Introduction
With a large cohort of the population approaching their autumn years, it is imperative that the effect of health conditions on the elderly are better understood. In addition to the physical ailments that are often associated with aging, mental health disorders must also be considered. Unfortunately, research is lacking with respect to how certain mental health problems manifest themselves in the context of old age. One such disorder is post traumatic stress disorder (PTSD), which may emerge as a consequence of a traumatic event, even if the event occurred decades previously (Hiskey et al., Reference Hiskey, Luckie, Davies and Brewin2008). With more and more survivors of the various wars of the twentieth century entering old age, and – with longer lifespans – more individuals having occasions to be exposed to traumatic experiences, further understanding of PTSD in the elderly is necessary. Indeed, some have called the effects of trauma the “hidden variables” in the lives of older adults (Cook and O'Donnell, Reference Cook and O'Donnell2005).
While PTSD is well-described in the general population, the literature concerning PTSD in the elderly is patchy (Averill and Beck, Reference Averill and Beck2000; Busuttil, Reference Busuttil2004; Cook and O'Donnell, Reference Cook and O'Donnell2005). Nevertheless, there is evidence that PTSD is a significant issue for older adults. Elderly individuals with full and subthreshold PTSD suffer significant impairment in daily life, are less satisfied, receive less than optimum care, and report older subjective age, which is in itself related to greater health problems (van Zelst et al., Reference van Zelst, de Beurs, Beekman, van Dyck and Deeg2006; Solomon et al., Reference Solomon, Helvitz and Zerach2009). For instance, PTSD has been associated with an increased risk of coronary heart disease in older men (Kubzansky et al., Reference Kubzansky, Koenen, Spiro, Vokonas and Sparrow2007) and an increased risk of comorbidity such as depression and anxiety (Spitzer et al., Reference Spitzer, Barnow, Volzke, John, Freyberger and Grabe2008). Most research has been conducted with Holocaust survivors, former prisoners of war (POWs) and combat veterans, but recent research has identified other types of potentially traumatic events experienced by the elderly such as the death of a loved one, physical injury, and serious disease (Elklit and O'Connor, Reference Elklit and O'Connor2005; Chung et al., Reference Chung, Berger, Jones and Rudd2008; Reference Chung2009).
There is evidence of similarities between PTSD in the general population and PTSD in the elderly, but there are also indications that PTSD in old age presents unique features. In the adult literature, PTSD is associated with various impairments including attention, memory, and other executive functions (Moore, Reference Moore2009), as well as altered stress hormones levels and changes in brain structure (Yehuda, Reference Yehuda2009). These are many of the same features that describe normal cognitive aging (Lupien et al., Reference Lupien2007). In fact, some studies of PTSD in the elderly have suggested that this disorder represents accelerated aging (Golier et al., Reference Golier, Yehuda, Lupien, Harvey, Grossman and Elkin2002; Yehuda et al., Reference Yehuda, Halligan, Grossman, Golier and Wong2002; Yaffe et al., Reference Yaffe2010). Thus, it is imperative that in contrast to PTSD in the adult population, PTSD in the elderly be understood in developmental terms. That is, we must superimpose PTSD onto the background of the normal biological, psychological and social changes that are seen concurrently with aging. This review attempts to collate the existing prevalence and longitudinal studies, and touches upon risk factors for PTSD in the elderly. We then direct the focus of the paper to explore how PTSD can be understood within the context of cognitive aging. To this end, a comprehensive search was performed with ISI Web of Science and PubMed for articles pertinent to the psychology and biology of PTSD, trauma and the elderly. The results of this search are presented below, followed by a discussion of caveats and further directions to be considered in this field of research.
Results
Presentation
PTSD is traditionally classified as an anxiety disorder in DSM-IV, but is also conceptualized as a disorder of memory: one of the cardinal features is the repeated reliving of the traumatic event (American Psychiatric Association, 1994). In order for a clinical diagnosis to be made, the individual must have experienced a traumatic event during which they felt intense fear, helplessness or horror. Subsequently, survivors may present three distinct clusters of symptoms that characterize PTSD: re-experiencing of the traumatic event (e.g. nightmares, intrusive thoughts), numbing and avoidance of stimuli associated with the trauma, and hyperarousal (e.g. problems with sleeping, exaggerated startle response). Formal diagnosis is only made after symptoms have been experienced for at least one month and have caused significant distress and functional impairment in daily living (American Psychiatric Association, 1994).
