. Neuroimmune regulation of homeostatic synaptic plasticity[J]. Neuropharmacology, 2014, 78: 13-22. PMID: 23774138. DOI: 10.1016/j.neuropharm.2013.06.008.
32 Gumusoglu SB, Fine RS, Murray SJ, et al. The role of IL-6 in neurodevelopment after prenatal stress[J]. Brain Behav Immun, 2017, 65: 274-283. PMID: 28546058. PMCID: PMC5537020. DOI: 10.1016/j.bbi.2017.05.015.
33 Mirabella F, Desiato G, Mancinelli S, et al. Prenatal interleukin 6 elevation increases glutamatergic synapse density and disrupts hippocampal connectivity in offspring[J]. Immunity, 2021, 54(11): 2611-2631.e8. PMID: 34758338. PMCID: PMC8585508. DOI: 10.1016/j.immuni.2021.10.006.
34 Rudolph MD, Graham AM, Feczko E, et al. Maternal IL-6 during pregnancy can be estimated from newborn brain connectivity and predicts future working memory in offspring[J]. Nat Neurosci, 2018, 21(5): 765-772. PMID: 29632361. PMCID: PMC5920734. DOI: 10.1038/s41593-018-0128-y.
35 Garbett KA, Hsiao EY, Kálmán S, et al. Effects of maternal immune activation on gene expression patterns in the fetal brain[J]. Transl Psychiatry, 2012, 2(4): e98. PMID: 22832908. PMCID: PMC3337077. DOI: 10.1038/tp.2012.24.
36 da Silveira VT, Medeiros DC, Ropke J, et al. Effects of early or late prenatal immune activation in mice on behavioral and neuroanatomical abnormalities relevant to schizophrenia in the adulthood[J]. Int J Dev Neurosci, 2017, 58: 1-8. PMID: 28122258. DOI: 10.1016/j.ijdevneu.2017.01.009.
37 Crum WR, Sawiak SJ, Chege W, et al. Evolution of structural abnormalities in the rat brain following in utero exposure to maternal immune activation: a longitudinal in vivo MRI study[J]. Brain Behav Immun, 2017, 63: 50-59. PMID: 27940258. PMCID: PMC5441572. DOI: 10.1016/j.bbi.2016.12.008.
38 Goeden N, Velasquez J, Arnold KA, et al. Maternal inflammation disrupts fetal neurodevelopment via increased placental output of serotonin to the fetal brain[J]. J Neurosci, 2016, 36(22): 6041-6049. PMID: 27251625. PMCID: PMC4887568. DOI: 10.1523/JNEUROSCI.2534-15.2016.
39 Luchicchi A, Lecca S, Melis M, et al. Maternal immune activation disrupts dopamine system in the offspring[J]. Int J Neuropsychopharmacol, 2016, 19(7): pyw007. PMID: 26819283. PMCID: PMC4966272. DOI: 10.1093/ijnp/pyw007.
40 Rahman T, Zavitsanou K, Purves-Tyson T, et al. Effects of immune activation during early or late gestation on N-methyl-d-aspartate receptor measures in adult rat offspring[J]. Front Psychiatry, 2017, 8: 77. PMID: 28928676. PMCID: PMC5591421. DOI: 10.3389/fpsyt.2017.00077.
41 Manjeese W, Mvubu NE, Steyn AJC, et al. Mycobacterium tuberculosis causes a leaky blood-brain barrier and neuroinflammation in the prefrontal cortex and cerebellum regions of infected mice offspring[J]. Int J Dev Neurosci, 2021, 81(5): 428-437. PMID: 33932039. DOI: 10.1002/jdn.10116.
42 Sarigedik E, Naldemir IF, Karaman AK, et al. Intergenerational transmission of psychological trauma: a structural neuroimaging study[J]. Psychiatry Res Neuroimaging, 2022, 326: 111538. PMID: 36113385. DOI: 10.1016/j.pscychresns.2022.111538.
43 Demers CH, Hankin BL, Hennessey EP, et al. Maternal adverse childhood experiences and infant subcortical brain volume[J]. Neurobiol Stress, 2022, 21: 100487. PMID: 36532374. PMCID: PMC9755027. DOI: 10.1016/j.ynstr.2022.100487.
44 Moog NK, Entringer S, Rasmussen JM, et al. Intergenerational effect of maternal exposure to childhood maltreatment on newborn brain anatomy[J]. Biol Psychiatry, 2018, 83(2): 120-127. PMID: 28842114. PMCID: PMC5723537. DOI: 10.1016/j.biopsych.2017.07.009.
45 Lyons-Ruth K, Li FH, Khoury JE, et al. Maternal childhood abuse versus neglect associated with differential patterns of infant brain development[J]. Res Child Adolesc Psychopathol, 2023, 51(12): 1919-1932. PMID: 37160577. DOI: 10.1007/s10802-023-01041-4.
46 Hendrix CL, Dilks DD, McKenna BG, et al. Maternal childhood adversity associates with frontoamygdala connectivity in neonates[J]. Biol Psychiatry Cogn Neurosci Neuroimaging, 2021, 6(4): 470-478. PMID: 33495120. PMCID: PMC8035139. DOI: 10.1016/j.bpsc.2020.11.003.
