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Original Article

Long-term outcome of serious traumatic brain injury

Wood, R. Ll.a

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European Journal of Anaesthesiology: February 2008 - Volume 25 - Issue - p 115-122
doi: 10.1017/S0265021507003432

Abstract

Psychosocial outcome

A recent study of nearly 3000 serious head-trauma cases found that 52% of survivors were either moderately or severely disabled at 1 yr [1]. Many of these individuals never recover full social independence, even though they may have no physical disability and a normal life expectancy. Teasdale and colleagues [2] suggested that psychological factors may be largely responsible for persisting disability and social handicap. This reflects observations from a number of studies that evaluate psychosocial outcome. Jacobs [3] found that most survivors lived with their families and neither worked nor attended school. Brooks and colleagues [4] comment on the psychological burden experienced by families who care for injured relatives. They found that 7 yr post injury, supporting relatives experienced emotional pressures that placed close relationships at risk. As a result, many marriages or partnerships fail [5], increasing the chance of social isolation, further increasing the risks of long-term psychological morbidity. Oddy and colleagues [6] have shown that mood disorders are very common after head trauma, with a high risk of suicide. There is little evidence of improvement in psychological problems between 2 and 7-yr post injury, prolonging the need for family support and imposing a long-term social burden on relatives [7].

Unfortunately, few studies have been conducted on very long-term outcome (≥10 yr post injury) to determine whether survivors of serious head trauma are capable of making gradual psychosocial adjustments to improve their lifestyle. Sbordone and colleagues [8] report on a cohort of 20 cases (and close relatives) at 10yr post injury. They described improved cognitive, vocational, motor, behavioural and interpersonal functions, suggesting that with the passage of time, there may be some form of personal adjustment that leads to better psychosocial outcome. Hoofien and colleagues [9] conducted a study in Israel on cases ranging from 10 to 20 yr post injury (average 14.1 yr) using a comprehensive range of outcome measures that included psychiatric symptoms, vocational status, family integration, social functioning and independence in daily routines. Many participants were found to be depressed and lonely with a high burden of care placed on relatives. The divorce rate was higher than the national average, possibly related to high levels of hostility and temper outbursts displayed by their sample. They found a fairly clear relationship between the presence of behaviour problems and poor psychosocial outcome. However, employment rates in their cohort were relatively high (60%), and 79% were still living with a spouse, or independently.

The longitudinal research conducted by Thomsen [10-12] is regarded by many as the seminal work on very long-term outcome. In a group of 40 very seriously injured cases evaluated at 2.5 yr post injury, psychosocial sequelae of brain injury, such as personality change and emotional problems, were more socially debilitating than physical disability, increasing the risks of social isolation, caregiver stress and unemployment. These problems persisted for a number of years after the initial follow-up but, after 10-15 yr, Thomsen pointed to a late improvement in some of the cases, ‘It is especially remarkable that half the patients who could not be left alone two years or more after the accident became independent during the following years. Several of the samples regained some work capacity but generally not until years after the injury. The late results thus indicate that though the patient with very severe head injury may remain disabled, improvement in psychosocial functions can continue for several years' (p. 267). In her final follow-up, 20 yr post injury, 31 patients were seen, nearly half (49.2%) of whom were capable of living alone, four (12.5%) were married, four (12.5%) continued to live with parents and eight (25.8%) were in a nursing home. Of the sample, 32% displayed threatening aggressive or sexual behaviour, and 61% had no social contacts. However, Thomsen again noted a range of psychosocial outcomes, judging 23% of her sample to have good or very good psychosocial outcomes. Thomsen does not make explicit the basis upon which these judgements of good psychosocial outcomes are made but she notes that the range of individual differences could not be explained by severity of injury, measured by post-traumatic amnesia (PTA), because amongst the best outcomes were cases with the longest PTAs. Information about the quality of long-term psychosocial outcome may therefore depend less on the severity of injury and more on the time post injury when follow-up studies are conducted.

