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Cultural trauma and epigenetic inheritance

Published online by Cambridge University Press:  28 September 2018

Amy Lehrner  and
Rachel Yehuda
Amy Lehrner*
Affiliation:
James J. Peters Veterans Affairs Medical Center Icahn School of Medicine at Mount Sinai
Rachel Yehuda
Affiliation:
James J. Peters Veterans Affairs Medical Center Icahn School of Medicine at Mount Sinai
*
Address correspondence and reprint requests to: Amy Lehrner, James J. Peters VA Medical Center, 130 W. Kingsbridge Road (526/OOMH), Bronx, NY 10468; E-mail: [email protected].
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Abstract

The question of whether and how the effects of cultural trauma can be transmitted intergenerationally from parents to offspring, or even to later generations, has evoked interest and controversy in academic and popular forums. Recent methodological advances have spurred investigations of potential epigenetic mechanisms for this inheritance, representing an exciting area of emergent research. Epigenetics has been described as the means through which environmental influences “get under the skin,” directing transcriptional activity and influencing the expression or suppression of genes. Over the past decade, this complex environment–biology interface has shown increasing promise as a potential pathway for the intergenerational transmission of the effects of trauma. This article reviews challenges facing research on cultural trauma, biological findings in trauma and posttraumatic stress disorder, and putative epigenetic mechanisms for transmission of trauma effects, including through social, intrauterine, and gametic pathways. Implications for transmission of cultural trauma effects are discussed, focused on the relevance of cultural narratives and the possibilities of resilience and adaptivity.

Type
Special Issue Articles
Information
Development and Psychopathology , Volume 30 , Special Issue 5: Cultural Development and Psychopathology , December 2018 , pp. 1763 - 1777
Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

The authors would like to thank Alex Ropes, Migle Staniskyte, and Emmanuel Ruhamya for assistance with manuscript preparation.

References

Aarons, V. (Ed.) (2016). Third-generation holocaust narratives: Memory in memoir and fiction. Lanham, MD: Lexington Books.Google Scholar
Abrams, M. S. (1999). Intergenerational transmission of trauma: Recent contributions from the literature of family systems approaches to treatment. American Journal of Psychotherapy, 53, 225–231. doi:10.1176/appi.psychotherapy.1999.53.2.225Google Scholar
Alexander, J. C. (2004). Toward a theory of cultural trauma. Cultural Trauma and Collective Identity, 76, 620–639. doi:10.1525/california/9780520235946.003.0001Google Scholar
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, DC: Author.Google Scholar
Anway, M. D., Cupp, A. S., Uzumcu, M., & Skinner, M. K. (2005). Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science, 308, 1466–1469. doi:10.1126/science.1108190Google Scholar
Argenti, N., & Schramm, K. (2009). Remembering violence: Anthropological perspectives on intergenerational transmission. New York: Berghahn Books.Google Scholar
Azarian-Ceccato, N. (2010). Reverberations of the Armenian genocide: Narrative's intergenerational transmission and the task of not forgetting. Narrative Inquiry, 20, 106–123. doi:10.1075/ni.20.1.06azaGoogle Scholar
Bader, H. N., Bierer, L. M., Lehrner, A., Makotkine, I., Daskalakis, N. P., & Yehuda, R. (2014). Maternal age at Holocaust exposure and maternal PTSD independently influence urinary cortisol levels in adult offspring. Frontiers in Endocrinology, 5, 1–8. doi:10.3389/fendo.2014.00103Google Scholar
Bale, T. L. (2014). Lifetime stress experience: Transgenerational epigenetics and germ cell programming. Dialogues in Clinical Neuroscience, 16, 297–305.Google Scholar
Barocas, H. A., & Barocas, C. B. (1980). Separation-individuation conflicts in children of Holocaust survivors. Journal of Contemporary Psychotherapy, 11, 6–14. doi:10.1007/BF00946270Google Scholar
Barron, I. G., & Abdallah, G. (2015). Intergenerational trauma in the occupied Palestinian territories: Effect on children and promotion of healing. Journal of Child & Adolescent Trauma, 8, 103–110. doi:10.1007/s40653-015-0046-zGoogle Scholar
Betancourt, T. S., McBain, R. K., Newnham, E. A., & Brennan, R. T. (2015). The intergenerational impact of war: Longitudinal relationships between caregiver and child mental health in postconflict Sierra Leone. Journal of Child Psychology and Psychiatry, 56, 1101–1107. doi:10.1111/jcpp.12389Google Scholar
Bezo, B., & Maggi, S. (2015). Living in “survival mode”: Intergenerational transmission of trauma from the Holodomor genocide of 1932–1933 in Ukraine. Social Science & Medicine, 134, 87–94. doi:10.1016/j.socscimed.2015.04.009Google Scholar
Blades, L. A. (2016). Trauma from slavery can actually be passed down through your genes. Retrieved from https://www.teenvogue.com/story/slavery-trauma-inherited-geneticsGoogle Scholar
