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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury 6 NEUROCOGNITIVE OUTCOMES This chapter highlights studies that examined outcomes related to alterations in neurocognition. Traumatic brain injury (TBI) can result in changes in neurocognitive performance as measured by tests of sensory integrity, motor speed and coordination, attention, working memory, episodic memory, processing speed, language processing, visual-spatial processing, and executive functions (such as higher-order planning, initiating and directing, monitoring, problem-solving, and inhibitory control). Findings of alterations in neurocognitive performance were carefully examined by the committee; there were over 430 studies of TBI and neurocognitive outcomes in the committee’s database. The committee chose studies that specifically answered the question related to its charge, that is, what long-term outcomes (lasting longer than 6 months) might be associated with a penetrating or closed head injury in adults and meet the general criteria for inclusion described in Chapter 4. The term neurocognitive outcome as used in this chapter refers to cognitive impairment while the word neuropsychologic refers to the kinds of measurements most studies utilized to determine the level of impairment. With regard to penetrating brain injury, it has been determined that the location of a brain injury and the volume of brain tissue lost affect the type and extent of neurocognitive deficits. Many scholarly articles and textbook chapters have described the relationship of localization of brain injury with specific outcomes (Damasio et al., 1994; Haas, 2001; Ratiu et al., 2004; Silver et al., 2005; Raymont et al., 2008), so it will not be discussed here. The chapter first discusses outcomes related to penetrating head injury and then outcomes related to closed head injury. Conclusions follow each section; the conclusions that follow the closed head injury section are further delineated by the severity of the injury. PENETRATING BRAIN INJURY Studies of penetrating brain injuries have been conducted primarily in military populations and are useful because they have long-term followup and preinjury neurocognitive-test information. Primary studies are presented first, followed by secondary studies, a summary and conclusion, and finally a table (Table 6.1) with information abstracted from the primary studies. Chapter 5 provides a detailed overview of many of the studies of military populations who have been injured during war. Some of the studies inform the discussion of long-term outcomes; others were not designed to answer the question posed to the committee regarding long-term sequelae of brain injury. The committee included the military studies that fit its task best; some of the studies are primary and others secondary, but they are all described in Chapter 5. The committee identified five primary studies of penetrating brain injury, and they are discussed below.
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury Primary Studies Teuber and Weinstein (1954) (see cohort description in Chapter 5) studied 35 World War II veterans selected from 185 veterans who had penetrating missile injuries and loss of brain tissue and 12 controls from 101 veterans who had missile injuries of peripheral nerves but no brain injury. All veterans had sustained their injuries 5–8 years before the study. The 35 brain-injured were selected by identifying equal numbers of men with injuries in the anterior or posterior one-third of the brain and in the right or left hemisphere. The control group consisted of nine men with arm injuries and three with leg injuries. All the men were tested with the Seguin-Goddard Formboard Test, which was administered with the men blindfolded first in its normal position and then after a 180-degree rotation. Men with brain injuries took more time, made more errors, and recalled fewer forms than the controls. Another study by Weinstein and Teuber (1957b) examined two groups of men: 62 who had loss of cerebral tissue due to penetrating head injury and 50 who had trauma of peripheral nerves. Preinjury Army General Classification Test (AGCT) scores, which had been administered on induction into the Army 13–15 years before the study, were available for all the men. Preinjury education level was determined by interview and from case records. The civilian edition of the AGCT was administered to all the study participants 10–12 years after their injuries. The findings indicate clearly that the change in AGCT score was significantly worse in the penetrating-injury group than in the peripheral-nerve–injured group. Furthermore, although the primary aim of the study was to investigate the connection between preinjury education and intelligence and intellectual deterioration after brain injury, the authors note that the findings were independent of any effects of differences in preinjury education or preinjury AGCT score. Corkin et al. (1989) conducted a 30-year longitudinal study of 84 World War II veterans to determine the cognitive effects of penetrating head injury: 57 veterans who had penetrating head injury and 27 veterans who had peripheral nerve injury who were matched with respect to age and premorbid intelligence and education. The veterans were examined in the 1950s and in the 1980s. The veterans selected were those who had been seen by Teuber and Weinstein in New York (see Chapter 5 for Teuber’s cohort of World War II veterans). Both groups of veterans had received an average of 12 years of education before injury and were tested with the AGCT before injury. Total scores of 42 veterans were available from military records. Review of the preinjury AGCT total scores showed no differences between the two groups. Both groups were given two cognitive tests after injury: the AGCT and the Hidden Figures Test. The AGCT contains three subscales—vocabulary, arithmetic, and block-counting—and the Hidden Figures Test measures the ability to discriminate figures from background. Ten years after the end of the war, in the 1950s, the penetrating-injury group showed poorer performance on both cognitive tests than the peripheral-nerve–injured controls. Forty years after the war, in the 1980s (when the study was conducted), the penetrating-injury group exhibited even poorer performance on every cognitive measure except vocabulary, which remained constant. When the data were examined by brain region with computed tomography, the site of the injury exerted an even stronger effect. Veterans with injuries of the left parietal lobe had a significantly greater decrease on the vocabulary and arithmetic subscales, and those with lesions in other brain regions showed a greater decrease on other subscales or on the Hidden Figures Tests. Penetrating-injury subjects lost an average of 7.9 points from the 1950s to the 1980s, and those with peripheral nerve injury gained an average of 0.4 point. The decline was most pronounced in older subjects. The results suggested accelerated aging in those with penetrating head injury.
