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33
NATAN P.F. KELLERMANN
AbstrAct
The Holocaust le its visible and invisible marks not only
on the survivors, but also on their children. Instead of
numbers taooed on their forearms, however, they may
have been marked epigenetically with a chemical coating
upon their chromosomes, which would represent a kind
of biological memory of what the parents experienced.
As a result, some suffer from a general vulnerability
to stress while others are more resilient. Previous
research assumed that such transmission was caused
by environmental factors, such as the parents’ child-
rearing behavior. New research, however, indicates that
these transgenerational effects may have been also (epi)
genetically transmied to their children. Integrating both
hereditary and environmental factors, epigenetics adds a
new and more comprehensive psychobiological dimension
to the explanation of transgenerational transmission of
trauma. Specifically, epigenetics may explain why latent
transmission becomes manifest under stress. A general
theoretical overview of epigenetics and its relevance to
research on trauma transmission is presented.
Address for Correspondence: Natan P.F. Kellermann, AMCHA, POB 2930, Jerusalem 91029, Israel. natank@netmedia.net.il
Apparently, not only children of Holocaust survivors,
but ospring of other PTSD parents are also vulnerable
to such a burdensome legacy, including descendants of
war veterans (1), survivors of war trauma and childhood
sexual abuse, refugees, torture victims and many others
(2). Moreover, the transmission may continue beyond the
second generation and also include the grandchildren,
great grandchildren and perhaps others as well. is
process of transgenerational transmission of trauma (TTT)
has been repeatedly described in the academic literature
for more than half a century (3).
Generally speaking, TTT refers to the process in
which a trauma that happened to the rst generation
was passed on to the second generation. Such a process
is deeply connected with the general theme of hered-
ity – the transmission of characteristics from parents to
their ospring. Despite more than 500 studies published,
however, we are still unable to suciently explain exactly
how the unconscious trauma of a PTSD parent can be
genetically transmitted to a child and to verify this idea
with sucient empirical evidence. Such a notion evades
any simple and logical explanations. How can a repressed
memory be passed on from one person to another? Can
a child really “inherit” the unconscious mind of a parent?
Is it possible for a child to remember what the parent has
forgotten? Will we ever be able to produce “hard” neuro-
biological evidence of such far-fetched and preposterous
assumptions and perhaps see traces of the unconscious
trauma of a PTSD parent in a blood specimen or an MRI
scan of the child? Probably not. But even though we still
know very little about the level of specic inheritance of
trauma, new research indicates that traumatic experiences
of parents may indeed lead to a general disposition to
PTSD in the ospring. Family and twin studies have
found that risk for PTSD is associated with an underly-
ing genetic vulnerability and that more than 30% of the
variance associated with PTSD is related to a heritable
component (4). Perhaps this heritable component can
Some children of Holocaust survivors have terrible night-
mares in which they are chased, persecuted, tortured or
annihilated, as if they were re-living the Second World
War over and over again. At these times, they suer
from debilitating anxiety and depression which reduce
their ability to cope with stress and adversely impact
their occupational and social function. It seems that
these individuals, who are now adults, somehow have
absorbed the repressed and insuciently worked-through
Holocaust trauma of their parents, as if they have actually
inherited the unconscious minds of their parents.
Epigenetic Transmission of Holocaust Trauma:
Can Nightmares Be Inherited?
Natan P.F. Kellermann
AMCHA, the National Israeli Center for Psychosocial Support of Survivors of the Holocaust and the Second Generation, Jerusalem, Israel
Isr J Psychiatry Relat Sci - Vol. 50 - No 1 (2013)
34
EPIGENETIC TRANSMISSION OF HOLOCAUST TRAUMA: CAN NIGHTMARES BE INHERITED?
be observed in the epigenetic marks that aect gene
expression patterns in the nervous system?