Brach, C., & Fraserirector, I. (2000). Can cultural competency reduce racial and ethnic health disparities? A review and conceptual model. Medical Care Research and Review, 57(Suppl. 2), 181–217. doi:10.1177/1077558700057001S09Google Scholar
Brave Heart, M. Y. H. (1998). The return to the sacred path: Healing the historical trauma and historical unresolved grief response among the Lakota through a psychoeducational group intervention. Smith College Studies in Social Work, 68, 287–305. doi:10.1080/00377319809517532Google Scholar
Breslau, N. (2009). The epidemiology of trauma, PTSD, and other posttrauma disorders. Trauma, Violence & Abuse, 10, 198–210. doi:10.1177/1524838009334448Google Scholar
Bronfenbrenner, U. (1977). Toward an experimental ecology of human development. American Psychologist, 32, 513–531. doi:10.1037/0003-066X.32.7.513Google Scholar
Bronfenbrenner, U. (2009). The ecology of human development: Experiments by nature and design. Cambridge, MA: Harvard University Press.Google Scholar
Calhoun, L. G., & Tedeschi, R. G. (Eds.) (2014). Handbook of posttraumatic growth: Research and practice. New York: Routledge.Google Scholar
Carpenter, T., Grecian, S., & Reynolds, R. (2015). Sex differences in early life programming of the hypothalamic-pituitary-adrenal axis in humans suggest increased vulnerability in females. Psychoneuroendocrinology, 61, 32. doi:10.1016/j.psyneuen.2015.07.476Google Scholar
Chaitin, J., & Steinberg, S. (2008). “You should know better”: Expressions of empathy and disregard among victims of massive social trauma. Journal of Aggression, Maltreatment & Trauma, 17, 197–226. doi:10.1080/10926770802344851Google Scholar
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., De Kloet, E. R., … Krugers, H. (2008). Maternal care and hippocampal plasticity: Evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. Journal of Neuroscience, 28, 6037–6045. doi:10.1523/JNEUROSCI.0526-08.2008Google Scholar
Chodoff, P. (1963). Late effects of the concentration camp syndrome. Archives of General Psychiatry, 8, 323–333. doi:10.1001/archpsyc.1963.01720100013002Google Scholar
Chorbov, V. M., Todorov, A. A., Lynskey, M. T., & Cicero, T. J. (2011). Elevated levels of DNA methylation at the OPRM1 promoter in blood and sperm from male opioid addicts. Journal of Opioid Management, 7, 258. doi:10.5055/jom.2011.0067Google Scholar
Chrousos, G. P. (2009). Stress and disorders of the stress system. Nature Reviews Endocrinology, 5, 374–381. doi:10.1038/nrendo.2009.106Google Scholar
Cortessis, V. K., Thomas, D. C., Levine, A. J., Breton, C. V., Mack, T. M., Siegmund, K. D., … Laird, P. W. (2012). Environmental epigenetics: Prospects for studying epigenetic mediation of exposure–response relationships. Human Genetics, 131, 1565–1589. doi:10.1007/s00439-012-1189-8Google Scholar
Danieli, Y. (1985). The treatment and prevention of long-term effects and intergenerational transmission of victimization: A lesson from Holocaust survivors and their children. In Figley, C. R. (Ed.), Trauma and its wake (pp. 295–313). New York: Brunner/Mazel.Google Scholar
Danieli, Y. (Ed.) (1998). International handbook of multigenerational legacies of trauma. New York: Plenun Press.Google Scholar
Daskalakis, N. P., Cohen, H., Cai, G., Buxbaum, J. D., & Yehuda, R. (2014). Expression profiling associates blood and brain glucocorticoid receptor signaling with trauma-related individual differences in both sexes. Proceedings of the National Academy of Sciences, 111, 13529–13534. doi:10.1073/pnas.1401660111Google Scholar
Daskalakis, N. P., Oitzl, M. S., Schächinger, H., Champagne, D. L., & de Kloet, E. R. (2012). Testing the cumulative stress and mismatch hypotheses of psychopathology in a rat model of early-life adversity. Physiology & Behavior, 106, 707–721. doi:10.1016/j.physbeh.2012.01.015Google Scholar
Daxinger, L., & Whitelaw, E. (2012). Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nature Reviews Genetics, 13, 153–164. doi:10.1038/nrg3188Google Scholar
DeGruy, J. (2017). Post traumatic slave syndrome: America's legacy of enduring injury and healing: Milwaukee, WI: Uptone Press.Google Scholar
de Jong, J. (Ed.) (2006). Trauma, war, and violence: Public mental health in socio-cultural context: New York: Kluwer Academic.Google Scholar
De Kloet, C., Vermetten, E., Geuze, E., Kavelaars, A., Heijnen, C., & Westenberg, H. (2006). Assessment of HPA-axis function in posttraumatic stress disorder: Pharmacological and non-pharmacological challenge tests, a review. Journal of Psychiatric Research, 40, 550–567. doi:10.1016/j.jpsychires.2005.08.002Google Scholar
De Kloet, E. R., Joëls, M., & Holsboer, F. (2005). Stress and the brain: From adaptation to disease. Nature Reviews Neuroscience, 6, 463–475. doi:10.1038/nrn1683Google Scholar
Desai, N., Ludgin, J., Sharma, R., Anirudh, R. K., & Agarwal, A. (2017). Female and male gametogenesis. In Falcone, T. & Hurd, W.W. (Eds.), Clinical reproductive medicine and surgery (pp. 43–62). New York: Springer.Google Scholar
de Tubert, R. H. (2006). Social trauma: The pathogenic effects of untoward social conditions. International Forum of Psychoanalysis, 15, 151–156. doi:10.1080/08037060500526037Google Scholar
