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Aging effect on psychosocial outcome in traumatic brain injury
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Aging Effect on Psychosocial Outcome in Traumatic Brain Injury Barbara Rothweiler, PhD, Nancy R. Temkin, PhD, Sureyya S. Dikmen, PhD ABSTRACT. Rothweiler B, Temkin NR, Dikmen SS. Aging effect on psychosocial outcome in traumatic brain injury. Arch Phys Med Rehabil 1998;79:881-7. Objective: To examine the effects of age on outcome in persons with traumatic brain injury. Design: Longitudinal cohort design. Setting: Level I trauma center. Patients: A total of 411 hospitalized subjects with mild to severe traumatic brain injury prospectively studied to 1 year; their age range was 18 to 89 years. Main Outcome Measures: Glasgow Outcome Scale, living situation, and employment. Results: Increasing age is associated with increasing levels of psychosocial limitations, especially in persons 60 years of age and older. Part of the reason is the greater severity of injury sustained by older persons as reflected in longer coma (despite equivalent initial coma depth) and greater numbers of complications and surgeries for subdural hematomas. However, the consequences of traumatic brain injuries appear to worsen with increasing age at each level of brain injury severity examined, including the milder injuries. Conclusions: Older adults clearly show less complete recovery 1 year after brain injury than younger adults, either because they have reduced reserves with which to tolerate brain injury or because their physiologic status creates a more destructive injury. Glasgow Coma Scale alone may underestimate the severity of brain injury in the aged as well as its associated consequences. Caution is advised in generalizing findings based principally on younger individuals to older adults with traumatic brain injuries. 0 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation
N
UMEROUS STUDIES have suggested that traumatic brain injury (TBI) is often associatedwith lasting disabilities that limit individuals in activities of daily living.lW3Much of the research involving psychosocial outcome after TBI has focused on young adults, who are overrepresented in the head-injured
From the Departments of Rehabilitation Medicine (Drs. Rothweiler, Dikmen), Neurological Surgery (Drs. Temkin, Dikmen), Biostatistics (Dr. Ten&in), and Psychiatry and Behavioral Sciences (Dr. Dikmen), University of Washington, Seattle, WA. Dr. Rothweiler is currently affiliated with North Central Wisconsin Rehabilitation Associates, Wausau, WI. Submitted for publication September 22, 1997. Accepted in revised form March 13, 1998. Supported by grants HS06497 from the Agency for Health Care Policy and Research. HD33677 from the National Institutes of Health-National Center for Medical Rehabilitation Research, and NS 19643 from the National Institutes of Health-National Institute of Neurologic Disorders and Stroke. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Rmrint reauests to Surevva Dikmen. PhD. Rehabilitation Medicine (Box 356490).,, \~ Univksity ofi?iashington, skattle, WA$X19<-6490. 0 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation 0003-9993/98/7908-4662$3.00/O
population.4 Traumatic injury, however, also affects a large number of elderly individuals, a segment of the population that is rapidly increasing.5-8 Epidemiologic studies of TBI indicate that there is a bimodal incidence of head trauma, one involving young adults and the other involving individuals over the age of 70.9-13Goldstein and Levin,” in their review of epidemiologic studies, indicated that brain injury incidence rates for older adults begin to increase gradually at 60 years of age and increase more dramatically after the age of 70. Schwab and Kauder7 suggested that because of general improvements in medical technology leading to increased survival and the rapid growth of the elderly population, an increase in the number of surviving elderly trauma victims can be expected. Higher mortality rates for older head-injured adults are commonly reported. 14-18For instance, Vollmer and colleagues18 reported that in a severely injured group mortality rates were 80% in individuals older than age 55 compared with 29% in individuals between the ages of 26 and 3.5 by 6 months postinjury. Additional studies have reported higher mortality rates in older adults with less severe head injuries. Kotwica and Jakubowski19 reported a mortality rate of 20% in older adults with mild head injuries, a rate that is substantially higher than that typically reported for younger adults with mild injuries.12,20 Disability in head injured survivors also increases with advancing age (see Goldstein and Levintt for a review). Primarily, studies have focused on global outcome such as Glasgow Outcome Scale (GOS)12*21and suggest that a greater proportion of older head trauma survivors show increased dependence after TBI and that older survivors show greater levels of dependence than do younger survivors. Additional indices of disability addressed in relation to elderly survivors have included length of hospital stay and discharge disposition. Such studies have indicated that the elderly generally require longer hospital staysI and are more likely to experience late neurologic decline (ie, following acute hospitalization).16 Many of the studies that have addressed the relation between increasing age and brain injury outcome have used samples that are restricted in terms of level of brain injury severity (eg, include only severehead injuries) or age range (eg, include only older adults or compare mean outcome of one older group to one younger group). Because age likely is related to mechanisms of injury (ie, motor vehicle accidents in younger vs falls in older adults), associated differential injury severity, and other medical comorbidities, it is important to further assessoutcome in broader ranges of age and injury severity to better understand the relation between these variables and brain injury outcome. For instance, further investigation is required to assesswhether brain injury severity as typically measured is equivalent across age groups (ie, is a moderate brain injury in a young adult equivalent to a moderate brain injury in an elderly adult?) with respect to its consequences. In addition, most of the studies addressing the relation between increasing age and outcome have focused on early outcome (ie, at discharge or within the first 6 months after injury). 16~18,21 Given potential differences in brain injury severity and/or recovery potential associated with age, it is important to examine longer-term outcome to assess Arch
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whether older individuals simply require longer to recover or whether their recovery is typically less complete in comparison to younger adults with head injuries of similar severity. The goal of this study was to assessthe relation between age and psychosocial outcome 1 year after injury in a large representative sample of head injured adults, including individuals of a broad range of ages and severity of brain injury. In particular, this study addressed three primary questions. (1) Is older age associated with greater psychosocial limitation. (2) If so, can the greater limitation be attributed to more severe injuries sustained by older adults as compared with younger adults? (3) In individuals with similar injury severity, what is the relation between age and psychosocial outcome? METHODS Subjects Subjects were adult TBI patients recruited at the time of injury into one of three prospective, longitudinal investigations and examined 1 year after injury. (The three studies were Behavioral Outcome in Head Injury, Patient Characteristics and Head Injury Outcome, and Dilantin Prophylaxis of Posttraumatic Seizures).’ The subjects were admitted to Harborview Medical Center in Seattle, WA. Level 1 trauma center. They were English-speaking adults in an inception cohort study who consented and who fulfilled minimum severity criteria, which consisted of any period of loss of consciousness,posttraumatic amnesia for at least 1 hour, or other objective evidence of brain injury (eg, hematoma). Additional selection criteria required that (1) the injury be serious enough to require hospitalization and (2) the patient survived at least 1 month after injury, the time of our first assessment.Twenty-one percent of the subjects came from the Behavioral Outcome Study, which recruited consecutively admitted subjects with a broad spectrum of brain injury severity and which excluded those with pre-existing conditions (eg, previous brain injury, alcohol abuse requiring treatment). The Patient Characteristics and Head Injury Outcome study contributed 49% of the subjects. This study also recruited consecutive admissions representing a broad injury severity but did not exclude cases on the basis of pre-existing conditions. The Dilantin Prophylaxis study contributed 30% of the subjects, which included patients with more severe TBI. Those subjects had a Glasgow Coma Scale (GCS) score of 10 or below on admission, or other evidence of increased risk for seizures such as cortical contusion, depressed skull fracture, or hematoma. Subjects with pre-existing conditions were excluded from this study. Participants were examined at 1 and 12 months postinjury in all three studies. Four hundred fifty-eight head-injured subjects between the ages of 18 and 89 were studied; 411 (90%) completed the l-year follow-up and were included in this study. Measures Independent variables. Age at the time of injury was the primary independent variable in this study. Participants were categorized into five age groups: 18 to 29, 30 to 39,40 to 49,50 to 59, and 60+. Depth of coma as measured using the GCS in the emergency room was the primary measure of injury severity.22Scores on the GCS range from 3 to 15, with 3 being the most severe (not responsive in eye opening, verbal, or motor modalities) to 15 being the least severe (fully oriented). Ratings of 13 to 15 are categorized as mild, 9 to 12 as moderate, and 8 or below as severe. Additional measures of brain injury severity included length of time from injury to consistently following simple commands (TFC), the presence of subdural mass lesions Arch
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requiring neurosurgery, and injury-related complications (eg, cardiac arrest, sepsis,ventriculitis). Dependent variables. Psychosocial functioning 1 year after the injury was assessed using three measures, which reflected postinjury changes from individuals’ own preinjury status. The GOS23 is a global measure of outcome that rates subjects on a combination of their dependence on others and neurologic impairments (eg, self-care, ability to participate in normal social life, and hemiparesis). The four categories used were good recovery (normal life is resumed, although patient may have minor deficits), moderate disability (disabled but independent in daily activities), severe disability/vegetative (dependent on others for daily support), and dead. In addition, information regarding living situation and employment status was gathered through a structured interview. Postinjury living situation for those living independently (including with a spouse) before injury was classified into four functional categories: those returning to preinjury living situation (eg, independent/with spouse), living with relatives or guardians (ie, representing increased dependence as compared to preinjury status), living in a group home, and living in an institution. Postinjury employment status for individuals who were employed before injury was classified into two groups: employed and unemployed. Data Analysis Kruskal-Wallis tests with correction for ties24with follow-up pairwise comparisons using the Newman-Keuls procedure25 were used to assess whether age is related to psychosocial outcome, as well as differences in demographic and injury severity indices. These analyses were supported by logistic regressions in an attempt to simultaneously account for other demographic (ie, education and gender) and injury severity indices described under the independent variables section above. RESULTS Demographics Demographic characteristics of the subjects are presented in table 1. The 18- to 29-year-old age group had the greatest number of subjects. The mean level of education by age group ranged from 12 to 13 years, with no significant differences in education across age groups. In each age group, a majority of the subjects were men, with no significant differences in the distribution of gender by age. Relation Between Age and Psychosocial Functioning Global outcome. Figure 1 shows the percentage of individuals rated as achieving good recovery, moderate disability, severe disability or vegetative, and dead as defined by the GOS for the different age groups. Note that the subjectsincluded in this study are those who survived for at least 1 month after their brain Table
1: Demographic
and Injury
Age
N
18-29 30-39 40-49
235 93
50-59 60+ There were variables.