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury As part of the Vietnam Head Injury Study (VHIS; see Chapter 5 for description of the study and the cohort), Grafman et al. (1988) studied the nature of intellectual function after penetrating missile wounds. The cohort consisted of 263 men who had penetrating brain injuries—96 with lesions in the right hemisphere, 78 in the left hemisphere, and 89 in both—and 64 uninjured controls who met the inclusion criteria: they served in Vietnam during the same years as the brain-injured, and they were stratified according to preinjury Armed Forces Qualification Test (AFQT) to be matched with the brain-injured. There were no significant differences between the groups in age, education, or preinjury AFQT percentile scores. Although Grafman and colleagues stratified head-injured subjects by location of brain injury, the study data clearly indicate that the head-injured showed worse change than the controls in performance on the AFQT. The authors also assessed whether brain-volume loss correlated with changes in cognitive function. As expected, greater total brain-volume loss correlated with greater declines in AFQT scores from before to after injury (p < 0.0001). The authors examined whether lesion location was associated with cognitive decline. No significant effects on AFQT scores by lesion location (right, left, or bilateral) were observed. Preinjury education level also did not correlate with AFQT. The results indicated several factors that influence cognitive decline after brain injury as measured with the AFQT: preinjury intelligence was the strongest predictor of postinjury intelligence scores, followed by the size of the lesion, and then the location of the lesion. Preinjury education level did not correlate with cognitive decline. Raymont et al. (2008) examined 182 Vietnam veterans as part of phase 3 of the VHIS. All were identified from the VHIS registry and had a history of penetrating head injury although an additional 17 patients who were assessed for phase 3 had not participated in phase 1 or 2. Controls were 32 veterans who had participated in phase 2 and an additional 23 who were recruited through advertisements in veteran publications; none of the controls had a history of head injury. All the veterans were assessed over 5–7 days at the National Naval Medical Center in Bethesda, Maryland. There were no significant differences between cases and controls with regard to age, years of education, or preinjury induction intelligence level (as measured with the AFQT). Brain lesions were identified with computed tomography. The median AFQT score in the entire sample was 65.0; in the penetrating-injury group, it was 54.0, and in the controls, 74.0. The penetrating-injury veterans had a significantly greater decrease in AFQT score than controls from phase 2 to phase 3 and from before injury to phase 3. The scores of the controls improved from before injury to phase 2 compared to those with penetrating head injuries. If officers were excluded from the sample, the AFQT scores of those with penetrating head injuries decreased significantly more than the scores of the controls over the entire period from before injury to phase 3. Those with penetrating injuries had lower AFQT scores at phase 3 (mean, 52.58) than the controls (mean, 68.50). The authors examined several risk factors for AFQT outcome at followup and for declining AFQT scores, including dementia, location of brain lesion, and genetic markers. They found that preinjury intelligence was the most consistent predictor of cognitive outcome at all followup times and of decline over time. There was no evidence that laterality of the lesion affected overall intelligence or decline. Specific brain regions, the degree of local and global atrophy, and some genetic markers were found to be associated with exacerbated decline. Thus, the long-term followup of Vietnam veterans with penetrating head injury found that exacerbated decline in intelligence is a significant risk.
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury Secondary Studies Like the primary studies, the secondary studies of penetrating TBI have been conducted in military cohorts (see Chapter 5), but they have methodologic limitations that prevented the committee from including them as primary studies. For example, many of the studies examined differences in specific cognitive domains as a function of the location of the brain injury or did not compare brain-injured people with a non-brain-injured control group. Weinstein and Teuber (1957a) examined the effects of penetrating brain injury on intelligence-test scores in patients who had stable, localized brain injury. The investigators obtained preinjury AGCT scores for 62 men who later sustained penetrating brain injury and for 50 controls who incurred arm or leg nerve injuries. All the men had been injured during World War II 1–3 years after the initial AGCT. A comparable AGCT was administered about 10 years after the men were injured. The preinjury scores of the brain-injured and control groups were almost identical: means, 105.0 and 106.4, respectively. Scores on the postinjury test showed some gain: 48 of the 50 controls increased their mean score to 119.4. The 62 brain-injured men were divided into groups according to the location of their injuries: frontal, temporal, parietal, or occipital, in the left, right, or both hemispheres. The investigators found that lesions in frontal and occipital lobes were not associated with a significant decrease in scores, but lesions in the parietal and temporal lobes of the left hemisphere were associated with a significant decrease. Weinstein et al. (1956) studied spatial orientation in 62 men who had loss of cerebral tissue because of penetrating head injury and 18 men who had leg peripheral nerve injuries. All the men had been injured during World War II (see cohort description in Chapter 5). The authors focused on a particular task of spatial orientation: finding a route on a map. Men with parietal lobe lesions (in either hemisphere) did more poorly than all the brain-injured men who did not have parietal lesions, and the men with brain damage, other than in the parietal lobe, did not perform more poorly than controls. The VHIS has resulted in numerous publications of long-term outcomes associated with penetrating head injury (see Chapter 5). Salazar et al. (1986) found that Vietnam veterans who had penetrating injuries of the basal forebrain had worse outcomes than uninjured controls with regard to episodic memory, reasoning, and arithmetic but not on tests of intelligence, attention, and language. Several studies by Grafman et al. (for example, 1986, 1990) provided evidence of the detrimental effects of penetrating head injuries on facial discrimination (1986) and examined neurocognitive performance on the Wisconsin Card Sorting Test, noting that brain-damaged Vietnam veterans made more errors than controls (1990). Although there have been additional studies in the VHIS series, many were not designed to answer the question specifically posed to the committee regarding long-term health outcomes. The studies that do shed light on long-term outcomes, other than neurocognitive effects, are discussed elsewhere in this volume. Summary and Conclusion The committee reviewed five primary studies (Teuber and Weinstein, 1954; Weinstein and Teuber, 1957b; Grafman et al., 1988; Corkin et al., 1989; Raymont et al., 2008) and five secondary studies (Weinstein et al., 1956; Weinstein and Teuber, 1957a; Grafman et al., 1986, 1990; Salazar et al., 1986) of penetrating head injury in military populations. The primary and secondary studies are consistent in pointing toward a decline in neurocognitive function after penetrating head injury.
