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Isr J Relat Sci - Vol. 52 - No 1 (2015) Social Disorder Comorbid with : The Importance of for This Underrecognized and Undertreated Condition

Katherine Moss Lowengrub, MD, Rafael Stryjer, MD, Moshe Birger, MD, and Iulian Iancu, MD

Rehovot Mental Center, Rehovot and the Beer Yaakov Center, Beer Yaakov, both affiliated with the Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Israel

and may be under-detected in the outpatient mental Abstract setting. Furthermore, the presence of SAD Background: While the presence of comorbid anxiety may lead to a decreased quality of life for patients with disorders such as obsessive-compulsive disorder and schizophrenia. Further studies should evaluate whether disorder have been well described in schizophrenia, the diagnosis and treatment of comorbid SAD would comorbid disorder (SAD) has been less improve the treatment and quality of life of patients emphasized. The goal of this study was to examine the with schizophrenia. 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 Scale INTRODUCTION (PANSS), the Schizophrenia Quality of Life Scale While acute psychotic episodes in schizophrenia generally (SQLS), the Liebowitz Social Anxiety Scale (LSAS) and respond well to treatment with , the Global Assessment of Functioning Scale (GAF). After the long-term course is characterized by marked impair- completion of assessments, a retrospective chart review ment in social and occupational functioning (1). Our lack was conducted on all study patients who met criteria for a of success in treating negative symptoms highlights the diagnosis of SAD in order to determine how many of these need for aggressively treating comorbid psychiatric condi- patients had been previously given a diagnosis of SAD. tions. For example, the current standard of care during the maintenance phase of treatment in schizophrenia is to Results: Based on a cutoff score of 29/30 on the total screen aggressively for concurrent and drug use, LSAS score, 38% of our sample had a comorbid diagnosis for it is known that these conditions lead to a worsening of SAD. Compared to patients who did not suffer from course in schizophrenia (2). The identification and treat- comorbid SAD, patients with schizophrenia and comorbid ment of comorbid medical and psychiatric conditions SAD had lower ratings of quality of life, but similar GAF in schizophrenia is critically important in preventing and PANSS scores. According to the results of the chart relapse and optimizing quality of life. review, none of the affected patients had been previously It has long been recognized that anxiety disorders such diagnosed with SAD. as obsessive-compulsive disorder, and Conclusions: According to the results of our study, SAD as post-traumatic disorder are common in schizo- a comorbid condition is highly prevalent in schizophrenia phrenia, and multiple studies have demonstrated that treatment of comorbid anxiety symptoms is associated

Address for Correspondence: Iulian Iancu, MD, Yavne Mental Health Center, 6 Dekel Street, Yavne 81200 Israel [email protected]

