Frequency of Social Phobia and Psychometric Properties of theLiebowitz Social Anxiety Scale in Parkinson’s Disease

Arthur Kummer, MD, Francisco Cardoso, MD, PhD, and Antonio L. Teixeira, MD, PhD*

Movement Disorders Clinic, Department of Internal Medicine, School of Medicine,Federal University of Minas Gerais (UFMG), Belo Horizonte, Brazil

Abstract: There are few studies about social anxiety disorderin Parkinson’s disease (PD). The objective of this study was toassess its frequency and to explore the psychometric propertiesof the Liebowitz social anxiety scale (LSAS) in PD. Ninetypatients with PD underwent neurologic and psychiatric exami-nation. Psychiatric examination was composed by a structuredclinical interview (MINI-Plus) followed by the application ofthe LSAS, the Hamilton depression rating scale (Ham-D), andthe Hamilton anxiety rating scale (Ham-A). Neurologic exami-nation included the MMSE, the UPDRS, the Hoehn-YahrScale, and the Schwab-England scale of activities of daily liv-ing. Social phobia was diagnosed in 50% of PD patients. The

disorder was not associated with any sociodemographic or neu-rological feature, but was associated to major depression (P 50.023), generalized anxiety disorder (P 5 0.023), and obses-sive-compulsive disorder (P 5 0.013). The score of LSAS cor-related positively with the scores of Ham-D and Ham-A (P <0.001 for both). A ROC curve analysis of the LSAS suggestedthat a cutoff score in 41/42 provided the best balance betweensensitivity and specificity. This disorder seems to be more com-mon and not just restricted to performance as previouslythought. � 2008 Movement Disorder SocietyKey words: Parkinson’s disease; social anxiety disorder;

social phobia; Liebowitz social anxiety scale

Some psychiatric disorders, such as depression and

generalized anxiety disorder, occur in Parkinson’s dis-

ease (PD) in a higher frequency than in general popu-

lation. However, just few studies investigated the fre-

quency of social anxiety disorder (i.e. social phobia) in

PD. One reason may be that DSM-IV excludes this di-

agnosis if anxiety is related to a general medical condi-

tion. Moreover, DSM-IV gives the supposed social fear

in PD due to its tremor as an example of a medical

condition which should not receive the diagnosis of

social phobia. However, it seems that PD patients may

have a more diffuse social anxiety unrelated to, and

sometimes even predating, motor symptoms.1 Thus,

these restrictive operational criteria may impair its rec-

ognition in PD, compromising its proper management.

In general population, studies reveal that social anxi-

ety disorder is the most frequent anxiety disorder, usu-

ally has an early onset, and is often associated with se-

rious effects on role functioning and quality of life.2,3

The disorder impairs social interaction; may lead to

psychological (e.g. depression and alcohol abuse) and

physical (e.g. cardiovascular) disorders; interferes with

occupational activities and with help-seeking.3 Those

subjects rarely seek professional help and most of the

time it is underrecognized and underestimated by clini-

cians.2,3 In PD, despite the lack of controlled and with

a sizeable cohort studies, previous studies suggested

that this disorder is also extremely prevalent.1,4,5

The objective of this study is to investigate the frequency

of social anxiety disorder and the psychometric properties

of the Liebowitz social anxiety scale (LSAS) in PD.

PATIENTS AND METHODS

A cross-sectional study was performed with 90

patients with PD (M/F: 54/36) recruited from the

No potential conflict of interest.

