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Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19
Neuropsychological recovery in patients with moderate to severe head injury: 2 year follow-up S. Dikmen McLean a
a b c
a
, J. Machamer , N. Temkin
b d
& A.
a
Departments of Rehabilitation Medicine , Seattle
b
Neurological Surgery , Psychiatry&Behavioral Sciences , c
Biostatistics , Seattle
d
University of Washington , Seattle Published online: 04 Jan 2008.
To cite this article: S. Dikmen , J. Machamer , N. Temkin & A. McLean (1990) Neuropsychological recovery in patients with moderate to severe head injury: 2 year follow-up, Journal of Clinical and Experimental Neuropsychology, 12:4, 507-519, DOI: 10.1080/01688639008400997 To link to this article: http://dx.doi.org/10.1080/01688639008400997
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Journal of Clinical and Experimental Neuropsychology 1990,Vol. 12, NO.4, pp. 507-519
0168-8634/90/1204-0507$3.00 0 Swets & Zeitlinger
Neuropsychological Recovery in Patients With Moderate To Severe Head Injury: 2 Year Follow-up* S. D i I ~ n e n ' * ~J.g ~Machamer', ,
N. Temkin2s4, and A. McLeanl
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Departments of Rehabilitation Medicine', Neurological Surgery', Psychiatry & Behavioral Sciences3, and Bio~tatistics~ University of Washington, Seattle.
ABSTRACT Neuropsychological outcome and recovery of a group of 31 consecutive adult patients with moderate to severe head injuries were prospectively investigated over a 2-year period. A friend control group was used for comparison purposes. Based on the results we conclude: (1) there is marked impairment of a broad spectrum of neuropsychological functions at 1,12, and 24 months postinjury; (2) coma length is significantly related to neuropsychological status at all three time periods, although the relationship is weaker at 12 and 24 months; (3) marked improvement in all functions occurs in the first year, while recovery in the second year appears more specific and may depend on the seventy of the injury and type of function: (4) practice effects and variability over repeated measures cause difficulties in determining recovery and need to be addressed with larger samples.
Accurate and quantitative information about the natural history of recovery from head injury and factors that influence recovery is needed. Such information could yield insights regarding mechanisms of recovery, provide a baseline against which the effectiveness of various interventions could be assessed, and thus allow formulation of rational treatment strategies to speed up recovery and/ or reduce disabilities. Prognostic information could also help early identification of patients at risk who need treatment, and aid patients and their families in the formulation of future plans.
*
This study was supported by Grant No. GO0800076 from the National Institute of Disability and Rehabilitation Research and Grant No. HS04146 and HS05304 from the National Center for Health Services Research Office of the Assistant Secretary for Health. Requests for reprints should be sent to Sureyya Dikmen, Ph.D., Rehabilitation Medicine, RJ-30, University of Washington, Seattle, WA 98195, USA. Accepted for publication: August 1 , 1989.
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Most studies have reported cognitive outcome based on single observation at some point in time after head injury. Fewer studies have reported recovery data using the same sample with repeated observations (Conkey, 1938; Dikmen & Reitan, 1976; Dikmen, Reitan, & Temkin, 1983; Drudge, Williams, Kessler, & Gomes, 1984; Gronwall, 1976,1977; Gronwall & Wrightson, 1974; Lezak, 1979; Mandleberg, 1975, 1976; Mandleberg & Brooks, 1975; Parker & Serrats, 1976; Tabaddor, Mattis, & Zazula, 1984). There are no reported recovery studies that have used prospective, cross-sectional design where different but comparable patient samples are studied at various time frames after head injury. The reasons for the very limited recovery studies are due to the considerable effort required and the many problems encountered in conducting them and interpreting their results. For a discussion of these issues, refer to Dikmen and Temkin (1987) and Brooks (1987). Generally speaking, the outcome studies have indicated that neuropsychological deficits occur as a function of head injury. Their presence and severity depend on the severity of the head injury and/or type of task (e.g., Alexandre, Colombo, Nertempi, & Benedetti. 1983; Bennett-Levy, 1984; Brooks, Aughton, Bond, Jones, & Rizvi, 1980; Dikmen, McLean, Temkin, & Wyler, 1986; Dikmen, Temkin, McLean, Wyler, & Machamer, 1987; Klave & Cleeland, 1972; Levin, Grossman, Rose, & Teasdale, 1979; Mandleberg, 1976). However, multiple differences between such studies have not allowed for systematic accumulation of information that is generalizable or sufficiently specific to be applicable to individual cases. Furthermore, very few studies have reported outcome past 1 year of injury. Although outcome studies are relevant to questions of recovery, they do not answer questions related to change over time. Most of the early information regarding recovery came from the studies by Jennett and his collaborators from Glasgow based on patients with severe head injuries. These studies indicated that recovery occurs, and is characterized by, rapid early improvement which slows down and levels off in most patients by 6 months (Jennett, Snoek, Bond, & Brooks, 1981; Jennett & Teasdale, 1981). These studies used the Glasgow Outcome Scale to measure outcome and change in outcome across time. Because the Glasgow Outcome Scale is a global measure, it may not have been sufficiently sensitive to subtle changes after 3 to 6 months. The results of neuropsychological studies and clinical observations are in general agreement with the conclusions, drawn from the Glasgow studies, of early rapid change followed by a decelerated rate of improvement. In milder injuries, this pattern has been reported by Gronwall and her collaborators over the first 1 to 2 months post injury (Gronwall, 1976,1977; Gronwall & Wrightson, 1974). The Wechsler Adult Intelligence Scale results reported by Mandleberg (1976) and Mandleberg and Brooks (1975) are in support of the same contention in more severe cases. However, based on the available literature, including the results of our own study (Dikmen et al., 1983), we concluded that there are no firm results as to when recovery slows down or stops and how recovery time varies as a function of head injury severity. In our previous study, we examined
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recovery of neuropsychological functions in 27 adults with mild to severe head injuries examined initially, and then at 12 and 18 months post injury. The purpose o f t h e present study is to report neuropsychological results of a group of patients with moderate to severe head injury at 1, 12, and 24 months post injury, and t o examine recovery of function over this time period.
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METHOD Subjects Head-injured. The 31 subjects for this study represent part of the sample of 102 consecutive head-injured patients studied by us and reported elsewhere (Dikmen et al., 1986; McLean, Dikmen, Temkin, Wyler, & Gale, 1984). The selection criteria for these 31 consecutively hospitalized patients included: (1) Glasgow Coma Scale score (Teasdale & Jennett, 1974) of 3 to 8 within 24 hours of injury and/or at least 2 weeks of PTA (Russell & Smith, 1961) and/or time to following commands > 24 hrs; (2) survival for at least 1 month; (3) availability for 1-, 12-, and 24-month neuropsychological assessments; (4) no history of neurological disease, mental retardation, psychiatric disorder or alcoholism; (5) age range between 15 and 60 years; (6) English-speaking; and (7) willingness to participate in the study. Of the 46 eligible patients fulfilling the above criteria, including having participated in the 1- and 12-month examinations, 31 subjects completed the 2-year follow-up. No significant differences between the groups (31 subjects who completed the 24-month exam vs 15 who were lost to follow-up) were found on demographic information and on neuropsychological measures performed at 1 and 12 months postinjury. The majority of subjects in the study were young, single men with a high-school education (see Table 1). Motor vehicle accidents were the cause of the injury in 27 cases, falls accounted for 2, and injury by falling objects for 2 others.
