Intergenerational consequences of the Holocaust on offspring mental health: a systematic review of associated factors and mechanisms

Figures & data

Figure 1. Flowchart study selection.

Table 1. Study characteristics.

Authors, year	HS sample characteristics: Number; gender; age; residence during the war	JC Comparison sample characteristics: Number, gender, age, residence	HSO sample characteristics: Number; gender; age; residence during study	JCO Comparison sample characteristics: Number, gender, age, residence	Recruitment	HS response rate; HSO response rate	Offspring mental health complaints compared to JCO (outcome symptom measure)	Study focus
Bader, Bierer, Lehrner, Makotkine, Daskalakis, & Yehuda., 2014			Convenience sample N= 69 Holocaust survivor offspring	N= 26 Jewish non-HSO	Through advertisements and participation in earlier study		NS 24-hr urinary cortisol Trend for difference in depression, life-time PTSD diagnosis, and childhood trauma	Urinary cortisol
Baider et al., 2006			Group 1 HSO + former breast cancer N = 193; all women; M age = 48.7, SD age = 5.0; Israel Group 3 HSO healthy: N = 176; all women; M age = 46.2, SD age = 5.8; Israel	Group 2 former breast cancer non-traumatized parents: N= 164; all women; M age = 48.7, SD age = 6.8; Israel Group 4 healthy women non-traumatized parents: N = 143; all women; M age = 46.5, SD age = 8.1; Israel	Former first-time breast cancer patients (i.e., no evidence of active disease at the time of study) recruited from list of all patients diagnosed with stages 1 and 2 breasts cancer in between 1994 and 2000 in two oncology centres. All HSO patients (group 1) and a random sample of non-HSO (group 2) were invited to participate. Random sample of healthy HSO (group 3) selected from the files of National Holocaust Archive Random sample from Israel Interior Ministry Census files (group 4). No current or previous psychiatric conditions.	Group 1: 193/212 = 91% Group 2: 164/174 = 94% Group 3: 176/190 = 93% Group 4: 143/150 = 95%	Psychological distress (intrusion, avoidance IES) sign higher in HOS with cancer than in comparisons with cancer. Of coping variables, only helplessness was different between HSO and comparisons (MAC).	Life time stressors, cancer diagnosis
Baider et al., 2008	Mother-daughter dyads: Group 1 HS mothers N = 20; M age = 73.6, SD age = 6.6; Israel Group 3 HS mothers: N = 20; M age = 76.5, SD age = 7.6; Israel	Mother-daughter dyads: Group 2 Non-traumatized mothers: N = 20; M age = 74.3, SD age = 10.1; Israel Group 4 Non-traumatized mothers: N= 20; M age = 72.5, SD age = 8.6; Israel	Mother-daughter dyads: Group 1 HSO & former breast cancer N = 20; M age = 46.9, SD age = 7.1; Israel Group 3 HSO healthy: N= 20; M age = 45.4, SD age = 7.3; Israel	Mother-daughter dyads: Group 2 former breast cancer patients: N = 20; M age = 46.3, SD age = 9.8; Israel Group 4 healthy women: N= 20; M age = 45.8, SD age = 6.8; Israel	Random selection of 24 dyads out of each group included in Baider et al., 2006	Group 1: 20/24 = 83% Group 2:19/24 = 79% Group 3: 22/24 = 92% Group 4: 20/24 = 83%	Global Severity Index (BSI) differentiated between HSO with cancer and JCO with and HSO without cancer.	Life time stressors, cancer diagnosis
Bierer, Bader, Dasklalakis, Lehrner, Makotkine, Seckl, & Yehuda, 2014			N= 85 HSO, 40% male; M age = 46.9, SD age = 7.6; Israel	N = 27 JCO, 48.1% male; M age = 42.6, SD age = 10.5; Israel	Through advertisements; in part among participants of earlier study.		HSO more lifetime anxiety disorder (SCID, d = 0.40), and stage-anxiety (STAI; d = 0.44)). Reduced cortisol excretion in HSO compared to JCO; 11ß-HSD-2 activity elevated in HSO compared to JCO, in particular among mothers who had been children during WWII (24-h urine sample).	Glucocorticoid metabolism, 11ß-HSD-2 activity
Gangi et al., 2009			N = 40 Italian-Jew Holocaust survivor offspring, 33% had received psychotherapy. 50% Female, M age = 38, SD age = 12.4, Italy	Comparison group of N = 37 Italian Jew offspring who were able to hide during the war. 43.2% Female, M age = 37, SD age = 13.7; Italy	Recruited via Jewish register and after identification of those who had children.	Response rate 100%	HSO had higher anxiety levels, low self-esteem, inhibition of aggression, and relational ambivalence than JCO.	Intra-familial dynamics, e.g. organization, expression of emotions.
Halligan & Yehuda, 2002			N= 87, 36% men, 64% women raised by parent(s) who survived the Nazi Holocaust	N = 39, 49% men, 51% women raised by parent(s) without Holocaust experience and free from current and lifetime axis I psychiatric disorders.	Participants were solicited from lists obtained from the Jewish community or responded to announcements and newspaper advertisements. In addition (N = 28) were enrolled through a specialized treatment programme. N = 7 participants new since Yehuda et al., 2001a.		Dissociative symptoms (DES) lower in JCO than sub-groups of HSO, being highest in HSO with current PTSD.	Mental health, PTSD in parents
Kellermann, 2008	HS characteristics provided by HSO: N = 273 mothers; born between 1905–1945; 65% born in Eastern Europe, 19% born in other occupied countries, 14% non-HS N = 273 fathers; born between 1895–1946; 70% born in Eastern Europe, 19% born in other occupied countries, 9% non-HS		N= 273 clinical offspring; 69% female; 48% born between 1945–1954, 37% born between 1955–1964, 15% born between 1965–1974; Israel	-	Consecutive admissions/referrals to a HSO specialized clinic	Information not provided	No comparison group	Identification of demographic factors
