Feasibility of a Brief Neuropsychologic Test Battery During Acute Inpatient Rehabilitation After Traumatic Brain Injury

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SPECIAL SECTION: ORIGINAL ARTICLE

Feasibility of a Brief Neuropsychologic Test Battery During Acute Inpatient Rehabilitation After Traumatic Brain Injury Kathleen Kalmar, PhD, Thomas A. Novack, PhD, Risa Nakase-Richardson, PhD, Mark Sherer, PhD, Alan B. Frol, PhD, Wayne A. Gordon, PhD, Robin A. Hanks, PhD, Joseph T. Giacino, PhD, Joseph H. Ricker, PhD ABSTRACT. Kalmar K, Novack TA, Nakase-Richardson R, Sherer M, Frol AB, Gordon WA, Hanks RA, Giacino JT, Ricker JH. Feasibility of a brief neuropsychologic test battery during acute inpatient rehabilitation after traumatic brain injury. Arch Phys Med Rehabil 2008;89:942-9. Objectives: To determine (1) if more than 50% of patients with moderate to severe traumatic brain injury (TBI) who met study criteria can complete a battery of neuropsychologic tests in less than 75 minutes 2 to 6 weeks after injury regardless of posttraumatic amnesia (PTA) status; (2) which tests are most likely to be completed; and (3) range of scores obtained. Design: Prospective multicenter observational study. Setting: Acute inpatient neurorehabilitation hospitals. Participants: Screened 543 Traumatic Brain Injury Model System patients with moderate to severe TBI; 354 were tested at 2 to 6 weeks postinjury. Interventions: Not applicable. Main Outcome Measure: Percentage of patients able to complete the neuropsychologic tests in less than 75 minutes. Results: Two hundred eighteen (62%) patients completed the battery in 66 minutes on average. Mean interval from injury to testing was 28.3⫾7.1 days. Tests completed with the highest frequency were California Verbal Learning Test⫺II, FAS, and animal naming. Performance was less impaired (P⬍.001) on all measures for patients who had emerged from PTA. Conclusions: Approximately two thirds of screened patients were able to complete a brief neuropsychologic test battery at 2 to 6 weeks postinjury, regardless of PTA status. Although patients out of PTA were less impaired on all test measures, confusion did not preclude participation in the test battery or prohibit assignment of test scores. Early neuropsychologic

From JFK Johnson Rehabilitation Institute at JFK Medical Center, Edison, NJ (Kalmar); Spain Rehabilitation Center, Birmingham, AL (Novack); James A. Haley VAMC, Tampa, FL (Nakase-Richardson); Memorial Hermann/TIRR, Houston, TX (Sherer); Department of Physical Medicine and Rehabilitation, Baylor Institute for Rehabilitation, Dallas, TX (Frol); Department of Rehabilitation Medicine, Mount Sinai School of Medicine, New York, NY (Gordon); Department of Physical Medicine and Rehabilitation, Wayne State University School of Medicine, Detroit, MI (Hanks); Department of Rehabilitation Psychology and Neuropsychology, Rehabilitation Institute of Michigan, Detroit, MI (Hanks); JFK Johnson Rehabilitation Institute and New Jersey Neuroscience Institute at JFK Medical Center, Edison, NJ (Giacino); and Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA (Ricker). Supported by the National Institute on Disability and Rehabilitation Research (grant nos. H133A020501, H133A020502, H133A020509, H133A020514, H133A020515, H133A020518, H133A020526). 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. Reprint requests to Kathleen Kalmar, PhD, JFK Johnson Rehabilitation Institute, JFK Medical Center, 3EA, Neuropsychology, Brain Trauma Unit, 65 James St, Edison, NJ 08818, e-mail: [email protected]. 0003-9993/08/8905-00056$34.00/0 doi:10.1016/j.apmr.2008.01.008

Arch Phys Med Rehabil Vol 89, May 2008

assessment after TBI is feasible even for many patients who are still in PTA. Key Words: Brain injuries; Rehabilitation. © 2008 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation HE TIMING OF THE INITIATION of neuropsychologic testing after traumatic brain injury (TBI) and which tests to T use are matters of debate. Many rehabilitation professionals 1