Dias, B. G., & Ressler, K. J. (2014). Experimental evidence needed to demonstrate inter- and trans-generational effects of ancestral experiences in mammals. Bioessays, 36, 919–923. doi:10.1002/bies.201400105Google Scholar
Dietz, D. M., LaPlant, Q., Watts, E. L., Hodes, G. E., Russo, S. J., Feng, J., … Nestler, E. J. (2011). Paternal transmission of stress-induced pathologies. Biological Psychiatry, 70, 408–414. doi:10.1016/j.biopsych.2011.05.005Google Scholar
Dimsdale, J. E. (1974). The coping behavior of Nazi concentration camp survivors. American Journal of Psychiatry, 131, 792–797. doi:10.1176/ajp.131.7.792Google Scholar
Dor-Shav, N. K. (1978). On the long-range effects of concentration camp internment on Nazi victims: 25 years later. Journal of Consulting and Clinical Psychology, 46, 1–11. doi:10.1037/0022-006X.46.1.1Google Scholar
Doucet, M., & Rovers, M. (2010). Generational trauma, attachment, and spiritual/religious interventions. Journal of Loss and Trauma, 15, 93–105. doi:10.1080/15325020903373078Google Scholar
Eitinger, L. (1961). Pathology of the concentration camp syndrome: Preliminary report. Archives of General Psychiatry, 5, 371–379. doi:10.1001/archpsyc.1961.01710160051006Google Scholar
Esmaeili, S. (2011). Intergenerational transmission of trauma: Traumatic impact on second-generation Armenian genocide survivors and its effects on parenting. San Francisco: Alliant International University, California School of Professional Psychology.Google Scholar
Evans-Campbell, T. (2008). Historical trauma in American Indian/Native Alaska communities: A multilevel framework for exploring impacts on individuals, families, and communities. Journal of Interpersonal Violence, 23, 316–338. doi:10.1177/0886260507312290Google Scholar
Eyerman, R. (2001). Cultural trauma: Slavery and the formation of African American identity. Cambridge: Cambridge University Press.Google Scholar
Faulk, C., & Dolinoy, D. C. (2011). Timing is everything: The when and how of environmentally induced changes in the epigenome of animals. Epigenetics, 6, 791–797. doi:10.4161/epi.6.7.16209Google Scholar
Field, N. P., Muong, S., & Sochanvimean, V. (2013). Parental styles in the intergenerational transmission of trauma stemming from the Khmer Rouge regime in Cambodia. American Journal of Orthopsychiatry, 83, 483–494. doi:10.1111/ajop.12057Google Scholar
Fowler, P. J., Tompsett, C. J., Braciszewski, J. M., Jacques-Tiura, A. J., & Baltes, B. B. (2009). Community violence: A meta-analysis on the effect of exposure and mental health outcomes of children and adolescents. Development and Psychopathology, 21, 227–259. doi:10.1017/S0954579409000145Google Scholar
Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., … Mansuy, I. M. (2010). Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry, 68, 408–415. doi:10.1016/j.biopsych.2010.05.036Google Scholar
Friedler, G. (1996). Paternal exposures: Impact on reproductive and developmental outcome. Pharmacology Biochemistry and Behavior, 55, 691–700. doi:10.1016/S0091-3057(96)00286-9Google Scholar
Galea, S., Nandi, A., & Vlahov, D. (2005). The epidemiology of post-traumatic stress disorder after disasters. Epidemiologic Reviews, 27, 78–91. doi:10.1093/epirev/mxi003Google Scholar
Galtung, J. (1990). Cultural violence. Journal of Peace Research, 27, 291–305. doi:10.1177/0022343390027003005Google Scholar
Gapp, K., Bohacek, J., Grossmann, J., Brunner, A. M., Manuella, F., Nanni, P., & Mansuy, I. M. (2016). Potential of environmental enrichment to prevent transgenerational effects of paternal trauma. Neuropsychopharmacology, 41, 2749–2758. doi:10.1038/npp.2016.87Google Scholar
Gapp, K., von Ziegler, L., Tweedie-Cullen, R. Y., & Mansuy, I. M. (2014). Early life epigenetic programming and transmission of stress-induced traits in mammals. Bioessays, 36, 491–502. doi:10.1002/bies.201300116Google Scholar
Gillman, M. W. (2005). Developmental origins of health and disease. New England Journal of Medicine, 353, 1848–1850. doi:10.1056/NEJMe058187Google Scholar
Glover, D. A., & Poland, R. E. (2002). Urinary cortisol and catecholamines in mothers of child cancer survivors with and without PTSD. Psychoneuroendocrinology, 27, 805–819. doi:10.1016/S0306-4530(01)00081-6Google Scholar
Goldberg, A. D., Allis, C. D., & Bernstein, E. (2007). Epigenetics: A landscape takes shape. Cell, 128, 635–638. doi:10.1016/j.cell.2007.02.006Google Scholar
Goldberg, R. (2015). Motherland: Growing up with the Holocaust: New York: New Press.Google Scholar
Gone, J. P. (2013). Redressing First Nations historical trauma: Theorizing mechanisms for indigenous culture as mental health treatment. Transcultural Psychiatry, 50, 683–706. doi:10.1177/1363461513487669Google Scholar
Gone, J. P., & Kirmayer, L. J. (2010). On the wisdom of considering culture and context in psychopathology. In Millon, T., Krueger, R. F., & Simonsen, E. (Eds.), Contemporary directions in psychopathology: Scientific foundations of the DSM-V and ICD-11 (pp. 72–96). New York: Guilford Press.Google Scholar