40 Katherine Moss Lowengrub et al. with an improved outcome in schizophrenia (2-4). More with views expressed by experts in the field, it has been our recently, the implications of comorbid Social Anxiety impression that patients with schizophrenia in our large Disorder (SAD) in schizophrenia have begun to be and demographically diverse outpatient population are addressed in the literature. The essential feature of SAD not systematically screened for the presence of comorbid is a marked and avoidance of one or more social SAD, and the working hypothesis of this study is that and/or public performance situations due to an excessive SAD is under-detected in schizophrenia. We aimed to concern about being humiliated while under the scrutiny determine the prevalence of SAD in a random cohort of others (5). Two subtypes of SAD are recognized: a of our outpatients with schizophrenia. generalized type, in which a person most social or performance situations and a non-generalized type in which fears are typically limited to public speaking or METHODS: few “performance” activities (5). Sample: The study was approved by the local Institutional Based on the premise that SAD is often under- Review Board. Fifty outpatients diagnosed with chronic diagnosed in schizophrenia because of with schizophrenia (n= 45) or (n= 5) negative symptoms, Pallanti et al. (6) conducted the first were recruited in a random fashion from our public men- comparison study between outpatients with schizophrenia tal health outpatient clinic and were invited to participate and concluded that comorbid SAD was common and in the study after giving written informed consent. The was strongly associated with increased . In the clinic is affiliated with Tel Aviv University and serves an limited number of studies available to date, prevalence ethnically diverse population in a catchment area of over rates for comorbid SAD in outpatients with schizophre- 120,000 residents. Inclusion criteria were a diagnosis of nia have ranged from 17-36.3% (6-8). Two studies with schizophrenia or schizoaffective disorder according to inpatients showed prevalence rates of 11-17% (9, 10). the Structured Clinical Interview for DSM-IV and age Clearly, prevalence studies are in their preliminary stages between 18 and 65. Exclusion criteria included difficulty with poor correlation between studies which might be with spoken and written Hebrew, organic accounted for by disparate treatment settings, as well as (such as , mental retardation or severe dyslexia), other variables including the demographic make-up of the comorbid (during the preceding year) study (age, socio-economic class, and years of education) and lack of cooperation (e.g., due to the presence of and the type of antipsychotic agents used (11). psychotic symptoms or negativism). Patients treated Schizophrenia is characterized by positive symptoms with selective reuptake inhibitors (SSRI) or (, ) and negative symptoms (flat serotonin norepinephrine reuptake inhibitors (SNRI) affect and emotions, and ). SAD shares were not excluded from the study. common elements with positive and negative symptoms The study population consisted of 26 men and 24 in schizophrenia. Neuropsychiatric studies and functional women. The mean age of the subjects was 45.4 years (S.D. MRI studies have shown that patients with SAD tend to = 13.4). The mean duration of illness was 20.3 years (S.D. misinterpret neutral facial expressions as being threatening =11). All patients were receiving antipsychotic treatment (12). This misreading of social expression may be seen on at the time of the evaluation. The mean daily defined dose a continuum with and ideas of reference. SAD (D.D.D.) was 1.23 (S.D. =0.7). This is a statistical mea- patients are known to be very sensitive to the scrutiny of sure of drug consumption, defined by the World Health others which leads to guarded and withdrawn behavior. Organization (http://www.whocc.no). It is the assumed The tendency of patients with SAD to suffer from average maintenance dose per day for a drug used for its and avoidance may likewise be seen as part of a continuum main indication in adults and also serves to compare drug with and avolition that comprise negative symptom use among patients taking different . clusters (13). The symptom overlap between SAD and The mean number of friends was 1.42 (S.D. =1.7) schizophrenia may result in missed diagnosis of comorbid with a minimum of 0 and maximum of 6 friends. Half SAD when positive symptoms mask SAD or SAD over- of the patients had distinct paranoid features (significant diagnosis if negative symptoms are prominent. paranoid ideation and paranoid delusions). Comorbid SAD in schizophrenia has been associated Fourteen patients (28%) were taking adjunctive anti- with more distress and disability, increased rates of sub- medication at the time the study was conducted. stance abuse and a decreased quality of life (6). Consistent Seven patients (14%) had made at least one attempt