Characteristics
Groups
Gender I% Men)
12 (1.8) 13 (2.3) 12 (3.3)
73 74 74
12 (3.5) 13 (2.5)
83 60
35 23 25 no significant
by Age
Education (yrs), Mean (SD)
differences
among
age groups
on these
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injury. One year after the injury, a significantly higher proportion of older adults were evaluated as disabled as compared with younger adults (Kruskal-Wallis x2(4) = 50.5, p < .OOOl),with individuals 60 or older significantlymore disabledthan thoseunder 50 and those 50 or older more disabledthan those under 30. As age increases,the proportion of individuals rated as achieving good recovery decreases.Approximately 70% to 75% of those under the age of 50 were rated asachieving good recovery.However, only 48% of those between the ages of 50 to 59 and 20% of those 60 and older were rated as achieving good recovery 1 year after injury. Likewise, the proportion of poor outcome is higher for older head-injured subjects. At 1 year, more than twice as many individuals older than age 60 were in a severedisability/vegetativestateor dead ascompared with those 50 to 59, and about five times asmany of those older than 60 were in a severedisability/vegetative state or dead compared with those younger than 50. These post hoc pairwise differences are all the more impressivebecauseof the relatively small sample sizes(23 and 25) in the two older age groups. The methods used account for the unequal sample sizesin a way that significancerequires larger differences in average rank when the sample sizesin the pair of categoriesare smaller. These data were also analyzed using logistic regression to examine the effects of age controlling for a variety of demographic and injury severity variables. The results of the logistic regression were consistent with those presented above (ie, age effect atp < .OOOl). A further evaluation of GOS ratings for those in the 60 + age group found that in each of the three decades represented (ie, 60s 70s and 80s) approximately 20% were rated as achieving good recovery by 1 year. However, mortality rates differed across decades within the oldest age group, with approximately 20% of those in their 60s and 70s having died by 1 year, and 4 of 6 in their 80s having died by 1 year. (The number of subjects in these subgroups was small.) Living situation. Postinjury living situation for survivors who were living independently or with a spouse preinjury is presented by age group in figure 2. Significantly fewer older individuals returned to their former living status 1 year after injury in comparison with younger individuals (Kruskal-Wallis x2(4) = 15.9, p < .004), indicating a greater likelihood of
100%
n=235
n=93
n=35
n=23
n=25
80% 60%
18-29
40-49
50-59
60+
We, vs Fig 1. GOS ratings (percentage in each category: q , dead; 0, severe/vegetative; 3, moderate; n , good) by age group (total N= 411). Individuals 60+ were significantly more disabled than those under 50 and those 50+ were more disabled than those under 30 (age effect, p < .OOOl).
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n=153
n=82
n=33
n=19
n=16
100%
80% 60% 40% 20% 0%
60+
40-49
18-29
Age, yrs Fig 2. Living situation (percentage in each category: institution; q , group home; igl, relatives; n , preinjury group for individuals who were living independently (total N= 303). Significantly more individuals over required a change to a more supervised living situation each age category less than 50 (age effect, p < .004).
II, other; q, status) by age before injury the age of 60 than those in
dependence in older individuals. That is, significantly more individuals over 60 required a change to a more supervised living situation than those in each age category younger than 50. A further examination of changes in living situation for those previously independent aged 60+ found no notable differences across decades (ie, 60s 70s and 80s). A logistic regression on whether the person was living independently controlling for demographic and injury severity variables revealed a significant linear and quadratic age effect (p < .OOl each). For individuals younger than the age of 40, changes in living situations during the first year after injury primarily reflected living with relatives, whereas changes in living situation for individuals older than the age of 50 were more likely to involve institutionalization (eg, in a nursing home) 1 year after injury. Employment. Postinjury employment status for survivors who were employed before injury is presented in figure 3. There was a trend suggesting that a smaller percentage of survivors over the age of 50 were working 1 year after the injury in comparison with younger brain injury survivors. Specifically, while half or more of preinjury workers younger than 50 were working 1 year after their injury, only about one third to one quarter of those older than 50 were working at 1 year. However, in part because of the small number of subjects in the older age groups, this trend was not significant (Kruskal-Wallis x2(4) = 8.0,p = .09). Relationship Between Age and Brain Injury Severity The second goal of this study was to examine different indices of brain injury severity in relation to increasing age and to determine whether GCS similarly classifies individuals on other brain injury severity indices in the different age groups. Table 2 provides brain injury severity information as assessed using various indices across the different age groups. Brain injury severity is most commonly assessedusing the GCS.22 The average severity of head injuries in each age group ranged from mild to moderate based on this rating (11 to 13). However, the full range of the GCS was represented in each of the age Arch
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n=147
n=74
n=24
n=lO
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n=8
80 60 40 20 0
18-29
30-39
60+
Age, yrs Fia 3. Percent of individuals who were emoloved 1 vear after iniurv by age group, for individuals who were’employeb before iniury (total A/ = 263). There was a trend, with fewer individuals over the age of 50 returning to work, that was not statistically significant (p = .09).
groups. This measure revealed no significant differences across age groups in depth of coma on admission to the emergency room (Kruskal-Wallis x2(4) = 5.9, p = .20). Individuals 60 and older required a significantly longer period of time to follow simple commands (ie, emerge from their coma) (Kruskal-Wallis x2(4) = 10.0, p < .04). The median length of time to follow commands is 24 hours or less for individuals in each category younger than age 60 as compared with 7 to 13 days for individuals in the 60+ age category. In addition, older individuals are significantly more likely to suffer complications (eg, cardiac arrest, ventriculitis, and sepsis)after brain injury than younger individuals (Kruskal-Wallis x2(4) = 11.7, p < .02), with the oldest three age groups (ie, 40t) being significantly more likely to suffer from complications than those in each of the two younger age groups. Finally, the incidence of neurosurgical interventions for subdural hematomas tends to increase with age, involving 11% of those under 30 versus 24% of those over 60, although this trend is not statistically significant (Kruskal-Wallis x2(4) = 6.0,~ = .20). Relation Between Age and Psychosocial Outcome in Subgroups of Similar Brain Injury Severity Given the differences among additional brain injury severity indices across age groups, it is important to examine the relation between age and psychosocial outcome in more tightly defined brain injury severity subgroups. To better account for brain injury severity, potential age effects were evaluated by time to Table
2: Indices GCS. Mean (SD)
of Head GCS (% 58)
Injury
TFC (Median)
Severity
by Age
Complications* 1%)
Groups Subdural Hematomas 1%)
18-29
11 (4.0)
29
6-24h
8
11
30-39 40-49 50-59
12 (3.4) 13 (3.3) 12 (3.6)
23 15 26
6-24h I-5h 6-2411
9 14 17
IO 12 22
60+
11 (3.8)
24
7-13d
28
24
* Pairwise comparisons revealed that the oldest three age groups (ie, 40+) were significantly more likely to suffer from complications than those in each of the two younger age groups.
