impact of age on long-term cognitive function

7/31/2019 Impact of Age on Long-Term Cognitive Function

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Impact of Age on Long-Term Cognitive FunctionAfter Traumatic Brain Injury

Dawn Senathi-Raja

Monash University

Jennie Ponsford

Monash University; Monash-Epworth Rehabilitation ResearchCentre, Epworth Hospital; and National Trauma ResearchInstitute

Michael SchonbergerMonash University; and Monash-Epworth Rehabilitation Research Centre,

Epworth Hospital

Objective: To examine the association of age and time postinjury with cognitive outcome 5–22 yearsfollowing traumatic brain injury (TBI), in relation to matched uninjured controls.Methods: One hundredtwelve participants with mild to very severe TBI, aged 16–81 years at the time of injury, werecognitively assessed on measures of processing speed and attention, verbal and visual memory, executivefunction, and working memory. Results were compared with those of 112 healthy controls individuallymatched for current age, gender, education, and estimated IQ. Results: Older injured individualsperformed worse than did younger injured individuals across all cognitive domains, after controlling forthe performance of controls. In relation to matched controls, long-time survivors performed dispropor-tionately worse than did more recently injured individuals, irrespective of age. Conclusions: Aftermaximum spontaneous recovery from TBI, poorer cognitive functioning appears to be associated withboth older age at the time of injury and increased time postinjury. These findings have implications forprognosis, early treatment recommendations, and long-term issues of differential diagnosis and manage-ment planning.

Keywords: aging, neuropsychology, traumatic brain injury, brain plasticity, long-term outcome

With advancing age, the volume of gray and white matter in thebrain has been shown to decrease (Raz & Rodrigue, 2006).Healthy aging is also associated with shrinking neuronal size(Shimada, 1999), reduced synaptic density (Terry & Katzman,

2001), and decreasing neurotransmitter levels (Volkow et al.,1998). These processes take place from the time of young adult-hood and occur at an increasing rate beyond the age of 50 years(Scahill et al., 2003). In order to compensate for cortical atrophywith increasing age, the brain generates richer dendritic connec-tions (Luebke & Rosene, 2003).

Previous research has identified age as a factor associated withoutcome following brain injury (Teuber, 1975). Histopathologicalstudies have provided evidence for increased amyloid depositionas a function of increasing age (Adle-Biassette et al., 1996).Clinical studies have shown that regardless of injury severity andmechanism, older individuals have a higher propensity for intra-cerebral and subdural hematomas, which may be explained, in

part, by the increased stretching and weakening of bridging veins,which is associated with age-related cerebral atrophy (Goleburn &Golden, 2001).

On the basis of animal research, Kolb (1995) has suggested that

the brain may use the same mechanisms for recovery and adapta-tion to aging and therefore have a finite capacity for plasticity. Heargues that as the injured brain ages, decline may occur morerapidly because the brain’s compensatory capacity may have al-ready been used in response to the earlier brain injury (Kolb,1995). Human studies have explored this notion and the field of penetrating head injury research has been instrumental in advanc-ing our understanding of the effect of age on long-term cognitiveoutcome (Raymont et al., 2008; Teuber, 1975). One such studyshowed that after missile wounds to the brain, survivors demon-strated accelerated cognitive decline with increasing age, in rela-tion to orthopaedic controls (Corkin, Rosen, Sullivan, & Clegg,1989). This led Corkin et al. (1989) to conclude that head injury

sustained in young adulthood has a negative impact on the agingprocess. Although the cognitive tests in this study were relativelyunsophisticated and the sample size small and comprising partic-ipants with penetrating head injury, these pioneer findings pro-vided the impetus for further investigations into aging and recov-ery from brain injury.

