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Isr J Psychiatry Relat Sci - Vol.

52 - No 1 (2015)

Social Anxiety Disorder Comorbid with
Schizophrenia: The Importance of Screening for
This Underrecognized and Undertreated Condition
Katherine Moss Lowengrub, MD, Rafael Stryjer, MD, Moshe Birger, MD, and Iulian Iancu, MD
Rehovot Mental Health Center, Rehovot and the Beer Yaakov Mental Health Center, Beer Yaakov, both affiliated with the Sackler School of
Medicine, Tel Aviv University, Ramat Aviv, Israel

Abstract
Background: While the presence of comorbid anxiety
disorders such as obsessive-compulsive disorder and
panic disorder have been well described in schizophrenia,
comorbid social anxiety disorder (SAD) has been less
emphasized. The goal of this study was to examine the
prevalence of SAD in our ambulatory population of
patients with schizophrenia.
Methods: A group of 50 outpatients with schizophrenia
randomly selected from our public mental health
outpatient population was evaluated with the Structured
Clinical Interview for DSM-IV (SCID)-schizophrenia
section, the Positive and Negative Syndrome Scale
(PANSS), the Schizophrenia Quality of Life Scale
(SQLS), the Liebowitz Social Anxiety Scale (LSAS) and
the Global Assessment of Functioning Scale (GAF). After
completion of assessments, a retrospective chart review
was conducted on all study patients who met criteria for a
diagnosis of SAD in order to determine how many of these
patients had been previously given a diagnosis of SAD.
Results: Based on a cutoff score of 29/30 on the total
LSAS score, 38% of our sample had a comorbid diagnosis
of SAD. Compared to patients who did not suffer from
comorbid SAD, patients with schizophrenia and comorbid
SAD had lower ratings of quality of life, but similar GAF
and PANSS scores. According to the results of the chart
review, none of the affected patients had been previously
diagnosed with SAD.
Conclusions: According to the results of our study, SAD as
a comorbid condition is highly prevalent in schizophrenia

Address for Correspondence:

40

and may be under-detected in the outpatient mental
health care setting. Furthermore, the presence of SAD
may lead to a decreased quality of life for patients with
schizophrenia. Further studies should evaluate whether
the diagnosis and treatment of comorbid SAD would
improve the treatment and quality of life of patients
with schizophrenia.

INTRODUCTION
While acute psychotic episodes in schizophrenia generally
respond well to treatment with antipsychotic medication,
the long-term course is characterized by marked impairment in social and occupational functioning (1). Our lack
of success in treating negative symptoms highlights the
need for aggressively treating comorbid psychiatric conditions. For example, the current standard of care during
the maintenance phase of treatment in schizophrenia is to
screen aggressively for concurrent alcohol and drug use,
for it is known that these conditions lead to a worsening
course in schizophrenia (2). The identification and treatment of comorbid medical and psychiatric conditions
in schizophrenia is critically important in preventing
relapse and optimizing quality of life.
It has long been recognized that anxiety disorders such
as obsessive-compulsive disorder, panic disorder and
post-traumatic stress disorder are common in schizophrenia, and multiple studies have demonstrated that
treatment of comorbid anxiety symptoms is associated