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follow command severity subgroupings, which correlate highly with other brain injury severity indices (eg, GCS, neurosurgical evacuation of subdural bleeds, etc) as well as with neurobehavioral outcome.26 The small numbers of subjects in some of these categories dictate caution when interpreting the results. Figure 4 illustrates the GOS ratings by age group for individuals with time to follow commands (TFC) 524 hours, TFC 25 hours to 13 days, and TFC 2 14 days. Age effects were found for each of the three brain injury severity subgroups (Kruskal-Wallis x2(4) = 29.8, p < .OOOlfor TFC 524 hours; Kruskal-Wallis x2(4) = 20.9, p < .OOl for TFC 25 hours to 13 days; and Kruskal-Wallis x2(4) = 11.8, p < .02 for TFC 214 days). For individuals with TFC 524 hours, those in the 60+ age group were rated as significantly more disabled than those in each of the age groups younger than 60, with 40% of those in the 60+ group being rated as achieving good recovery at 1 year in comparison to between 75% and 94% achieving good recovery in each of the younger groups. For individuals with TFC 25 hours to 13 days, those in the 60+ age group were rated as significantly more disabled than those in each of the groups under the age of 40 and those in their 50s were rated as significantly more disabled than those in each of the age categories less than 40. Note the poor outcome for all age groups in those with the most severe injuries (ie, TFC 214 days). Nevertheless, for individuals with such severe injuries, those 60 and older were significantly more disabled than those under 40. To further reduce variability due to brain injury severity, several measures were used to select a more homogeneous group of subjects with milder head injuries. Figure 5 illustrates GOS ratings for individuals with the least severe injuries represented in the group, ie, individuals with TFC 524 hours, GCS 13 to 15, no head injury-related complications, and no neurosurgical interventions for subdural hematomas. A few of these patients did have surgery for epidural hematomas or contusion. None of these patients, however, were older than 50 years of age. Again, these results are tempered by a relatively small number of subjects. However, even for individuals with the least severe injuries represented in this group, age is associated with a significantly greater likelihood of disability 1 year after brain injury (Kruskal-Wallis x2(4) = 20.7, p < <.0005), with those 60 and older rated as significantly more dependent than those less than 60. For individuals with milder, uncomplicated brain injuries, 4 of 7 individuals over the age of 60 were rated as at least moderately disabled 1 year after the injury as compared with less than 14% in those younger than 50 years of age. DISCUSSION The results of this study suggest that there is a systematic relationship between age and psychosocial morbidity, such that older adults exhibit a less favorable outcome after TBI than younger adults. Poorer outcome associated with increased age is illustrated in terms of general level of dependence on others in daily life (ie, GOS ratings) and changes in living situation also reflecting increased dependence, with these changes being significantly greater than for younger individuals. In general, our study suggests that head injured survivors older than age 60 exhibit significantly greater morbidity 1 year after injury than younger adults. In this sample, which included survivors with a wide range of initial brain injury severity, a substantial proportion of individuals over the age of 60 showed marked psychosocial limitations. Eighty percent of individuals older than the age of 60 were rated as at least moderately disabled 1 year after injury, reflecting the need for assistancein basic daily activities and an inability to resume preinjury activities. Additionally,
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n=l IO n=138
n=56
n=12
n=28
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n=45
n=9
w.22
n=7
n=lO
80% 80% 60% 60% 40% 20% 0%
18-29
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50-59
40-49
60+
40-49
18-29
60+
Age, yrs
Age, yrs A
Time
to Follow n=51
Commands n=16
224
hours n=l
n=5
100%
n=3
-r
80% 60%
30-39
40-49
T ime to Follow ’ Commands
25 hours
18-29
60+
Age, yrs 5
100%
n=46
n=21
- 13 days
n=6
n=6
n=ll
80% 60%
40-49
18-29
50-59
Age, vs C
Time
to Follow
Commands
14 days
+
60+
Fig 5. GOS ratings (percentage in each category: S#Z, dead; 0, severe/vegetative; W, moderate; n , good) by age group for individuals with a GCS of 13 to 15, TFC of 524 hours, no head injury-related complications, and no subdural hematomas requiring surgical intervention (A/= 193). Those 60+ were rated as significantly more disabled than those younger than 60 (age effect, p < .0005).
31% of individuals over the age of 60 who were living independently before injury were residing in an institution 1 year after injury. Of those over the age of 60 who were employed before injury, only 25% were employed 1 year after injury. The results of this study, however, suggest that the ageassociated decrement with recovery from TBI begin to become apparent in the previous decade (ie, 50 to 59 years of age). In terms of general level of dependence on others (ie; GOS), significantly fewer individuals in their 50s were rated as achieving good recovery and more were rated as at least moderately disabled compared with those younger than 30 years of age. In addition, although the numbers are small, moving to an institution or group home is about twice as common among the 50- to 59-year-olds as among those younger than 50, which may be related to differential social support across the adult age spectrum. Age-associated disability indicated in this study reflects decline over and beyond what would be expected based on normal aging. Each of these measures reflects changes from preinjury status (eg, living situation for those living independently before injury) and appears to be substantially greater than would be expected to naturally occur in 1 year associated with normal aging. Predicting long-term outcome may be particularly difficult with respect to older individuals. Despite a strong trend toward increasing dependence associated with increasing age, variability in outcome was notable in the present study. For instance, Fig 4. GOS ratings (percentage in each category: E?& dead; 0, severe/vegetative; H, moderate; n , good) by age group. (A) Individuals with a TFC of 524 hours (N = 244). Those in the 60+ age group were rated as significantly more disabled than those in each of the age groups younger than 60 (age effect p < .OOOl). (B) Individuals with a TFC of 25 hours to 13 days (N = 76). Those in the 60+ age group were rated as significantly more disabled than those in each of the groups under the age of 40 and those in their 50s were rated as significantly more disabled than those in each of the age categories less than 40 (age effect p < .OOl). (C) Individuals with a TFC of 214 days (N = 90). Those 60+ were rated as significantly more disabled than those under 40 (age effect, p < .02).