Findings from closed head injury research regarding theimpact of age on outcome have been mixed (Himanen et al.,2006; Johnstone, Childers, & Hoerner, 1998; Klein, Houx, &Jolles, 1996; Wood & Rutterford, 2006). Klein et al. (1996)tested the hypothesis that traumatic brain injury (TBI) accen-tuates the effects of normal biological aging in a mild to

Dawn Senathi-Raja, School of Psychology, Psychiatry and Psychologi-cal Medicine, Monash University; Jennie Ponsford, School of Psychology,Psychiatry and Psychological Medicine, Monash University, Monash-Ep-worth Rehabilitation Research Centre, Epworth Hospital, and NationalTrauma Research Institute; and Michael Schonberger, School of Psychol-ogy, Psychiatry and Psychological Medicine, Monash University, andMonash-Epworth Rehabilitation Research Centre, Epworth Hospital.

Correspondence concerning this article should be addressed to JenniePonsford, School of Psychology, Psychiatry and Psychological Medicine,Monash University, Melbourne, Victoria 3800 Australia. E-mail: [email protected]

Neuropsychology © 2010 American Psychological Association2010, Vol. 24, No. 3, 336–344 0894-4105/10/$12.00 DOI: 10.1037/a0018239

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moderately injured closed head injury population. On a percep-tual interference task, the performance of injured middle-agedindividuals was disproportionately worse than that of olderinjured individuals, and more akin to that of the older controlgroup. They explained this finding by suggesting that age-related decline that normally manifests after the age of 60 yearsin healthy individuals occurs prematurely by the age of 40 –50years if an individual has sustained a TBI. The interpretation of this finding is open to question, given that only a single testmeasure was used in cognitive assessment, there was no methodfor ensuring comparable educational background or estimatedgeneral intelligence, and heterogeneity in time point postinjurywas not controlled for. Johnstone et al.’s (1998) cross-sectionalstudy found no relative decline in memory, attention, or pro-cessing speed with increasing age. This led Johnstone et al. toconclude that aging has a neutral effect on the degree of cognitive impairment after TBI. However, without factoringinto their analyses crucial variables such as the time elapsedsince injury, age at injury, and severity of injury, any relation-ship inferred between age and level of cognitive impairment is

tenuous.Himanen et al.’s (2006) longitudinal study found that higher

age at injury (especially age over 60 years) was a significantrisk factor for cognitive decline, whereas younger age at injurywas predictive of improvement in cognition. However, someelderly patients in their study had dementia, making it difficultto attribute their findings to TBI-related effects not confoundedby other neurodegenerative pathology. Moreover, acutely in-

jured individuals were included at the first assessment. Drawingcomparisons between acute stage cognition and cognitive per-formance several decades later can provide an overly optimisticimpression of cognitive gains, given that spontaneous recoveryis likely in the early post-TBI stage. Finally, the original as-sessment included pediatric patients, whose long-term improve-ments may in part have been attributable to normal develop-mental gains. In Wood and Rutterford’s (2006) investigation of the notion of accelerated cognitive aging in closed TBI, com-parisons between National Adult Reading Test (NART)-pre-dicted preaccident IQ and full-scale IQ scores at the first andsecond time points revealed that age at injury had a negativeimpact on long-term cognitive outcome. They interpreted theminor percentage of deterioration found in their longitudinalstudy as evidence against accelerated aging following TBI.However, they rightly acknowledged the confounding effect of including patients seen for assessment within 2 years of injury(some as early as 1 week postinjury) on their findings of minimal decline, particularly given that these patients com-

prised 79% of their cohort.The present study aimed to examine, in individuals with TBI

who were at least 5 years postinjury—in relation to uninjuredcontrols individually matched for age, gender, and IQ—the fol-lowing: (1) the association between age at injury and cognitiveperformance; it was hypothesized that patients who were older attime of injury would show more impaired performance on cogni-tive tasks than would younger individuals; (2) the associationbetween time postinjury and cognitive performance; greater timepostinjury was predicted to be associated with poorer cognitiveperformance; and (3) whether there was an interaction betweentime postinjury and age at injury in terms of cognitive perfor-

mance; it was expected that greater time postinjury would beassociated with more impaired cognitive performance in olderpatients than in younger patients.

