Hansen Tang

To recognize the role epigenetics in resilience after trauma, in both individuals who experience trauma and their descendants.

After participating in this activity, you should be better prepared to:

1. Understand how various mechanisms of epigenetics can potentially contribute to transgenerational transmission of resilience.

2. Discuss the various interpretations of the American Psychiatric Association’s definition of resilience.

3. Review the different treatment modalities that could prevent transmission of trauma.

4. Understand the potential variables that either strengthen or weaken an individual’s resilience and positive health outcomes.

This continuing education (CE) activity is intended for psychiatrists, psychologists, primary care physicians, physician assistants, nurse practitioners, and other health care professionals who seek to improve their care for patients with mental health disorders.

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 The fear, grief, social isolation, and loss associated with COVID-19 are all potentially traumatic. The ongoing pandemic makes the study of resilience mechanisms after catastrophic experience all the more timely, since what is true for the pandemic experience may be true for any traumatic experience that causes long-term isolation and helplessness. Based on the epigenetic mechanisms that promote transgenerational transmission of resilience, a growing body of research points the way to promising clinical and public health interventions. By applying what we are learning about the potential biopsychosocial mechanisms for transgenerational resilience, we can begin to design interventions to promote resilience, study their relative effectiveness, and implement them accordingly.

, approximately 70% of people worldwide will experience at least 1 traumatic event during their lifetimes, with 30.5% reporting more than 4 incidents.

 (PTSD) or other trauma- and stressor-related disorders.

 Traumatic events such as threats to one’s life, natural disasters (including the current pandemic), exposure to war and conflict, torture, discrimination, and decimation of communities serve as brutal reminders of our past. However, a clear resilience to such stressors enables the individual to thrive in spite of hardship and social isolation, as well as to endure the memories of these ordeals. The offspring of such survivors have been shown to thrive and they are often better adapted and more resilient than the previous generation.

 Awareness of potential epigenetic mechanisms may help to guide clinical and public mental health interventions to ensure that future generations are better equipped to avoid trauma- or stressor-related disorders.

Epigenetics is the study of heritable changes that occur without directly altering the nucleotide sequence of a genome. Various epigenetic processes function to determine an individual’s phenotype and control the expression of various proteins and their corresponding functional pathways. Epigenetic mechanisms of transmission include CpG islands (sites in the genome containing large numbers of CpG dinucleotide repeats), histones, and noncoding RNA. Methylation, the process of adding or removing a methyl group (–CH

), can occur at CpG islands and on histone proteins. In addition, histones can be altered in a variety of other ways, including acetylation, ubiquitination, phosphorylation, and the addition or removal of various sugars. These modifications alter the capacity for further transcription factors to express a gene.

Exposure to traumatic events can produce long-term epigenetic changes in consistent regions of the genome. 

 during episodes of trauma have long-term effects on glucocorticoid receptors, adipose tissue, the hypothalamic–pituitary–adrenal (HPA) axis, hippocampus, and amygdala.

 A combination of these factors may influence not only an individual’s own phenotype, but also how that individual and their offspring will respond to further stressors in life.

The ability to transmit epigenetic changes caused by trauma has been seen within both 

 Studies by Suter et al showed that plants such as 

 such as DNA methylation induced by life-threatening heat stress over 3 consecutive generations.

 Migicovsky et al found that when the first-generation (F

 were exposed to the same heat-induced stress as the parental generation, there was a significant decrease in the amount of global DNA methylation. The 

 developed larger leaves than the control group but became more resistant to further methylation, despite exposure to the same external stressor as the parental generation.

 Other studies have shown that various sites of 

Animal models using rodents have also shown consistent patterns of transmission across multiple generations. Dias and Ressler showed that rodents conditioned with a fear response to acetophenone gave birth to F

 (second-generation) offspring exhibiting similar fear behaviors. They determined that a persistent CpG hypomethylation of the 

 Exposure to social stressors has led to impaired rodent maternal behaviors across several generations, leading to offspring that consistently produce 

abnormal amounts of cortisone, oxytocin, and prolactin

 These findings are consistent with hormonal changes in human families who experienced similar 

Resilience is often cited as a key factor in preventing adverse changes in personality or affect in reaction to stressors experienced in one’s life.