Hamad, M., Shelko, N., Kartarius, S., Montenarh, M., & Hammadeh, M. (2014). Impact of cigarette smoking on histone (H2B) to protamine ratio in human spermatozoa and its relation to sperm parameters. Andrology, 2, 666–677. doi:10.1111/j.2047-2927.2014.00245.xGoogle Scholar
Harper, L. (2005). Epigenetic inheritance and the intergenerational transfer of experience. Psychological Bulletin, 131, 340–360. doi:10.1037/0033-2909.131.3.340Google Scholar
Heard, E., & Martienssen, R. A. (2014). Transgenerational epigenetic inheritance: Myths and mechanisms. Cell, 157, 95–109. doi:10.1016/j.cell.2014.02.045Google Scholar
Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., … Lumey, L. (2008). Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proceedings of the National Academy of Sciences, 105, 17046–17049. doi:10.1073/pnas.0806560105Google Scholar
Hooker, D. A., & Czajkowski, A.P. (n.d.). Transforming historical harms. Manual published by Coming to the Table, a project of Eastern Mennonite University's Center for Justice and Peacebuilding. Harrisonburg, VA: Eastern Mennonite University.Google Scholar
Jablonka, E., & Raz, G. (2009). Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. Quarterly Review of Biology, 84, 131–176. doi:10.1086/598822Google Scholar
Jaenisch, R., & Bird, A. (2003). Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nature Genetics, 33, 245–250. doi:10.1038/ng1089Google Scholar
Juster, R.-P., McEwen, B. S., & Lupien, S. J. (2010). Allostatic load biomarkers of chronic stress and impact on health and cognition. Neuroscience & Biobehavioral Reviews, 35, 2–16. doi:10.1016/j.neubiorev.2009.10.002.Google Scholar
Kaati, G., Bygren, L. O., Pembrey, M., & Sjöström, M. (2007). Transgenerational response to nutrition, early life circumstances and longevity. European Journal of Human Genetics, 15, 784–790. doi:10.1038/sj.ejhg.5201832Google Scholar
Karenian, H., Livaditis, M., Karenian, S., Zafiriadis, K., Bochtsou, V., & Xenitidis, K. (2011). Collective trauma transmission and traumatic reactions among descendants of Armenian refugees. International Journal of Social Psychiatry, 57, 327–337. doi:10.1177/0020764009354840Google Scholar
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62, 593–602. doi:10.1001/archpsyc.62.6.593Google Scholar
Kessler, R. C., Sonnega, A., Bromet, E., Hughes, M., & Nelson, C. B. (1995). Posttraumatic stress disorder in the National Comorbidity Survey. Archives of General Psychiatry, 52, 1048–1060. doi:10.1001/archpsyc.1995.03950240066012Google Scholar
Kosten, T. R., Mason, J. W., Giller, E. L., Ostroff, R. B., & Harkness, L. (1987). Sustained urinary norepinephrine and epinephrine elevation in post-traumatic stress disorder. Psychoneuroendocrinology, 12, 13–20. doi:10.1016/0306-4530(87)90017-5Google Scholar
Leacock, E. B. (Ed.) (1971). The culture of poverty: A critique. New York: Simon and Schuster.Google Scholar
Lehrner, A., Bierer, L. M., Passarelli, V., Pratchett, L. C., Flory, J. D., Bader, H. N., … Makotkine, I. (2014). Maternal PTSD associates with greater glucocorticoid sensitivity in offspring of Holocaust survivors. Psychoneuroendocrinology, 40, 213–220. doi:10.1016/j.psyneuen.2013.11.019Google Scholar
Leon, G. R., Butcher, J. N., Kleinman, M., Goldberg, A., & Almagor, M. (1981). Survivors of the Holocaust and their children: Current status and adjustment. Journal of Personality and Social Psychology, 41, 503–516. doi:10.1037//0022-3514.41.3.503Google Scholar
Liberzon, I., Abelson, J. L., Flagel, S. B., Raz, J., & Young, E. A. (1999). Neuroendocrine and psychophysiologic responses in PTSD: A symptom provocation study. Neuropsychopharmacology, 21, 40–50. doi:10.1016/S0893-133X(98)00128-6Google Scholar
Lim, J. P., & Brunet, A. (2013). Bridging the transgenerational gap with epigenetic memory. Trends in Genetics, 29, 176–186. doi:10.1016/j.tig.2012.12.008Google Scholar
Linden, M., Baumann, K., Lieberei, B., Lorenz, C., & Rotter, M. (2011). Treatment of posttraumatic embitterment disorder with cognitive behaviour therapy based on wisdom psychology and hedonia strategies. Psychotherapy and Psychosomatics, 80, 199–205. doi:10.1159/000321580Google Scholar
Linden, M., & Rutkowski, K. (2013). Hurting memories and beneficial forgetting: Posttraumatic stress disorders, biographical developments, and social conflicts. London: Elsevier.Google Scholar
Martino, J. (1980). Collective memory of cultural trauma in Peru: Efforts to move from blame to reconciliation. In Yovanovich, G. & Huras, A. (Eds.), Latin American identities after 1980 (pp. 235–255). Waterloo: Wilfrid Laurier University Press.Google Scholar
Mason, J. W., Giller, E. L., Kosten, T. R., & Harkness, L. (1988). Elevation of urinary norepinephrine/cortisol ratio in posttraumatic stress disorder. Journal of Nervous and Mental Disease, 176, 498–502. doi:10.1097/00005053-198808000-00008Google Scholar
Mason, J. W., Giller, E. L., Kosten, T. R., Ostroff, R. B., & Podd, L. (1986). Urinary free-cortisol levels in posttraumatic stress disorder patients. Journal of Nervous and Mental Disease, 174, 145–149. doi:10.1097/00005053-198603000-00003Google Scholar
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 33–44. doi:10.1111/j.1749-6632.1998.tb09546.xGoogle Scholar