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury With regard to increased errors on the formboard test, Teuber and Weinstein (1954) showed that veterans who had penetrating head injury took more time, made more errors, and recalled fewer forms than the controls. A later study by Weinstein and Teuber (1957b) examined the change in AGCT score from before injury to after injury and found that subjects who had penetrating head injury had a greater decline in score than the group who had peripheral nerve injury independently of preinjury education and preinjury AGCT scores. Grafman et al. (1988) found cognitive decline after brain injury as measured the AFQT. However, preinjury intelligence score was the most predictive factor in postinjury intelligence score, followed by the size of the lesion; the location of the injury was the least important. In contrast, preinjury education level did not correlate with cognitive decline. The study of World War II veterans by Corkin et al. (1989) demonstrated poorer performance on cognitive tests in veterans who had penetrating head injury than in controls and continued decline over 30 years in the brain-injured veterans on every cognitive measure except vocabulary, which remained constant. It was noted that the site of the injury exerted a strong effect on the type of deficits. Finally, the study of Vietnam veterans by Raymont et al. (2008) demonstrated that exacerbated decline in intelligence over 30–40 years is a significant risk for veterans with penetrating head injury. The five secondary studies also showed long-term deficits in neurocognition including intelligence (Weinstein and Teuber, 1957a); spatial orientation (Weinstein et al., 1956); memory, reasoning, and arithmetic (Salazar et al., 1986); facial discrimination (Grafman et al., 1986); and neurocognitive decline as measured with the Wisconsin Card Sorting Test (Grafman et al., 1990). Those studies, particularly the secondary studies, suffer from various limitations, including small samples, a focus on injury sites and localization of functional outcomes (which were outside the committee’s charge), incomplete description of how subjects and controls were selected, and apparent high rates of loss of the original sample at followup times. However, the studies had advantages not seen in studies of civilian injury, including the availability of baseline cognitive test scores and the long-term nature of followup (in some cases, 40 years or more). The overall body of evidence demonstrates poor neurocognitive outcomes in people who suffer penetrating head injury. The committee concludes, on the basis of its evaluation, that there is sufficient evidence of a relationship between sustaining a penetrating TBI and decline in neurocognitive function associated with the affected region of the brain and the volume of brain tissue lost.
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury TABLE 6.1 Penetrating Head Injury and Neurocognitive Outcomes Reference Study Design Population Type of TBI: Mild, Moderate, Severe; Blunt, Penetrating, Blast Health Outcomes or Outcome Measures Results Adjustments Comments or Limitations Teuber and Weinstein, 1954 Cohort 35 men with brain injury selected from 185 with missile wounds of head, 12 controls with peripheral nerve injury wounds of head controls chosen from 101 with missile wounds of peripheral nerves Penetrating missile injuries of head or peripheral nerves Form Board Test Brain-injured subjects took more time, made more errors, recalled fewer forms than controls Subjects, controls sustained injuries 5–8 years before testing Subjects grouped on basis of location of lesions Weinstein and Teuber, 1957b Cohort 62 men with loss of cerebral tissue due to penetrating head trauma, 50 controls with peripheral nerve injury Penetrating head trauma or peripheral nerve trauma AGCT administered 13–15 years before injury (on induction into Army) Controls had mean increase of 13.0 AGCT points from preinjury to postinjury testing Eliminated men with aphasic difficulties that prevented them from reading practice-test questions Preinjury AGCT score available for 53 subjects Preinjury educational level determined by interview and from case records Brain-injured group, excluding aphasics, had average increase of 5.2 points; total brain-injured group had increase of 1.6 points AGCT administered again 10–12 years after injury Education before injury did not influence extent to which performance on intelligence test was affected after injury
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury Reference Study Design Population Type of TBI: Mild, Moderate, Severe; Blunt, Penetrating, Blast Health Outcomes or Outcome Measures Results Adjustments Comments or Limitations Corkin et al., 1989 Cohort 84 World War II veterans: 57 with penetrating head injury, 27 with peripheral nerve injury Penetrating head injury; injury severity determined by number of cortical lobes involved, presence of tantalum plate, history of seizures, use of anticonvulsant medication AGCT (including Total, Vocabulary, Arithmetic, Block counting subscales), figure-ground discrimination (measured with Hidden Figures Test) 10 years after end of war (in 1950s), TBI group had poorer performance on both cognitive tests Matched with respect to age, premorbid intelligence, premorbid education Existence of baseline performance, retesting at 10 and 40 years after penetrating brain injury compared with appropriate controls are strengths of study; possible limitation is how representative the subjects were of all those injured in World War II; subsamples selected from 314 studied by Teuber and Weinstein (1956, 1957); age, performance correlated only in brain-injured subjects, so age-related factors might have contributed to exacerbated decline (This population was first seen in Teuber’s NY laboratory) 18–34 years old at time of injury, first testing 10 years after injury (1950s), and testing 40 years after injury (1980s) 30 years after war, TBI veterans, as a group, exhibited even poorer performance on every cognitive measure except vocabulary, which was constant Grafman et al., 1988 Prospective, long-term followup of Vietnam War veterans (Part of VHIS) 263 brain-injured veterans, 64 uninjured controls matched on preinjury AFQT scores Penetrating head injury Cognitive-outcome, AFQT Preinjury AFQT score was most predictive factor for postinjury intelligence scores, followed by brain-volume loss, location of injury; preinjury ANOVAs, multiple regression analysis performed to assess association between size and location of
