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Effect of Anxiety

Disorder on Impairment
and Recovery From
Stroke
Kengo Shimoda, M.D.
Robert G. Robinson, M.D.

The effect of anxiety disorder on recovery from


impairment following stroke was examined in 142 T he relationship between anxiety disorder and de-
pressive disorder has been a topic of great interest
in psychiatry. Comorbidity of anxiety and depressive
patients with acute stroke who had follow-up eval- disorders has been shown to influence many clinical as-
uations. Anxiety disorder significantly interacted pects of these disorders, including onset, duration, re-
with depression to influence the severity and sponse to treatment, and severity, when compared with
course of depression, outcome of activities of daily each condition alone.14 Thus, the comorbid condition
living, and social functioning. Anxiety disorder, appears to have important implications for both long-
however, did not affect cognitive impairment, term outcome and response to treatment.
During the past few years, we have been examining
which was influenced only by major depression. the clinical and neuropathological correlates of anxiety
These data suggest that the existence of anxiety disorder following acute stroke.5,6 These studies have
disorders plays an important role in the prognosis identified the frequent comorbidity of depressive dis-
of patients with poststroke depression. These data orders and anxiety disorders in patients with acute
also suggest that depression and anxiety disorder stroke. Comorbid major depression and generalized
may have different mechanisms. anxiety disorder were associated with left frontal corti-
(The Journal of Neuropsychiatry and Clinical cal lesions.5 Similarly, anxiety disorder, but not comor-
Neurosciences 1998; 10:3440) bid anxiety and depression, was associated with in-
creased frequency of alcohol abuse and right
hemisphere lesions.6 These data, as well as other similar
findings, suggest that comorbid anxiety and depression
may have a different etiological basis than depression
alone or anxiety without depressive disorder.
Previous studies have shown that poststroke depres-
sive disorders influence the cognitive7,8 and physical9

Received March 6, 1996; revised August 20, 1996; accepted September


26, 1996. From the Department of Psychiatry, University of Iowa Col-
lege of Medicine, Iowa City, Iowa; and Department of Neuropsychi-
atry, Nippon Medical School, Tokyo, Japan. Address correspondence
to Dr. Robinson, Department of Psychiatry, University of Iowa Hos-
pitals and Clinics, 200 Hawkins Drive #2887 JPP, Iowa City, IA 52242-
1057.
Copyright q 1998 American Psychiatric Press, Inc.