argue that testing is not appropriate before resolution of posttraumatic amnesia (PTA), often determined on the basis of recovery of orientation as measured by tests such as the Galveston Orientation and Amnesia Test (GOAT).2 Others argue that a delay of cognitive testing distorts our understanding of recovery after TBI. A number of studies examining the association between early cognitive testing and late outcome3-5 have only included people who have emerged from PTA, essentially focusing on those with the best recovery. For example, in a study by Sherer et al5 investigating the relationship between early cognitive status and employment outcome, 16% of potential participants with TBI were not included because their PTA did not resolve before rehabilitation discharge. Awaiting the resolution of PTA before initiating neuropsychologic testing confounds test results with injury severity. For example, a person with a PTA duration of 1 week is less severely injured than a person with PTA duration of 2 months, but if testing is deferred until the resolution of PTA, the results of cognitive testing may be similar. This may limit the ability of neuropsychologic test scores to predict outcome, a significant issue clinically. Additionally, Wilson et al6 have shown that patients in PTA can participate in neuropsychologic testing. A difference between TBI samples in or out of PTA was noted on only 2 tests involving cognitive processing speed (simple reaction time, animal fluency). This finding opens doors for clinicians to provide more timely and extensive information about cognitive deficits after TBI. These concerns have prompted some researchers to explore the possibility of neuropsychologic testing at a fixed time postinjury. For example, Dikmen7 and Pastorek8 and colleagues in several studies elected to test subjects at 1 month after injury, regardless of PTA status, to ensure that data from the most severely injured people were represented in the sample of subjects studied. One result of their work was the finding that being untestable at 1 month after injury was itself a strong predictor of outcome, as defined by return to employment. This finding was confirmed by Pastorek8 who administered 4 measures of attention and language comprehension to subjects with TBI a month after injury regardless of their orientation status. Cognitive performance at the time of testing was predictive of outcome at 6 months after injury, controlling for age, education, Glasgow Coma Scale (GCS) score, and pupil response. Unfortunately, Pastorek did not provide the proportion of those able to complete the test battery, so the

FEASIBILITY OF NEUROPSYCHOLOGY TEST BATTERY, Kalmar

question of how many people were able to complete the battery of tests at 1 month after injury in their sample is not known. Testing at a fixed time after injury early in the course of recovery may also allow cognitive test data to become a marker for the severity of injury, an important supplement to existing measures, such as the GCS. In addition, recent work draws into question the concept of PTA as a distinct cognitive phase. Stuss et al9 have shown that a range of cognitive deficits exist during what has been traditionally labeled as PTA, and the pace of recovery varies for different areas of cognition. As a result, Stuss has advocated that this phase of recovery be described as a “posttraumatic confusional state,” reflecting the breadth of potential impairments and their differential rates of recovery. Labeling the phase as PTA is regarded as a limited description of the diversity of cognitive function and is thus possibly misleading. Nakase-Thompson et al10 have added to this impression, showing that early recovery after severe TBI can be described in terms of delirium. One impact of viewing early recovery of cognitive function after TBI in terms of a confusional state is that there is no reason to withhold testing based on performance in 1 specific area of cognition (such as orientation). Stuss9 has shown the clinical value of testing during a confusional state by focusing on the extent and pace of recovery, which potentially could guide cognitive rehabilitation efforts. As yet, the feasibility of testing early in the course of TBI recovery, particularly for those who are severely injured, has not been adequately shown. For purposes of this study, we define feasibility as the ability of the examiner to present a cognitive test to the patient and assign a score that reflects the patient’s performance on the test. The present study was designed to determine the following: (1) if more than 50% of patients with moderate to severe TBI meeting study criteria during acute inpatient rehabilitation 2 to 6 weeks after injury can complete a battery of neuropsychologic tests in less than 75 minutes, regardless of PTA status; (2) which tests in the battery were most likely to be completed; and (3) the range of scores obtained by these subjects. METHODS Participants The sample was comprised of all patients admitted to 7 collaborating centers as part of the National Institute on Disability and Rehabilitation Research Traumatic Brain Injury Model Systems (TBIMS) program from July 1, 2004, through July 30, 2006. Criteria for the TBIMS program include (1) medically documented TBI, (2) treatment at an affiliated level I trauma center within 72 hours of injury, (3) receipt of inpatient rehabilitation within the TBIMS, (4) admission to inpatient rehabilitation within 72 hours of discharge from acute care, (5) age of at least 16 years at the time of injury, and (6) provision of informed consent by the person with the injury or a legal proxy.11 Additional qualifying criteria for the current investigation included: (1) availability for testing between 2 and 6 weeks postinjury and (2) adequate English fluency to complete cognitive tests. Data Collection Procedures The current project was a multicenter collaborative prospective observational study with measures selected by consensus of the authors (all neuropsychologists) for appropriateness and sensitivity to the cognitive impairments most frequently reported in people with TBI12,13 and the availability of demographically corrected norms. All persons meeting TBIMS pro-

