Upload
others
View
1
Download
0
Embed Size (px)
Citation preview
University of Groningen
Intergenerational consequences of the Holocaust on offspring mental healthDashorst, Patricia; Mooren, Trudy M.; Kleber, Rolf J.; de Jong, Peter J.; Huntjens, Rafaele J.C.Published in:European Journal of Psychotraumatology
DOI:10.1080/20008198.2019.1654065
IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite fromit. Please check the document version below.
Document VersionPublisher's PDF, also known as Version of record
Publication date:2019
Link to publication in University of Groningen/UMCG research database
Citation for published version (APA):Dashorst, P., Mooren, T. M., Kleber, R. J., de Jong, P. J., & Huntjens, R. J. C. (2019). Intergenerationalconsequences of the Holocaust on offspring mental health: a systematic review of associated factors andmechanisms. European Journal of Psychotraumatology, 10(1), [1654065].https://doi.org/10.1080/20008198.2019.1654065
CopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).
Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.
Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.
Download date: 27-08-2020
Full Terms & Conditions of access and use can be found athttps://www.tandfonline.com/action/journalInformation?journalCode=zept20
European Journal of Psychotraumatology
ISSN: 2000-8198 (Print) 2000-8066 (Online) Journal homepage: https://www.tandfonline.com/loi/zept20
Intergenerational consequences of the Holocauston offspring mental health: a systematic review ofassociated factors and mechanisms
Patricia Dashorst, Trudy M. Mooren, Rolf J. Kleber, Peter J. de Jong & RafaeleJ. C. Huntjens
To cite this article: Patricia Dashorst, Trudy M. Mooren, Rolf J. Kleber, Peter J. de Jong &Rafaele J. C. Huntjens (2019) Intergenerational consequences of the Holocaust on offspringmental health: a systematic review of associated factors and mechanisms, European Journal ofPsychotraumatology, 10:1, 1654065, DOI: 10.1080/20008198.2019.1654065
To link to this article: https://doi.org/10.1080/20008198.2019.1654065
© 2019 The Author(s). Published by InformaUK Limited, trading as Taylor & FrancisGroup.
Published online: 30 Aug 2019.
Submit your article to this journal
Article views: 365
View related articles
View Crossmark data
REVIEW ARTICLE
Intergenerational consequences of the Holocaust on offspring mental health:a systematic review of associated factors and mechanismsPatricia Dashorsta, Trudy M. Moorenb,c, Rolf J. Kleberb,c, Peter J. de Jongd and Rafaele J. C. Huntjensd
aStichting Centrum’45/partner in Arq, Oegstgeest, The Netherlands; bStichting Centrum’45/partner in Arq, Diemen, The Netherlands;cDepartment of Clinical & Health Psychology, Utrecht University, Utrecht, The Netherlands; dDepartment of Clinical Psychology &Experimental Psychopathology, University of Groningen, Groningen, The Netherlands
ABSTRACTExposure to war and violence has major consequences for society at large, detrimentalimpact on people’s individual lives, and may also have intergenerational consequences. Togain more insight into these intergenerational consequences, research addressing theimpact of the Holocaust on offspring is an important source of information. The aim ofthe current study was to systematically review the mechanisms of intergenerational con-sequences by summarizing characteristics in Holocaust survivors and their offspring sug-gested to impact the offspring’s mental health. We focused on: 1) parental mental healthproblems, 2) (perceived) parenting and attachment quality, 3) family structure, especiallyparental Holocaust history, 4) additional stress and life events, and 5) psychophysiologicalprocesses of transmission. We identified 23 eligible studies published between 2000 and2018. Only Holocaust survivor studies met the inclusion criteria. Various parent and childcharacteristics and their interaction were found to contribute to the development ofpsychological symptoms and biological and epigenetic variations. Parental mental healthproblems, perceived parenting, attachment quality, and parental gender appeared to beinfluential for the mental well-being of their offspring. In addition, having two survivorparents resulted in higher mental health problems compared to having one survivor parent.Also, there was evidence suggesting that Holocaust survivor offspring show a heightenedvulnerability for stress, although this was only evident in the face of actual danger. Finally,the results also indicate intergenerational effects on offspring cortisol levels. Clinical andtreatment implications are discussed.
Las consecuencias intergeneracionales del Holocausto en la saludmental de la descendencia: Una revisión sistemática de los factores ylos mecanismos asociadosLa exposición a la guerra y la violencia tiene consecuencias importantes para la sociedaden general, un impacto perjudicial en la vida individual de las personas, y tambiénpuede tener consecuencias intergeneracionales. Para obtener más información sobreestas consecuencias intergeneracionales, la investigación que aborda el impacto delHolocausto en la descendencia es una fuente importante de información. El objetivodel presente estudio fue revisar sistemáticamente los mecanismos de las consecuenciasintergeneracionales resumiendo las características de los sobrevivientes del Holocausto ysus descendientes, que podrían impactar la salud mental de la descendencia. Noscentramos en: 1) los problemas de salud mental de los padres, 2) la calidad (percibida)de la crianza y el apego, 3) la estructura familiar, especialmente antecedentes delHolocausto de los padres, 4) el estrés y los eventos de la vida adicionales, y 5) losprocesos psicofisiológicos de la transmisión. Identificamos 23 estudios elegibles publica-dos entre 2000 y 2018. Solo los estudios de sobrevivientes del Holocausto cumplieroncon los criterios de inclusión. Se descubrió que diversas características de los padres y delos hijos y su interacción contribuyen al desarrollo de los síntomas psicológicos y lasvariaciones biológicas y epigenéticas. Los problemas de salud mental de los padres, lacrianza percibida, la calidad del apego, y el género parental parecieron influir en elbienestar mental de sus hijos. Además, tener dos padres sobrevivientes resultó enmayores problemas de salud mental en comparación con tener uno de los padressobrevivientes. Además, hubo evidencia que sugiere que los descendientes de lossobrevivientes del Holocausto muestran una mayor vulnerabilidad al estrés, aunqueesto fue solo evidente ante el peligro real. Finalmente, los resultados también indicanlos efectos intergeneracionales en los niveles de cortisol de la descendencia. Se discutenlas implicaciones clínicas y de tratamiento.
ARTICLE HISTORYReceived 22 December 2018Revised 14 July 2019Accepted 28 July 2019
KEYWORDSHolocaust; intergenerational;trauma; offspring
PALABRAS CLAVEHolocausto;intergeneracional; trauma;descendencia
关键词
大屠杀; 代际; 创伤; 后代
HIGHLIGHTS• The aim was to review themechanisms ofintergenerationalconsequences of theholocaust.• Survivor mothers weremore influential for the well-being of their offspring thanfathers.• Having two survivorparents resulted in highermental health problemscompared to one.• Heightened vulnerabilityfor stress in offspring wasfound in the presence ofactual danger• The results indicatedintergenerational effectswith regard to cortisollevels.
CONTACT Patricia Dashorst [email protected] Stichting Centrum’45/partner in Arq, Rijnzichtweg 35, Oegstgeest 2342AX, TheNetherlands
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY2019, VOL. 10, 1654065https://doi.org/10.1080/20008198.2019.1654065
© 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/),which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
大屠杀对后代心理健康的代际影响:一个相关因素和机制的系统综述
暴露于战争和暴力会对整个社会产生重大影响,会对人们的个人生活造成不利影响,并也可能产生代际影响。为了更深入地了解这些代际影响,探讨大屠杀对后代影响的研究是一个重要的信息来源。本研究的目的是通过总结大屠杀幸存者及其后代中暗示会影响后代心理健康的特征来系统地回顾代际影响的机制。我们重点关注:1)父母的心理健康问题,2)(感知到的)父母养育和依恋质量,3)家庭结构,尤其是父母的大屠杀史,4)额外的应激和生活事件,以及5)传递的心理生理过程。我们确定出23项发表于2000年至2018年间符合条件的研究。只有大屠杀幸存者的研究符合纳入标准。多种亲子特征及其互动方式被发现会促进心理症状的发展、生物及表观遗传变异。父母的心理健康问题、感知到的养育、依恋质量和父母的性别似乎对他们后代的心理健康有影响。此外,有两名幸存者父母相较于有一名幸存者父母的后代会出现更多的心理健康问题。另外有证据表明,大屠杀幸存者后代会表现出更高的应激脆弱性,尽管只是在面对实际危险时才明显。最后,结果也表明了在后代皮质醇水平上的代际影响。文中还讨论了临床和治疗意义。
1. Introduction
War and violence have been part of human history.Nowadays more than 65 million people around theworld have been forced to leave home as a result ofarmed conflicts; more than 21 million of them arerefugees of whom more than half younger than 18years of age (www.UNHCR.org). Exposure to warand violence not only has major consequences forsociety at large but also has detrimental impact onpeople’s individual lives. Besides trauma-related psy-chopathology of those exposed, violence and war mayalso have intergenerational consequences (Betancourt,2015; Danieli, 1998; Havinga et al., 2017). The term‘transmission’ of trauma has been used to describethese consequences, defined as thoughts, feelings, andbehaviours generated from the survivors’ experiencesand transmitted to their offspring (Fonagy, 1999;Kretchmar & Jacobovitz, 2002; Munroe et al., 1995).While some definitions describe similar symptoms forsurvivors and their offspring, other describe a moreindirect process, through which, consciously or uncon-sciously, the experiences of the earlier generation influ-ence (first and second generation) parenting attitudeand behaviour (Baider et al., 2000; Van IJzendoorn &Schuengel, 1996). A better understanding of the inter-generational impact of violence and war is importantnot only from a theoretical perspective but also para-mount for generating ideas for (more) effective inter-ventions to help minimize these consequences insurvivors of war.
While empirical research on the intergenerationalconsequences of violence and war focused mainly onoffspring of Holocaust survivors, exceptions have alsoconsidered other violence-stricken populations such asrefugees and survivors of repressive regimes and tor-ture (Bloch, 2018; Sangalang, Jager, & Harachi, 2017;Sangalang & Vang, 2017). Methodologically, this fieldhas evolved from clinical case studies in the 1960s todescriptive patient group studies in the seventies, andto studies including clinical and non-clinical groups in
the eighties and nineties (Danieli, 1998; Solkoff, 1981,1992). In the last two decades, integrative reviewsreached the conclusion that, overall, Holocaust survi-vor offspring (HSO) did not present quantitativelymore signs of mental health problems than non-survi-vor offspring. The authors of these analyses doacknowledged, however, the existence of a group ofoffspring characterized by psychopathological symp-toms (in)directly related to their parents’ war experi-ences, their parents’ war-related psychopathology, and/or the impact of growing up in a Holocaust survivorfamily (Felsen, 1998; Kellermann, 2001; Solomon,1998; Van IJzendoorn, Bakermans-Kranenburg, &Sagi-Schwartz, 2003). In addition, a review by Leen-Feldner et al. (2013) among parents with PTSD (i.e.,including but not restricted to Holocaust survivors)suggested that parental symptoms of PTSD are asso-ciated to various offspring mental health problems,including internalizing-type problems, general beha-vioural problems, and altered hypothalamic-pituitary-adrenal axis functioning. The important question thenarises how parental war experiences contribute to themental health problems of the HSO.
The aim of this systematic review was to increase ourunderstanding of intergenerational consequences of(mass) violence by examining possible mechanisms thatare associated with and may contribute to the develop-ment of mental health problems in World War II andspecifically Holocaust survivor offspring. More specifi-cally, five possible mechanisms will be evaluated thathave been identified on the basis of theoretical andempirical studies as factors that may play a critical rolein HSO mental health (Kellermann, 2001; Leen-Feldneret al., 2013;McGuire, Palaniappan, & Larribas, 2015; VanIJzendoorn et al., 2003). The current review focused on:(a) parental mental health problems; (b) (perceived)parenting and attachment; (c) parental Holocaust his-tory; (d) additional stress and traumatic life events inHSO; and (e) cortisol metabolism, epigenetic factors, andgenetic predisposition.
2 P. DASHORST ET AL.
1.1. Parental mental health problems
Severe mental illness may affect not only thosesuffering from it but also those who are in closepersonal contact with them (Lombardo & Motta,2008). For example, parents with severe anxietyand/or depression may model patterns of thinking,feeling and behaving for their children (Katz,Hammen, & Brennan, 2013; Rasic, Hajek, Alda,& Uher, 2014). Low self-esteem, distrust towardsfellow human beings, and a pessimistic outlook onthe world in general and on the future may be thedominant message conveyed to their offspring. Wehypothesized therefore that a higher incidence ofcurrent and lifetime mental health problems andpsychiatric diagnoses in Holocaust survivors arerelated to a higher incidence of mental healthproblems in HSO.
1.2. (Perceived) parenting and attachment
The attachment theory prescribes parenting that isresponsive and attuned to the needs of the youngchild to grow up, thrive and explore the world(Bowlby, 1982; Winnicott, 1971). Parents who have todeal with unresolved problems from their past, forinstance loss or maltreatment, may have difficulty inattuning to the needs of their offspring, impacting thequality of the interactions of parents with their children.Parents may, for example, exhibit frightened, frighten-ing, or unexpected behaviour when they associatestressful situations in their current life with traumaticexperiences in the past. These parenting practices ordynamics in the parent–child relationship may, in turn,underlie disorganized attachment and contribute to off-spring’s mental health problems (Hesse, 1999).
Furthermore, the caregiving style of Holocaustsurvivor parents has been characterized by a per-ceived inability to provide physical and emotionalcare and the perceived reversal of parent and childroles, as was stated by Wiseman et al. (2002) intheir qualitative assessment of the characteristicsof growing up in Holocaust survivor families (asperceived by offspring). Scharf and Mayseless(2011) indicated three major themes that charac-terized the parent–child relationship quality ofHSO: Survival issues (e.g. overprotection and fearof separation), lack of emotional resources (e.g.emotional neglect and unpredictable emotionalreaction), and coercion of the child to please theparents and satisfy their needs (e.g. push to achieveand role reversal). Following this, we hypothesizedthat Holocaust experiences of the parents are asso-ciated with an unfavourable attachment style andrelated to unfavourable psychological developmentof HSO.
1.3. Parental Holocaust history
As a result of themere absence of family members due tothe Holocaust, the offspring may have had less familysupport available compared to non-Holocaust offspring.Moreover, survivor parent(s) possibly were less able toprovide direct and indirect care, such as acting as anadequate role model or providing emotional supportand advise (Chaitin, 2002; Krell, Suedfeld, & Soriano,2004; Wiseman et al., 2002). Children in one-survivorfamilies (i.e., with the other parent alive and non-survi-vor) may be better off compared to children in two-survivor families, as the non-survivor parent can com-plement some of the tasks that are difficult for thesurvivor parent. We therefore hypothesized that growingup in a two-survivor family versus a one-survivor familyis associated with more mental health problems inoffspring.
Next, both parents will exert a different influenceon the child’s psychological development, for exam-ple in the processes of socialization; mothers stillbeing dominant as a caregiver in particular whenchildren are young (Kellermann, 2008; Wiseman etal., 2002). Besides the difference in parenting stylebetween fathers and mothers it is becoming increas-ingly clear that severe stress in mothers during preg-nancy can affect the development of the unborn child(Glover, 2015; Reynolds et al., 2015; Taouk &Schulkin, 2016). We thus expected a higher incidenceof mental health problems in offspring of mothersurvivors compared to father survivors.
1.4. Additional stress and traumatic life events inHSO
Several authors have suggested a diathesis-stressmodel that predicts heightened vulnerability in HSOfor stressful life events occurring later in life(Kellermann, 2001; Van IJzendoorn et al., 2003). Inother words, HSO may show increased vulnerabilityto develop psychological disturbances when affectedby serious physical or psychological stressors addi-tional to the familial Holocaust experiences, likebreast cancer (Baider et al., 2000) or combat experi-ences (Solomon, Kotler, & Mikulincer, 1988). Wethus hypothesized that HSO suffer from more mentalhealth problems as a result of cumulating negative lifeevents than non-survivor offspring.
1.5. Cortisol metabolism, epigenetic factors,genetic predisposition
Besides the impact of psychological mechanisms link-ing parental trauma and offspring mental distress, agrowing number of studies have considered biologicaland (epi)genetic mechanisms linking parental trauma
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 3
with changes in offspring’s cortisol metabolism com-pared to offspring of non-traumatized parents (e.g.Yehuda & Bierer, 2008b; Yehuda et al., 2005). It isbecoming increasingly clear that parental stress, in apre- or post-natal period, affects the stress system ofoffspring leading to epigenetic and cortisol levelchanges (Betancourt, 2015; Heim & Binder, 2012).The hypothalamic-pituitary-adrenal (HPA)-axis andthe autonomic nervous system are central elements ofthe biological stress system. The HPA-axis function-ing includes a cascade of neuroendocrine reactionswith corticotrophin-releasing hormone (CRH) andadrenocorticotropic hormone (ACTH), which stimu-lates the secretion of the glucocorticoid cortisol and afeedback loop of cortisol binding with mineralocorti-coid receptors (MR) and glucocorticoid receptors(GR). During stress, cortisol levels are high. The feed-back loop prevents the stress-reaction from cortisolovershooting and promotes restoration after stress.When this stress system is activated for a longerperiod, however, or if there is no proper negativefeedback inhibition of cortisol, basal hormone levelsare not properly restored and this can lead to distur-bances of the stress response and, in the long run, tothe development of various types of disease. People inconditions of acute or chronic stress, and withoutPTSD, have heightened cortisol levels. In contrast,in individuals with PTSD, basal cortisol levels havedecreased and cortisol receptors appear to be moresensitive to cortisol.