Table 1. Demographic characteristics VARIABLES
Head-injured
Controls
Mean Age (yr) Mean Education (yr)
24.16 11.74
24.52 12.39
Sex Male Female
20 11
65 37
Race White Non-White
30 1
99 3
19 4 4 3
73 21 6 2 0
Marital Status Single Married Divorced Separated Widowed
1
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Subjects were administered a battery of neuropsychological tests 1, 12, and 24 months postinjury. Considerable effort was made to test the subjects as close to those time periods as possible. At 1 month postinjury, 84% (including 9 subjects who were neurologically too impaired to be tested) were scheduled within 1 week of their projected test dates (range 23 to 42 days). At the 1-year test session, 90% of the head-injured were assessed within 2 weeks of their I-year projected date (range: I1 months, 17 days to 13 months, 23 days). Two years postinjury, 93% of the subjects returned within 2 months of their due dates (range: 23 months, 7 days to 27 months, 1 day).
Comparison Group. This group consisted of 102 noninjured subjects selected from friends of the head-injured. There were more comparison subjects than head-injured because the controls were selected to match the entire head-injured group mentioned above @&men et al.. 1986. McLean et al., 1984). The comparison group was chosen by methods suggested by Pocock and Simon (1975) and Taves (1974). The head-injured subjects provided names of friends similar to themselves in age, education, and background. The rationale was that people usually have friends who are similar to themselves on potentially important cognitive and psychosocial characteristics not easily assessed and matched between groups. As in the head-injured sample. those with a history of alcoholism, psychiatric disorder, mental retardation, or neurological disease were excluded. Subjects that best matched the head-injured on age, sex, education, and race were chosen for the study. The majority of the comparison subjects were young, white, unmarried men with a high-school education. The demographic characteristics of the comparison group are summarized in Table 1. Comparison subjects were tested on the same battery of neuropsychological measures at the time of recruitment into the study and 11 months later. Eighty-eight of the 102 comparison subjects returned for the follow-up assessment.
Measures
Neurological Severity; Time from injury to consistently following commands (TFC) was used as an index of length of coma. TFC was operationally defined as a consistent score of 6 on the motor component of the Glasgow Coma Scale. Neuropsychological Measures: All subjects were assessed with ill? expanded HalsteadReitan Neuropsychological Test Battery. The measures administered included the Finger Tapping Test with the dominant and nondominant hand (Tapping-D and ND); Seashore Rhythm Test (Rhythm); the Wechsler Memory Scale Logical Memory subtest (WMSLM), Visual Reproduction subtest ( W S - V R ) , the Memory Quotient (MQ); the Selective Reminding Test (Buschke. 1973), the sum of Recall score (SR-RCL), the sum of Consistent Long Term Recall score (SR-CLTR); the Tactual Performance Test, Total time (TPTT), Memory (TPT-M), and Localization score (TPT-L); and the Wechsler Adult Intelligence Scale, Verbal (VIQ), Performance (PIQ), and Full Scale (FSIQ) IQ scores. A higher score represents better performance on the tests listed above, with the exception of TPT-T time. The Speech-Sounds Perception Test (Speech Sounds), the Trail Making Test (Trails A and B), the Category Test (Category), and the Stroop Test (Stroop Part 1 and Part 2; Dyer, 1973; & Stroop, 1933, were also administered. A lower score on these measures represents better performance. The Impairment Index (11) is a composite score that is based on the number of Halstead’s tests that are in the impaired range. A low score on this measure represents better performance. For a more complete description of the tests in the Halstead-Reitan battery, see Reitan and Wolfson, 1985.
Data Analysis The first set of analyses were performed to determine neuropsychological impairment at 1 . 12, and 24 months postinjury. Wilcoxon Rank Sum tests compared head-injured and
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comparison group performance on neuropsychological test scores at each time period. Two reasons led to the choice of a distribution-free test. First, a substantial fraction of the head-injured patients were untestable at 1 month due to the seventy of their head injury. The distribution-free procedure only assumes that these patients scored most poorly (i.e., more poorly than the worst score observed among the patients actually tested) and does not assign them an actual numeric value. Second, with skewed or long-tailed distributions such as we have, distribution-free procedures are actually more powerful in detecting a difference than the more common parametric t-test or analysis of variance. This is because they are less affected by the variability within the group caused by a skewed or long-tailed distribution. Head-injured subject data obtained at 1 month and at 12 months postinjury were compared with initial control test scores. Test scores obtained 24 months postinjury in the head-injured group were compared with control data obtained at follow-up, 11 months after initial testing. These comparisons were chosen in order to more closely equate practice effects between the groups. The benefit of practice for the head-injured from the 1-month evaluation was considered to be low because many subjects (9/31) were neurologically too impaired to receive 1-month testing and those who were tested at 1 month were probably unable to benefit fully from the previous exposure to the tests because of initial poor functioning. When using repeated testing, there is no perfect solution to the problem of practice effects. Comparison of the 12-month testing of the head-injured with the first testing of the controls is conservative and would lead to a potential underestimation of a deficit due to practice effects. In contrast, comparison of the 12-month testing of the head-injured with the follow-up evaluation of the controls would lead to overestimation of a deficit due to probable differential practice effects in the controls as described above. Since the sample of this study consisted of severely injured patients and we were unlikely to overlook a deficit, we selected the first alternative. Head-injured subjects who were neurologically too impaired to be tested 1 month after injury were assigned a worse score than the worst observed score for that time. A significance level of .01 was accepted as evidence of neuropsychological deficit in the head injury group at each of the three time periods. The second set of analyses were performed to determine if the degree of neuropsychological impairment at 1. 12, and 24 months postinjury was related to head injury severity, as defined by TFC. Head-injured subjects were divided into three TFC groups: those with TFC 2 7 days ( n = 12). 25 hours to 6 days ( n = 7), and < 24 hours ( n = 12). Kruskal-Wallis nonparametric analysis of variance compared the head injury groups with the control data. As in the previous analyses, the 1- and 12- month results of the headinjured patients were compared to the first testing of the controls and 24-month testing of the head-injured to the follow-up examination of the controls. The untestables, as before, were assigned a worse than the worst observed score. Significant results were subjected to subgroup comparisons using Tukey’s method adapted for and applied to the ranks (Marascuilo & McSweeney, 1977). The third set of analyses examined the change in neuropsychological test performance in the head-injured group up to 2 years postinjury on a short list of neuropsychological measures. Two methods were used to examine change. First, practice effects were ignored, and change from 1 month to 1 year and 1 year to 2 years were tested in the headinjured using Wilcoxon Signed Rank Tests. This method overestimates recovery by not adjusting for potential practice effects. Second, the change from 1 month to 1 year, 1 year to 2 years, and 1 month to 2 years in the head-injured were compared with the test-retest values of the controls. Wilcoxon Rank Sum Tests were used for these comparisons. It is possible that these comparisons underestimate recovery due to lessened ability of the head-injured to benefit from practice in the first year, and perhaps decreased gains from practice effects with further exposure in the second year.