Four major theoretical approaches to understanding
trauma transmission have been earlier suggested by
Kellermann (5): (1) psychodynamic relational models
(6); (2) sociocultural and socialization models (7); (3)
family systems and communication models; and (4)
biological or genetic models. Children are of course
inuenced by their parents in a variety of ways, either
through upbringing or heredity, or through both (8) and
such an integrative view of trauma transmission seems
to make perfect sense. Upon further inspection however,
these theories are too general to suciently explain the
specic process of how the impact of trauma can cross
generations and how social and biological inuences
interact to produce TTT.
As emphasized by Jablonka and Lamb (9), genetic mech-
anisms alone cannot explain how some cellular traits are
propagated and heritable changes in gene expression and
regulation that have little to do with DNA sequence seem
to be more relevant to explain TTT. Any theory explaining
transgenerational transmission of trauma must therefore
take into account the powerful hereditary variations which
would explain how parental trauma may be biologically
passed on to the child before birth. ese theories should
explain how children who have not themselves been trau-
matized tend to manifest inherited emotional problems.
Even though empirical data are still poor in com-
parison to the ideas presented here and my assump-
tions may sound bold, speculative and unfounded at this
point in time, I suggest that epigenetics may introduce
a promising new and more comprehensive explanatory
variable of TTT than the earlier ones. Since it includes
both hereditary and environmental factors, it may add
a signicant psychobiological dimension which could
conrm clinical observations with empirical research.
e purpose of this paper is therefore to explore what
epigenetics can teach us about TTT and to review some
of the prevalent empirical research in this eld. Finally, I
will show how the inclusion of epigenetics would explain
some of the discrepant ndings from previous research on
the transgenerational transmission of Holocaust trauma.
EpigEnEtic trAnsmission
More than two centuries ago, the founder of evolution,
Jean-Baptiste Lamarck, suggested that acquired char-
acteristics may be transmitted from one generation to
another. Ever since, evolutionary developmental biology
has continued to study this assumption. Recent advances
in the eld of epigenetics are now revealing a molecular
basis for how heritable information other than DNA
sequence can inuence gene function (10, 11). ese
advances may add greatly to our understanding of trauma
transmission and may even establish a promising new
research paradigm in the eld, as recently pointed out by
Yehuda and Bierer (12): “Epigenetic modications, such
as DNA methylation, can occur in response to environ-
mental inuences to alter the functional expression of
genes in an enduring and potentially, intergenerationally
transmissible manner. As such, they may explain inter-
individual variation, as well as the long-lasting eects
of trauma exposure. Although there are currently no
ndings that suggest epigenetic modications that are
specic to posttraumatic stress disorder or PTSD risk,
many recent observations are compatible with epigen-
etic explanations” (p. 427). Naturally, various questions
remain regarding such assumptions, and we still know
too little about where to draw the line between PTSD
based on a single traumatic event, complex and chronic
PTSD, as well as individuals who have largely overcome
their responses to overwhelming stress.
Epigenetics is typically dened as the study of heritable
changes in gene expression that are not due to changes in
the underlying DNA sequence. Such heritable changes in
gene expression oen occur as a result of environmental
stress or major emotional trauma and would then leave
certain marks on the chemical coating, or methylation,
of the chromosomes (13). e coating becomes a sort
of “memory” of the cell and since all cells in our body
carry this kind of memory, it becomes a constant physi-
cal reminder of past events, our own and those of our
parents, grandparents and beyond. “e body keeps the
score” (14), not only in the rst generation of trauma
survivors, but possibly also in subsequent ones. Because
of their neurobiological susceptibility to stress, children of
Holocaust survivors may thus easily imagine the physical
suering of their parents and almost “remember” the
hunger, the frozen limbs, the smell of burned bodies
and the sounds that made them scared.