In addition, (epigenetic) alterations have been asso-ciated with parental PTSD, major depression and inter-generational effects on cortisolmetabolism. FKBP5 is oneof the genes that have impact on the stress response andspecifically on glucocorticoid receptor sensitivity (GR-sensitivity) and responsiveness by altered methylation(Naumova et al., 2016). Increased FKBP5 methylationgives rise to decreased GR-sensitivity. Cortisol levelsand responsivity thus appear to be an important indexof the stress system and were therefore used as an indi-cator for heightened stress levels within the currentreview (Duthie & Reynolds, 2013; Klaassens, 2010). Wehypothesized that HSO show increased basal cortisollevels, show less cortisol reactivity, and increased FKBP5methylation.
2. Methods
2.1. Search strategy, study selection, and datacoding
We conducted a systematic literature search using thePreferred Reporting items for Systematic Reviews andMeta-Analyses (PRISMA) criteria (Liberati et al., 2009)to identify studies on offspring of World War Twosurvivors, published between 2000 and February 2018with regard to the aforementioned factors. This
timespan was chosen because studies up to 2000were included in comprehensive former reviews(Kellermann, 2001; Van IJzendoorn et al., 2003). Thesearch was performed using the following databases:PsycINFO, Pilots, Ovid Medline and Embase. Thedomains of the search and their synonyms were com-bined into syntaxes using Boolean operators. Onlystudies written in the English language were selected.The key-words have been chosen to closely align withthe central concepts in our hypotheses. The list of key-terms (including synonyms) was as follows: SecondWorld War, Holocaust, concentration camp, survivor,child, adult offspring, second generation, mental orpsychological disorders, symptoms, specific disorders(e.g. PTSD, depression, anxiety disorders, personalitydisorders), mental illness, symptoms, comorbidities,well-being, quality of life, identity, individuation, neu-robiology, neuropsychology, genetic, epigenetic, corti-sol metabolism. For the full syntax (PsycINFO) seeappendix 1.
Figure 1 contains a flowchart of the study selec-tion. World War Two survivor offspring was definedas being born after the war had ended, and havinghad at least one parent that was exposed to WorldWar Two cruelties. The studies were considered eli-gible for inclusion if they: (a) were written in theEnglish language, (b) included World War Two sur-vivors and offspring and (c) contained quantitativedata. Excluded were (d) narrative or qualitative stu-dies without quantitative data and (e) case reports,dissertations, book reviews, conference reports, theo-retical papers and studies which had already beenincorporated in earlier reviews (Kellermann, 2001;Van IJzendoorn et al., 2003).
In the initial search, 1372 studies were retrieved.After excluding duplicates, 392 studies remained, and319 remained after screening of titles. Next, tworesearchers (PD & RK) independently reviewed theabstracts. After screening the abstracts, 34 articlesremained and based on the full text, the final selec-tion consisted of 23 articles. The reviewers agreed on98% of the selected studies. After the debate, consen-sus was achieved on the remaining studies. Withregard to data extraction, two authors (RH & TM)independently checked the accuracy of the firstreviewer (PD) who extracted the data from the 23included studies. Disagreements were resolved bydiscussion.
3. Results
3.1. General study characteristics
The study characteristics of the selected studies arepresented in Table 1. Several quality assessment toolswere considered to evaluate the quality of the reviewedstudies including the Cochrane Collaboration tool
4 P. DASHORST ET AL.
(Deeks et al., 2003; Downs & Black, 1998), the CASP-Qualitative Checklist (2018) and the quality assessmentcriteria forwarded by the Joanna Briggs Institute(Moola et al., 2017). Unfortunately, most criteria werenot applicable to the studies included in this review andnot useful to evaluate their quality. Only a few generalitems of the instruments were suitable. Applying onlypart of the criteria of those standardized checklists hasthe disadvantage of having an incomplete assessmentscore which will be hard to interpret and compare toother studies. Therefore, we focused on the relevantmethodological variables (i.e., recruitment and sampledetails, instruments used for diagnosis, measurement ofoutcomes, and statistical results) mentioned in Table 1.
The final selection of studies all pertained to HSO;studies that focused on the intergenerational impact ofany other World War Two survivors did not meet theinclusion criteria and therefore could not be included.Comparison groups in these studies mostly consisted ofnon-traumatized Jewish people (JCO). Most studiesused convenient samples, recruited by advertisementor at conferences or meetings of Holocaust-relatedorganizations. Sample-sizes were: Holocaust survivorsN between 32 and 178, mean age range 69 to 76 year;HSO N between 20 and 300, mean age range 38 to 57;
JCO N between 9 and 149, mean age range between 37and 58. In some studies, the same, or partially over-lapping, samples were used. Five studies included twogenerations (i.e., parents and offspring). Most studiesincluded only offspring and data of the parents wereobtained through reports of their children. Thirteen ofthe 23 studies included males and females, other studiesconsisted of only women. Participants in three studieswere recruited through mental health-care providers.Usually, participants with severe mental disorders, suchas psychosis or bipolar disorder, alcohol or substancedependence or major medical illness were excluded. Allstudies entailed a cross-sectional design. Comparingmental health problems between HSO and JCO (seeTable 1), it can be concluded that HSO reported morelifetime symptoms of anxiety disorders (includingPTSD according to DSM-IV (Diagnostic andStatistical Manual of Mental Disorders, AmericanPsychiatric Association [APA], 2000)) and depression,lower self-esteem, and difficulties in interpersonal func-tioning, they also showed difficulties in aggression reg-ulation, a higher vulnerability to psychological distress,and they showed biological changes such as lower cor-tisol levels and epigenetic changes, with lower FKBP5methylation compared to JCO.
Records identified through data base searching PsycINFO (n= 344) OVID Medline and Embase (n = 489) PILOTS (n = 539)
Total (n = 1372) Records after duplicates removed and publication date between
2000 and February 2018 Total (n = 392)
Articles screened on the basis of title (n = 392)
Articles screened on the basis of abstract (n = 319)
Full text articles on basis of full text (n = 34)
Articles excluded (73)
Articles excluded (285)
Total studies included in review (n = 23)
Articles excluded (n = 11)
Figure 1. Flowchart study selection.
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 5
Table1.
Stud
ycharacteristics.
Authors,year
HSsample
characteristics:
Num
ber;gend
er;age;
residencedu
ringthe
war
JCCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
HSO
sample
characteristics:
Num
ber;gend
er;age;
residencedu
ringstud
y
JCOCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
Recruitm
ent
HSrespon
serate;H
SOrespon
serate
Offspringmentalh
ealth
complaintscomparedto
JCO(outcomesymptom
measure)
Stud
yfocus
Bader,Bierer,Lehrner,
Makotkine,D
askalakis,&
Yehu
da.,2014
ConveniencesampleN=
69Holocaust
survivor
offspring
N=26
Jewishno
n-HSO
Throug
hadvertisem
ents
andparticipationin
earlier
stud
y
NS24-hrurinarycortisol
Trendfordiffe
rencein
depression
,life-time
PTSD
diagno
sis,and
childho
odtrauma
Urin
arycortisol
Baider
etal.,2006
Group
1HSO
+form
erbreastcancer
N=193;
allw
omen;M
age=
48.7,SDage=5.0;
Israel
Group
3HSO
healthy:N
=176;
allw
omen;M
age=46.2,SDage=
5.8;
Israel
Group
2form
erbreastcancer
non-traumatized
parents:N=164;
allw
omen;M
age
=48.7,SDage=
6.8;
Israel
Group
4healthy
wom
enno
n-traumatized
parents:N=143;
allw
omen;M
age
=46.5,SDage=
8.1;
Israel
Form
erfirst-timebreast
cancer
patients(i.e.,n
oevidence
ofactive
diseaseat
thetim
eof
stud
y)recruitedfrom
listof
allp
atients
diagno
sedwith
stages
1and2breastscancer
inbetween1994
and
2000
intwoon
cology
centres.AllH
SOpatients(group
1)and
arand
omsampleof
non-HSO
(group
2)wereinvitedto
participate.
Rand
omsampleof
healthyHSO
(group
3)selected
from
thefiles
ofNationalH
olocaust
Archive
Rand
omsamplefrom
Israel
Interio
rMinistry
Census
files
(group
4).
Nocurrentor
previous
psychiatric
cond
ition
s.
Group
1:193/212=
91%
Group
2:164/174=
94%
Group
3:176/190=93%
Group
4:143/150=
95%
Psycho
logicald
istress
(intrusion,
avoidance
IES)
sign
high
erin
HOS
with
cancer
than
incomparison
swith
cancer.O
fcoping
variables,o
nly
helplessness
was
diffe
rent
betweenHSO
andcomparison
s(M
AC).
Lifetim
estressors,cancer
diagno
sis
Baider
etal.,2008
Mother-daug
hter
dyads:
Group
1HSmothersN
=20;M
age=73.6,
SDage=6.6;
Israel
Group
3HSmothers:N
=20;M
age=76.5,
SDage=7.6;
Israel
Mother-daug
hter
dyads:
Group
2Non
-traumatized
mothers:N
=20;
Mage=74.3,
SDage=10.1;
Israel
Group
4Non
-traumatized
mothers:N
=20;
Mage=72.5,
SDage=8.6;
Israel
Mother-daug
hter
dyads:
Group
1HSO
&form
erbreast
cancer
N=20;
Mage=46.9,SDage
=7.1;
Israel
Group
3HSO
healthy:
N=20;M
age=45.4,
SDage=7.3;
Israel
Mother-daug
hter
dyads:
Group
2form
erbreastcancer
patients:N=20;
Mage=46.3,SD
age=9.8;
Israel
Group
4healthy
wom
en:N
=20;
Mage=45.8,SD
age=6.8;
Israel
Rand
omselectionof
24dyadsou
tof
each
grou
pinclud
edin
Baider
etal.,2006
Group
1:20/24=83%
Group
2:19/24=79%
Group
3:22/24=92%
Group
4:20/24=83%
GlobalS
everity
Index
(BSI)diffe
rentiated
betweenHSO
with
cancer
andJCOwith
andHSO
with
out
cancer.
Lifetim
estressors,cancer
diagno
sis (C
ontin
ued)
6 P. DASHORST ET AL.
Table1.
(Con
tinued).
Authors,year
HSsample
characteristics:
Num
ber;gend
er;age;
residencedu
ringthe
war
JCCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
HSO
sample
characteristics:
Num
ber;gend
er;age;
residencedu
ringstud
y
JCOCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
Recruitm
ent
HSrespon
serate;H
SOrespon
serate
Offspringmentalh
ealth
complaintscomparedto
JCO(outcomesymptom
measure)
Stud
yfocus
Bierer,B
ader,D
asklalakis,
Lehrner,Makotkine,Seckl,
&Yehu
da,2
014
N=85
HSO
,40%
male;M
age=46.9,SDage=
7.6;
Israel
N=27
JCO,4
8.1%
male;M
age=
42.6,SDage=
10.5;Israel
Throug
hadvertisem
ents;
inpartam
ong
participants
ofearlier
stud
y.
HSO
morelifetime
anxietydisorder
(SCID,
d=0.40),andstage-
anxiety(STA
I;d=
0.44)).
Redu
cedcortisol
excretionin
HSO
comparedto
JCO;1
1ß-
HSD
-2activity
elevated
inHSO
comparedto
JCO,inparticular
amon
gmotherswho
hadbeen
children
durin
gWWII(24-h
urinesample).
Glucocorticoid
metabolism,1
1ß-HSD
-2activity
Gangi
etal.,2009
N=40
Italian-Jew
Holocaust
survivor
offspring,
33%
had
received
psycho
therapy.
50%
Female,M
age=
38,SDage=12.4,
Italy
Comparison
grou
pof
N=37
Italian
Jew
offspring
who
wereableto
hide
durin
gthe
war.
43.2%
Female,M
age=37,SDage
=13.7;Italy
RecruitedviaJewish
register
andafter
identificationof
those
who
hadchildren.
Respon
serate
100%
HSO
hadhigh
eranxiety
levels,low
self-esteem
,inhibitio
nof
aggression
,and
relatio
nala
mbivalence
than
JCO.
Intra-familialdynamics,e.
g.organizatio
n,expression
ofem
otions.
Halligan
&Yehu
da,2
002
N=87,3
6%men,6
4%wom
enraised
byparent(s)who
survived
theNazi
Holocaust
N=39,4
9%men,
51%
wom
enraised
byparent
(s)with
out
Holocaust
experienceand
free
from
current
andlifetimeaxisI
psychiatric
disorders.
Participants
were
solicitedfrom
lists
obtained
from
the
Jewishcommun
ityor
respon
dedto
anno
uncements
and
newspaper
advertisem
ents.In
additio
n(N
=28)were
enrolledthroug
ha
specialized
treatm
ent
prog
ramme.N=7
participants
new
since
Yehu
daet
al.,2001a.
Dissociativesymptom
s(DES)lower
inJCO
than
sub-grou
psof
HSO
,being
high
estin
HSO
with
current
PTSD
.
Mentalh
ealth
,PTSDin
parents
(Con
tinued)
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 7
Table1.
(Con
tinued).
Authors,year
HSsample
characteristics:
Num
ber;gend
er;age;
residencedu
ringthe
war
JCCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
HSO
sample
characteristics:
Num
ber;gend
er;age;
residencedu
ringstud
y
JCOCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
Recruitm
ent
HSrespon
serate;H
SOrespon
serate
Offspringmentalh
ealth
complaintscomparedto
JCO(outcomesymptom
measure)
Stud
yfocus
Kellerm
ann,
2008
HScharacteristics
provided
byHSO
:N=273mothers;b
orn
between1905–
1945;6
5%bo
rnin
EasternEurope,19%
born
inother
occupied
coun
tries,
14%
non-HS
N=273fathers;bo
rnbetween1895–
1946;7
0%bo
rnin
EasternEurope,19%
born
inother
occupied
coun
tries,
9%no
n-HS
N=273clinicaloffspring;
69%
female;48%
born
between1945–
1954,3
7%bo
rnbetween1955–1964,
15%
born
between
1965–1974;
Israel
-Co
nsecutiveadmission
s/referralsto
aHSO
specialized
clinic
Inform
ationno
tprovided
Nocomparison
grou
pIdentificationof
demog
raph
icfactors
Lehrner,Bierer,P
assarelli,
Pratchett,Flory,Bader,
Makotkine
&Yehu
da,2014
N=80,8
3%wom
en,
74%
men,M
age=
56.6,SD=8.5;
USA
N=15,6
0%wom
en,4
0%men,M
age=
58.7,SD=11.2;
USA
Throug
hprintandon
line
advertisem
ents
inJewishnewsou
tlets,
second
generatio
nand
otherJewishelectron
icmailinglists,
advertisem
ents
andby
word-of-m
outh
(2010–
2012).
HSO
morelikelythan
JCO
tohave
acurrent
anxietydisorder
diagno
sis(SCID;d
=0.45)andto
repo
rtsymptom
sof
depression
(BDI;d=
0.78)and
anxiety(STA
I;d=
0.79),as
wellasto
repo
rtmorechild
abuseandneglect(d=
0.70;C
TQ).HSO
had
high
er24-h
urinary
cortisol
levels(LST).
Glucocorticoidsensitivity
Letzter-Pouw
etal.,2014
Sampleon
en=
172a
;48.3%
wom
en;
Mage42.8,SDage=
7.3;
Israel
Sampletwo
n=161;
58.4%
wom
en;
Mage55.4,SDage=
5.3;
Israelisfrom
families
ofEuropean
origin.A
tleaston
eparent
who
was
under
Nazio
rpro-Nazi
occupatio
nor
dominationin
Europe
durin
gtheSecond
World
War.
Sampletwo
N=124parents
with
out
holocaust
backgrou
nd;
54.4%
wom
en;M
age54.4,SDage
=5.7;
Sampleon
enatio
nally
representativesample
recruitedby
contactin
geveryone
onalist(n
=272)
provided
byMinistryof
Interio
rof
person
sliving
throug
hout
Israel,b
orn
between1928
and
1945
inaEuropean
coun
trythat
suffe
red
Nazio
ccup
ationand
who
immigratedto
Israel
after1945.
Sampletwoconvenience
samplecommun
ity-
dwelling,
recruitedacross
the
coun
try.
Sampleon
eHSO
63%
Sampletwo
HSO
60%
Sampleon
ewas
not
compared
Sampletwo
HSO
repo
rted
high
erHolocaust
salience
(n2p
=.36);
transm
ission
ofbu
rden
(PPRBQ
)from
mother
(n2p
=.11)
andfather
(n2p
=.09).
Perceivedparental
burden.
(Con
tinued)
8 P. DASHORST ET AL.
Table1.