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RESULTS The results of the Wilcoxon Rank Sum Tests comparing the control and headinjured groups I, 12, and 24 months postinjury are summarized in Table 2. The groups differed significantly (p x.01) on almost all neuropsychologicalmeasures at each time period. Kruskal-Wallis nonparametric analyses between the control group and the three TFC groups demonstrated significant differences on most measures at all
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Table 2. Median Scores On Neuropsychological Measures HEAD-INJURED Measures Motor functions Tapping-D Tapping-ND Attention, Concentration Flexibility & Quickness Speech Sounds Rhythm Trails A Trails B Stroop, Part 1 Stroop, Part 2 Memory
WMS-LM WMS-VR SR-RCL SR-CLTR TPT-M TPT-L Verbal VIQ Performance Skills PIQ TPT-T Reasoning Category Overall I1 FSIQ MQ
1' month
12' months
CONTROLS
24b months
39** 36**
45** 42**
47**
11**
6** 26* 30** 66* 50** 119** 9.5 12 80**
51 46
52 50
3 26* 26** 66** 48** 101**
4 28 19 39 91
3 28 19 45 39 85
7** 3**
lo** 12 83** 66** 7** 3**
12 13 90 83 8 5
13 12 90 83 9 6
80**
97**
101**
112
112
74** 1.24**
99** .48**
106** .47**
112 .35
119 .29
108**
25
21**
23
13
1.o** 70**
.4**
.3** 104**
.1 112 118
.1
22** 64** 140** 76** 254** 6** 8** 45** 2** 4* * 1**
78**
SO**
loo** 106**
45**
104**
a. 1 and 12 month Head-injured compared with 1 month Controls b. 24 month Head-injured compared with 12 month Controls
** p < .001 * p < .01
1 month 12 months
48
115 118
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time periods as a function of severity of head injury. Significant Kruskal-Wallis analyses were subjected to distribution-free analogues of Tukey post-hw comparisons to determine which groups were different from one another. A significance level of p < .01 was accepted. Table 3 summarizes the number of tests significantly different and the number of tests with medians lower than controls (regardless of statistical significance) for the three severity groups at the three time periods on 21 neuropsychological measures used. The most severe TFC group ( 2 7 days) was significantly different from the control group on most measures at all times. The next most severe TFC group (25 hours - 6 days) was significantly impaired on one-half of the measures at 1 month as compared to controls. At 1 year post injury, only I1 was significantly different from controls. By 2 years postinjury, there were no significant differences between the head-injured group with TFC between 25 hours to 6 days and controls. The least severe TFC group’s ( 5 24 hours) median scores were consistently better than the two more severely injured groups and were slightly worse than controls. This group was significantly impaired on only a few variables, including the overall measures of 11, IQ, and measures of speed and distractibility at 1 month. There was only one significant difference at 1 year and no significant differences at 2 years postinjury. Because of the small sample size of each subgroup and the variability within them, lack of statistically reliable results pertaining to the impairment in the two less severe groups probably reflect the lack of power of the study as much as the actual state of functioning of the patients. Table 3 indicates that the medians of all the head-injured subgroups were consistently, although not significantly, lower than those of controls on the majority of the 21 neuropsychological measures utilized. The results do indicate that there is a clear ordering effect of performance by severity. However, all of the subgroups seem to show head injury effects over the 2-year time period. The results of the Wilcoxon Signed Rank Tests comparing head-injured group performance at 1 month with performance at 1 year and at 2 years demonstrated significant change from 1 month to 1 year and 1 month to 2 years on all neuro-
Table 3. Number (Out of the 21 NeuropsychologicalTests) Where the Head Injury Severity Sub-Group Medians Were Poorer Than, or Significantly Different from, the
Control Group 1 Month
TFC 5 1 day
25 hours - 6 days 7 + days
poorer significant 21 21 21
24 Months
12 Months
6 11 21
poorer significant 17 21 21
1 1
17
poorer significant 16 19 21
0 0 18
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psychological measures. There were significant differences between 1-year and 2-year head-injured test data on some measures (Tapping-D, Tapping-ND, Speech Sounds, VIQ, PIQ, Category). Wilcoxon Rank Sum tests revealed that the change scores in the head-injured group from 1 month to 1 year and from 1 month to 2 years were significantly different from the change in the test-retest values of the comparison group on almost all neuropsychological measures. However, when the change in the comparison group was contrasted with the change in the head-injured group from 1 to 2 years postinjury, only Speech Sounds and VIQ showed significant differences between the groups. In order to examine recovery further, change as a function of head injury severity and abilities assessed was examined by descriptive plotting of the data. Figure l a and l b show sample performances of the three severity subgroups on Trails B and Rhythm. The results indicate that improvement occurred during the first year for each of the subgroups on both measures. Change in the second year is more complicated. The results are suggestive of no change on Rhythm, irrespective of severity of head injury, and continued improvement for patients with TFC 1 7 days on Trails B. To explore how variability of performance over repeated measures may have contributed to difficulties in demonstrating recovery, the performances of the
l b . Rhythm
l a . Trails B 300
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u
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c. 40
1-
Ot
,
1 Month
1
1 2 Month 2 4 Month
A
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I
1 Month 1 2 Monln 2 4 Month
Figure 1. Recovery as a function of head injury severity and type of task.
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2a. W A l S
- VlQ
r
2b. SR 100
r
I20
80
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100
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L 1 Month
0' I
1
12 Monlh 24 Month
-
r
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1
1 Month 12 Month 2 4 Month
Figure 2. Recovery curves for individual patients.
individual subjects were plotted over three repeated administrations on VIQ and SR-CLTR. As reported earlier, recovery was concluded on VIQ and not on SRCLTR, a memory measure. As Figure 2 indicates, changes appear to be much more consjstent on VIQ than on SR-CLTR.