The elderly may be at more risk, or at least may present additional complexity, regarding the development of psychopathology following a traumatic event. Compared with the general population, the elderly more often suffer from chronic physical and mental disorders; social networks tend to narrow with time; and financial means are often reduced. All of these factors, in addition to the social zeitgeist of the time and particular generation (Averill and Beck, Reference Averill and Beck2000), must be taken into account when considering PTSD in this population. Nevertheless, most research into PTSD excludes older adults (Spitzer et al., Reference Spitzer, Barnow, Volzke, John, Freyberger and Grabe2008).
PTSD in the elderly is noteworthy in that it can emerge and develop in several ways. Several possible forms of presentation have been postulated (Busuttil, Reference Busuttil2004). First is de novo, due to a trauma experienced in old age. Second is chronic, where the trauma is experienced much earlier in life, and leads to PTSD that follows a chronic course with possible periods of fluctuation with respect to symptom severity. Third, PTSD can manifest itself with delayed onset; after years of absent, low or well-controlled symptoms, full-blown PTSD surfaces in old age. This last characterization is not without controversy, however. Some maintain that PTSD with delayed onset is in fact a misnomer – the apparent absence of PTSD is actually due to under-reporting, delayed referral, exacerbation of subclinical PTSD, or misdiagnosis (Hiskey et al., Reference Hiskey, Luckie, Davies and Brewin2008). Fourth is chronic PTSD with enduring personality changes, and lastly, is chronic complex PTSD with multiple psychiatric disturbances.
Several hypotheses regarding PTSD in the elderly have been advanced, and evidence can be found for each. The opposing hypotheses can be described as (i) the inoculation hypothesis, whereby older adults are more resistant because prior experience of traumatic events is protective (Eysenck, Reference Eysenck and Cooper1983), and (ii) the vulnerability hypothesis, which states that the accumulation of previous traumatic experience, combined with the additional stresses of aging, may render older people more vulnerable when faced with a novel stressful event (Solomon and Ginzburg, Reference Solomon and Ginzburg1998). The crisis resolution hypothesis ostensibly accounts for the discrepancy between the aforementioned theories: previous exposure to extreme stress can either predispose or protect the older adult against subsequent traumatic experience depending on how that prior experienced was resolved (Hantman and Solomon, Reference Hantman and Solomon2007). A cognitive aging hypothesis has been put forward to describe the re-emergence of PTSD that can occur in old age (Floyd et al., Reference Floyd, Rice and Black2002). In this explanation, the age-related decreases in attention and memory function account for the possible recurrence of PTSD (Floyd et al., Reference Floyd, Rice and Black2002). Likewise, neurodegenerative underpinnings of aging have been implicated in explaining the recurrence of PTSD in old age (Ruzich et al., Reference Ruzich, Looi and Robertson2005).
Possible explanations for delayed onset PTSD include (i) the fact that, because of decreased physical and mental resilience over time, the elderly become less able to “ward off” PTSD (Aarts and Op den Velde, Reference Aarts, Op den Velde, van der Kolk, McFarlane and Weisaeth1996); (ii) age-related stressors such as retirement or bereavement may induce the presentation of PTSD; (iii) in old age, people start to reflect more on their lives, often in a search for life meaning, and may increase their focus on traumatic memories (Erikson, Reference Erikson1966); and (iv) the psychodynamic view that re-emergence of PTSD is due to a failure of repression (Horowitz, Reference Horowitz1974). It must be noted that several different terms can be found in the literature, including “delayed onset”, “re-emergent”, or “re-activated” PTSD (Port et al., Reference Port, Engdahl and Frazier2001; Bramsen et al., Reference Bramsen, van der Ploeg and Boers2006; Hiskey et al., Reference Hiskey, Luckie, Davies and Brewin2008). As Hiskey and colleagues note, a clear definition of what is meant by recurrent or delayed onset PTSD must be constructed in order for accurate prevalence rates to be measured and the underlying mechanisms to be discovered (Hiskey et al., Reference Hiskey, Luckie, Davies and Brewin2008).
Another unclear concept in the literature is the definition of trauma itself with respect to the elderly population. An aged individual will generally have experienced a lifetime of stressful events, more so than their younger counterparts. Does this change the threshold for which an event is experienced as traumatic? Are the same events experienced as traumatic for the elderly compared with younger individuals? Methodologically, it must be agreed upon as to how “trauma” is operationalized: do we include all potentially negative events as traumatic, or simply those that are beyond the realm of typical experience? This question is not new within the adult PTSD literature (for example, see McNally, Reference McNally2003); however, there is potentially an additional dimension to this discussion when the context of aging is introduced.