Method

Participants

Participants with TBI were recruited from the database of pa-tients with TBI receiving rehabilitation between 1984 and 2002 atEpworth Hospital, Melbourne, Australia. In order to examine theinfluences of age, an attempt was made to recruit equal numbersof participants across age groups with a broad representation of time postinjury, from 5 to 22 years postinjury. An independentresearcher divided the database into subgroups of those aged16–34, 35–54, and 55 years or older at the time of injurywith a mean time postinjury of 11.36 (SD 2.91), 11.97(SD 4.00), and 10.21 (SD 3.86) years, respectively. Indi-vidual SPSS codes were entered into a random number gener-ator program from the website www.random.org. Randomlyselected participants from each age group were contacted until

there were three approximately equal groups of consenting andeligible participants. Patients were excluded from the study if there was evidence of subsequent head injury (n 1), historyof other neurological disease (n 1) or degenerative dementia(n 6), significant psychiatric illness (n 2), or drug oralcohol dependency (n 1). Twenty-three patients were ex-cluded because they were inappropriate for neuropsychologicalassessment owing to poor vision, hearing, physical function, orgeneral health. An additional 27 patients were deceased, 52were living interstate or overseas, and 62 declined to partici-pate.

Of the TBI cohort recruited, 39 participants (34.8%) were aged16–34 years, 39 participants (34.8%) were aged 35–54 years,and 34 participants (30.4%) were aged 55 years and over, with theproportion of men in each of the groups being 61.5, 64.1, and 52.9,respectively. On the basis of tests of analysis of variance(ANOVA) and Pearson’s 2 analysis, there was no significantdifference in time postinjury, F (2, 109) 2.22, p .11,gender, 2(2, N 112) 1.02, p .60, posttraumatic amnesia(PTA), F (2, 109) 0.14, p .87, and estimated premorbidintelligence, F (2, 109) 0.84, p .44, across the threesubgroups. Across the three age-atinjury groups from young-est to oldest, the mean scores for time postinjury were 11.36(SD 2.91), 11.97 (SD 4.00), and 10.21 (SD 3.86); forPTA were 27.46 (SD 25.60), 24.26 (SD 29.97) and 26.44(SD 24.88); and for estimated premorbid intelligence were103.15 (SD 9.65), 101.54 (SD 10.17), and 100.24

(SD 9.08). According to Pearson’s 2

analyses, there was nosignificant difference in age between those who had neurosur-gery and those who did not, 2(2, N 112) 0.38, p .83,and between those with and without positive computerizedtomography (CT) brain scan evidence, 2(2, N 112) 2.36, p .31. Pearson’s 2 analyses revealed that the gender ratios ineach age bracket were commensurate with those of the TBIpopulation in Australia (O’Connor & Cripps, 1999). Chi-squared analyses, Mann–Whitney U tests, and t tests revealedno significant differences between the original database and theselected study group in terms of gender, PTA duration, Glas-gow Coma Scale (GCS) scores, and years of education. Chi-

337IMPACT OF AGE ON COGNITIVE FUNCTION



squared analysis revealed that the deceased group and the groupof TBI individuals who refused to participate included a sig-nificantly higher proportion of older (55 years) individuals.

A pool of 112 healthy controls was recruited from the generalcommunity in order to evaluate the cognitive impairments of theTBI group. Controls were individually matched with TBI partici-pants in terms of age, gender, education, and estimated IQ. Themean age of control participants at the time of assessmentwas 55.07 years (SD 17.25; range 29– 89). The mean break-down of gender, education, and estimated IQ is shown in Table 1.Exclusionary criteria for controls included history of TBI, neuro-logic disease, psychiatric illness, drug or alcohol dependency, orgeneral medical condition. The demographic characteristics of thepatients and controls are presented in Table 1.