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for those over 60 years of age, 20% were rated as achieving good outcome on the GOS, 16% as moderately disabled, 32% as severely disabled or vegetative, and 32% as dead. In comparison, the majority of individuals younger than age 40 were rated as achieving good recovery, with less variability in outcome. This study yielded a conservative estimate of the relation between increasing age and brain injury outcome, particularly for those with severe injuries. Only those who survived the first month after their head trauma were included, eliminating those with the most severe injuries who died early on. As mortality rates increase with increasing age,‘* the true relationship is likely to be even stronger than our findings suggest. Of course, since most brain injury mortality occurs in the first month, the mortality rates in this study should not be compared with those in studies that follow patients from injury or admission to the hospital. One possible explanation that has been advanced to account for older adults’ generally poorer outcomes after traumatic injury is that they may suffer more destructive or severe injuries than do younger adults. l4 Studies have suggested that older individuals’ recovery from traumatic head injuries is complicated by additional factors that contribute to mortality and morbidity, including a higher incidence of subdural bleeds, a higher incidence of medical complications (eg, cardiac arrest), and more comorbid health problems as compared with younger adu1ts.7~14,16,18~27 These complicating factors may in part result in more severe overall injuries in older adults than suggested by the initial GOS. The results of this study confirm significantly higher rates of complications and trends toward higher rates of subdural hematomas associated with traumatic head injuries in older adults. Head injured survivors over 60 require dramatically longer to emerge from coma than individuals in each of the younger age groups (longer than 1 week vs less than 1 day), despite equivalence in initial depth of coma. The relative overrepresentation of complications and subdural hematomas in older head-injured patients likely contributes to increased length of coma and poorer outcome found in relation to increased age. Of particular importance, these results suggest that GCS alone may underestimate the severity of the brain injury in the elderly. Therefore, age effects need to be separately added or accounted for. This finding is analogous to the greater morbidity reported by Williams and colleagues” in those with GCS of 13 to 15 whose injuries were complicated by mass lesions or skull fractures. These types of findings would be useful to consider in efforts to construct higher order brain injury severity classifications that are clinically easy to use and that attempt to improve outcome prediction. Studies examining outcome from general trauma (ie, not involving the head) in the elderly indicate markedly increased mortality, even in relation to fairly mild injuries. Champion and colleagues6 suggested that “an injury that is easily survivable in the younger population can result in life-threatening consequences for the older group.” Increased morbidity (eg, longer hospitalization, decreased functional outcome) is also associated with general trauma in the elderly.6x7Increased medical complications and comorbid health problems have been suggested as one possible cause of the age effects seen with increased age in older adults.7 Although comorbidities, as well as other system injuries sustained in the same accident that caused the brain injury, may contribute to poorer outcome in older brain injury survivors, the results of this study suggest that age-related effects still persist even when the more obvious neurologic and nonneurologic complications are controlled. In the current study, increasing Arch
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age was significantly associated with increased disability in a sample of those with milder, uncomplicated head injuries, (ie, GCS 13 to 15, TFC 524 hours, no surgery for subdural hematomas, no complications). This finding is consistent with and expands the results of Vollmer and colleagues,r8 who found that in a series of severely head-injured patients, older adults demonstrated a poorer outcome independently of other clinical variables that have a negative impact on outcome (presence of mass lesions, etc), perhaps supporting the theory that similar neurologic insults are less well tolerated by the aging brain, or the aged brain may have reduced capacity to recover. Our results have implications for sequelae associated with mild brain injury. This is an area of great interest and controversy.29-34Although differences in opinion continue, it is generally agreed that single mild TBI, in itself, in previously healthy young people is not likely to lead to persistent and significant neuropsychologic and psychosocial impairments and disabilities. 1,35Our results suggest caution in generalizing these conclusions to older persons. Note that the “milder” cases in this study did not necessarily all have “mild” injuries. TFC could have been up to 24 hours, and although the patients did not have surgery for subdural hematomas and did not have major complicating events, they could have had contusions or other bleeds (eg, epidural) including surgeries for these bleeds. These events, however, were not the cause of the age effects seen. The important point to be made is that the consequences of TBI appear to be worse as a function of age at different levels of brain injury severity, including in those with less severebrain injuries. This study rea&ms and expands upon previous studies that found that older adults demonstrate poorer outcome associated with a TBI than younger adults. This study extends previous research by prospectively examining l-year outcome in headinjured adults of a wide range of age and brain injury severity. By examining multiple brain injury severity indices and their relation to outcome acrossthe adult age spectrum, the results of this study would suggest that common categorizations of brain injury severity may require cautious use for older head-injured patients. Older adults clearly have less complete recovery by 1 year after injury than younger adults, either because of reduced reserves with which to tolerate TBI or because their physiologic status creates a more destructive injury. References
1. Dikmen SS, Ross BL, Machamer JE, Temkin NR. One year psychosocialoutcome in head injury. J Int Neuropsychol Sot 1995;1:67-77. 2. McLean A, Jr.,D&men S, Temkin N. Psychosocialrecoveryafter headinjury. Arch PhysMed Rehabil 1993;74:1041-6. 3. Oddy M, HumphreyM. Socialrecoveryduring the year following severehead injury. J Neurol NeurosurgPsychiatry1980;43:798802. 4. Roy CW, PentlandB, Miller JD. The causesand consequences of
minor headinjury in the elderly.Injury. 1986;17:220-3.
5. AmacherAL, BybeeDE. Tolerationof headinjury by the elderly.
Neurosurgery1987;20:954-8.
6. ChampionHR, CopesWS, BuyerD, FlanaganME, Bain L, Sacco
WJ. Major trauma in geriatric patients. Am J Public Health 1989;79:1278-82. I. SchwabCW, Kauder DR. Trauma in the geriatric patient. Arch Surg 1992;127:701-6. 8. Zwimpfer TJ, Moulton RJ. Neurologictraumaconcerns. Crit Care Clin 1993;9:727-39. 9. GoldsteinFC, Levin HS, PresleyRM, Seamy J, Colohan ART,
EisenbergHM, et al. Neurobehaviouralconsequencesof closed head injury in older adults. J Neurol Neurosurg Psychiatry 1994;57:961-6.
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10. Frankowski RF. Descriptive epidemiologic studies of head injury in the United States: 1974-1984. Adv Psychosom Med 1986;16: 1.53-72. 11. Goldstein FC, Levin HS. Neurobehavioral outcome of traumatic brain injury on older adults: initial findings. J Head Trauma Rehabil1995;10:57-73. 12. Miller JD, Pentland B. Head injuries in elderly patients. Neurosur-gery_ 1989;12 Suppl1:441-5. 13. Kraus JF. Epidemiology of head injury. In: Cooper PR, editor. Head iniurv. Baltimore (MD): Williams & Wilkins: 1987. v. 1-19. 14. Howard MA, Gross AS, Dacey RG, Winn HR. Acute subdural hematomas: an age-dependent clinical entity. J Neurosurg 1989;71: 858-63. 15. Mamelak AN, Pitts LH, Damron S. Predicting survival from head trauma 24 hours after the injury: a practical method with therapeutic implications. J Trauma 1996;41:91-9. 16. Pennings JL, Bachulis BL, Simons CT, Slazinski T. Survival after severe brain iniurv in the aged. Arch Sum 1993:128:787-94. 17. Teasdale G, Skene A, Pa&er L, Jenneg B. Age and outcome of severe head injury. Acta Neurochir Suppl 1979;Suppl28: 140-3. 18. Vollmer DG, Torner JC, Jane JA, Sadovnic B, Charlebois D, Eisenberg HM, et al. Age and outcome following traumatic coma: why do older patients fare worse? J Neurosurg 1991;75 Suppl:S37s49. 19. Kotwica Z, Jakubowski JK. Acute head injuries in the elderly: an analysis of 136 consecutive patients. Acta Neurochir 1992;118:98102. 20. Leurssen T, Klauber M, Marshall L. Outcome from head injury related to patient’s age. J Neurosurg 1988;68:409-16. 21. Pentland B. Jones PA. Rov CW. Miller JD. Head iniurv ., i in the elderly. Age Ageing 1986;15: 193-202. 22. Teasdale G, Jennett B. Assessment of coma and impaired consciousness: a practical scale. Lancet. 1974;ii:Sl-4. 23. Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet. 1975;i:480-4.
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24. Marascuilo LA, McSweeney M. Nonparametric and distribution free methods for the social sciences. Monterey (CA): Brooks/Cole; 1977. 25. Zar JH. Biostatistical analysis. 3rd ed. Englewood Cliffs (NJ): Prentice Hall; 1995. 26. Dacey R, Dikmen S, Temkin N, McLean A, Jr., Armsden G, Winn HR. Relative effects of brain and non-brain injuries on neuropsychological and psychosocial outcome. J Trauma 1991;31:217-22. 27. Ross A, Pitts L, Kobayashi S. Prognosticators of outcome after major head injury in the elderly. J Neurosci Nurs 1992;24:88-93. 28. Williams DH, Levin HS, Eisenberg HM. Mild head injury classification. Neurosurgery 1990;27:422-8. 29. Alexander MP. Mild traumatic brain injury: pathophysiology, natural history, and clinical management. Neurology 1995;45: 1253-60. 30. Levin HS, Mattis S, Ruff RM, Eisenberg HM, Marshall LF, Tabaddor K, et al. Neurobehavioral outcome following minor head injury: a three-center study. J Neurosurg 1987;66:234-43. 31. Putnam SH, Millis SR, Adams KM. Mild traumatic brain injury: beyond cognitive assessment. In: Grant I, Adams KM, editors. Neuropsychological assessment of neuropsychiatric disorders. New York: Oxford University Press; 1996. p. 429-551. 32. Binder LM, Rohling ML, Larrabee GJ. A review of mild head trauma. Part I: meta-analytic review of neuropsychological studies. J Clin Exp Neuropsychol1997;19:421-31. 33. Binder LM. A review of mild head trauma. Part II: clinical implications. J Clin Exp Neuropsychol1997;19:432-57. 34. Dikmen S, McLean A, Ten&in N. Neuropsychological and psychosocial consequences of minor head injury. J Neurol Neurosurg Psychiatry 1986;49:1227-32. 35. D&men SS, Machamer JE, Winn HR, Temkin NR. Neuropsychological outcome at l-year post head injury. Neuropsychology 1995:9:80-90.