34 VOLUME 10 NUMBER 1 WINTER 1998


SHIMODA AND ROBINSON

consequences of stroke. Major depressive disorder is as- was evaluated with the Mini-Mental State Examina-
sociated with a significantly greater degree of cognitive tion16 (MMSE). Scores range from 0 to 30, with lower
impairment than can be explained by the presence of scores indicating greater impairment. Activities of daily
the lesion alone.10,11 Parikh et al.,9 as well as Sinyor et living were quantified by use of the Johns Hopkins
al.,12 demonstrated that physical and language recovery Functioning Inventory17 (JHFI). Scores range from 0 to
from stroke were adversely affected by the existence of 27, with higher scores indicating greater impairment.
depressive disorder. We have not, however, previously Social functioning was assessed by use of the Social
examined the influence of comorbid anxiety and de- Functioning Exam18 (SFE). Scores range from 0.00 to
pressive disorder on cognitive or physical recovery from 1.00, with higher scores indicating greater perception of
stroke or the longitudinal course of depression. There- impaired social function.
fore, the present study examined the hypothesis that the
comorbid existence of anxiety and depressive disorder Lesion Location
would be associated with a greater degree of impair- Computed tomography scans were obtained from 73
ment in cognitive function and a poorer recovery from (51.4%) of the patients included in the study and were
depression and physical impairment than would de- evaluated by a neurologist who was blind to the psy-
pressive disorder without comorbid anxiety disorder. chiatric findings. All CT scans had consistent 10-mm
slice thickness and consistent angle to the canthomeatal
line. Methods for determining lesion location (lesion
METHODS volume, interrater reliability, cortical-subcortical loca-
tion) have been described in a previous report.5
Patient Population
A consecutive series of 142 patients who were admitted Statistical Analysis
to University of Maryland Hospital, Baltimore, MD, A 222 design was used in this study. Analysis of vari-
with a diagnosis of either acute intracerebral hemor- ance (ANOVA) and repeated-measures ANOVA were
rhage or acute cerebral infarction and who were seen in performed to analyze the relation between dependent
the follow-up clinic were examined for psychiatric dis- variables such as MMSE scores and each of the depen-
order after providing informed consent. Patients were dent variables such as the existence of depression or
excluded only if they were unable to undergo a verbal GAD. If the ANOVA was significant, each group was
interview. Nearly one-third of patients admitted with compared by using post hoc planned tests (Scheffe). Chi-
acute stroke were unable to complete an interview be- square tests were performed to analyze frequency dis-
cause of decreased level of consciousness or aphasia tributions. Yates correction was used to adjust for ex-
with impaired comprehension. Of these 142 patients, pected cell sizes below 5, and two-tailed P-values were
110 patients (77.5%) were examined at either 3-month used.
or 6-month follow-up (short-term follow-up), and 102 pa-
tients (71.8%) were examined at either 12-month or 24-
month follow-up (long-term follow-up). Patients were lost RESULTS
to follow-up due to mortality (15%) or failure to show
up for appointments (10%). Background Characteristics
Subjects were divided into four groups: control
Psychiatric and Neurological Evaluations (n4100), generalized anxiety disorder only (n415), ma-
After obtaining informed consent, we examined the pa- jor depressive disorder only (n49), and MDD plus GAD
tients by using a structured mental status examination, (n418).
the Present State Examination13 (PSE). We made diag- The background characteristics of these groups are
noses of major depression (MDD) or generalized anxiety shown in Table 1. There were significantly more female
disorder (GAD) by using the symptoms elicited on the patients in the MDD and MDD plus GAD groups than
PSE and the DSM-IV14 symptom criteria for major de- in the non-MDD groups (v2412.9, df43, P40.049);.
pressive disorder and generalized anxiety disorder. The
diagnostic criteria for GAD were slightly modified from CT Findings
DSM-IV criteria as follows: patients had to acknowledge Of the 142 patients in this study, 48 had single lesions
the presence of worry or anxious foreboding, and du- restricted to cortical or subcortical structures as assessed
ration criteria were excluded. In addition, the severity by CT scan. In all cases, brain lesions were found by a
of depression was measured with the Hamilton Rating neurologist to be compatible with findings on neuro-
Scale for Depression15 (Ham-D). Cognitive functioning logic examination. Cortical lesions were found in 13 of

JOURNAL OF NEUROPSYCHIATRY 35
ANXIETY DISORDER AND STROKE

27 patients (48.1%) in the control group, 0 of 4 patients patients than for patients with MDD only or control sub-
(0%) in the MDD-only group, and 4 of 5 patients (80%) jects, but there were no significant differences among the
in the MDD plus GAD group. These were statistically groups at long-term follow-up (initial: F448.4, df42,86,
significant intergroup differences in the frequency of P,0.0001; long-term follow-up: F41.6, df42,86,
cortical lesions (v247.4, df42, P40.03). P.0.1).