 The American Psychiatric Association (APA) 

 as the ability to adapt in the face of adversity, trauma, tragedy, threats, or significant stress.

 Various interpretations of the APA’s definition have included an absence of psychopathology, an ability to return to homeostasis unimpaired by the traumatic event, or adaptive responses after exposure to adversity.

Some researchers have highlighted a combination of core, internal, and external resilience factors that can also contribute to how one succeeds in life.

 Core resilience is largely defined by one’s genome. Internal resilience, on the other hand, is distinguished by learned and shared behaviors that can be influenced by family, friends, and life experiences. These involve the development of healthy behaviors such as autonomy, self-control, hardiness, toughness, coping style, past experiences, resourcefulness, social competence, and grit. External resilience focuses primarily on socioecological factors, such as support from one’s community and access to social and health care services. Recognizing the different ways in which resilience can manifest and understanding these manifestations in multifactorial terms is the best method of combating and resisting traumatic adversity.

 Standardizing measures of resilience and change with respect to trauma has, however, proven to be difficult across disparate events, populations, and generations.

One measure of the impact of trauma on an individual is posttraumatic growth (PTG), which was defined in 1996 by Tedeschi and Calhoun to describe 

 Key components of affect were divided into 5 categories to measure and compare positive change due to trauma in various populations (

Table. Potential Positive Posttrauma Changes

 in a longitudinal study of 200 Israeli prisoners of war during the 1973 Yom Kippur War. Forty-three male Israeli combat veterans were second-generation survivors of the Holocaust. Dekel measured changes in PTG among both groups of veterans, with data sets collected at 30 and 35 years after the end of the war. The study found that veterans who were offspring of Holocaust survivors scored lower on PTG and had a lower likelihood of developing PTSD than veterans in the control group. A lower score on PTG as well as PTSD symptoms may indicate resilience to change as a result of trauma, whereas the effects of trauma may have been more pronounced in the control group (who were not offspring of Holocaust survivors). Whether a genetic component was responsible was not clear, but the authors proposed it as an area of further study.

Our genome and epigenetics may provide explanations of human resilience in the face of trauma. For example, the FK506-binding protein 51 (FKBP5) is a biomolecule that appears to modulate our reaction to stress and ability to exhibit resilience. The 

 for glucocorticoid receptors on chromosome 6 (6p21.31).

 Research has shown that behavioral responses to stress are 

—as is the HPA axis—and can be affected by factors such as exposure to trauma.

 In animal studies, mice with the gene for 

 removed show a stronger resilience to stressors by exhibiting a lowered fear response.

In another study of Holocaust survivors, 

 looked at the epigenetic mechanisms of transmission of the 

 gene, focusing primarily on DNA methylation of the CpG sites located in and proximal to intron 7 of 

 Methylation of bin 3/site 6 was found to be 10% higher in Holocaust survivors, but methylation of the same bin 3/site 6 was 7.7% lower in the offspring of Holocaust survivors than in the control groups. These findings were consistent when controlling for lifetime PTSD in the offspring and for possible childhood trauma. The 30-year age difference between the parents and their offspring could explain the differences in methylation; however, Yehuda et al noted that even a 1% to 2% difference in gene methylation can significantly alter gene expression.

 Furthermore, the study of Miller et al showed that methylation of specific CpG sites of 

 Greater methylation of the CpG site cg07485685 decreased PTSD symptom severity while increasing resiliency scores measured via the Brief Resilience Scale. A PTG inventory was also used to measure any positive changes as a result of trauma. Lower levels of PTG after trauma were associated with methylation of the same CpG site cg07485685 on

. These findings are consistent with the lower scores on PTG and lower levels of PTSD found in the study of Dekel et al in 2013.