Iulian Iancu, MD, Yavne Mental Health Center, 6 Dekel Street, Yavne 81200 Israel

  iulian1@bezeqint.net

Fifty outpatients diagnosed with chronic schizophrenia (n= 45) or schizoaffective disorder (n= 5) were recruited in a random fashion from our public mental health outpatient clinic and were invited to participate in the study after giving written informed consent. it has been our impression that patients with schizophrenia in our large and demographically diverse outpatient population are not systematically screened for the presence of comorbid SAD. Consistent with views expressed by experts in the field.Katherine Moss Lowengrub et al. The study population consisted of 26 men and 24 women. alogia and avolition). Half of the patients had distinct paranoid features (significant paranoid ideation and paranoid delusions). Two studies with inpatients showed prevalence rates of 11-17% (9. mental retardation or severe dyslexia).23 (S. In the limited number of studies available to date. This is a statistical measure of drug consumption.D.D. = 13. The essential feature of SAD is a marked fear and avoidance of one or more social and/or public performance situations due to an excessive concern about being humiliated while under the scrutiny of others (5). 10). The mean number of friends was 1. increased rates of substance abuse and a decreased quality of life (6). Fourteen patients (28%) were taking adjunctive antidepressant medication at the time the study was conducted.D. Pallanti et al.3% (6-8). The symptom overlap between SAD and schizophrenia may result in missed diagnosis of comorbid SAD when positive symptoms mask SAD or SAD overdiagnosis if negative symptoms are prominent. The tendency of patients with SAD to suffer from shyness and avoidance may likewise be seen as part of a continuum with apathy and avolition that comprise negative symptom clusters (13). Two subtypes of SAD are recognized: a generalized type. Comorbid SAD in schizophrenia has been associated with more distress and disability.D. prevalence rates for comorbid SAD in outpatients with schizophrenia have ranged from 17-36.g. hallucinations) and negative symptoms (flat affect and emotions. and the working hypothesis of this study is that SAD is under-detected in schizophrenia. =0. Seven patients (14%) had made at least one suicide attempt 41 . Based on the premise that SAD is often underdiagnosed in schizophrenia because of confusion with negative symptoms. SAD shares common elements with positive and negative symptoms in schizophrenia. with an improved outcome in schizophrenia (2-4). The mean daily defined dose (D. in which a person fears most social or performance situations and a non-generalized type in which fears are typically limited to public speaking or few “performance” activities (5). comorbid substance abuse (during the preceding year) and lack of cooperation (e.000 residents. and years of education) and the type of antipsychotic agents used (11). All patients were receiving antipsychotic treatment at the time of the evaluation.no). (6) conducted the first comparison study between outpatients with schizophrenia and concluded that comorbid SAD was common and was strongly associated with increased disability.3 years (S. prevalence studies are in their preliminary stages with poor correlation between studies which might be accounted for by disparate treatment settings. METHODS: Sample: The study was approved by the local Institutional Review Board.7) with a minimum of 0 and maximum of 6 friends.42 (S. The mean age of the subjects was 45. due to the presence of psychotic symptoms or negativism). More recently. =11). The clinic is affiliated with Tel Aviv University and serves an ethnically diverse population in a catchment area of over 120. Neuropsychiatric studies and functional MRI studies have shown that patients with SAD tend to misinterpret neutral facial expressions as being threatening (12). Schizophrenia is characterized by positive symptoms (delusions. Inclusion criteria were a diagnosis of schizophrenia or schizoaffective disorder according to the Structured Clinical Interview for DSM-IV and age between 18 and 65. as well as other variables including the demographic make-up of the study (age. defined by the World Health Organization (http://www. socio-economic class. This misreading of social expression may be seen on a continuum with paranoia and ideas of reference. =1. the implications of comorbid Social Anxiety Disorder (SAD) in schizophrenia have begun to be addressed in the literature.) was 1.whocc. SAD patients are known to be very sensitive to the scrutiny of others which leads to guarded and withdrawn behavior.. organic brain disease (such as dementia. The mean duration of illness was 20. It is the assumed average maintenance dose per day for a drug used for its main indication in adults and also serves to compare drug use among patients taking different medications. Clearly. We aimed to determine the prevalence of SAD in a random cohort of our outpatients with schizophrenia.D.D. Patients treated with selective serotonin reuptake inhibitors (SSRI) or serotonin norepinephrine reuptake inhibitors (SNRI) were not excluded from the study.7).4 years (S. Exclusion criteria included difficulty with spoken and written Hebrew.4).