Some support for this was provided by Wood and Rutterford [13] who evaluated very long-term outcome in a large severely brain-injured cohort, at a mean (range) time of 17 (10-32) yr post injury. They recognized that a range of factors can reflect psychosocial outcome, such as employment status, social functioning, activities of daily living, financial status, cognitive impairment and emotional disorders. Therefore, they used a number of psychosocial outcome measures to examine the notion that individual cases of serious head trauma are capable of achieving reasonably good long-term psychosocial outcome. Their data suggested that very long-term psychosocial outcome following serious head injury may be better than expected from data reported at earlier stages of recovery. Of the cases in their study, 72% were rated as capable of independent living and 41% were in either full- or part-time employment. None were in residential care and only one (with serious physical disability) had care support at home. A total of 60% were married or co-habiting and there was a low divorce/separation rate. Most participants rated their functional competency as slightly below that of non-brain-injured individuals, a perception that may be associated with sub-optimal social participation as measured by the Community Integration Questionnaire. The group only described themselves as ‘slightly dissatisfied' with life, which might reflect a gradual adjustment to persisting difficulties imposed by brain injury. However, there was no indication that relatively low satisfaction with life ratings translated into psychological morbidity. The group reported only mild levels of anxiety and normal ratings of mood.

Long-term cognitive recovery

Cognitive impairment is a major neuropsychological legacy of head trauma. However, there is no particular relationship between severity of brain injury and type or degree of intellectual impairment or quality of psychosocial recovery [14]. Measures of intelligence cannot therefore be relied upon as an index of impairment or recovery after head trauma [15], nor can they predict the psychosocial impact of brain injury [16]. Clinical experience indicates that many cases of severe brain injury show no reduction in the measured levels of intellectual ability, compared with estimates of pre-morbid ability, even though performance on a range of real-life activities indicates that many individuals are not capable of functioning at a level compatible with their measured intelligence. Walsh [15] noted that persons with seemingly preserved intelligence fail to cope with demands of their occupation or profession and refers to this as the ‘frontal lobe paradox'. Therefore, neuropsychologists should be cautious about using measures of intelligence as an index of recovery, from which one can predict return to employment and other forms of social functioning.

Many people with cognitive impairment following head trauma exhibit problems of social functioning that are reminiscent of elderly people. They are very forgetful and have difficulty adapting to change or novelty. They often exhibit a slightly concrete or rigid style of thinking and have stereotyped patterns of behaviour, organized around regular routines. It is therefore understandable that many clinicians regard head trauma as a high risk for accelerated or abnormal ageing. One possible mechanism for accelerated ageing relates to the predominantly frontal nature of head trauma, which, in cases of motor vehicle accident and falls, involves decelerative mechanical forces that impact frontal brain systems. Phillips and Della Salla [17] have argued that the most likely mechanism for cognitive decline is neural deterioration in the dorsolateral pre-frontal cortex (DLPFC) because this will impact fluid intelligence, abstract thinking and executive function. Literature on the neurobiology of healthy ageing supports this notion. The DLPFC mediates the activities of various cognitive domains [18] and that the pre-frontal region is affected by increasing age [19]. Measures of cognitive function in healthy ageing have identified deficits in episodic memory, working memory, prospective memory, inhibition, attention and ‘executive' function [20].

Injury to the pre-frontal cortex is a frequent legacy of decelerative head trauma. Consequently, individuals who sustain such injuries are likely to be at high risk of premature ageing. However, data examining associations between head injury and Alzheimer's disease remain equivocal. Fleminger and colleagues [21] conducted a meta-analytical study to determine the role of head injury as a risk factor for Alzheimer's disease. Fleminger and colleagues examined 15 case-control studies that met rigorous inclusion criteria. Seven studies had already been the subject of an earlier meta-analysis conducted by Mortimer and colleagues [22]. Fleminger and his colleagues found that only studies prior to 1991 (those examined by Mortimer and colleagues) showed a significant risk factor for Alzheimer's disease, the seven studies conducted since 1991 did not reach significance. Overall, analysis of the 15 case-controlled studies did show a significant odds ratio, indicating an excess history of head injury in males (but not females) with Alzheimer's disease (OR 1.58, 95% CI 1.21-2.06), showing that a theoretical risk for Alzheimer's disease exists after head trauma but one which, so far, has failed to be paralleled by any direct evidence.