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury Reference Study Design Population Type of TBI: Mild, Moderate, Severe; Blunt, Penetrating, Blast Health Outcomes or Outcome Measures Results Adjustments Comments or Limitations education level not associated with cognitive decline brain lesions predicted cognitive function after injury Raymont et al., 2008 Prospective, long-term followup of Vietnam War Veterans (part of VHIS phase 3) Subjects drawn from VHIS registry; 92% had penetrating head injury; of 520 from phase 2, 484 are still alive, and 182 attended phase 3 Penetrating head injury Cognitive-outcome, AFQT At phase 3, no significant differences between head-injured and controls in age, education, intelligence ANOVAs, linear logistic and stepwise multiple regression procedures preformed to assess impact of demographic factors, preinjury intelligence, brain-volume loss, lesion location, genetic markers on cognitive ability 36–39 years after injury Those with penetrating head injury had lower AFQT scores at phase 3 than controls, significantly greater decrease in AFQT score than controls from phase 2 to phase 3 and from preinjury to phase 3; when impact of education, preinjury intelligence, brain volume loss, lesion location on postinjury intelligence was examined, most important determinant of postinjury intelligence was preinjury performance as measured by AFQT 2,000 patients entered in registry in 1967–1970 The more global the cognitive test, the greater the effect of brain-volume loss NOTE: AFQT = Armed Forces Qualification Test, AGCT = Army General Classification Test, ANOVA = analysis of variance, TBI = traumatic brain injury, VHIS = Vietnam Head Injury Study.
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury CLOSED HEAD INJURY This section focuses on studies of closed (nonpenetrating) head injuries. These injuries are typically categorized as mild, moderate, or severe TBI. One of the problems encountered by the committee in evaluating studies of closed TBI is the difficulty in comparing severity of TBI among studies. Papers are inconsistent in the measurement of severity, particularly of moderate TBI. As in the previous section, primary studies are presented first and followed by secondary studies, a summary and conclusions, and finally a table (Table 6.2) with information abstracted from the primary studies. Primary Studies The committee selected six primary studies of closed head injury. They differ from the studies of penetrating head injury in that they examined civilian populations with TBI resulting from motor-vehicle crashes, falls, assaults, or sports activities. A study by Dikmen et al. (1986), using a cohort from the trauma center at Harborview Medical Center in Seattle, Washington (previously described in Chapter 5), examined neurocognitive outcomes after mild TBI. The head-injured, drawn from a larger cohort, were 20 consecutive patients 15–60 years old who had mild TBI. The 19 controls were friends of the TBI patients from the larger head-injured group (see Chapter 5) who were matched with regard to age, education, and sex; exclusionary criteria included evidence of preinjury central nervous system (CNS) disease or alcoholism. Neuropsychologic tests were administered at 1 month and 12 months after injury; controls were tested at the same intervals. The Halstead-Reitan Neuropsychological Test Battery and additional measures of memory were administered. The head-injured group performed slightly less well than the uninjured group on 2 of the 21 measures (the Seashore Rhythm Test and the Selective Reminding Test) at 1 month after injury. At 1 year, none of the neuropsychologic measures showed significant differences. Thus, although subtle neuropsychologic effects were found at 1 month after a mild TBI, they could no longer be detected at 1 year. In another study by Dikmen et al. (1987) (see Chapter 5), the relationship between injury severity and memory was examined in 102 consecutive head-injured patients admitted into Harborview Medical Center. All patients had sustained blunt head injury; most of the cases were mild or moderate. The uninjured comparison group consisted of 102 friends of the head-injured matched on age, education, race, and sex. Head-injury severity was measured with the Glasgow Coma Scale (GCS), assessed within 24 hours of injury to determine the depth of coma; time from injury to consistent ability to follow simple commands (TFC), used as an index of coma length; and posttraumatic amnesia (PTA), used to determine the length of impaired consciousness. The Wechsler Memory Scale (WMS) and the Selective Reminding Test (SRT) were used at 1 and 12 months after injury. The head-injured group performed more poorly than the uninjured controls (p < 0.001) on each of the subscales of the WMS and the SRT. Similarly, at 1 year, there was significant impairment on most subscales of the tests administered. However, head-injured patients performed better at 1 year than at 1 month. With regard to severity of
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury injury, only those with deep or prolonged impaired consciousness (TFC over 1 day, PTA at least 14 days, and GCS less than 8) were performing significantly worse at 1 year than the controls. Dikmen et al. (1995) conducted a prospective study of 436 adults with mild, moderate, or severe TBI recruited at the time of injury from Harborview Medical Center, a level 1 trauma center (see Chapter 5). The study included English-speaking adults who had TBI with loss of consciousness for any period or PTA for at least 1 hour or with objective evidence of TBI (such as hematoma) and who were hospitalized and survived at least 1 month after injury. Most TBI patients (74%) had sustained their injuries in motor-vehicle crashes (car or motorcycle drive, pedestrian, or bicyclist), 11% in falls, 8% in fights or assaults, and the remaining 6% in other activities. Controls were 121 patients admitted into the emergency room at Harborview Medical Center after injury to any part of the body except the head and matched to the TBI cases on age, sex, and education. Subjects and controls received a neuropsychologic assessment at 1 year after injury, which included the Halstead-Reitan Neuropsychological Test Battery and additional measures of attention and memory. The battery evaluated various neuropsychologic functions, including sensory and motor skills, attention, concentration, memory, verbal and