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2002,
VOL.
16,
NO.
6, 509 516
Introduction
Apathy is a common consequence of traumatic brain injury (TBI). Apathy has been
represented as a state characterized by decreased initiative and akinesia [1 3]. Marin
[3] defined apathy as a `lack of motivation not attributable to diminished level of
consciousness, cognitive impairment, or emotional distress. Marin describes three
domains that lead one to recognize apathy: (1) `deficits in goal-directed behaviour,
(2) `a decrement in goal-related thought content, and (3) emotional indifference
with flat affect [4].
Van Zomeran and Van den Burg [5] found that 23% of subjects with TBI
complained of decreased initiative 2 years after injury. In a survey of people with
TBI 6 months after injury, 21% reported `difficulty in becoming interested ([6], p.
615). In a follow-up survey 7 years from the time of injury, 28% cited `difficulty in
becoming interested as a problem, while 43% of their relatives endorsed this item as
an issue for the subjects with TBI ([7], p. 565). Despite its frequent occurrence and
Correspondence to: Mel B. Glenn, MD, Spaulding Rehabilitation Hospital, 125 Nashua St.,
Boston, MA 02114, USA. e-mail: mglenn@partners.org
Brain Injury ISSN 0269 9052 print/ISSN 1362 301X online # 2002 Taylor & Francis Ltd
http://www.tandf.co.uk/journals
DOI: 10.1080/02699050110119132
510
M. B. Glenn et al.
Table 1.
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
Items are rated and assigned points as follows: not at all true 0, slightly true 1, somewhat true 2, very
true 3.
Adapted with permission from Marin [4].
511
Methods
Subjects
Subjects were outpatients with TBI who were included if they were 16 years of age
and over, presented with Rancho Los Amigos Levels of Cognitive Functioning
Scale (RLAS) [13] level of V or higher at time of study participation, and did not
have other significant neurologic diagnoses or acute medical or behavioural conditions. Subjects were excluded if they had had psychostimulant or dopaminergic
medication dosage changes over the previous 6 weeks or antidepressant changes
over the past 8 weeks.
Subjects were classified as mild TBI if there was a change in mental status with
initial Glasgow Coma Scale (GCS) score of 13 15 following a loss of consciousness
(LOC) of 0 30 minutes, and if the period of post-traumatic amnesia was less than 24
hours. Subjects were classified as moderate TBI if the initial GCS score was 9 12 or
if LOC was 30 minutes to 6 hours. Those classified as severe TBI had an initial GCS
score of less than 9 with LOC greater than 6 hours.
Thirty-two (70%) subjects were male and 14 (30%) female. The mean age across
all subjects was 43.1 years (17.7 74.3, SD 14.9). The mean time since injury was
43.9 months (4.3 260.2, SD 57.7). GCS information, in some cases obtained retrospectively, was available on 41 subjects: 23 (52%) were classified as mild, eight (18%)
as moderate, and 13 (30%) as severe TBI. The mean Disability Rating Scale (DRS)
[14] score at the time of study participation was 3.0 (0 10.5, SD 2.6).
Instruments
The AES is an 18-item scale with the following scoring system for each item: not at
all true 0, slightly true 1, somewhat true 2, very true 3 (see table 1).
Validity has been studied in several populations, but not in subjects with TBI
[10]. Reliability has been studied in TBI [12] and in several other populations [10].
The RLAS is an 8-level observational scale describing a continuum of cognitive
and behavioural function following TBI. Inter-rater and test re-test reliability, as
well as concurrent and predictive validity have been reported [13].
The DRS is a 30-point rating scale measuring a continuum of outcomes following TBI. It covers a spectrum of impairment, disability, and handicap from basic
responsivity to employability. Inter-rater reliability, as well as concurrent and predictive validity have been established [14].
The BDI-II is a 21-item self-report inventory used to assess the severity of
depression. Test re-test reliability and convergent validity have been reported [15].
Procedures
Of 53 consecutive outpatients with TBI seen in follow-up visits with the studys
three clinician investigators, 46 consented to participate. Forty-five completed the
AES-S at the time of an outpatient visit. One subject did not complete the AES-S
due to aphasia. The Beck Depression Inventory-II (BDI-II) [15] was filled out as
well. Thirty-seven family members, friends, or significant others were available at
the time of the outpatient visit or within several days, and filled out the AES-I.
Subjects were assisted with reading the form when necessary.
512
M. B. Glenn et al.
Table 2.
(1)
(2)
(3)
(4)
(5)
(6)
(7)
Rating on scale
Best cutoff by
ROC curve
2 or higher
3 or higher
AES-S > 32
AES-S > 41
Table 4.
Rating on scale
2 or higher
3 or higher
Sensitivity
(%)
Specificity
(%)
0.81
0.61
95
68
0
45
Best cutoff by
ROC curve
Area under
ROC curve
Sensitivity
(%)
Specificity
(%)
AES-I > 24
AES-I > 35
0.77
0.71
100
77
17
60
Severity category
SD
38.5
35.0
35.3
37.0
38.8
24.4
8.3
10.7
8.1
8.6
9.8
4.5
23
7
13
43
83
127
Mild
Moderate
Severe
Total
Kant et al.s subjectsb
Kant et al.s healthy control subjects
b
Area under
ROC curve
Table 5.
513
improved the ROC curve such that the sensitivity was 86% and the specificity 97%
(area under ROC 0:97).