Lehrner, Bierer, Passarelli, Pratchett, Flory, Bader, Makotkine & Yehuda, 2014			N = 80, 83% women, 74% men, M age = 56.6, SD = 8.5; USA	N= 15, 60% women, 40% men, M age = 58.7, SD = 11.2; USA	Through print and online advertisements in Jewish news outlets, second generation and other Jewish electronic mailing lists, advertisements and by word-of-mouth (2010–2012).		HSO more likely than JCO to have a current anxiety disorder diagnosis (SCID; d = 0.45) and to report symptoms of depression (BDI; d= 0.78) and anxiety (STAI; d= 0.79), as well as to report more child abuse and neglect (d= 0.70; CTQ). HSO had higher 24-h urinary cortisol levels (LST).	Glucocorticoid sensitivity
Letzter-Pouw et al., 2014			Sample one n= 172^a; 48.3% women; M age 42.8, SD age = 7.3; Israel Sample two n= 161; 58.4% women; M age 55.4, SD age = 5.3; Israelis from families of European origin. At least one parent who was under Nazi or pro-Nazi occupation or domination in Europe during the Second World War.	Sample two N= 124 parents without holocaust background; 54.4% women; M age 54.4, SD age = 5.7;	Sample one nationally representative sample recruited by contacting everyone on a list (n = 272) provided by Ministry of Interior of persons living throughout Israel, born between 1928 and 1945 in a European country that suffered Nazi occupation and who immigrated to Israel after 1945. Sample two convenience sample community-dwelling, recruited across the country.	Sample one HSO 63% Sample two HSO 60%	Sample one was not compared Sample two HSO reported higher Holocaust salience (n2p = .36); transmission of burden (PPRBQ) from mother (n2p = .11) and father (n2p = .09).	Perceived parental burden.
Letzter-Pouw & Werner, 2013	N= 178 ^a dyads; (almost equally divided between both genders; M age 69.8, SD age = 5.1); 87% born in Eastern Europe, 13% born in Western Europe		N= 178 ^a, first-born; almost equally divided between both genders; M age = 43.8, SD age = 7.3); Israel	-	Sample recruited by contacting everyone on a representative list (N = 272) provided by national Ministry of Interior of persons living throughout Israel, born between 1928 and 1945 in a European country that suffered Nazi occupation and who immigrated to Israel after 1945.	HS 178/272 = 65%; HSO 178/272 = 65%	No comparison group	Intrusive memories in Holocaust child survivors and well-being of HSO.
Sagi-Schwartz et al., 2003	HS who immigrated as orphans from Europe to Israel during or after the war, HSO (N = 48). Born in Europe between 1926 and 1937.	Comparison group of subjects in same age range, also born in Europe but immigrated to Israel before the war.	N = 50 Mother offspring HSO, females, born between 1947 and 1970.	JCO, females, born between 1947 and 1970.	Population register provided by Israeli government. Thereupon 30.000 standardized telephone calls.		HS showed more traumatic stress and less lack of resolution of trauma than JC (d = .77) HS fewer secure attachment representations than JC; HSO not different in attachment classification from JCO.	Attachment impacted by Holocaust trauma
Shrira, 2015			Study 1 N= 63; M age = 57.1, SD = 6.26, 61.9% women Study 2 N = 300 respondents with at least one Holocaust survivor parent. M age = 57.8, SD = 4.6, 59% women.	N1= 43, M age= 54.7, SD= 8.56, 55.8% women N2= 150, M age = 57.12, SD= 4.64, 56.8% women.	Study 1 Convenience sample of community-dwelling, Hebrew speaking Jewish Israelis from families of European origin living in Tel Aviv and its surroundings. Data collection in June 2012. Study 2 had similar procedures as in Study 1. Data collection 2012–2013.		HSO reported higher Iranian nuclear threat salience (8-items) than JCO. HSO also reported more anxiety symptoms (Study 1, TMAS-SF); and psychological distress (Study 2, BSI-18).	Coping with threat: Iranian nuclear threat salience
Shrira et al., 2011			N= 215 born in 1945 or later, in Israel, Europe/USA or in the Former Soviet Union, with a father born in Europe/USA (except for 20 respondents who were born in Europe/USA but had a father from a non-European origin),	N = 149; neither parent had lived under Nazi or pro-Nazi occupation/domination	Probability sample drawn from the Israeli component of the Survey of Health, Ageing and Retirement in Europe. Interviewed in 2005–2006. Also, drop-off questionnaire.	66.6% of total sample completed the questionnaire	Differences between HSO and JCO in number of major health problems, of physical symptoms and number of medications. HSO also reported higher optimism and hope, and better life satisfaction.	Function of number of survivor parents.
Yehuda et al., 2008a			N = 211; 117 men, 167 women (M age = 43.2; SD age = 9.1; born 1938–1979) with at least one parent interned in a Nazi-concentration camp during WW II or had faced comparably severe threats in hiding.	N= 73 comparable age, with parents who were not exposed to the Holocaust or war-events.	Community sample recruited through advertisements. N = 145 new observations since Yehuda et al., 2001a.		A higher prevalence of lifetime PTSD, mood, anxiety disorders, and to a lesser extent, substance abuse disorders, was observed in HSO than in JCO (SCID, CAPS).	Maternal vs paternal PTSD and PTSD occurrence in HSO.