In the same way as parents can pass on genetic charac-
teristics to their children, they would also be able to pass
on all kinds of “acquired” (or epigenetic) characteristics,
especially if these were based on powerful life-threatening
experiences, such as survival from starvation, torture or
persecution. Such environmental conditions would leave
an imprint on the genetic material in eggs and sperm
and pass along new traits even in a single generation.
35
NATAN P.F. KELLERMANN
Such an explanation of TTT can be described in com-
puter terminology in which the genome would represent a
kind of hardware that remains xed, while the epigenome
would represent the variable soware with all the memory
les. e epigenome thus would function like a “switch,”
which has the inherent ability to turn certain functions
“on” or “o.” From such a point of view, ospring of
trauma survivors would be somehow “programmed”
to express a specic cognitive and emotional response
in certain dicult situations. In eect, these children of
PTSD parents would be suering from a kind of “soware
bug,” an error in a computer program or system that
produces incorrect or unexpected results, or causes it to
behave irrationally. is bug would for example switch
on a panic attack and instruct the genes to prepare for
“ght and ight” when triggered, as if the individual were
thrown into a Nazi persecution manuscript of catastrophic
proportions, even in a relatively non-threatening situa-
tion. Metaphorically, such an epigenetic coating would
aect the child of survivors in a way which is similar to
a computer infected with a malicious virus, a malware
that inicts harm at certain unpredictable points in time.
Any such explanation in epigenetic terms of how
the Holocaust trauma can “run in families” must rst
show that the PTSD parent was somehow “damaged”
with some kind of brain short-circuit or constitutional
“PTSD bug” and then demonstrate that the child was
born with this same “bug.” Among children and grand-
children of Holocaust survivors as well as ospring of
other traumatized populations, this “bug” would be
manifested as a latent susceptibility to (secondary) PTSD
and would cause increased vulnerability to stress under
certain conditions, such as when a new stress becomes
the trigger to a past traumatic event. At such times the
epigenetic switch would turn the survival strategy “on”
and activate a specic neuro-biological response. Initially,
most aected ospring would not be aware of its origin
or even of its existence until a new trauma occurs, and
then be surprised that some old trauma of the parents
would suddenly be surfacing.
If any specic past memory can be epigenetically trans-
mitted or not, however, must be le open to speculation
and we should be careful not to slip from reasonable
assumptions to fantastic and unsupported scenarios.
While a general tendency for having frightening night-
mares may well be epigenetically transmitted, and the
persecution nightmares of children of Holocaust survivors
may be colored by their Holocaust imagery, we are obvi-
ously still unable to show that the content of a specic
nightmare is aected by epigenetic marks transmitted in a
reproductive cell or in the womb. Eva Jablonka (personal
communication) writes: “We have good reasons to believe
that epigenetic marks can be inherited between genera-
tions, including marks that aect gene expression patterns
in the nervous system. Of course, we need evidence that
this actually happens in the case of human PTSD, but
we do know that the eects of psychological stress are
inherited in mice and rats. It would therefore not surprise
me if we nd out that the disposition to PTSD is inherited
via an epigenetic route, and that traumatic experiences
of parents lead to extra-sensitivity to traumatic inputs in
ospring, and this may linger for some generations. If the
eects of trauma are inherited we shall have to nd out
for how many generations (this may vary, depending on
genetic background, type of trauma, and the persistence
of traumatic experiences) and whether the eects make
the descendants more prone to develop PTSD. Even if the
disposition to develop PTSD is found to be increased in
descendants, it is important to emphasize that the specic
trauma is unlikely to be inherited. So the fact that children
of Holocaust survivors dream of the Holocaust was not
transmitted through gametic epigenetic inheritance (as
a mark on the chromosomes of the parental sex cells).
What could have been inherited is the disposition to
have nightmares, and of course if they know something
about the Holocaust through primary exposure, from
stories and so on, the nightmares will take this form.
What we know about epigenetic marks is that they can
dispose one towards developing some behaviors, but the
specic behavior depends on specic inputs the person
gets in its own lifetime.”