DISCUSSION The present study provides convincing evidence of (a) persistent cognitive difficulties in patients with moderate to severe head injuries over a 2-year period, (b) of significant association between coma length and cognitive functioning, and (c) marked improvement in the first year postinjury. Recovery in the second year is modest and its determination is complicated by practical problems. Our finding of a significant relationship between cognitive functioning and coma length is consistent with our previous reports (Dikmen et al., 1986, 1987) but not with those of others (Alexandre et al., 1983; Brooks et al., 1980; and Levin et al., 1979). Although some differences in definition of coma length are a potential cause, other potential causes include differences in subject selection, head
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injury severity represented in the samples, and whether or not time from injury to testing was controlled. Marked improvement exceeding the change seen in controls occurred in headinjured patients on all neuropsychological measures within the first year post injury. During the second year, improvement occurred for the head-injured group, but on fewer measures, and reliably exceeded the change seen in the controls on only two measures (VIQ & Speech Sounds). The marked improvement in the first year is consistent with other reports in the literature (Dikmen et al., 1983; Drudge et al., 1984; Mandleberg, 1976; Parker & Serrats, 1976; Tabaddor et al., 1984). Although recovery in the first year appears clear-cut, the important question is: What can be concluded about recovery during the second year? Based on the statistical results, one possible conclusion is that recovery during the second year occurs but is very modest. A small change is always difficult to demonstrate in a statistical fashion. In this case, the demonstration is made more difficult by the heterogeneity among head-injured subjects, the likely overestimation of practice effects discussed more below, and the perhaps diminished statistical power obtained with the use of nonparametric tests. An alternative conclusion is that recovery during the second year occurs, but the picture is much more complicated: Recovery is more selective, complex, and varies with the type of function assessed and the severity of the injury, as illustrated in Figure l a and lb. Differential recovery rate as a function of type of ability has been also indicated by the results of other studies (Lezak, 1979; Mandleberg, 1976; Tabaddor et al., 1984). Two important factors or complications need to be discussed in relation to the recovery findings during the second year. One relates to whether or not the comparison subjects represented appropriate controls for practice effects, and the other relates to the variability in test-retest observed on certain measures and the implications of this variability for documenting recovery. The use of normal comparison subjects to control for practice in the headinjured assumes that the effect of practice on performance is equal in the two groups. This may not be accurate, as normal subjects with intact memory are likely to benefit more from prior exposure than do the patients with significant head injury. Therefore, the magnitude of recovery in the second year may have been underestimated due to overestimation of the magnitude of practice effects. In addition, the effect of practice in our study may have been overestimated in the head-injured group because the number of repeated assessments differed between the head-injured and control groups. Due to study limitations, we were only able to test the control subjects twice while the head-injured received three evaluations. When the change in the head-injured in the second year post injury was compared to the test-retest values in the control group, the control group had the benefit of the initial practice effect while the head-injured had multiple exposure to the tests. Although there is no literature available, clinical experience suggests that the magnitude of change as a result of practice is high initially and diminishes with additional exposure due to ceiling effects. Practice effects,
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and how to control them, is one of the enormous practical problems in conducting recovery studies and in interpreting results of individual clinical cases (Brooks, 1987; Dikmen & Temkin, 1987). The other complication that may cause difficulties in documenting recovery is test-retest variability, particularly on certain measures. The results of the current study and of a previous sample (Dikmen et al., 1983) indicate that there is substantial variability with repeated measurements, especially on certain tests. Variability in test-retest scores may be the result of unreliability of the measure or of the construct measured, or it may reflect true change (i.e., recovery or deterioration). An examination of individual recovery curves of VIQ and SRCLTR (Figure 2) indicates that the improvement in performance is modest for both measures but is more consistent for VIQ than for the SR-CLTR. As a result, the change in VIQ is statistically significant but that in SR-CLTR is not. It is not entirely clear why the fluctuations across time occur on individuals’ memory scores. It may be that the factors which contribute to subject unreliability are particularly important on memory tasks. For example, inattention on the Selective Reminding Test or the WMS can lower the patient’s score. A similar level of inattention on the WAIS is likely to lead to repetition of the question or the instructions. Unreliability of measures may be an especially pertinent problem in the head-injured population where factors such as fatigue and distractibility make the possibility of obtaining the subject’s best performance at one given time somewhat less likely. While the unreliability of head-injured patients is a suspected and clinically important phenomenon in its own right, it is unwanted error variance from the point of view of measuring recovery based on single observation. These results point out the need for measures with better psychometric properties when attempting to examine certain constructs and/or the use of repeated observations to arrive at a value more representative of the ability being measured in a given time frame. Although test-retest differences may reflect true change, they may also reflect the effects of unwanted factors and could lead to erroneous conclusions showing no improvement in recovery studies and improvement or deterioration in interpreting the results of individual cases. Research examining group performance with large samples can overcome the impact of a certain amount of variability. However, clinical evaluation of the individual case over time must always consider the possibility that variability in the data, especially on certain types of measures, reflects unreliability and not true change. The results of this project do not provide conclusive evidence for continued recovery or, for that matter, cessation of change in the second year post injury. There are indications that recovery continues, but the issues of practice effects and variability within the data must be first addressed with larger samples.
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REFERENCES Alexandre, A., Colombo, F., Nertempi, P., & Benedetti, A. (1983). Cognitive outcome and early indices of seventy of head injury. Journal of Neurosurgery, 59,751-761. Bennett-Levy, J.M. (1984). Long-term effects of severe closed head injury on memory: Evidence from a consecutive series of young adults. Acta Neurologica Scandinavica, 70,285-298. Brooks, D.N. (1987). Measuring neuropsychological and functional recovery. In H.S. Levin. J. Grafman, & H.M. Eisenberg (Eds.), Neurobehavioral recovery from head injury (pp. 57-72). New York Oxford University Press. Brooks, D.N.. Aughton, M.E., Bond, M.R., Jones, P., & Rizvi, S. (1980). Cognitive sequelae in relationship to early indices of severity of brain damage after severe blunt head injury. Journal of Neurology, Neurosurgery, and Psychiatry, 43,529-534. Buschke, H. (1973). Selective reminding for analysis of memory and learning. Journal of Verbal Learning and Verbal Behavior, 12,543-550. Conkey, R. C. (1938). Psychological changes associated with head injuries. Archives of Psychology, 32,l-62. Dikmen, S . , McLean, A., Temkin, N.R., & Wyler, A.R. (1986). Neuropsychologic outcome at 1-month post injury. Archives of Physical Medicine and Rehabilitation, 67, 507-5 13. Dikmen, S., & Reitan, R.M. (1976). Psychological deficits and recovery of functions after head injury. Transactions of the American Neurological Association, 101,72-17. Dikmen. S . , Reitan. R.M., & Temkin. N.R. (1983). Neuropsychological recovery in head injury. Archives of Neurology, 40,333-338. Dikmen, S., & Ternkin, N. (1987). Determination of the effects of head injury and recovery in behavioral research. In H.S. Levin, J. Grafman, & H.M.Eisenberg (Eds.), Neurobehavioral recovery from head injury (pp 73-87). New York Oxford University Press. Dikmen, S., Temkin, N.R., McLean, A., Wyler, A., & Machamer, J. (1987). Memory and head injury seventy. Journal of Neurology, Neurosurgery, and Psychiatry, SO, 16131618. Drudge, O.W., Williams, J.M., Kessler, M., & Gomes, F.B. (1984). Recovery from severe closed head injuries: Repeat testings with the Halstead-Reitan Neuropsychological Battery. Journal of Clinical Psychology, 40, 259-265. Dyer, F.N. (1973). Stroop phenomenon and its use in study of perceptual, cognitive, and response processes. Memory and Cognition, I , 106-120. Gronwall, D. (1976). Performance changes during recovery from closed head injury. Proceedings of the Australian Association of Neurologists, 13,143-141. Gronwall, D. (1977). Paced auditory serial-addition task: A measure of recovery from concussion. Perceptual and Motor Skills, 44, 367-373. Gronwall, D., & Wrightson, P. (1974). Delayed recovery of intellectual function after minor head injury. Lancet, 2, 605-609. Jennett, B., Snoek, J., Bond, M.R. & Brooks, N. (1981). Disability after severe head injury: Observations on the use of the Glasgow Outcome Scale. Journal of Neurology, Neurosurgery, and Psychiatry, 44,285-293. Jennett, B., & Teasdale, G. (1981). Management of head injuries. Philadelphia: F.A. Davis Co. Klove, H.,& Cleeland, C.S. (1972). The relationship of neuropsychological impairment to other indices of seventy of head injury. Scandinavian Journal of Rehabilitation Medicine, 4, 55-60. Levin, H.S., Grossman, R.G., Rose, J.E.,& Teasdale (1979). Long term neuropsychological outcome of closed head injury. Journal of Neurosurgery, SO, 412-422.