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gram inclusion criteria, as described earlier, were screened for potential participation in this study, and all participating centers obtained review and approval for this project by their institutional review boards. Research assistants collected information regarding demographic characteristics and injury severity. All eligible subjects were administered formal neuropsychologic testing at 4 weeks postinjury (⫾2wk) by psychologists, research assistants, or others (eg, psychometrists) with appropriate training to correctly administer the study measures (see table 1 for a listing and description of test measures). If possible, testing was completed in 1 testing session and tests were administered using standardized protocols and given in the sequence listed in table 1. Tests were scored using demographically corrected transformed norms as available.14-18 Psychometric properties for these measures, such as test-retest reliabilities and validity, are available in published manuals for these measures and/or other published works.12,13 Battery- and test-completion codes were used to describe the patient’s ability to complete the entire neuropsychologic test battery and specific testing tasks (see appendix 1 for a detailed description of these codes and procedures). Tests were considered to be completed if the patient finished the test as indicated by test instructions or if the patient attempted the test but was unable to make progress so that the examiner discontinued the test. As an example, if a patient initially attempted to connect circles in numeric order, as required on the Trail-Making Test part A (TMT-A), but then discontinued connecting circles, doodled, and could not be redirected to the task, that performance would be considered a complete test administration. The examiner would discontinue the test and assign the most impaired possible score. Data Analysis Demographic data of study patients and patients who did not meet inclusion criteria were compared on a variety of study measures. These include chi-square analyses for qualitative variables, Mann-Whitney U analyses for ordinal data, and t tests for interval data. The range of scores among tests is presented as T scores to allow for comparability within and between the various measures studied. A T score is a standard score with a mean of 50 and a standard deviation (SD) of 10. The use of T scores permits comparison to other standard scores as well as application of percentile ranks to facilitate comparison of scores between persons or between groups of persons. To explore the relationship between PTA and patient performance, patients who had emerged from PTA were separated from those still in PTA based on TBIMS criteria for emergence. PTA was defined as the interval from injury until 2 consecutive observations were obtained within a period of 24 to 72 hours in which a patient scored in target range on either the GOAT score (⬎75) or the Orientation-Log (O-Log score ⬎24).2,19,20 For patients admitted to rehabilitation who were observed to be already emerged from PTA, a chart review procedure was conducted to determine if there were 2 consecutive observations within a 24- to 72-hour period in which he/she was determined to be “oriented ⫻ 3” without interval notes denoting disorientation. Note that these data (GOAT and O-Log scores for determining PTA groups) were collected separately from the neuropsychologic test battery and were extracted from the TBIMS database. Based on this criterion, 112 subjects were assigned to the in-PTA group, and 241 were assigned to the out-of-PTA group. These 2 groups were compared on neuropsychologic test raw scores using analysis of variance (ANOVA). Arch Phys Med Rehabil Vol 89, May 2008

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FEASIBILITY OF NEUROPSYCHOLOGY TEST BATTERY, Kalmar Table 1: Description of Neuropsychologic Measures and Order of Test Administration Neuropsychologic Measures

Description 2

Galveston Orientation and Amnesia Test California Verbal Learning Test–II Standard Form15

Trail-Making Test parts A and B21

Symbol Digit Modalities Test16 Grooved pegboard test22

FAS/animal naming verbal fluency23

Wechsler Test of Adult Reading17 Wisconsin Card Sorting Test–6418

A measure of PTA with 10 questions covering orientation and memory for circumstances of injury A verbal learning/memory measure composed of 5 learning trials of 16 words with recall of an intervening word list before presenting a shortdelay free and cued recall followed later by long delay-free, short recall, and recognition trial Measures of attention and executive functions (cognitive flexibility) that involve numeric sequencing and alternating sequential numbers and letters, respectively A measure of information-processing speed involving graphomotor copying of numbers associated with symbols for 90s A measure of fine motor speed and dexterity that involves placement of 25 pegs into slots first with the dominant hand followed by a trial with the nondominant hand Verbal fluency measures that are associated with executive functions and semantic memory, respectively, as measured by phonemic fluency for three, 60-s trials of word generation of the letters F, A, and S with category fluency measured by 60-s generation of animal names A measure of reading recognition for 50 words that provides an estimate of premorbid intelligence A measure of executive functions with 64 items designed to assess the capacity for strategic planning, organized searching, the ability to use environmental feedback to shift cognitive sets, goal-directed behavior, and the ability to modulate impulsive responding12

RESULTS Testability of Patients During the study period, 543 patients with TBI meeting TBIMS inclusion criteria were admitted to the 7 study sites. Of these, 140 (26%) were admitted greater than 6 weeks postinjury or were discharged before 2 weeks postinjury, were not adequately fluent in English to permit testing, or were discharged before testing because of scheduling problems. Another 49 (9%) were nonresponsive, minimally conscious, or so aggressive as to pose a safety risk. After these exclusions, there were 354 qualified patients for whom testing was attempted. Demographic data for the study patients compared with those who were not included are presented in table 2. Patients who were not tested were statistically older, had longer durations of PTA, and were represented by a higher proportion of Hispanic individuals (likely representing, to some degree, persons who did not possess adequate English fluency to complete cognitive tests as part of the study inclusion criteria). Among these 354 patients, it was possible for the examiner to present each test and assign a score that reflected the patient’s performance on the test for 312 (88%) patients. Of these 312 patients, 218 (70%) were able to complete all tests in a manner consistent with test demands. For 94 of the 312 (30%) patients, some tests were not completed in a manner consistent with test demands, and the examiner assigned the lowest possible score for the test to indicate that the patient was not able to complete the test. For the remaining 42 (12%) of the 354 patients, some tests could not be attempted. Reasons for failure to attempt a specific test would have been the patient became ill or was needed for a medical test or some other reason that was beyond the control of the patient or examiner and/or an attempt to readminister the test was not possible within the testing window. For more than 75% (n⫽273) of the 354 patients, the testing time was equal to or less than 75 minutes. These 273 people Arch Phys Med Rehabil Vol 89, May 2008