One index of accelerated ageing could be a reduced intelligence test performance over long intervals of time. However, studies that have examined cognitive ageing in those who suffered war-time missile wounds have yielded conflicting results. Corkin and colleagues [23] assessed 57 World War II missile-injury survivors 40 yr after head injury and found that many had become less mentally ‘sharp', raising the possibility of premature ageing in their sample. Walker and Blumer [24] found that 45 yr post injury, 25% of their cohort displayed varying degrees of mental deterioration. Plassman and colleagues [25] reported a raised prevalence of Alzheimer's disease in brain-injured veterans, compared with non head-injured, age-matched controls. However, the methodology employed by these studies was not as rigorous as that reported by Newcombe [26], who used a test-retest longitudinal paradigm. She failed to find evidence of mental deterioration in her military sample, employing measures of both verbal and non-verbal ability, plus tasks considered sensitive to lateralized lesions.

In a civilian context, Millar and colleagues [27] examined the cognitive status of 396 cases of head injury, 18-yr post injury. Cognitive ability was assessed using the mini-mental state examination and composite performance scores from the logical memory test, digit span and paired associate test, the Stroop, and verbal fluency tests, all of which were thought to be sensitive to prodromal stages of Alzheimer's disease. A measure of cognitive decline was obtained by comparing composite scores to an estimate of pre-morbid intellectual function. The authors report ‘profound' cognitive impairment, relative to estimates of pre-morbid ability. However, they did not compare test scores with measures obtained at an earlier stage of recovery; hence it was not possible to determine evidence of cognitive deterioration between injury and follow-up. The authors also point to the young age of their cohort (mean age 42.1 yr) as a constraint on assessing risks of cognitive deterioration and Alzheimer's disease.

Wood and Rutterford [28] compared the cognitive performance in 80 cases of severe head trauma 15-30 yr post injury (X = 20.45 yr). Performance on cognitive tests administered early in recovery was compared with measures of intelligence at a late recovery stage to see whether cognitive impairment continued to be a very long-term legacy of head trauma relative to estimates of pre-accident ability. This test-retest design also allowed an assessment of possible cognitive deterioration between early (T1) and late (T2) cognitive measures. They found that while long-term intellectual impairment clearly existed, relative to pre-accident estimates of intelligence, there was no evidence of generalized decline in performance over time that might indicate accelerated cognitive ageing. When severity of injury, age, time since injury, gender and years of education were taken into account, only years of education proved to be correlated with a change in level of intellectual performance between T1 and T2. Those who stayed in education beyond secondary school years showed a trend towards improvement on some measures of ability. While this trend was not significant, the possibility of continuing improvement occurring at very late stages of recovery could not be ruled out. The authors concluded that these findings might provide scope for optimism regarding long-term outcome of intellectual functions after head trauma. However, when data were analysed from a subgroup of their cohort, representing cases who were assessed more than 2 yr post injury, they found significant differences in those who had suffered the most severe injuries (PTA > 14 days) and those who were more than 20 yr post injury at T2. This suggests that people with the most severe injuries may well be at risk of accelerated ageing over an extended period of time, providing support for Lewin and colleagues [29] who reported deterioration in a small number of very seriously injured cases. The proportion of Wood and Rutterford's cohort that showed a reduction in intellectual functioning over time was similar to that reported by Himanen and colleagues [30] even though their sample was generally older, at a later stage post injury and included some cases of very mild injury, while the Wood and Rutterford cohort comprised cases of predominantly severe head injury.