McEwen, B. S. (2012). Brain on stress: How the social environment gets under the skin. Proceedings of the National Academy of Sciences, 109(Suppl. 2), 17180–17185. doi:10.1073/pnas.1121254109Google Scholar
McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 2–15. doi:10.1016/s0018-506x(02)00024-7Google Scholar
McGlothlin, E. H. (2006). Second-generation Holocaust literature: Legacies of survival and perpetration. Boston: Camden House.Google Scholar
McGowan, P. O., Sasaki, A., D'alessio, A. C., Dymov, S., Labonté, B., Szyf, M., … Meaney, M. J. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience, 12, 342–348. doi:10.1038/nn.2270Google Scholar
Meaney, M. J., Aitken, D. H., Bodnoff, S. R., Iny, L. J., & Sapolsky, R. M. (1985). The effects of postnatal handling on the development of the glucocorticoid receptor systems and stress recovery in the rat. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 9, 731–734. doi:10.1016/0278-5846(85)90050-8Google Scholar
Meaney, M. J., Aitken, D. H., Bodnoff, S. R., Iny, L. J., Tatarewicz, J. E., & Sapolsky, R. M. (1985). Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Behavioral Neuroscience, 99, 765–770. doi:10.1037/0735-7044.99.4.765Google Scholar
Meaney, M. J., Aitken, D. H., van Berkel, C., Bhatnagar, S., & Sapolsky, R. M. (1988). Effect of neonatal handling on age-related impairments associated with the hippocampus. Science, 239(4841, Pt. 1), 766–768. doi:10.1126/science.3340858Google Scholar
Mendeloff, D. (2009). Trauma and vengeance: Assessing the psychological and emotional effects of post-conflict justice. Human Rights Quarterly, 31, 592–623. doi:10.1353/hrq.0.0100Google Scholar
Miller, G. (2010). The seductive allure of behavioral epigenetics. Science, 329, 24–27. doi:10.1126/science.329.5987.24Google Scholar
Mohatt, N. V., Thompson, A. B., Thai, N. D., & Tebes, J. K. (2014). Historical trauma as public narrative: A conceptual review of how history impacts present-day health. Social Science & Medicine, 106, 128–136. doi:10.1016/j.socscimed.2014.01.043Google Scholar
Moon, C. (2009). Healing past violence: Traumatic assumptions and therapeutic interventions in war and reconciliation. Journal of Human Rights, 8, 71–91. doi:10.1080/14754830902717726Google Scholar
Morris, M. C., Compas, B. E., & Garber, J. (2012). Relations among posttraumatic stress disorder, comorbid major depression, and HPA function: A systematic review and meta-analysis. Clinical Psychology Review, 32, 301–315. doi:10.1016/j.cpr.2012.02.002Google Scholar
Mulligan, C., D'Errico, N., Stees, J., & Hughes, D. (2012). Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics, 7, 853–857. doi:10.4161/epi.21180Google Scholar
Münyas, B. (2008). Genocide in the minds of Cambodian youth: Transmitting (hi) stories of genocide to second and third generations in Cambodia. Journal of Genocide Research, 10, 413–439. doi:10.1080/14623520802305768Google Scholar
Niederland, W. G. (1981). The survivor syndrome: Further observations and dimensions. Journal of the American Psychoanalytic Association, 29, 413–425. doi:10.1177/000306518102900207Google Scholar
Nugent, B. M., & Bale, T. L. (2015). The omniscient placenta: Metabolic and epigenetic regulation of fetal programming. Frontiers in Neuroendocrinology, 39, 28–37. doi:10.1016/j.yfrne.2015.09.001Google Scholar
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics, 3, 97–106. doi:10.4161/epi.3.2.6034Google Scholar
O'Nell, T. D. (1996). Disciplined hearts: History, identity, and depression in an American Indian community. Berkeley, CA: University of California Press.Google Scholar
Ouko, L. A., Shantikumar, K., Knezovich, J., Haycock, P., Schnugh, D. J., & Ramsay, M. (2009). Effect of alcohol consumption on CpG methylation in the differentially methylated regions of H19 and IG-DMR in male gametes—Implications for fetal alcohol spectrum disorders. Alcoholism: Clinical and Experimental Research, 33, 1615–1627. doi:10.1111/j.1530-0277.2009.00993.xGoogle Scholar
Painter, R. C., Osmond, C., Gluckman, P., Hanson, M., Phillips, D. I., & Roseboom, T. J. (2008). Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. British Journal of Obstetrics and Gynaecology, 115, 1243–1249. doi:10.1111/j.1471-0528.2008.01822.xGoogle Scholar
Pembrey, M. E., Bygren, L. O., Kaati, G., Edvinsson, S., Northstone, K., Sjöström, M., & Golding, J. (2006). Sex-specific, male-line transgenerational responses in humans. European Journal of Human Genetics, 14, 159–166. doi:10.3109/14647273.2010.524721Google Scholar
Perroud, N., Rutembesa, E., Paoloni-Giacobino, A., Mutabaruka, J., Mutesa, L., Stenz, L., … Karege, F. (2014). The Tutsi genocide and transgenerational transmission of maternal stress: Epigenetics and biology of the HPA axis. World Journal of Biological Psychiatry, 15, 334–345. doi:10.3109/15622975.2013.866693Google Scholar
Pihama, L., Reynolds, P., Smith, C., Reid, J., Smith, L. T., & Nana, R. T. (2014). Positioning historical trauma theory within Aotearoa New Zealand. AlterNative, 10, 248–262. doi:10.1177/117718011401000304Google Scholar
Prager, J. (2003). Lost childhood, lost generations: The intergenerational transmission of trauma. Journal of Human Rights, 2, 173–181. doi:10.1080/1475483032000078161Google Scholar