Yehuda & Bierer, 2008b			N= 41 HSO N= 18 HSO with maternal PTSD; M age= 49.8, SD age =6.5; N = 6 men, N= 12 women N = 23 HSO without maternal PTSD (M age = 50.4, SD age = 7.3 N = 7 men, N= 16 women	N= 19 JCO (M age = 44.4, SD age =9.5; N = 12 men, N= 7 women			Trauma exposure (Mississippi PTSD Scale; CTQ; PPQ) Depression symptoms (BDI)	Urinary and salivary cortisol levels PTSD risk
Yehuda, Blair, Labinsky, Bierer, 2007a			N= 25 HSO n = 23 HSO with PTSD n = 10 HSO without PTSD, USA	N= 16 JCO, USA	Recruitment through advertisements.		Cortisol levels were lowest in HSO with parental PTSD (plasma levels), higher in HSO without parental PTSD and highest in JCO.	Plasma cortisol levels.
Yehuda et al., 2016	N = 32, including both parents for 5 HSO; 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 multiple siblings in N = 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 part of a larger sample of HSO, of which the majority was recruited 1993–1995 and longitudinally followed-up 10 years after.		Holocaust exposure had an effect on FKBP5 methylation observed in exposed parents as well as their offspring. Methylation was lower in HSO compared to controls.	Cytosine methylation within the gene encoding for FK506-binding-protein-5 (FKBP5)
Yehuda, Daskalakis, Lehrner, Desarnaud, Bader, Makotikine, Flory, Bierer & Meaney, 2014			N = 80 HSO 75% had both parents exposed n = 53 (55.8%) maternal PTSD n = 42 (44.2%) paternal PTSD n = 15 no parental PTSD, USA	N = 15 JCO no parental PTSD, USA	95/120 = 79% response rate		Alterations of specific methylation were demonstrated in relation to parental PTSD and neuroendocrine outcomes. Interaction effect of paternal and maternal PTSD was found.	Influence of maternal and paternal PTSD on DNA methylation and its relationship to glucocorticoid receptor sensitivity
Yehuda et al., 2001a			N =95 (33.3% men, 66.7% women) having been born to at least one biological parent who experienced the Nazi Holocaust.	N = 40 (57% men, 43% women) Jewish individuals in the same age range who did not have a parent who was a Holocaust survivor, not necessarily without psychiatric diagnoses.	Recruitment from lists obtained from the Jewish community or through community group announcements (N = 109); or through a specialized treatment programme (N = 26). N = 42 (26 HSO; 16 JCO) subjects were new participants compared to prior publications.		HSO differed from JCO in mean number of lifetime diagnoses, in particular PTSD, depressive and (trend:) anxiety disorders (SCID, CAPS).	Development of PTSD, depressive and anxiety disorders in HSO as a function of parental exposure and PTSD.
Yehuda et al., 2002			N =39 (18% men, 82% women) having been born to at least one biological parent who experienced the Nazi Holocaust; USA.	N = 15 (53.3% men, 46.7% women) Jewish individuals in the same age range who did not have a parent who was a Holocaust survivor, free from psychiatric diagnoses; USA.	Described in Yehuda et al., (2000)		HSO and JCO did not differ in urinary cortisol concentration. The occurrence of (lifetime and current) psychiatric disorder was higher in HSO than in JCO.	Cortisol levels related to severity of PTSD symptoms Number of parents affected
Yehuda et al., 2001b			N= 51, 20 men, 31 women having been born to at least one biological parent who experienced the Nazi Holocaust. M age = 40.9, SD = 7.6; USA.	N = 41, 23 men, 18 women, with the same age range (24–60 years) who did not have a parent who was a Holocaust survivor. M age = 38.3, SD = 8.8; USA.	Participants were solicited from lists obtained from the Jewish community, through advertisements (n = 79), and via short-term group psychotherapy (n = 13).		HSO reported more emotional abuse, neglect, physical neglect and (trend:) sexual abuse than JCO (CTQ).	The impact of childhood trauma; influenced by parental trauma exposure and parental PTSD.
Yehuda et al., 2007b			N = 33 HSO N = 23 HSO with parental PTSD N = 10 HSO no parental PTSD	N = 16 JCO			Offspring with paternal PTSD only were not significantly different in mean cortisol level than offspring with no parental PTSD or comparison subjects (JCO). Mean cortisol levels were similar for offspring with PTSD in both parents and those with maternal PTSD only, whereas both groups differed from offspring with no parental PTSD (p= .02 and p= .045, respectively) and from comparison subjects (p= .009 and p= .02, respectively).	Cortisol levels related to parental PTSD
Van IJzendoorn et al., 2013	Mother-daughter dyads: HS parents: N= 32; 100% female, M age = 76.98, SD = 2.99, Israel	JC parents: N= 33; 100% female; M age = 76.98, SD = 2.99.	Mother-daughter dyads: N= 47 HSO, M age = 47.46, SD = 4.41, daughters in Israel	Mother-daughter dyads: N= 32 JCO M age = 47.46, SD = 4.41, daughters in Israel	Recruitment through register of Israeli Ministry.	82.3% first generation; 82.3% second generation	HSO showed lower cortisol levels only when surviving parents displayed more dissociation (whereas HS showed higher levels of daily cortisol versus comparisons).	Dissociation as moderating factor in the biological stress regulation system in HSO.