*Correspondence to: Dr. Antonio Lucio Teixeira, Departamento deClınica Medica, Faculdade de Medicina, UFMG. 30130-100 Av.Prof. Alfredo Balena, 190. Santa Efigenia, Belo Horizonte, Brazil.E-mail: altexr@gmail.com

Received 15 March 2008; Revised 30 April 2008; Accepted 17June 2008

Published online 25 July 2008 in Wiley InterScience (www.

interscience.wiley.com). DOI: 10.1002/mds.22221

1739

Movement DisordersVol. 23, No. 12, 2008, pp. 1739–1743� 2008 Movement Disorder Society

Movement Disorders Clinic of the School of Medicine

of the Federal University of Minas Gerais (UFMG),

Brazil. PD was diagnosed according to the United

Kingdom Parkinson’s Disease Society Brain Bank clin-

ical diagnostic criteria.6 Exclusion criteria were as fol-

lows: previous neurosurgery, other neurologic disorder

or delirium, and dementia. Dementia was diagnosed

according to DSM-IV diagnostic criteria7 and to the

score obtained in the Folstein’s mini-mental state ex-

amination (MMSE)8 adapted for the Brazilian elderly

population.9 Delirium was diagnosed according to

DSM-IV diagnostic criteria,7 during the neurological

examination.

Patients underwent a psychiatric interview and a

neurologic examination. A semistructured interview

was initially performed to obtain demographic and

clinical data. Psychiatric interview was composed by a

structured psychiatric interview (MINI-Plus) and by

the administration of psychometric scales assessing

phobic, anxious, and depressive symptoms. The scales

used in this study were the LSAS,10 the Hamilton anxi-

ety rating scale (Ham-A),11 and the Hamilton depres-

sion rating scale of 24 items (Ham-D).12

The MINI-Plus is an internationally validated short-

structured diagnostic psychiatric interview.13 All sec-

tions of the instrument were administered. Although

Mini-Plus was developed for DSM-IV psychiatric diag-

nosis, there are some discordant points. For instance,

the MINI-Plus does not have the exclusion criteria for

somatic disease, use of substances or mental disorder

as a cause of social anxiety disorder. Thus, the instru-

ment is of special usefulness if an inclusive approach

is desirable as in the present study. Also, whereas the

MINI-Plus diagnoses a 30-day social phobia, the

DSM-IV simply states that symptoms should be ‘‘per-

sistent" not specifying the time period. Furthermore,

MINI-Plus considers social phobia as generalized if the

patient fear or avoid four or more social situations,

while DSM-IV characterizes the generalized subtype

just by fear of most social situations.

LSAS was one of the first scales to evaluate social

phobia.10 It has 24 items divided in two subscales that

assess situations of performance (13 items) and of

social interaction (11 items) that people with social

phobia tend to fear or avoid. The original scale evalu-

ates these items in a Likert-type scale (0–3) and has

two factors: anxiety and avoidance. Thus, LSAS pro-

vides six subscales scores: total anxiety, anxiety of

social interaction, anxiety of performance, total avoid-

ance, avoidance of social interaction, and avoidance of

performance. Their psychometric properties are satis-

factory and have been also internationally validated.14

However, the LSAS has not been previously used or

validated in PD. The Ham-D and Ham-A are also

instruments commonly used to assess depressive and

anxious symptoms in scientific and clinical settings.

Neurologic examination included the mini-mental

status examination, the Unified Parkinson’s Disease

Rating Scale (UPDRS), the Hoehn-Yahr Scale (HY),

and the Schwab-England scale of activities of daily liv-

ing (SES). All the psychiatric and neurologic assess-

ment was conducted by only one psychiatrist (AK) and

one neurologist (ALT) with PD patients in the on-med-

ication state.

Comparisons of categorical data among the groups

of patients with and without social phobia were exe-

cuted using the v2 and the Fisher’s exact tests. For

continuous variables, Student’s t-test was performed

when variables had a normal distribution. When con-

tinuous variables had a nonparametric distribution,

Mann-Whitney U tests were carried out. Correlation

between scales was calculated using Spearman’s q. AllP-values were two-tailed and a significance level of

0.05 was chosen. Statistical analyses were performed

using SPSS v15.0 and MedCalc v8.0 softwares.

This study was approved by the local ethics commit-

tee, and all subjects gave their informed consent.