TBI participants were seen at an average of 11.22 yearspostinjury (SD 3.65; range 5–22 years). The number of participants in the 5–10 years postinjury group, 11–16 yearspostinjury group, and 17–22 years postinjury group was 63, 35,and 14, respectively. The mean age of participants at the time of injury was 43.62 years (SD 17.59; range 16–81). The

mean age of TBI participants at the time of assessmentwas 54.88 years (SD 17.54; range 26–89). Sixty percentof the sample were men (n 67). Cause of injury for 88.68%was motor vehicle accident. Injury severity ranged from mild tosevere as measured by GCS and PTA. Of the 83 participants(74.10%) for whom GCS scores were available, the mean GCSwas 8.11 (SD 4.45; range 3–15), with 20.5%, 9.8%,and 42.9% falling in the mild (GCS 13–15), moderate(GCS 9–12), and severe (GCS 3–8) ranges, respectively.Prospectively determined PTA duration (Shores, Marosszeky,Sandanam, & Batchelor, 1986) was available for all partici-pants; the mean PTA duration was 26.04 days (SD 26.78;range 0.1–120), with 9.8% having PTA 24 hr, 30.4% 1–7days, 19.64% 1–4 weeks, and 39.29% 4 weeks. There wereno participants who had a GCS 12 and a PTA 24 hours anda CT scan showing no abnormality. Furthermore, all TBI par-ticipants had received inpatient or outpatient rehabilitation, orboth. Taken together, this indicates that even those classified ashaving mild TBI under one method of classification are morelikely to have been at least at the complicated end of the mildspectrum. Given that previous studies have shown the enhancedpredictive ability of estimated PTA over GCS when estimatingcognitive outcome (Cattelani, Tanzi, Lombardi, & Mazzucchi,2002), PTA was selected as the main index for injury severity.

Bivariate analyses (using Pearson product–moment correlationcoefficients) revealed no significant correlations between age atinjury and PTA or between age at injury and time since injury.A Kruskal–Wallis test showed no significant difference in ageacross the various accident causes.

MeasuresEstimates of premorbid intelligence were obtained using the

Wechsler Test of Adult Reading (Wechsler, 2001). Attention andinformation processing speed was measured by the WechslerAdult Intelligence Scale (WAIS–III) Digit Symbol Coding task(DSCT; Wechsler, 1997), Symbol Digit Modalities Test (SDMT;Smith, 1973), and Trail Making Test, Part A (TMT–A; Reitan &Wolfson, 1988). In the SDMT (oral version), participants wereasked to convert a series of geometric shapes into spoken numberresponses in 90 s. The TMT–A required participants to draw aconnecting line that joined 25 numbers randomly arranged on apage in numerical order as quickly as possible. On the DSCT,participants had 120 s to transcribe a series of numbers into their

corresponding symbols according to a key.Verbal learning was measured with the Rey Auditory Verbal

Learning Test (RAVLT; Lezak, 1976). Participants were re-quired to learn a list of 15 words over five trials. The People andNames tests were also used as measures of verbal learning(Baddeley, Emslie, & Nimmo-Smith, 1994). The People testrequired participants to learn the names of four people, pre-sented in written form under photos, over three trials and thenrecall them after a long delay. The Names test required partic-ipants to identify previously seen names from a set of distractornames across two trials. Visual memory recognition was as-sessed by the Doors test (Baddeley et al., 1994); participantswere asked to identify previously seen target doors f rom a set of distractor doors across two trials.

Initiation speed and response inhibition was measured withthe Hayling Sentence Completion test, which has been shown tobe sensitive to cognitive impairment associated with frontallobe lesions (Burgess & Shallice, 1997). This task requiredparticipants to provide the final word of two sets of sentences inthe fastest time possible, the first set in a straightforwardmanner (Part A) and the second set in such a way that the finalword was unrelated to the sentence (Part B). Rule detection andadherence was evaluated by the Brixton Spatial Anticipationtest (Burgess & Shallice, 1997), in which participants were

Table 1 Demographic Profile of TBI Group and Individually Matched Control Participants

Age atassessment

(years)

TBI (n 112) Control (n 112)

Education(years) Estimated IQ

PTA duration(days)