included 87 (32%) patients who were still in PTA at the time of testing. The mean days postinjury ⫾ SD at the time of testing was 28.3⫾7.1, and the average patient completed testing in 66⫾14.3 minutes. Frequency of Tests Completed Tests completed in a manner consistent with the demands of the test with the highest frequencies were measures of verbal fluency (FAS, 93%; animal naming, 93%), and verbal memory California Verbal Learning Test⫺II (CVLT-II) (92%). Measures completed in a manner consistent with the demands of the test with the lowest frequencies were grooved pegboard test, nondominant hand (72%), dominant hand (78%), and the TrailMaking Test part B (TMT-B) (78%). The Range of Scores Obtained The range of scores across tests is depicted as T scores in figure 1. Higher scores were noted on the Wisconsin Card Sorting Test (WCST) (n⫽337) in which the average patient obtained mean T scores of 34 for both number of perseverative responses, which constitutes persisting responding to a principle despite examiner feedback that the response is correct or incorrect (SD⫽10.7), and total errors, which represents the average total number of incorrect responses across the 64 trials (SD⫽9.7). These scores fell 1.5 SDs below the expected scores for uninjured persons. The average number of categories completed, which is the number of blocks of 10 consecutive correct matches to the currently correct principle, was 1.5⫾1.4.18 On the CVLT-II, patients (n⫽349) had, on average, T scores of 30.3⫾11.1 for trials 1 to 5, a measure of total immediate recall of word list material presented over 5 learning trials; 31.5⫾8 for short-delay free recall, which assesses the capacity for spontaneous retrieval of the word list material after a brief distractor activity; and 30.8⫾7.8 for long-delay free recall, which assesses the ability to spontaneously retrieve the word list material after a 20-minute delay. These scores are almost 2

FEASIBILITY OF NEUROPSYCHOLOGY TEST BATTERY, Kalmar Table 2: Descriptive Information for Study and Nonstudy Patients Characteristics

Sex, n (%) Male Female Missing Age (y) Mean ⫾ SD n Race, n (%) White Black Hispanic Other Missing Years of education, n (%) ⬍12y High school diploma ⬎Some college Missing/unknown PTA duration (d) Mean ⫾ SD n Cause of injury, n (%) Motor Fall Blunt injury Gunshot wound Pedestrian Hit/flying object Other Missing GCS emergency department admission score, n (%) 3–8 9–12 13–15 Missing

Study Sample Excluded Sample (n⫽354) (n⫽189)

252 (71) 102 (29) 0 (0)

135 (71) 52 (28) 2 (1)

38.8⫾18.8 354

47.9⫾21.6 187

233 (66) 94 (27) 18 (5) 9 (2) 0 (0)

115 (61) 35 (19) 27 (14) 9 (5) 2 (1)

P

NS

⬍.001

⬍.01

NS 131 (37) 99 (28) 124 (35) 0 (0)

70 (36) 05 (30) 61 (32) 04 (2)

22.9⫾14.1 306

37.5⫾43.9 110

215 (61) 64 (18) 20 (5) 13 (4) 17 (5) 3 (1) 22 (6)

87 (46) 61 (32) 8 (4) 6 (3) 16 (8) 5 (3) 4 (2) 2 (1)

⬍.001 NS

NS 189 (53) 66 (19) 89 (25) 10 (03)

91 (48) 25 (13) 56 (30) 17 (09)

Abbreviation: NS, not significant.

SDs below the expected scores for noninjured persons. For total recognition discriminability, an index of correct recognition responses relative to total false-positive responses on a word list recognition trial, the mean T score was 34.1⫾9.3, greater than 1.5 SDs below the expected mean for noninjured persons. Additionally, the mean total recognition hits raw score, which quantifies the number of correct word list items identified by the patient on the recognition trial, was 11 of 16, a score that is 3.7 SDs below the mean for noninjured persons. This score does not get transformed to a T score and is therefore not presented in figure 1. Scores indicating even greater impairment were observed on the grooved pegboard test. Performance with the nondominant hand (n⫽329) averaged a T score of 22.1⫾10.2, and T scores with the dominant hand had a mean of 22.8⫾10.8. Patients also showed substantial difficulty with the Symbol Digit Modalities Test (SDMT) on which the lowest attainable T score was 24. The average T score on the written trial was 28.4⫾6, and, on the oral trial, it was 28.6⫾6.1, indicating a skewed distribution and floor effect. Taking SDs into consideration, performance within all tests varied from borderline to normal range (⬎4th percentile) to profoundly impaired. The average Wechsler Test