RESULTS

Patients had a mean age of 56.9 6 10.3 years, a

mean age of PD onset of 48.2 6 10.9 years, and a

mean disease length of 8.7 6 4.9 years. Neurologic ex-

amination showed that patients had a mean UPDRS of

49.4 6 25.4, a median HY of 2 (range 1–4), and a

mean SES of 81.5 6 13.0%. The diagnosis of 30-day

social phobia was performed in 50% of PD patients.

Ten patients had the nongeneralized subtype (11.1%),

while 35 (38.9%) had generalized social phobia. Social

phobia was not associated with gender, age, age of dis-

ease onset, and disease length. The mean UPDRS

score, HY stage, and SES score did not differ between

patients with or without social phobia. The relationship

between social phobia and other mood and anxiety dis-

orders are shown in Table 1. Patients with social pho-

bia scored higher in Ham-D (P 5 0.010) and in Ham-

A (P 5 0.004). When considered separately, social

phobia subtypes did not associate with other anxiety or

mood disorders.

Eight (17.8%) of the 45 patients with social phobia

had no DSM-IV Axis I disorder; three (6.7%) of them

had OCD as the only Axis I comorbidity; six (13.3%)

had other anxiety disorders such as specific phobia or

generalized anxiety disorder; and 28 (62.2%) had

1740 A. KUMMER ET AL.

Movement Disorders, Vol. 23, No. 12, 2008

depressive disorders (major depression and dysthymia),

frequently associated with other anxiety disorders. The

psychoactive medications used by patients with and

without social anxiety disorder are shown in Table 2.

As expected, the diagnosis of social phobia accord-

ing to the structured clinical interview associated with

higher scores in LSAS and in all its subscales, as

shown in Table 3. The score of LSAS correlated posi-

tively with the scores of Ham-D (q 5 0.51; P <0.001) and Ham-A (q 5 0.55; P < 0.001). For screen-

ing social anxiety disorders in clinical settings, it has

been previously proposed a cutoff score of 29/30 and

59/60 in the LSAS, respectively, for the nongeneral-

ized and the generalized subtypes.15 According to these

criteria, 31 patients (34.4%) had the nongeneralized

subtype of social phobia (i.e. scored between 30 and

60), and 32 patients (35.6%) had the generalized sub-

type. Of note, the referred study used the subjective

DSM-IV criteria to discriminate subtypes of social

phobia, namely, that the generalized subtype character-

izes by fear of most situations.15

Using the proposed cutoff point of 29/30, LSAS

diagnosed as socially anxious 70% of the sample, pro-

viding a sensitivity of 86.7% and a specificity of

42.9%. If the adjusted higher cutoff was used (59/60),

LSAS diagnosed 36.8% of the sample as socially anx-

ious, and provided a sensitivity of 53.3% and a speci-

ficity of 80.9%. However, a ROC curve analysis sug-

gested that a cutoff score of 41/42 provided the best

balance between sensitivity and specificity in this sam-

ple. This cutoff score provided a sensitivity of 77.8%,

a specificity of 64.3%, a positive predictive value of

68.5%, and a negative predictive value of 74.3%, with

an area under the curve of 0.767 (Fig. 1).

DISCUSSION

More than two decades ago, Liebowitz et al. alerted

that, despite the increased attention to most of anxiety

disorders, social phobia was still neglected.16 Unfortu-

nately, their criticism remains actual, at least for PD.

Frequency of anxiety disorders was already known to

be higher in PD than in general population,17 but data

concerning social anxiety disorder were scarce.

In general population, life-time and 30-day preva-

lence estimates of social phobia are 13.3 and 4.5%,

respectively.2 Adopting an inclusive approach, we have

showed that half of patients with PD may suffer from

social anxiety disorder. The frequency of social phobia

in our study was higher than the few previous ones.