Yearspostinjury

Education(years) Estimated IQ

M (SD) Range M (SD) Range M (SD) Range M (SD) Range M (SD) Range M (SD) Range

26–39 12.65 (2.54) 8–18 103.00 (9.90) 85–124 29.81 (26.82) 0–90 11.16 (2.72) 9–22 12.71 (2.61) 10–21 104.39 (8.62) 86–11740–59 12.00 (2.85) 9–19 102.37 (10.26) 85–122 24.63 (27.55) 1–99 10.37 (2.77) 7–20 11.63 (2.17) 8–17 102.47 (8.72) 86–12060–89 10.56 (2.30) 6–16 100.53 (9.18) 84–118 24.57 (26.64) 0–120 11.76 (4.44) 5–20 10.74 (2.29) 8–18 101.24 (8.65) 85–125

Note. TBI traumatic brain injury; PTA posttraumatic amnesia.

338 SENATHI-RAJA, PONSFORD, AND SCHÖNBERGER



required to predict the location of a colored circle in a arrayof 10 circles across 56 trials. The Controlled Oral Word Asso-ciation Test (COWAT; Benton, Hamsher, & Rey, 1994) wasused as a measure of verbal association fluency, whereby par-ticipants were required to generate as many words as possiblebeginning with a specific letter within 1 min. The Porteus MazeTest, Vineland Revision (Porteus, 1933), was used as a measureof executive function. Participants were instructed to drawthe correct path through a maze while maintaining the standardrules. Response inhibition was measured by the Sustained At-tention to Response Task (SART; Robertson, Manly, Andrade,Baddeley, & Yiend, 1997), a computerized task of 4.3 minduration. After a brief practice set, participants were asked topress a key as quickly as possible in response to every digit thatwas serially presented on the screen, except for the number 3,which appeared in a quasi-random sequence over the 216 trials.Mental flexibility was evaluated by the Trail-Making Test, PartB (TMT–B; Reitan & Wolfson, 1988), in which participantswere required to join 25 numbers and letters in alternating orderas quickly as possible. The WAIS–III Digit Span Backwards

task (DS–B; Wechsler, 1997) was used to assess workingmemory.

Procedure

The study protocol was approved by the ethics committees of Monash University and Epworth Hospital. After recruitment, theprimary researcher contacted each consenting person to arrangeassessment at the hospital or the participant’s home. A semistruc-tured interview was conducted to determine current and preinjurydemographic and medical information, including current medica-tions used. Participants then completed a cognitive assessment,with the order of tests randomly selected from five predeterminedsequences. Further medical and treatment details—including med-ical history, date of injury, cause of injury, GCS scores, andestimated PTA duration—were obtained from medical records.TBI participants each identified a healthy individual to serve astheir matched control. Healthy controls were interviewed over thetelephone to assess their suitability in terms of age, gender, edu-cation, employment, and general health. Those selected for partic-ipation were scheduled for an appointment to complete a cognitiveassessment.

Data Analysis

Because there were a small number of valid univariate out-liers in the cognitive test data, these scores were windsorized by

applying a cut-off z value of 3.29, in order to utilize allinformation in the data set while eliminating the influence of extreme values on the mean (Barnet & Lewis, 1978; Kohnert,1995). Scatterplots comparing cognitive data with age at injury,time postinjury, and PTA were visually examined, and therewas no evidence of nonlinear bivariate relationships. Paired-samples t tests were conducted to compare cognitive perfor-mances of participants with TBI with those of their individuallymatched controls. Those tests on which TBI participantsshowed poorer performance than did controls, with large effectsizes, were entered as dependent variables in separate multiplelinear regression analyses, along with the controls’ perfor-

mances on the same test, injury severity (measured by PTAduration), age at injury, and time postinjury used as the inde-pendent variables. Analyses were performed to ensure no vio-lation of the assumptions of normality, linearity, and homosce-dasticity. The independent variables were mean centered inorder to compute interaction variables in the regression analy-ses, and product terms were computed for PTA Age at Injury,PTA Time Postinjury, and Age at Injury Time Postinjury.