Radomislensky, I., & Shemesh, A. A. (2007). Psychopathology and other health dimensions among the offspring of Holocaust survivors: Results from the Israel National Health Survey. Israel Journal of Psychiatry and Related Sciences, 44, 144–151.Google Scholar
Radtke, K. M., Ruf, M., Gunter, H. M., Dohrmann, K., Schauer, M., Meyer, A., & Elbert, T. (2011). Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Translational Psychiatry, 1, e21. doi:10.1038/tp.2011.21Google Scholar
Raphael, B., Swan, P., & Martinek, N. (1998). Intergenerational aspects of trauma for Australian Aboriginal people. In Danieli, Y. (Ed.), International handbook of multigenerational legacies of trauma (pp. 327–339). New York: Plenun Press.Google Scholar
Ravelli, G.-P., Stein, Z. A., & Susser, M. W. (1976). Obesity in young men after famine exposure in utero and early infancy. New England Journal of Medicine, 295, 349–353. doi:10.1056/NEJM197608122950701Google Scholar
Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S., & Bale, T. L. (2013). Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. Journal of Neuroscience, 33, 9003–9012. doi:10.1523/JNEUROSCI.0914-13.2013Google Scholar
Rosenheck, R. (1986). Impact of posttraumatic stress disorder of World War II on the next generation. Journal of Nervous and Mental Disease, 174, 319–327. doi:10.1097/00005053-198606000-00001Google Scholar
Roth, M., Neuner, F., & Elbert, T. (2014). Transgenerational consequences of PTSD: Risk factors for the mental health of children whose mothers have been exposed to the Rwandan genocide. International Journal of Mental Health Systems, 8, 12. doi:10.1186/1752-4458-8-12Google Scholar
Ryan, W. (1976). Blaming the victim. New York: Random House.Google Scholar
Santarelli, S., Lesuis, S. L., Wang, X.-D., Wagner, K. V., Hartmann, J., Labermaier, C., … Schmidt, M. V. (2014). Evidence supporting the match/mismatch hypothesis of psychiatric disorders. European Neuropsychopharmacology, 24, 907–918. doi:10.1016/j.euroneuro.2014.02.002Google Scholar
Schagdarsurengin, U., & Steger, K. (2016). Epigenetics in male reproduction: Effect of paternal diet on sperm quality and offspring health. Nature Reviews Urology, 13, 584–595. doi:10.1038/nrurol.2016.157Google Scholar
Schmidt, M. V. (2011). Animal models for depression and the mismatch hypothesis of disease. Psychoneuroendocrinology, 36, 330–338. doi:10.1016/j.psyneuen.2010.07.001Google Scholar
Schwab, G. (2010). Haunting legacies: Violent histories and transgenerational trauma. New York: Columbia University Press.Google Scholar
Shrira, A., Palgi, Y., Ben-Ezra, M., & Shmotkin, D. (2011). Transgenerational effects of trauma in midlife: Evidence for resilience and vulnerability in offspring of Holocaust survivors. Psychological Trauma: Theory, Research, Practice, and Policy, 3, 394–402. doi:10.1037/a0020608Google Scholar
Smith, S. M., & Vale, W. W. (2006). The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues in Clinical Neuroscience, 8, 383–395.Google Scholar
Solkoff, N. (1981). Children of survivors of the Nazi Holocaust: A critical review of the literature. American Journal of Orthopsychiatry, 51, 29–42. doi:10.1111/j.1939-0025.1981.tb01345.xGoogle Scholar
Solomon, Z., Kotler, M., & Mikulincer, M. (1988). Combat-related posttraumatic stress disorder among second-generation Holocaust survivors: Preliminary findings. American Journal of Psychiatry, 145, 865–868. doi:10.1176/ajp.145.7.865Google Scholar
Sorel, E. (2010). The WHO World Mental Health Surveys: Global perspectives on the epidemiology of mental disorders: American Psychiatric Association, 167, 354–355. doi:10.1176/appi.ajp.2009.09081218Google Scholar
Spiegelman, A. (2003). The complete maus. London: Penguin Books Limited.Google Scholar
Steel, Z., Silove, D., Phan, T., & Bauman, A. (2002). Long-term effect of psychological trauma on the mental health of Vietnamese refugees resettled in Australia: A population-based study. Lancet, 360, 1056–1062. doi:10.1016/s0140-6736(02)11142-1Google Scholar
Steinitz, L. Y. (1982). Psycho-social effects of the Holocaust on aging survivors and their families. Journal of Gerontological Social Work, 4, 145–152. doi:10.1300/j083v04n03_13Google Scholar
Sullivan, P. (1986). The generation of cultural trauma: What are anthropologists for? Australian Aboriginal Studies, 1, 13–23.Google Scholar
Svob, C., Brown, N. R., Takšić, V., Katulić, K., & Žauhar, V. (2016). Intergenerational transmission of historical memories and social-distance attitudes in post-war second-generation Croatians. Memory & Cognition, 44, 846–855. doi:10.3758/s13421-016-0607-xGoogle Scholar
Tedeschi, R. G., & Calhoun, L. G. (2004). Posttraumatic growth: Conceptual foundations and empirical evidence. Psychological Inquiry, 15, 1–18. doi:10.1207/s15327965pli1501_01Google Scholar
Tobi, E. W., Slieker, R. C., Luijk, R., Dekkers, K. F., Stein, A. D., Xu, K. M., … Heijmans, B. T. (2018). DNA methylation as a mediator of the association between prenatal adversity and risk factors for metabolic disease in adulthood. Science Advances, 4, 1–10. doi:10.1126/sciadv.aao4364Google Scholar