Wood and Rutterford advise cautious interpretation of their conclusions because of the relatively small number of cases that comprised the subgroup who were first assessed after a time when no further spontaneous recovery was likely, and because some cases from the original archive of records were either not available to follow-up or refused to participate. These cases may have experienced a poor outcome, making it possible that the cases included in the follow-up study were not representative of the sample as a whole. The age of the cohort at follow-up was also a problem because many were only in the middle or late-middle age. However, studies of normal ageing have shown that while the influence of age on cognitive functioning is generally greater for those over 50 yr, significant negative age-cognition relations are evident in 18-50-yr olds, allowing for decline in some types of cognitive performance to be identified, even before the age of 50 yr [31]. Even so, there remains a need for a large prospective long-term follow-up of cases, using a test-retest paradigm that includes both a sufficient number and range of cognitive tests. However, it is encouraging that 16 yr after serious head trauma, there are no signs of major intellectual decline that might have an impact on psychosocial outcome.

Predicting long-term outcome

A variety of factors have been examined to determine how well they can predict long-term outcome after head trauma. These factors, most frequently reported in the literature, are reviewed below.

Injury severity

At early stages in recovery, injury severity has been associated with poor outcome [32-34]. However, injury severity has less influence on outcome as time from injury increases. For example, by 8 yr post injury, injury severity only reliably predicts occupational and social outcome if it is combined with age at the time of injury [35,36]. Wood and Rutterford [37] found that demographic and cognitive variables predicted outcome criteria at very late stages following head trauma more reliably than injury severity, which only predicted life satisfaction; those with less severe injuries being more satisfied with their lives. This confirms earlier impressions that the importance of injury severity as an outcome predictor reduces as time from injury progresses [35,36].

Gender

Seibert and colleagues [38] found that gender differences influenced quality of life (QoL) at 1 yr post injury, with significantly more females (69%) reporting a worse overall QoL than males (21%). Dijkers [39] also reported gender to be an important factor contributing to life satisfaction and community integration but some studies have failed to find any association with life satisfaction or depression at later stages post injury [40,41]. Kirkness and colleagues [42] assessed the interaction between gender and age in relation to outcome at 3 and 6 months post injury in a population of 157 TBI patients (124 males, 33 females) using the Extended Glasgow Outcome Scale and Functional Status Examination. They found that females aged 30 yr or older had significantly poorer outcome than either males or younger females. There was also a different rate of recovery, with women age 30 yr and older showing no improvement between 3 and 6 months post injury. The impression that outcome of TBI may be worse in women than in men has also been supported by a multi-centre study [43], which showed that women are more likely to report cognitive, affective and somatic symptoms than men. Recent meta-analytical research on eight studies, with 20 outcome variables [44], with follow-up periods ranging from 6 weeks to more than 6 yr also found that outcome was worse in women than in men. Outcome variables included death, days of PTA, length of hospitalization, return to work and a number of subjective post-concussional symptoms. Women proved to have worse outcomes on 85% of the measured variables, with an average effect size of −0.15.

Neuropsychological impairment

Evidence appears to support the view that the greater the degree of post-injury cognitive impairment, the lower the level of post-accident productivity [45]. In a review of the clinical literature, Sherer and colleagues [46] concluded that there was strong support for a relationship between neuropsychological test results and employment outcome after TBI. Klonoff and colleagues [47] found that tests of motor functioning, memory and constructional ability were related to QoL at 2-4 yr post injury. Ross and colleagues [48] also report that when combined with age, tests that measure speed of information processing significantly predicted psychosocial outcome 1 yr after severe injury. However, Wood and Rutterford [37] found that cognitive variables had a limited capacity to predict very late outcome. The only cognitive domain that made a significant contribution was working memory, which predicted community integration, satisfaction with life, and depression. Those who continue to experience problems of working memory appeared to have a low perception of their ability to deal with situations effectively, which appeared to be associated with low mood and dissatisfaction with life. They also found that a sense of self-efficacy acted as a mediator between impairment of working memory, depression and satisfaction with life.

Education

At 1 yr post injury, low pre-morbid educational levels seem to determine post injury employment, or successful return to productive activity [49,50]. The TBI Model Systems database [50] found that only 10% of those without school-leaving certificates at the time of injury were in work 2 yr later, compared to twice the number who had gone on to further education. Length of full-time education may therefore determine the nature and extent of cognitive impairment after head trauma, or be a factor influencing how well an individual adjusts to neuropsychological disability.