Multivariate outliers in the regression analyses were identi-fied, as defined by Cooke’s distance 1, and data were reana-lyzed with the exclusion of 3 patients aged over 60 years atassessment. Because this did not change the multiple regressionresults, these patients were included in the final analyses. Mul-tiple correlations between independent variables were low, as isindicated by tolerance levels no less than 0.71, suggesting noevidence of multicollinearity. The significance level was setto 0.05 (two tailed) for all analyses. The effect size measureused was eta-squared (2), representing the proportion of vari-ance in the dependent variable explained by the independentvariable. Cohen’s (1988) guidelines suggest that 2 0.01,

0.06, and 0.14 indicate small, moderate, and large effects,respectively.

Results

Paired-samples t tests revealed that the TBI group performedsignificantly worse than did the individually matched control group onmeasures of processing speed, working memory, verbal and visualmemory, and executive function, as is shown in Table 2. The largesteffect sizes were seen in the cognitive domain of processing speedand attention, followed by verbal and visual memory, executivefunction, and working memory.

Multiple linear regression analyses revealed that after control-

ling for controls’ test performances, time since injury, age atinjury, and all interaction terms, PTA was significantly associ-ated with TBI participants’ test performances on all measures,with the exception of Hayling, Brixton, and Porteus Maze errors(see Table 3).

Relationship Between Long-Term Cognitive

Impairment and Age at Injury

As is seen in Table 3, multiple regression analyses showed thatafter controlling for the controls’ performances and other predictorvariables, the effect of age at injury was significant for all cogni-tive measures except for SART accuracy. The difference between

older TBI participants and their age-matched controls was dispro-portionately greater than was the difference between young TBIparticipants and their age-matched controls, as is seen in Figures 1and 2.

Relationship Between Long-Term Cognitive

Impairment and Time Postinjury

The same multiple regression analyses revealed that time postinjury was a significant predictor of TBI performance on the SDMTand DSC tasks, with longer time postinjury associated with slowerperformance (see Table 3).




Interaction Between Age at Injury and Time

Postinjury for Long-Term Cognitive Performance

Cognitive test performance of TBI participants on a numberof measures was significantly related to an interaction betweenage at injury and time postinjury (see Table 3). Significant R2

when entering the Age Time Postinjury interaction term intothe regression was noted on TMT–A ( R2 change 0.05),SDMT ( R2 change 0.04), DSC ( R2 change 0.03), totalitems learned on RAVLT ( R2 change 0.03) and Names ( R2

change 0.06), RAVLT immediate recall ( R2

change 0.03),and COWAT ( R2 change 0.03). In TBI individuals aged

16–34 years, greater time postinjury was associated with bettercognitive performance, controlled for healthy individuals’ per-formance. In TBI individuals aged 35–54 years, time postinjurywas not related to test performance. In TBI individuals aged 55years and older, greater time postinjury was associated withworse cognitive performance. The Age Time Postinjuryinteraction was exemplified in performance on the SDMT, as isillustrated in Figure 3. As Figure 4 illustrates, in TBI individ-uals 5–10 years postinjury, younger age was associated withbetter cognitive performance, controlled for healthy individu-

als’ performance. In TBI individuals 11–16 years postinjury,age was not related to test performance. In TBI individuals

Table 2Comparison of TBI Group and Individually Matched Control Group on Cognitive Measures

Cognitive domain Measure

TBI group(n 112)

Control group(n 112)

p 2 M (SD) M (SD)

Processing speed & attention SDMT 43.2 (14.7) 54.0 (11.3) 0.001 0.37DSC 54.4 (22.2) 68.6 (17.2) 0.001 0.32TMT–A 46.2 (34.7) 31.2 (10.4) 0.001 0.24

Verbal & visual memory RAVLT total learned 43.1 (14.3) 51.5 (9.0) 0.001 0.31People total learned 17.9 (10.1) 21.9 (7.5) 0.001 0.16Names total learned 16.8 (4.1) 19.1 (2.6) 0.001 0.22Doors total learned 15.5 (4.4) 18.0 (3.5) 0.001 0.22