Tyrka, A. R., Parade, S. H., Eslinger, N. M., Marsit, C. J., Lesseur, C., Armstrong, D. A., … Seifer, R. (2015). Methylation of exons 1D, 1F, and 1H of the glucocorticoid receptor gene promoter and exposure to adversity in preschool-aged children. Development and Psychopathology, 27, 577–585. doi:10.1017/S095457941500017Google Scholar
Tyrka, A. R., Parade, S. H., Welch, E. S., Ridout, K. K., Price, L. H., Marsit, C., … Carpenter, L. L. (2016). Methylation of the leukocyte glucocorticoid receptor gene promoter in adults: Associations with early adversity and depressive, anxiety and substance-use disorders. Translational Psychiatry, 6, e848. doi:10.1038/tp.2016.112Google Scholar
Tyrka, A. R., Price, L. H., Marsit, C., Walters, O. C., & Carpenter, L. L. (2012). Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: Preliminary findings in healthy adults. PLOS ONE, 7, e30148. doi:10.1371/journal.pone.0030148Google Scholar
van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., & Sagi-Schwartz, A. (2003). Are children of Holocaust survivors less well-adapted? A meta-analytic investigation of secondary traumatization. Journal of Traumatic Stress, 16, 459–469. doi:10.1023/A:1025706427300Google Scholar
Veenendaal, M. V., Painter, R. C., Rooij, S., Bossuyt, P. M., Post, J., Gluckman, P. D., … Roseboom, T. J. (2013). Transgenerational effects of prenatal exposure to the 1944–45 Dutch famine. BJOG: International Journal of Obstetrics & Gynaecology, 120, 548–554. doi:10.1111/j.1471-0528.2009.02108.xGoogle Scholar
Volkan, V. D. (2001). Transgenerational transmissions and chosen traumas: An aspect of large-group identity. Group Analysis, 34, 79–97. doi:10.1177/05333160122077730Google Scholar
Weaver, I. C. (2007). Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: Let's call the whole thing off. Epigenetics, 2, 22–28. doi:10.4161/epi.2.1.3881Google Scholar
Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., … Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854. doi:10.1038/nn1276Google Scholar
Widom, C. S. (1989). Does violence beget violence? A critical examination of the literature. Psychological Bulletin, 106, 3–28. doi:10.1037//0033-2909.106.1.3Google Scholar
Wright, S. E. (1993). Blaming the victim, blaming society or blaming the discipline: Fixing responsibility for poverty and homelessness. Sociological Quarterly, 34, 1–16. doi:10.1111/j.1533-8525.1993.tb00127.xGoogle Scholar
Yahyavi, S. T., Zarghami, M., Naghshvar, F., & Danesh, A. (2015). Relationship of cortisol, norepinephrine, and epinephrine levels with war-induced posttraumatic stress disorder in fathers and their offspring. Revista Brasileira de Psiquiatria, 37, 93–98. doi:10.1590/1516-4446-2014-1414Google Scholar
Yehuda, R. (2009). Status of glucocorticoid alterations in post-traumatic stress disorder. Annals of the New York Academy of Sciences, 1179, 56–69. doi:10.1111/j.1749-6632.2009.04979.xGoogle Scholar
Yehuda, R., Bierer, L. M., Andrew, R., Schmeidler, J., & Seckl, J. R. (2009). Enduring effects of severe developmental adversity, including nutritional deprivation, on cortisol metabolism in aging Holocaust survivors. Journal of Psychiatric Research, 43, 877–883. doi:10.1016/j.jpsychires.2008.12.003Google Scholar
Yehuda, R., Bierer, L. M., Schmeidler, J., Aferiat, D. H., Breslau, I., & Dolan, S. (2000). Low cortisol and risk for PTSD in adult offspring of holocaust survivors. American Journal of Psychiatry, 157, 1252–1259. doi:10.1176/appi.ajp.157.8.1252Google Scholar
Yehuda, R., Blair, W., Labinsky, E., & Bierer, L. M. (2007). Effects of parental PTSD on the cortisol response to dexamethasone administration in their adult offspring. American Journal of Psychiatry, 164, 163–166. doi:10.1176/ajp.2007.164.1.163Google Scholar
Yehuda, R., Boisoneau, D., Mason, J. W., & Giller, E. L. (1993). Glucocorticoid receptor number and cortisol excretion in mood, anxiety, and psychotic disorders. Biological Psychiatry, 34, 18–25. doi:10.1016/0006-3223(93)90252-9Google Scholar
Yehuda, R., Daskalakis, N. P., Lehrner, A., Desarnaud, F., Bader, H. N., Makotkine, I., … Meaney, M. J. (2014). Influences of maternal and paternal PTSD on epigenetic regulation of the glucocorticoid receptor gene in Holocaust survivor offspring. American Journal of Psychiatry, 171, 872–880. doi:10.1176/appi.ajp.2014.13121571Google Scholar
Yehuda, R., Engel, S. M., Brand, S. R., Seckl, J., Marcus, S. M., & Berkowitz, G. S. (2005). Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. Journal of Clinical Endocrinology & Metabolism, 90, 4115–4118. doi:10.1210/jc.2005-0550Google Scholar
Yehuda, R., Flory, J. D., Bierer, L. M., Henn-Haase, C., Lehrner, A., Desarnaud, F., … Meaney, M. J. (2015). Lower methylation of glucocorticoid receptor gene promoter 1F in peripheral blood of veterans with posttraumatic stress disorder. Biological Psychiatry, 77, 356–364. doi:10.1016/j.biopsych.2014.02.006Google Scholar
Yehuda, R., Golier, J. A., Yang, R.-K., & Tischler, L. (2004). Enhanced sensitivity to glucocorticoids in peripheral mononuclear leukocytes in posttraumatic stress disorder. Biological Psychiatry, 55, 1110–1116. doi:10.1016/s0006-3223(04)00188-xGoogle Scholar