visuospatial intellectual skills, and executive function, such as problem solving and flexibility of thinking. A year after injury, the TBI group performed significantly worse than controls on 18 of the 21 measures used for comparison. There was a dose–response relationship: longer coma (from time of injury to consistently following commands) was associated with greater neurocognitive impairment. Fifty percent of the subjects with the most severe TBI (those with TFC of 29 days or longer) were cognitively too impaired even to be formally tested. Tate et al. (1991) studied a consecutive series of 87 of 100 patients who had severe TBI and were admitted into a rehabilitation facility in Australia. The patients, 15–45 years old, were compared with sibling controls on 15 factors related to various neurobehavioral impairments. Of the TBI patients, 70% had current and clinically significant impairments. Disorders of learning and memory were the most common findings 6 years after injury and differed between TBI patients (56.5%) and controls (5%). Disturbances in basic neurocognition (such as orientation, visual perception, dyspraxia, and language) were least frequent (16.5% in TBI patients and 2.5% in controls). Slowness in information processing was found in 34.1% of the TBI patients and 2.5% of the controls, and posttraumatic personality changes were found in 40% of the TBI patients, while only 7.5% of the controls exhibited personality changes. The differences appear large, but the authors did not provide tests of their significance. Lannoo et al. (1998) examined neurocognitive outcomes in 85 consecutive patients who had moderate to severe head injury and were admitted into the intensive care unit (ICU) of the University Hospital of Ghent in Belgium from September 1993 to February 1996 with a GCS score of 3–12. The patients were 15–65 years old and had no previous history of CNS disease or mental retardation. The control group consisted of 32 trauma patients who had injuries of the body but not the head and were admitted into the ICU during the same study period. The controls were also 15–65 years old and had no previous history of CNS disease or mental retardation. Neuropsychologic testing was completed at 6 months after injury in 79 of the TBI patients (93%) and 22 of the controls (69%). The neuropsychologic test battery consisted of measures of attention and information processing, visual reaction time, memory and learning, verbal fluency, and mental flexibility. A multivariate analysis of variance on neuropsychologic test performance revealed that the TBI group performed significantly below the control group at 6 months after injury on most of the test measures.
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury Heitger et al. (2006) studied 37 patients who had mild TBI and presented to Christchurch Hospital, New Zealand, and compared them with 37 controls individually matched to each case with respect to age, sex, and years of formal education. The controls were volunteers recruited through a database at the Department of Psychology of the University of Canterbury, Christchurch, New Zealand. Patients and controls were assessed at 1 week, 3 months, and 6 months injury; and 31 pairs were at 12 months after injury. Neurocognitive assessments include d tests of attention, working memory, episodic memory, and speed of information processing and used the Paced Auditory Serial Addition Test, the California Verbal Learning Test-I (CVLT-I), the Symbol Digit Modalities Test, and the Trail Making Test. General cognitive performance was evaluated with the vocabulary and matrix-reasoning subtests of the Wechsler Abbreviated Scale of Intelligence. Results at 3 and 6 months showed deficits in verbal learning in the mild-TBI group, but results of neurocognitive tests at 12 months showed no deficits except for a marginal difference on the CVLT total standard score (p < 0.07). Secondary Studies The committee chose 17 secondary studies for review. The studies discussed here did not meet the committee’s criteria for primary studies as described in Chapter 4. In this discussion, the studies are grouped as follows: TBI associated with sports and then mild TBI, moderate or severe TBI, and varied severity typically in populations other than athletes. Traumatic Brain Injury Associated with Sports People involved in various sports may suffer repeated head injuries, including concussions and mild TBIs. It is often difficult to determine whether the outcome of an injury is related to a single incident or to repeated incidents. When TBI is determined retrospectively by self-report, especially after a period of months or years, it is difficult to be certain about the reliability and validity of the report; this is the case particularly in sports injuries. Studies of TBI associated with sports have found some evidence of long-term cognitive dysfunction (Matser et al., 1998, 1999, 2001; Guskiewicz et al., 2005; Moser et al., 2005; Wall et al., 2006), but the findings are not entirely consistent (Straume-Naesheim et al., 2005). Moser et al. (2005) studied 223 high school athletes (13–19 years old) who participated in a variety of sports (primarily ice hockey, football, field hockey, lacrosse, and soccer). The authors sought to identify the long-term effects of self-reported concussion on neuropsychologic functioning by determining whether there were any differences among four groups of athletes: the recently concussed (within 1 week of neuropsychologic testing), those with no concussion history, those with one concussion sustained at least 6 months previously, and those with two or more concussions sustained at least 6 months previously. The results indicated significant differences among the groups in attention (p = 0.012) and cognitive flexibility and executive functioning (p = 0.006). Post hoc analysis demonstrated that recently concussed athletes perform worse on the attention measure than athletes with no concussion history or a history of one concussion and worse on the cognitive-flexibility measure than those with no concussion history. There were no differences between those with recent concussions and those with two or more concussions on any measures; the authors suggest that this indicates long-term neuropsychologic effects in those with multiple concussions. However, the authors do not report significant differences between athletes with two or more concussions and those with no concussion or one concussion, so their conclusions are uninterpretable.