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Lezak, M.D. (1979). Recovery of memory and learning functions following traumatic brain injury. Cortex, 15, 63-72. Mandleberg, I.A. (1975). Cognitive recovery after severe head injury: 2. Wechsler Adult Intelligence Scale during post-traumatic amnesia. Journal of Neurology, Neurosurgery, and Psychiatry, 38,1127-1132. Mandleberg, I.A. (1976). Cognitive recovery after severe head injury: 3. WAIS verbal and performance IQs as a function of post-traumatic amnesia duration and time from injury. Journal of Neurology, Neurosurgery, and Psychiatry, 39, 1001-1007. Mandleberg, LA., & Brooks, D.N. (1975). Cognitive recovery after severe head injury 1. Serial testing on the Wechsler Adult Intelligence Scale. Journal of Neurology, Neurosurgery, and Psychiatry, 38, 1121-1126. Marascuilo, LA., & McSweeney, M. (1977). Nonpararnetric and distribution-free methods for social sciences. Monterey, CA: BrookslCole. McLean, A., Dikmen, S., Temkin, N., Wyler, A.R., & Gale, J.L. (1984). Psychosocial functioning at 1 month after head injury. Neurosurgery, 14, 393-399. Parker, S.A., & Serrats, A.F. (1976). Memory recovery after traumatic coma. Acta Neurochirurgica, 34, 71-77. Pocock, S.J., & Simon, R. (1975). Sequential treatment assignment with balancing for prognostic factors in controlled clinical trial. Biornetrics, 31, 103-1 15. Reitan, R.M., & Wolfson, D.(1985). The Halstead-Reitan Neuropsychological Test Battery: Theory and clinical interpretation. Tucson: Neuropsychology Press. Russell, W.R., & Smith, A. (1961). Post-traumatic amnesia in closed head injury. Archives of Neurology, 5,4-17. Stroop, J.R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18,643-662. Tabaddor, K., Mattis. S., & Zazula, T. (1984). Cognitive sequelae and recovery course after moderate and severe head injury. Neurosurgery, 1 4 , 701-708. Taves, D.R. (1974). Minimization: New method of assigning patients to treatment and control groups. Clinical Pharmacology and Therapeutics, 15,443-453. Teasdale, G., & Jennett, B. (1974). Assessment of coma and impaired consciousness: A practical scale. Lancet, 2, 8 1-84.
Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19
Neuropsychological recovery in patients with moderate to severe head injury: 2 year follow-up S. Dikmen McLean a
a b c
a
, J. Machamer , N. Temkin
b d
& A.
a
Departments of Rehabilitation Medicine , Seattle
b
Neurological Surgery , Psychiatry&Behavioral Sciences , c
Biostatistics , Seattle
d
University of Washington , Seattle Published online: 04 Jan 2008.
To cite this article: S. Dikmen , J. Machamer , N. Temkin & A. McLean (1990) Neuropsychological recovery in patients with moderate to severe head injury: 2 year follow-up, Journal of Clinical and Experimental Neuropsychology, 12:4, 507-519, DOI: 10.1080/01688639008400997 To link to this article: http://dx.doi.org/10.1080/01688639008400997
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Journal of Clinical and Experimental Neuropsychology 1990,Vol. 12, NO.4, pp. 507-519
0168-8634/90/1204-0507$3.00 0 Swets & Zeitlinger
Neuropsychological Recovery in Patients With Moderate To Severe Head Injury: 2 Year Follow-up* S. D i I ~ n e n ' * ~J.g ~Machamer', ,
N. Temkin2s4, and A. McLeanl
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Departments of Rehabilitation Medicine', Neurological Surgery', Psychiatry & Behavioral Sciences3, and Bio~tatistics~ University of Washington, Seattle.
ABSTRACT Neuropsychological outcome and recovery of a group of 31 consecutive adult patients with moderate to severe head injuries were prospectively investigated over a 2-year period. A friend control group was used for comparison purposes. Based on the results we conclude: (1) there is marked impairment of a broad spectrum of neuropsychological functions at 1,12, and 24 months postinjury; (2) coma length is significantly related to neuropsychological status at all three time periods, although the relationship is weaker at 12 and 24 months; (3) marked improvement in all functions occurs in the first year, while recovery in the second year appears more specific and may depend on the seventy of the injury and type of function: (4) practice effects and variability over repeated measures cause difficulties in determining recovery and need to be addressed with larger samples.
Accurate and quantitative information about the natural history of recovery from head injury and factors that influence recovery is needed. Such information could yield insights regarding mechanisms of recovery, provide a baseline against which the effectiveness of various interventions could be assessed, and thus allow formulation of rational treatment strategies to speed up recovery and/ or reduce disabilities. Prognostic information could also help early identification of patients at risk who need treatment, and aid patients and their families in the formulation of future plans.
*
This study was supported by Grant No. GO0800076 from the National Institute of Disability and Rehabilitation Research and Grant No. HS04146 and HS05304 from the National Center for Health Services Research Office of the Assistant Secretary for Health. Requests for reprints should be sent to Sureyya Dikmen, Ph.D., Rehabilitation Medicine, RJ-30, University of Washington, Seattle, WA 98195, USA. Accepted for publication: August 1 , 1989.