Yehuda, R., Halligan, S. L., & Bierer, L. M. (2002). Cortisol levels in adult offspring of Holocaust survivors: Relation to PTSD symptom severity in the parent and child. Psychoneuroendocrinology, 27, 171–180. doi:10.1016/s0306-4530(01)00043-9Google Scholar
Yehuda, R., Halligan, S. L., Grossman, R., Golier, J. A., & Wong, C. (2002). The cortisol and glucocorticoid receptor response to low dose dexamethasone administration in aging combat veterans and holocaust survivors with and without posttraumatic stress disorder. Biological Psychiatry, 52, 393–403. doi:10.1016/s0006-3223(02)01357-4Google Scholar
Yehuda, R., Kahana, B., Binder-Brynes, K., & Southwick, S. M. (1995). Low urinary cortisol excretion in Holocaust survivors with posttraumatic stress disorder. American Journal of Psychiatry, 152, 982. doi:10.1176/ajp.152.7.982Google Scholar
Yehuda, R., Kahana, B., Schmeidler, J., & Southwick, S. M. (1995). Impact of cumulative lifetime trauma and recent stress on current posttraumatic stress disorder symptoms in Holocaust survivors. American Journal of Psychiatry, 152, 1815–1818. doi:10.1176/ajp.152.12.1815Google Scholar
Yehuda, R., & Lehrner, A. (2018). Intergenerational transmission of trauma effects: Putative role of epigenetic mechanisms. World Psychiatry, 17, 243–257. doi:10.1002/wps.20568.Google Scholar
Yehuda, R., Lehrner, A., & Bierer, L. M. (2018). The public reception of putative epigenetic mechanisms in the transgenerational effects of trauma. Environmental Epigenetics, 4, 1–7. doi:10.1093/eep/dvy018.Google Scholar
Yehuda, R., Lowy, M. T., Southwick, S. M., Shaffer, D., & Giller, E. L. Jr. (1991). Lymphocyte glucocorticoid receptor number in posttraumatic stress disorder. American Journal of Psychiatry, 148, 499–504. doi:10.1176/ajp.148.4.499Google Scholar
Yehuda, R., & McFarlane, A. (1995). Conflict between current knowledge about posttraumatic stress disorder and its original conceptual basis. American Journal of Psychiatry, 152, 1705–1713. doi:10.1176/ajp.152.12.1705Google Scholar
Yehuda, R., McFarlane, A., & Shalev, A. (1998). Predicting the development of posttraumatic stress disorder from the acute response to a traumatic event. Biological Psychiatry, 44, 1305–1313. doi:10.1016/s0006-3223(98)00276-5Google Scholar
Yehuda, R., Morris, A., Labinsky, E., Zemelman, S., & Schmeidler, J. (2007). Ten-year follow-up study of cortisol levels in aging holocaust survivors with and without PTSD. Journal of Traumatic Stress, 20, 757–761. doi:10.1002/jts.20228Google Scholar
Yehuda, R., Schmeidler, J., Siever, L. J., Binder-Brynes, K., & Elkin, A. (1997). Individual differences in posttraumatic stress disorder symptom profiles in Holocaust survivors in concentration camps or in hiding. Journal of Traumatic Stress, 10, 453–463. doi:10.1002/jts.2490100310Google Scholar
Yehuda, R., Schmeidler, J., Wainberg, M., Binder-Brynes, K., & Duvdevani, T. (1998). Vulnerability to posttraumatic stress disorder in adult offspring of Holocaust survivors. American Journal of Psychiatry, 155, 1163–1171. doi:10.1176/ajp.155.9.1163Google Scholar
Yehuda, R., Siever, L. J., Teicher, M. H., Levengood, R. A., Gerber, D. K., Schmeidler, J., & Yang, R.-K. (1998). Plasma norepinephrine and 3-methoxy-4-hydroxyphenylglycol concentrations and severity of depression in combat posttraumatic stress disorder and major depressive disorder. Biological Psychiatry, 44, 56–63. doi:10.1016/s0006-3223(98)80007-3Google Scholar
Yehuda, R., Southwick, S. M., Giller, E. L., Ma, X., & Mason, J. W. (1992). Urinary catecholamine excretion and severity of PTSD symptoms in Vietnam combat veterans. Journal of Nervous and Mental Disease, 180, 321–325. doi:10.1097/00005053-199205000-00006Google Scholar
Yehuda, R., Southwick, S. M., Krystal, J. H., Bremner, D., Charney, D. S., & Mason, J. W. (1993). Enhanced suppression of cortisol following dexamethasone administration in posttraumatic stress disorder. American Journal of Psychiatry, 150, 83. doi:10.1176/ajp.150.1.83Google Scholar
Yehuda, R., Southwick, S. M., Nussbaum, G., Wahby, V. S., Giller, E. L., & Mason, J. W. (1990). Low urinary cortisol excretion in patients with posttraumatic stress disorder. Journal of Nervous and Mental Disease, 35, 710–711. doi:10.1016/0006-3223(94)91000-6Google Scholar
Yehuda, R., Teicher, M. H., Seckl, J. R., Grossman, R. A., Morris, A., & Bierer, L. M. (2007). Parental posttraumatic stress disorder as a vulnerability factor for low cortisol trait in offspring of holocaust survivors. Archives of General Psychiatry, 64, 1040–1048. doi:10.1001/archpsyc.64.9.1040Google Scholar
Yehuda, R., Teicher, M. H., Trestman, R. L., Levengood, R. A., & Siever, L. J. (1996). Cortisol regulation in posttraumatic stress disorder and major depression: A chronobiological analysis. Biological Psychiatry, 40, 79–88. doi:10.1016/0006-3223(95)00451-3Google Scholar
Young, E. A., & Breslau, N. (2004). Cortisol and catecholamines in posttraumatic stress disorder: An epidemiologic community study. Archives of General Psychiatry, 61, 394–401. doi:10.1001/archpsyc.61.4.394Google Scholar