Lifelong impact of extreme stress on the human brain: Holocaust survivors study
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
33869682
PubMed Central
PMC8039853
DOI
10.1016/j.ynstr.2021.100318
PII: S2352-2895(21)00026-6
Knihovny.cz E-zdroje
- Klíčová slova
- Holocaust survivors, Lifelong impact, MRI, Posttraumatic growth, Posttraumatic stress,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: We aimed to assess the lifelong impact of extreme stress on people who survived the Holocaust. We hypothesised that the impact of extreme trauma is detectable even after more than 70 years of an often complicated and stressful post-war life. METHODS: Psychological testing was performed on 44 Holocaust survivors (HS; median age 81.5 years; 29 women; 26 HS were under the age of 12 years in 1945) and 31 control participants without a personal or family history of the Holocaust (control group (CG); median 80 years; 17 women). Magnetic resonance imaging (MRI) using the 3T Siemens Prisma scanner was performed on 29 HS (median 79 years; 18 women) and 21 CG participants (median 80 years; 11 women). The MRI-tested subgroup that had been younger than 12 years old in 1945 was composed of 20 HS (median 79 years; 17 women) and 21 CG (median 80 years; 11 women). RESULTS: HS experienced significantly higher frequency of depression symptoms, posttraumatic stress symptoms, and posttraumatic growth, and lower levels of well-being. The MRI shows a lifelong neurobiological effect of extreme stress. The areas with reduced grey matter correspond to the map of the impact of stress on the brain structure: insula, anterior cingulate, ventromedial cortex including the subgenual cingulate/orbitofrontal cortex, temporal pole, prefrontal cortex, and angular gyrus. HS showed good adjustment to post-war life conditions.Psychological growth may contribute to compensation for the psychological and neurobiological consequences of extreme stress.The reduction of GM was significantly expressed also in the subgroup of participants who survived the Holocaust during their childhood. CONCLUSION: The lifelong psychological and neurobiological changes in people who survived extreme stress were identified more than 70 years after the Holocaust. Extreme stress in childhood and young adulthood has an irreversible lifelong impact on the brain.
Zobrazit více v PubMed
Ansell E.B., Rando K., Tuit K., Guarnaccia J., Sinha R. Cumulative adversity and smaller gray matter volume in medial prefrontal, anterior cingulate, and insula regions. Biol. Psychiatr. Endocrinol. Epigenetics, Extinction, and Early Life Traumatization. 2012;72:57–64. doi: 10.1016/j.biopsych.2011.11.022. PubMed DOI PMC
Arnsten A.F.T., Raskind M.A., Taylor F.B., Connor D.F. The effects of stress exposure on prefrontal cortex: translating basic research into successful treatments for post-traumatic stress disorder. Neurobiol. Stress, Stress Resilience. 2015;1:89–99. doi: 10.1016/j.ynstr.2014.10.002. PubMed DOI PMC
Barel E., Van IJzendoorn M.H., Sagi-Schwartz A., Bakermans-Kranenburg M.J. Surviving the Holocaust: a meta-analysis of the long-term sequelae of a genocide. Psychol. Bull. 2010;136:677–698. doi: 10.1037/a0020339. PubMed DOI
Blais M.A., Lenderking W.R., Baer L., deLorell A., Peets K., Leahy L., Burns C. Development and initial validation of a brief mental health Outcome measure. J. Pers. Assess. 1999;73:359–373. doi: 10.1207/S15327752JPA7303_5. PubMed DOI
Bolsinger J., Seifritz E., Kleim B., Manoliu A. Neuroimaging correlates of resilience to traumatic events—a comprehensive review. Front. Psychiatr. 2018;9 doi: 10.3389/fpsyt.2018.00693. PubMed DOI PMC
Bremner J.D. Neuroimaging in posttraumatic stress disorder and other stress-related disorders. Neuroimaging Clin. N. Am., Imaging of the Mind. 2007;17:523–538. doi: 10.1016/j.nic.2007.07.003. PubMed DOI PMC
Bremner J.D. Traumatic stress: effects on the brain. Dialogues Clin. Neurosci. 2006;8:445–461. PubMed PMC
Bremner J.D. Long-term effects of childhood abuse on brain and neurobiology. Child Adolesc. Psychiatr. Clin. N. Am. 2003;12:271–292. doi: 10.1016/S1056-4993(02)00098-6. PubMed DOI
Bremner J.D., Narayan M., Anderson E.R., Staib L.H., Miller H.L., Charney D.S. Hippocampal volume reduction in major depression. Am. J. Psychiatr. 2000;157:115–118. doi: 10.1176/ajp.157.1.115. PubMed DOI