Relationship to Diagnostic Outcome Effect of MDD and GAD on Impairment and Recovery
We next examined diagnostic outcome among groups. We found that non-MDD patients tended to be older
There were significant intergroup differences in the fre- than patients with MDD (non-MDD, 59.2512.4, vs.
quency of major depression at short-term follow-up MDD, 54.0513.0: t41.93, df4140, P40.056), and non-
(control: 5 of 73; MDD only: 0 of 8; MDD`GAD: 9 of GAD patients tended to have larger lesion volumes than
14; v2424.7, df42, P,0.0001). Most patients with MDD patients with GAD (non-GAD, 7.457.3, vs. GAD,
plus GAD remained depressed at short-term follow-up, 3.452.8: t41.97, df465, P40.054). Values are reported
whereas none of the MDD-alone patients remained de- as means and standard deviations.
pressed (MDD only vs. MDD`GAD, v246.3, P40.02). For the purpose of excluding factors other than MDD
There were no significant intergroup differences, how- or GAD that were known to effect stroke outcome, the
ever, in the persistence of major depression at long-term following analyses were done, using patients who were
follow-up (control: 12 of 78; MDD only: 1 of 4; matched for age (52 years), education (52 years), and
MDD`GAD: 0 of 9; v243.2, df42, P.0.1). lesion volume (52% of total brain volume).
We also examined changes in the severity of depres-
sion (Ham-D scores) during the follow-up evaluation. A Relationship to Cognitive Impairment and Recovery: In
one-way ANOVA of Ham-D scores for the patients with short-term follow-up, repeated-measures ANOVA of
3- to 6-month follow-up showed that patients who had MMSE scores (factor 1: presence or absence of MDD;
MDD plus GAD in-hospital had significantly higher de- factor 2: presence or absence of GAD) showed signifi-
pression scale scores at both time evaluations than did cant effects for MDD (F421.7, df41,56, P,0.0001) and
patients with MDD only or control subjects (initial: time (F47.23, df41,56, P40.009), but no significant ef-
F487.8, df42,86, P,0.0001; short-term follow-up: fect for an MDD2time interaction and no significant
F415.4, df42,86, P,0.0001). Post hoc test (Scheffe) effect for GAD (Table 2). A two-way ANOVA at each
demonstrated that patients with MDD plus GAD had time showed a significant effect for MDD at both initial
significantly higher depression scale scores at both time and short-term follow-up (initial: F429.68, df41,56,
evaluations than did patients with MDD only (initial: P,0.0001; short-term: F48.04, df41,56, P40.006), but
P,0.001; short-term follow-up: P,0.05). In contrast, no effect for GAD and no MDD2GAD interaction. Sim-
one-way ANOVA of Ham-D scores for the patients with ilarly, in long-term follow-up, repeated-measures
12- to 24-month follow-up showed significantly higher ANOVA of MMSE scores showed a significant effect of
in-hospital depression scores for the MDD plus GAD MDD2time interaction (F46.57, df41,58, P,0.01), but

TABLE 1. Demographics of sample


Non-MDD MDD
Characteristic Control GAD only MDD only MDD~GAD
n 100 15 9 18
Age (years, mean5SD) 59.5512.2 56.9514.0 53.6512.7 54.2514.2
Education (years, mean5SD) 9.354.1 9.654.7 7.853.8 9.453.2
Sex (% female)a 37.0 33.3 77.8 72.2
Race (% black) 67.0 60.0 77.8 55.6
Marital status (% married) 49.0 60.0 11.1 50.0
Alcohol abuse (% positive) 6.0 13.3 11.1 16.7
Socioeconomic status (% class IV-V) 26.0 26.7 88.9 83.3
Family psychiatric history (% positive) 6.0 0.0 11.1 11.1
Past psychiatric history (% positive) 11.0 20.0 44.4 22.2
Medication
Antidepressants (% positive) 5.0 0.0 22.2 11.1
Other psychotropics (% positive) 0.0 0.0 0.0 0.0

Note: MDD4major depressive disorder; GAD4generalized anxiety disorder.