Prevalence and course
Epidemiological studies indicate significant lifetime prevalence rates for trauma exposure in the general population, with men consistently at higher risk than women (Kessler et al., Reference Kessler, Sonnega, Bromet, Hughes and Nelson1995). Lifetime prevalence rates for PTSD from South America (Zlotnick et al., Reference Zlotnick, Johnson, Kohn, Vicente, Rioseco and Saldivia2006), North America (Kessler et al., Reference Kessler, Sonnega, Bromet, Hughes and Nelson1995; Norris et al., Reference Norris, Murphy, Baker, Perilla, Rodriguez and Rodriguez2003; van Ameringen et al., Reference van Ameringen, Mancini, Patterson and Boyle2008), and Europe (Frans et al., Reference Frans, Rimmo, Aberg and Fredrikson2005; de Vries and Olff, Reference de Vries and Olff2009) have reported rates between 4.4% and 11.2%. Most of the prevalence studies have not examined elderly individuals; however, a handful of recent studies has begun to address this gap. A six-month prevalence study found rates of 0.9% for full PTSD and 13.1% for subthreshold PTSD in a group of older adults (van Zelst et al., Reference van Zelst, de Beurs, Beekman, Deeg and van Dyck2003). More recently, a community study comprising three groups (aged ≤44, 45–64, ≥65 years) found that lifetime prevalence of PTSD in the elderly was 3.1% and did not significantly differ from the other age groups (Spitzer et al., Reference Spitzer, Barnow, Volzke, John, Freyberger and Grabe2008). Aged individuals who endorse a diagnosis of PTSD were found to meet mild or moderate severity rather than extreme symptom severity (Yehuda et al., Reference Yehuda, Schmeidler, Siever, Binder-Brynes and Elkin1997). Overall, these results suggest that older adults present lower rates of PTSD than the general population. However, this conclusion should be interpreted with care. Some have cautioned that these rates may be artificially low due to under-reporting or because the elderly may attribute or experience their PTSD symptoms as somatic rather than psychological (van Zelst et al., Reference van Zelst, de Beurs, Beekman, Deeg and van Dyck2003; Owens et al., Reference Owens, Baker, Kasckow, Ciesla and Mohamed2005). Additionally, changes in response to stress with age may affect both the experience and presentation of PTSD, and older adults may attribute their symptoms to aging itself rather than to trauma (Owens et al., Reference Owens, Baker, Kasckow, Ciesla and Mohamed2005).
The paucity of cohort studies conducted after a traumatic event makes it premature to conclude that the elderly are at a greater risk of PTSD. Still, the extant literature seems to suggest that, compared with younger adults, they are not (however, for contrary findings, see Lee et al., Reference Lee, Chi, Chung and Chou2006; Liu et al., Reference Liu2006). In community samples comprised of younger, middle aged, and elderly individuals, there was no significant difference in PTSD symptoms between groups after technological disasters (Chung et al., Reference Chung, Werrett, Easthope and Farmer2004), natural disaster (Kohn et al., Reference Kohn, Levav, Garcia, Machuca and Tamashiro2005), and interpersonal violence (Acierno et al., Reference Acierno, Brady, Gray, Kilpatrick, Resnick and Best2002). A community prevalence study that measured trauma exposure across the lifespan uncovered a differential pattern between men and women (Creamer and Parslow, Reference Creamer and Parslow2008). Traumatic exposure over the lifespan followed an inverted-U pattern for women and a linear pattern for men, the difference being explained by male combat experience. Overall, this study found that the net prevalence of PTSD declined with age (Creamer and Parslow, Reference Creamer and Parslow2008).
PTSD prevalence has also been studied specifically in older adults after particular types of events. These include after myocardial infarction (Chung et al., Reference Chung, Berger, Jones and Rudd2006), spinal cord injury (Chung et al., Reference Chung, Preveza, Papandreou and Prevezas2006), bereavement (Elklit and O'Connor, Reference Elklit and O'Connor2005), and falls (Chung et al., Reference Chung2009), and these studies advocate the consideration of these events as being potentially traumatic in the elderly. Another study has investigated the possibility of reactivation of PTSD after a secondary trauma (Bramsen et al., Reference Bramsen, van der Ploeg and Boers2006). Survivors of World War II who experienced a fireworks disaster in the Netherlands were compared with WWII survivors who did not, and were assessed both before and after the fireworks disaster. PTSD symptoms as well as war-related re-experiencing increased in the former group, and supported the conclusion that reactivation of previous traumatic events can occur. Additionally, there was no evidence for delayed onset PTSD, consistent with several other studies that do not support an association between recent life events and an increase in PTSD (Dirkzwager et al., Reference Dirkzwager, Bramsen and van der Ploeg2001; van Achterberg et al., Reference van Achterberg, Rohrbaugh and Southwick2001; Port et al., Reference Port, Engdahl, Frazier and Eberly2002; but see Op den Velde et al., Reference Op den Velde, Wilson and Raphael1993; Macleod, Reference Macleod1994; Hiskey et al., Reference Hiskey, Luckie, Davies and Brewin2008).