47 van den Heuvel MI, Monk C, Hendrix CL, et al. Intergenerational transmission of maternal childhood maltreatment prior to birth: effects on human fetal amygdala functional connectivity[J]. J Am Acad Child Adolesc Psychiatry, 2023, 62(10): 1134-1146. PMID: 37245707. DOI: 10.1016/j.jaac.2023.03.020.
48 Zhang L, Lu Q, Chang C. Epigenetics in health and disease[J]. Adv Exp Med Biol, 2020, 1253: 3-55. PMID: 32445090. DOI: 10.1007/978-981-15-3449-2_1.
49 Stenz L, Schechter DS, Serpa SR, et al. Intergenerational transmission of DNA methylation signatures associated with early life stress[J]. Curr Genomics, 2018, 19(8): 665-675. PMID: 30532646. PMCID: PMC6225454. DOI: 10.2174/1389202919666171229145656.
50 Bierer LM, Bader HN, Daskalakis NP, et al. Intergenerational effects of maternal holocaust exposure on FKBP5 methylation[J]. Am J Psychiatry, 2020, 177(8): 744-753. PMID: 32312110. DOI: 10.1176/appi.ajp.2019.19060618.
51 Schechter DS, Moser DA, Paoloni-Giacobino A, et al. Methylation of NR3C1 is related to maternal PTSD, parenting stress and maternal medial prefrontal cortical activity in response to child separation among mothers with histories of violence exposure[J]. Front Psychol, 2015, 6: 690. PMID: 26074844. PMCID: PMC4447998. DOI: 10.3389/fpsyg.2015.00690.
52 Cordero MI, Stenz L, Moser DA, et al. The relationship of maternal and child methylation of the glucocorticoid receptor NR3C1 during early childhood and subsequent child psychopathology at school-age in the context of maternal interpersonal violence-related post-traumatic stress disorder[J]. Front Psychiatry, 2022, 13: 919820. PMID: 36061270. PMCID: PMC9437341. DOI: 10.3389/fpsyt.2022.919820.
53 Kohlhoff J, Karlov L, Dadds M, et al. The contributions of maternal oxytocin and maternal sensitivity to infant attachment security[J]. Attach Hum Dev, 2022, 24(4): 525-540. PMID: 34963414. DOI: 10.1080/14616734.2021.2018472.
54 Gouin JP, Zhou QQ, Booij L, et al. Associations among oxytocin receptor gene (OXTR) DNA methylation in adulthood, exposure to early life adversity, and childhood trajectories of anxiousness[J]. Sci Rep, 2017, 7(1): 7446. PMID: 28785027. PMCID: PMC5547144. DOI: 10.1038/s41598-017-07950-x.
55 Toepfer P, O'Donnell KJ, Entringer S, et al. Dynamic DNA methylation changes in the maternal oxytocin gene locus (OXT) during pregnancy predict postpartum maternal intrusiveness[J]. Psychoneuroendocrinology, 2019, 103: 156-162. PMID: 30690225. PMCID: PMC6554513. DOI: 10.1016/j.psyneuen.2019.01.013.
56 Luo S, Chen D, Li C, et al. Maternal adverse childhood experiences and behavioral problems in preschool offspring: the mediation role of parenting styles[J]. Child Adolesc Psychiatry Ment Health, 2023, 17(1): 95. PMID: 37563663. PMCID: PMC10416370. DOI: 10.1186/s13034-023-00646-3.
57 Wright DB, Laurent HK, Ablow JC. Mothers who were neglected in childhood show differences in neural response to their infant's cry[J]. Child Maltreat, 2017, 22(2): 158-166. PMID: 28413918. DOI: 10.1177/1077559516683503.
58 Bravo P, Kim Y, Xerxa Y, et al. Maternal history of maltreatment and offspring's emotional and behavioral problems in adolescence: do family factors contribute to the intergenerational risk transmission?[J]. Child Abuse Negl, 2023, 141: 106228. PMID: 37172532. DOI: 10.1016/j.chiabu.2023.106228.
59 Fuchs A, M?hler E, Resch F, et al. Impact of a maternal history of childhood abuse on the development of mother-infant interaction during the first year of life[J]. Child Abuse Negl, 2015, 48: 179-189. PMID: 26140735. DOI: 10.1016/j.chiabu.2015.05.023.
60 Madigan S, Cyr C, Eirich R, et al. Testing the cycle of maltreatment hypothesis: meta-analytic evidence of the intergenerational transmission of child maltreatment[J]. Dev Psychopathol, 2019, 31(1): 23-51. PMID: 30757994. DOI: 10.1017/S0954579418001700.
61 Wang X. Intergenerational effects of childhood maltreatment: the roles of parents' emotion regulation and mentalization[J]. Child Abuse Negl, 2022, 128: 104940. PMID: 33500161. DOI: 10.1016/j.chiabu.2021.104940.
62 Warmingham JM, Rogosch FA, Cicchetti D. Intergenerational maltreatment and child emotion dysregulation[J]. Child Abuse Negl, 2020, 102: 104377. PMID: 32018212. PMCID: PMC7067645. DOI: 10.1016/j.chiabu.2020.104377.