EpigEnEtic rEsEArch
e eld of epigenetics is becoming increasingly more
accepted by the scientic community and there has been
a large increase in studies conducted during the last
decade. A comprehensive review of more than hundred
studies of transgenerational epigenetic inheritance was
compiled by Jablonka and Raz (15) who described the
phenomena in a wide range of organisms, including bac-
teria, plants and animals. ese studies included various
kinds of adverse conditions, early stress and “emotional
trauma” of the “rst generation” which altered the gene
expression in the subsequent generations. Reik, Dean
and Walter (16) also reviewed what is known about
reprogramming in mammals and discussed how it might
relate to developmental potency and imprinting. More
36
EPIGENETIC TRANSMISSION OF HOLOCAUST TRAUMA: CAN NIGHTMARES BE INHERITED?
recently, Franklin et al. (17) showed that chronic and
unpredictable maternal separation induces depressive-like
behaviors, not only in the rst generation of mice, but
also in their ospring. Empirical evidence of epigenetic
transmission in human beings, however, is very scarce
because of the diculties in gathering relevant data from
human as compared to animal subjects. Some of these
will be summarized here briey.
One of the rst epigenetic studies on human beings
was carried out by Bygren et al. (18) in Överkalix in
Northern Sweden. He found that overeating as a youngster
could initiate a biological chain of events that would lead
one’s grandchildren to die decades earlier than their
peers did (19). us it was shown – perhaps for the rst
time – that a famine or overeating at critical times in the
lives of the grandparents could inuence the life expec-
tancy of the grandchildren. In their eorts to replicate
this astounding nding, Pembrey et al. (20) conducted
another transgenerational study which showed that sons
of men who smoke in pre-puberty were found to be at
higher risk for obesity and other health problems than
sons of non-smoking fathers. Much later, a series of
unique post-mortem studies on the brains of men who
had committed suicide in Canada (21) found that the
chemical coating on genes seem to have been inuenced
by exposure to childhood abuse.
Additional indirect evidence came from the Dutch
Famine Birth Cohort study (22) who concluded that
exposure to acute, severe famine during pregnancy alters
the distribution of birth weights of both the women born
at the time of the famine and, through a phenotypic
response, that of their own ospring. Even though it is
clearly dicult to separate phenotypic (i.e., potentially
modiable) and genotypic (i.e., immutable) eects across
generations, the complex mechanisms by which trans-
generational transmission of stress responsiveness occur
are rapidly becoming a focus of investigation (23). Rachel
Yehuda and her team from the Mount Sinai School of
Medicine have been at the forefront of this research for
more than a decade (24). Having found that parental
PTSD appeared to be a relevant risk factor for the develop-
ment of PTSD in adult ospring of Holocaust survivors
with PTSD, Yehuda and Bierer (25) summarized recent
neuro-endocrine studies in ospring of parents with
PTSD. ese studies indicated that ospring of trauma
survivors with PTSD had signicantly lower urinary
cortisol excretion and salivary cortisol levels as well as
enhanced plasma cortisol suppression than ospring of
survivors without PTSD. In all cases, neuro-endocrine
measures were negatively correlated with severity of
parental PTSD symptoms, even aer controlling for
PTSD and other symptoms in ospring.
ough the majority of their work focused on adult
ospring of Holocaust survivors, more recent observa-
tions in infants born to mothers who were pregnant
on 9/11 demonstrated that low cortisol in relation to
parental PTSD appears to be present early in the course
of development and may be inuenced by gluco-corticoid
programming in unborn children. Lower cortisol lev-
els were found in mothers who developed PTSD aer
exposure to the attacks on September 11 compared with
similarly exposed mothers who did not develop PTSD
(26). Pregnant women, who had been close to the World
Trade Center on September 11th, 2001, gave birth to
babies who had elevated levels of stress agents in their
saliva (27-29). ese data suggest that eects of mater-
nal PTSD on cortisol can be observed very early in the
life of the ospring and highlight the in utero eects
as contributors to biological risk factor for PTSD (30).