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Most studies have reported cognitive outcome based on single observation at some point in time after head injury. Fewer studies have reported recovery data using the same sample with repeated observations (Conkey, 1938; Dikmen & Reitan, 1976; Dikmen, Reitan, & Temkin, 1983; Drudge, Williams, Kessler, & Gomes, 1984; Gronwall, 1976,1977; Gronwall & Wrightson, 1974; Lezak, 1979; Mandleberg, 1975, 1976; Mandleberg & Brooks, 1975; Parker & Serrats, 1976; Tabaddor, Mattis, & Zazula, 1984). There are no reported recovery studies that have used prospective, cross-sectional design where different but comparable patient samples are studied at various time frames after head injury. The reasons for the very limited recovery studies are due to the considerable effort required and the many problems encountered in conducting them and interpreting their results. For a discussion of these issues, refer to Dikmen and Temkin (1987) and Brooks (1987). Generally speaking, the outcome studies have indicated that neuropsychological deficits occur as a function of head injury. Their presence and severity depend on the severity of the head injury and/or type of task (e.g., Alexandre, Colombo, Nertempi, & Benedetti. 1983; Bennett-Levy, 1984; Brooks, Aughton, Bond, Jones, & Rizvi, 1980; Dikmen, McLean, Temkin, & Wyler, 1986; Dikmen, Temkin, McLean, Wyler, & Machamer, 1987; Klave & Cleeland, 1972; Levin, Grossman, Rose, & Teasdale, 1979; Mandleberg, 1976). However, multiple differences between such studies have not allowed for systematic accumulation of information that is generalizable or sufficiently specific to be applicable to individual cases. Furthermore, very few studies have reported outcome past 1 year of injury. Although outcome studies are relevant to questions of recovery, they do not answer questions related to change over time. Most of the early information regarding recovery came from the studies by Jennett and his collaborators from Glasgow based on patients with severe head injuries. These studies indicated that recovery occurs, and is characterized by, rapid early improvement which slows down and levels off in most patients by 6 months (Jennett, Snoek, Bond, & Brooks, 1981; Jennett & Teasdale, 1981). These studies used the Glasgow Outcome Scale to measure outcome and change in outcome across time. Because the Glasgow Outcome Scale is a global measure, it may not have been sufficiently sensitive to subtle changes after 3 to 6 months. The results of neuropsychological studies and clinical observations are in general agreement with the conclusions, drawn from the Glasgow studies, of early rapid change followed by a decelerated rate of improvement. In milder injuries, this pattern has been reported by Gronwall and her collaborators over the first 1 to 2 months post injury (Gronwall, 1976,1977; Gronwall & Wrightson, 1974). The Wechsler Adult Intelligence Scale results reported by Mandleberg (1976) and Mandleberg and Brooks (1975) are in support of the same contention in more severe cases. However, based on the available literature, including the results of our own study (Dikmen et al., 1983), we concluded that there are no firm results as to when recovery slows down or stops and how recovery time varies as a function of head injury severity. In our previous study, we examined
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recovery of neuropsychological functions in 27 adults with mild to severe head injuries examined initially, and then at 12 and 18 months post injury. The purpose o f t h e present study is to report neuropsychological results of a group of patients with moderate to severe head injury at 1, 12, and 24 months post injury, and t o examine recovery of function over this time period.
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METHOD Subjects Head-injured. The 31 subjects for this study represent part of the sample of 102 consecutive head-injured patients studied by us and reported elsewhere (Dikmen et al., 1986; McLean, Dikmen, Temkin, Wyler, & Gale, 1984). The selection criteria for these 31 consecutively hospitalized patients included: (1) Glasgow Coma Scale score (Teasdale & Jennett, 1974) of 3 to 8 within 24 hours of injury and/or at least 2 weeks of PTA (Russell & Smith, 1961) and/or time to following commands > 24 hrs; (2) survival for at least 1 month; (3) availability for 1-, 12-, and 24-month neuropsychological assessments; (4) no history of neurological disease, mental retardation, psychiatric disorder or alcoholism; (5) age range between 15 and 60 years; (6) English-speaking; and (7) willingness to participate in the study. Of the 46 eligible patients fulfilling the above criteria, including having participated in the 1- and 12-month examinations, 31 subjects completed the 2-year follow-up. No significant differences between the groups (31 subjects who completed the 24-month exam vs 15 who were lost to follow-up) were found on demographic information and on neuropsychological measures performed at 1 and 12 months postinjury. The majority of subjects in the study were young, single men with a high-school education (see Table 1). Motor vehicle accidents were the cause of the injury in 27 cases, falls accounted for 2, and injury by falling objects for 2 others.
Table 1. Demographic characteristics VARIABLES
Head-injured
Controls
Mean Age (yr) Mean Education (yr)
24.16 11.74
24.52 12.39
Sex Male Female
20 11
65 37
Race White Non-White
30 1
99 3
19 4 4 3
73 21 6 2 0
Marital Status Single Married Divorced Separated Widowed
1
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Subjects were administered a battery of neuropsychological tests 1, 12, and 24 months postinjury. Considerable effort was made to test the subjects as close to those time periods as possible. At 1 month postinjury, 84% (including 9 subjects who were neurologically too impaired to be tested) were scheduled within 1 week of their projected test dates (range 23 to 42 days). At the 1-year test session, 90% of the head-injured were assessed within 2 weeks of their I-year projected date (range: I1 months, 17 days to 13 months, 23 days). Two years postinjury, 93% of the subjects returned within 2 months of their due dates (range: 23 months, 7 days to 27 months, 1 day).
Comparison Group. This group consisted of 102 noninjured subjects selected from friends of the head-injured. There were more comparison subjects than head-injured because the controls were selected to match the entire head-injured group mentioned above @&men et al.. 1986. McLean et al., 1984). The comparison group was chosen by methods suggested by Pocock and Simon (1975) and Taves (1974). The head-injured subjects provided names of friends similar to themselves in age, education, and background. The rationale was that people usually have friends who are similar to themselves on potentially important cognitive and psychosocial characteristics not easily assessed and matched between groups. As in the head-injured sample. those with a history of alcoholism, psychiatric disorder, mental retardation, or neurological disease were excluded. Subjects that best matched the head-injured on age, sex, education, and race were chosen for the study. The majority of the comparison subjects were young, white, unmarried men with a high-school education. The demographic characteristics of the comparison group are summarized in Table 1. Comparison subjects were tested on the same battery of neuropsychological measures at the time of recruitment into the study and 11 months later. Eighty-eight of the 102 comparison subjects returned for the follow-up assessment.
Measures
Neurological Severity; Time from injury to consistently following commands (TFC) was used as an index of length of coma. TFC was operationally defined as a consistent score of 6 on the motor component of the Glasgow Coma Scale. Neuropsychological Measures: All subjects were assessed with ill? expanded HalsteadReitan Neuropsychological Test Battery. The measures administered included the Finger Tapping Test with the dominant and nondominant hand (Tapping-D and ND); Seashore Rhythm Test (Rhythm); the Wechsler Memory Scale Logical Memory subtest (WMSLM), Visual Reproduction subtest ( W S - V R ) , the Memory Quotient (MQ); the Selective Reminding Test (Buschke. 1973), the sum of Recall score (SR-RCL), the sum of Consistent Long Term Recall score (SR-CLTR); the Tactual Performance Test, Total time (TPTT), Memory (TPT-M), and Localization score (TPT-L); and the Wechsler Adult Intelligence Scale, Verbal (VIQ), Performance (PIQ), and Full Scale (FSIQ) IQ scores. A higher score represents better performance on the tests listed above, with the exception of TPT-T time. The Speech-Sounds Perception Test (Speech Sounds), the Trail Making Test (Trails A and B), the Category Test (Category), and the Stroop Test (Stroop Part 1 and Part 2; Dyer, 1973; & Stroop, 1933, were also administered. A lower score on these measures represents better performance. The Impairment Index (11) is a composite score that is based on the number of Halstead’s tests that are in the impaired range. A low score on this measure represents better performance. For a more complete description of the tests in the Halstead-Reitan battery, see Reitan and Wolfson, 1985.