(Con
tinued).
Authors,year
HSsample
characteristics:
Num
ber;gend
er;age;
residencedu
ringthe
war
JCCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
HSO
sample
characteristics:
Num
ber;gend
er;age;
residencedu
ringstud
y
JCOCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
Recruitm
ent
HSrespon
serate;H
SOrespon
serate
Offspringmentalh
ealth
complaintscomparedto
JCO(outcomesymptom
measure)
Stud
yfocus
Letzter-Pouw
&Werner,2013
N=178
adyads;
(almostequally
dividedbetween
both
gend
ers;M
age69.8,SDage=
5.1);8
7%bo
rnin
EasternEurope,13%
born
inWestern
Europe
N=178
a ,first-born;
almostequally
dividedbetweenbo
thgend
ers;M
age=
43.8,SDage=7.3);
Israel
-Samplerecruitedby
contactin
geveryone
onarepresentativelist
(N=272)
provided
bynatio
nalM
inistryof
Interio
rof
person
slivingthroug
hout
Israel,b
ornbetween
1928
and1945
ina
European
coun
trythat
suffe
redNazi
occupatio
nandwho
immigratedto
Israel
after1945.
HS178/272=65%;
HSO
178/272=65%
Nocomparison
grou
pIntrusivemem
oriesin
Holocaust
child
survivorsandwell-
beingof
HSO
.
Sagi-Schwartz
etal.,2003
HSwho
immigratedas
orph
ansfrom
Europe
toIsrael
durin
gor
afterthe
war,H
SO(N
=48).
Born
inEurope
between1926
and
1937.
Comparison
grou
pof
subjects
insameagerang
e,also
born
inEurope
but
immigratedto
Israel
before
the
war.
N=50
Motheroffspring
HSO
,fem
ales,b
orn
between1947
and
1970.
JCO,fem
ales,b
orn
between1947
and1970.
Popu
latio
nregister
provided
byIsraeli
government.
Thereupo
n30.000
standardized
teleph
onecalls.
HSshow
edmore
traumaticstress
and
less
lack
ofresolutio
nof
traumathan
JC(d
=.77)
HSfewer
secure
attachment
representatio
nsthan
JC;H
SOno
tdiffe
rent
inattachment
classificationfrom
JCO.
Attachmentimpacted
byHolocaust
trauma
Shrira,2015
Study1N=63;M
age=
57.1,SD=6.26,61.9%
wom
enStud
y2N=300
respon
dentswith
atleaston
eHolocaust
survivor
parent.M
age
=57.8,SD=4.6,
59%
wom
en.
N1=
43,M
age=
54.7,SD=8.56,
55.8%
wom
enN2=
150,
Mage=
57.12,
SD=4.64,
56.8%
wom
en.
Stud
y1Co
nvenience
sampleof
commun
ity-
dwelling,
Hebrew
speaking
Jewish
Israelisfrom
families
ofEuropean
origin
living
inTelA
vivandits
surrou
ndings.D
ata
collectionin
June
2012.
Stud
y2hadsimilar
procedures
asin
Stud
y1.
Datacollection
2012–2013.
HSO
repo
rted
high
erIranian
nuclearthreat
salience(8-item
s)than
JCO.
HSO
also
repo
rted
more
anxietysymptom
s(Study
1,TM
AS-SF);
andpsycho
logical
distress
(Study
2,BSI-
18).
Coping
with
threat:
Iranian
nuclearthreat
salience
Shriraet
al.,2011
N=215bo
rnin
1945
orlater,inIsrael,Europ
e/USA
orin
theForm
erSoviet
Union
,with
afather
born
inEurope/
USA
(exceptfor20
respon
dentswho
werebo
rnin
Europe/
USA
buthadafather
from
ano
n-European
origin),
N=149;
neith
erparent
hadlived
underNazio
rpro-Nazi
occupatio
n/do
mination
Prob
ability
sampledraw
nfrom
theIsraeli
compo
nent
ofthe
Survey
ofHealth
,Ag
eing
andRetirem
ent
inEurope.Interview
edin
2005–2006.
Also,
drop
-offqu
estio
nnaire.
66.6%
oftotalsam
ple
completed
the
questio
nnaire
DifferencesbetweenHSO
andJCOin
numberof
major
health
prob
lems,
ofph
ysical
symptom
sandnu
mberof
medications.
HSO
also
repo
rted
high
erop
timism
andho
pe,
andbetter
life
satisfaction.
Functio
nof
numberof
survivor
parents.
(Con
tinued)
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 9
Table1.
(Con
tinued).
Authors,year
HSsample
characteristics:
Num
ber;gend
er;age;
residencedu
ringthe
war
JCCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
HSO
sample
characteristics:
Num
ber;gend
er;age;
residencedu
ringstud
y
JCOCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
Recruitm
ent
HSrespon
serate;H
SOrespon
serate
Offspringmentalh
ealth
complaintscomparedto
JCO(outcomesymptom
measure)
Stud
yfocus
Yehu
daet
al.,2008a
N=211;
117men,1
67wom
en(M
age=43.2;
SDage=9.1;
born
1938–1979)
with
atleaston
eparent
interned
inaNazi-
concentrationcamp
durin
gWW
IIor
had
facedcomparably
severe
threatsin
hiding
.
N=73
comparable
age,with
parents
who
wereno
texpo
sedto
the
Holocaustor
war-
events.
Commun
itysample
recruitedthroug
hadvertisem
ents.N
=145new
observations
sinceYehu
daet
al.,
2001a.
Ahigh
erprevalence
oflifetimePTSD
,mood,
anxietydisorders,and
toalesser
extent,
substanceabuse
disorders,was
observed
inHSO
than
inJCO(SCID,C
APS).
Maternalvspaternal
PTSD
andPTSD
occurrence
inHSO
.
Yehu
da&Bierer,2
008b
N=41
HSO
N=18
HSO
with
maternalP
TSD;M
age=
49.8,SDage
=6.5;
N=6men,N
=12
wom
enN=23
HSO
with
out
maternalP
TSD(M
age
=50.4,SDage=7.3N
=7men,N
=16
wom
en
N=19
JCO(M
age=
44.4,SDage
=9.5;
N=12
men,N
=7
wom
en
Traumaexpo
sure
(Mississippi
PTSD
Scale;
CTQ;P
PQ)Depression
symptom
s(BDI)
Urin
aryandsalivary
cortisol
levels
PTSD
risk
Yehu
da,B
lair,
Labinsky,
Bierer,2
007a
N=25
HSO
n=23
HSO
with
PTSD
n=10
HSO
with
out
PTSD
,USA
N=16
JCO,U
SARecruitm
entthroug
hadvertisem
ents.
Cortisol
levelswere
lowestin
HSO
with
parentalPTSD
(plasm
alevels),high
erin
HSO
with
outparental
PTSD
andhigh
estin
JCO.
Plasmacortisol
levels.
Yehu
daet
al.,2016
N=32,including
both
parentsfor5HSO
;37.5%
male,62.5%
female,M
age=
77.9,SD=5.2.
N=8,25.0%
male,
75.0%
female,M
age=73.1,SD=
8.5.
N=22,including
multip
lesiblings
inN
=2.
27.3%
male,
72.7%
female,M
age
=46.0,SD=8.0,
USA
N=9.
11.1%
male,
88.9%
female,M
age=47.0,SD=
8.5,
USA
Dataset
partof
alarger
sampleof
HSO
,of
which
themajority
was
recruited1993–1995
andlong
itudinally
followed-up10
years
after.
Holocaust
expo
sure
had
aneffect
onFKBP5
methylatio
nob
served
inexpo
sedparentsas
wellastheiroffspring.
Methylatio
nwas
lower
inHSO
comparedto
controls.
Cytosine
methylatio
nwith
inthegene
encoding
forFK506-
bind
ing-protein-5
(FKB
P5)
Yehu
da,D
askalakis,Lehrner,
Desarnaud
,Bader,
Makotikine,Flory,Bierer
&Meaney,2014
N=80
HSO
75%
hadbo
thparents
expo
sed
n=53
(55.8%
)maternal
PTSD
n=42
(44.2%
)paternal
PTSD
n=15
noparentalPTSD
,USA
N=15
JCOno
parentalPTSD
,USA
95/120
=79%
respon
serate
Alteratio
nsof
specific
methylatio
nwere
demon
stratedin
relatio
nto
parental
PTSD
and
neuroend
ocrin
eou
tcom
es.Interactio
neffect
ofpaternaland
maternalP
TSDwas
foun
d.
Influence
ofmaternal
andpaternalPTSD
onDNAmethylatio
nand
itsrelatio
nshipto
glucocorticoid
receptor
sensitivity
(Con
tinued)
10 P. DASHORST ET AL.
Table1.
(Con
tinued).
Authors,year
HSsample
characteristics:
Num
ber;gend
er;age;
residencedu
ringthe
war
JCCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
HSO
sample
characteristics:
Num
ber;gend
er;age;
residencedu
ringstud
y
JCOCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
Recruitm
ent
HSrespon
serate;H
SOrespon
serate
Offspringmentalh
ealth
complaintscomparedto
JCO(outcomesymptom
measure)
Stud
yfocus
Yehu
daet
al.,2001a
N=95
(33.3%
men,
66.7%
wom
en)having
been
born
toat
least
onebiolog
icalparent
who
experienced
the
NaziH
olocaust.
N=40
(57%
men,
43%
wom
en)
Jewish
individu
alsin
the
sameagerang
ewho
didno
thave
aparent
who
was
aHolocaust
survivor,n
otnecessarily
with
out
psychiatric
diagno
ses.
Recruitm
entfrom
lists
obtained
from
the
Jewishcommun
ityor
throug
hcommun
itygrou
panno
uncements
(N=109);orthroug
ha
specialized
treatm
ent
prog
ramme(N
=26).
N=42
(26HSO
;16JCO)
subjects
werenew
participants
compared
topriorpu
blications.
HSO
diffe
redfrom
JCOin
meannu
mberof
lifetimediagno
ses,in
particular
PTSD
,depressive
and(trend
:)anxietydisorders(SCID,
CAPS).
Develop
mentof
PTSD
,depressive
andanxiety
disordersin
HSO
asa
functio
nof
parental
expo
sure
andPTSD
.
Yehu
daet
al.,2002
N=39
(18%
men,8
2%wom
en)having
been
born
toat
leaston
ebiolog
icalparent
who
experienced
theNazi
Holocaust;U
SA.
N=15
(53.3%
men,
46.7%
wom
en)
Jewish
individu
alsin
the
sameagerang
ewho
didno
thave
aparent
who
was
aHolocaust
survivor,free
from
psychiatric
diagno
ses;USA
.
Described
inYehu
daet
al.,(2000)
HSO
andJCOdidno
tdiffe
rin
urinarycortisol
concentration.
Theoccurrence
of(lifetim
eandcurrent)
psychiatric
disorder
was
high
erin
HSO
than
inJCO.
Cortisol
levelsrelatedto
severityof
PTSD
symptom
sNum
berof
parents
affected
Yehu
daet
al.,2001b
N=51,2
0men,3
1wom
enhaving
been
born
toat
leaston
ebiolog
icalparent
who
experienced
theNazi
Holocaust.M
age=
40.9,SD=7.6;
USA
.
N=41,2
3men,1
8wom
en,w
iththe
sameagerang
e(24–60
years)
who
didno
thave
aparent
who
was
aHolocaust
survivor.M
age=
38.3,SD=8.8;
USA
.
Participants
were
solicitedfrom
lists
obtained
from
the
Jewishcommun
ity,
throug
hadvertisem
ents
(n=
79),andviashort-term
grou
ppsycho
therapy
(n=13).
HSO
repo
rted
more
emotionalabu
se,
neglect,ph
ysical
neglectand(trend
:)sexualabusethan
JCO
(CTQ
).
Theimpact
ofchildho
odtrauma;influencedby
parental
trauma
expo
sure
andparental
PTSD
.
(Con
tinued)
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 11
Table1.
(Con
tinued).
Authors,year
HSsample
characteristics:
Num
ber;gend
er;age;
residencedu
ringthe
war
JCCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
HSO
sample
characteristics:
Num
ber;gend
er;age;
residencedu
ringstud
y
JCOCo
mparison
sample
characteristics:
Num
ber,gend
er,age,
residence
Recruitm
ent
HSrespon
serate;H
SOrespon
serate
Offspringmentalh
ealth
complaintscomparedto
JCO(outcomesymptom
measure)
Stud
yfocus
Yehu
daet
al.,2007b
N=33
HSO
N=23
HSO
with
parental
PTSD
N=10
HSO
noparentalPTSD
N=16
JCO
Offspringwith
paternal
PTSD
onlywereno
tsign
ificantlydiffe
rent
inmeancortisol
level
than
offspringwith
noparentalPTSD
orcomparison
subjects
(JCO
).Meancortisol
levelsweresimilarfor
offspringwith
PTSD
inbo
thparentsandthose
with
maternalP
TSD
only,w
hereas
both
grou
psdiffe
redfrom
offspringwith
noparentalPTSD
(p=.02
andp=
.045,
respectively)
andfrom
comparison
subjects
(p=.009
andp=
.02,
respectively).
Cortisol
levelsrelatedto
parental
PTSD
VanIJzend
oorn
etal.,2013
Mother-daug
hter
dyads:
HSparents:N=32;
100%
female,M
age
=76.98,
SD=2.99,
Israel
JCparents:N=33;
100%
female;M
age=76.98,
SD=2.99.
Mother-daug
hter
dyads:
N=47
HSO
,Mage=
47.46,
SD=4.41,
daug
htersin
Israel
Mother-daug
hter
dyads:
N=32
JCOM
age=
47.46,
SD=4.41,
daug
htersin
Israel
Recruitm
entthroug
hregister
ofIsraeli
Ministry.
82.3%
firstgeneratio
n;82.3%
second
generatio
n
HSO
show
edlower
cortisol
levelson
lywhensurvivingparents
displayedmore
dissociatio
n(whereas
HSshow
edhigh
erlevelsof
daily
cortisol
versus
comparison
s).
Dissociationas
mod
eratingfactor
inthebiolog
ical
stress
regu
latio
nsystem
inHSO
.
a=Sampleoverlap,inthe2014
repo
rt,sixparticipantswereexclud
edas
noteligibleforthe
research
purposes;H
S=HolocaustSurvivors;HSO
=HolocaustSurvivor
offspring;JCO=Jewishcomparison
soffspring;Onlyou
tcom
esymptom
measuresrelevant
forthecurrentreview
wereinclud
ed:B
DI=
Beck
DepressionInventory(Becket
al.,1961);BSI=
BriefSymptom
Inventory(Derog
atis&Melisaratos,1983);C
TQ=Ch
ildho
odTrauma(Bernstein
etal.,1997);CA
PS=
ClinicianAd
ministeredPTSD
Scale(Blake
etal.,1990);DES
=DissociativeExperiences
Scale(Bernstein
&Putnam
,1986);IES
=Impactof
EventScale(Horow
itz,W
ilner,&
Alvarez,1979);MAC
=MentalA
djustm
entto
Cancer
(Watsonet
al.,1988);NHSPQ/PPRBQ
=New
Holocaust
Survivor
ParentingQuestionn
aire/Perceived
Parental
Rearingbehaviou
rQuestionn
aire
(Kellerm
ann,
2001);PPQ=Parental
PTSD
Scale(Yehud
aet
al.,2000;Y
ehud
aet
al.,2008a);S
CID=
Structured
ClinicalInterview
forDSM
-IV(Spitzer
etal.,1995);STAI
=SpielbergerStateTraitAn
xietyInventory(Spielberger,1
968);TMAS
-SF=Taylor
ManifestAn
xietyScale-ShortForm
(Bendig,
1956).
12 P. DASHORST ET AL.
The results of the reviewed studies are displayed inTables 2–6. Effect sizes are reported in the correspond-ing tables whenever the necessary data were provided.
3.2. Association between parental andoffspring’s mental health problems
The association between mental health problems ofthe Holocaust survivors and of their offspring bornafter the war has been the subject of five studies (seeTable 2). Letzter-Pouw and Werner (2013) first of allfound no direct association between survivor andoffspring symptoms of psychological and physicaldistress in a sample of 178 Holocaust survivors andtheir first-born offspring. However, they did find asignificant indirect relation, with survivor and off-spring distress mediated by the perceived mother’stransmission of trauma by the offspring. Also, inanother study, posttraumatic symptoms in offspringwere significantly predicted by perceived ‘transmis-sion’ of parental burden (medium effect size), deter-mined by items such as ‘My parent transmitted his orher burden of the Holocaust onto me’ (Letzter-Pouw,Shrira, Ben-Ezra, & Palgi, 2014).