41 Isr J Psychiatry Relat Sci - Vol. 52 So- Nocial 1 (2015) Comorbid with Schizophrenia in the past. Four patients (8%) abused drugs in the past Within the subset of study patients who met crite- and two (4%) abused alcohol in the past. ria for SAD, we examined whether this diagnosis had been previously detected by the treating and Research instruments: Assessment tools included the appeared in the patients’ files. following questionnaires: 1. Structured Clinical Interview for DSM-IV (SCID), a structured tool for the diagnosis for schizophrenia Results (14), All SCID assessments were performed by the The scores on the various questionnaires are presented last author (I.I.). in Table 1. In the majority of cases (78%), the social 2. The -report version of the Liebowitz Social Anxiety fears were judged by the clinician to be neurotic (non- Scale (LSAS-SR) (15), whose objective is to assess the psychotic). Based on a cutoff score of 29/30 on the total range of social interaction and performance situations LSAS score, 38% of our patients had a diagnosis of SAD which patients with SAD may fear and/or avoid. (12 males and 7 females). Based on a cutoff score of the 3. The Positive and Negative Syndrome Scale (PANSS) total LSAS score of 59/60, 10% of our sample had gen- (16) measuring symptom severity of patients with eralized SAD. None of the patients with schizophrenia+ schizophrenia with positive, negative and general SAD were diagnosed as such by the treating psychiatrist. subscales. Table 1 also presents the characteristics of those with 4. The Schizophrenia Quality of Life Scale (SQLS) (17) and without SAD (based on a cutoff score of 29/30). The is a practical and acceptable method of measuring self two sub-samples had similar age, gender distribution, reported quality of life in people with schizophrenia. Table 1. Clinical characteristics of SAD positive (LSAS>30) and 5. The Global Assessment of Functioning scale (GAF) SAD negative subjects (5). This is a numeric scale (0 through 100) used by Total SAD SAD Statistical mental health clinicians to rate subjectively the social sample Positive Negative Significance and occupational functioning of adults. (n=50) (n=19) (n=31) (df= degrees Variable Mean (S.D.) Mean (S.D.) Mean (S.D.) of freedom) The GAF and the PANSS scores were rated by the clinicians, Age (years) 45.4(13.4) 43.9(13.8) 46.3 (13.3) p=0.539, whereas the LSAS and SQLS were in a self-report format. t=0.61, df=48 Duration of 20.3 (11) 20.4(10.1) 20.2 (11.7) p=0.939, Statistical analysis: TheLSAS-SR questionnaire was Illness (years) t=-0.07, df=48 used as a screening tool for the presence of SAD using a Number of 1.42 (1.7) 1.37 (1.9) 1.45 (1.7) p=0.872, cutoff of 30 or more (indicating the presence of focused Friends t=0.16, df=48 SAD). A secondary measure was for generalized SAD PANSS total 62.7(16.8) 67.7 (19) 59.6 (14.9) p=0.099, (range 35-100) t=-1.68, df=48 based on a score of 60 or more on the LSAS. As men- PANSS 13.1 (4.8) 14.68(5.7) 12.09(3.9) p=0.092, tioned above, the specifier “generalized” is used in the positive t=-1.91, df=48 DSM-IV to denote a subgroup of individuals who suffer (range 7-23) from anxiety in most social and performance situations. PANSS 18.9 (6.7) 20.05 (7.2) 18.19 (6.3) p=0.345, Although the higher cutoff score might be correlated negative t=-9.54, (range 7-39) df=48 with greater specificity in screening for SAD, the lower PANSS general 30.7 (9) 32.94 (9.9) 29.29 (8.1) p= 0.165, cutoff score was also found to predict non-generalized (range 16-49) t=-1.41, df=48 SAD (18, 19). We compared the characteristics of those LSAS total 27.7 (24.9) 52.1 (23.1) 12.8 (9.3) p<0.001, with SAD and schizophrenia versus those with schizo- (range 0-118) t=-8.44, df=48 phrenia alone. This was done as follows: the distribution SQLS 78.5 (18.1) 87.1 (18.7) 73.2 (15.8) p=0.007, of gender and of those taking in both (range 43-113) t=-2.82, df=48 groups was examined by chi square analyses and we GAF 52.8 (8.9) 51.8 (6.1) 53.4 (10.3) p=0.553, (range 35-75) t=0.59, df=48 used an analysis of t-test for independent samples for D.D.D. 1.23 (0.7) 1.3 (0.84) 1.2 (0.6) p=0.527, continuous variables. (range 0.4-3.7) t=-0.63, df=48 Correlations were reviewed between the LSAS and Abbreviations: Liebowitz Social Anxiety Scale (LSAS), the Positive and PANSS, between the “fear” subscale of the LSAS and Negative Syndrome Scale (PANSS), the Schizophrenia Quality of Life positive symptoms, and between the “avoidance” LSAS Scale (SQLS), Global Assessment of Functioning scale (GAF) and Daily Defined Dose (DDD). subscale and negative symptoms on the PANSS.