Bremner J.D., Randall P., Scott T.M., Bronen R.A., Seibyl J.P., Southwick S.M., Delaney R.C., McCarthy G., Charney D.S., Innis R.B. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am. J. Psychiatr. 1995;152:973–981. PubMed PMC
Bruce S.E., Buchholz K.R., Brown W.J., Yan L., Durbin A., Sheline Y.I. Altered emotional interference processing in the amygdala and insula in women with Post-Traumatic Stress Disorder. NeuroImage Clin. 2013;2:43–49. doi: 10.1016/j.nicl.2012.11.003. PubMed DOI PMC
Burke W.J., Roccaforte W.H., Wengel S.P. The short form of the geriatric depression scale: a comparison with the 30-item form. Top. Geriatr. 1991;4:173–178. doi: 10.1177/089198879100400310. PubMed DOI
Cai N., Fňašková M., Konečná K., Fojtová M., Fajkus J., Coomber E., Watt S., Soranzo N., Preiss M., Rektor I. No evidence of persistence or inheritance of mitochondrial DNA copy number in holocaust survivors and their descendants. Front. Genet. 2020;11 doi: 10.3389/fgene.2020.00087. PubMed DOI PMC
Chodoff P. Late effects of the concentration camp syndrome. Arch. Gen. Psychiatr. 1963;8:323–333. doi: 10.1001/archpsyc.1963.01720100013002. PubMed DOI
Cohen R.A., Grieve S., Hoth K.F., Paul R.H., Sweet L., Tate D., Gunstad J., Stroud L., McCaffery J., Hitsman B., Niaura R., Clark C.R., MacFarlane A., Bryant R., Gordon E., Williams L.M. Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol. Psychiatr. 2006;59:975–982. doi: 10.1016/j.biopsych.2005.12.016. PubMed DOI
Conybeare D., Behar E., Solomon A., Newman M.G., Borkovec T.D. The PTSD Checklist-Civilian Version: reliability, validity, and factor structure in a nonclinical sample. J. Clin. Psychol. 2012;68:699–713. doi: 10.1002/jclp.21845. PubMed DOI
Dannlowski U., Stuhrmann A., Beutelmann V., Zwanzger P., Lenzen T., Grotegerd D., Domschke K., Hohoff C., Ohrmann P., Bauer J., Lindner C., Postert C., Konrad C., Arolt V., Heindel W., Suslow T., Kugel H. Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biol. Psychiatr. Mech. Compromised Stress Resilience During Develop. Aging. 2012;71:286–293. doi: 10.1016/j.biopsych.2011.10.021. PubMed DOI
Devinsky O., Morrell M.J., Vogt B.A. Contributions of anterior cingulate cortex to behaviour. Brain. 1995;118:279–306. doi: 10.1093/brain/118.1.279. PubMed DOI
Diekhof E.K., Geier K., Falkai P., Gruber O. Fear is only as deep as the mind allows: a coordinate-based meta-analysis of neuroimaging studies on the regulation of negative affect. Neuroimage. 2011;58:275–285. doi: 10.1016/j.neuroimage.2011.05.073. PubMed DOI
Dragomirecka E., Lenderking W.R., Motlova L., Goppoldova E., Šelepova P. A brief mental health outcomes measure: translation and validation of the Czech version of the Schwartz outcomes scale-10. Qual. Life Res. 2006;15:307–312. doi: 10.1007/s11136-005-1389-y. PubMed DOI
Drevets W.C., Savitz J., Trimble M. The subgenual anterior cingulate cortex in mood disorders. CNS Spectr. 2008;13:663–681. PubMed PMC
Dye H. The impact and long-term effects of childhood trauma. J. Hum. Behav. Soc. Environ. 2018;28:381–392. doi: 10.1080/10911359.2018.1435328. DOI
Eitinger L. Concentration camp survivors IN the postwar world*. Am. J. Orthopsychiatry. 1962;32:367–375. doi: 10.1111/j.1939-0025.1962.tb00283.x. PubMed DOI
Elliott D.M., Briere J. Sexual abuse trauma among professional women: validating the Trauma Symptom Checklist-40 (TSC-40) Child Abuse Negl. 1992;16:391–398. doi: 10.1016/0145-2134(92)90048-V. PubMed DOI
Erikson E.H., Erikson J.M. W. W. Norton & Company; 1998. The Life Cycle Completed (Extended Version)
Ferren P.M. Comparing perceived self-efficacy among adolescent Bosnian and Croatian refugees with and without posttraumatic stress disorder. J. Trauma Stress. 1999;12:405–420. doi: 10.1023/A:1024749118463. PubMed DOI
Golier J.A., Yehuda R., De Santi S., Segal S., Dolan S., de Leon M.J. Absence of hippocampal volume differences in survivors of the Nazi Holocaust with and without posttraumatic stress disorder. Psychiatry Res. Neuroimaging. 2005;139:53–64. doi: 10.1016/j.pscychresns.2005.02.007. PubMed DOI
Graaf T.D. Pathological patterns of identification in families of survivors of the Holocaust. Isr. Ann. Psychiatry Relat. Discip. 1975;13:335–363. PubMed
Heitlinger A. Transaction Publishers; 2011. In the Shadows of the Holocaust and Communism: Czech and Slovak Jews since 1945.