Other studies did find a direct association betweenHolocaust survivors and HSO’s mental symptoms ordiagnoses, in particular Posttraumatic Stress Disorder(PTSD). In their study of 2001, first of all, Yehuda,Halligan, and Bierer (2001a) pointed to parentalPTSD as a significant predictor of the occurrence ofPTSD in HSO (large effect size). In a later studyYehuda, Bell, Bierer, and Schmeidler (2008a) foundan association between maternal (or both parentswith) PTSD and PTSD, mood disorder or any psy-chiatric disorders among offspring (large effect size)Next, Halligan and Yehuda (2002) investigatedwhether dissociative symptoms were related to theimpact of parental PTSD on the mental health con-dition of their offspring. Parental PTSD was reportedmore often by HSO with PTSD than without PTSD.Their findings demonstrated that dissociative symp-toms in HSO were significantly elevated in HSO withcurrent PTSD and parental PTSD (medium effectsize), whereas this elevation was absent in offspringwith past PTSD, only parental PTSD or only parentalHolocaust exposure (Halligan & Yehuda, 2002).
We expected a significant association between psy-chiatric symptoms in survivors and offspring. In linewith this, evidence was found for associationsbetween parental PTSD after Holocaust experiencesand current psychiatric symptoms (including PTSDand anxiety/mood symptoms) in offspring. The cor-relation between parental PTSD and depression orPTSD among HSO appeared to be different amongoffspring samples with paternal, maternal or bothparents with PTSD. A significant relation with largeeffect sizes has been found between maternal PTSD
and PTSD in offspring, while PTSD in both parentsmay be related to either PTSD or depressive symp-toms in the next generation (Yehuda et al., 2008a).
3.3. Perceived parenting and attachment
The perceived quality of the parent–child relation-ship, the (perceived) quality of parenting and thefamily climate, and/or attachment characteristicswere assessed in 10 studies (see Table 3). Letzter-Pouw and Werner (2013) reported in particular theimpact of mother’s ‘transmission’ of Holocaust: off-spring experienced their mothers as significantlymore affectionate (small effect size) and demonstrat-ing more over-involvement than fathers (large effectsize), and this style of mothering significantly pre-dicted posttraumatic symptoms at HSO (large effectsize) (Letzter-Pouw et al., 2014). As noted above, thisperceived ‘transmission’ of trauma by mothermediated the relation between survivor and offspringdistress (Letzter-Pouw & Werner, 2013). ParentalPTSD was significantly associated with higherreported occurrence of child maltreatment in HSO,more specifically emotional abuse and neglect, physi-cal neglect and sexual abuse (medium to large effectsizes) (Yehuda, Blair, Labinsky, & Bierer, 2007a;Yehuda, Halligan, & Grossman, 2001b). Mentalhealth symptoms were highly correlated (large effectsize) with emotional abuse, physical neglect and highCTQ scores (Yehuda et al., 2007a).
In order to examine the social climate in thefamilies, the Family Environment Scale (FES) wasused in two studies (Gangi, Talamo, & Ferracuti,2009; Lehrner et al., 2014). Results indicated thatoffspring of Holocaust survivors could be distin-guished significantly (medium effect sizes) fromJewish comparisons by a number of characteristics:They perceived their family as expressing emotionsmore poorly than offspring of comparison families.Next, HSO parents were likely to attribute greaterimportance to organizing and planning of familyactivities and responsibilities, and to put greateremphasis on following family rules. Family goalswere considered strongly oriented towards competi-tion and accepting challenges. Moreover, offspringreported to be less assertive and less able to maketheir own decisions. Holocaust offspring in this studydid not differ significantly from comparisons on theirreports of family cohesion, family conflict, achieve-ment orientation, intellectual-cultural orientation,active-recreational orientation, and moral-religiousemphasis (Gangi et al., 2009).
Lehrner et al. (2014) studied the moderatingeffects of parenting style and family functioning onthe relation between survivor PTSD and offspringmental health symptoms. They found that bothmaternal and paternal PTSD were significantly
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 13
Table2.
Mentalh
ealth
complaintsin
parentsandtheirchildren.
Author
Results
(assessm
entinstruments)pertaining
toparent
psycho
patholog
yandfunctio
ning
Results
(assessm
entinstruments)
pertaining
tooffspring
psycho
patholog
yandfunctio
ning
Results
(assessm
entinstruments)p
ertainingto
theassociationbetween
parent
andoffspringpsycho
patholog
yandfunctio
ning
Halligan
&Yehu
da,2
002
N=57
(66%
)on
eor
both
parentswith
PTSD
(PPQ
)Dissociativesymptom
s(DES)were
elevated
inindividu
alswith
current
PTSD
(CAP
S),b
utno
tin
thosewith
pastPTSD
orwith
theriskfactor
ofparentalPTSD
(PPQ
).
24HSO
with
PTSD
(27.5%
)hadon
eor
both
parentswith
PTSD
(PPQ
).Dissociativesymptom
s(DES)w
ereon
lyelevated
inHSO
with
current
PTSD
andparentalPTSD
butwereno
televated
inotherHSO
with
PTSD
orwith
parentalPTSD
orparentalHolocaustexpo
sure
with
out
PTSD
(PPQ
).Ofthen=27
(31%
)offspringwith
currentor
pastPTSD
,24(89%
)indicatedthat
theirparent(s)hadhadPTSD
.Ofthen=60
offspring
with
outcurrentor
pastPTSD
,n=33
(55%
)indicatedthat
their
parent(s)hadhadPTSD
(φ=.35).
Kellerm
ann,
2008
Perceivedmentalh
ealth
father:
Difficult17%
Middle40%
Good28%
Missing
value15%
Perceivedmentalh
ealth
mother:
Difficult24%
Middle37%
Good22%
Missing
value17%
Perceivedfunctio
ning
father:
Fully
66%
Partly20%
Impaired1%
Missing
value13%
Perceivedfunctio
ning
mother:
Fully
64%
Partly19%
Impaired3%
Missing
value14%
Not
stud
ied
Not
stud
ied
Letzter-Pouw
&Werner,2013
Symptom
sof
psycho
logicaland
physical
distress
M=1.71,
SD=0.52
(BSI).
84%
suffe
redfrom
intrusivemem
ories,M
=16.32,SD
=6.64
(IES)
Symptom
sof
psycho
logicaland
physicaldistress
M=1.51,SD=
0.48
(BSI).
HSpsycho
logicaland
physicaldistress
(BSI)indirectlypredicted
offspringdistress
(BSI).Therelatio
nwas
mediatedby
perceived
perceivedmother’s
“transmission
”of
trauma(NHSPQ/PPRBQ
).
Letzter-Pouw
etal.,2014
PTSD
symptom
sM
=1.73,SD=1.78
(CAP
S)Aftercontrolling
forage,gend
er,edu
catio
n,andlifeevents,p
erceived
“transmission
”of
burden
from
mother(NHSPQ/PPRB
Q)(β=.31)
[as
wellasnu
mberof
survivor
parents(β=.16])predictedHSO
posttraumaticsymptom
s(CAP
S).
Inaseparate
analysis,and
aftercontrolling
forage,gend
er,edu
catio
n,andlifeevents,p
erceived
“transmission
”of
burden
from
father
(NHSPQ/PPRB
Q)predictedHSO
posttraumaticsymptom
s(CAP
S)(β=
.23).
Lehrneret
al.,2014
Ofthe
N=80
parentswith
Holocaustexpo
sure
(11.6%
father,
9.5%
mother,63.2%
both
parents),3
2.6%
both
parents
hadPTSD
,23.2%
maternalPTSD,and
11.6%
paternalPTSD
(PPQ
).
5.4%
HSO
hadmajor
depressive
disorder,4
1.1%
anxietydisorder
(MINI)
Not
stud
ied
(Con
tinued)
14 P. DASHORST ET AL.
Table2.
(Con
tinued).
Author
Results
(assessm
entinstruments)pertaining
toparent
psycho
patholog
yandfunctio
ning
Results
(assessm
entinstruments)
pertaining
tooffspring
psycho
patholog
yandfunctio
ning
Results
(assessm
entinstruments)p
ertainingto
theassociationbetween
parent
andoffspringpsycho
patholog
yandfunctio
ning
Yehu
daet
al.,2001a
N=60
(64.5%
)HSwith
PTSD
(ParentalP
TSDscale)
N=33
(35,5%
)HSwith
outPTSD
56%
HSO
haddepressive
disorder
while
29%
HSO
hadPTSD
N=93
HSO
,ofwho
mN=60
(64.5%
)parentalPTSD
;N=33
(35.4%
)HSO
non-parental
PTSD
(PPQ
);N=42
JCO
Aftercontrolling
forgend
er,p
arentalP
TSDwas
associated
with
offspringPTSD
(φ=.52)
andwith
offspringdepression
(φ=.34).
Yehu
daet
al.,2001b
n=32
(62.7%
)HSO
hadon
eor
both
parentswith
PTSD
,n=
17(33%
)hadtwoparentswith
PTSD
;n=19
(37.3%
)HSO
with
outparentalPTSD
.
N=17;3
3.3%
PTSD
Not
stud
ied
Yehu
daet
al.,2007a
n=13
HSwith
PTSD
;N=12
HSwith
outPTSD
;N=16
JCN=4(66.7%
)HSO
met
criteria
for
lifetimePTSD
(non
eforcurrent
PTSD
)
Not
stud
ied
Yehu
daet
al.,2008a
N=211HS
N=49
(30.4%
)with
paternalPTSD
;N=40
(24.8%
)with
maternalP
TSD;N
=35
(21.7%
)bo
thparentswith
PTSD
;N=37
(23%
)no
parental
PTSD
(PPQ
).
69.5%
HSO
hadanylifetime
psychiatric
diagno
sis.More
specifically,p
revalencein
HSO
(N=
200):P
TSD19.0%;m
ooddisorder
45.5%;anxiety
disorder
(32.5%
);eatin
gdisorder
6.0%
;sub
stance
abuse10.5%,and
adjustment
disorder
10.0%
(SCIDDSM
IV;
CAPS).
Basedon
theprevalence
ratesrepo
rted
foroccurrence
ofPTSD
,mood
disorder
oranypsychiatric
disorder
inHSO
,havingamother(OR
2.40)or
both
parentswith
PTSD
(OR3.21)in
creasedthelikelihoodof
having
PTSD
comparedto
having
noparentalPTSD
.Higher
associationof
mooddisordersandparental
PTSD
versus
non-
parental
PTSD
(PaternalP
TSDOR=3.66,m
aternalP
TSDOR=3.06,
both
parentsPTSD
OR=3.21).
Yehu
daet
al.,2014
N=95
(75%
)HSO
both
parentsexpo
sed
n=31
both
parentsPTSD
n=53
(55.8%
)maternalP
TSD,n
=22
onlymaternalP
TSD;
n=42
(44.2%
)paternal
PTSD
n=11
onlypaternal
PTSD
;n=31
noparentalPTSD
Measuresof
social-emotional
functio
ning
inHSO
wereused
(BDI,
CTQ,STA
I,PEH,R
SQ,D
ES.P
PQ))
with
outrepo
rtingprevalence
ofpsychiatric
disordersin
thissample.
Not
stud
ied
Yehu
daet
al.,2016
N=16
(51.6%
)PTSD
N=4(13.8%
)An
xietydisorder
(other
than
PTSD
)N=9(31.0%
)Mooddisorder
(SCID,C
APS)
Aswas
retrospectivelyevaluatedby
HSO
(PPQ
):MaternalP
TSD;N
=11
(52.4%
)PaternalPTSD;N
=11
(52.4%
)An
yparent
with
PTSD
;N=16
(76.2%
)(PPQ
)
N=8(36.4%
)An
xietydisorder
(other
than
PTSD
)N=3(13.6%
)Mooddisorder
(SCID)
Not
stud
ied
HSO
=Holocaustsurvivor
offspring;JCO=offspringof
Jewishcomparison
s;BD
I=Beck
DepressionInventoryCA
PS=ClinicalAd
ministeredPTSD
Scale(Blake
etal.,1995);PD
S=PosttraumaticDiagn
ostic
scale(Foa
etal.,1997);;N
HSPQ
New
HolocaustSurvivor
Questionn
aire
(Kellerm
ann,2001);PEH=PerceivedEm
otionalH
ealth
(Flory,Bierer,&Yehu
da,2011);PPQ
=ParentalPTSD
Scale(Yehud
aet
al.,2000;Yehud
aet
al.,2008a);PPRBQ
=PerceivedParentalRearing
Behaviou
rQuestionn
aire
(Kellerm
ann,
2001);RSQ=Relatio
nScales
Questionn
aire
(Griffin
&Bartho
lomew
,1994);SCID=Structured
ClinicalInterview
forDSM
-IV(Spitzer
etal.,1995);STAI
=SpielbergerState-TraitAn
xietyInventory
(Spielberger,1
968).
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 15
Table 3. Perceived parenting, attachment and mental health complaints in HSO.
AuthorHSO results on attachment/perceived parenting
(instruments)Results pertaining to association between parent andoffspring attachment and offspring mental health
Gangi et al., 2009 HSO differed from JCO in terms of perceiving their family asexpressing emotions poorly (d= .56); not being assertiveand make their own decisions (d= .57); attribute greaterimportance on organizing and planning of familyactivities and responsibilities (d= .51) and put greateremphasis on following family rules (d= .43). Theydescribed their ideal family as being strongly orientedtowards competition and accepting challenges (d= .64)(FES).
HSO did not differ from JCO on scales of family cohesion,family conflict, achievement orientation, intellectual-cultural orientation, active-recreational orientation, andmoral-religious basis.
Not studied
Lehrner et al., 2014 Emotional abuse (CTQ) was positively associated with bothmaternal and paternal PTSD (r = .30; r = .32).
Of family environment factors (cohesion, expressiveness,conflict, organization, and control; FES) only conflict wascorrelated to glucocorticoid sensitivity (LST) in HSO.When family conflict was included as a covariateincluding maternal and paternal PTSD and Holocaustexposure, the main effect of maternal PTSD wasunchanged. Family conflict moreover, was correlatedwith paternal, but not maternal PTSD (r = .36).
Emotional abuse and family conflict moderated the effectsof parental PTSD on stress sensitivity in offspring.
Letzter-Pouw & Werner,2013
Perceived parenting: HSO reported more affection (d = .28),over-involvement (d = .54), and transmission (d = .31) ofthe Holocaust from mothers than fathers, no differencesbetween mothers and fathers on punishing (NHSPQ).
The relation between HS psychological and physicaldistress (BSI) and HSO distress (BSI) was mediated byperceived parenting, more specifically perceivedmother’s “transmission” of trauma (NHSPQ/PPRBQ).
Letzter-Pouw et al., 2014 Sample oneMothers were perceived to transmit more burden to theiroffspring than fathers (NHSPQ) (d = .33).
Sample twoHSO perceived more transmission of burden from mother(d= .70) and father (d = .64) versus comparisons (NHSPQ).
After controlling for age, gender, education, and lifeevents, perceived “transmission” of burden from mother(NHSPQ/ PPRBQ) (β= .31) (as well as number of survivorparents (β= .16) predicted HSO posttraumatic symptoms(CAPS).
In a separate analysis, and after controlling for age, gender,education, and life events, perceived “transmission” ofburden from father (NHSPQ/ PPRBQ) predicted HSOposttraumatic symptoms (CAPS) (β= .23).
Sagi-Schwartz et al., 2003 No differences in proportion HSO (54%) and JCO (42%) withinsecure attachment (AAI).
No differences in proportion HSO (17%) and JCO (8%) withunresolved loss (AAI)
No difference between HSO and JCO on mother-infantinteractions (disorganizing maternal behaviours; MIDBS).
No differences between HSO and JCO in satisfaction withrelationship with mothers (CS).
Interaction between attachment type (secure vs insecure) xgeneration (first, second) indicated less insecureattachment in the second generation, both for theHolocaust and comparison group.φ = .07
In 60% of the cases, survivors and offspring show the same(secure or insecure) attachment representation.
Insecure attachment in 77% of HS and HSO dyads vs. 54%in the comparison sample. Insecure attachmentrepresentation of mothers among HSO, higher but thesame as intergenerational attachment representation ingeneral (kappa = .21).
No evidence of intergenerational transmission ofunresolved attachment Interaction of unresolved lossand trauma between HS and HSO (φ= .53).
Yehuda et al., 2001b Adult Holocaust survivor offspring reported significant morechildhood trauma, particularly emotional abuse (d = 1.02),emotional neglect (d = .96) and physical neglect (d = .94),compared to non-Holocaust survivor offspring.
Parental PTSD was associated with a higher incidence ofemotional abuse (66% with parental PTSD vs. 37%without parental PTSD), and physical neglect (56% vs21%).
CTQ scores were associated with PTSD in HSO foremotional abuse r = .24; emotional neglect r = .34;physical neglect r = .36 and sexual abuse r = .27.
Yehuda & Bierer, 2008b HSO with maternal PTSD (n= 23) HSO without maternalPTSD (n= 18)
Based on the PBS HSO with maternal PTSD hadsignificantly lower scores on perceived maternal careand higher scores on maternal overprotection than HSOwithout maternal PTSD paternal values were notsignificant.
Yehuda et al., 2007a Parental PTSD symptoms were significantly correlated withchildhood emotional abuse (r = .33) and physical neglect(r = .38) (CTQ), and total CTQ score (r = .41).
HSO mental health symptoms (CMS) were correlated withchildhood emotional abuse (r = .55), physical neglect (r= .49) (CTQ) and total CTQ score (r = .52).