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of Adult Reading (WTAR)–predicted full-scale IQ score for the study sample was 96⫾8.8. The average GOAT score obtained as part of the cognitive test battery to assess orientation independent of PTA status for the total sample of tested patients was 79.2⫾17.5, (range, – 8 to 100). Almost three quarters of these patients (n⫽249/342) obtained scores above the standard cutoff of 75. Note that PTA status was determined separately by using the standard TBIMS guideline that requires 2 consecutive GOAT or O-Log scores within a 24- to 72-hour interval. These data were drawn from the TBIMS database rather than by the single GOAT score obtained as part of the brief cognitive test battery for purposes of establishing the patient’s level of orientation. Characteristics of Patients In and Out of PTA Of the 354 study patients, 242 (68%) were emerged from PTA by TBIMS criteria and 112 (32%) were still in PTA (group assignment criteria were discussed earlier in the Data Analysis section). The average age for patients still in PTA was 44 years, whereas those who emerged from PTA were younger, with a mean age of 36. However, the level of education was essentially the same regardless of PTA status. People still in PTA were tested an average of 31 days postinjury and people out of PTA were tested on average 27 days postinjury. Test-completion times did not differentiate groups (table 3). As expected, the in-PTA group obtained a lower (more impaired) GOAT score mean of 60 as compared with the out-of-PTA group with an average GOAT score of 89. Predicted WTAR full-scale IQ scores were similar between the groups despite the fact that patients who had emerged from PTA performed significantly better on all other neuropsychologic test measures (P⬍.001) based on ANOVA tests of raw scores of the 6 tests (table 4, fig 2).a These test raw scores are also presented as T scores to show the degree of impairment between the 2 PTA groups (fig 3). Interestingly, the presence or absence of PTA only modestly influenced test-completion profiles. For both participants in and out of PTA, FAS, animal naming, and CVLT-II were among the most frequently completed tests (range for patients in PTA, 81%– 86%; range for patients out of PTA, 97%–99%), whereas grooved pegboard and TMT-B were the least frequently completed tests (table 5). Although test-completion rates were consistently lower for patients in PTA, the majority were able to respond in a manner consistent with the demands of the test. DISCUSSION The present investigation shows the feasibility of completing a brief neuropsychologic battery of tests with patients in early recovery from moderate to severe TBI independent of whether or not PTA had resolved at the time of testing. Well over 50% of eligible patients completed the battery in under 75 minutes. The primary reasons that patients were not tested was because they were not available for testing during the planned interval or because they were not English speaking, rather than their inability to attempt to perform the tests. Although test compliance was poorer for those still in PTA, a high percentage of individuals in both groups were able to complete most of the neuropsychologic tests. The fact that such an assessment can be accomplished in a relatively brief time is encouraging. The findings are particularly important to consider in a time of earlier rehabilitation admissions and shorter inpatient rehabilitation Arch Phys Med Rehabil Vol 89, May 2008

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FEASIBILITY OF NEUROPSYCHOLOGY TEST BATTERY, Kalmar

50 45

Test Scores (T-Scores and SD Ranges)

40 35 30 25 20 15 10 5 0 Trial-1-5 SDFR LDFR RecogD

A

CVLT-II

B TMT

Written Oral SDMT

DH

NDH

GPB

FAS

Naming

Per Res Tot Err

Fluency

WCST

Neuropsychologic Tests

stays, each of which increase the probability that persons with TBI will be treated and even discharged from acute inpatient rehabilitation programs while they are still in PTA. Tests of verbal fluency and verbal memory were completed at the highest rates. Verbal learning and executive functioning, as measured by tests in this battery, represented areas of relatively less impaired test performance, yet, even on these tests, the mean scores were 1.5 to 2 SDs below the mean of noninjured persons. Performance on the other test measures was generally greater than 2 SDs below the normal distribution mean. As expected, patients whose PTA had resolved exhibited more intact performance on all neuropsychologic measures than those who remained in PTA. Additionally, decreased fine motor speed and dexterity appear to be significant factors that influence early test results in persons with TBI. Tasks requiring rapid responding and fine motor dexterity were completed at the lowest rates regardless of PTA status. However, when the patients were divided by PTA status, these motor tasks were less frequently completed by those still in PTA, supporting the findings of Wilson et al6 that processing speed and cognitive flexibility are factors differentiating those in and out of PTA. Reassuringly, a measure designed to estimate premorbid intellectual level (WTAR) was not affected by whether or not PTA had resolved and showed that differences between the