Genes that are responsible for regulation of the HPA axis may also confer resilience to trauma. For example, multiple studies have found that childhood trauma and mistreatment are a risk factor for methylation of the human glucocorticoid receptor (NR3C1) gene and changes to the HPA axis.

 in newborn infants has been linked to prenatal exposure to stress.

 For instance, Perroud and colleagues examined the epigenetic changes in pregnant Tutsi survivors of the Rwandan genocide and their offspring. The mothers and their offspring were found to have 

Variations in single-nucleotide polymorphisms (SNPs), specifically rs10482672, were also found to increase the risk of psychopathology. 

 found that children who were identified as having this genotype were more vulnerable to developing substance abuse and antisocial behavior under adverse conditions, but at the same time were more likely to benefit from advantageous conditions.

 Children were placed in a fast-track program, which fostered the development of emotional regulation, self-control, and other treatments to minimize the effects of harsh parenting and violent environment. Those who received early intervention to reduce risks of developing psychopathology had a significantly decreased risk of external psychopathology via substance abuse or antisocial behavior later in life. Those in the control group, who had SNP rs10482672 but did not receive early treatment, had a higher likelihood of external psychopathology by the time they reached 25 years of age.

 In 2020, Miller et al also found methylation of 5 CpG sites in the 

 gene that were significantly linked with resilience.

 Three CpG sites were correlated with an increased score (indicating higher resilience) on the Brief Resilience Scale, whereas 2 CpG sites were correlated with decreased resilience. Authors in all studies noted the need for larger sample sizes as well as additional longitudinal studies.

What can be done to prevent transmission of past trauma to future generations? Studies have shown that nonpharmacological treatment of trauma- and stressor-related disorders can induce epigenetic changes in the genome responsible for the HPA axis.

 Roberts et al examined the methylation of 

 before and after exposure-based cognitive behavioral therapy (CBT) in patients previously diagnosed with agoraphobia. Those who reported benefits from CBT after completing treatment were found to have lower levels of methylation at a CpG island at intron 7 of 

. The severity of symptoms was reduced by an average of 69.5% in those who received exposure-based CBT, which correlated with the decrease in methylation. Individuals who reported little change from CBT were found to have either no significant changes or even increases in methylation of CpG islands at intron 7 of 

Bishop et al found similar results in patients with PTSD who received mindfulness-based stress reduction interventions. These patients showed levels of methylation of intron 7 of 

 significantly different after intervention compared with initial levels. Those who responded to treatment, as indicated by a 10-point drop in PTSD severity via a PTSD checklist, had 

significantly decreased levels of methylation

, whereas those who did not respond to treatment showed higher levels of methylation in a different site at bin 2 of 

 Mindfulness and techniques that encourage thought and understanding, such as CBT and storytelling, might 

Figure 1. Factors predictive of resilience from trauma and social isolation

Family and community play a strong role in enhancing an individual’s resilience. 

Fundamental building blocks for resilience

 include a secure foundation and promotion of self-esteem and self-efficacy.

 Strong bonds with caregivers and shared values and religious beliefs that find meaning in suffering are protective against adverse effects of trauma in children. Longitudinal studies of the effects of social relationships have found that support from family, friends, colleagues, and community leaders leads to a reduction in psychological distress, as well as a more rapid recovery from the effects of trauma.

Likewise, the World Health Organization has found that the arts have contributed to the improvement of public health. Music, art, dance, and communication through storytelling about past events at an early age not only reduce anxiety but also protect against cognitive decline later in life. Exposure to and involvement with the arts “trigger psychological, physiological, social, and behavioral responses” associated with positive health outcomes that may be linked to 

Exercise has long been associated with various health benefits and has been documented to be valuable for regulating reactions to stress, sleep, and resilience to mood disorders.