Yehuda et al., 2007b HSO with parental PTSD reported significantly morenegative consequences of being raised by Holocaustsurvivor parents than those without parental PTSD (d=1.28) (CTQ).
Not studied
Yehuda et al., 2016 No significant differences in childhood trauma (CTQ)between HSO and JCO.
Parental trauma, more than offspring’s own childhoodtrauma (CTQ), impacted on changes of epigeneticmarkers (methylation at different gene-sites) (β= −.36).
HSO = Holocaust survivor offspring; JCO = offspring of Jewish comparisons; AAI = Adult Attachment Inventory (Hesse, 1999); CAPS = ClinicianAdministered PTSD Scale (Blake et al., 1990); CS = Caregiving Scale, Scale especially designed for this study; CTQ = Childhood Trauma Questionnaire(Bernstein et al., 1997); FES = Family Environment Scale (Moos & Moos, 1994); LST = Lysozyme suppression test; NSPHQ = New Holocaust SurvivorParenting Questionnaire (Kellermann, 2001); PPRBQ = Perceived Parental Rearing Behaviour Questionnaire (Kellermann, 2001); CMS = CivilianMississippi Scale (Keane et al., 1988); MIDBS = Maternal Inappropriate and Disorganizing Behaviour Scale (Lyons-Ruth et al., 1999).
16 P. DASHORST ET AL.
related to emotional abuse in the family rearing style,and family conflict was significantly associated withpaternal, rather than maternal PTSD (all mediumeffect sizes). In HSO with maternal PTSD, perceivedmaternal care was significantly lower while maternaloverprotection was experienced as higher. No signifi-cant association with paternal PTSD was found(Yehuda & Bierer, 2008b).
The Adult Attachment Interview (AAI; Hesse,1999) was used to assesses the attachment stylebetween parents (caregivers) and children and adultmental representations of childhood attachmentexperiences, including loss and trauma experiences(Sagi-Schwartz et al., 2003). It was demonstratedthat a non-clinical sample of Holocaust survivormothers showed significantly more insecure attach-ment than a comparison group of non-survivormothers. More specifically, survivor mothers scoredhigh on unresolved attachment (i.e., either a disor-iented attachment style because of lack of resolutionof loss and trauma or a mixture of diverging insecure
attachment styles). In contrast, Holocaust offspringshowed no evidence of higher insecure attachmentclassification compared to the comparison group.
Finally, the data were consistent with the hypoth-esis that Holocaust survivor parents were not alwaysable to be responsive and attuned to the child becauseof their traumatic experiences and mental symptoms.Overall, the reviewed studies demonstrated withmedium to large effect sizes, a significant associationbetween (perceived) parental PTSD symptoms andchildhood trauma experiences of HSO. In particulara significant association with experiences of emo-tional abuse, neglect, and physical neglect (e.g.Yehuda et al., 2007a, 2001b), was found in parents,who were diagnosed with PTSD, emotional abuse andfamily conflict moderated the relationship betweenPTSD and offspring’s glucocorticoid sensitivity(Lehrner et al., 2014). Yehuda et al. (2016) reportedsignificantly higher prediction of epigenetic conse-quences from parental trauma than offspring’s ownchildhood trauma (medium effect size).
Table 4. Parental Holocaust history and mental health complaints in HSO.
AuthorResults (assessment instruments) pertaining to parental
Holocaust history and mental health outcomes in offspringResults (assessment instruments) pertaining to parental
gender and mental health outcomes in offspring
Letzter-Pouw & Werner,2013
57.3% had two HS parents.Having two HS parents was associated with more intrusivememories (IES) (r= .38).
Perceived parenthood: HSO reported more affection (d = .28),over-involvement (d= .54), and transmission (d= .31) of theHolocaust from mothers than fathers, no differencesbetween mothers and fathers on punishing (NHSPQ).
Mother’s transmission of trauma (NHSPQ) was related topsychological distress (BSI) and with offspring’spsychological coping resources
Mother’s transmission of the Holocaust (NHSPQ) related tointrusive memories (IES; r = .24). No association withperceived affection, punishment or over-involvement andno association with father’s perceived parenthood(NHSPQ).
Letzter-Pouw et al., 2014 Sample one57.0% had two HS parents.HSO who had two HS parents showed more posttraumaticsymptoms (CAPS) than those with one HS parent (d =.34).
Sample oneMothers were perceived to transmit more burden to theiroffspring than fathers (NHSPQ) (d = .33).
After controlling for age, gender, education and life events,perceived transmission from mother (β= .31) and father(NHSPQ) (β= .23) were positively related withposttraumatic symptoms (CAPS).
Sample twoHSO perceived more transmission of burden from mother(d = .70) and father (d = .64) versus comparisons(NHSPQ).
Shrira et al., 2011 10.2% (n = 37) had one HS parent; 49% (n = 178) had twoHS parents with a higher proportion of immigrants fromEurope and the USA (φ= .46). There were no differencesbetween both groups in health reports, life satisfaction oroptimism and hope.
Not studied.
Yehuda et al., 2001b No significant differences between offspring with one versustwo parents with PTSD on CTQ scales.
There was a similar relationship between childhood trauma(abuse and neglect; CTQ total scores) and maternal (r = .45)and paternal (r = .39) PTSD symptoms.
Yehuda et al., 2008a 70.5% (n= 200) had two HS parents; of these 49 fathers hadPTSD; 40 mothers had PTSD, while 35 HSO had twoparents with PTSD. The relationship of HS exposure andmental health in HSO was not studied.
Prevalence of PTSD among offspring impacted by maternal(φ= .27), not paternal PTSD (φ= .12) (PPQ, CAPS).
Depressive disorder in offspring was significantlyassociated with paternal PTSD (48.1% compared to17.6% in the comparison group) OR = .73, maternalPTSD (46.3%) OR 2.40; the effect cumulated when bothparents had PTSD (56.9%) OR 3.21.
Females with a father who had PTSD were more likely todevelop PTSD, while males with a father who had PTSDwere slightly less likely to develop PTSD φ = .21.
Note. HSO = Holocaust survivor offspring; JCO = offspring of Jewish comparisons; Correlation was only included when zero-order correlations wereprovided. SCID = Structured Clinical Interview for DSM IV (Spitzer et al., 1995); STAI = Spielberger State-Trait Anxiety Inventory (Spielberger, 1968);CTQ = Childhood Trauma Questionnaire (Bernstein et al., 1997); FES = Family Environment Scale (Horowitz, 1979); PPQ = Parental PTSD Questionnaire(Yehuda et al., 2000).
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 17
3.4. Parental Holocaust history
Five studies specifically addressed the association ofhaving either one or two Holocaust survivor parents,and/or survivor gender with the offspring’s mentalhealth problems (see Table 4). Having two parentswho were survivors of the Holocaust instead of oneparent was significantly associated with more intrusivememories and other posttraumatic symptoms in theoffspring group (Letzter-Pouw et al., 2014; Letzter-Pouw & Werner, 2013). Although being raised by atleast one Holocaust survivor parent was associated witha risk of less optimal or adequate parenting in the studyby Lehrner et al. (2014), no further data were providedon mental health outcomes related to which parent wasa survivor in this study. Research of Letzter-Pouw andWerner (2013, 2014) indicated that offspring’s mentalhealth problems as well as their experience of parentaltrauma transmission, with transmission defined by theauthors as the extent to which they received the innerpains of their parents, in turn causing them to feelresponsible for their parents, was significantly morepronounced in cases when their mother was aHolocaust survivor compared to when their father was(small to medium effect sizes). The offspring reportedmore affection, more overinvolvement, and more‘transmission of the Holocaust’ from their mothersthan from their fathers (Letzter-Pouw et al., 2014).
Yehuda et al. (2008a) compared offspring witheither a mother, a father or both parents with a life-time diagnosis of PTSD. Maternal PTSD was asso-ciated with a significantly higher prevalence oflifetime PTSD among offspring and the effect wasstronger in the co-presence of paternal PTSD
(medium effect size). Depressive disorder in offspringwas significantly associated with maternal and/orpaternal PTSD, while the effect was strongest whenboth parents had PTSD. In this study, Yehuda et al.(2008a) found a differential effect of parental PTSDon sons and daughters. Daughters of a father whohad PTSD were more likely to develop PTSD, whilesons with a father with PTSD were slightly less likelyto develop PTSD (small effect size) (Yehuda et al.,2008a).
Finally in a study by Shrira, Palgi, Ben-Ezra, andShmotkin (2011), no significant differences werefound between offspring with one or with both parentsbeing Holocaust survivors, they did not differ withrespect to self-reported health, life satisfaction andoptimism and hope (Shrira et al., 2011). The absenceof significant differences between HSO having eitherone or two parents with Holocaust exposure was alsoreported by Yehuda et al. (2001b). The studies agree,although with small to medium effect sizes, with ourhypothesis that parental gender is associated with theimpact of mental health problems in HSO. More spe-cifically, the presence of Holocaust survivor motherswas related to a higher prevalence of HSO distress,anxiety disorders, mood disorders, and substanceabuse than in JCO. Having two survivor parentsinstead of one increased the risk for (biological) vul-nerability, stress sensitivity, and mental health pro-blems in adulthood. This relationship was especiallypronounced in the presence of maternal PTSD.Lifetime PTSD and depression in HSO were higherin the presence of maternal PTSD and increased whenpaternal PTSD was also present. Daughters of a father
Table 5. Heightened vulnerability to the development of mental complaints after additional stress and traumatic life events in HSO.
AuthorAdditional stress/traumatic life
event HSOResults (and instruments) pertaining to association between additional HSO exposure to
stress/traumatic events, coping, and mental distress
Baider et al., 2006 Breast cancer Psychological distress levels (BSI), intrusions (d = −.68) and avoidance (d = .84) (IES),and helplessness/hopelessness coping (d = .29) (MAC) higher in HSO patients withbreast cancer compared to non-HSO cancer patients. No difference on other copingstyles (fighting spirit, anxious preoccupation, fatalistic acceptance (MAC).
Effects of being HSO on most subscales of the BSI larger compared to effect of diagnosisof cancer (e.g. effect of being HSO generation (d = .76) compared to diagnosis ofcancer (d = .49) on distress levels GSI scale BSI).
Interaction between having breast cancer and being HSO on depression andpsychoticism (BSI). The impact of cancer on the levels of depression and psychoticismin HSO was significantly stronger than the impact of cancer in the controls.
Baider et al., 2008 Breast cancer GSI score (BSI) highest in HSO with breast cancer compared to other three groups.Controlling for the significant effects of mothers’ distress and being a second-generation daughter, among others, the impact of cancer diagnosis on daughterlevel of distress was not significant (GSI index BSI).
Shrira et al., 2011 Various, cumulative life stressors Cumulative life event distress (TEI) did not have more of an effect on middle-aged HSOrelative to the comparison group. HSO seem to cope with stress as well as others.
Shrira, 2015 Iranian nuclear threat; and theperception of a hostile world
Iranian nuclear threat salience (constructed for this study) studied in two HSO samples(n1 = 106’ n2 = 450) and related to anxiety symptoms (TMAS-S): among HSO, Iraniannuclear threat salience showed a strong relationship to anxiety symptoms (r= .33).
Probing the interaction showed that, although among comparisons there was norelationship between Iranian nuclear threat salience and anxiety symptoms (β= 0.07),among HSO, Iranian nuclear threat salience showed a strong relationship to anxietysymptoms (β= 3.24)
This relation was not mediated by a perception of the world as hostile by HSO.aPartly same sample. HSO = Holocaust survivor offspring; IES = Impact of Event Scale (Horowitz et al., 1979); GSI = Global Inventory Index, based on BSI(Derogatis et al., 1982); MAC = Mental Adjustment to Cancer (Watson, 1988); HWS = Hostile World Scenario (Shrira et al., 2011); TEI = Traumatic EventsInventory (Shmotkin et al., 2009)); TMAS-S = Taylor Manifest Anxiety Scale – Short Form (Bendig, 1956).
18 P. DASHORST ET AL.
Table6.
Biolog
icalparameters:cortisol,epigenetic
factorsandgenetic
predispo
sitio
n.
Author
Sample
Results
onoffspringbiolog
ical
parameters
Results
pertaining
toassociationbetweenparent
andoffspringcortisol
metabolism
andepigenetics
Baderet
al.,2014
N=69
Nosign
ificant
diffe
rencein
24-h
urinarycortisol
levelsbetweenHSO
andJCO.
Sign
ificant
diffe
renceurinarycortisol
inoffspringof
mothers
who
wereadults
(low)
andwho
werechildren(high)
(r=−.35)
Nosign
ificant
diffe
rencein
each
combinatio
nbetweenHSO
with
mothersexpo
sedin
childho
odandin
adolescenceor
notexpo
sed.
Controlledforage,gend
er,and
currentdepressive
disorder,m
aternalage
atHolocaust
(β=−.56)
andmaternalP
TSD(β
=−.32)
(d=0.43)wereindepend
ent
predictorsof
lower
offspringurinarycortisol,w
hereas
offspringchildho
odadversity
andoffspringPTSD
symptom
swereno
t.Nointeractionof
effect
ofPTSD
andmaternalage
ofexpo
sure.
Norelatio
nof
mother’s
ageat
birthwith
cortisol
levelsin
HSO
.Sign
ificant
effect
ofmaternalP
TSD(β
=−.32)
onHSO
24-h
cortisol
levels(lower
levelswhenmotherhadPTSD
).Sign
ificant
maineffect
ofmaternalP
TSDon
HSO
urinarycortisol
d=.64.
Bierer
etal.,2014
N=85
femaleHSO
N=27
femaleJCO
24hcortisol
levelH
SOlower
than
JCOd=
0.45
and
5α-THFd=0.34
Totalg
lucocorticoidd=
0.43.
Sign
ificant
diffe
rencein
11β-HSD
-2-activity
betweenmaternalexposurein
childho
odandJCOp=.029.
HSO
show
edtrendsign
ificant
lower
levelsof
cortisol
(d=.45),5α-TH
F(d=.39)
(major
metabolite
ofcortisol)andtotalg
lucocorticoids
(d=.43)
comparedto
JCO.N
osign
diffe
rences
inthelevelsof
othermetabolites.
11β-HSD
-2activity
sign
ificantlyelevated
inHSO
whenmothersexpo
sedto
Holocaust
inchildho
od(β
=.25).
11β-HSD
-2activity
was
high
erbetweenHSO
motherswith
outPTSD
than
with
PTSD
andJCOthisremainedalso
sign
ificant
afterinclud
ingfather
with
PTSD
ascovariate.
Noeffect
ofgend
eron
11β-HSD
-2activity.
Maternalage
ofexpo
sure,ratherthanmaternalPTSD,predicted
offspring11β-HSD
-2activity
(β=.34).
Lehrneret
al.,2014
N=95
HSO
N=26
JCO
MaternalP
TSDon
lyHSO
cortisol
supp
ressionon
DST
69.75%
,bothparentsPTSD
82.49%
PaternalPTSD
high
er24-h
urinarycortisol
levelsin
HSO
than
whenmotherhadPTSD
d=−.84andwhenbo
thparentshadPTSD
MaternalP
TSDassociated
with
sign
ificantlyhigh
erglucocorticoidsensitivity
and
lower
24-h
urinarycortisol
excretionin
HSO
(β=–.41).Thiswas
thesamewhen
both
maternaland
paternalPTSD
was
present.Whenon
lythefather
hadPTSD
,an
oppo
site
effect
was
observed
lower
glucocorticoidsensitivity
andhigh
er24-h
urinarycortisol
excretion.
VanIJzend
oorn
etal.,
2013
N=29
survivor
parents
N=45
HSO
daug
hters
N=29
matched
JCno
n-survivor
parents
N=29
JCOdaug
hters
Allfem
aleandlivingin
Israel
Nosign
diffe
rencein
cortisol
levelsof
HSO
comparedto
non-HSO
Sign
ificantlylower
levelsof
daily
salivarycortisol
inHSO
with
survivor
parentswith
high
erscores
ondissociatio
n(DES)d=
.73
Yehu
daet
al.,2001b
N=51
HSO
N=41
JCO
N=20
HSO
+parental
PTSD
(24-hcortisol
secretionM
=42.06SD
=21.87)
N=8HSO
noparentalPTSD
(24-hcortisolsecretionM=67.90SD
=29.82)
(d=0.895).24-h
Urin
arycortisol
excretionsign
ificantlylower
inoffspringwith
parentalPTSD
comparedto
offspringwith
outparentalPTSD
(d=.92)
andJCO.Emotionalabu
seandparentalPTSD
appear
tobe
associated
with
low
cortisol
andriskforPTSD
.Yehu
daet
al.,2002
N=39
HSO
N=15
JCO
Offspringcortisol
levelssign
ificantlyassociated
with
sum
ofPTSD
symptom
sseverity
offather
andmothercombined(r=0.40).
24-h
Urin
arycortisollevelsinHSO
wereassociated
with
parentalPTSD
symptom
s(r=
−.40)
asmuchas
with
theirow
nPTSD
symptom
s(r=−.47).