^a= Sample overlap, in the 2014 report, six participants were excluded as not eligible for the research purposes; HS = Holocaust Survivors; HSO = Holocaust Survivor offspring; JCO = Jewish comparisons offspring; Only outcome symptom measures relevant for the current review were included: BDI = Beck Depression Inventory (Beck et al., 1961); BSI = Brief Symptom Inventory (Derogatis & Melisaratos, 1983); CTQ = Childhood Trauma (Bernstein et al., 1997); CAPS = Clinician Administered PTSD Scale (Blake et al., 1990); DES = Dissociative Experiences Scale (Bernstein & Putnam, 1986); IES = Impact of Event Scale (Horowitz, Wilner, & Alvarez, 1979); MAC = Mental Adjustment to Cancer (Watson et al., 1988); NHSPQ/PPRBQ = New Holocaust Survivor Parenting Questionnaire/Perceived Parental Rearing behaviour Questionnaire (Kellermann, 2001); PPQ = Parental PTSD Scale (Yehuda et al., 2000; Yehuda et al., 2008a); SCID = Structured Clinical Interview for DSM-IV (Spitzer et al., 1995); STAI = Spielberger State Trait Anxiety Inventory (Spielberger, 1968); TMAS-SF = Taylor Manifest Anxiety Scale-Short Form (Bendig, 1956).