42 Katherine Moss Lowengrub et al. duration of illness, number of friends and D.D.D. The patient selection and choice of screening tools for SAD group with schizophrenia and SAD included 12 males (SCID vs LSAS-SR). Additionally, several recent studies and 7 females, whereas the group with schizophrenia have examined the prevalence of SAD in acutely hospital- alone included 14 males and 17 females. This difference ized schizophrenic patients with prevalence rates ranging in gender distribution (37% females vs 55%, respectively) from 5.7-25% (9, 10, 24). These different rates may be due was not significant (chi square = 1.529, df=1, p=0.22). The to the difficulty of administering screening instruments subjects with schizophrenia and SAD took antidepres- to patients who are not clinically stable and are paranoid. sant medications in a similar proportion as the subjects Consistent with data presented by Pallanti et al. (6), with schizophrenia (26% vs 29%, chi square =0.043, a clear finding of our study was that relative to patients p=1, degrees of freedom=1). Subjects with schizophrenia without comorbid SAD, patients with schizophrenia and SAD had a lower quality of life (the SQLS score is with SAD had a lower overall quality of life (see Table 1). inversely correlated with quality of life). According to Kumazaki et al. (25), the association between Correlations: We found significant Pearson correla- social anxiety symptoms and a lower subjective quality of tions between LSAS Fear subscale and PANSS general life suggests that it is clinically important to recognize the subscale (r=0.28 [p=0.046] and SQLS presence of social anxiety. These authors maintain that [r=0.45, p=0.001]), and also between LSAS avoidance anxiety symptoms are often under-diagnosed because subscale and PANSS general psychopathology subscale clinicians usually pay more to psychotic symp- (r=0.34, p=0.016), PANSS total (r=0.29, p=0.037) and toms. In addition, they point out that recent criteria for SQLS (r=0.48, p=0.001). No significant correlations were remission in schizophrenia mainly rely on psychotic found between LSAS fear subscale and positive PANSS symptoms (26, 27) and, therefore, the risk of under- and between LSAS avoidance subscale and PANSS nega- diagnosing anxiety factors is increased. However, this tive. The LSAS (total score) correlated significantly with issue is far from simple. Whereas some authors conclude the PANSS general psychopathology subscale (r=0.31, that social anxiety may lead to a decreased quality of life p=0.024) and with the SQLS (r=0.47, p<0.01). An addi- (6), others maintain, for example in community-dwelling tional finding was that paranoid patients had lower GAF patients with remitted schizophrenia, that a lower sub- scores (p=0.017). jective quality of life might lead to the development of social anxiety symptoms (25), due to life’s hardships and a lack of social communication skills. Discussion Contrary to our expectations, we found no significant To date, only a handful of studies have examined the difference between patients with and without comorbid prevalence rates of comorbid SAD in ambulatory patients SAD in terms of the GAF scores. One explanation for with schizophrenia. The results of our study show that this finding is that the GAF provides a relatively rough 38% of our patients met criteria for SAD (based on a estimate of the overall severity of psychiatric symptoms score of 30 or greater on the LSAS) and that 10% of our and may not be sensitive enough to detect variances in patients met criteria for generalized SAD (based on a functioning within a group of patients afflicted with score of 60 or greater on the LSAS). The distinction schizophrenia. Accordingly, we note that the mean GAF between focused social anxiety and generalized social score for both cohorts (with and without SAD) was in the anxiety disorder is important, as the generalized form low end of the moderate range showing that all patients is associated with greater disability [20]. had relatively poor functioning. Our prevalence rate of 38% for comorbid SAD is con- While the results of our study show that SAD is associ- sistent with that reported by both Pallanti et al. and Tibbo ated with an impaired quality of life, experts generally agree et al. in their studies of chronic ambulatory patients where that the distinction between comorbid SAD and symptoms prevalence rates were 36.3% and 23.3%, respectively (6, related to the natural course of schizophrenia is challeng- 21). Likewise several studies among first-episode patients ing. A major question in this field is that of the ability to have reported rates between 25-32% (22, 23). We note that differentiate SAD symptoms from positive symptoms (i.e., our prevalence is higher than that reported by Braga et paranoia, ideas of reference) and negative symptoms (social al. (8) who found comorbid SAD in 17% of outpatients withdrawal) which are inherent in the disease process of (n=53) with schizophrenia. The lower rate reported by schizophrenia. In the case of a chronic patient who refuses Braga may relate to differences in study variables, such as to go to a vocational rehabilitation program, it is mandatory