Fig 1. Mean T scores with 1 SD score ranges for neuropsychologic tests across measures for all patients. NOTE. CVLT total number of words remembered, TMT total seconds to test completion, SDMT total number correct in 90 seconds, grooved pegboard test (GPB) total seconds to test completion, fluency total number of words generated in 1 minute per trial, and WCST total number of perseverative responses and total errors. Higher scores indicate better performance on the CVLT, SDMT, and fluency measures (FAS/animal naming). Higher scores indicate poorer performance on the TMT, grooved pegboard test, and WCST. Abbreviations: DH, dominant hand; LDFR, long delay, free recall; Naming, animal naming; NDH, nondominant hand; Per Res, perseverative response; RecogD, recognition delayed; SDFR, short delay, free recall; Tot Err, total errors.

groups in test performance was not attributable to differences in estimated premorbid intellectual function, suggesting it is not a sensitive index of cognitive function at the acute stage of recovery. Although group differences were substantial, both those in PTA and not in PTA showed a wide range of performances on all measures. Various patients whose PTA had resolved still showed very severe impairments on some tests, whereas other patients still in PTA showed surprisingly intact abilities. Although test performance for patients in PTA was undoubtedly influenced by residual confusion, this variability suggests that even at an early time postinjury, neuropsychologic test profiles may reveal relative strengths and weaknesses that could have implications for current rehabilitation therapies and planning for placement in the postacute period. The results of this study are consistent with the finding of Stuss et al9 that people in PTA show a range of cognitive abilities and underscores the importance of evaluating a broad array of mental capacities early in recovery, beyond measuring orientation alone. Measures of orientation can document progress but in a limited sphere of cognition. A broader assessment of cognition early in recovery, such as the battery of tests used in this study, may provide a better basis for recommendations regarding rehabilitation activities and possibly a firmer foundation for projecting outcome.

Table 3: Descriptive Information for Patients In and Out of PTA In PTA

Out of PTA

Statistics

Characteristics

Mean ⫾ SD

n

Mean ⫾ SD

n

Age (y) Education (y) Postinjury at testing (d) Battery completion time (min) GOAT score Predicted WTAR full-scale IQ

43.9⫾16.2 12.0⫾2.1 31.0⫾7.6 64.9⫾16.3 59.6⫾22.9 96.2⫾8.2

112 112 112 109 111 105

36.4⫾15.5 12.2⫾1.9 27.0⫾6.4 67.1⫾14.0 88.6⫾9.0 96.0⫾9.1

240 240 241 233 231 236

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P

t⫽3.50 t⫽–0.50 t⫽4.13 t⫽0.88 t⫽12.16 t⫽0.20

⬍.001 .560 ⬍.001 .381 ⬍.001 .844

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FEASIBILITY OF NEUROPSYCHOLOGY TEST BATTERY, Kalmar Table 4: Statistical Analyses and Test Means and SDs for Neuropsychologic Test Performance for Patients In and Out of PTA ANOVA Tests

Test Statistics In PTA

Test

CVLT-II trials 1–5 CVLT-II short-delay free recall CVLT-II long-delay free recall CVLT-II recognition hits Multiple variance test statistic WCST perseverative errors WCST total errors WCST categories complete Multiple variance test statistic TMT-A TMT-B SDMT written SDMT oral Grooved pegboard DH Grooved pegboard NDH Fluency: FAS Fluency: animal naming

P

Mean ⫾ SD

n

Mean ⫾ SD

n

⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001

18.5⫾10.4 1.7⫾2.0 1.7⫾2.1 8.6⫾5.0

110 110 110 110

34.3⫾9.9 5.4⫾2.8 5.4⫾2.9 12.1⫾2.8

239 239 239 239

38.2⫾19.6 42.9⫾12.0 0.6⫾0.9

105 105 105

25.0⫾14.9 30.1⫾12.2 1.9⫾1.3

232 232 232

77.0⫾17.9 253.2⫾63.6 14.3⫾11.2 16.0⫾12.8 146.9⫾26.0 171.0⫾40.6 10.6⫾7.3 6.3⫾4.3

110 108 109 109 107 104 108 109

54.3⫾19.0 170.6⫾81.1 28.21⫾10.9 32.8⫾11.6 114.2⫾32.6 141.2⫾43.5 20.5⫾7.9 12.0⫾4.2

236 236 235 237 225 225 241 239

Univariate Tests

F1,347⫽119.45 F1,347⫽98.77 F1,347⫽90.34 F1,347⫽46.54 F4,344⫽31.14 F1,335⫽34.40 F1,335⫽54.56 F1,335⫽50.94 F3,333⫽19.32 F1,344⫽79.19 F1,342⫽67.57 F1,342⫽77.68 F1,344⫽92.74 F1,330⫽57.69 F1,327⫽25.86 F1,347⫽76.42 F1,346⫽84.51

Out of PTA

Abbreviations: DH, dominant hand; NDH, nondominant hand.

