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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

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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

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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.

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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.

http://www.UNHCR.org

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


(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.


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)


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


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)


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


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)


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


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)


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


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)


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


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)


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


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).


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


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)


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).


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).


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).


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).


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)


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.


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,


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


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


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.


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.

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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.


intergenerational consequences of the holocaust on ... · also, there was evidence suggesting that...

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