 In animal models, exercise serves a protective role in lowering the rates of 

 Mice who exercised via long-term wheel running had increased levels of galanin, a neuropeptide that has been 

 as well as the regulation of norepinephrine and other products of the HPA axis.

 in mice was also consistent with a significant increase in stress resilience, inducing methylation of 

 and downregulating noncoding RNA such as microRNA-124 in areas such as the hippocampus.

 Epigenetic changes as a result of exercise improved cognition in the mice of the parental generation as well as subsequent offspring.

 have correlated with findings in human studies, as mothers who exercised regularly before and during pregnancy had offspring who achieved higher levels of academic performance, excelling in language and math and having higher overall grade point averages.

 Other factors, such as shared environments and positive parental influences, may have played a part in the success, but they do not account for epigenetic differences in DNA seen at birth. Regular moderate exercise seems to confer a protective effect that enables future generations to adapt to and thrive in their new world.

Patients diagnosed with trauma- and stressor-related disorders show evidence of dysregulation of their HPA axis, resulting in persistent personality changes.

 The diagnosis of Enduring Personality Change After Catastrophic Experience (EPCACE) is defined as an enduring personality change lasting at least 2 years that a patient experiences following a catastrophic stressor (ICD-10). Thus, the presence or absence of a diagnosis of EPCACE may serve as a predictive factor for resilience and vulnerability in the face of trauma.

 Long-lasting epigenetic changes may present themselves as enduring 

 Those diagnosed with EPCACE often are socially isolated, fearing the stigma of their suffering. This may lead to a vicious cycle by which epigenetic effects are compounded and changes further solidified until a persistent and permanent change in personality has taken place (

Figure 2. Compoundinig Effects of Trauma and Isolation on Worsening Physical and Mental Health

As the COVID-19 pandemic waxes and wanes and the fear, grief, and stress of the pandemic itself and preventive social isolation measures take their toll, it is paramount that we identify the most trauma-vulnerable patients and populations early on. Individuals 

 and other trauma-related disorders are heritably linked to autoimmune diseases, dementia, schizophrenia, bipolar, and major depressive disorders.

 Chronic stress and isolation continue to be correlated with increased risks for anxiety and depression, leading to higher rates of infection and early mortality.

Fortunately, those who are most vulnerable to isolation and demoralization are often most likely to benefit from preventive intervention,

 the need for which is all too evident in our current circumstances. At the same time, there is a lack of transgenerational studies of, and a dearth of instruments to reliably study, the effectiveness of interventions to promote resilience in communities.

With the COVID-19 pandemic coming to an end, it is time to apply what we know about potential biopsychosocial mechanisms for transgenerational resilience in order to design alternative interventions to promote such resilience. We can then study the relative effectiveness of such interventions and support those that are most effective, in keeping with considerations of social justice and equity. Otherwise, even as we win the battle to defeat COVID-19, we may lose the transgenerational war to 

is a second-year medical student at Pacific Northwest University Health Sciences. 

is an assistant professor of psychiatry in the Oregon Health & Science University (OHSU) School of Medicine.

is the cofounder of the Program in Psychiatry and the Law at Harvard Medical School and President of the American Unit of the UNESCO Bioethics Chair (Haifa). He is the coauthor of

 Medical Choices, Medical Chances: How Patients, Families, and Physicians Can Cope with Uncertainty 

(1981/1990). He practices clinical and forensic psychiatry and risk management in Cambridge, Massachusetts.

The authors thank Raquelle Mesholam-Gately, PhD, and Anthony Cunningham, PhD, for their thoughtful reading of an earlier draft.

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Articles

How can we begin to design interventions to promote resilience, study their relative effectiveness, and implement them accordingly?