Table 2. Mental health complaints in parents and their children.

Author	Results (assessment instruments) pertaining to parent psychopathology and functioning	Results (assessment instruments) pertaining to offspring psychopathology and functioning	Results (assessment instruments) pertaining to the association between parent and offspring psychopathology and functioning
Halligan & Yehuda, 2002	N= 57 (66%) one or both parents with PTSD (PPQ)	Dissociative symptoms (DES) were elevated in individuals with current PTSD (CAPS), but not in those with past PTSD or with the risk factor of parental PTSD (PPQ).	24 HSO with PTSD (27.5%) had one or both parents with PTSD (PPQ). Dissociative symptoms (DES) were only elevated in HSO with current PTSD and parental PTSD but were not elevated in other HSO with PTSD or with parental PTSD or parental Holocaust exposure without PTSD(PPQ). Of the n = 27 (31%) offspring with current or past PTSD, 24 (89%) indicated that their parent(s) had had PTSD. Of the n = 60 offspring without current or past PTSD, n = 33 (55%) indicated that their parent(s) had had PTSD (φ = .35).
Kellermann, 2008	Perceived mental health father: Difficult 17% Middle 40% Good 28% Missing value 15% Perceived mental health mother: Difficult 24% Middle 37% Good 22% Missing value 17% Perceived functioning father: Fully 66% Partly 20% Impaired 1% Missing value 13% Perceived functioning mother: Fully 64% Partly 19% Impaired 3% Missing value 14%	Not studied	Not studied
Letzter-Pouw & Werner, 2013	Symptoms of psychological and physical distress M = 1.71, SD= 0.52 (BSI). 84% suffered from intrusive memories, M = 16.32, SD = 6.64 (IES)	Symptoms of psychological and physical distress M = 1.51, SD = 0.48 (BSI).	HS psychological and physical distress (BSI) indirectly predicted offspring distress (BSI). The relation was mediated by perceived perceived mother’s “transmission” of trauma (NHSPQ/PPRBQ).
Letzter-Pouw et al., 2014		PTSD symptoms M = 1.73, SD = 1.78 (CAPS)	After controlling for age, gender, education, and life events, perceived “transmission” of burden from mother (NHSPQ/ PPRBQ) (β= .31) [as well as number of survivor parents (β= .16]) predicted HSO posttraumatic symptoms (CAPS). In a separate analysis, and after controlling for age, gender, education, and life events, perceived “transmission” of burden from father (NHSPQ/ PPRBQ) predicted HSO posttraumatic symptoms (CAPS) (β= .23).
Lehrner et al., 2014	Of the N = 80 parents with Holocaust exposure (11.6% father, 9.5% mother, 63.2% both parents), 32.6% both parents had PTSD, 23.2% maternal PTSD, and 11.6% paternal PTSD (PPQ).	5.4% HSO had major depressive disorder, 41.1% anxiety disorder (MINI)	Not studied
Yehuda et al., 2001a	N= 60 (64.5%) HS with PTSD (Parental PTSD scale) N= 33 (35,5%) HS without PTSD	56% HSO had depressive disorder while 29% HSO had PTSD	N = 93 HSO, of whom N= 60 (64.5%) parental PTSD; N = 33 (35.4%) HSO non-parental PTSD (PPQ); N = 42 JCO After controlling for gender, parental PTSD was associated with offspring PTSD (φ = .52) and with offspring depression (φ = .34).
Yehuda et al., 2001b	n = 32 (62.7%) HSO had one or both parents with PTSD, n = 17 (33%) had two parents with PTSD; n = 19 (37.3%) HSO without parental PTSD.	N= 17; 33.3% PTSD	Not studied
Yehuda et al., 2007a	n =13 HS with PTSD; N = 12 HS without PTSD; N = 16 JC	N = 4 (66.7%) HSO met criteria for lifetime PTSD (none for current PTSD)	Not studied
Yehuda et al., 2008a	N= 211 HS N = 49 (30.4%) with paternal PTSD; N= 40 (24.8%) with maternal PTSD; N= 35 (21.7%) both parents with PTSD; N = 37 (23%) no parental PTSD (PPQ).	69.5% HSO had any lifetime psychiatric diagnosis. More specifically, prevalence in HSO (N = 200): PTSD 19.0%; mood disorder 45.5%; anxiety disorder (32.5%); eating disorder 6.0%; substance abuse 10.5%, and adjustment disorder 10.0% (SCID DSM IV; CAPS).	Based on the prevalence rates reported for occurrence of PTSD, mood disorder or any psychiatric disorder in HSO, having a mother (OR 2.40) or both parents with PTSD (OR 3.21)increased the likelihood of having PTSD compared to having no parental PTSD. Higher association of mood disorders and parental PTSD versus non-parental PTSD (Paternal PTSD OR = 3.66, maternal PTSD OR = 3.06, both parents PTSD OR = 3.21).
Yehuda et al., 2014	N = 95 (75%) HSO both parents exposed n =31 both parents PTSD n= 53 (55.8%) maternal PTSD, n =22 only maternal PTSD; n =42 (44.2%) paternal PTSD n= 11 only paternal PTSD; n =31 no parental PTSD	Measures of social-emotional functioning in HSO were used (BDI, CTQ, STAI, PEH, RSQ, DES. PPQ)) without reporting prevalence of psychiatric disorders in this sample.	Not studied
Yehuda et al., 2016	N= 16 (51.6%) PTSD N = 4 (13.8%) Anxiety disorder (other than PTSD) N = 9 (31.0%) Mood disorder (SCID, CAPS) As was retrospectively evaluated by HSO (PPQ): Maternal PTSD; N =11 (52.4%) Paternal PTSD; N = 11 (52.4%) Any parent with PTSD; N = 16 (76.2%) (PPQ)	N = 8 (36.4%) Anxiety disorder (other than PTSD) N = 3 (13.6%) Mood disorder (SCID)	Not studied

HSO = Holocaust survivor offspring; JCO = offspring of Jewish comparisons; BDI = Beck Depression Inventory CAPS = Clinical Administered PTSD Scale (Blake et al., 1995); PDS = Posttraumatic Diagnostic scale (Foa et al., 1997); ; NHSPQ New Holocaust Survivor Questionnaire (Kellermann, 2001); PEH = Perceived Emotional Health (Flory, Bierer, & Yehuda, 2011); PPQ = Parental PTSD Scale (Yehuda et al., 2000; Yehuda et al., 2008a); PPRBQ = Perceived Parental Rearing Behaviour Questionnaire (Kellermann, 2001); RSQ = Relation Scales Questionnaire (Griffin & Bartholomew, 1994); SCID = Structured Clinical Interview for DSM-IV (Spitzer et al., 1995); STAI = Spielberger State-Trait Anxiety Inventory (Spielberger, 1968).

Table 3. Perceived parenting, attachment and mental health complaints in HSO.