The reasons may include differences in diagnostic cri-

teria, in instruments used, and in sample characteristics

(e.g. exclusion of demented patients and an unusually

low mean age of onset). It should be highlighted that

TABLE 1. Frequency of mood and anxiety disorders inParkinson’s disease patients (n 5 90) with and without

social phobia

With socialphobia(n 5 45)

Without socialphobia(n 5 45) P value

Major depressiona 19 (42.2%) 9 (20.0%) 0.023Dysthymiaa 9 (20.0%) 4 (8.8%) 0.134Generalized anxiety

disordera19 (42.2%) 9 (20.0%) 0.023

Panic disorderb 5 (11.1%) 1 (2.2%) 0.203Obsessive-compulsive

disordera10 (22.2%) 2 (4.4%) 0.013

av2 test.bFisher’s exact test.

TABLE 2. Psychoactive medications used by patients withand without social phobia

With socialphobia(n 5 45)

Without socialphobia(n 5 45) P value

L-Dopaa 29 (64.4%) 32 (71.1%) 0.499Dopaminergic agonistsa 23 (51.1%) 19 (42.2%) 0.398Anticholinergic drugsa 19 (42.2%) 22 (48.9%) 0.525Amantadinea 20 (44.4%) 9 (20%) 0.013COMT inhibitorsb 2 (4.4%) 2 (4.4%) 1.000Antidepressantsa,c 15 (33.3%) 18 (40.0%) 0.512Benzodiazepinesa 11 (24.4%) 4 (8.9%) 0.048Valproic acidb 2 (2.2%) 0 (0.0%) 1.000Clozapineb 0 (0.0%) 2 (4.4%) 0.494

av2 test.bFisher’s exact test.cAntidepressants in use: tricyclic (23), selective serotonin reuptake

inhibitor (8), serotonin and noradrenalin reuptake inhibitor (2).

TABLE 3. Comparison of mean scores of Liebowitz socialanxiety scale (LSAS) and of its subscales between

Parkinson’s disease patients (n 5 90) with and withoutsocial phobia

With socialphobia(n 5 45)

Withoutsocialphobia(n 5 45) P value

LSAS total 66.4 6 28.8 36.9 6 29.4 <0.001Total anxiety 34.7 6 14.9 20.0 6 15.0 <0.001Anxiety of performance 20.1 6 8.8 11.9 6 8.1 <0.001Anxiety of social

situations14.5 6 7.1 8.1 6 7.5 <0.001

Total avoidance 31.8 6 14.7 16.8 6 15.1 <0.001Avoidance of performance 18.8 6 8.8 10.2 6 8.3 <0.001Avoidance of social

situations13.0 6 7.3 6.6 6 7.2 <0.001

1741SOCIAL ANXIETY DISORDER IN PD

Movement Disorders, Vol. 23, No. 12, 2008

Mini-Plus does not take into consideration that the

phobic symptoms could be accounted for by a disease

or by a mental disorder. According to the DSM-IV cri-

teria, a diagnosis of social anxiety disorder is inad-

equate if the fear is due to or related to a general med-

ical condition or a mental disorder. Although this could

reduce the estimation of social anxiety disorder in this

group of patients, it should be considered that patients

with social anxiety have frequent comorbid disorders,

notably mood and anxiety disorders.15

Stein et al. studied 24 nondemented PD patients and

found a frequency of 16.6% of social phobia.1 These

authors excluded from the group of anxious patients

three subjects who had significant social anxiety but

their symptoms were judged to be secondary to worries

about their parkinsonian symptoms being visible to

others. If Stein et al. had adopted an inclusive

approach, the frequency of social phobia in their sam-

ple would raise to 29.2%. Lauterbach and Duvoisin

examined 38 patients with familial parkinsonism and

reported a frequency of 5.3% of social phobia.4,5 The

authors also excluded 5 patients with ‘‘embarrassment’’

about their parkinsonism which would raise the fre-

quency of social phobia to 18.4%.4 Most of the phobic

symptoms preceded the PD onset. Of note, none of the

demented patients of this sample had social phobia.5

In our study, the presence of social anxiety disorder

was not associated with any sociodemographic or clini-

cal data, including severity of motor symptoms. Social

anxiety seemed to be more generalized and not just re-

stricted to performance situations (nongeneralized sub-

type) as one could hypothesize taking into account PD

motor symptoms. Interestingly, the proportion of

patients with the generalized subtype of social anxiety

disorder in our sample (77.8% of patients with the dis-

order) was higher to what is expected in the general

population, namely, about half the prevalence of social

phobia for each subtype.18 Altogether, despite the fact

that it was not possible to investigate adequately if

social phobia predates or not the onset of PD, these

data suggest that this disorder is not a reaction to

motor impairment.