43 Isr J Psychiatry Relat Sci - Vol. 52 So- Nocial 1 (2015) Anxiety Disorder Comorbid with Schizophrenia to discern whether his behavior results from fears that spies 1) a lack of knowledge of the high prevalence rates of will attack him (positive symptoms), avolition (negative comorbid SAD in schizophrenia, 2) failure to appreciate symptoms) or fears that in the rehabilitation center he the clinical relevance and additional morbidity con- will sweat excessively and therefore will be mocked and ferred by the presence of SAD in schizophrenia, 3) lack will feel embarrassed (possibly SAD). For example, Mazeh of knowledge regarding screening procedures, and 4) the et al. (9) concluded that it is difficult to differentiate SAD tendency (bias) among clinicians to attribute poor social from positive symptoms, although we note that their study functioning to negative symptoms without exploring examined a cohort of acutely ill patients in which prominent other comorbid conditions. positive symptoms may confound the assessment of SAD. A limitation of our study is the small sample size. In concordance with current studies (6, 22), the results of Another limitation may be the relative homogeneity of our study show that compared to patients who did not suf- our sample which was composed primarily of patients fer from comorbid SAD, patients with schizophrenia and with chronic schizophrenia, and, therefore, the results of comorbid SAD had similar rates of negative and positive our study may not generalize to a more diverse population symptoms (see Table 1). Our results, therefore, support including first episode patients. The inclusion of patients findings by Pallanti et al. (6) and Michail and Birchwood with schizoaffective disorder in our study population may (22) that social anxiety appears to be unrelated to the pres- also be considered as a limitation of our study, for the pres- ence of clinical psychotic symptoms. ence of affective symptoms may represent a confounding In our opinion, screening for SAD in outpatients with variable in the assessment of SAD. Patients with schizoaf- schizophrenia may be best accomplished by asking if the fective disorder, however, comprised only a minority patient has a fear of embarrassment or has avoidance in of the sample. The inclusion of patients medicated with particular social situations (eating in public, going to medication may have biased the results, for job interviews or using a public restroom), for the core the pharmacotherapy may have masked symptoms of SAD features of SAD are a fear of embarrassment and an intense although we attempted to conduct our study under natu- apprehension about being negatively evaluated by others ralistic conditions. Furthermore, the use of the LSAS-SR to which lead to social avoidance. The patient with comorbid screen for the presence of SAD (in contrast to the clinician- SAD complicating schizophrenia will experience the administered LSAS and the SCID) may have possibly avoidant behavior as ego-dystonic and therefore qualita- decreased the reliability of our results, although both LSAS tively different from avoidant behavior due to scales have been shown to be equivalent in several studies or lack of social interest. Furthermore, the patient with (18, 19). Seedat et al. (24) observed the low agreement comorbid SAD is generally motivated to gain control of between the Mini International Neuropsychiatric Interview the anxiety symptoms, whereas avoidant behavior due to (MINI) and a diagnosis of anxiety disorders on symptom negative symptoms is typically accompanied by impaired status measures. While these authors suggest that existing to change. We note that user-friendly self- cutoff scores on these measures may not be appropriate report instruments (such as the Mini-SPIN) are available for psychotic individuals, we note that the MINI also is for identifying SAD in the managed care setting and problematic due to its brevity and the possibility that it appear to distinguish between the generalized and non- arouses dissimulation and denial in persons with . generalized subtypes (19, 28, 29). However, the While the rate in our study is much higher and ease of administration of these tools in patients with than chance alone, its cause is unclear. Is it a result of schizophrenia deserves further study. the fear of stigma and rejection while having a mental We have provided a synopsis of screening techniques disorder or due to a common biological underpinning, or for SAD, for an important finding of our study was rather a medication-induced ? Schizophrenia that according to the results of the retrospective chart is associated with excessive activity, which is review, the diagnosis of comorbid SAD had been missed related to novelty seeking and exploratory behaviors. in every affected patient. We note that this failure to Introversion and social anxiety are related to decreased detect comorbid SAD occurred in a university-affiliated dopamine levels (30) and indeed Pallanti et al. (11) clinical setting which is staffed by experienced senior reported that anti- drugs cause SAD symp- . We propose that several clinician-related toms in a higher rate than expected. variables contributed to the failure to correctly diagnose We conclude that a failure to systematically screen for the comorbid SAD in our study population including: comorbid SAD in schizophrenia leads to underdetec-

44 Katherine Moss Lowengrub et al. tion of this potentially treatable disorder. SAD results in whether the diagnosis and treatment of comorbid SAD patients with schizophrenia in reduced quality of life and would improve the treatment and quality of life of patients perhaps in other impairments. We note that clinicians with schizophrenia. also need to be aware that the use of atypical neuroleptic medications such as and may lead References to the emergence of SAD during treatment (11). Patients 1. Carpenter WT, Jr. The deficit syndrome. Am J Psychiatry 1994; 151: with comorbid SAD appear to be sensitive to the social 327-329. 2. Buckley PF, Miller BJ, Lehrer DS, Castle DJ. Psychiatric stigma linked to schizophrenia and tend to feel socially and schizophrenia. Schizophr Bull 2009; 35: 383-402. marginalized (23). 3. Bayle FJ, Krebs MO, Epelbaum C, Levy D, Hardy P. Clinical features Whereas a range of effective cognitive behavioral thera- of panic attacks in schizophrenia. 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