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury functioning before injury or before exposure. The problem here is that demographic differences between the groups may have predated the exposures and potential TBIs, and this would make interpretation of results difficult. Mild Traumatic Brain Injury Vanderploeg et al. (2005) examined long-term neurocognitive outcomes of self-reported mild TBI in a nonreferred sample of male veterans. The study was a cross-sectional cohort of veterans derived from the Vietnam Experience Study (see Chapter 5). Veterans were questioned about health-related events that may have occurred any time in the roughly 16 years from military discharge to the time of the study. A subsample of veterans (excluding 40 who were hospitalized after injury and the 38 for whom data were incomplete) were categorized into three groups based on subjects’ responses on a questionnaire: no history of motor-vehicle accident (MVA) and no history of TBI (normal controls, n = 3,214), injured in an MVA but no history of TBI (MVA controls, n = 539), and TBI with altered consciousness (mild TBI, n = 254). A 15-measure neuropsychologic battery and neurologic tests of tandem gait and peripheral visual attention were administered. Results revealed no statistically significant difference in any of the neuropsychologic measures among the three groups. However, on the basis of further exploratory analyses of the data, the authors concluded that the mild-TBI group showed more proactive interference on the verbal-learning measure and a tendency to give up more than controls on difficult attention tasks. The results of the study are limited by the long retrospective, self-reporting nature of the data, which could introduce considerable error. Moderate or Severe Traumatic Brain Injury Ruff et al. (1986) assessed neurocognitive functioning after TBI in 15 patients who had moderate TBI (GCS, 9–12), 20 patients who had severe TBI (GCS, 3–8), and 50 healthy controls. All patients were tested at least 6 months after injury; mean duration between injury and assessment was 1 year in patients with moderate TBI and 2 years in those with severe TBI. The subjects were given a battery of neuropsychologic tests, including IQ, motor, memory, attention, and fluency measures. Although the moderate-TBI group performed worse on all measures than the healthy control group, differences were significant only on the fluency measures. In contrast, the severe-TBI group was significantly different from the healthy controls on almost all measures. The severe-TBI group performed significantly worse than the moderate-TBI group in IQ, attention, and fluency measures. Zec et al. (2001) compared long-term memory impairment in 32 severe-TBI patients living independently or in an intermediate-care facility at least 2 years after injury, 15 spinal-cord–injury patients, and 27 uninjured controls. The TBI patients were in coma or had altered consciousness for at least 3 days. Of the TBI patients, 25 (78%) had either hemiplegia (15) or quadriplegia (10), 19 (59%) had premorbid histories of at least mild alcohol or drug use, and 8 (25%) were intoxicated or under the influence of drugs at the time of injury. Spinal-cord–injury patients were recruited from the same facilities as the TBI patients, had sustained a severe spinal-cord injury, and were at least 2 years after injury. Of that group, 13 (87%) were quadriplegic, and 2 (13%) were paraplegic. The 27 healthy controls were matched for premorbid socioeconomic background and had no statistically significant differences in age and education from the other groups. A comprehensive neuropsychologic battery was administered to assess intelligence,
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury achievement, general cognitive functioning, and memory. The TBI group scored significantly worse than the spinal-cord–injury and control groups on almost all the tests. Bate et al. (2001) studied 35 consecutive patients admitted into an outpatient rehabilitation center over a 3-year period to identify discrete deficits of attention. All patients had severe TBI as defined by a GCS under 8 or PTA over 24 hours. Thirty-five controls were matched on age, premorbid IQ, and education. Participants and controls were given an attention test and an auditory language task. The TBI participants’ reaction times were significantly longer than those of the controls, but TBI participants and controls oriented their visual attention in a similar manner. TBI participants made significantly more errors on the auditory language task than controls when they were performing under dual-task conditions; this suggested a deficit in auditory-verbal attention. Incoccia et al. (2004) studied reaction time in 18 people who had severe TBI (GCS, under 8 for at least 6 hours), a mean interval since injury of 39 months (SD, 38 months), and an average coma duration of 20 days (SD, 12.8 days); their mean age was 32 years (SD, 12.6 years). All TBI participants had good motor recovery as evaluated clinically and had good recovery on the Glasgow Outcome Scale. The controls were 36 people who were closely matched in age and schooling. Simple visual stimuli (alertness condition) and the go-no-go tests (which require response inhibition under particular conditions) were administered. In the test with simple visual stimuli, the TBI group and the controls performed similarly; in the go-no-go tests, the TBI group performed more slowly. The authors noted that the findings indicate that people with TBI show deficits in motor programming despite good motor recovery as evaluated clinically. Studies of Varied Severity: Mild, Moderate, or Severe Traumatic Brain Injury Novack et al. (2000) prospectively examined 72 patients who had TBI to assess cognitive and functional recovery. Inclusion criteria involved loss of consciousness (any duration), skull fracture, PTA (any duration), and objective neurologic findings. Most subjects (49, 68%) sustained a severe TBI (GCS no higher than 8). Subjects were evaluated at 6 and 12 months after injury with a battery of neuropsychologic tests to assess orientation, speed of information processing, concentration, memory, constructional abilities, and verbal skills. Test scores were transformed to standard scores by using norms that account for age and education effects, if available. Change in performance from 6 to 12 months after injury was analyzed. Although participants with severe TBI continued to perform worse than participants with mild to moderate TBI, both groups recovered at a similar rate. Summary and Conclusions The committee reviewed 6 primary studies and 17 secondary studies. Primary and secondary studies are consistent in demonstrating sufficient evidence of an association between severe brain injury and neurocognitive deficit. Neurocognitive impairments result in a host of difficulties in people who sustain severe TBI, ranging from attention, memory, information-processing speed, and executive functions to even more robust functions, such as language and visuospatial constructional skills. Such deficits are likely to affect psychosocial outcomes, such as the ability to drive, return to work, and adjust successfully to societal demands (see Chapter 9).