Executive function & working memory Hayling total errors 6.2 (4.9) 3.1 (3.0) 0.001 0.23DS–B 5.9 (2.5) 7.2 (2.0) 0.001 0.15Brixton errors 20.0 (8.9) 16.3 (5.9) 0.001 0.15COWAT total words 33.6 (13.1) 41.5 (12.2) 0.001 0.20TMT–B 134.3 (115.5) 70.5 (28.1) 0.001 0.25Porteus Maze errors 5.5 (5.4) 3.0 (2.8) 0.001 0.18SART accuracy 13.7 (5.6) 17.3 (5.2) 0.001 0.20

Note. TBI traumatic brain injury; SDMT Symbol Digit Modalities Test; DSC Digit Symbol Coding task; TMT–A Trail-Making Test, Part A;RAVLT Rey Auditory Verbal Learning Test; DS–B Digit Span Backwards test; COWAT Controlled Oral Word Association Test; TMT–B

Trail-Making Test, Part B; SART Sustained Attention to Response Test.

Table 3 Multiple Regression Predicting TBI Patients’ Cognitive Performances After Controlling for Controls’ Performances

and Predictor Variables

Measure

PTA Age at injury Time postinjuryTime postinjury

Age at injury

R2 p p p p p

SDMT correct 0.35 0.001 0.53 0.001 0.19 0.018 0.22 0.005 0.52 0.001DSC correct 0.30 0.001 0.53 0.001 0.17 0.024 0.21 0.006 0.56 0.001

TMT–A (seconds) 0.30 0.001 0.62 0.001 0.10 0.245 0.19 0.021 0.46 0.001RAVLT total 0.35 0.001 0.29 0.001 0.00 0.999 0.18 0.025 0.49 0.001People total 0.20 0.007 0.51 0.001 0.06 0.469 0.01 0.907 0.50 0.001Names total 0.22 0.003 0.54 0.001 0.06 0.461 0.29 0.001 0.50 0.001Doors total 0.27 0.001 0.39 0.001 0.07 0.444 0.03 0.705 0.39 0.001Hayling errors 0.14 0.087 0.58 0.001 0.12 0.177 0.29 0.741 0.39 0.001Brixton errors 0.12 0.134 0.62 0.001 0.06 0.518 0.04 0.676 0.42 0.001COWAT words 0.32 0.001 0.26 0.003 0.03 0.725 0.21 0.031 0.26 0.001TMT–B (seconds) 0.19 0.032 0.51 0.001 0.00 0.943 0.04 0.685 0.30 0.001SART accuracy 0.33 0.001 0.16 0.102 0.12 0.246 0.17 0.11 0.20 0.001Porteus errors 0.13 0.13 0.44 0.001 0.18 0.061 0.02 0.87 0.29 0.001

Note. TBI traumatic brain injury; PTA posttraumatic amnesia; standardized beta coefficient; SDMT Symbol Digit Modalities Test; DSC Digit Symbol Coding task; TMT–A Trail-Making Test, Part A; RAVLT Rey Auditory Verbal Learning Test; COWAT Controlled Oral WordAssociation Test; TMT–B Trail-Making Test, Part B; SART Sustained Attention to Response Test.




more than 16 years postinjury, older TBI individuals showed abetter cognitive performance than did young individuals.

Discussion

The results showed clear evidence of persisting cognitive im-pairment in the TBI participants across all domains assessed. Evenwith family-wise Bonferroni corrections, for separate cognitivedomains, the results are highly significant. Impairment was signif-icantly associated with injury severity, as is measured by PTAduration. The first aim of the study was to investigate whether ageat the time of traumatic brain injury affects cognitive performancemany years later. As was predicted, our results showed that olderage was associated with poorer performance across all cognitive

domains, after accounting for normal age-related cognitive de-cline. The disproportionately worse performance of older TBIparticipants in comparison with younger TBI participants is con-sistent with Himanen et al.’s (2006) findings. Our results are alsoconsistent with Teuber’s penetrating head injury research, suggest-ing that injury in adolescence or young adulthood has less severe

consequences than do injuries sustained later in life (Teuber,1975). It appears that the combined effects of TBI and older agemay have a synergistic deleterious effect on long-term cognitiveoutcome. This poorer outcome for older individuals may be due tothe older brain’s poorer capacity to compensate during initialrecovery or greater deterioration beyond the period of initial re-covery due to reduced plasticity in the aging brain.