Significant differences between 4 groups (v2412.9, df43, P40.049).
a

36 VOLUME 10 NUMBER 1 WINTER 1998


SHIMODA AND ROBINSON

not of GAD or other interaction. A two-way ANOVA at way ANOVA at each time showed no significant effect
each time showed a significant effect of MDD at initial at the initial evaluation. In contrast, however, patients
evaluation (F45.16, df41,58, P40.03), but not at long- with major depression had significantly lower JHFI
term follow-up (F40.10, df41,58, P40.8). In contrast, scores at short-term follow-up than those who were not
there was no significant effect of GAD, and there were depressed (MDD: F416.27, df41,57, P40.0002).
no significant interaction effects at either time. Repeated-measures ANOVA of JHFI scores for pa-
tients with 12- to 24-month follow-up showed signifi-
Relationship to Physical Impairment and Recovery: Re- cant effects for MDD (F44.50, df41,55, P40.04) and
peated-measures ANOVA of JHFI scores for the patients MDD2GAD interaction (F45.63, df41,55, P40.02),
with 3- to 6-month follow-up showed a significant effect but no significant effect for GAD or other interaction. A
for MDD (F48.78, df41,57, P40.004) and time two-way ANOVA at each time showed significant ef-
(F425.60, df41,57, P,0.0001), but no significant effect fects for MDD and an interaction with GAD at long-term
for GAD or MDD2GAD interaction (Table 3). A two- follow-up (MDD: F45.94, df41,55, P40.02;

TABLE 2. Mini-Mental State Examination scores at short-term and long-term follow-ups


Two-Way Analysis of Variance
Follow-up and Mean%SD MDD GAD Interaction
Time of Test Control GAD only MDD only MDD~GAD F P F P F P
(n436) (n49) (n46) (n49)
Short-term FU
Initial 26.153.5 24.754.1 18.553.4 18.355.6 29.68 0.0001 0.37 0.54 0.23 0.63
Short terma,b 26.455.3 26.353.8 21.754.1 21.756.2 8.04 0.006 0.001 0.98 0.001 0.98
(n445) (n47) (n43) (n47)
Long-term FU
Initial 25.453.6 24.753.4 22.0510.4 20.156.9 5.16 0.03 0.54 0.47 0.10 0.75
Long termc,d 25.653.6 24.955.2 25.755.1 24.455.3 0.10 0.92 0.36 0.55 0.03 0.87

Note: MDD4major depressive disorder; GAD4generalized anxiety disorder; FU4follow-up.


Repeated-measures analysis of variance:
a
Significant effect for MDD (F421.73, P,0.0001).
b
Significant effect for time (F47.23, P40.009).
c
Significant effect for time (F47.47, P40.008).
d
Significant effect for MDD(time (F46.57, P,0.01).

TABLE 3. Johns Hopkins Functioning Inventory scores at short-term and long-term follow-ups
Two-Way Analysis of Variance
Follow-up and Mean % SD MDD GAD Interaction
Time of Test Control GAD only MDD only MDD~GAD F P F P F P
(n436) (n49) (n46) (n410)
Short-term FU
Initial 5.854.4 6.254.4 6.855.5 9.856.6 2.23 0.14 1.21 0.28 0.64 0.43
Short terma,b 1.852.2 4.556.9 4.554.9 6.654.6 16.27 0.0002 0.25 0.62 2.25 0.14
(n445) (n46) (n43) (n45)
Long-term FU
Initial 5.253.7 4.855.2 4.353.5 10.054.5 1.61 0.21 2.46 0.12 3.29 0.08
Long termc,d,e 1.752.8 0.751.2 2.052.6 6.254.5 5.94 0.02 1.76 0.19 4.74 0.03

Note: MDD4major depressive disorder; GAD4generalized anxiety disorder; FU4follow-up.


Repeated-measures analysis of variance:
a
Significant effect for MDD (F48.78, P40.004).
b
Significant effect for time (F425.60, P40.009).
c
Significant effect for MDD (F44.50, P40.04).
d
Significant effect for MDD2GAD (F45.63, P40.02).
e
Significant effect for time (F47.47, P40.008).