Helweg-Larsen P., Hoffmeyer H., Kieler J., Thaysen E.H., Thaysen J.H., Thygesen P., Wulff M.H. Famine disease in German concentration Camps : complications and sequels with special reference to tuberculosis, mental disorders and social consequences. Acta Med. Scand. 1952;144 PubMed
Holland A.C., Addis D.R., Kensinger E.A. The neural correlates of specific versus general autobiographical memory construction and elaboration. Neuropsychologia. 2011;49:3164–3177. doi: 10.1016/j.neuropsychologia.2011.07.015. PubMed DOI PMC
Joffe C., Brodaty H., Luscombe G., Ehrlich F. The Sydney Holocaust study: posttraumatic stress disorder and other psychosocial morbidity in an aged community sample. J. Trauma Stress. 2003;16:39–47. doi: 10.1023/A:1022059311147. PubMed DOI
Kasai K., Yamasue H., Gilbertson M.W., Shenton M.E., Rauch S.L., Pitman R.K. Evidence for acquired pregenual anterior cingulate gray matter loss from a twin study of combat-related posttraumatic stress disorder. Biol. Psychiatr. 2008;63:550–556. doi: 10.1016/j.biopsych.2007.06.022. PubMed DOI PMC
Kassem M.S., Lagopoulos J., Stait-Gardner T., Price W.S., Chohan T.W., Arnold J.C., Hatton S.N., Bennett M.R. Stress-induced grey matter loss determined by MRI is primarily due to loss of dendrites and their synapses. Mol. Neurobiol. 2013;47:645–661. doi: 10.1007/s12035-012-8365-7. PubMed DOI
Keilson H., Sarphatie H.R. Magnes Press; Jerusalem, Israel: 1992. Sequential Traumatization in Children: A Clinical and Statistical Follow-Up Study on the Fate of the Jewish War Orphans in the Netherlands, Sequential Traumatization in Children: A Clinical and Statistical Follow-Up Study on the Fate of the Jewish War Orphans in the Netherlands.
Konečná K., Lyčka M., Nohelová L., Petráková M., Fňašková M., Koriťáková E., Sováková P.P., Brabencová S., Preiss M., Rektor I., Fajkus J., Fojtová M. Holocaust history is not reflected in telomere homeostasis in survivors and their offspring. J. Psychiatr. Res. 2019;117:7–14. doi: 10.1016/j.jpsychires.2019.06.018. PubMed DOI
Krell R. Child survivors of the holocaust — strategies of adaptation. Can. J. Psychiatr. 1993;38:384–389. doi: 10.1177/070674379303800603. PubMed DOI
Kuo J.R., Kaloupek D.G., Woodward S.H. Amygdala volume in combat-exposed veterans with and without posttraumatic stress disorder: a cross-sectional study. Arch. Gen. Psychiatr. 2012;69:1080–1086. doi: 10.1001/archgenpsychiatry.2012.73. PubMed DOI
Landau R., Litwin H. The effects of extreme early stress in very old age. J. Trauma Stress. 2000;13:473–487. doi: 10.1023/A:1007737425260. PubMed DOI
Levav I., Abramson J.H. Emotional distress among concentration camp survivors – a community study in Jerusalem. Psychol. Med. 1984;14:215–218. doi: 10.1017/S003329170000324X. PubMed DOI
Li L., Wu M., Liao Y., Ouyang L., Du M., Lei D., Chen L., Yao L., Huang X., Gong Q. Grey matter reduction associated with posttraumatic stress disorder and traumatic stress. Neurosci. Biobehav. Rev. 2014;43:163–172. doi: 10.1016/j.neubiorev.2014.04.003. PubMed DOI
Lindemer E.R., Salat D.H., Leritz E.C., McGlinchey R.E., Milberg W.P. Reduced cortical thickness with increased lifetime burden of PTSD in OEF/OIF Veterans and the impact of comorbid TBI. NeuroImage Clin. 2013;2:601–611. doi: 10.1016/j.nicl.2013.04.009. PubMed DOI PMC