The handful of longitudinal studies reveals that the course of PTSD into old age may not necessarily be summarized by a simple trajectory. Rather, different trajectories may exist depending on the type of trauma experienced, duration of trauma, and other factors. There is evidence for symptom stability (Dirkzwager et al., Reference Dirkzwager, Bramsen and van der Ploeg2001), exacerbation (Port et al., Reference Port, Engdahl and Frazier2001; Joffe et al., Reference Joffe, Brodaty, Luscombe and Ehrlich2003; Solomon and Mikulincer, Reference Solomon and Mikulincer2006; Trappler et al., Reference Trappler, Cohen and Tulloo2007), reduction (Kluznick et al., Reference Kluznick, Speed, van Valkenburg and Magraw1986; Tennant et al., Reference Tennant, Fairley, Dent, Sulway and Broe1997), and fluctuation (Dirkzwager et al., Reference Dirkzwager, Bramsen and van der Ploeg2001); in short, the literature is unsettled. In trying to make sense of such equivocal data, Yehuda and colleagues suggested that an array of trajectories may be possible, related to particular factors or individual differences (Yehuda et al., Reference Yehuda2009). Their ten-year longitudinal study of Holocaust survivors supported this: there was an overall reduction in symptoms with time, but, more accurately, those who endorsed PTSD at time 1 experienced a reduction in symptom severity by time 2. Meanwhile those without PTSD at time 1 showed an increase in symptom severity by time 2. A small portion of the sample presented delayed onset PTSD at time 2; however this subset did have higher symptom severity at time 1 than the others who did not develop PTSD at time 2. The authors emphasize that the possibility of delayed onset PTSD complicates any projection of a simple trajectory for PTSD in this population. Furthermore, delayed onset PTSD may be understood as a redistribution of PTSD symptoms rather than a dichotomous measure of the presence or lack of PTSD symptoms per se (Yehuda et al., Reference Yehuda2009).
A final note of caution is suggested when interpreting the aforementioned prevalence studies because of the possibility of sample bias. It is conceivable that the elderly populations investigated in the handful of epidemiological studies performed are more resilient in some respect (for example, biological, psychological, attachment style, etc.) compared with their younger counterparts, for presumably there are many individuals who have not fared as well as they have over the years. This potentially significant factor should be kept in mind when considering PTSD in this population, as well as when comparing findings with younger cohorts.
Risk factors
PTSD is not an inevitable consequence of a traumatic experience; most people in fact recover. The mystery remains as to why some people who are exposed to traumatic stress develop PTSD while others do not, and much research has sought to identify the particular factors that may explain the discrepant reactions. Risk factors associated with the development of PTSD are well described in the general PTSD literature (Brewin et al., Reference Brewin, Andrews and Valentine2000; Ozer et al., Reference Ozer, Best, Lipsey and Weiss2003). Overall, peri- and post-traumatic factors seem to be stronger predictors of PTSD than pre-traumatic factors. Factors more proximal to the trauma, such as perceived life threat, perceived support, trauma severity, peri-traumatic emotionality, and peri-traumatic dissociation, are stronger predictors than more distal factors such as prior adjustment, prior history of trauma, and family history of psychopathology (Brewin et al., Reference Brewin, Andrews and Valentine2000; Ozer et al., Reference Ozer, Best, Lipsey and Weiss2003). PTSD severity has also been related to particular cognitive decrements such as problems with episodic memory, working memory, verbal memory, and negative trauma-related and self-related appraisals (Ehring et al., Reference Ehring, Ehlers and Glucksman2008; Field et al., Reference Field, Norman and Barton2008), and there is evidence to suggest these features might represent premorbid traits (Moore, Reference Moore2009). Several prospective studies suggest that negative cognitions directed towards the self prior to or immediately after the trauma may predict PTSD severity (Bryant and Guthrie, Reference Bryant and Guthrie2007; Ehring et al., Reference Ehring, Ehlers and Glucksman2008).