Yehu
daet
al.,2007a
N=16
JCO
N=25
HSO
N=12
HSO
noparentalPTSD
N=13
HSO
+parentalPTSD
high
ercortisol
DEX
supp
ressionin
HSO
with
parentalPTSD
than
with
outparental
PTSD
d=0.93)o
rJCO(d
=0.91)b
utno
tsign
ificant
betweenHSO
with
outparental
PTSD
andJCO
anassociationpersistedbetweencortisol
supp
ressionandparentalPTSD
after
controlling
forchildho
odtraumaandHSO
ownPTSD
.r=−.35
Yehu
daet
al.,2007b
N=33
HSO
N=16
JCO
N=23
HSO
with
parental
PTSD
N=10
HSO
noparentalPTSD
Theestim
ated
mean±SE
plasmacortisollevelswere8.92
±.41μg/dL
forJCO;8.84±
0.52
μg/dL
foroffspringwith
outparentalPTSD
;and
with
one7.39
±0.44
μg/dL
ortwoparents6.97
±0.56
μg/dL
with
PTSD
.
Whenthewho
lesamplewas
considered,there
was
asign
ificant
associationbetween
meancortisollevelsandseverityof
parentalPTSD
(r42
=−0.41)thatwas
redu
ced
whenon
lyHolocaust
offspringwereconsidered
(r26
=−0.39)andwas
further
redu
cedto
non-sign
ificancewhenexam
ined
inthesm
alleroffspringsubg
roup
with
parentalPTSD
(r16
=−0.36).
Offspringwith
maternalr
=−.41or
paternalPTSD
r=−.32on
lyho
wever
after
additio
nally
controlling
forPTSD
intheotherparent
onlymaternalP
TSDretained
sign
ificant
associationwith
HSO
cortisol
level(paternal
r=−.21;
maternalr
=−.34).
(Con
tinued)
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 19
Table6.
(Con
tinued).
Author
Sample
Results
onoffspringbiolog
ical
parameters
Results
pertaining
toassociationbetweenparent
andoffspringcortisol
metabolism
andepigenetics
Yehu
da&Bierer,
2008b
N=41
HSO
N=19
JCO
N=6on
lypaternalPTSD
andN=16
noparentalPTSD
mean24-h
urinarycortisol
leveln
osign
ificant
diffe
rence.
N=9bo
thparentsPTSD
andN=8on
lymaternalP
TSDsimilarmean24-h
urinary
cortisol
anddiffe
redfrom
noparentalPTSD
andJCO.
HSO
andmaternalP
TSDlower
24hurinarycortisol
than
with
outmaternalP
TSD(r=
−.61);H
SOwith
outmaternalP
TSDtrendlower
levelthanJCO(r=−.17).
Sign
ificant
negativeassociationof
maternalo
verprotectionandPTSD
with
offspring
meancortisol
(r=−.54).
Yehu
daet
al.,2014
N=120
HSO
N=95
(75%
)HSO
both
parentsexpo
sed
n=31
both
parentsPTSD
n=53
(55.8%
)maternalP
TSD;n
=43
(44.2%
)paternalPTSD
n=
11on
lymaternalP
TSD;n
=11
onlypaternal
PTSD
;n=31
noparentalPTSD
Intheabsenceof
maternalP
TSD,o
ffspringwith
paternalPTSD
onlyshow
edhigh
erGR-1F
prom
otor
methylatio
n,whereas
offspringwith
both
maternaland
paternal
PTSD
show
edlower
GR-1F
prom
otor
methylatio
n(d=.75;
r=.35).
GR-1F
prom
otor
methylatio
nwas
negativelycorrelated
with
GR-1F
expression
(%methylatio
n:r=−.35;nu
mberof
methylatedsites:r=
−.36),ind
icatingthevalidity
oftheGR-1F
prom
otor
methylatio
nprocedures.
Presence
orabsenceof
maternalP
TSDmod
erated
paternal
PTSD
effect
onGR-1 F
prom
otor
methylatio
n.OnlypaternalPTSD
high
erGR-1 F
prom
otor
methylatio
n.Bo
thparentsPTSD
lower
GR-1 F
prom
otor
methylatio
n.HSbo
thparentsand
with
outPTSD
noeffectof
expo
sure
orinteractionbetweenmaternaland
paternal
expo
sure.
Yehu
daet
al.,2016
N=32
survivor
parentsN=22
HSO
N=8JC
parents
N=9JCO
HSbin/3site
6methylatio
ncorrelated
with
HSO
methylatio
nat
thesamesite
(r=.44).
ParentalHolocaust
expo
sure
sign
ificant
predictorof
HSO
bin/3site
6methylatio
nparentalPTSD
andFKBP5risk-allele,childho
odadversity
andem
otionalabu
sewere
notsign
ificant
associated.
FKBP5methylatio
nisseen
inHolocaustsurvivors(higherthan
comparison
)andtheir
offspring(lower
than
comparison
)on
thesamesite
inafunctio
nalintronicregion
ofFKBP5in
theop
posite
direction(β=−.37).
Nosign
ificant
associations
werefoun
dof
theFKBP5risk-allele
with
HSO
own
psycho
patholog
y,trauma-expo
sure
orotherexam
ined
characteristicsthat
might
independ
ently
affect
methylatio
nof
thisgene.
Epigeneticchangesweredemon
strated(bychangesin
methylatio
nlevels)in
two
generatio
ns(HSandHSO
)that
werecorrelated
(r=.44).A
fter
controlling
for
FKBP5riskallele
theassociationremained(r=.56),after
regression
bin3/site
6methylatio
nparental
Holocaust
expo
sure
remainedsign
ificant
(β=.42).
Bin/3site
6methylatio
nHolocaust
expo
sedcorrelated
with
HSO
methylatio
nat
the
samesite,the
presence
ofFKBP5risk-allele
inbo
thgeneratio
nsdidno
tsubstantially
altertheassociationof
bin3/site
6methylatio
nbetweensurvivor
andoffspring(r=.44)
orwith
inHolocaust-exposed
families
(r=.56).
HSO
=Holocaust
survivor
offspring;
JCO=offspringof
Jewishcomparison
s;11β-HSD
-2=11β-hydroxysteroid-dehydrog
enasetype
2;FKBP5=FK506-bind
ing-protein-5gene;P
BMCs
=perip
heralbloodmon
onuclear
cells;IC 5
0-DEX
=concentrationat
which
lysozymeactivity
isdiminishedby
50%;D
ST=dexamethasone
supp
ressiontest.
20 P. DASHORST ET AL.
who had PTSD were more likely to develop PTSD thansons of a father with PTSD.
3.5. Additional stress and traumatic life events inHSO
We found two studies with regard to the development ofmental health symptoms resulting from additional stressand traumatic experiences (see Table 5). First of all, astudy by Baider, Goldzweig, Ever-Hadani, and Peretz(2006, 2008) distinguished four groups: An HSO and anon-HSO group either with or without a diagnosis ofbreast cancer. The results indicated that coping withbreast cancer was significantly more strongly character-ized by helplessness and hopelessness in the HSO thanthe non-HSO group (medium effect size) (Baider et al.,2006; Baider, Goldzweig, Ever-Hadani, & Peretz, 2008).They also scored significantly higher on measures ofposttraumatic symptoms (i.e., intrusions and avoidance)as well as general psychological distress when faced witha diagnosis of breast cancer compared to non-HSO can-cer patients (large effect sizes). The association betweensymptoms and being HSO was even stronger comparedto the association between having symptoms and havinga diagnosis of cancer. In addition, the cumulative effect ofhaving Holocaust parents and a diagnosis of breast can-cer was significantly higher than the impact of each singlefactor on symptoms of depression and psychoticism butnot on other BSI subscales of distress or general level ofdistress. Thus, the psychological burden of cancer waslarger for these women than for women with non-trau-matized mothers, supporting the hypothesis of heigh-tened vulnerability in HSO (i.e., but only for depressionand psychoticism) (Baider et al., 2006, 2008).
Shrira (2015) and Shrira et al. (2011) demonstratedthat the mere threat of a disaster in itself is not related toheightened stress levels in Holocaust survivor offspring.They conducted a study among Israeli civilian HSO andJCO on the perception of threat of an Iranian nuclearattack. HSO reported no significantly higher scores ofanxiety than JCO and also revealed no more othermental health difficulties (medium effect size). Ourhypothesis of higher vulnerability to additional stressin HSO is partly supported by the results of this limitednumber of studies that indicate that having a seriousillness is accompanied with relatively high levels ofdistress in HSO, whereas the mere threat of a disasteris not differentially related to heightened distress inHSO (Shrira, 2015; Shrira et al., 2011).
3.6. Cortisol metabolism, epigenetic factors,genetic predisposition
Eleven studies reported about intergenerational effectson cortisol levels in offspring (see Table 6). Although nosignificant differences were found between 24-hr urin-ary cortisol levels between HSO and JCO, the results
indicated that parental, and specifically maternal, PTSD(i.e., status and level of symptoms) was associated withlower 24-hr urinary cortisol levels in offspring, evenafter accounting for offspring’s own traumatizationand PTSD (Bader et al., 2014; Bierer et al., 2014;Lehrner et al., 2014; Yehuda et al., 2008a; Yehuda &Bierer, 2008b; Yehuda, Bierer, Andrew, Schmeidler, &Seckl, 2009; Yehuda et al., 2007a, 2001a, 2002; Yehudaet al., 2001b, 2007b). The general level of the 24-hurinary cortisol level is lower in HSO of parents withPTSD than in HSO of parents without PTSD and lowerthan in JCO. Maternal PTSD had a significantly stron-ger association (medium effect sizes) with the loweringof this curve than paternal PTSD (Yehuda et al., 2007b).Most of these studies were conducted with maternalsurvivors so evidence for paternal impact is limited.The few studies that compared the impact of paternalandmaternal PTSD in HSO revealed significantly lower24-h urinary cortisol levels when either both parents oronly mothers with PTSD were concerned than whenonly fathers had PTSD (medium effect sizes) (Bader etal., 2014; Lehrner et al., 2014; Yehuda & Bierer, 2008b;Yehuda et al., 2007a, 2007b). Lehrner et al. (2014)observed significantly higher 24-hr urinary cortisollevels and lower glucocorticoid sensitivity in HSOwith only paternal PTSD (large effect size). VanIJzendoorn, Fridman, Bakermans-Kranenburg, andSagi-Schwartz (2013) described significantly lowerlevels of daily salivary cortisol in HSO in the presenceof higher parental dissociation scores (large effect size).These results were confirmed by studies using dexa-methasone concentrations (IC50-DEX value) to deter-mine glucocorticoid sensitivity (Lehrner et al., 2014;Yehuda et al., 2007b). Bader et al. (2014) reported asignificant association of 24-h cortisol levels in HSOwith the age of the mother during Holocaust exposure(large effect size). HSO with mothers who were adultduring Holocaust exposure had significantly lower 24-hr urinary cortisol levels then HSO with mothers whowere adolescents, children or JCO and this was inde-pendent of the presence of parental PTSD.
Heightened baseline cortisol levels in Holocaustsurvivors as a result of enduring stress might haveexposed HSO to heightened intrauterine cortisollevels. To protect the unborn child from exposure toheightened cortisol levels of mother, placental 11β –hydroxysteroid dehydrogenase type 2 (11β-HSD-2) isbeing produced which neutralizes almost 90% ofmaternal cortisol (Duthie & Reynolds, 2013). 11β-HSD-2 activity was significantly higher in HSO withmothers exposed to the Holocaust during childhoodcompared to JCO. Also, HSO without maternal PTSDshowed significantly higher 11β-HSD-2 activity com-pared to HSO with maternal PTSD and JCO (Biereret al., 2014). This remained significant when paternalPTSD was included. In this study, it appeared thatmaternal age at exposure, exposure during childhood,
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 21
rather than maternal PTSD, predicted offspring’s11β-HSD-2 activity (medium effect sizes).
Recent studies have focused on epigeneticmechanisms and PTSD. Alterations were found inrelation to parental PTSD on DNA methylation andits relationship to glucocorticoid receptor sensitivity(Yehuda et al., 2016). The study by Yehuda et al.(2016) demonstrated methylation changes (largeeffect sizes) at the FKBP-5 gene, in the oppositedirection, survivors had significantly higher andHSO significantly lower methylation. This was notsignificantly associated with the FKBP5-risk-alleleand could not be attributed to offspring’s own traumaexposure, offspring’s psychopathology, cortisol levelsor demographic characteristics that might indepen-dently affect methylation of this gene. Maternal orpaternal influences on in utero effect could not bedifferentiated because both parents were Holocaustsurvivors in this sample. According to the resultsdescribed above, it can be concluded that parentalHolocaust trauma may affect offspring’s cortisolmetabolism. Maternal symptoms as PTSD and disso-ciation give rise to decrease of cortisol levels, butmaternal atrocities during childhood give rise toincrease of cortisol levels, increased 11β-HSD-2 activ-ity in HSO and increased FKBP-5 gene methylation.The findings of these psychobiological markersshowed a significant contribution to intergenerationalconsequences on HSO. The epigenetic consequences(FKBP5 methylation) with large effect sizes seem tocontribute to a larger part than the other psychobio-logical markers with medium effect sizes.
4. Discussion
The aim of this review was to increase our understand-ing of the impact of being raised in a family withHolocaust survivor parents on the mental health oftheir offspring. We conducted a systematic literaturesearch and included 23 studies published betweenJanuary 2000 and February 2018. Because of the largeheterogeneity in the type of samples across the reviewedstudies (e.g. only offspring or both parents and off-spring, heterogeneity in comparison groups) and thelarge heterogeneity in the mechanisms of interest andassociated measurement instruments (i.e., varying fromattachment interviews to biological parameters), thissystematic review was restricted to a qualitativeapproach (Aromataris & Munn, 2017).
This systematic review focused on the followingfactors that may contribute to this multi-causality: (a)parental mental health problems; (b) (perceived) par-enting and attachment; (c) parental Holocaust his-tory; (d) the occurrence of life-time HSO stressors;and (e) cortisol metabolism, epigenetic factors, andgenetic predisposition. Overall, we found that inter-generational consequences may be best understood
by the impact of (and interaction between) multiplefactors, and not by one single factor determiningmental health outcomes in offspring.
a. Association between parental and offspring’smental health problems. The hypothesis ofincreased prevalence of psychiatric symptomsin offspring because of parental symptoms isconfirmed by the findings. Parental mentalhealth problems were clearly found to be asso-ciated with offspring’s mental health problems,in particular with regard to the occurrence ofHSO mood disorders, anxiety disorders, andsubstance abuse. Especially parental PTSD wasassociated with PTSD and depressive symptomsin HSO. This last result is in line with theconclusion of the review by Leen-Feldner etal. (2013) that parental PTSD is associatedwith offspring PTSD.
b. Perceived parenting and attachment. As weexpected, several factors related to (perceived)parental parenting and attachment were alsofound to be related to psychological functioningand mental health problems in offspring. HSOfamilies were characterized by relatively manyand/or intense conflicts within families and byless cohesion. Survivor mothers were perceivedas being more over involved than fathers and inthe presence of parental PTSD, there was anincreased risk of emotional and physical abuseor neglect.
c. Parental Holocaust history. The hypothesisthat growing up in a two-survivor family ver-sus a one-survivor family and the gender ofthe survivor will affect the incidence of men-tal health problems in offspring was con-firmed. The results of the studies indicatedthat overall Holocaust survivor mothersappeared to be more influential for the men-tal well-being of their offspring than fathers.In addition, having two survivor parentsresulted in higher mental health problemscompared to having one survivor parent.This pattern appeared evident even if parentsdid not show mental health problems. As weexpected, findings are consistent with theview that the parental Holocaust history isassociated with the development of symp-toms, and especially strong when maternalPTSD is present.
d. Additional stress and traumatic life events inHSO. Empirical support for the hypothesis ofheightened vulnerability to stress in HSO afterserious life events is consistent but limited. Theresults of one study among HSO with cancerindicated that having a serious illness (e.g. incase of cancer) was accompanied but with
22 P. DASHORST ET AL.
higher levels of distress. In contrast to what wasexpected, HSO and JCO showed the sameheightened vulnerability for stress in case ofmere threat (e.g. nuclear threat).
e. Cortisol metabolism, epigenetic factors, andgenetic predisposition. As a last factor of inter-generational consequences of trauma, wereviewed studies on cortisol metabolism, epige-netic factors, and genetic predisposition. Thestudies demonstrated intergenerational effectswith regard to cortisol levels (with lower urin-ary cortisol levels in offspring whose motherswere adults during the Holocaust compared tooffspring of younger mothers), increasedmethylation in specific gene-segments(FKBP5), and increased 11β–HSD-2 activitywith maternal PTSD. These findings are inline with studies focusing on epigenetic andphysiological consequences of other forms ofmass violence and stress such as the 9/11 ter-rorist attack (Yehuda & Bierer, 2008b). Overall,we found indications that special attentionshould be paid to maternal age at exposureand parental PTSD because each may affectdifferent components of the cortisol metabo-lism and bring about various changes in corti-sol metabolism.