Lack of insight

Poor self-awareness can act as a significant barrier to social reintegration, and is regarded by some as one of the most significant predictors of late psychosocial outcome and employment [10,46,51]. Awareness of disability allows individuals to be more realistic about their ability to perform functional tasks, reducing the risk of experiencing distress when failing to cope with life demands [52-54]. An individual's ability to recognize the need for, and value of, social support can also influence life satisfaction and psychosocial adjustment [55,56]. However, the importance of social awareness is tempered by studies showing that recovery of insight can also increase the risk of depression, possibly due to a realization that expectations about recovery are not being met [57].

Personality

Kurtz and colleagues [58] and Tate [59] report a high incidence of neuroticism and decreased extraversion at 1 yr post injury. Malec and colleagues [60] found that neuroticism significantly influenced measures of participation and independence at 3 months post injury. Tyerman and Humphrey [61] reported that 72% of their cohort reported some negative changes in self-concept at just 7 months post injury. Schretlen [62] found that those with a better behavioural adjustment at 8 yr post injury had a low trait of neuroticism.

Moore and Stambrook [63] found that a ‘self-controlling' coping style and a ‘positive reappraisal' coping strategy was associated with fewer disturbances of mood and reduced the impact of physical disability, especially when combined with lower external locus of control. Williams and colleagues [64] also report that those who externally attribute the cause of their injury suffered greater anxiety and depression up to 5-yr post injury. Finset and Andersson [65] and McMillan and colleagues [66] have found that an avoidant coping style was associated with depression and reduced self-esteem.

Cognitive and demographic factors influencing very late recovery

Wood and Rutterford [37,67] used the theoretical framework provided by Kendall and Terry [68] to investigate how well cognitive and demographic variables can explain outcome at very late stages (more than 10 yr) post injury. This framework helps identify antecedents specific to head injury, to see whether people are capable of making gradual adjustments and adaptations that improve functional abilities that lead to a better quality of life. The Kendall and Terry framework hypothesizes that antecedents such as an individual's pre-injury psychosocial functioning (such as employment, marital status, etc.), combined with personal resources (such as self-concept and coping style) and environmental resources (such as social or family support), and finally situational factors, implicit to the injury (such as physical injury), would influence outcome via the mediation of appraisal and coping variables. The presence of cognitive impairment could influence the accuracy of how a person appraises their situation or selects appropriate coping methods.

The results of the Wood and Rutterford study only partially supported the existence of direct relationships between demographic and cognitive variables with very late psychosocial adjustment as depicted by the model of Kendall and Terry. They found that demographic variables predicted satisfaction with life, community integration and employment status, but not anxiety, depression or QoL. There was no evidence to indicate that appraisal and coping variables mediate relationships between psychosocial outcomes. However, when appraisal and coping were combined with other psychosocial variables as the direct predictors of outcome, every outcome, except employment status, was reliably predicted. Personality was the only variable to significantly influence all outcomes. Self-efficacy also appeared influential because it contributed to the prediction of all outcomes except for QoL. The ability of neurological variables, demographic variables and cognitive functioning to predict very long-term outcome was limited. There was little evidence to suggest that cognitive impairment indirectly affected long-term outcomes through the mediation of appraisal and coping variables.

The inability of the Kendall and Terry theory to explain psychosocial adjustment at very late stages after brain injury may be because psychological impact is greatest soon after the event. At a late stage post injury, the impact will be less and therefore the same personal resources are not required. In addition, specific demographic variables differentially influence outcome dimensions: gender appears important regarding community integration; severity influences life satisfaction; while age at injury helps to determine employment status. However, it would appear that psychosocial variables, specifically personality and self-efficacy, have the largest impact on very long-term outcome.

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Keywords:

BRAIN INJURY; TRAUMA; PSYCHOLOGY; OUTCOME; NEUROBEHAVOURAL MANIFESTATIONS

© 2008 European Society of Anaesthesiology