As in the general PTSD literature, several risk factors have been specifically associated with PTSD in the elderly after an array of trauma types. These include being female (e.g. van Zelst et al., Reference van Zelst, de Beurs, Beekman, Deeg and van Dyck2003; Liu et al., Reference Liu2006) although gender is not always significant, for example (Brodaty et al., Reference Brodaty, Joffe, Luscombe and Thompson2004); adverse events in childhood (van Zelst et al., Reference van Zelst, de Beurs, Beekman, Deeg and van Dyck2003), low self-efficacy (van Zelst et al., Reference van Zelst, de Beurs, Beekman, Deeg and van Dyck2003), having lower IQ (e.g. Hart et al., Reference Hart2008), lower social support (Acierno et al., Reference Acierno, Brady, Gray, Kilpatrick, Resnick and Best2002; Alpass et al., Reference Alpass, Long, Blakey and Pachana2004), current level of PTSD symptoms of spouse (Bramsen et al., Reference Bramsen, van der Ploeg and Twisk2002), use of immature defense mechanisms (Brodaty et al., Reference Brodaty, Joffe, Luscombe and Thompson2004), and personality factors such as neuroticism and antagonism (van Zelst et al., Reference van Zelst, de Beurs, Beekman, Deeg and van Dyck2003; Brodaty et al., Reference Brodaty, Joffe, Luscombe and Thompson2004; Chung et al., Reference Chung, Berger, Jones and Rudd2006). Current cognitive status may also represent a noteworthy risk factor in the elderly population, especially with respect to the emergence or re-emergence of PTSD in old age after years of absent or well-controlled symptoms (Johnston, Reference Johnston2000; Mittal et al., Reference Mittal, Torres, Abashidze and Jimerson2001; van Achterberg et al., Reference van Achterberg, Rohrbaugh and Southwick2001; Floyd et al., Reference Floyd, Rice and Black2002; Cook et al., Reference Cook, Ruzek and Cassidy2003; Alpass et al., Reference Alpass, Long, Blakey and Pachana2004; Ruzich et al., Reference Ruzich, Looi and Robertson2005).
An additional vulnerability when considering trauma across the lifespan is attachment style. Although discussion of attachment theory and PTSD in the literature is sparse, there is a basis for thinking about the reaction to traumatic events across the lifespan within the context of attachment (Cassidy and Mohr, Reference Cassidy and Mohr2001). Attachment theory was initially conceived of to explain, in both psychological and biological terms, how individuals respond to danger and threat (Bowlby, Reference Bowlby1973). Later research has examined how early experiences with fear and separation relate to how adults cope with trauma later in life (e.g. Diamond and Fagundes, Reference Diamond and Fagundes2010). Differential attachment patterns established in childhood, adolescence, and adulthood may explain some of the individual variability in reactions to trauma in the elderly years, in terms of both vulnerability and resilience. In fact, recent research has considered dementia and aging in terms of the attachment styles established earlier in life as well as in the later years (Browne and Shlosberg, Reference Browne and Shlosberg2006). Other investigators have begun to study the relationship between attachment style and the functioning of the hypothalatmic-pituitary-adrenocortical axis, which is integrally affected in trauma, stress and PTSD (and will be discussed in later sections below) (Diamond and Fagundes, Reference Diamond and Fagundes2010).
PTSD and the interaction with healthy aging
PTSD, as with normal aging, is associated with an array of biological alterations and, at times, cognitive impairment. Certain biological features are similar between the elderly and younger samples with PTSD, while others deviate and seem more similar to the biological changes associated with normal aging. These findings have led investigators to postulate that there is a superimposition of aging and PTSD in certain respects, and that, in fact, the interaction between aging and PTSD may lead to accelerated aging in particular domains (e.g. Yaffe et al., Reference Yaffe2010). Although this hypothesis is by no means proven (e.g. Pitman, Reference Pitman2010), it is clear that PTSD in the elderly must nevertheless be considered against the backdrop of the expected behavioral, hormonal, and cerebral changes associated with aging. This discussion mainly concerns chronic PTSD, or PTSD that stems from a traumatic event experienced many years earlier, since de novo PTSD seems to be associated with similar or even lower prevalence levels with respect to younger cohorts, as expounded in the preceding sections.