Arch
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Aging Effect on Psychosocial Outcome in Traumatic Brain Injury Barbara Rothweiler, PhD, Nancy R. Temkin, PhD, Sureyya S. Dikmen, PhD ABSTRACT. Rothweiler B, Temkin NR, Dikmen SS. Aging effect on psychosocial outcome in traumatic brain injury. Arch Phys Med Rehabil 1998;79:881-7. Objective: To examine the effects of age on outcome in persons with traumatic brain injury. Design: Longitudinal cohort design. Setting: Level I trauma center. Patients: A total of 411 hospitalized subjects with mild to severe traumatic brain injury prospectively studied to 1 year; their age range was 18 to 89 years. Main Outcome Measures: Glasgow Outcome Scale, living situation, and employment. Results: Increasing age is associated with increasing levels of psychosocial limitations, especially in persons 60 years of age and older. Part of the reason is the greater severity of injury sustained by older persons as reflected in longer coma (despite equivalent initial coma depth) and greater numbers of complications and surgeries for subdural hematomas. However, the consequences of traumatic brain injuries appear to worsen with increasing age at each level of brain injury severity examined, including the milder injuries. Conclusions: Older adults clearly show less complete recovery 1 year after brain injury than younger adults, either because they have reduced reserves with which to tolerate brain injury or because their physiologic status creates a more destructive injury. Glasgow Coma Scale alone may underestimate the severity of brain injury in the aged as well as its associated consequences. Caution is advised in generalizing findings based principally on younger individuals to older adults with traumatic brain injuries. 0 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation
N
UMEROUS STUDIES have suggested that traumatic brain injury (TBI) is often associatedwith lasting disabilities that limit individuals in activities of daily living.lW3Much of the research involving psychosocial outcome after TBI has focused on young adults, who are overrepresented in the head-injured
From the Departments of Rehabilitation Medicine (Drs. Rothweiler, Dikmen), Neurological Surgery (Drs. Temkin, Dikmen), Biostatistics (Dr. Ten&in), and Psychiatry and Behavioral Sciences (Dr. Dikmen), University of Washington, Seattle, WA. Dr. Rothweiler is currently affiliated with North Central Wisconsin Rehabilitation Associates, Wausau, WI. Submitted for publication September 22, 1997. Accepted in revised form March 13, 1998. Supported by grants HS06497 from the Agency for Health Care Policy and Research. HD33677 from the National Institutes of Health-National Center for Medical Rehabilitation Research, and NS 19643 from the National Institutes of Health-National Institute of Neurologic Disorders and Stroke. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Rmrint reauests to Surevva Dikmen. PhD. Rehabilitation Medicine (Box 356490).,, \~ Univksity ofi?iashington, skattle, WA$X19<-6490. 0 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation 0003-9993/98/7908-4662$3.00/O
population.4 Traumatic injury, however, also affects a large number of elderly individuals, a segment of the population that is rapidly increasing.5-8 Epidemiologic studies of TBI indicate that there is a bimodal incidence of head trauma, one involving young adults and the other involving individuals over the age of 70.9-13Goldstein and Levin,” in their review of epidemiologic studies, indicated that brain injury incidence rates for older adults begin to increase gradually at 60 years of age and increase more dramatically after the age of 70. Schwab and Kauder7 suggested that because of general improvements in medical technology leading to increased survival and the rapid growth of the elderly population, an increase in the number of surviving elderly trauma victims can be expected. Higher mortality rates for older head-injured adults are commonly reported. 14-18For instance, Vollmer and colleagues18 reported that in a severely injured group mortality rates were 80% in individuals older than age 55 compared with 29% in individuals between the ages of 26 and 3.5 by 6 months postinjury. Additional studies have reported higher mortality rates in older adults with less severe head injuries. Kotwica and Jakubowski19 reported a mortality rate of 20% in older adults with mild head injuries, a rate that is substantially higher than that typically reported for younger adults with mild injuries.12,20 Disability in head injured survivors also increases with advancing age (see Goldstein and Levintt for a review). Primarily, studies have focused on global outcome such as Glasgow Outcome Scale (GOS)12*21and suggest that a greater proportion of older head trauma survivors show increased dependence after TBI and that older survivors show greater levels of dependence than do younger survivors. Additional indices of disability addressed in relation to elderly survivors have included length of hospital stay and discharge disposition. Such studies have indicated that the elderly generally require longer hospital staysI and are more likely to experience late neurologic decline (ie, following acute hospitalization).16 Many of the studies that have addressed the relation between increasing age and brain injury outcome have used samples that are restricted in terms of level of brain injury severity (eg, include only severehead injuries) or age range (eg, include only older adults or compare mean outcome of one older group to one younger group). Because age likely is related to mechanisms of injury (ie, motor vehicle accidents in younger vs falls in older adults), associated differential injury severity, and other medical comorbidities, it is important to further assessoutcome in broader ranges of age and injury severity to better understand the relation between these variables and brain injury outcome. For instance, further investigation is required to assesswhether brain injury severity as typically measured is equivalent across age groups (ie, is a moderate brain injury in a young adult equivalent to a moderate brain injury in an elderly adult?) with respect to its consequences. In addition, most of the studies addressing the relation between increasing age and outcome have focused on early outcome (ie, at discharge or within the first 6 months after injury). 16~18,21 Given potential differences in brain injury severity and/or recovery potential associated with age, it is important to examine longer-term outcome to assess Arch
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whether older individuals simply require longer to recover or whether their recovery is typically less complete in comparison to younger adults with head injuries of similar severity. The goal of this study was to assessthe relation between age and psychosocial outcome 1 year after injury in a large representative sample of head injured adults, including individuals of a broad range of ages and severity of brain injury. In particular, this study addressed three primary questions. (1) Is older age associated with greater psychosocial limitation. (2) If so, can the greater limitation be attributed to more severe injuries sustained by older adults as compared with younger adults? (3) In individuals with similar injury severity, what is the relation between age and psychosocial outcome? METHODS Subjects Subjects were adult TBI patients recruited at the time of injury into one of three prospective, longitudinal investigations and examined 1 year after injury. (The three studies were Behavioral Outcome in Head Injury, Patient Characteristics and Head Injury Outcome, and Dilantin Prophylaxis of Posttraumatic Seizures).’ The subjects were admitted to Harborview Medical Center in Seattle, WA. Level 1 trauma center. They were English-speaking adults in an inception cohort study who consented and who fulfilled minimum severity criteria, which consisted of any period of loss of consciousness,posttraumatic amnesia for at least 1 hour, or other objective evidence of brain injury (eg, hematoma). Additional selection criteria required that (1) the injury be serious enough to require hospitalization and (2) the patient survived at least 1 month after injury, the time of our first assessment.Twenty-one percent of the subjects came from the Behavioral Outcome Study, which recruited consecutively admitted subjects with a broad spectrum of brain injury severity and which excluded those with pre-existing conditions (eg, previous brain injury, alcohol abuse requiring treatment). The Patient Characteristics and Head Injury Outcome study contributed 49% of the subjects. This study also recruited consecutive admissions representing a broad injury severity but did not exclude cases on the basis of pre-existing conditions. The Dilantin Prophylaxis study contributed 30% of the subjects, which included patients with more severe TBI. Those subjects had a Glasgow Coma Scale (GCS) score of 10 or below on admission, or other evidence of increased risk for seizures such as cortical contusion, depressed skull fracture, or hematoma. Subjects with pre-existing conditions were excluded from this study. Participants were examined at 1 and 12 months postinjury in all three studies. Four hundred fifty-eight head-injured subjects between the ages of 18 and 89 were studied; 411 (90%) completed the l-year follow-up and were included in this study. Measures Independent variables. Age at the time of injury was the primary independent variable in this study. Participants were categorized into five age groups: 18 to 29, 30 to 39,40 to 49,50 to 59, and 60+. Depth of coma as measured using the GCS in the emergency room was the primary measure of injury severity.22Scores on the GCS range from 3 to 15, with 3 being the most severe (not responsive in eye opening, verbal, or motor modalities) to 15 being the least severe (fully oriented). Ratings of 13 to 15 are categorized as mild, 9 to 12 as moderate, and 8 or below as severe. Additional measures of brain injury severity included length of time from injury to consistently following simple commands (TFC), the presence of subdural mass lesions Arch