Author	HSO results on attachment/perceived parenting (instruments)	Results pertaining to association between parent and offspring attachment and offspring mental health
Gangi et al., 2009	HSO differed from JCO in terms of perceiving their family as expressing emotions poorly (d= .56); not being assertive and make their own decisions (d= .57); attribute greater importance on organizing and planning of family activities and responsibilities (d= .51) and put greater emphasis on following family rules (d= .43). They described their ideal family as being strongly oriented towards 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, and moral-religious basis.	Not studied
Lehrner et al., 2014	Emotional abuse (CTQ) was positively associated with both maternal and paternal PTSD (r = .30; r = .32).	Of family environment factors (cohesion, expressiveness, conflict, organization, and control; FES) only conflict was correlated to glucocorticoid sensitivity (LST) in HSO. When family conflict was included as a covariate including maternal and paternal PTSD and Holocaust exposure, the main effect of maternal PTSD was unchanged. Family conflict moreover, was correlated with paternal, but not maternal PTSD (r = .36). Emotional abuse and family conflict moderated the effects of 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) of the Holocaust from mothers than fathers, no differences between mothers and fathers on punishing (NHSPQ).	The relation between HS psychological and physical distress (BSI) and HSO distress (BSI) was mediated by perceived parenting, more specifically perceived mother’s “transmission” of trauma (NHSPQ/PPRBQ).
Letzter-Pouw et al., 2014	Sample one Mothers were perceived to transmit more burden to their offspring than fathers (NHSPQ) (d = .33). Sample two HSO perceived more transmission of burden from mother (d= .70) and father (d = .64) versus comparisons (NHSPQ).	After controlling for age, gender, education, and life events, perceived “transmission” of burden from mother (NHSPQ/ PPRBQ) (β= .31) (as well as number of survivor parents (β= .16) predicted HSO posttraumatic symptoms (CAPS). In a separate analysis, and after controlling for age, gender, education, and life events, perceived “transmission” of burden from father (NHSPQ/ PPRBQ) predicted HSO posttraumatic symptoms (CAPS) (β= .23).
Sagi-Schwartz et al., 2003	No differences in proportion HSO (54%) and JCO (42%) with insecure attachment (AAI). No differences in proportion HSO (17%) and JCO (8%) with unresolved loss (AAI) No difference between HSO and JCO on mother-infant interactions (disorganizing maternal behaviours; MIDBS). No differences between HSO and JCO in satisfaction with relationship with mothers (CS).	Interaction between attachment type (secure vs insecure) x generation (first, second) indicated less insecure attachment in the second generation, both for the Holocaust 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 attachment representation of mothers among HSO, higher but the same as intergenerational attachment representation in general (kappa = .21). No evidence of intergenerational transmission of unresolved attachment Interaction of unresolved loss and trauma between HS and HSO (φ= .53).
Yehuda et al., 2001b	Adult Holocaust survivor offspring reported significant more childhood 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 of emotional abuse (66% with parental PTSD vs. 37% without parental PTSD), and physical neglect (56% vs 21%). CTQ scores were associated with PTSD in HSO for emotional 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 maternal PTSD (n= 18)	Based on the PBS HSO with maternal PTSD had significantly lower scores on perceived maternal care and higher scores on maternal overprotection than HSO without maternal PTSD paternal values were not significant.
Yehuda et al., 2007a	Parental PTSD symptoms were significantly correlated with childhood emotional abuse (r = .33) and physical neglect (r = .38) (CTQ), and total CTQ score (r = .41).	HSO mental health symptoms (CMS) were correlated with childhood 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 more negative consequences of being raised by Holocaust survivor 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 childhood trauma (CTQ), impacted on changes of epigenetic markers (methylation at different gene-sites) (β= −.36).

HSO = Holocaust survivor offspring; JCO = offspring of Jewish comparisons; AAI = Adult Attachment Inventory (Hesse, 1999); CAPS = Clinician Administered 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 Survivor Parenting Questionnaire (Kellermann, 2001); PPRBQ = Perceived Parental Rearing Behaviour Questionnaire (Kellermann, 2001); CMS = Civilian Mississippi Scale (Keane et al., 1988); MIDBS = Maternal Inappropriate and Disorganizing Behaviour Scale (Lyons-Ruth et al., 1999).

Table 4. Parental Holocaust history and mental health complaints in HSO.

Author	Results (assessment instruments) pertaining to parental Holocaust history and mental health outcomes in offspring	Results (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 intrusive memories (IES) (r= .38).	Perceived parenthood: HSO reported more affection (d = .28), over-involvement (d = .54), and transmission (d= .31) of the Holocaust from mothers than fathers, no differences between mothers and fathers on punishing (NHSPQ). Mother’s transmission of trauma (NHSPQ) was related to psychological distress (BSI) and with offspring’s psychological coping resources Mother’s transmission of the Holocaust (NHSPQ) related to intrusive memories (IES; r = .24). No association with perceived affection, punishment or over-involvement and no association with father’s perceived parenthood (NHSPQ).
Letzter-Pouw et al., 2014	Sample one 57.0% had two HS parents. HSO who had two HS parents showed more posttraumatic symptoms (CAPS) than those with one HS parent (d = .34).	Sample one Mothers were perceived to transmit more burden to their offspring 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 with posttraumatic symptoms (CAPS). Sample two HSO 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 two HS parents with a higher proportion of immigrants from Europe and the USA (φ= .46). There were no differences between both groups in health reports, life satisfaction or optimism and hope.	Not studied.
Yehuda et al., 2001b	No significant differences between offspring with one versus two 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 had PTSD; 40 mothers had PTSD, while 35 HSO had two parents with PTSD. The relationship of HS exposure and mental 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 significantly associated with paternal PTSD (48.1% compared to 17.6% in the comparison group) OR = .73, maternal PTSD (46.3%) OR 2.40; the effect cumulated when both parents had PTSD (56.9%) OR 3.21. Females with a father who had PTSD were more likely to develop PTSD, while males with a father who had PTSD were 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 were provided. 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).