Since low cortisol levels are particularly associated with
the presence of maternal PTSD, the ndings suggested
the involvement of epigenetic mechanisms. In a more
recent study on combat war veterans with and without
PTSD, this line of research was continued and the PTSD+
group again showed greater cortisol and ACTH sup-
pression (31, 32).
In an early study of maternal Hypothalamic-Pituitary-
Adrenal Axis (HPA-axis) functioning, Schechter et al.
(33) measured maternal salivary cortisol within a clini-
cal sample of mothers before and aer a mother-child
interaction protocol involving separations and reunions.
e study showed modest, but signicant associations
between pre-separation cortisol as well as cortisol reac-
tivity with the severity of maternal PTSD, dissociative
symptoms, and atypical care giving behavior. Later studies
of gene environment interactions focused on environ-
mental stressors such as interpersonal violence and the
regulatory eects of the serotonin transporter gene and
other genes with which it is known to interact on the
HPA axis (34).
Apparently, parenting itself may be epigenetically
transmitted from parent to child. In a fascinating study
of gene-environment interaction, Beaver and Belsky (35)
recently found a signicant interaction between parenting
quality and cumulative genetic plasticity in the predic-
tion of parental stress during adulthood. Depending on
genotype, parenting quality was thus shown to dieren-
tially aect future parental stress. Exposure to maternal
37
NATAN P.F. KELLERMANN
parenting was measured prospectively when respondents
were adolescents and parental stress was measured when
they were parents themselves, some 14 years later. Some
genes that seem to aect neural plasticity were shown
to be involved and the variation in these genes aected
parental behavior and the response to stressful parenting.
Finally, a range of dierent neurotransmitters have
been investigated, from serotonin and dopamine to
neuro-peptide Y, brain-derived neuro-trophic factor,
and the gluco-corticoid receptor in the predisposition
to PTSD. In their review of molecular genetic studies
relating to PTSD, Broekman, Ol and Boer (36) found
inconsistent results among eight major genotypes: sero-
tonin (5-HTT), dopamine (DRD2, DAT), gluco-corticoid
(GR), GABA (GABRB), apolipoprotein systems (APOE2),
brain-derived neuro-trophic factor (BDNF) and neuro-
peptide Y (NPY). According to Binder et al. (37), several
single-nucleotide polymorphisms (SNPs) in FK506 bind-
ing protein 5 (FKBP5) interact with childhood trauma to
predict severity of adult PTSD. ese ndings suggest that
individuals with these SNPs who are abused as children
are more susceptible to PTSD as adults (38).
As can be seen from the above examples, the potential
for creative research in this eld is huge. However, though
it is widely accepted that epigenetic factors can play an
important role in the development and transmission of
PTSD, “there have been no empirical demonstrations of
epigenetic modications per se in association with PTSD
or PTSD risk” (12, p. 430). Uncovering the heritable
biomarkers that are involved in TTT would thus be an
important task for future research.
Many years of brain research has shown that human
beings are “hard-wired” for stress through an intricate
pattern of neural pathways designed for the ght-or-
ight response. Research also suggests that chronic stress
appears to destroy brain tissue, specically the hippo-
campus and much of research on the fear response in
humans has focused on the activating of the amygdala
in subjects with PTSD (39).