4.1. An integrative perspective
To understand intergenerational consequences ofmassive trauma an integrative perspective is needed.This perspective needs to include psychological,family system, and biological and sociological char-acteristics. It should also be noted that intergenera-tional consequences do not necessarily lead topsychological symptoms (Denham, 2008; Kirmayer,Gone, & Moses, 2014). However, despite the caveatsin the studies included in this review, the findingsprovided considerable evidence in support of thehypothesis that HSO is indirectly affected by theHolocaust experiences of their survivor parents.There was also evidence that the psychobiologicalsystems changed in response to severe stress relatedto Holocaust experiences: Children with motherswho have experienced the Holocaust developed analtered cortisol metabolism due to epigeneticsincreased FKBP-5 methylation and increased 11β–HSD-2 activity. This may provoke altered reactionsto stress in HSO compared to offspring withunchanged cortisol metabolism. Depending on thetype of cortisol metabolism modification, this maygive rise to heightened vulnerability to stress, dis-tress and mental symptoms but it may also bringabout resilience and even increased resistance tostressful events (Bonanno & Mancini, 2012; Harel,Kahana, & Kahana, 1988).
Furthermore, in the presence of parental mentaldisorders, especially maternal PTSD, offspring is vul-nerable to developmental problems. And less attunedparenting, family conflicts, and emotional abuse havebeen found to be occurring relatively often inHolocaust survivor families. Only little evidence wasfound for HSO to be vulnerable to traumatic orstressful life events that really happened and not tomere threat.
4.2. Methodological issues
The strength of this study is that we have systematicallyanalysed all empirical studies that have been publishedon intergenerational consequences of the Holocaust inthe past two decades. Further, we evaluated character-istics, including parental mental health problems, per-ceived parenting, gender, additional life-time stress,cortisol and epigenetics, that were only partly addressedin previous reviews within this domain.
A limitation of the current findings is that only arestricted number of researchers have addressed inter-generational consequences. Thus, the studies includedin this review were designed and carried out by only asmall group of scientists. Further empirical studies andreplications among offspring of war survivors by alarger variety of research groups are of great impor-tance. Another limitation is that we narrowed our focusto a selection of possible influential intergenerationalfactors. This selection was based on both theoreticalhypotheses and factors that were proposed in earlierresearch (e.g. Felsen, 1998; Kellermann, 2001; Solomon,1998; Van IJzendoorn et al., 2003). Nevertheless, theremay be other relevant factors that have not been cov-ered by the current study. For example, the birth orderand the presence or absence of siblings may have animpact on the development of the HSO mental health(Kellermann, 2008; Letzter-Pouw & Werner, 2013).Examples of other factors that we did not considerand that might be of influence are: themigration historyand the circumstances in the host countries; the currentliving conditions of feeling safe and welcome or livingin a condition of continuing threat as in Israel or theinfluence of living among a high percentage ofHolocaust survivors (Kirmayer et al., 2014).
The recruitment methods that were used in thereviewed studies varied from convenience samples (e.g. gathered through advertisement, survivor associa-tions or networks, meetings or conferences, mentalhealth clinics) and snowball methods to a morerepresentative selection of participants (e.g. randomselection from national case register such as theMinistry of Interior; Sagi-Schwartz et al., 2003).Both convenience sampling and representative sam-pling methods have advantages and disadvantages. Inour review, we focused on the clinical group of HSO,which is obviously not representative of the total
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 23
population of HSO. The choice was made because thesample of clinical HSO was expected to show suffi-cient variation in mental health problems allowing toinvestigate a possible association between symptomsand parental as well as offspring characteristics. Thus,studying this group could contribute to a betterunderstanding of underlying mechanisms for pre-sumed transmission of parental-experienced massivetrauma. Furthermore, samples by recruitment withthe use of a national case register suffer from lowresponse rates (e.g. 60% in a study by Letzter-Pouw etal., 2014) and therefore reduce representativity.Participants may refuse to participate because, forexample, they do not want to be reminded of thewar, they feel that the Holocaust did not play asignificant role in their lives, or they are afraid tobecome too emotional. Consequently, selective non-response may have introduced bias in the resultsgathered and reported (Letzter-Pouw et al., 2014;Letzter-Pouw & Werner, 2013).
Additionally, the Jewish comparison samples in thereviewed studies were from the same catchment area butwith parents who were non-Holocaust survivors. Thesesamples varied widely, depending on the method ofrecruitment and in- and exclusion criteria possibly intro-ducing selection bias. The comparison samples includedfurther differed in health status (e.g. from completelysymptom-free to general population samples withselected exclusion criteria like florid psychotic disorders).Moreover, despite careful screening procedures, compar-ison survivor and offspring groups were not alwayscomparable on important demographic variables likeeducation level (e.g. non-Holocaust survivors receivedmore education during the holocaust years), religion, orbackground of partner (Holocaust survivor or not).
Most studies reviewed were one-generation studies(i.e., with an absence of direct assessments in the first-generation survivors) and mental health functioningand other survivor characteristics (e.g. perceived par-enthood) were estimated by the HSO, introducingretrospective bias. Symptoms of PTSD may changeover time and the current symptoms or the symptomsduring the last period of the parents’ lives may bemore explicit in memory and therefore no properrepresentation of the symptoms during the earlier orentire upbringing period. Moreover, in the few two-generations studies the associations between survivorand offspring functioning were not always computed.
Finally, it is important to mention that all studiesthat met our inclusion criteria pertained only toHolocaust survivors. Offspring of parents who sur-vived World War Two by hiding or in the resistance,as well as parents who survived the Japanese occupa-tion and internment camps in Asia were not repre-sented. This reduces the external validity, that is, thegeneralizability of the findings of the current reviewto other survivors of World War Two and survivors
of other atrocities or war as well as other groups withsevere parental trauma. We also have to keep in mindthat Holocaust survivors might have lived in morehospitable or stable countries than the circumstancesof refugees now living in temporary housing in refu-gee camps or unhospitable and unstable hostcountries.
4.3. Clinical implications and implications forfuture research
First of all, this research has implications with regardto diagnostic assessment. The findings of this reviewindicate that intergenerational effects may not bedirectly observed in the occurrence of particular dis-orders in offspring, but appear to be reflected by adiversity of mental health problems that are influ-enced by both parental and offspring characteristics.Diagnostic procedures should thus take this into con-sideration and incorporate instruments capturing thisvariety of symptoms and contributing factors. Inaddition, to minimize intergenerational consequencesfor children with severely traumatized parents (e.g.refugees), treatment should be provided to both sur-vivor and offspring for their mental health problems.Also, the findings emphasize the importance of pro-viding support for traumatized parents in raisingtheir children (see also Ee, Sleijpen, Kleber, &Jongmans, 2013).
For future research, it is important to examine ifspecific characteristics of Holocaust survivors are alsoevident in survivors of genocide or survivors of warin general (Kirmayer et al., 2014). More insight intothe presence of intergenerational consequences ofwar does not have to be limited to HSO but canalso be developed in prospective research amongsurvivors of current wars such as in Syria or inrefugee camps. Studies entailing a longitudinal designincorporating both psychosocial and psychobiologicalparameters will be of great value to closely examineinterference of parental characteristics with the devel-opment of offspring. Because most studies reviewedby us relied on cross-sectional designs, longitudinalresearch is of great importance because the conse-quences of parental trauma may only become visibleafter a long time. Our review also made clear that it isrelevant not to limit future studies to offspring thatexperienced warfare or was born during the war butalso focus on children born after the war, as (inter-generational) consequences sometimes may onlybecome evident many years after traumatic warevents. This will contribute to increasing insight onchild, parental and parenting factors as well as ontheir mutual influence. The focus on malleable factorscan be used as a starting point for (preventive)interventions.
24 P. DASHORST ET AL.
5. Conclusion
To conclude, the available evidence suggests that bothparent and child characteristics and their interactioncontribute to the vulnerability and to the develop-ment of symptoms in the HSO group. Holocaustsurvivor mothers have been observed to be moreinfluential for the mental well-being of their offspringthan fathers, and having two survivor parentsresulted in even higher mental health problems.This is confirmed by studies of intergenerationaleffects with regard to parental PTSD and maternalage during the Holocaust. Those studies showedstrong evidence for the effect on cortisol metabolismmodification and epigenetics in HSO with survivormothers. Also, intergenerational effects have beenfound with regard to cortisol levels. There is someempirical support for a heightened vulnerability forstress in HSO. These results indicate that diagnosticprocedures and treatment, but also future theorizingand empirical studies should be multifactorial in try-ing to delineate the causal factors involved in mentalhealth functioning in intergenerational consequencesof war. In this context, it is important to note that,although the current review has predominantlyfocused on HSO suffering from mental health pro-blems, it is relevant to examine those parents andchildren who managed to cope, adjust and/or builda healthy life, as this might help unveil factors con-tributing to resilience. Attention should be paid tothese specific psychological and biological factorssafeguarding offspring against distress.
Acknowledgments
We would like to thank the staff of the Arq PsychotraumaExpert Group library for their assistance in the databasesearch for this review.
Disclosure statement
No potential conflict of interest was reported by theauthors.
References
American Psychiatric Association (APA). (2000). Diagnosticand statistical manual of mental disorders 4th ed. text revi-sion: DSM-IV-TR. Washington, DC: APA.
Aromataris, E., & Munn, Z. (2017). Chapter 1: JBI systema-tic reviews. In Joanna Briggs Institute reviewer’s manual,299.
Bader, H. N., Bierer, L. M., Lehrner, A., Makotkine, I.,Daskalakis, N. P., & Yehuda, R. (2014). Maternal age atHolocaust exposure and maternal PTSD independentlyinfluence urinary cortisol levels in adult offspring.Frontiers in Endocrinology, 5, 103.
Baider, L., Goldzweig, G., Ever-Hadani, P., & Peretz, T.(2006). Psychological distress and coping in breast
cancer patients and healthy women whose parents sur-vived the Holocaust. Psycho-Oncology, 15(7), 635–646.
Baider, L., Goldzweig, G., Ever-Hadani, P., & Peretz, T.(2008). Breast cancer and psychological distress:mothers’ and daughters’ traumatic experiences.Supportive Care in Cancer, 16(4), 407–414.
Baider, L., Peretz, T., Hadani, P. E., Perry, S., Avramov, R.,& De-Nour, A. K. (2000). Transmission of response totrauma? Second-generation Holocaust survivors’ reac-tion to cancer. American Journal of Psychiatry, 157(6),904–910.
Beck, A. T., Ward, C., Mendelson, M., Mock, J., & Erbaugh,J. (1961). Bewck depression inventory (bdi). Archives ofGeneral Psychiatry, 4(6), 561-571.
Bendig, A. W. (1956). The development of a short form ofthe manifest anxiety scale. Journal of ConsultingPsychology, 20(5), 384. doi:10.1037/h0045580
Bernstein, D. P., Ahluvalia, T., Pogge, D., & Handelsman,L. (1997). Validity of the childhood trauma question-naire in an adolescent psychiatric population. Journal ofThe American Academy of Child & AdolescentPsychiatry, 36(3), 340–348.
Bernstein, E. M, & Putnam, F. W. (1986). Development,reliability, and validity of a dissociation scale. Journal ofNervous and Mental Disease.
Betancourt, T. S. (2015). The intergenerational effect ofwar. JAMA Psychiatry, 72(3), 199–200.
Bierer, L. M., Bader, H. N., Daskalakis, N. P., Lehrner, A.L., Makotkine, I., Seckl, J. R., & Yehuda, R. (2014).Elevation of 11β-hydroxysteroid dehydrogenase type 2activity in Holocaust survivor offspring: Evidence for anintergenerational effect of maternal trauma exposure.Psychoneuroendocrinology, 48, 1–10.
Blake, D. D., Weathers, F. W., Nagy, L. M., Kaloupek, D.G., Gusman, F. D., Chamey, D. S., & Keane, T. M.(1995). The development of a clinician-administerdPTSD scale. Journal of Traumatic Stress, 8(1), 75-90.
Bloch, A. (2018). Talking about the past, locating it in thepresent: The second generation from refugee back-grounds making sense of their parents’ narratives, nar-rative gaps and silences. Journal of Refugee Studies, 31(4),647–663.
Bonanno, G. A., & Mancini, A. D. (2012). Beyond resili-ence and PTSD: Mapping the heterogeneity of responsesto potential trauma. Psychological Trauma: Theory,Research, Practice, and Policy, 4(1), 74–78.
Bowlby, J. (1982). Attachment and loss: Retrospect andprospect. American Journal of Orthopsychiatry, 52,664–678.
Chaitin, J. (2002). Issues and interpersonal values amongthree generations in families of Holocaust survivors.Journal of Social and Personal Relationships, 19(3),379–402.
Critical Appraisal Skills Program. (2018). CASP checklist.[online] Retrieved from http://www.casp-uk.net/checklists
Danieli, Y. (Ed.). (1998). International handbook of multige-nerational legacies of trauma. New York, NY: Plenum Press.
Deeks, J. J., Dinnes, J., D’Amico, R., Sowden, A. J.,Sakarovitch, C., Song, F., … Altman, D. G. (2003).Evaluating non-randomised intervention studies.Health Technology Assessment (Winchester, England), 7(27), iii–x. Retrieved from http://researchonline.lshtm.ac.uk/id/eprint/8742
Denham, A. R. (2008). Rethinking historical trauma:Narratives of resilience. Transcultural Psychiatry, 45(3),391–414.
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 25
Derogatis, L. R., & Meilisaratos, N. (1983). The brief symp-tom inventory: an introductory report. PsychologicalMedicine, 13(3), 595–605.
Downs, S. H., & Black, N. (1998). The feasibility of creatinga checklist for the assessment of the methodologicalquality both of randomised and non-randomised studiesof health care interventions. Journal of Epidemiology &Community Health, 52(6), 377–384.
Duthie, L., & Reynolds, R. M. (2013). Changes in thematernal hypothalamic-pituitary-adrenal axis in preg-nancy and postpartum: Influences on maternal andfetal outcomes. Neuro-endocrinology, 98, 106–115.
Ee, E. V., Sleijpen, M., Kleber, R. J., & Jongmans, M. J.(2013). Father-involvement in a refugee sample:Relations between post-traumatic stress and care-giving.Family Process, 52, 723–735.
Felsen, I. (1998). transgenerational transmission of effectsot the Holocaust. In Y. Danieli (Ed.), International hand-book of multigenerational legacies of trauma (pp. 43–68).New York, NY: Plenum Press.
Flory, J. D., Bierer, L. M., & Yehuda, R. (2011). Maternalexposure to the holocaust and health complaints in off-spring. Disease Markers, 30(2–3), 133–139.
Foa, E. B, Cashman, L, Jaycox, L, & Perry, K. (1997). Thevalidation of a self-report measure of posttraumaticstress disorder: the posttraumatic diagnostic scale.Psychological Assesment, 9(4), 445.
Fonagy, P. (1999). The transgenerational transmission ofholocaust trauma. Attachment & Human Development, 1(1), 92–114.
Gangi, S., Talamo, A., & Ferracuti, S. (2009). The long-termeffects of extreme war-related trauma on the secondgeneration of Holocaust survivors. Violence andVictims, 24(5), 687–700.
Glover, V. (2015). Prenatal stress and its effects on the fetusand the child: Possible underlying biological mechan-isms. In Perinatal programming of neurodevelopment(pp. 269–283). New York, NY: Springer.
Griffin, D. W., & Bartholomew, K. (1994). Models of theself and other: Fundamental dimensions underlyingmeasures of adult attachment. Journal of Peronality andSocial Psychology, 67, 340.
Halligan, S. L., & Yehuda, R. (2002). Assessing dissociationas a risk factor for posttraumatic stress disorder: A studyof adult offspring of holocaust survivors. The Journal ofNervous and Mental Disease, 190(7), 429–436.
Harel, Z., Kahana, B., & Kahana, E. (1988). Psychologicalwell-being among Holocaust survivors and immigrantsin Israel. Journal of Traumatic Stress Studies, 1, 413–428.
Havinga, P. J., Boschloo, L., Bloemen, A. J. P., Nauta, M.H., de Vries, S. O., Penninx, B. W. J. H., & Hartman, C.A. (2017). Doomed for disorder? High incidence ofmood and anxiety disorders in offspring of depressedand anxious patients: a prospective cohort study. TheJournal of Clinical Psychiatry, 78, 8–17.
Heim, C., & Binder, E. B. (2012). Current research trends inearly life stress and depression: Review of human studieson sensitive periods, gene–environment interactions, andepigenetics. Experimental Neurology, 233(1), 102–111.
Hesse, E. (Ed.). (1999). The adult attachment interview:Historical and current perspectives. New York, NY:Guilford.
Horowitz, M., Wilner, N., & Alvarez, W. (1979). Impact ofevent scale: A measure of subjective stress.Psychosomatic Medicine, 41(3), 209–218.
Katz, S. J., Hammen, C. L., & Brennan, P. A. (2013).Maternal depression and the intergenerational
transmission of relational impairment. Journal ofFamily Psychology, 27, 86–95.