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury However, there is limited/suggestive evidence that moderate TBI is associated with neurocognitive deficits. Assessment of outcomes in moderate TBI is complicated by the use of many criteria for categorizing “mild,” “moderate,” and “severe” injuries. Thus, in some studies, persons with “moderate” injuries had significantly greater indications of injury (more similar to other categorizations of “severe” injuries), whereas in other studies, persons with “moderate” injuries had significantly smaller indications of injury (more similar to other categorizations of “mild” injuries). The lack of consensus about what constitutes a “moderate” injury complicates understanding of the effects of such injuries. There is inadequate and insufficient evidence of association between mild TBI and neurocognitive deficits more than 6 months after injury. Although there are known to be subjective neurocognitive complaints in some persons with mild TBI after 6 months, the studies show inconsistent results with regard to objective measures of neurocognitive performance in this group. The committee concludes, on the basis of its evaluation, that there is sufficient evidence of an association between severe TBI and neurocognitive deficits. The committee concludes, on the basis of its evaluation, that there is limited/suggestive evidence of an association between moderate TBI and neurocognitive deficits. The committee concludes, on the basis of its evaluation, that there is inadequate/insufficient evidence to determine whether an association exists between mild TBI and neurocognitive deficits.
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury TABLE 6.2 Closed Head Injury and Neurocognitive Outcomes Reference Study Design Population Type of TBI: Mild, Moderate, Severe; Blunt, Penetrating, Blast Health Outcomes or Outcome Measures Results Adjustments Comments or Limitations Dikmen et al., 1995 Prospective cohort 436 adults, head-injured patients recruited at time of injury in one of three prospective longitudinal studies: behavioral outcome of head injury, patient characteristics and head-injury outcome, Dilantin prophylaxis of posttraumatic seizures Minimal severity criteria: any period of LOC, PTA for at least 1 h, or other objective evidence of head trauma Subjects assessed 1 mo, 1 year after injury At 1 year after injury: head-injured significantly worse than controls (p < 0.01) on neuropsychologic tests except difference on Category Test (p < 0.05) Controls matched on age, sex, education Study subjects included 85% of 514 subjects recruited from three longitudinal studies Neuropsychologic tests included Halstead Reitan Neuropsychological Test Battery; motor function assessed with finger-tapping, name-writing for dominant, nondominant hands; attention, concentration, flexibility, quickness measured with Seashore Rhythm Test, TMT A and TMT B, Stroop Color and Word Test Parts 1 and 2; memory evaluated with WMS, WMS-LM, WMS-VR, SR; verbal skills measured with WAIS VIQ; performance skills measured Results represent weighted averages that adjust for differences between studies in inclusion criteria Head-injury severity assessed with GCS, number of nonreactive pupils, mass lesions requiring craniotomy, TFC Nonsignificant differences on two memory measures Severely head-injured (TFC 29 days or greater) had significant impairments on all measures (p < 0.001) except WMS-LM (p < 0.01), WMS-VR (p < 0.05) 121 general TCs enrolled as part of patient-characteristics study Coma from < 1 h to more than 4 weeks Clear dose–response relationship between length of coma (TFC), level of performance on neuropsychologic measures; for example, median II for TC = 0.1; TFC < 1 h = 0.1, 1–24 h = 0.3, 25 h–6 days = 0.4, 7–13 days = 0.4, 14–28
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury Reference Study Design Population Type of TBI: Mild, Moderate, Severe; Blunt, Penetrating, Blast Health Outcomes or Outcome Measures Results Adjustments Comments or Limitations with WAIS PIQ, Tactual Performance Test; reasoning measured with Category Test; overall performance measured with Halstead Impairment Index days = 0.7, ≥ 29 days = 1.0 Dikmen et al., 1986 Prospective cohort 20 hospitalized subjects with mild head injury; 19 uninjured friend controls Mild; subjects met following criteria: coma not over 1 h or, if no coma, PTA of at least 1 h; GCS ≥ 12 on admission; no clinical evidence of cortical or brainstem contusion Motor, psychomotor skills (finger-tapping speed); attention, flexibility, quickness (Speech Sounds Perception, Seashore Rhythm, TMT A, TMT B); memory and learning (WMS, SR); reasoning (Category Test); health status in terms of sickness (Sickness Impact Profile); symptoms frequently reported as part of TBI (Head Injury Symptom 1 mo after TBI, mild neuropsychologic effects found, none significantly different; at 1 year after TBI, similar post-TBI symptoms reported in TBI, non-TBI subjects Matched on age, education, sex Exclusion criteria: subjects with prior head injury, alcoholism, cerebral disease, mental retardation, significant psychiatric disorder 19 of 20 seen at 1 year 15–60 years old Healthy friend controls may not control for general effects of trauma Small sample