Intergenerational eects related to PTSD and HPA-axis
stress reactivity are also likely via epigenetic mecha-
nisms (26). New techniques are investigated to search the
genome or gene modications that have been identied
as epigenetic risk factors. But while the majority of the
initial investigations into main eects of candidate genes
hypothesized to be associated with PTSD risk have been
negative (40), promising avenues of inquiry into the role
of epigenetic modications have been proposed and future
studies of PTSD epigenotypes may help to elucidate the
neurobiology of inherited PTSD. Epigenomic studies
that look at patterns of methylation in many loci and
particularly on candidate genes are presently conducted
in various places. Similar to the Human Genome Project
(41), a new public/private collaboration has initiated
a Human Epigenome Project which aims to “identify,
catalogue and interpret genome-wide DNA methylation
patterns of all human genes in all major tissues” (42).
is project is searching for a particular form of a gene
variation on a specic chromosome which makes some
people more likely to develop PTSD than others. While
simplied biological models may not properly capture
the complex etiology of PTSD (43), and though studies
of genotype may only present a limited picture of the
molecular biology of this disorder, there seems to be a
clear rationale for examining genetic factors in PTSD in
conjunction with environmental factors, such as trauma
exposure. e examination of epigenetic mechanisms
together with gene expression might help rene models
that explain how PTSD-risk and recovery are mediated
by the environment (32).
conclusion
Presenting such veriable data of TTT would have far
reaching consequences. First of all, it would continue
to reinforce the paradigm shi in scientic thinking
that underscores the impact of stressful events on the
physiology not only of the trauma survivors themselves,
but also of their ospring (23). Furthermore, improved
understanding of epigenetic transmission of PTSD in
children of trauma survivors would allow a more accurate
diagnosis, improved prevention and more targeted treat-
ment interventions of such clients, possibly leading to
a sort of “epigenetic medicine” (44). Specic epigenetic
therapies could hold promise for a wide range of biological
applications, from cancer treatment to the development
of induced stem cells (45), as well as for a more targeted
treatment of TTT. Finally, any such veriable data of
trauma transmission would have legal consequences for
generations of trauma survivors who may want to claim
reparation for their epigenetically inicted wounds.
Most importantly, however, new epigenetic data have
the potential to settle some controversies from previ-
ous research. Recent overviews of such research (46-49)
concluded that the contrasting forces of vulnerability
and resilience were both present in Holocaust survivors
and their children. But how did the rst generation of
severely traumatized survivors achieve so much, and how
38
EPIGENETIC TRANSMISSION OF HOLOCAUST TRAUMA: CAN NIGHTMARES BE INHERITED?
can their children function so well when bearing such a
heavy burden? And how can we explain that ospring
who came to psychotherapy complained so much about
various kinds of secondary traumatization eects, while
epidemiological studies repeatedly failed to show that they
were any dierent from comparable populations? Clinical
observations and controlled research were consistently
divided in their assessment of this population for many
decades. With the added use of epigenetics, however, this
dispute becomes much more reconcilable. Epigenetic trans-
mission models make the discrepant ndings regarding
the presence or absence of specic psychopathology as well
as the simultaneous presence of both frailty and hardiness
in this population much more explicable. Because from
the point of view of epigenetics, any inherited (genetic)
dispositions can be either turned on or o, and thus acti-
vate either overwhelming anxiety or sucient coping in
the same person at dierent times, according to certain
aggravating and mitigating (environmental) factors (3).
As emphasized by Yehuda and Bierer (12), “integrating
epigenetics into a model that permits prior experience to
have a central role in determining individual dierences is
also consistent with a developmental perspective of PTSD
vulnerability” (p. 432).
Finally, epigenetics opens up a potentially more
optimistic view of health and disease in ospring of
trauma survivors. Since epigenetics conveys that human
beings are not only predestined, but also highly malleable
creatures, they are able to reverse the deleterious eects
of trauma and nd some closure to the endless multi-
generational saga. is may be achieved either through
a variety of established psychotherapeutic interventions
or through new psycho-pharmacological drugs, or a
combination of both. Even though such ospring might
still be more or less inuenced by their genes and despite
their physiological predestination, they might realize
that it’s up to them to decide what to do with all of it.
Instead of succumbing to the emotional eects of the
past tragedies, they might search and nd some kind of
personal transformation journey that gives new meaning
to their legacy.
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