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requiring neurosurgery, and injury-related complications (eg, cardiac arrest, sepsis,ventriculitis). Dependent variables. Psychosocial functioning 1 year after the injury was assessed using three measures, which reflected postinjury changes from individuals’ own preinjury status. The GOS23 is a global measure of outcome that rates subjects on a combination of their dependence on others and neurologic impairments (eg, self-care, ability to participate in normal social life, and hemiparesis). The four categories used were good recovery (normal life is resumed, although patient may have minor deficits), moderate disability (disabled but independent in daily activities), severe disability/vegetative (dependent on others for daily support), and dead. In addition, information regarding living situation and employment status was gathered through a structured interview. Postinjury living situation for those living independently (including with a spouse) before injury was classified into four functional categories: those returning to preinjury living situation (eg, independent/with spouse), living with relatives or guardians (ie, representing increased dependence as compared to preinjury status), living in a group home, and living in an institution. Postinjury employment status for individuals who were employed before injury was classified into two groups: employed and unemployed. Data Analysis Kruskal-Wallis tests with correction for ties24with follow-up pairwise comparisons using the Newman-Keuls procedure25 were used to assess whether age is related to psychosocial outcome, as well as differences in demographic and injury severity indices. These analyses were supported by logistic regressions in an attempt to simultaneously account for other demographic (ie, education and gender) and injury severity indices described under the independent variables section above. RESULTS Demographics Demographic characteristics of the subjects are presented in table 1. The 18- to 29-year-old age group had the greatest number of subjects. The mean level of education by age group ranged from 12 to 13 years, with no significant differences in education across age groups. In each age group, a majority of the subjects were men, with no significant differences in the distribution of gender by age. Relation Between Age and Psychosocial Functioning Global outcome. Figure 1 shows the percentage of individuals rated as achieving good recovery, moderate disability, severe disability or vegetative, and dead as defined by the GOS for the different age groups. Note that the subjectsincluded in this study are those who survived for at least 1 month after their brain Table
1: Demographic
and Injury
Age
N
18-29 30-39 40-49
235 93
50-59 60+ There were variables.
Characteristics
Groups
Gender I% Men)
12 (1.8) 13 (2.3) 12 (3.3)
73 74 74
12 (3.5) 13 (2.5)
83 60
35 23 25 no significant
by Age
Education (yrs), Mean (SD)
differences
among
age groups
on these
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injury. One year after the injury, a significantly higher proportion of older adults were evaluated as disabled as compared with younger adults (Kruskal-Wallis x2(4) = 50.5, p < .OOOl),with individuals 60 or older significantlymore disabledthan thoseunder 50 and those 50 or older more disabledthan those under 30. As age increases,the proportion of individuals rated as achieving good recovery decreases.Approximately 70% to 75% of those under the age of 50 were rated asachieving good recovery.However, only 48% of those between the ages of 50 to 59 and 20% of those 60 and older were rated as achieving good recovery 1 year after injury. Likewise, the proportion of poor outcome is higher for older head-injured subjects. At 1 year, more than twice as many individuals older than age 60 were in a severedisability/vegetativestateor dead ascompared with those 50 to 59, and about five times asmany of those older than 60 were in a severedisability/vegetative state or dead compared with those younger than 50. These post hoc pairwise differences are all the more impressivebecauseof the relatively small sample sizes(23 and 25) in the two older age groups. The methods used account for the unequal sample sizesin a way that significancerequires larger differences in average rank when the sample sizesin the pair of categoriesare smaller. These data were also analyzed using logistic regression to examine the effects of age controlling for a variety of demographic and injury severity variables. The results of the logistic regression were consistent with those presented above (ie, age effect atp < .OOOl). A further evaluation of GOS ratings for those in the 60 + age group found that in each of the three decades represented (ie, 60s 70s and 80s) approximately 20% were rated as achieving good recovery by 1 year. However, mortality rates differed across decades within the oldest age group, with approximately 20% of those in their 60s and 70s having died by 1 year, and 4 of 6 in their 80s having died by 1 year. (The number of subjects in these subgroups was small.) Living situation. Postinjury living situation for survivors who were living independently or with a spouse preinjury is presented by age group in figure 2. Significantly fewer older individuals returned to their former living status 1 year after injury in comparison with younger individuals (Kruskal-Wallis x2(4) = 15.9, p < .004), indicating a greater likelihood of
100%
n=235
n=93
n=35
n=23
n=25
80% 60%
18-29
40-49
50-59
60+
We, vs Fig 1. GOS ratings (percentage in each category: q , dead; 0, severe/vegetative; 3, moderate; n , good) by age group (total N= 411). Individuals 60+ were significantly more disabled than those under 50 and those 50+ were more disabled than those under 30 (age effect, p < .OOOl).
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n=153
n=82
n=33
n=19
n=16
100%
80% 60% 40% 20% 0%
60+
40-49
18-29
Age, yrs Fig 2. Living situation (percentage in each category: institution; q , group home; igl, relatives; n , preinjury group for individuals who were living independently (total N= 303). Significantly more individuals over required a change to a more supervised living situation each age category less than 50 (age effect, p < .004).
II, other; q, status) by age before injury the age of 60 than those in
dependence in older individuals. That is, significantly more individuals over 60 required a change to a more supervised living situation than those in each age category younger than 50. A further examination of changes in living situation for those previously independent aged 60+ found no notable differences across decades (ie, 60s 70s and 80s). A logistic regression on whether the person was living independently controlling for demographic and injury severity variables revealed a significant linear and quadratic age effect (p < .OOl each). For individuals younger than the age of 40, changes in living situations during the first year after injury primarily reflected living with relatives, whereas changes in living situation for individuals older than the age of 50 were more likely to involve institutionalization (eg, in a nursing home) 1 year after injury. Employment. Postinjury employment status for survivors who were employed before injury is presented in figure 3. There was a trend suggesting that a smaller percentage of survivors over the age of 50 were working 1 year after the injury in comparison with younger brain injury survivors. Specifically, while half or more of preinjury workers younger than 50 were working 1 year after their injury, only about one third to one quarter of those older than 50 were working at 1 year. However, in part because of the small number of subjects in the older age groups, this trend was not significant (Kruskal-Wallis x2(4) = 8.0,p = .09). Relationship Between Age and Brain Injury Severity The second goal of this study was to examine different indices of brain injury severity in relation to increasing age and to determine whether GCS similarly classifies individuals on other brain injury severity indices in the different age groups. Table 2 provides brain injury severity information as assessed using various indices across the different age groups. Brain injury severity is most commonly assessedusing the GCS.22 The average severity of head injuries in each age group ranged from mild to moderate based on this rating (11 to 13). However, the full range of the GCS was represented in each of the age Arch
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n=147
n=74
n=24
n=lO
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n=8
80 60 40 20 0
18-29
30-39
60+
Age, yrs Fia 3. Percent of individuals who were emoloved 1 vear after iniurv by age group, for individuals who were’employeb before iniury (total A/ = 263). There was a trend, with fewer individuals over the age of 50 returning to work, that was not statistically significant (p = .09).
groups. This measure revealed no significant differences across age groups in depth of coma on admission to the emergency room (Kruskal-Wallis x2(4) = 5.9, p = .20). Individuals 60 and older required a significantly longer period of time to follow simple commands (ie, emerge from their coma) (Kruskal-Wallis x2(4) = 10.0, p < .04). The median length of time to follow commands is 24 hours or less for individuals in each category younger than age 60 as compared with 7 to 13 days for individuals in the 60+ age category. In addition, older individuals are significantly more likely to suffer complications (eg, cardiac arrest, ventriculitis, and sepsis)after brain injury than younger individuals (Kruskal-Wallis x2(4) = 11.7, p < .02), with the oldest three age groups (ie, 40t) being significantly more likely to suffer from complications than those in each of the two younger age groups. Finally, the incidence of neurosurgical interventions for subdural hematomas tends to increase with age, involving 11% of those under 30 versus 24% of those over 60, although this trend is not statistically significant (Kruskal-Wallis x2(4) = 6.0,~ = .20). Relation Between Age and Psychosocial Outcome in Subgroups of Similar Brain Injury Severity Given the differences among additional brain injury severity indices across age groups, it is important to examine the relation between age and psychosocial outcome in more tightly defined brain injury severity subgroups. To better account for brain injury severity, potential age effects were evaluated by time to Table
2: Indices GCS. Mean (SD)
of Head GCS (% 58)
Injury
TFC (Median)
Severity
by Age
Complications* 1%)
Groups Subdural Hematomas 1%)
18-29
11 (4.0)
29
6-24h
8
11
30-39 40-49 50-59
12 (3.4) 13 (3.3) 12 (3.6)
23 15 26
6-24h I-5h 6-2411
9 14 17
IO 12 22
60+
11 (3.8)
24
7-13d
28
24
* Pairwise comparisons revealed that the oldest three age groups (ie, 40+) were significantly more likely to suffer from complications than those in each of the two younger age groups.