Case studies
The first indications that PTSD and aging may have a particular relationship came from several case series. In general, they described how select individuals, after decades of absent or well-controlled symptoms, developed PTSD in old age that coincided with the onset of cognitive decline or neurological illness. Mittal et al. (Reference Mittal, Torres, Abashidze and Jimerson2001) documented three cases of war-related PTSD that was under control until the development of Alzheimer's disease, vascular, and alcohol-related dementia, respectively. The authors highlight the fact that these patients, despite undergoing significant cognitive decline, experienced intense recollections of their traumatic event, and hypothesize that the aging process may disinhibit the neural pathways and lead to a worsening of traumatic memories. Similar cases have been noted in Holocaust survivors (Grossman et al., Reference Grossman, Levin, Katzen and Lechner2004) and combat veterans (Johnston, Reference Johnston2000). The cases of a Holocaust survivor, a World War II veteran, and a survivor of the Titanic, who all showed mild symptoms during the majority of their lives, only to exhibit significant worsening of PTSD symptoms with the onset of dementia have been described by van Achterberg et al. (Reference van Achterberg, Rohrbaugh and Southwick2001). In none of these cases can the psychosocial stressors associated with aging, such as retirement or death of a loved one, account for the aggravation of PTSD symptoms. These results suggest that trauma-related memories are perhaps more resistant to the effects of dementia, and that the dementing process may interfere with cognitive strategies or defense mechanisms previously employed to keep traumatic memories in check (van Achterberg et al., Reference van Achterberg, Rohrbaugh and Southwick2001). However, in 15 elderly combat veterans who reported delayed onset PTSD, their disorder coincided with the onset of unrelated medical problems, psychosocial stress related to aging, and/or mild cognitive impairment (Ruzich et al., Reference Ruzich, Looi and Robertson2005). The authors suggest that age-related psychosocial stress and neurodegeneration interact, and that this occurs in the context of past traumatic experience, which may account for the possible re-emergence of symptoms in later life (Ruzich et al., Reference Ruzich, Looi and Robertson2005).
Behavioral studies
Concerning the cognitive profile associated with PTSD, research in adult cohorts has revealed relatively consistent episodic memory impairment (e.g. Moore, Reference Moore2009). Episodic, or declarative, memory refers to the effortful and conscious recollection of events and facts (Tulving, Reference Tulving1985). Research with aged Holocaust survivors has revealed both content independent and dependent episodic memory impairment (Golier et al., Reference Golier, Yehuda, Lupien, Harvey, Grossman and Elkin2002; Reference Golier, Yehuda, Lupien and Harvey2003). In fact, 36% of Holocaust survivors performed at a level of frank cognitive impairment (Golier et al., Reference Golier, Yehuda, Lupien, Harvey, Grossman and Elkin2002). Further studies were conducted with both aged combat veterans (Yehuda et al., Reference Yehuda, Golier, Tischler, Stavitsky and Harvey2005a) and Holocaust survivors (Yehuda et al., Reference Yehuda, Golier, Halligan and Harvey2004) using the California Verbal Learning Test (CVLT), which can parse apart the different aspects of episodic learning and memory (Delis et al., Reference Delis, Kramer, Kaplan and Ober1987). Similar to younger veterans, but unlike Holocaust survivors with PTSD, these elderly combat veterans had impaired delayed free recall (Yehuda et al., Reference Yehuda, Golier, Tischler, Stavitsky and Harvey2005a). However unlike the younger veterans and similar to the Holocaust survivors, these aged veterans showed reduced total learning, indicating problems with encoding and consolidation in both elderly samples (Yehuda et al., Reference Yehuda, Golier, Halligan and Harvey2004; Reference Yehuda, Golier, Tischler, Stavitsky and Harvey2005a). This suggests that a reduced rate of total learning may be attributable to an interaction between PTSD and aging, while the reduced delayed free recall is a particularity of combat veterans with PTSD. In addition, in all of these studies, age was negatively correlated with memory performance only in the PTSD groups, while no such correlation was uncovered in the exposed and healthy control groups (Golier et al., Reference Golier, Yehuda, Lupien, Harvey, Grossman and Elkin2002; Reference Golier, Yehuda, Lupien and Harvey2003; Yehuda et al., Reference Yehuda, Golier, Halligan and Harvey2004; Reference Yehuda, Golier, Tischler, Stavitsky and Harvey2005a). In a longitudinal study of Holocaust survivors with PTSD, compared with controls, a decrease in symptom severity, and decrease in paired word association performance was found, while there was an improvement in performance on the California Verbal Learning Test (CVLT) that correlated with symptom improvements (Yehuda et al., Reference Yehuda2006). Paired learning is influenced by age but not symptom severity, suggesting an interaction between PTSD and age, while the CVLT is associated with severity and not age. This is consistent with the idea that a trauma-related biological change at an earlier time can be related to the trajectory of memory changes (Yehuda et al., Reference Yehuda2006). It seems that the effects of aging on explicit memory are greater in the PTSD group, which again is consistent with the idea of accelerated aging. Overall, the memory deficits are more substantial and generalized in the elderly with PTSD compared with younger individuals. Investigators have thus hypothesized that aging and PTSD interact and can lead to accelerated, age-related cognitive decline in some aspects.