On the AES-I, the best ROC curve (area under ROC curve 0:77) was at a
cutoff score of > 24 for a prediction of at least 2 on the 7-point scale (sensitivity
100%, specificity of 17%; PPV 86%, NPV 100%). For a prediction of at least 3 on
the scale, the best area under the ROC curve was 0.71 for a cutoff score of > 35,
with a sensitivity of 77% and specificity of 60% (PPV 74%, NPV 64%) (see table 4).
Given an inability to find a cutoff score that resulted in reasonable sensitivity and
specificity, the authors are unable to report the prevalence of apathy in this group.
The mean AES-S score was 37.3 (SD 8:8, n 45) and the mean AES-I score was
39.4 (SD 9:1, n 37) The difference was not significant. The correlation (r)
between AES-S and AES-I was 0.55. There was no significant difference in scores
among the mild, moderate and severe groups on the AES-S or AES-I (see tables 5
and 6). The greatest difference was between moderate severe and mild groups, the
latter having slightly higher scores (p 0:21).
Correlation coefficients (r) for the association between BDI-II scores with AESS and AES-I scores were 0.56 and 0.52, respectively. The results of the depression
survey are reported elsewhere [16]. Cronbachs was 0.90 for the AES-S, 0.92 for
the AES-I, and 0.93 for the BDI-2.
514
M. B. Glenn et al.
Table 6.
Severity category
Mild
Moderate
Severe
Total
Kant et al.s subjectsb
a
b
SD
38.0
39.7
40.1
38.9
50.5
9.8
5.9
8.7
8.8
6.6
19
6
10
35
28
Discussion
The authors were unable to find a cutoff score on the AES-S or AES-I that
provided reasonable sensitivity and specificity with respect to a clinicians designation or rating of a subject as apathetic. When the AES-S was included in a logistic
model with several other variables, good sensitivity and specificity resulted, which
indicates that the clinicians were making a predictable distinction among the subjects, but that the AES did not capture this characteristic. This may reflect a discrepancy between the authors use of the term `apathy and that which the AES
measures or a problem with the validity and/or reliability of the AES-S. This studys
explicit allowance of depression as a cause of apathy could have contributed to the
discrepancy. Marin et al. [10] did not include many items reflecting emotional
aspects of apathy in the AES, as their scale development procedures tended to
eliminate such items. These procedures included item total correlations, factor
analysis, and the choice of seven items that did not correlate with the Hamilton
Rating Scale for Depression in order to allow the scale to discriminate apathy from
depression [10]. Nonetheless, Kant et al. [12] found that 85% of subjects who were
apathetic according to their AES-S criteria also met their BDI criteria for depression.
In the analysis of the BDI-II scores in these subjects, the authors found a greater
prevalence of depression among those with mild TBI [16]. Although one might
expect to find greater apathy among those with severe TBI, on both the AES-S and
AES-I, scores were similar among those with mild, moderate and severe TBI. In
fact, AES-S scores were somewhat higher among those with mild TBI. This could
be a result of the influence of depression on AES scores, which correlated modestly
with BDI-II scores. These factors argue against the possibility that this studys
allowance of depression as a cause of apathy interfered with the AESs ability to
predict the clinicians designation of apathy, but does indicate that the AES may not
discriminate between neurologically-based apathy and apathy caused by depression.
It is also possible that the AES is not a psychometrically sound measurement
tool, i.e. that there are reliability problems, or that it does not accurately reflect
either Marin et al.s or the authors definition of apathy. Test re-test reliability for
the AES-I and AES-C (clinician as rater based upon a single interview) have been
found to be good, but the test re-test reliability of the AES-S for subjects with
Alzheimers disease was not adequate [10]. AES test re-test reliability has not been
assessed in subjects with TBI. The authors did find good internal consistency for
both the AES-S and AES-I.
Intercorrelations among the AES-S, AES-I and AES-C ranged from 0.43 0.72,
the lowest correlation being between the AES-S and AES-I [10]. There was a
515
modest correlation between the two in this study (r 0:55). Kant et al. [12] found a
discrepancy between AES-S and AES-I results, with subjects rating themselves as
less apathetic. As hypothesized, this may be the result of having a subject with
frontal lobe disorders attempt to self-evaluate. However, the authors did not find
a significant difference between AES-S and AES-I results (p 0:31).
Marin et al. [10] did two types of predictive validity studies, with several items in
each study. These studies resulted in non-significant correlations between AES
scores and more than half of the predictive measures. For those that were significant,
correlations (Pearsons r) were no better than 0.45 between the scores and any single
predictive measure.
Stuss et al. [17] reviewed the various definitions of apathy seen in the literature.
They argue that it is problematic to rely upon the concept of motivation to define
apathy, as do Marin et al. [10], since motivation is an internal state and cannot be
directly measured. Marin [4] addresses this issue by providing behavioural anchors to
his definition. However, Stuss et al. [17] have also presented evidence that apathy is
not a single neuroanatomic nor neuropsychologic entity, which certainly could lead
to problems with validity for any tool that attempts to measure it as such.
The authors are unable to report the prevalence of apathy in this population.
However, the AES-S scores in the study population were in the vicinity of those
described by Kant et al. [12] in an outpatient population (see tables 4 and 5) with
TBI. Although, as noted above, this studys AES-I scores were not significantly
above the AES-S scores.
This studys findings suggest that the AES requires further study before it can be
confidently used to measure apathy. The AES-I may turn out to be a better measure
of apathy than the AES-S.
Acknowledgements
Supported by grant H133A980034-00 from the National Institute on Disability and
Rehabilitation Research, United States Department of Education.
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