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follow command severity subgroupings, which correlate highly with other brain injury severity indices (eg, GCS, neurosurgical evacuation of subdural bleeds, etc) as well as with neurobehavioral outcome.26 The small numbers of subjects in some of these categories dictate caution when interpreting the results. Figure 4 illustrates the GOS ratings by age group for individuals with time to follow commands (TFC) 524 hours, TFC 25 hours to 13 days, and TFC 2 14 days. Age effects were found for each of the three brain injury severity subgroups (Kruskal-Wallis x2(4) = 29.8, p < .OOOlfor TFC 524 hours; Kruskal-Wallis x2(4) = 20.9, p < .OOl for TFC 25 hours to 13 days; and Kruskal-Wallis x2(4) = 11.8, p < .02 for TFC 214 days). For individuals with TFC 524 hours, those in the 60+ age group were rated as significantly more disabled than those in each of the age groups younger than 60, with 40% of those in the 60+ group being rated as achieving good recovery at 1 year in comparison to between 75% and 94% achieving good recovery in each of the younger groups. For individuals with TFC 25 hours to 13 days, those in the 60+ age group were rated as significantly more disabled than those in each of the groups under the age of 40 and those in their 50s were rated as significantly more disabled than those in each of the age categories less than 40. Note the poor outcome for all age groups in those with the most severe injuries (ie, TFC 214 days). Nevertheless, for individuals with such severe injuries, those 60 and older were significantly more disabled than those under 40. To further reduce variability due to brain injury severity, several measures were used to select a more homogeneous group of subjects with milder head injuries. Figure 5 illustrates GOS ratings for individuals with the least severe injuries represented in the group, ie, individuals with TFC 524 hours, GCS 13 to 15, no head injury-related complications, and no neurosurgical interventions for subdural hematomas. A few of these patients did have surgery for epidural hematomas or contusion. None of these patients, however, were older than 50 years of age. Again, these results are tempered by a relatively small number of subjects. However, even for individuals with the least severe injuries represented in this group, age is associated with a significantly greater likelihood of disability 1 year after brain injury (Kruskal-Wallis x2(4) = 20.7, p < <.0005), with those 60 and older rated as significantly more dependent than those less than 60. For individuals with milder, uncomplicated brain injuries, 4 of 7 individuals over the age of 60 were rated as at least moderately disabled 1 year after the injury as compared with less than 14% in those younger than 50 years of age. DISCUSSION The results of this study suggest that there is a systematic relationship between age and psychosocial morbidity, such that older adults exhibit a less favorable outcome after TBI than younger adults. Poorer outcome associated with increased age is illustrated in terms of general level of dependence on others in daily life (ie, GOS ratings) and changes in living situation also reflecting increased dependence, with these changes being significantly greater than for younger individuals. In general, our study suggests that head injured survivors older than age 60 exhibit significantly greater morbidity 1 year after injury than younger adults. In this sample, which included survivors with a wide range of initial brain injury severity, a substantial proportion of individuals over the age of 60 showed marked psychosocial limitations. Eighty percent of individuals older than the age of 60 were rated as at least moderately disabled 1 year after injury, reflecting the need for assistancein basic daily activities and an inability to resume preinjury activities. Additionally,
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n=l IO n=138
n=56
n=12
n=28
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n=45
n=9
w.22
n=7
n=lO
80% 80% 60% 60% 40% 20% 0%
18-29
30-39
50-59
40-49
60+
40-49
18-29
60+
Age, yrs
Age, yrs A
Time
to Follow n=51
Commands n=16
224
hours n=l
n=5
100%
n=3
-r
80% 60%
30-39
40-49
T ime to Follow ’ Commands
25 hours
18-29
60+
Age, yrs 5
100%
n=46
n=21
- 13 days
n=6
n=6
n=ll
80% 60%
40-49
18-29
50-59
Age, vs C
Time
to Follow
Commands
14 days
+
60+
Fig 5. GOS ratings (percentage in each category: S#Z, dead; 0, severe/vegetative; W, moderate; n , good) by age group for individuals with a GCS of 13 to 15, TFC of 524 hours, no head injury-related complications, and no subdural hematomas requiring surgical intervention (A/= 193). Those 60+ were rated as significantly more disabled than those younger than 60 (age effect, p < .0005).
31% of individuals over the age of 60 who were living independently before injury were residing in an institution 1 year after injury. Of those over the age of 60 who were employed before injury, only 25% were employed 1 year after injury. The results of this study, however, suggest that the ageassociated decrement with recovery from TBI begin to become apparent in the previous decade (ie, 50 to 59 years of age). In terms of general level of dependence on others (ie; GOS), significantly fewer individuals in their 50s were rated as achieving good recovery and more were rated as at least moderately disabled compared with those younger than 30 years of age. In addition, although the numbers are small, moving to an institution or group home is about twice as common among the 50- to 59-year-olds as among those younger than 50, which may be related to differential social support across the adult age spectrum. Age-associated disability indicated in this study reflects decline over and beyond what would be expected based on normal aging. Each of these measures reflects changes from preinjury status (eg, living situation for those living independently before injury) and appears to be substantially greater than would be expected to naturally occur in 1 year associated with normal aging. Predicting long-term outcome may be particularly difficult with respect to older individuals. Despite a strong trend toward increasing dependence associated with increasing age, variability in outcome was notable in the present study. For instance, Fig 4. GOS ratings (percentage in each category: E?& dead; 0, severe/vegetative; H, moderate; n , good) by age group. (A) Individuals with a TFC of 524 hours (N = 244). Those in the 60+ age group were rated as significantly more disabled than those in each of the age groups younger than 60 (age effect p < .OOOl). (B) Individuals with a TFC of 25 hours to 13 days (N = 76). Those in the 60+ age group were rated as significantly more disabled than those in each of the groups under the age of 40 and those in their 50s were rated as significantly more disabled than those in each of the age categories less than 40 (age effect p < .OOl). (C) Individuals with a TFC of 214 days (N = 90). Those 60+ were rated as significantly more disabled than those under 40 (age effect, p < .02).