JOURNAL OF NEUROPSYCHIATRY 37
ANXIETY DISORDER AND STROKE

MDD2GAD: F44.45, df41,40, P40.04). Thus, patients patients with MDD plus GAD in the hospital were more
who had both MDD and GAD in-hospital were more socially impaired at long-term follow-up than control
impaired in their activities of daily living at long-term patients or patients with MDD alone.
follow-up than were control patients or patients with
GAD alone.
DISCUSSION
Relationship to Social Functioning: Repeated-measures
ANOVA of SFE scores for the patients with 3- to 6- The present study was undertaken to evaluate the effect
month follow-up showed significant effects for MDD of comorbid anxiety disorder and depressive disorder
(F428.43, df41,54, P,0.0001), GAD (F416.93, df41,54, on impairment following acute stroke. Our findings
P,0.0001), GAD2time interaction (GAD2time: demonstrated for the first time that anxiety disorder fol-
F44.88, df41,54, P40.03) and MDD2GAD2time lowing stroke influenced the severity and course of re-
interaction (MDD2GAD2time: F46.56, df41,54, covery from stroke. Anxiety disorder interacted with de-
P,0.01), but no significant effect for MDD2GAD pression to influence the degree of impairment in
interaction (Table 4). A two-way ANOVA at each time activities of daily living and the course of recovery in
showed a significant effect for MDD at both times (ini- social functioning at long-term follow-up. On the other
tial: F413.48, df41,54, P,0.001; short-term: F421.52, hand, depression, but not an interaction with GAD, ex-
df41,54, P,0.0001). There were significant effects for plained our previously demonstrated finding that de-
GAD and interaction with MDD at short-term follow- pression affects cognitive function following acute
up (GAD: F425.90, df41,54, P,0.0001; MDD2GAD: stroke.7,11
F412.06, df41,54, P,0.001). Before further discussing these findings, we should
Repeated-measures ANOVA of SFE scores for pa- address several methodological limitations. First, cog-
tients with 12- to 24-month follow-up showed signifi- nitive function was evaluated by using only the brief,
cant effects for MDD (F411.65, df41,56, P,0.001), language-dominated MMSE. Because of the limited
GAD2time (F45.79, df41,56, P40.02), and number of cognitive functions evaluated by MMSE, we
MDD2GAD2time interaction (F45.20, df41,56, were unable to determine whether there may have been
P40.03). A two-way ANOVA at each time showed a a subtle effect of GAD on cognitive function. This will
significant effect for MDD at initial evaluation (F412.20, require a study using a more detailed neuropsycholog-
df41,56, P40.0009). In contrast, there were significant ical assessment.11 Second, patients with severe compre-
effects for GAD (F46.80, df41,56, P,0.01) and hension deficits were excluded, and the population of
MDD2GAD interaction (F46.46, df41,56, P,0.01) at this study was predominantly black and of lower socio-
long-term follow-up, but not at initial evaluation. Thus, economic status. Therefore, the results of this study may

TABLE 4. Social Functioning Exam scores at short-term and long-term follow-ups


Two-Way Analysis of Variance
Follow-up and Mean%SD MDD GAD Interaction
Time of Test Control GAD only MDD only MDD~GAD F P F P F P
(n436) (n48) (n46) (n48)
Short-term FU
Initial 0.1250.08 0.1750.08 0.2450.15 0.2850.11 13.48 0.0006 2.53 0.12 0.02 0.88
Short terma,b,c,d 0.1750.09 0.1650.09 0.3750.10 21.52 0.0001 25.90 0.0001 12.06 0.001
(n445) (n47) (n43) (n45)
Long-term FU
Initial 0.1750.09 0.1750.08 0.3450.25 0.2950.13 12.20 0.0009 0.42 0.52 0.64 0.43
Long terme,f,g 0.1550.14 0.1550.08 0.0950.06 0.3750.16 2.30 0.14 6.80 0.01 6.46 0.14

Note: MDD4major depressive disorder; GAD4generalized anxiety disorder; FU4follow-up.


Repeated-measures analysis of variance:
a
Significant effect for MDD (F428.43, P,0.0001).
b
Significant effect for AD (F416.93, P,0.0001).
c
Significant effect for GAD2time (F44.88, P40.03).
d
Significant effect for MDD2GAD2time (F46.56, P,0.01).
e
Significant effect for MDD (F411.65, P,0.001).
f
Significant effect for GAD2time (F45.79, P40.02).
g
Significant effect for MDD2GAD2time (F45.20, P40.03).