Unfortunately, it is difficult to specify a typical pattern or level of deficits for patients with TBI of varying severity at a fixed time postinjury. First, injury characteristics (eg, location and extent of neuropathology) and premorbid variables influence the pattern of deficits observed so that there is not 1 general pattern of performance but, instead, a large number of possible patterns of performance determined by the areas of the brain predominantly affected, premorbid ability, age, years of education, and other factors. Second, different tests were originally standardized on different groups at different times. This

makes comparison of performances between tests more of a clinical art than a scientific endeavor. For example, our finding that patients showed relatively less impairment on the complex abilities measured by the WCST as compared with the relatively more simple demands of TMT-A is conceptually difficult to explain. One could argue that this finding likely represents an artifact because of how the tests were normed or the impact of reduced processing speed or fine motor dexterity as opposed to an accurate reflection of the neurocognitive effects of TBI. The efforts of Heaton et al14 to provide norms for a wide range

Fig 2. A comparison of neuropsychologic test performance (raw scores) by PTA status (determined by TBIMS criteria as described in the Data Analysis section). Abbreviations: see figure 1.

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FEASIBILITY OF NEUROPSYCHOLOGY TEST BATTERY, Kalmar

Fig 3. A comparison of neuropsychologic test performance (T scores and 1 SD score ranges) by PTA status (determined by TBIMS criteria as described in the Data Analysis section). NOTE. T scores of 40 equal performance at 1 SD below the mean of normative persons, T scores of 30 equal performance at 2 SDs below the mean, and T scores of 20 equal performance at 3 SDs below the mean. Higher T scores indicate better performance across all tests.

of tests derived from the same normative sample must be continued and expanded. Study Limitations The present investigation sought to address only the limited question of whether it is feasible to assess cognitive functioning in all patients with TBI who are available for testing early after injury. This article does not examine the clinical or research utility of these early assessments, leaving this for a follow-up study. Although we have established the feasibility of the use of a brief neuropsychologic battery for use at the acute level of rehabilitation, this investigation does not examine the individual utility of the various tests. Such information, at the very least, has implications for further reducing the battery by removing those measures that offer little in terms of predictive validity. Investigation into this question is being conducted concurrently as part of a separate study.

Although it was possible to obtain test scores for a high percentage of those who met criteria for testing, a substantial number of potential patients were not available during the target window of 2 to 6 weeks postinjury. This might have created an unintended selection bias in those who were tested. In clinical care, these persons could still be tested before or after this window as needed. For research, this unavailability poses a challenge because it is likely to be related to other factors such as injury severity, comorbidities, and age, which also influence eventual outcome. CONCLUSIONS Our investigation shows that early neuropsychologic testing of patients with TBI is feasible whether or not they have emerged from PTA. Additional investigation of the clinical utility of these findings is needed.

Table 5: Percentage of Complete (TCCⴝ1) and Partially Complete (TCCⴝ2) Neuropsychologic Tests Obtained from Patients by PTA Group In PTA

Out of PTA

Test

Completed

Partial

Test

Completed

Partial

Animal naming FAS WTAR CVLT-II WCST TMT-A SDMT oral SDMT written Grooved pegboard test DH Grooved pegboard test NDH TMT-B

86 85 82 81 81 78 74 72 66 61 59

14 15 18 19 19 22 26 28 34 39 41

CVLT-II Animal naming FAS SDMT oral WTAR TMT-A SDMT written WCST Grooved pegboard test DH TMT-B Grooved pegboard test NDH

99 98 98 98 97 96 95 94 91 91 86

1 2 2 2 3 4 5 6 9 9 14

NOTE. Values are percent. PTA determined by TBIMS criteria described in the Data Analysis section.

Arch Phys Med Rehabil Vol 89, May 2008

FEASIBILITY OF NEUROPSYCHOLOGY TEST BATTERY, Kalmar

APPENDIX 1: DESCRIPTION OF BATTERY AND TEST-COMPLETION CODES AND SCORING SCHEMA Battery Completion Codes 1. Complete Battery Given: All tests were administered. 2. Partial Completion: Some but not all tests were administered (see Test-Completion Codes below). 3. Battery Not Given, Patient Factors: No tests were given because of patient factors such as medical reasons or neurologic status such that the patient is not capable of purposeful behavior or command following. 4. Battery Not Given, External Factors: No tests were given because the patient was discharged prematurely, falls outside of the “testable” window, insufficient staffing and/or scheduling problems, or the patient does not speak English or English is not the primary language. Test Completion Codes 1. Test Completed: The patient responded in a manner consistent with the demands of the test. For example, the patient may have performed well or poorly (can include neologisms [ie, distorted or fragmented words, made up words] for California Verbal Learning Test⫺II [CVLT] or FAS, not placing all the pegs on grooved pegboard test [GPT] or connecting all the circles on Trail-Making Test [TMT]). Use the patient’s actual score. 2. Test Administration Attempted: The patient could not or would not respond in a manner consistent with the demands of the test as a result of the brain injury. The lowest possible score is assigned (can include the patient who draws only a smiley face on TMT, touches none of the pegs on GPT, talks about going home instead of giving CVLT words, and so on). This code should also be used for a patient who initially complies with task demands but then refuses to complete the test or begins responding in a manner inconsistent with task demands. Use the lowest possible raw score available for the test, taking demographic information into consideration as appropriate in calculating the corresponding standardized score. 3. Test Administration Not Attempted: The patient became ill or was needed for a medical test or some other reason that was beyond the control of the patient or examiner. An attempt to readminister the test was not possible within the testing window. No score is used for study purposes and will be considered as missing data. References 1. Sherer M, Novack T. Neuropsychological assessment for monitoring recovery after traumatic brain injury and making treatment recommendations in adults. In: Prigatano G, Cullum M, Pliskin N, editors. Demonstrating the utility and cost effectiveness in clinical neuropsychology. New York: Psychology Pr; 2003. p 39-60. 2. Levin HS, O’Donnell VM, Grossman RG. The Galveston Orientation and Amnesia Test: a practical scale to assess cognition after head injury. J Nerv Ment Dis 1979;167:675-84. 3. Cifu DX, Keyser-Marcus L, Lopez E, et al. Acute predictors of successful return to work 1 year after traumatic brain injury: a multicenter analysis. Arch Phys Med Rehabil 1997;78:125-31.