41.9) 1.7) 12.3 (13.1) p= 0. t=0.1) 53. 38% of our patients had a diagnosis of SAD (12 males and 7 females).). df=48 Number of Friends 1.3) p=0.2 (0. The Global Assessment of Functioning scale (GAF) (5).1) 12.54.I.092. t=-9.68.3) p=0. Based on a cutoff score of 29/30 on the total LSAS score.29 (8.44.2 (15.9(13.59. 5. Statistical analysis: The LSAS-SR questionnaire was used as a screening tool for the presence of SAD using a cutoff of 30 or more (indicating the presence of focused SAD).8 (8.63.007.6 (14.45 (1. df=48 D. We compared the characteristics of those with SAD and schizophrenia versus those with schizophrenia alone. between the “fear” subscale of the LSAS and positive symptoms. negative and general subscales. 3.19 (6.9) 29. Correlations were reviewed between the LSAS and PANSS.7) 1. t=-0. This is a numeric scale (0 through 100) used by mental health clinicians to rate subjectively the social and occupational functioning of adults.001. 42 Within the subset of study patients who met criteria for SAD.527.9) 51. t=-1.7 (9) (range 16-49) 32.553. 4.1 (23.7) p=0. whose objective is to assess the range of social interaction and performance situations which patients with SAD may fear and/or avoid.D.099.165.61.82.9) p=0.9) 52. df=48 PANSS total (range 35-100) 62. we examined whether this diagnosis had been previously detected by the treating psychiatrist and appeared in the patients’ files.68(5.8) 14.D. 10% of our sample had generalized SAD.D. whereas the LSAS and SQLS were in a self-report format. 52 Social .8 (9. df=48 Abbreviations: Liebowitz Social Anxiety Scale (LSAS).1 (4. t=-8.9 (6. All SCID assessments were performed by the last author (I. the Schizophrenia Quality of Life Scale (SQLS).3 (11) 20.) SAD Positive (n=19) Mean (S.D. Based on a cutoff score of the total LSAS score of 59/60. Although the higher cutoff score might be correlated with greater specificity in screening for SAD.8) p=0.7) p=0. the social fears were judged by the clinician to be neurotic (nonpsychotic). The two sub-samples had similar age.6) p=0. Results The scores on the various questionnaires are presented in Table 1.) Statistical Significance (df= degrees of freedom) Age (years) 45.4(10.4-3.4) 43. a structured tool for the diagnosis for schizophrenia (14). t=-0.1 (18.872.No 1 (2015) in the past.Vol. A secondary measure was for generalized SAD based on a score of 60 or more on the LSAS. and between the “avoidance” LSAS subscale and negative symptoms on the PANSS.7) 1.D.3 (0. 2. (range 0.23 (0. t=-1. Table 1 also presents the characteristics of those with and without SAD (based on a cutoff score of 29/30).7 (24. the Positive and Negative Syndrome Scale (PANSS).8) 67. Table 1. The GAF and the PANSS scores were rated by the clinicians. df=48 LSAS total (range 0-118) 27. df=48 SQLS (range 43-113) 78. The Schizophrenia Quality of Life Scale (SQLS) (17) is a practical and acceptable method of measuring self reported quality of life in people with schizophrenia. df=48 Duration of Illness (years) 20. The self-report version of the Liebowitz Social Anxiety Scale (LSAS-SR) (15).539.) SAD Negative (n=31) Mean (S.2) 18. the lower cutoff score was also found to predict non-generalized SAD (18.8) 46.4(13. The Positive and Negative Syndrome Scale (PANSS) (16) measuring symptom severity of patients with schizophrenia with positive.91.3) p<0. t=-1.84) 1.94 (9.9) p=0. Research instruments: Assessment tools included the following questionnaires: 1.2 (11. Global Assessment of Functioning scale (GAF) and Daily Defined Dose (DDD). Structured Clinical Interview for DSM-IV (SCID).16. Four patients (8%) abused drugs in the past and two (4%) abused alcohol in the past.939.7) 1.4 (10. gender distribution. t=0. df=48 GAF (range 35-75) 52. the specifier “generalized” is used in the DSM-IV to denote a subgroup of individuals who suffer from anxiety in most social and performance situations.1) 87.05 (7.8 (6. t=0. 19). Clinical characteristics of SAD positive (LSAS>30) and SAD negative subjects Variable Total sample (n=50) Mean (S.42 (1. df=48 PANSS positive (range 7-23) 13.07.7(16. As mentioned above. None of the patients with schizophrenia+ SAD were diagnosed as such by the treating psychiatrist.345.37 (1.09(3.Anxiety Disorder Comorbid with Schizophrenia Isr J Psychiatry Relat Sci .1) 20.7 (19) 59.5 (18. df=48 PANSS negative (range 7-39) 18. t=-2. .7) 73. df=48 PANSS general 30. This was done as follows: the distribution of gender and of those taking antidepressants in both groups was examined by chi square analyses and we used an analysis of t-test for independent samples for continuous variables.7) 20.3) p=0. In the majority of cases (78%).