38 VOLUME 10 NUMBER 1 WINTER 1998


SHIMODA AND ROBINSON

not apply to a more general population of poststroke patients with MDD or GAD alone. These findings sug-
patients. Another limitation was the potential effect of gest that anxiety disorder is an important variable af-
medications on cognitive function or recovery. Benzo- fecting long-term prognosis of depression following
diazepines or other sleeping medications are commonly stroke. We have previously reported that major depres-
prescribed in this population and may contribute to cog- sion adversely affects the course of physical recovery.9
nitive impairment or slower speed of recovery. When Thus, one possible explanation is that since, as discussed
we examined the frequency of various psychotropic below, MDD with GAD has a longer duration of de-
medications at the in-hospital evaluation, we did not pression than MDD alone, this prolonged depression
find significant differences in the frequency of antide- may have led to these adverse physical and social func-
pressant medications among groups, and we did not tioning outcomes.
find any patients who were treated with other psycho- Another interesting finding in this study was that pa-
tropics such as benzodiazepines (Table 1). However, we tients with MDD plus GAD had significantly longer and
did not examine the frequency of medication use at fol- more severe depressions than patients with MDD only.
low-up. Thus, there may have been medication effects The most obvious explanation is that cortical lesions (as-
that were missed. Another limitation is that the number sociated with anxious depressions) in some way pro-
of follow-up patients who were initially diagnosed with duced more refractory depressions. We previously re-
GAD only or MDD only was small. Thus, the power of ported that patients who failed to recover from
our analysis was limited, and some significant effect of depression during the first 6 months following stroke
GAD may have been masked by this. In addition, mor- had mainly cortical lesion location.20 Feeney and Baron21
tality or failure to comply with follow-up evaluation led reported that cortical lesions produced long-lasting hy-
to some attrition at each follow-up (24% at short-term pometabolic areas of brain, distant from the site of the
and 29% at long-term follow-up). About 20% of this lesion. These distant effects may be more extensive and
study population died within the 2-year follow-up pe- persistent after cortical lesion than after subcortical le-
riod.19 sion and may lead to longer-lasting depressions. We pre-
The most surprising finding in this study was that viously found that depressed mood following stroke
neither GAD nor an interaction of GAD with MDD in- was associated with an increased risk of mortality over
fluenced cognitive impairment either in-hospital or dur- the first 10 years poststroke.19 These findings suggest
ing follow-up. The failure of GAD to worsen the im- that MDD plus GAD, and perhaps MDD only, may be
pairment did not support our original hypothesis. This associated with increased risk of mortality. However, it
finding also suggests that the mechanism of cognitive remains to be determined whether anxious depression
impairment associated with depression is not altered by has different survival probability than depression alone
or no mood disorder and whether this risk may be im-
comorbid anxiety disorder, implying perhaps the inde-
proved by treatment with anxiolytic or antidepressant
pendence of anxiety and depressive disorders. This find-
medications. Although depression appears to be the ma-
ing also supports our group designation of MDD plus
jor factor in cognitive and physical impairment follow-
GAD. It might be argued, however, that these are not
ing stroke, the intriguing therapeutic issue raised by this
comorbid disorders but rather are a type of anxious
study is whether anxiolytic treatment might improve
depression. This issue will require further research.
physical and psychosocial as well as emotional recovery
Perhaps the most significant finding was that patients from stroke.
with MDD plus GAD had greater impairment in activ-
ities of daily living at long-term follow-up than did pa- This work was supported in part by National Institute of
tients with MDD alone, and the course of recovery in Mental Health Grants MH40355 and Research Scientist
social functioning was significantly worse in patients Award MH00163 (R.G.R.) and a grant from the Nippon
with GAD plus MDD compared with control subjects or Medical School Department of Neuropsychiatry.

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40 VOLUME 10 NUMBER 1 WINTER 1998