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for those over 60 years of age, 20% were rated as achieving good outcome on the GOS, 16% as moderately disabled, 32% as severely disabled or vegetative, and 32% as dead. In comparison, the majority of individuals younger than age 40 were rated as achieving good recovery, with less variability in outcome. This study yielded a conservative estimate of the relation between increasing age and brain injury outcome, particularly for those with severe injuries. Only those who survived the first month after their head trauma were included, eliminating those with the most severe injuries who died early on. As mortality rates increase with increasing age,‘* the true relationship is likely to be even stronger than our findings suggest. Of course, since most brain injury mortality occurs in the first month, the mortality rates in this study should not be compared with those in studies that follow patients from injury or admission to the hospital. One possible explanation that has been advanced to account for older adults’ generally poorer outcomes after traumatic injury is that they may suffer more destructive or severe injuries than do younger adults. l4 Studies have suggested that older individuals’ recovery from traumatic head injuries is complicated by additional factors that contribute to mortality and morbidity, including a higher incidence of subdural bleeds, a higher incidence of medical complications (eg, cardiac arrest), and more comorbid health problems as compared with younger adu1ts.7~14,16,18~27 These complicating factors may in part result in more severe overall injuries in older adults than suggested by the initial GOS. The results of this study confirm significantly higher rates of complications and trends toward higher rates of subdural hematomas associated with traumatic head injuries in older adults. Head injured survivors over 60 require dramatically longer to emerge from coma than individuals in each of the younger age groups (longer than 1 week vs less than 1 day), despite equivalence in initial depth of coma. The relative overrepresentation of complications and subdural hematomas in older head-injured patients likely contributes to increased length of coma and poorer outcome found in relation to increased age. Of particular importance, these results suggest that GCS alone may underestimate the severity of the brain injury in the elderly. Therefore, age effects need to be separately added or accounted for. This finding is analogous to the greater morbidity reported by Williams and colleagues” in those with GCS of 13 to 15 whose injuries were complicated by mass lesions or skull fractures. These types of findings would be useful to consider in efforts to construct higher order brain injury severity classifications that are clinically easy to use and that attempt to improve outcome prediction. Studies examining outcome from general trauma (ie, not involving the head) in the elderly indicate markedly increased mortality, even in relation to fairly mild injuries. Champion and colleagues6 suggested that “an injury that is easily survivable in the younger population can result in life-threatening consequences for the older group.” Increased morbidity (eg, longer hospitalization, decreased functional outcome) is also associated with general trauma in the elderly.6x7Increased medical complications and comorbid health problems have been suggested as one possible cause of the age effects seen with increased age in older adults.7 Although comorbidities, as well as other system injuries sustained in the same accident that caused the brain injury, may contribute to poorer outcome in older brain injury survivors, the results of this study suggest that age-related effects still persist even when the more obvious neurologic and nonneurologic complications are controlled. In the current study, increasing Arch
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age was significantly associated with increased disability in a sample of those with milder, uncomplicated head injuries, (ie, GCS 13 to 15, TFC 524 hours, no surgery for subdural hematomas, no complications). This finding is consistent with and expands the results of Vollmer and colleagues,r8 who found that in a series of severely head-injured patients, older adults demonstrated a poorer outcome independently of other clinical variables that have a negative impact on outcome (presence of mass lesions, etc), perhaps supporting the theory that similar neurologic insults are less well tolerated by the aging brain, or the aged brain may have reduced capacity to recover. Our results have implications for sequelae associated with mild brain injury. This is an area of great interest and controversy.29-34Although differences in opinion continue, it is generally agreed that single mild TBI, in itself, in previously healthy young people is not likely to lead to persistent and significant neuropsychologic and psychosocial impairments and disabilities. 1,35Our results suggest caution in generalizing these conclusions to older persons. Note that the “milder” cases in this study did not necessarily all have “mild” injuries. TFC could have been up to 24 hours, and although the patients did not have surgery for subdural hematomas and did not have major complicating events, they could have had contusions or other bleeds (eg, epidural) including surgeries for these bleeds. These events, however, were not the cause of the age effects seen. The important point to be made is that the consequences of TBI appear to be worse as a function of age at different levels of brain injury severity, including in those with less severebrain injuries. This study rea&ms and expands upon previous studies that found that older adults demonstrate poorer outcome associated with a TBI than younger adults. This study extends previous research by prospectively examining l-year outcome in headinjured adults of a wide range of age and brain injury severity. By examining multiple brain injury severity indices and their relation to outcome acrossthe adult age spectrum, the results of this study would suggest that common categorizations of brain injury severity may require cautious use for older head-injured patients. Older adults clearly have less complete recovery by 1 year after injury than younger adults, either because of reduced reserves with which to tolerate TBI or because their physiologic status creates a more destructive injury. References
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WJ. Major trauma in geriatric patients. Am J Public Health 1989;79:1278-82. I. SchwabCW, Kauder DR. Trauma in the geriatric patient. Arch Surg 1992;127:701-6. 8. Zwimpfer TJ, Moulton RJ. Neurologictraumaconcerns. Crit Care Clin 1993;9:727-39. 9. GoldsteinFC, Levin HS, PresleyRM, Seamy J, Colohan ART,
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10. Frankowski RF. Descriptive epidemiologic studies of head injury in the United States: 1974-1984. Adv Psychosom Med 1986;16: 1.53-72. 11. Goldstein FC, Levin HS. Neurobehavioral outcome of traumatic brain injury on older adults: initial findings. J Head Trauma Rehabil1995;10:57-73. 12. Miller JD, Pentland B. Head injuries in elderly patients. Neurosur-gery_ 1989;12 Suppl1:441-5. 13. Kraus JF. Epidemiology of head injury. In: Cooper PR, editor. Head iniurv. Baltimore (MD): Williams & Wilkins: 1987. v. 1-19. 14. Howard MA, Gross AS, Dacey RG, Winn HR. Acute subdural hematomas: an age-dependent clinical entity. J Neurosurg 1989;71: 858-63. 15. Mamelak AN, Pitts LH, Damron S. Predicting survival from head trauma 24 hours after the injury: a practical method with therapeutic implications. J Trauma 1996;41:91-9. 16. Pennings JL, Bachulis BL, Simons CT, Slazinski T. Survival after severe brain iniurv in the aged. Arch Sum 1993:128:787-94. 17. Teasdale G, Skene A, Pa&er L, Jenneg B. Age and outcome of severe head injury. Acta Neurochir Suppl 1979;Suppl28: 140-3. 18. Vollmer DG, Torner JC, Jane JA, Sadovnic B, Charlebois D, Eisenberg HM, et al. Age and outcome following traumatic coma: why do older patients fare worse? J Neurosurg 1991;75 Suppl:S37s49. 19. Kotwica Z, Jakubowski JK. Acute head injuries in the elderly: an analysis of 136 consecutive patients. Acta Neurochir 1992;118:98102. 20. Leurssen T, Klauber M, Marshall L. Outcome from head injury related to patient’s age. J Neurosurg 1988;68:409-16. 21. Pentland B. Jones PA. Rov CW. Miller JD. Head iniurv ., i in the elderly. Age Ageing 1986;15: 193-202. 22. Teasdale G, Jennett B. Assessment of coma and impaired consciousness: a practical scale. Lancet. 1974;ii:Sl-4. 23. Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet. 1975;i:480-4.
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24. Marascuilo LA, McSweeney M. Nonparametric and distribution free methods for the social sciences. Monterey (CA): Brooks/Cole; 1977. 25. Zar JH. Biostatistical analysis. 3rd ed. Englewood Cliffs (NJ): Prentice Hall; 1995. 26. Dacey R, Dikmen S, Temkin N, McLean A, Jr., Armsden G, Winn HR. Relative effects of brain and non-brain injuries on neuropsychological and psychosocial outcome. J Trauma 1991;31:217-22. 27. Ross A, Pitts L, Kobayashi S. Prognosticators of outcome after major head injury in the elderly. J Neurosci Nurs 1992;24:88-93. 28. Williams DH, Levin HS, Eisenberg HM. Mild head injury classification. Neurosurgery 1990;27:422-8. 29. Alexander MP. Mild traumatic brain injury: pathophysiology, natural history, and clinical management. Neurology 1995;45: 1253-60. 30. Levin HS, Mattis S, Ruff RM, Eisenberg HM, Marshall LF, Tabaddor K, et al. Neurobehavioral outcome following minor head injury: a three-center study. J Neurosurg 1987;66:234-43. 31. Putnam SH, Millis SR, Adams KM. Mild traumatic brain injury: beyond cognitive assessment. In: Grant I, Adams KM, editors. Neuropsychological assessment of neuropsychiatric disorders. New York: Oxford University Press; 1996. p. 429-551. 32. Binder LM, Rohling ML, Larrabee GJ. A review of mild head trauma. Part I: meta-analytic review of neuropsychological studies. J Clin Exp Neuropsychol1997;19:421-31. 33. Binder LM. A review of mild head trauma. Part II: clinical implications. J Clin Exp Neuropsychol1997;19:432-57. 34. Dikmen S, McLean A, Ten&in N. Neuropsychological and psychosocial consequences of minor head injury. J Neurol Neurosurg Psychiatry 1986;49:1227-32. 35. D&men SS, Machamer JE, Winn HR, Temkin NR. Neuropsychological outcome at l-year post head injury. Neuropsychology 1995:9:80-90.
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