The distinction between focused social anxiety and generalized social anxiety disorder is important.28 [p=0. p=0.024) and with the SQLS (r=0.037) and SQLS (r=0.3% and 23.D. PANSS total (r=0. Additionally. Our prevalence rate of 38% for comorbid SAD is consistent with that reported by both Pallanti et al. An additional finding was that paranoid patients had lower GAF scores (p=0. Discussion To date.31. p=0.. we found no significant difference between patients with and without comorbid SAD in terms of the GAF scores.001). 27) and. p=0. In the case of a chronic patient who refuses to go to a vocational rehabilitation program. p<0. the association between social anxiety symptoms and a lower subjective quality of life suggests that it is clinically important to recognize the presence of social anxiety.22). ideas of reference) and negative symptoms (social withdrawal) which are inherent in the disease process of schizophrenia. The LSAS (total score) correlated significantly with the PANSS general psychopathology subscale (r=0. However. therefore. such as patient selection and choice of screening tools for SAD (SCID vs LSAS-SR). A major question in this field is that of the ability to differentiate SAD symptoms from positive symptoms (i.7-25% (9. that a lower subjective quality of life might lead to the development of social anxiety symptoms (25). degrees of freedom=1). this issue is far from simple. Accordingly. Whereas some authors conclude that social anxiety may lead to a decreased quality of life (6). we note that the mean GAF score for both cohorts (with and without SAD) was in the low end of the moderate range showing that all patients had relatively poor functioning. experts generally agree that the distinction between comorbid SAD and symptoms related to the natural course of schizophrenia is challenging. 24). respectively) was not significant (chi square = 1. in their studies of chronic ambulatory patients where prevalence rates were 36.e. p=0. patients with schizophrenia with SAD had a lower overall quality of life (see Table 1). This difference in gender distribution (37% females vs 55%. While the results of our study show that SAD is associated with an impaired quality of life.529.016).046] and SQLS [r=0.Katherine Moss Lowengrub et al. (25). Subjects with schizophrenia and SAD had a lower quality of life (the SQLS score is inversely correlated with quality of life). only a handful of studies have examined the prevalence rates of comorbid SAD in ambulatory patients with schizophrenia. 10. the risk of underdiagnosing anxiety factors is increased.29. One explanation for this finding is that the GAF provides a relatively rough estimate of the overall severity of psychiatric symptoms and may not be sensitive enough to detect variances in functioning within a group of patients afflicted with schizophrenia. (8) who found comorbid SAD in 17% of outpatients (n=53) with schizophrenia. df=1. they point out that recent criteria for remission in schizophrenia mainly rely on psychotic symptoms (26. p=1. The subjects with schizophrenia and SAD took antidepressant medications in a similar proportion as the subjects with schizophrenia (26% vs 29%. for example in community-dwelling patients with remitted schizophrenia. These different rates may be due to the difficulty of administering screening instruments to patients who are not clinically stable and are paranoid. 23). These authors maintain that anxiety symptoms are often under-diagnosed because clinicians usually pay more attention to psychotic symptoms.34. The results of our study show that 38% of our patients met criteria for SAD (based on a score of 30 or greater on the LSAS) and that 10% of our patients met criteria for generalized SAD (based on a score of 60 or greater on the LSAS). several recent studies have examined the prevalence of SAD in acutely hospitalized schizophrenic patients with prevalence rates ranging from 5. duration of illness. The group with schizophrenia and SAD included 12 males and 7 females.01). and Tibbo et al. due to life’s hardships and a lack of social communication skills.48. Consistent with data presented by Pallanti et al.47. In addition. 21). it is mandatory 43 .3%. as the generalized form is associated with greater disability [20]. No significant correlations were found between LSAS fear subscale and positive PANSS and between LSAS avoidance subscale and PANSS negative. p=0. number of friends and D. respectively (6.D. whereas the group with schizophrenia alone included 14 males and 17 females. We note that our prevalence is higher than that reported by Braga et al.017). Contrary to our expectations. According to Kumazaki et al. The lower rate reported by Braga may relate to differences in study variables. Correlations: We found significant Pearson correlations between LSAS Fear subscale and PANSS general psychopathology subscale (r=0. chi square =0. and also between LSAS avoidance subscale and PANSS general psychopathology subscale (r=0. paranoia. (6).001]).45. others maintain. p=0. Likewise several studies among first-episode patients have reported rates between 25-32% (22.043. a clear finding of our study was that relative to patients without comorbid SAD.