Transgenerational Transmission of Resilience After Catastrophic Trauma

Any psychiatric diagnosis has the potential for empowering the clinician to treat the patient’s suffering as well as inspiring the patient to participate in an effective treatment. Alas, diagnosis also has the potential for stigmatization and dehumanization. Whereas diagnoses of personality disorder all too often have been used to stigmatize patients, the rush to eliminate Enduring Personality Change After Catastrophic Experience (EPCACE) from the International Statistical Classification of Diseases, Revision 11 (ICD-11) is foreseeably an instance in which patients vulnerable to aloneness will be less likely to receive effective treatment and thus will become even more voiceless, further disempowered, and more vulnerable to humiliation throughout the life cycle’s inevitable stressors and losses.

EPCACE was incorporated into ICD-11 as a form of Complex PTSD (cPTSD) as of June 2018. EPCACE is defined as an enduring personality change lasting for a minimum of 2 years that a patient experiences following a catastrophic stressor (ICD-10). The events of the stressor must also be so extreme that one should disregard any genetic vulnerabilities or predispositions that would further influence personality changes. These experiences can include imprisonment in concentration camps, disasters, and long-lasting capture with a persistent threat to life.

ICD-10 EPCACE represents the experiences of a particularly vulnerable population group, one marked by great loss, separation from a community, and aloneness. Such isolation from nourishing connections is a major dimension of deep and enduring personality change. Especially in cases of massive psychic trauma such as the Holocaust, involving the loss of an entire community and its way of life, fundamental bonds of social connection, trust, and support are broken, and the individual is left profoundly alone. Such affective changes point to the insufficiency of research on survivors left in such a devastated state.

We acknowledge that there is great variability in the experience and suffering of survivors of catastrophic events. As with any clinical diagnosis, a diagnosis of EPCACE is no substitute for a formulation tailored to the needs of the individual patient and that patient’s family. An EPCACE-based formulation can highlight such factors as extreme helplessness and aloneness, whether human agency was the cause of the catastrophic event, whether the event involved humiliation of the survivor, and whether the survivor remained in the zone of danger after the catastrophic event. These factors may be evident both individually and transgenerationally, as they are in the suffering of some of the survivors of the Holocaust who remained in areas where anti-Semitism and its dangers continued to be prevalent.

With careful attention to individualization of formulation, there is evidence for the benefits of EPCACE being included in the next revision of DSM as its own unique diagnosis. While care needs to be taken to avoid a reductionist and dehumanizing misuse of the diagnosis of EPCACE, the presence of this diagnosis in standard diagnostic taxonomies of psychiatric disorders can guide treatment formulations to good effect. Furthermore, EPCACE is an integrative diagnosis that offers clinicians the capacity to transcend diagnostic categorization by bridging personality disorder with trauma-related disorder, fulfilling an integrated biopsychosocial approach.

Our proposal has strong historical precedent. By 1992, the concept of trauma-inflicted personality changes had been well studied, as described by Herman and colleagues

 and later confirmed by many others, including Beltran and Silove,

 In an effort to distinguish personality changes as a result of catastrophic events from those with other causes, the ICD-10 task force decided on the inclusion of EPCACE. Personality traits such as hostile or distrustful attitude toward the world and social withdrawal, chronic feelings of emptiness or hopelessness, of being on edge as if constantly threatened, and estrangement distinguished EPCACE from related disorders.

With catastrophic genocidal trauma that includes extreme helplessness, humiliation, and the destruction of a validating community, resulting in aloneness, there is also a potentially lifelong vulnerability to shame.

 Such personality traits may emerge post-catastrophe and then become dormant. Nonetheless, they may reemerge with disruptive life-cycle events such as helplessness, humiliation, separation, loss, and grief or with news events, such as can occur for Holocaust survivors when anti-Semitism reemerges. Similar events may result in seemingly divergent personality traits emerging among survivors or even within a survivor, such as when there is an intensification of efforts to avoid massive grief concurrent with a counterphobic adaptation.