Logue M.W., van Rooij S.J.H., Dennis E.L., Davis S.L., Hayes J.P., Stevens J.S., Densmore M., Haswell C.C., Ipser J., Koch S.B.J., Korgaonkar M., Lebois L.A.M., Peverill M., Baker J.T., Boedhoe P.S.W., Frijling J.L., Gruber S.A., Harpaz-Rotem I., Jahanshad N., Koopowitz S., Levy I., Nawijn L., O'Connor L., Olff M., Salat D.H., Sheridan M.A., Spielberg J.M., van Zuiden M., Winternitz S.R., Wolff J.D., Wolf E.J., Wang X., Wrocklage K., Abdallah C.G., Bryant R.A., Geuze E., Jovanovic T., Kaufman M.L., King A.P., Krystal J.H., Lagopoulos J., Bennett M., Lanius R., Liberzon I., McGlinchey R.E., McLaughlin K.A., Milberg W.P., Miller M.W., Ressler K.J., Veltman D.J., Stein D.J., Thomaes K., Thompson P.M., Morey R.A. Smaller hippocampal volume in posttraumatic stress disorder: a multisite ENIGMA-PGC study: subcortical volumetry results from posttraumatic stress disorder consortia. Biol. Psychiatr. 2018;83:244–253. doi: 10.1016/j.biopsych.2017.09.006. PubMed DOI PMC
Lupien S.J., Lepage M. Stress, memory, and the hippocampus: can't live with it, can't live without it. Behav. Brain Res. 2001;127:137–158. doi: 10.1016/S0166-4328(01)00361-8. PubMed DOI
Lupien S.J., Mcewen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. Lond. 2009;10:434–445. doi: 10.1038/nrn2639. PubMed DOI
Marečková K., Klasnja A., Bencurova P., Andrýsková L., Brázdil M., Paus T. Prenatal stress, mood, and gray matter volume in young adulthood. Cerebr. Cortex. 2019;29:1244–1250. doi: 10.1093/cercor/bhy030. PubMed DOI PMC
McEwen B.S., Morrison J.H. The brain on stress: vulnerability and plasticity of the prefrontal cortex over the life course. Neuron. 2013;79:16–29. doi: 10.1016/j.neuron.2013.06.028. PubMed DOI PMC
McEwen B.S., Nasca C., Gray J.D. Stress effects on neuronal structure: Hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology. 2016;41:3–23. doi: 10.1038/npp.2015.171. PubMed DOI PMC
Menon V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cognit. Sci. 2011;15:483–506. doi: 10.1016/j.tics.2011.08.003. PubMed DOI
Noriuchi M., Kikuchi Y., Mori K., Kamio Y. The orbitofrontal cortex modulates parenting stress in the maternal brain. Sci. Rep. 2019;9:1658. doi: 10.1038/s41598-018-38402-9. PubMed DOI PMC
Paulus M.P., Stein M.B. An insular view of anxiety. Biol. Psychiatr. 2006;60:383–387. doi: 10.1016/j.biopsych.2006.03.042. PubMed DOI
Perez D.L., Dworetzky B.A., Dickerson B.C., Leung L., Cohn R., Baslet G., Silbersweig D.A. An integrative neurocircuit perspective on psychogenic nonepileptic seizures and functional movement disorders: neural functional unawareness. Clin. EEG Neurosci. 2015;46:4–15. doi: 10.1177/1550059414555905. PubMed DOI PMC
Perez D.L., Matin N., Barsky A., Costumero-Ramos V., Makaretz S.J., Young S.S., Sepulcre J., LaFranceJr W.C., Keshavan M.S., Dickerson B.C. Cingulo-insular structural alterations associated with psychogenic symptoms, childhood abuse and PTSD in functional neurological disorders. J. Neurol. Neurosurg. Psychiatry. 2017;88:491–497. doi: 10.1136/jnnp-2016-314998. PubMed DOI PMC
Phillips M.L., Drevets W.C., Rauch S.L., Lane R. Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol. Psychiatr. 2003;54:504–514. doi: 10.1016/S0006-3223(03)00168-9. PubMed DOI
Prager E., Solomon Z. Perceptions of world benevolence, meaningfulness, and self-worth among elderly israeli holocaust survivors and non-survivors. Hist. Philos. Logic. 1995;8:265–277. doi: 10.1080/10615809508249378. DOI
Rolls E.T., Cheng W., Gong W., Qiu J., Zhou C., Zhang J., Lv W., Ruan H., Wei D., Cheng K., Meng J., Xie P., Feng J. Cereb. Cortex N. Y. N; 2018. Functional connectivity of the anterior cingulate cortex in depression and in health. 1991. PubMed DOI
Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat. Rev. Neurosci. 2009;10:423–433. doi: 10.1038/nrn2651. PubMed DOI
Rousseau C., Drapeau A., Rahimi S. The complexity of trauma response: a 4-year follow-up of adolescent Cambodian refugees. Child Abuse Negl. 2003;27:1277–1290. doi: 10.1016/j.chiabu.2003.07.001. PubMed DOI
Sagi-Schwartz A., Bakermans-Kranenburg M.J., Linn S., IJzendoorn M.H. van. Against all odds: genocidal trauma is associated with longer life-expectancy of the survivors. PloS One. 2013;8 doi: 10.1371/journal.pone.0069179. PubMed DOI PMC
Sagi-Schwartz A., van IJzendoorn M.H., Grossmann K.E., Joels T., Grossmann K., Scharf M., Koren-Karie N., Alkalay S. Attachment and traumatic stress in female holocaust child survivors and their daughters. Am. J. Psychiatr. 2003;160:1086–1092. doi: 10.1176/appi.ajp.160.6.1086. PubMed DOI
Sigal J.J., Weinfeld M. Do children cope better than adults with potentially traumatic stress? A 40-year follow-up of holocaust survivors. Psychiatr. Interpers. Biol. Process. 2001;64:69–80. doi: 10.1521/psyc.64.1.69.18236. PubMed DOI
Solomon P.R., Hirschoff A., Kelly B., Relin M., Brush M., DeVeaux R.D., Pendlebury W.W. A 7 minute neurocognitive screening battery highly sensitive to alzheimer's disease. Arch. Neurol. 1998;55:349–355. doi: 10.1001/archneur.55.3.349. PubMed DOI
Steffens R.F., Andrykowski M.A. Posttraumatic growth inventory: overview. In: Martin C.R., Preedy V.R., Patel V.B., editors. Comprehensive Guide to Post-Traumatic Stress Disorder. Springer International Publishing; Cham: 2015. pp. 1–14. DOI
Stevens J.S., Jovanovic T. Role of social cognition in post-traumatic stress disorder: a review and meta-analysis. Gene Brain Behav. 2019;18 doi: 10.1111/gbb.12518. PubMed DOI PMC
Tedeschi R.G., Calhoun L.G. The posttraumatic growth inventory: measuring the positive legacy of trauma. J. Trauma Stress. 1996;9:455–471. doi: 10.1007/BF02103658. PubMed DOI
Teicher M.H., Andersen S.L., Polcari A., Anderson C.M., Navalta C.P., Kim D.M. The neurobiological consequences of early stress and childhood maltreatment. Neurosci. Biobehav. Rev., Brain Develop. Sex Diff. Stress: Implicat. Psychopathol. 2003;27:33–44. doi: 10.1016/S0149-7634(03)00007-1. PubMed DOI
Thomason M.E., Marusak H.A. Toward understanding the impact of trauma on the early developing human brain. Neurosci. Early Adversity and Brain Develop. 2017;342:55–67. doi: 10.1016/j.neuroscience.2016.02.022. PubMed DOI PMC
Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15:273–289. doi: 10.1006/nimg.2001.0978. PubMed DOI
Villarreal G., Hamilton D.A., Petropoulos H., Driscoll I., Rowland L.M., Griego J.A., Kodituwakku P.W., Hart B.L., Escalona R., Brooks W.M. Reduced hippocampal volume and total white matter volume in posttraumatic stress disorder. Biol. Psychiatr. 2002;52:119–125. doi: 10.1016/S0006-3223(02)01359-8. PubMed DOI
Yaribeygi H., Panahi Y., Sahraei H., Johnston T.P., Sahebkar A. The impact of stress on body function: a review. EXCLI J. 2017;16:1057–1072. doi: 10.17179/excli2017-480. PubMed DOI PMC
Yehuda R., Schmeidler J., Giller E.L., Siever L.J., Binder-Brynes K. Relationship between posttraumatic stress disorder characteristics of holocaust survivors and their adult offspring. Am. J. Psychiatr. 1998;155:841–843. doi: 10.1176/ajp.155.6.841. PubMed DOI
Young J.L., Waehler C.A., Laux J.M., McDaniel P.S., Hilsenroth M.J. Four studies extending the utility of the Schwartz Outcome scale (SOS-10) J. Pers. Assess. 2003;80:130–138. doi: 10.1207/S15327752JPA8002_02. PubMed DOI