going to job interviews or using a public restroom). support findings by Pallanti et al. therefore. However. although we note that their study examined a cohort of acutely ill patients in which prominent positive symptoms may confound the assessment of SAD. the results of our study may not generalize to a more diverse population including first episode patients. 19). patients with schizophrenia and comorbid SAD had similar rates of negative and positive symptoms (see Table 1). and. 28. While these authors suggest that existing cutoff scores on these measures may not be appropriate for psychotic individuals. although both LSAS scales have been shown to be equivalent in several studies (18. We note that this failure to detect comorbid SAD occurred in a university-affiliated clinical setting which is staffed by experienced senior psychiatrists. its cause is unclear. the results of our study show that compared to patients who did not suffer from comorbid SAD. which is related to novelty seeking and exploratory behaviors. (11) reported that anti-dopaminergic drugs cause SAD symptoms in a higher rate than expected. 22). or rather a medication-induced side effect? Schizophrenia is associated with excessive dopamine activity. Another limitation may be the relative homogeneity of our sample which was composed primarily of patients with chronic schizophrenia. We have provided a synopsis of screening techniques for SAD. screening for SAD in outpatients with schizophrenia may be best accomplished by asking if the patient has a fear of embarrassment or has avoidance in particular social situations (eating in public. We propose that several clinician-related variables contributed to the failure to correctly diagnose the comorbid SAD in our study population including: 44 1) a lack of knowledge of the high prevalence rates of comorbid SAD in schizophrenia. Patients with schizoaffective disorder. Furthermore. While the comorbidity rate in our study is much higher than chance alone. We conclude that a failure to systematically screen for comorbid SAD in schizophrenia leads to underdetec- . 3) lack of knowledge regarding screening procedures. Seedat et al. therefore. the patient with comorbid SAD is generally motivated to gain control of the anxiety symptoms. Is it a result of the fear of stigma and rejection while having a mental disorder or due to a common biological underpinning.Anxiety Disorder Comorbid with Schizophrenia Isr J Psychiatry Relat Sci . however. 29). For example.Vol. The inclusion of patients with schizoaffective disorder in our study population may also be considered as a limitation of our study. The inclusion of patients medicated with antidepressant medication may have biased the results. 52 Social . comprised only a minority of the sample. we note that the MINI also is problematic due to its brevity and the possibility that it arouses dissimulation and denial in persons with psychosis. In concordance with current studies (6. (6) and Michail and Birchwood (22) that social anxiety appears to be unrelated to the presence of clinical psychotic symptoms. (24) observed the low agreement between the Mini International Neuropsychiatric Interview (MINI) and a diagnosis of anxiety disorders on symptom status measures. whereas avoidant behavior due to negative symptoms is typically accompanied by impaired motivation to change. and 4) the tendency (bias) among clinicians to attribute poor social functioning to negative symptoms without exploring other comorbid conditions. The patient with comorbid SAD complicating schizophrenia will experience the avoidant behavior as ego-dystonic and therefore qualitatively different from avoidant behavior due to anhedonia or lack of social interest. the diagnosis of comorbid SAD had been missed in every affected patient. the validity and ease of administration of these tools in patients with schizophrenia deserves further study. We note that user-friendly selfreport instruments (such as the Mini-SPIN) are available for identifying SAD in the managed care setting and appear to distinguish between the generalized and nongeneralized subtypes (19. In our opinion. for the presence of affective symptoms may represent a confounding variable in the assessment of SAD. Furthermore.No 1 (2015) to discern whether his behavior results from fears that spies will attack him (positive symptoms). for the pharmacotherapy may have masked symptoms of SAD although we attempted to conduct our study under naturalistic conditions. Mazeh et al. (9) concluded that it is difficult to differentiate SAD from positive symptoms. the use of the LSAS-SR to screen for the presence of SAD (in contrast to the clinicianadministered LSAS and the SCID) may have possibly decreased the reliability of our results. for the core features of SAD are a fear of embarrassment and an intense apprehension about being negatively evaluated by others which lead to social avoidance. Our results. Introversion and social anxiety are related to decreased dopamine levels (30) and indeed Pallanti et al. for an important finding of our study was that according to the results of the retrospective chart review. A limitation of our study is the small sample size. 2) failure to appreciate the clinical relevance and additional morbidity conferred by the presence of SAD in schizophrenia. avolition (negative symptoms) or fears that in the rehabilitation center he will sweat excessively and therefore will be mocked and will feel embarrassed (possibly SAD).

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