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4. Boake C, Millis SR, High WM Jr, et al. Using early neuropsychologic testing to predict long-term productivity outcome from traumatic brain injury. Arch Phys Med Rehabil 2001;82:761-8. 5. Sherer M, Sander AM, Nick TG, High WM Jr, Malec JF, Rosenthal M. Early cognitive status and productivity outcome after traumatic brain injury: findings from the TBI model systems. Arch Phys Med Rehabil 2002;83:183-92. 6. Wilson BA, Evans JJ, Emslie H, Balleny H, Wason PC, Baddeley AD. Measuring recovery from post traumatic amnesia. Brain Inj 1999;13:505-20. 7. Dikmen S, McLean A Jr, Temkin NR, Wyler AR. Neuropsychologic outcome at one-month postinjury. Arch Phys Med Rehabil 1986;67:507-13. 8. Pastorek NJ, Hannay HJ, Contant CS. Prediction of global outcome with acute neuropsychological testing following closedhead injury. J Int Neuropsychol Soc 2004;10:807-17. 9. Stuss DT, Binns MA, Carruth FG, et al. The acute period of recovery from traumatic brain injury: posttraumatic amnesia or posttraumatic confusional state? J Neurosurg 1999;90:635-43. 10. Nakase-Thompson R, Sherer M, Yablon SA, Nick TG, Trzepacz PT. Acute confusion following traumatic brain injury. Brain Inj 2004;18:131-42. 11. Gordon WA, Mann N, Willer B. Demographic and social characteristics of the traumatic brain injury model system database. J Head Trauma Rehabil 1993;8(2):26-33. 12. Spreen O, Strauss E. A compendium of neuropsychological tests: administration, norms and commentary. 2nd ed. New York: Oxford Univ Pr; 1998. 13. Lezak MD. Neuropsychological assessment. 3rd ed. New York: Oxford Univ Pr; 1995. 14. Heaton RK, Miller W, Taylor MJ, Grant I. Revised comprehensive norms for an expanded Halstead-Reitan Battery: demographically adjusted neuropsychological norms for African American and Caucasian adults. Odessa: Psychological Assessment Resources; 2004. 15. Delis DC, Dramer JH, Kaplan E, Ober BA. California Verbal Learning Test. 2nd ed. Adult version manual. San Antonio: Psychological Corp; 2000. 16. Smith A. Symbol digit modalities test manual. Los Angeles: Western Psychological Services; 1973. 17. Wechsler Test of adult reading manual. San Antonio: Psychological Corp; 2001. 18. Kongs SK, Thompson LL, Iverson GL, Heaton RK. Wisconsin Card Sorting Test-64 Card Version professional manual. Odessa: Psychological Assessment Resources; 2000. 19. Novack TA, Dowler RN, Bush BA, Glen T, Schneider JJ. Validity of the Orientation Log, relative to the Galveston Orientation and Amnesia Test. J Head Trauma Rehabil 2000;15:957-61. 20. Jackson WT, Novack TA, Dowler RN. Effective serial measurement of cognitive orientation in rehabilitation: the Orientation Log. Arch Phys Med Rehabil 1998;79:718-20. 21. Reitan RM, Wolfson D. The Halstead-Reitan neuropsychological test battery: theory and clinical interpretation. 2nd ed. Tucson: Neuropsychological Pr; 1993. 22. Lafayette Instrument. Lafayette: Lafayette Instrument; 1989. 23. Gladsjo JA, Schuman CC, Evans JD, Peavy GM, Miller SW, Heaton RK. Norms for letter and category fluency: demographic corrections for age, education, and ethnicity. Assessment 1999;6: 147-78. Supplier a. Systat 8.0; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.

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