To test the validity of such an EPCACE diagnosis, Beltran and colleagues

 undertook a comprehensive survey of clinical psychologists and psychiatrists: 89% of respondents agreed that personality can be altered by trauma occurring in adulthood. Of those 89% of respondents, torture and concentration camp exposure were identified by 91% and 90% respectively as likely to produce changes to personality, followed by 72% for war exposure, 66% for sexual assault, 57% for hostage situations, 52% for domestic violence, 25% for natural disasters, and 24% for motor vehicle accidents.

Despite this substantial evidence, only 16% of clinicians had ever used EPCACE as a diagnosis for their patients, although it had been a valid ICD-10 diagnosis for 7 years before Beltran’s survey. Those who responded to the survey also cited issues of symptom overlap between EPCACE and more commonly used diagnoses, specifically depressive disorders and borderline personality disorder. However, EPCACE is marked by stable changes in personality, whereas borderline and depressive disorders are marked by instability in mood and affect.

It is foreseeable that post-traumatic avoidance of reminders by both patient and clinician is even more pronounced in catastrophic trauma. This may be another factor that contributed to the underutilization of EPCACE in its debut as a diagnosis. Alas, the underutilization of EPCACE is a loss for a significant proportion of patients who might otherwise have united as a treatment community. This loss is compounded by the fact that aloneness is often seen in the transgenerational transmission of EPCACE-related suffering. Group therapy is therefore a vital modality in EPCACE treatment across generations and in fostering the transgenerational transmission of resilience.

A follow-up study of the validity and utility of EPCACE in 2008 by Beltran attempted to redefine the broad aspects of the diagnosis and identify the key criteria that described a person with EPCACE. Twenty-four mental health clinicians who worked with patients who had experienced war and sexual assault as well as recently displaced refugees provided valuable feedback. Not only were the key attributes of “A hostile or mistrustful attitude toward the world, social withdrawal, feelings of emptiness or hopelessness, a chronic feeling of being ‘on edge,’ as if constantly threatened, and estrangement” identified, but mental health practitioners felt significant features were excluded from EPCACE’s operational definition. These include “somatization, self-injurious/self-damaging behaviors, sexual dysfunction, and enduring guilt,” which if included would differentiate EPCACE from complex PTSD and strengthen the operational validity of the diagnosis.

 Since then, no changes to criteria or follow-up studies have been conducted to improve the utility of EPCACE.

Research into EPCACE has been limited, as manifestations of the core symptoms can often differ depending on viewpoints and type of trauma. A core feature of EPCACE such as “a hostile or mistrustful attitude toward the world” can be operationally expressed by multiple symptoms such as anger, aggression, and other countless variations.

 Holocaust survivors who were identified as “feeling as if the Holocaust experience was continuing” were more likely to suffer symptoms of mental disorder, whereas those who avoided the traumatic memories altogether had a higher mortality rate due to illness.

 Patients with a diagnosis of EPCACE may isolate themselves not only from their communities, but also from proper mental health care.

Alternatives to inclusion of EPCACE as a distinct diagnosis

Critics of the inclusion of EPCACE in diagnostic taxonomy claim that it lacks specificity and is insufficiently utilized. To address these concerns, Maercker and colleagues

 proposed to reconceive EPCACE as part of cPTSD in ICD-11. Following this recommendation, the World Health Organization trauma team eliminated the diagnosis of EPCACE.

 cPTSD incorporates patients with personality changes as a result of exposure to single or multiple traumatic experiences, as long as the requirement of three core features of PTSD is met; these core features include changes in affect, self-concept, and relational function.

Alas, modifying the diagnostic criteria for cPTSD to consolidate EPCACE and other trauma-related disorders may also lead to mislabeling and downgrading the seriousness of personality changes, as well as overlooking potentially transgenerational personality changes. Because different experiences may produce different neurological and behavioral effects, it would be unwise to disregard the type of event and its impact on affect.

This article explores why Enduring Personality Change After Catastrophic Experience (EPCACE) is a clinically useful diagnosis.

Hansen Tang

Articles

Transgenerational Transmission of Resilience After Catastrophic Trauma

How Catastrophe Can Change Personality