Table 5. Heightened vulnerability to the development of mental complaints after additional stress and traumatic life events in HSO.

Author	Additional stress/traumatic life event HSO	Results (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 with breast cancer compared to non-HSO cancer patients. No difference on other coping styles (fighting spirit, anxious preoccupation, fatalistic acceptance (MAC). Effects of being HSO on most subscales of the BSI larger compared to effect of diagnosis of cancer (e.g. effect of being HSO generation (d = .76) compared to diagnosis of cancer (d = .49) on distress levels GSI scale BSI). Interaction between having breast cancer and being HSO on depression and psychoticism (BSI). The impact of cancer on the levels of depression and psychoticism in 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 daughter level 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 HSO relative to the comparison group. HSO seem to cope with stress as well as others.
Shrira, 2015	Iranian nuclear threat; and the perception 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, Iranian nuclear threat salience showed a strong relationship to anxiety symptoms (r= .33). Probing the interaction showed that, although among comparisons there was no relationship between Iranian nuclear threat salience and anxiety symptoms (β= 0.07), among HSO, Iranian nuclear threat salience showed a strong relationship to anxiety symptoms (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 Events Inventory (Shmotkin et al., 2009)); TMAS-S = Taylor Manifest Anxiety Scale – Short Form (Bendig, 1956).

Table 6. Biological parameters: cortisol, epigenetic factors and genetic predisposition.