The second aim of our study was to determine the impact of time postinjury on long-term cognitive outcome. As was expected,we found that cognitive impairment was greater with increasingyears after injury, as was suggested by Wood and Rutterford’s(2006) findings. Unlike the study by Himanen et al. (2006), ourstudy did not find that increased time postinjury had a positiveimpact on younger individuals; rather, our findings support Ray-mont et al.’s (2008) claim that slow cognitive decline may occurfrom the time of injury across all ages. Arguably, Himanen et al.’sinclusion of some pediatric patients may have confounded theeffects of normal developmental gains and long-term recovery.Recent magnetic resonance imaging (MRI) studies have confirmed

Figure 1. Relationship between age at injury (in years, y) and performance on Trail Making Test, Part A(TMT-A). TBI traumatic brain injury.

Figure 2. Relationship between age at injury (in years, y) and performance on Names Test. TBI traumaticbrain injury.




that cerebral atrophy continues into the chronic phase followingsevere TBI, particularly when there has been diffuse axonal injury,providing some basis for the observed cognitive decline (Wilde,Bigler, Pedroza, & Ryser, 2006).

The final objective of this study was to ascertain whether long-term cognitive outcome was influenced by an interaction betweenage at injury and time postinjury. Contrary to predictions, wefound that the presence of disproportionately poorer cognitivefunction in long-time survivors, in comparison with relativelyrecent survivors, was more evident in younger individuals. Whilein most age groups, longer time postinjury was related to poorerperformance, time postinjury was related to better performance inthe older TBI participants, and this may be explained by the fact

that these older participants were examined closer to the time of injury.

The present study had certain limitations, most notably itscross-sectional design. Where certain results of our study con-flicted with those of longitudinally designed studies, we acknowl-edge that our study’s cross-sectional design, being suboptimal inaddressing trend over time, may have been a contributor to thisdiscrepancy. Whereas some previous studies have lacked controlgroups altogether, the matched-pairs design of the current studywas advantageous; however, future research may benefit frominclusion of a comparison group of individuals who sustainedextracranial injury to control for risk factors. The potential for

some sample bias cannot be ruled out, given that the rate of attrition and participation refusal was higher in older nonpartici-pants, which is not unexpected in a study including individualsabove the age of 60 years. It is possible that TBI led to earlier deathor more severe injury in these individuals, which may have weak-ened the age and time postinjury effects and possibly explains thecounterintuitive Age Time Postinjury interaction.

Despite these limitations, this study has provided importantinsights into the long-term cognitive trajectory following TBIacross the adult age spectrum. Previous studies have recruitedfew participants over the age of 60 at the time of injury(Himanen et al., 2006; Johnstone et al., 1998; Klein et al.,1996). The relatively large sample of older participants in the

present study, together with the inclusion of individuallymatched controls, strengthens its findings. Moreover, its exclu-sion of patients in the acute stages of recovery and focus oncognitive performance in the chronic stage has appropriatelyaddressed the question of long-term outcome.

The finding of poorer cognitive outcome in older injured indi-viduals has a number of clinical implications. With respect toissues of differential diagnosis, disproportionately worse cognitiveimpairment should be first interpreted within the context of TBIbefore considering any newly emerging pathological process.Poorer cognitive functioning with greater time postinjury empha-sizes the importance of flexible management plans that allow the

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Figure 3. Age at Injury Time Postinjury interaction effect on Symbol Digits Modalities Test (SDMT),layered for age at injury.




opportunity for further neuropsychological intervention, reevalua-tion of activity programs, and increased structured supports overthe long term.

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Received January 16, 2009Revision received September 25, 2009Accepted October 7, 2009

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