Endocrinological studies
Endocrinological studies with aged PTSD samples have also suggested an interaction. In the general PTSD population, there seems to be a pattern of increased type II glucocorticoid receptor responsiveness, and lower or normal ambient cortisol levels (e.g. Yehuda, Reference Yehuda2009). In elderly Holocaust survivors with PTSD, a flatter circadian rhythm of cortisol release was found, which is similar to that seen in healthy aging, and in contrast to younger samples (Yehuda et al., Reference Yehuda, Golier and Kaufman2005b). Yehuda et al. (Reference Yehuda, Golier and Kaufman2005b) interpret this pattern as reflecting a superimposition of PTSD and aging. In a subsequent study, Yehuda et al. (Reference Yehuda2005c) found a negative correlation between cortisol concentrations and episodic memory performance, even though the aged PTSD sample had lower ambient cortisol levels overall. This finding can seem paradoxical at face value given the cognitive impairment associated with PTSD, and especially in face of the glucocorticoid cascade hypothesis, which holds that stress is associated with elevated cortisol (Sapolsky et al., Reference Sapolsky, Krey and McEwen1986). However, cortisol is presumed to relate to cognitive ability in terms of an inverted-U function: either too low or too high levels can induce cognitive impairment (Lupien and McEwen, Reference Lupien and McEwen1997; Erickson et al., Reference Erickson, Drevets and Schulkin2003). More recently, cortisol was administered to aging combat veterans and healthy controls (Yehuda et al., Reference Yehuda, Harvey, Buchsbaum, Tischler and Schmeidler2007a). In both groups, episodic memory was enhanced, while working memory was enhanced only in the PTSD group, which is in contrast to younger samples where working memory was impaired (Grossman et al., Reference Grossman, Yehuda, Golier, McEwen, Harvey and Maria2006; Yehuda et al., Reference Yehuda, Harvey, Buchsbaum, Tischler and Schmeidler2007a). The older sample had worse working memory performance at baseline than did the younger sample in the previous study, which the authors interpret as evidence for accelerated age-related decline (Yehuda et al., Reference Yehuda, Harvey, Buchsbaum, Tischler and Schmeidler2007a).
Neuroimaging studies
Given that the cognitive impairment that has been typically associated with PTSD is assumed to be dependent on the medial temporal lobe (MTL), combined with the centrality of memory to the disorder (i.e. intrusive memories, flashbacks), much neuroimaging research has been conducted on this region (e.g. Shin et al., Reference Shin, Rauch and Pitman2006). In the bulk of these studies, PTSD has been associated with smaller hippocampal volume compared with healthy controls. Still, it is difficult to attribute this to glucocorticoid toxicity since PTSD is not associated with elevated ambient cortisol levels (Yehuda et al., Reference Yehuda2007b). However, the results are not unequivocal. In fact, a minority of studies have found cognitive impairment in the absence of hippocampal abnormality, or vice versa. In the handful of neuroimaging studies conducted with aged PTSD samples of Holocaust survivors, POWs and combat veterans, respectively, no difference was found in hippocampal volumes compared with controls (Golier et al., Reference Golier, Yehuda, De Santi, Segal, Dolan and de Leon2005; Freeman et al., Reference Freeman2006; Yehuda et al., Reference Yehuda2007b).