Patients with social phobia also had higher fre-

quency of other anxiety disorders and major depres-

sion, and scored higher in scales measuring the sever-

ity of these symptoms. In addition, the LSAS, Ham-D

and Ham-A correlated positively, suggesting that the

greater the phobic symptoms, the more severe are the

anxiety and depressive symptoms. The higher propor-

tion of patients with social anxiety using benzodiaze-

pines might be related to these data. As expected,

patients with social phobia scored higher in LSAS and

in all its subscales, but patients without social phobia

also had high scores in this scale supporting the hy-

pothesis that the cutoff score for social phobia in PD

must be higher. The cut-off score should be adjusted

depending on one’s particular purpose. If the correct

identification of positive cases is more important, then

sensitivity should be emphasized. Otherwise, when a

genuinely homogeneous population for study is

requested, specificity is to be emphasized. In our sam-

ple, the best balance between sensitivity and specificity

was achieved with the cutoff score of 42. Different

cut-off scores for the nongeneralized and the general-

ized subtypes (29/30 and 59/60 respectively) have been

suggested.15 LSAS was designed to dimensionally

assess the phobic symptoms. Someone with mild but

diffuse symptoms may present a score similar to some-

one with impairing symptoms restricted to performance

situations. Therefore, care should be taken while using

LSAS as a screening or diagnostic tool. In addition, it

is more important and reliable to screen for a disorder

than for its subtypes.

Some limitations of the present study should be

mentioned. First, the study was conducted in a tertiary

center where patients with already known complica-

tions, including psychiatric disorders, are referred to.

Second, there are limitations intrinsic to the instru-

ments and methods used. It is a relevant issue whether

social anxiety disorder occurred before or after the

FIG. 1. ROC curve of the Liebowitz social anxiety scale.

1742 A. KUMMER ET AL.

Movement Disorders, Vol. 23, No. 12, 2008

onset of PD. However, although the Mini-Plus does

question when the patient started to fear social situa-

tions, it does not mean that Mini-Plus is capable to

diagnose life-time social anxiety disorder. Actually,

there is dissociation between the existence of phobic

symptoms and the diagnosis of social phobia. In our

study, there were some patients who scored extremely

high in LSAS, but paradoxically stated that their symp-

toms were not impairing or distressful. Furthermore,

most patients could not precise when they started to

fear social situations.

On the other hand, it should be pointed out that the

strengths of the present study are the considerably

large cohort of nondemented patients, the use of inter-

nationally validated instruments to assess a range of

related psychiatric disorders, and the fact that the

patients were blindly assessed by a single neurologist

and a single psychiatrist.

This study provides additional evidence that patients

with PD have an increased risk of social anxiety disor-

der. As occurs in general population, this disorder in

PD is frequently associated with other depressive and

anxiety disorder. Social phobia was not associated with

severity of motor symptoms, and seemed to be not re-

stricted to embarrassment or worries about them. Thus,

neurobiological changes, which usually start years

before the onset of motor symptoms, may account for

the increased rates of psychiatric disorders, including

social phobia. Clinicians who treat patients with PD

must be aware of these findings as patients with social

phobia rarely expose their phobic complaints. Other-

wise, social phobia will remain in the shadow of other

anxiety disorders.

Acknowledgments: This investigation was partly fundedby Conselho Nacional de Desenvolvimento Cientıfico e Tec-nologico (CNPq, Brazil) and Fundacao de Amparo a Pesquisado Estado de Minas Gerais (FAPEMIG, Brazil).

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