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury Reference Study Design Population Type of TBI: Mild, Moderate, Severe; Blunt, Penetrating, Blast Health Outcomes or Outcome Measures Results Adjustments Comments or Limitations Checklist); resumption of major activities, including work, school, homemaking (Function Status Index) Dikmen et al., 1987 Prospective cohort 102 people with closed head injury admitted into Harborview Medical Center, Seattle; 102 friend controls Mild, moderate, severe Memory (WMS, SRP) At 1 mo after TBI, head-injured group performed significantly worse on both memory tests (p < 0.001); at 1 year after TBI, most subscales still show significant impairment Matched on age, education, race, sex Exclusion criteria: prior CNS injury, significant neuropsychiatric difficulties Subjects met following criteria: LOC or PTA over 1 h or evidence of cerebral trauma 15–60 years old 97 of 102 head-injured, 88 of 102 controls evaluated at 1 year after injury 30% GCS 3–8, 12% GCS 9–11, 59% GCS > 12 Memory performance a function of head-injury severity, length of coma at 1 mo; weaker relationship at 1 year after TBI 23% PTA < 24 h, 25% PTA 1–6 days, 20% PTA 7– 13 days, 32% PTA > 14 days 77% moving-vehicle accidents, 10% falls, 8% fights or assaults, 5% other Tate et al., 1991 Cohort Consecutive series of first 100 admissions into adult head-injury Severe, blunt TBI: sustained open head injury, initial Subjects examined by trained clinical 70% of head-injured showed impairments: 56.5% of head-injured Controls matched on age, sex, education, Australian rehabilitation population
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury Reference Study Design Population Type of TBI: Mild, Moderate, Severe; Blunt, Penetrating, Blast Health Outcomes or Outcome Measures Results Adjustments Comments or Limitations rehabilitation unit closed head injury later required neurosurgery neuropsychologist had disorders of learning, memory vs 5% in sibling control group; 16.5% of head-injured had disturbances in basic neurocognitive skills vs 2.5% in sibling control group; 34.1% of head-injured had slowness in information processing vs 2.5% in sibling control group; 40% of head-injured had posttraumatic personality change vs 7.5% in sibling control group SES 82 of 100 subjects completed neuropsychologic tests Followed average of 6.3 years after trauma Neuropsychologic impairment evaluated with MMS, Incomplete Letters, ideomotor praxis tasks, ROCF, WAIS-R Digit Span and Vocabulary subtests, Schonell Reading Test, TMT, SR, AM, Corsi test of recency memory, WCST, TT, Word Fluency Test of Thurstone and Thurstone, DF, BCT Head-injured group sustained severe injuries: 98% had PTA over 1 week, 74% over 1 mo Eligible: 66 males, 21 females, sibling controls 15–45 years old Crude ORs Lannoo et al., 1998 Cohort 85 patients consecutively admitted into the ICU of University Hospital of Gent in September 1993–February 1996 Moderate to severe TBI (GCS score 3–12) Administered neuropsychologic test battery at 6 mo after injury, including tests of: attention, information processing; visual reaction time; memory, learning; verbal fluency; mental flexibility MANOVA on neuropsychologic test battery indicated significant difference between groups (p < 0.05); univariate analyses showed significant differences (p < 0.05) on almost all tests, with TBI group performing worst Inclusion criteria for patients and controls: ages 15–65 years, no history of CNS disease or mental retardation 32 TCs (traumatic injuries of parts of body other than head) admitted into ICU during same
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Gulf War and Health, Volume 7: Long-Term Consequences of Traumatic Brain Injury Reference Study Design Population Type of TBI: Mild, Moderate, Severe; Blunt, Penetrating, Blast Health Outcomes or Outcome Measures Results Adjustments Comments or Limitations study period Heitger et al., 2006 Prospective cohort 37 patients with mild head injury, 37 controls; patients recruited from ED of Christchurch Hospital, New Zealand; controls recruited from database of interested students Mild Neurocognitive testing: PASAT, TMT A and TMT B, WASI At 12 mo, no neurocognitive deficits remained Controls matched on age, sex, education Exclusion criteria included alcohol or drug use; CNS disorder; psychiatric conditions; structural brain damage or hematoma on CT scan; oculomotor or somatomotor deficits; strabismus, poor visual acuity, skull fracture, or history of prior TBI Marginal group differences on CVLT total standard score NOTE: AM = Austin Maze, BCT = Booklet Category Test, CNS = central nervous system, CT = computed tomography, CVLT = California Verbal Learning Test, DF = Design Fluency Test, ED = emergency department, GCS = Glasgow Coma Scale, ICU = intensive care unit, LOC = loss of consciousness, MANOVA = multivariate analysis of variance, MMS = Mini Mental Status, OR = odds ratio, PASAT = Paced Auditory Serial Addition Test, PIQ = performance intelligence quotient, PTA = posttraumatic amnesia, ROCF = Rey-Osterrieth Complex Figure Test, SES = socioeconomic status, SR = Selective Reminding Test, SRP = Selective Reminding Procedure, TBI = traumatic brain injury, TC = trauma control, TFC = time to follow commands, TMT A and TMT B = Trail Making Test A and B, TT = Tower of London Test, VIQ = Verbal Intelligence Quotient, WAIS = Wechsler Adult Intelligence Scale, WAIS-R = Wechsler Adult Intelligence Scale—Revised, WASI = Wechsler Abbreviated Scale of Intelligence, WCST = Wisconsin Card Sorting Test, WMS = Wechsler Memory Scale, WMS-LM = Wechsler Memory Scale, Logical Memory, WMS-VR = Wechsler Memory Scale-Visual Reproduction.
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