The discrepant findings concerning hippocampal volume between young and elderly PTSD samples and controls could be explained by several not necessarily mutually exclusive hypotheses. First, it could be that the atrophy that occurs with normal aging may mask the reduced hippocampal volume associated with PTSD in adults, such that in the elderly, the differences are no longer significant. Second, perhaps a lifetime of lower ambient cortisol levels manifested itself as cognitive impairment, but at the same time, protected the hippocampus from stress-related atrophy (Yehuda et al., Reference Yehuda2005c). Third, Freeman et al. (Reference Freeman2006) hypothesized that since POWs have significantly higher morbidity than civilians, high attrition over time could have resulted in an exceptionally robust and healthy sample that lack reduced hippocampal volume (Freeman et al., Reference Freeman2006). Fourth, it has been proposed that smaller hippocampal volume represents a predisposing factor rather than a consequence of PTSD itself. By interpreting the glucocorticoid and hippocampal characteristics as pre-trauma traits, researchers are able to explain why only a minor subset of individuals experience higher arousal and distress as a response to traumatic stress and go on to develop PTSD, and why PTSD is not always associated with smaller hippocampal volumes or cognitive impairment (Gilbertson et al., Reference Gilbertson2002; Moore, Reference Moore2009; Yehuda et al., Reference Yehuda2009). That no difference in hippocampal volume was found in the Holocaust survivors with PTSD could be because, in this unique sample, the main risk factors were being Jewish in a particular time and place (Yehuda et al., Reference Yehuda2009), which trumps every other predisposing risk factor. Furthermore, in the aged sample of combat veterans studied by Yehuda et al. (Reference Yehuda2007b), smaller left hippocampal volume was only found in those who developed PTSD after their first traumatic exposure, compared to those who went on to develop PTSD after subsequent traumatic events, suggesting that the latter individuals were more resilient. Finally, Yehuda et al. (Reference Yehuda2006) suggest that biological alterations present at one point during the lifespan can be related to particular trajectories of changes at a later time, and furthermore, that these alterations do not need to be present at that later time. They parallel the finding that increased heart rate immediately subsequent to traumatic exposure can be predictive of later PTSD, but that increased heart rate is no longer present when the PTSD is finally diagnosed (Yehuda et al., Reference Yehuda2006).
Discussion
Any clear relationship between PTSD and aging is challenging since aging is associated with significant heterogeneity. For instance, although aging is associated with cognitive decline, the elderly exhibit wide variation in cognitive function. Some individuals enjoy stable cognitive function with age while others experience severe decline. Lupien et al. (Reference Lupien2005; Reference Lupien2007) have shown that there is much heterogeneity within the elderly population in terms of cortisol levels and diurnal patterns. They identified three subgroups of elderly people: two with increasing cortisol levels over time, with either currently high, or currently moderate levels, and a third group with decreasing cortisol levels over time with currently moderate levels. In the first group, hippocampal volume is 14% smaller than the other groups and is also associated with episodic memory impairment. Lupien et al. (Reference Lupien2007) have pointed out that while the hippocampus is generally smaller and atrophies at a faster rate with age, there is significant overlap between the mean hippocampal volumes between old and young cohorts. Thus, because the cerebral and endocrinological findings associated both with healthy aging and with PTSD in the general population are highly heterogeneous and complex, making claims about the interaction between aging and PTSD is difficult. But it is clear from recent findings that PTSD in the elderly is associated with some unique characteristics, probably in part due to age.
In general, the epidemiological studies concerning PTSD in the elderly suggest a complex situation. The elderly seem to be at no worse risk than the rest of the population for developing PTSD after experiencing a traumatic event, although the evidence is not incontrovertible. Regarding PTSD that has its roots in a trauma experienced many decades previously, the research suggests that PTSD symptoms may persist significantly for some individuals. The course of PTSD over the lifespan can wax and wane, can remain stable, and can even seemingly disappear for decades only to reappear in old age. The fact of the matter is that the elderly represent a heterogeneous population that has experienced myriad types of traumas at various points during the lifespan. The trajectory of PTSD throughout life seems highly variable, and probably depends on a multitude of factors. Only additional, well-designed longitudinal studies will reveal which factors are involved.
Overall, it seems that PTSD and the associated cognitive profile and biological features are not necessarily static over the lifespan. In certain respects, the trajectory of PTSD-related changes apparently interact with the normal aging process, perhaps leading to accelerated, age-related changes. Although it is difficult to elucidate clearly what these changes are, and how we may predict them, it is clear that the aging process in combination with PTSD presents a unique situation. The enhanced cognitive impairment in the elderly samples must be taken into consideration in the development and administration of treatment (Cook and O'Donnell, Reference Cook and O'Donnell2005). Again, more longitudinal studies focusing on the biological and cognitive changes over time are required in order to verify how PTSD interacts with age.
Conflict of interest
None.
Description of authors' roles
FF and LL conceived the topic and scope of paper. LL wrote the paper, and CA and FF read and commented on the final draft.
Acknowledgment
We would like to thank Dr Jonathan Lapp and Dr Serge Gauthier for their careful reading of the manuscript.