Author	Sample	Results on offspring biological parameters	Results pertaining to association between parent and offspring cortisol metabolism and epigenetics
Bader et al., 2014	N = 69	No significant difference in 24-h urinary cortisol levels between HSO and JCO. Significant difference urinary cortisol in offspring of mothers who were adults (low) and who were children (high) (r = −.35) No significant difference in each combination between HSO with mothers exposed in childhood and in adolescence or not exposed.	Controlled for age, gender, and current depressive disorder, maternal age at Holocaust (β = −.56) and maternal PTSD (β = −.32) (d =0.43) were independent predictors of lower offspring urinary cortisol, whereas offspring childhood adversity and offspring PTSD symptoms were not. No interaction of effect of PTSD and maternal age of exposure. No relation of mother’s age at birth with cortisol levels in HSO. Significant effect of maternal PTSD (β = −.32) on HSO 24-h cortisol levels (lower levels when mother had PTSD). Significant main effect of maternal PTSD on HSO urinary cortisol d = .64.
Bierer et al., 2014	N = 85 female HSO N = 27 female JCO	24 h cortisol level HSO lower than JCO d= 0.45 and 5α-THF d = 0.34 Total glucocorticoid d= 0.43. Significant difference in 11β-HSD-2- activity between maternal exposure in childhood and JCO p =.029. HSO showed trend significant lower levels of cortisol (d= .45), 5α-THF (d= .39) (major metabolite of cortisol) and total glucocorticoids (d= .43) compared to JCO. No sign differences in the levels of other metabolites.	11β-HSD-2 activity significantly elevated in HSO when mothers exposed to Holocaust in childhood (β = .25). 11β-HSD-2 activity was higher between HSO mothers without PTSD than with PTSD and JCO this remained also significant after including father with PTSD as covariate. No effect of gender on 11β-HSD-2 activity. Maternal age of exposure, rather than maternal PTSD, predicted offspring 11β-HSD-2 activity (β = .34).
Lehrner et al., 2014	N = 95 HSO N = 26 JCO	Maternal PTSD only HSO cortisol suppression on DST 69.75%, both parents PTSD 82.49% Paternal PTSD higher 24-h urinary cortisol levels in HSO than when mother had PTSD d = −.84 and when both parents had PTSD	Maternal PTSD associated with significantly higher glucocorticoid sensitivity and lower 24-h urinary cortisol excretion in HSO (β= – .41). This was the same when both maternal and paternal PTSD was present. When only the father had PTSD, an opposite effect was observed lower glucocorticoid sensitivity and higher 24-h urinary cortisol excretion.
Van IJzendoorn et al., 2013	N= 29 survivor parents N = 45 HSO daughters N = 29 matched JC non-survivor parents N = 29 JCO daughters All female and living in Israel	No sign difference in cortisol levels of HSO compared to non-HSO	Significantly lower levels of daily salivary cortisol in HSO with survivor parents with higher scores on dissociation (DES) d= .73
Yehuda et al., 2001b	N= 51 HSO N = 41 JCO	N = 20 HSO + parental PTSD (24-h cortisol secretion M = 42.06 SD= 21.87) N = 8 HSO no parental PTSD (24-h cortisol secretion M = 67.90 SD= 29.82) (d = 0.895).	24-h Urinary cortisol excretion significantly lower in offspring with parental PTSD compared to offspring without parental PTSD (d = .92) and JCO. Emotional abuse and parental PTSD appear to be associated with low cortisol and risk for PTSD.
Yehuda et al., 2002	N = 39 HSO N = 15 JCO	Offspring cortisol levels significantly associated with sum of PTSD symptoms severity of father and mother combined (r= 0.40).	24-h Urinary cortisol levels in HSO were associated with parental PTSD symptoms (r= −.40) as much as with their own PTSD symptoms (r = −.47).
Yehuda et al., 2007a	N = 16 JCO N = 25 HSO	N= 12 HSO no parental PTSD N = 13 HSO + parental PTSD higher cortisol DEX suppression in HSO with parental PTSD than without parental PTSD d = 0.93) or JCO (d = 0.91) but not significant between HSO without parental PTSD and JCO	an association persisted between cortisol suppression and parental PTSD after controlling for childhood trauma and HSO own PTSD .r = −.35
Yehuda et al., 2007b	N = 33 HSO N = 16 JCO	N = 23 HSO with parental PTSD N = 10 HSO no parental PTSD The estimated mean ± SE plasma cortisol levels were 8.92 ± .41 μg/dL for JCO; 8.84 ± 0.52 μg/dL for offspring without parental PTSD; and with one 7.39 ± 0.44 μg/dL or two parents 6.97 ± 0.56 μg/dL with PTSD.	When the whole sample was considered, there was a significant association between mean cortisol levels and severity of parental PTSD (r42 = −0.41) that was reduced when only Holocaust offspring were considered (r26 = −0.39) and was further reduced to non-significance when examined in the smaller offspring subgroup with parental PTSD (r16 = −0.36). Offspring with maternal r = −.41 or paternal PTSD r = −.32 only however after additionally controlling for PTSD in the other parent only maternal PTSD retained significant association with HSO cortisol level (paternal r = −.21; maternal r = −.34).
Yehuda & Bierer, 2008b	N = 41 HSO N = 19 JCO	N = 6 only paternal PTSD and N = 16 no parental PTSD mean 24-h urinary cortisol level no significant difference. N = 9 both parents PTSD and N = 8 only maternal PTSD similar mean 24-h urinary cortisol and differed from no parental PTSD and JCO. HSO and maternal PTSD lower 24h urinary cortisol than without maternal PTSD (r = −.61); HSO without maternal PTSD trend lower level than JCO (r = −.17).	Significant negative association of maternal overprotection and PTSD with offspring mean cortisol (r = −.54).
Yehuda et al., 2014	N = 120 HSO N = 95 (75%) HSO both parents exposed n = 31 both parents PTSD n= 53 (55.8%) maternal PTSD; n = 43 (44.2%) paternal PTSD n = 11 only maternal PTSD; n = 11 only paternal PTSD; n = 31 no parental PTSD	In the absence of maternal PTSD, offspring with paternal PTSD only showed higher GR-1F promotor methylation, whereas offspring with both maternal and paternal PTSD showed lower GR-1F promotor methylation (d= .75; r = .35). GR-1F promotor methylation was negatively correlated with GR-1F expression (% methylation: r = −.35; number of methylated sites: r= −.36), indicating the validity of the GR-1F promotor methylation procedures.	Presence or absence of maternal PTSD moderated paternal PTSD effect on GR-1F promotor methylation. Only paternal PTSD higher GR-1F promotor methylation. Both parents PTSD lower GR-1F promotor methylation. HS both parents and without PTSD no effect of exposure or interaction between maternal and paternal exposure.
Yehuda et al., 2016	N = 32 survivor parents N = 22 HSO N = 8 JC parents N = 9 JCO	HS bin/3site 6 methylation correlated with HSO methylation at the same site (r = .44). Parental Holocaust exposure significant predictor of HSO bin/3site 6 methylation parental PTSD and FKBP5 risk-allele, childhood adversity and emotional abuse were not significant associated. FKBP5 methylation is seen in Holocaust survivors (higher than comparison) and their offspring (lower than comparison) on the same site in a functional intronic region of FKBP5 in the opposite direction (β= −.37).	No significant associations were found of the FKBP5 risk-allele with HSO own psychopathology, trauma-exposure or other examined characteristics that might independently affect methylation of this gene. Epigenetic changes were demonstrated (by changes in methylation levels) in two generations (HS and HSO) that were correlated (r = .44). After controlling for FKBP5 risk allele the association remained (r = .56), after regression bin 3/site 6 methylation parental Holocaust exposure remained significant (β = .42). Bin/3site 6 methylation Holocaust exposed correlated with HSO methylation at the same site, the presence of FKBP5 risk-allele in both generations did not substantially alter the association of bin 3/site 6 methylation between survivor and offspring (r = .44) or within Holocaust-exposed families (r = .56).

HSO = Holocaust survivor offspring; JCO = offspring of Jewish comparisons; 11β-HSD-2 = 11β-hydroxysteroid-dehydrogenase type 2; FKBP5 = FK506-binding-protein-5 gene; PBMCs = peripheral blood mononuclear cells; IC_50-DEX = concentration at which lysozyme activity is diminished by 50%; DST = dexamethasone suppression test.

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