Data Analysis The first set of analyses were performed to determine neuropsychological impairment at 1 . 12, and 24 months postinjury. Wilcoxon Rank Sum tests compared head-injured and
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comparison group performance on neuropsychological test scores at each time period. Two reasons led to the choice of a distribution-free test. First, a substantial fraction of the head-injured patients were untestable at 1 month due to the seventy of their head injury. The distribution-free procedure only assumes that these patients scored most poorly (i.e., more poorly than the worst score observed among the patients actually tested) and does not assign them an actual numeric value. Second, with skewed or long-tailed distributions such as we have, distribution-free procedures are actually more powerful in detecting a difference than the more common parametric t-test or analysis of variance. This is because they are less affected by the variability within the group caused by a skewed or long-tailed distribution. Head-injured subject data obtained at 1 month and at 12 months postinjury were compared with initial control test scores. Test scores obtained 24 months postinjury in the head-injured group were compared with control data obtained at follow-up, 11 months after initial testing. These comparisons were chosen in order to more closely equate practice effects between the groups. The benefit of practice for the head-injured from the 1-month evaluation was considered to be low because many subjects (9/31) were neurologically too impaired to receive 1-month testing and those who were tested at 1 month were probably unable to benefit fully from the previous exposure to the tests because of initial poor functioning. When using repeated testing, there is no perfect solution to the problem of practice effects. Comparison of the 12-month testing of the head-injured with the first testing of the controls is conservative and would lead to a potential underestimation of a deficit due to practice effects. In contrast, comparison of the 12-month testing of the head-injured with the follow-up evaluation of the controls would lead to overestimation of a deficit due to probable differential practice effects in the controls as described above. Since the sample of this study consisted of severely injured patients and we were unlikely to overlook a deficit, we selected the first alternative. Head-injured subjects who were neurologically too impaired to be tested 1 month after injury were assigned a worse score than the worst observed score for that time. A significance level of .01 was accepted as evidence of neuropsychological deficit in the head injury group at each of the three time periods. The second set of analyses were performed to determine if the degree of neuropsychological impairment at 1. 12, and 24 months postinjury was related to head injury severity, as defined by TFC. Head-injured subjects were divided into three TFC groups: those with TFC 2 7 days ( n = 12). 25 hours to 6 days ( n = 7), and < 24 hours ( n = 12). Kruskal-Wallis nonparametric analysis of variance compared the head injury groups with the control data. As in the previous analyses, the 1- and 12- month results of the headinjured patients were compared to the first testing of the controls and 24-month testing of the head-injured to the follow-up examination of the controls. The untestables, as before, were assigned a worse than the worst observed score. Significant results were subjected to subgroup comparisons using Tukey’s method adapted for and applied to the ranks (Marascuilo & McSweeney, 1977). The third set of analyses examined the change in neuropsychological test performance in the head-injured group up to 2 years postinjury on a short list of neuropsychological measures. Two methods were used to examine change. First, practice effects were ignored, and change from 1 month to 1 year and 1 year to 2 years were tested in the headinjured using Wilcoxon Signed Rank Tests. This method overestimates recovery by not adjusting for potential practice effects. Second, the change from 1 month to 1 year, 1 year to 2 years, and 1 month to 2 years in the head-injured were compared with the test-retest values of the controls. Wilcoxon Rank Sum Tests were used for these comparisons. It is possible that these comparisons underestimate recovery due to lessened ability of the head-injured to benefit from practice in the first year, and perhaps decreased gains from practice effects with further exposure in the second year.
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RESULTS The results of the Wilcoxon Rank Sum Tests comparing the control and headinjured groups I, 12, and 24 months postinjury are summarized in Table 2. The groups differed significantly (p x.01) on almost all neuropsychologicalmeasures at each time period. Kruskal-Wallis nonparametric analyses between the control group and the three TFC groups demonstrated significant differences on most measures at all
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Table 2. Median Scores On Neuropsychological Measures HEAD-INJURED Measures Motor functions Tapping-D Tapping-ND Attention, Concentration Flexibility & Quickness Speech Sounds Rhythm Trails A Trails B Stroop, Part 1 Stroop, Part 2 Memory
WMS-LM WMS-VR SR-RCL SR-CLTR TPT-M TPT-L Verbal VIQ Performance Skills PIQ TPT-T Reasoning Category Overall I1 FSIQ MQ
1' month
12' months
CONTROLS
24b months
39** 36**
45** 42**
47**
11**
6** 26* 30** 66* 50** 119** 9.5 12 80**
51 46
52 50
3 26* 26** 66** 48** 101**
4 28 19 39 91
3 28 19 45 39 85
7** 3**
lo** 12 83** 66** 7** 3**
12 13 90 83 8 5
13 12 90 83 9 6
80**
97**
101**
112
112
74** 1.24**
99** .48**
106** .47**
112 .35
119 .29
108**
25
21**
23
13
1.o** 70**
.4**
.3** 104**
.1 112 118
.1
22** 64** 140** 76** 254** 6** 8** 45** 2** 4* * 1**
78**
SO**
loo** 106**
45**
104**
a. 1 and 12 month Head-injured compared with 1 month Controls b. 24 month Head-injured compared with 12 month Controls
** p < .001 * p < .01
1 month 12 months
48
115 118
513
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time periods as a function of severity of head injury. Significant Kruskal-Wallis analyses were subjected to distribution-free analogues of Tukey post-hw comparisons to determine which groups were different from one another. A significance level of p < .01 was accepted. Table 3 summarizes the number of tests significantly different and the number of tests with medians lower than controls (regardless of statistical significance) for the three severity groups at the three time periods on 21 neuropsychological measures used. The most severe TFC group ( 2 7 days) was significantly different from the control group on most measures at all times. The next most severe TFC group (25 hours - 6 days) was significantly impaired on one-half of the measures at 1 month as compared to controls. At 1 year post injury, only I1 was significantly different from controls. By 2 years postinjury, there were no significant differences between the head-injured group with TFC between 25 hours to 6 days and controls. The least severe TFC group’s ( 5 24 hours) median scores were consistently better than the two more severely injured groups and were slightly worse than controls. This group was significantly impaired on only a few variables, including the overall measures of 11, IQ, and measures of speed and distractibility at 1 month. There was only one significant difference at 1 year and no significant differences at 2 years postinjury. Because of the small sample size of each subgroup and the variability within them, lack of statistically reliable results pertaining to the impairment in the two less severe groups probably reflect the lack of power of the study as much as the actual state of functioning of the patients. Table 3 indicates that the medians of all the head-injured subgroups were consistently, although not significantly, lower than those of controls on the majority of the 21 neuropsychological measures utilized. The results do indicate that there is a clear ordering effect of performance by severity. However, all of the subgroups seem to show head injury effects over the 2-year time period. The results of the Wilcoxon Signed Rank Tests comparing head-injured group performance at 1 month with performance at 1 year and at 2 years demonstrated significant change from 1 month to 1 year and 1 month to 2 years on all neuro-
Table 3. Number (Out of the 21 NeuropsychologicalTests) Where the Head Injury Severity Sub-Group Medians Were Poorer Than, or Significantly Different from, the
Control Group 1 Month
TFC 5 1 day
25 hours - 6 days 7 + days
poorer significant 21 21 21
24 Months
12 Months
6 11 21
poorer significant 17 21 21
1 1
17
poorer significant 16 19 21
0 0 18
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psychological measures. There were significant differences between 1-year and 2-year head-injured test data on some measures (Tapping-D, Tapping-ND, Speech Sounds, VIQ, PIQ, Category). Wilcoxon Rank Sum tests revealed that the change scores in the head-injured group from 1 month to 1 year and from 1 month to 2 years were significantly different from the change in the test-retest values of the comparison group on almost all neuropsychological measures. However, when the change in the comparison group was contrasted with the change in the head-injured group from 1 to 2 years postinjury, only Speech Sounds and VIQ showed significant differences between the groups. In order to examine recovery further, change as a function of head injury severity and abilities assessed was examined by descriptive plotting of the data. Figure l a and l b show sample performances of the three severity subgroups on Trails B and Rhythm. The results indicate that improvement occurred during the first year for each of the subgroups on both measures. Change in the second year is more complicated. The results are suggestive of no change on Rhythm, irrespective of severity of head injury, and continued improvement for patients with TFC 1 7 days on Trails B. To explore how variability of performance over repeated measures may have contributed to difficulties in demonstrating recovery, the performances of the
l b . Rhythm
l a . Trails B 300
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.-E
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c. 40
1-
Ot
,
1 Month
1
1 2 Month 2 4 Month
A
,
I
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Figure 1. Recovery as a function of head injury severity and type of task.