Keane, T. M., Caddell, J. M., & Taylor, K. L. (1988).Mississippi scale for combat-related posttraumatic stressdisorder: Three studies in rehability an validity. Journalof Consulting and Clinical Psychology, 56, 85–90.
Kellermann, N. P. (2001). Transmission of Holocausttrauma–an integrative view. Psychiatry, 64(3), 256–267.
Kellermann, N. P. (2008). Transmitted Holocaust trauma:curse or legacy? The aggravating and mitigating factorsof Holocaust transmission. Israel Journal of Psychiatry &Related Sciences, 45(4), 263–270.
Kirmayer, L. J., Gone, J. P., & Moses, J. (2014). Rethinkinghistorical trauma. Transcultural Psychiatry, 51(3), 299–319.
Klaassens, E. R. (2010). Bouncing back. GVO drukkers &vormgevers B. V. Ponsen & Looijen.
Krell, R., Suedfeld, P., & Soriano, E. (2004, October). ChildHolocaust survivors as parents: A transgenerational perspec-tive. American Journal of Orthopsychiatry, 74, 502–508.
Kretchmar, M. D., & Jacobovitz, D. B. (2002). Observingmother-child relationships across generations: Boundarypatterns, attachment, and the transmission of caregiving.Family Process, 41(3), 351–374.
Leen-Feldner, E. W., Feldner, M. T., Knapp, A., Bunaciu,L., Bumenthal, H., & Armstadter, A. B. (2013). Offspringpsychological and biological correlates of parental post-traumatic stress: Review of the literature and researchagenda. Clinical Psychology Review, 33(8), 1006–1133.
Lehrner, A., Bierer, L. M., Passarelli, V., Pratchett, L. C., Flory,J. D., Bader, H. N., … Yehuda, R. (2014). Maternal PTSDassociates with greater glucocorticoid sensitivity in off-spring of Holocaust survivors. Psychoneuroendocrinology,40, 213–220.
Letzter-Pouw, S. E., Shrira, A., Ben-Ezra, M., & Palgi, Y.(2014). Trauma transmission through perceived parentalburden among Holocaust survivors’ offspring andgrandchildren. Psychological Trauma: Theory, Research,Practice, and Policy, 6(4), 420–429.
Letzter-Pouw, S. E., & Werner, P. (2013). The relationshipbetween females Holocaust child survivors’ unresolvedlosses and their offspring’s emotional well-being. Journalof Loss and Trauma, 18(5), 396–408.
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P.C., Ioannidis, J. P. A., … Moher, D. (2009). The PRISMAStatement for reporting systematic reviews and meta-ana-lyses of studies that evaluate health care interventions:Explanation and elaboration.PLoSMedicine, 6(7), e1000100.
Lombardo, K. L., & Motta, R. W. (2008). Secondary traumain children of parents with mental illness. Traumatology,8;(15), 57–67.
Lyons-Ruth, K., Bronfman, E., & Atwood, G J. A relationaldiathesis model of hostile-helpless states of mind:Expression in mother-infant interaction. In J. Solomon& C. George (Eds.), Attachment disorganization (pp. 33–70). New York, NY: Guilford.
McGuire, S., Palaniappan, M., & Larribas, T. (2015). Thesibling relationship as a source of shared environment.In B. Horwitz & J. Neiderhiser (Eds.), Gene-environmentinterplay in interpersonal relationships across the lifespan.advances in behavior genetics (Vol. 3). New York, NY:Springer. doi:10.1007/978-1-4939-2923-8_4
Moola, S., Munn, Z., Tufanaru, C., Aromataris, E., Sears,K., Sfetcu, R., … Mu, P. F. (2017). Chapter 7: Systematicreviews of etiology and risk. In E. Aromataris & Z.Munn (Eds.), Joanna Briggs Institute reviewer’s manual.The Joanna Briggs . Retrieved from https://reviewersmanual.joannabriggs.org/
26 P. DASHORST ET AL.
Moos, R. H., & Moos, B. S. (1994). Family environmentscale manual. Consulting Psychologists Press.
Munroe, J. F., Shay, J., Fisher, L., Makary, C., Rapperport,K., & Zimering, R. (1995). Preventing compassion fati-gue: A team treatment model. In C. R. Figley (Ed.),Compassion fatigue: Coping with secondary traumaticstress disorder in those who treat the traumatized (pp.209–231). Routledge
Naumova, O. Y., Hein, S., Suderman, M., Barbot, B., Lee,M., Raefski, A., … Grigorenko, E. L. (2016). Epigeneticpatterns modulate the connection between developmen-tal dynamics of parenting and offspring psychosocialadjustment. Child Development, 87, 98–110.
Rasic, D., Hajek, T., Alda, M., & Uher, R. (2014). Risk ofmental illness in offspring of parents with schizophrenia,bipolar disorder, and major depressive disorder: A meta-analysis of family high-risk studies. SchizophreniaBulletin, 40, 28–38.
Reynolds, R. M., Pesonen, A.-K., O’Reilly, J. R., Tuovinen,S., Lahti, M., Kajantie, E., … Räikkönen, K. (2015).Maternal depressive symptoms throughout pregnancyare associated with increased placental glucocorticoidsensitivity. Psychological Medicine, 45(10), 2023–2030.
Sagi-Schwartz, A., Van IJzendoorn, M. H., Grossmann, K.E., Joels, T., Grossmann, K., Scharf, M., … Alkalay, S.(2003). Attachment and traumatic stress in female holo-caust child survivors and their daughters. AmericanJournal of Psychiatry, 160(6), 1086–1092.
Sangalang, C., Jager, J., & Harachi, T. W. (2017). Effects ofmaternal traumatic distress on family functioning andchild mental health: An examination of Southeast Asianrefugee families in the U.S. Social Science & Medicine,184, 178–186.
Sangalang, C. C., & Vang, C. (2017). Intergenerational traumain refugee families: A systematic review. Journal ofImmigrant and Minority Health, 19(3), 745–754.
Scharf, M., & Mayseless, O. (2011). Disorganizing experi-ences in second- and third-generation holocaust survi-vors. Qualitative Health Research, 21(11), 1539–1553.
Shmotkin, D., & Litwin, H. (2009). Cumulative adversityand depressive symptoms among older adults in Israel:The diffrential role of self-oriented versus other-orientedevents of potential trauma. Social Psychiatry andPsychiatric Epidemiology, 44, 579–585.
Shrira, A. (2015). Transmitting the sum of all fears: Iraniannuclear threat salience among offspring of Holocaustsurvivors. Psychological Trauma: Theory, Research,Practice, and Policy, 7(4), 364–371.
Shrira, A., Palgi, Y., Ben-Ezra, M., & Shmotkin, D. (2011).Transgenerational effects of trauma in midlife: Evidencefor resilience and vulnerability in offspring of Holocaustsurvivors. Psychological Trauma: Theory, Research,Practice, and Policy, 3(4), 394–402.
Solkoff, N. (1981). Children of survivors of the NaziHolocaust: A critical review of the literature. AmericanJournal of Orthopsychiatry, 51(1), 29–42.
Solkoff, N. (1992). Children of survivors of the NaziHolocaust: A critical review of the literature. AmericanJournal of Orthopsychiatry, 62(3), 342–358.
Solomon, Z. (1998). Transgenerational effects of theHolocaust: The Israeli perspective. In Y. Danieli (Ed.),International handbook of multigenerational legacies oftrauma (pp. 69–83). New York, NY: Plenum Press.
Solomon, Z., Kotler, M., & Mikulincer, M. (1988). Combat-related posttraumatic stress disorder among second-gen-eration Holocaust survivors: Preliminary findings.American Journal of Psychiatry, 145, 865–868.
Spielberger, C. D., Gorsuch, R. L., & Lushene, R. E. (1968).State-Trait Anxiety Inventory (STAI): Test Manual forForm X. Consulting Psychologists Press.
Spitzer, R. L, Gibbon, M., & Williams, J. B. (1995).Structured clinical interview for axis I DSM-IV disorders(SCID). Washington, DC: American PsychiatricAssociation.
Taouk, L., & Schulkin, J. (2016). Transgenerational trans-mission of pregestational and prenatal experience:maternal adversity, enrichment, and underlying epige-netic and environmental mechanisms. Journal ofDevelopmental Origins of Health and Disease, 7(6),588–601.
Van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., &Sagi-Schwartz, A. (2003). Are children of Holocaustsurvivors less well-adapted? A meta-analytic investiga-tion of secondary traumatization. Journal of TraumaticStress, 16(5), 459–469.
Van IJzendoorn, M. H., Fridman, A., Bakermans-Kranenburg, M. J., & Sagi-Schwartz, A. (2013).Aftermath of genocide: Holocaust survivors’ dissociationmoderates offspring level of cortisol. Journal of Loss andTrauma, 18(1), 64–80.
Van IJzendoorn, M. H., & Schuengel, C. (1996). The mea-surement of dissociation in normal and clinical popula-tions: Meta analytic validation of the dissociativeexperiences scale (DES). Clinical Psychology Review, 16,365–382.
Watson, M., Greer, S., Young, J., Inayat, Q., Burgess, C., &Robertson, B. (1988). Development of a questionnairemeasure of adjustment to cancer: the MAC scale.Psychological Medicine, 18(1), 203–209.
Winnicott, D. W. (1971). Playing and reality. Hove andNew York: Brunner-Routledge.
Wiseman, H., Barber, J. P., Raz, A., Yam, I., Foltz, C., &Livne-Snir, S. (2002). Parental communication ofHolocaust experiences and interpersonal patterns in off-spring of Holocaust survivors. International Journal ofBehavioral Development, 26(4), 371–381.
Yehuda, R., Bell, A., Bierer, L. M., & Schmeidler, J. (2008a).Maternal, not paternal, PTSD is related to increased riskfor PTSD in offspring of Holocaust survivors. Journal ofPsychiatric Research, 42(13), 1104–1111.
Yehuda, R., & Bierer, L. M. (2008b). Transgenerationaltransmission of cortisol and PTSD risk. Progress inBrain Research, 167, 121–135.
Yehuda, R., Bierer, L. M., Andrew, R., Schmeidler, J., &Seckl, J. R. (2009). Enduring effects of severe develop-mental adversity, including nutritional deprivation, oncortisol metabolism in aging Holocaust survivors.Journal of Psychiatric Research, 43(9), 877–883.
Yehuda, R., Bierer, L. M., Schmeidler, J., Aferiat, D. H.,Breslau, I., & Dolan, S. (2000). Low cortisol and risk forPTSD in adult offspring of holocaust survivors.American Journal of Psychiatrym, 157, 1252–1259.
Yehuda, R., Blair, W., Labinsky, E., & Bierer, L. M. (2007a).Effects of parental PTSD on the cortisol response todexamethasone administration in their adult offspring.American Journal of Psychiatry, 164(1), 163–166.
Yehuda, R., Daskalakis, N. P., Bierer, L. M., Bader, H. N.,Klengel, T., Holsboer, F., & Binder, E. B. (2016). Holocaustexposure induced intergenerationaleffects on FKBP5methylation. Journal of Biological Psychiatry, 80(5), 372–380.
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 epigeneticregulation of the glucocorticoid receptor gene in
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 27
Holocaust survivor offspring. American Journal ofPsychiatry, 171(8), 872–880.
Yehuda, R., Engel, S.M., Brand, S. R., Seckl, J., Marcus, S. M., &Berkowitz, G. S. (2005). Transgenerational effects of post-traumatic stress disorder in babies of mothers exposed to theWorld Trade Center attacks during pregnancy. The Journalof Clinical Endocrinology & Metabolism, 90(7), 4115–4118.
Yehuda, R., Halligan, S. L., & Bierer, L. M. (2001a).Relationship of parental trauma exposure and PTSD toPTSD, depressive and anxiety disorders in offspring.Journal of Psychiatric Research, 35(5), 261–270.
Yehuda, R., Halligan, S. L., & Bierer, L. M. (2002). Cortisollevels in adult offspring of Holocaust survivors: relation
to PTSD symptom severity in the parent and child.Psychoneuroendocrinology, 27(1–2), 171–180.
Yehuda, R., Halligan, S. L., & Grossman, R. (2001b).Childhood trauma and risk for PTSD: relationship tointergenerational effects of trauma, parental PTSD, andcortisol excretion. Development & Psychopathology, 13(3), 733–753.
Yehuda, R., Teicher, M. H., Seckl, J. R., Grossman, R.A., Morris, A., & Bierer, L. M. (2007b). Parentalposttraumatic stress disorder as a vulnerability factorfor low cortisol trait in offspring of holocaust survi-vors. Archives of General Psychiatry, 64(9), 1040–1048.
28 P. DASHORST ET AL.
Appendix 1
The search syntax was: (SecondWorldWar orWorldWar II orWorldWar 2 orWWII orWW2orWorldwar-2 orWorldwar-II orWorldWar Two or 2WAR2 or Holocaust) and (Child* of Holocaust Survivor* or child* of concentration camp survivor* or secondgeneration or adult offspring) and (adult offspring/ or daughters/ or sons/) and Acute Stress or C*PTSD or chronic trauma* orCombat disorder* or combat fatigue or Combat Neuros#s or combat stress or Complicated Trauma* or comorbid* or Complextrauma* or DES*NOS or “Disorders of Extreme Stress“ or Dual Diagnos#s or emotional trauma* or Enduring Personality Changeafter Catastrophic Experience* or EPCACE or Multiple Trauma* or posttraumatic neuros#s or post-traumatic neuros#s orposttraumatic psychic syndrome* or post-traumatic psychic syndrome* or posttraumatic psychos#s or post-traumatic psychos#sor posttraumatic stress or post-traumatic stress or posttraumatic syndrome* or post-traumatic syndrome* or Psychotrauma* orPTSD or shell shock or traumati#ed or traumatic stress or Type II trauma* or Type I trauma* or war neuros#s.ti,ab. and(Posttraumatic Stress Disorder/ or Emotional Trauma/ or acute stress disorder/ or combat experience/ or trauma/ or traumaticneurosis/) and (depress* or melanchol* or low mood) And (Anxiety Disorder* or panic disorder* or anxiety symptom* or panicsymptom* or Anxiety attack* or panic attack* or Agoraphobia) and (exp Anxiety Disorders) and (neurotic depression* ordysthymic disorder* or chronic depression* or mood disorder*) and (exp Dysthymic Disorder) and (eating disorder* or anorexianervosa or bulimia nervosa or Compulsive overeating or Diabulimia or Drunkorexia or Gourmand syndrome) and (exp EatingDisorders) and (Personality disorder* or obsessive-compulsive disorder or borderline or Paranoid or Schizoid or Narcissistic orHistrionic or Schizotypal or antisocial or avoidant or masochistis or sadistic or negativistic) and (exp Personality Disorders) and(exp Drug Abuse/ or exp addiction) and (addict* or alcohol* or Amphetamine or Angel Dust or Binge Drinking or Cannabis orCocaine or Delirium Tremens or dependen* or Drug Abus* or Drug Addicti* or Drug Dependen* or Drug Habit* or DrugOverdose* or Drug psychos* or “DrugUse disorder*“ or DrugWithdrawal or Drunkenness* or Ethanol or FAE* or FASD* or Glueor Hashish or Heroin or Inhalant abus* or Intravenous Drug* or Intravenous Substance* or Marihuana or Morphine or Narcotic*or Neonatal Abstinence or Nicotine or Opiate* or Opioid* or PCP abus* or Phencyclidine or smoker* or Smoking* or Substanceabus* or Substance addict* or Substance dependen* or Substance Induced or ”Substance Use” or Substance-Induced or Substance-Related or Tobacco or Withdrawal) and (somatization/ or exp somatoform disorders) and (somatization* or somatoform or BodyDysmorphic Disorder or Conversion Disorder or Hypochondriasis or Neurasthenia or Neurodermatitis or Somatization Disorderor SomatoformPainDisorder) and (mental disorder* ormental illness or psychological disorder* or psychiatric disorder*) and (expMental Disorders) and (exp Symptoms) and (Arousal or Hyperarousal or Avoidance or Reexperienc* or Intrusion or Reliv* ornightmare* or sleep* or flashback* or belief* or feeling*) and (Comorbidity) and (comorbid* or Multiple Disorders or DualDiagnosis) and (expMental Health/ orWell Being/ or exp ”Quality of Life”) and (mental health or well-being or Quality of Life) and(exp social identity/ or identity formation/ or Identity Crisis/ or exp Separation Anxiety/ or exp Separation Reactions/ or expSeparation Individuation) and (identit* or individuation or separation) and (Heredity or genetic* or epigenetic* or Epigenomic* orcortisol or Hydrocortisone or Epicortisol or 11?Epicortisol or Cortifair or Cortril or neurobiolog* or neuropsycholog* or DNA orDeoxyribonucleic Acid or biomarker* or ((Biologic* or Biochemical or Clinical or Laboratory or Serum or Viral or Immunologic orImmune or Surrogate) adj (end?point* or Marker*)) or phenotype*) ti,ab.and (exp Genetics/ or Hydrocortisone/ or expNeurobiology/ or Neuropsychology/ or DNA/ or Biological Markers/ or Phenotypes.
EUROPEAN JOURNAL OF PSYCHOTRAUMATOLOGY 29