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2a. W A l S
- VlQ
r
2b. SR 100
r
I20
80
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L 1 Month
0' I
1
12 Monlh 24 Month
-
r
I
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Figure 2. Recovery curves for individual patients.
individual subjects were plotted over three repeated administrations on VIQ and SR-CLTR. As reported earlier, recovery was concluded on VIQ and not on SRCLTR, a memory measure. As Figure 2 indicates, changes appear to be much more consjstent on VIQ than on SR-CLTR.
DISCUSSION The present study provides convincing evidence of (a) persistent cognitive difficulties in patients with moderate to severe head injuries over a 2-year period, (b) of significant association between coma length and cognitive functioning, and (c) marked improvement in the first year postinjury. Recovery in the second year is modest and its determination is complicated by practical problems. Our finding of a significant relationship between cognitive functioning and coma length is consistent with our previous reports (Dikmen et al., 1986, 1987) but not with those of others (Alexandre et al., 1983; Brooks et al., 1980; and Levin et al., 1979). Although some differences in definition of coma length are a potential cause, other potential causes include differences in subject selection, head
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injury severity represented in the samples, and whether or not time from injury to testing was controlled. Marked improvement exceeding the change seen in controls occurred in headinjured patients on all neuropsychological measures within the first year post injury. During the second year, improvement occurred for the head-injured group, but on fewer measures, and reliably exceeded the change seen in the controls on only two measures (VIQ & Speech Sounds). The marked improvement in the first year is consistent with other reports in the literature (Dikmen et al., 1983; Drudge et al., 1984; Mandleberg, 1976; Parker & Serrats, 1976; Tabaddor et al., 1984). Although recovery in the first year appears clear-cut, the important question is: What can be concluded about recovery during the second year? Based on the statistical results, one possible conclusion is that recovery during the second year occurs but is very modest. A small change is always difficult to demonstrate in a statistical fashion. In this case, the demonstration is made more difficult by the heterogeneity among head-injured subjects, the likely overestimation of practice effects discussed more below, and the perhaps diminished statistical power obtained with the use of nonparametric tests. An alternative conclusion is that recovery during the second year occurs, but the picture is much more complicated: Recovery is more selective, complex, and varies with the type of function assessed and the severity of the injury, as illustrated in Figure l a and lb. Differential recovery rate as a function of type of ability has been also indicated by the results of other studies (Lezak, 1979; Mandleberg, 1976; Tabaddor et al., 1984). Two important factors or complications need to be discussed in relation to the recovery findings during the second year. One relates to whether or not the comparison subjects represented appropriate controls for practice effects, and the other relates to the variability in test-retest observed on certain measures and the implications of this variability for documenting recovery. The use of normal comparison subjects to control for practice in the headinjured assumes that the effect of practice on performance is equal in the two groups. This may not be accurate, as normal subjects with intact memory are likely to benefit more from prior exposure than do the patients with significant head injury. Therefore, the magnitude of recovery in the second year may have been underestimated due to overestimation of the magnitude of practice effects. In addition, the effect of practice in our study may have been overestimated in the head-injured group because the number of repeated assessments differed between the head-injured and control groups. Due to study limitations, we were only able to test the control subjects twice while the head-injured received three evaluations. When the change in the head-injured in the second year post injury was compared to the test-retest values in the control group, the control group had the benefit of the initial practice effect while the head-injured had multiple exposure to the tests. Although there is no literature available, clinical experience suggests that the magnitude of change as a result of practice is high initially and diminishes with additional exposure due to ceiling effects. Practice effects,
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and how to control them, is one of the enormous practical problems in conducting recovery studies and in interpreting results of individual clinical cases (Brooks, 1987; Dikmen & Temkin, 1987). The other complication that may cause difficulties in documenting recovery is test-retest variability, particularly on certain measures. The results of the current study and of a previous sample (Dikmen et al., 1983) indicate that there is substantial variability with repeated measurements, especially on certain tests. Variability in test-retest scores may be the result of unreliability of the measure or of the construct measured, or it may reflect true change (i.e., recovery or deterioration). An examination of individual recovery curves of VIQ and SRCLTR (Figure 2) indicates that the improvement in performance is modest for both measures but is more consistent for VIQ than for the SR-CLTR. As a result, the change in VIQ is statistically significant but that in SR-CLTR is not. It is not entirely clear why the fluctuations across time occur on individuals’ memory scores. It may be that the factors which contribute to subject unreliability are particularly important on memory tasks. For example, inattention on the Selective Reminding Test or the WMS can lower the patient’s score. A similar level of inattention on the WAIS is likely to lead to repetition of the question or the instructions. Unreliability of measures may be an especially pertinent problem in the head-injured population where factors such as fatigue and distractibility make the possibility of obtaining the subject’s best performance at one given time somewhat less likely. While the unreliability of head-injured patients is a suspected and clinically important phenomenon in its own right, it is unwanted error variance from the point of view of measuring recovery based on single observation. These results point out the need for measures with better psychometric properties when attempting to examine certain constructs and/or the use of repeated observations to arrive at a value more representative of the ability being measured in a given time frame. Although test-retest differences may reflect true change, they may also reflect the effects of unwanted factors and could lead to erroneous conclusions showing no improvement in recovery studies and improvement or deterioration in interpreting the results of individual cases. Research examining group performance with large samples can overcome the impact of a certain amount of variability. However, clinical evaluation of the individual case over time must always consider the possibility that variability in the data, especially on certain types of measures, reflects unreliability and not true change. The results of this project do not provide conclusive evidence for continued recovery or, for that matter, cessation of change in the second year post injury. There are indications that recovery continues, but the issues of practice effects and variability within the data must be first addressed with larger samples.
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