Diagnostic and Statistical Manual of Mental Disorders (DSM), 4th edition fifth revision and International Classification of Diseases-11 are moving from the categorical concept toward the dimensional concept in diagnosing psychiatric disorders. By adding the dimensional component to diagnosis , future research will highlight the symptomatic heterogeneity of different psychiatric disorders and investigate its clinical correlates.
Schizophrenia is a heterogeneous disorder with a variety of phenotypic expressions. Delineation of clinically distinct subtypes of the disorder, based on the severity of the concurrent symptom(s), is a valuable step in the new era of classification.
Anxiety is commonly observed in schizophrenia as one ofeither symptoms or disorders. Comorbid anxiety disorders are reported in more than 50% of patients with schizophrenia ; 17% of the patients with schizophrenia had social anxiety disorders (SADs), 13% had obsessive–compulsive disorder, 12% had generalized anxiety disorder , and 24% had panic disorder . However, research has neglected the study of the anxiety symptoms ‘sub syndrome’ in schizophrenia with a few studies reporting that approximately 47.5% had a lifetime history of panic attacks .
Social anxiety is a frequent but often unrecognized feature in schizophrenia and is associated with a severe level of disability [6,7]. It ranged from 6.9 to 42.8%, with most studies finding 10–20% [8,9], and in epidemiological studies, the rate of SAD ranges from 13 to 39% [3,10–12].
Currently, a research effort is undertaken to define operational guidelines for specific treatment for patients with schizophrenia with social anxiety; however, no data confirmed the difference among patients with schizophrenia with no social anxiety (NSA), with social anxiety symptoms (SAS), and those with SAD. It is a very important step to define who will be treated and why?
Aim of the work
This study aimed at determination of the prevalence, types (fear and avoidance), and severity of social anxiety (syndrome and sub syndrome) among patients with schizophrenia, to compare among patients with schizophrenia with NSA, with SAS, and those with SAD to identify the different determinants of social anxiety in terms of sociodemographic, clinical data, and the Scale forthe Assessment of Positive and Negative Symptoms (PANSS) (negative, positive, and general psychopathology) symptom scores, and to describe the quantitative and qualitative relationship between anxiety symptoms and psychotic symptoms.
Patients and methods
Between January and December 2009, all new patients with schizophrenia presenting to the Institute of Psychiatry Ain Shams University hospital were invited to participate in the study after obtaining a written informed consent. Two hundred and forty-one patients diagnosed with schizophrenia according to the DSM 4th edition criteria and the Structured Clinical Interview for Diagnosis, either outpatients or inpatients, met the study inclusion criteria and agreed to participate. During the recruitment period, 73 patients with schizophrenia refused to participate.
To include all the types and different course patterns of schizophrenia and not depending only on clinical samples from academic centers, we invited all inpatients with schizophrenia in the long-term wards of Al Abassia hospital (including patients admitted for long time periods up to 30–40 years) during the recruiting period to join the study. Only one hundred and forty-four inpatients fitted the inclusion criteria of the study and agreed to participate.
The study exclusion criteria were as follows: uncooperative patient, patient unable to understand the questions, mentally subnormal patient as clinically judged, a history of acute fulminating physical disorder, and a history of significant head trauma or convulsions. Other exclusion criteria that were added regarding the patients from AL Abassia hospital were patients with no enough information, with severe formal thought disorder interfered with proper clinical assessment, and patients more than 85 years to avoid comorbid organic factors.
All the recruited patients were asked to complete the Structured Clinical Interview for diagnosis , sociodemographic sheet, medical history sheet, the Social Anxiety Scale , and the PANSS .
The sociodemographic sheet included age, sex, social class scale , years of education, marital status, original/current residence, order of birth, occupation, religion, and parental consanguinity.
The medical history sheet included the site of recruitment whether outpatient or inpatient, past and current history of medical/psychiatric illness, history of admission, family history of psychiatric illness, types of patient's andrelative's complaints, subtype, duration and course of schizophrenia, duration of current hospitalization, current treatment, and past/current history of electroconvulsive therapy (ECT).
PANSS is a 30-item 7-point (1–7) rating scale. It is consistent in scoring individual patients over time and the course of the illness. It is divided into positive, negative, and general psychopathology subscales. Subscale scores were shown to be normally distributed and independent of each other. It includes four readings: one for the positive symptoms, one for the negative symptoms, one for the general psychopathology symptoms, and one for the total score [17–19].
The Liebowitz Social Anxiety Scale (LSAS)  is a Likert-type self-evaluation test composed of 24 questions. It is composed of 2 subscales; the first measures the level of anxiety/fear that arises in social settings and the second measures the severity of avoidance/withdrawal behavior. The subscale total score ranges from 0 to 72 and the total scale score ranges between 0 and 144. Higher scores indicate greater severity of social anxiety and avoidance/withdrawal. The recommended cutoff point for diagnosing SAD in each subscale is a score of 25 and in the total scale is a score of 50 points . For the noneducated patients, the scale was explained and then marked according to their response. LSAS seemed adequate and reliable in assessing SAD in patients with schizophrenia [7,22].
The patients with schizophrenia in the studied sample were classified according to the severity of social anxiety as measured by LSAS into three groups: (i) patients with schizophrenia NSA if the total scale scored zero, (ii) patients with SAS if the total scale scored less than 50, and (iii) patients with schizophrenia with SAD if total scale scored more than or equal to 50. The severity of SAD was classified as follows: mild (if the total scale scored less than 55), moderate (if the total scale scored 55 to 64), marked (if the total scale scored 65 to 80), severe (if the total scale scored 81 to 95), and very severe (if the total scale scored less than 95) . For statistical purposes, the latest three groups were gathered into one category named severe (if the total scale scored ≥65).
Statistical analysis was carried out by using the PASW statistical software package (v. 18.0). The χ2 test was used to study the comparison between two independent groups as regard the categorized data. The probability of error at 0.05 was considered to be significant, whereas at 0.01 and 0.001 were considered to be highly significant. Logistic stepwise multiregression analysis was used to search for a panel (independent parameters) that can predict the target parameter (dependant variable). By using logistic stepwise multiregression analysis, we can get the most sensitive ones that predict the dependant variable. They can be sorted according to their sensitivity to discriminate according to their P values.
Three hundred and eighty-five Egyptian patients with schizophrenia were included in this study with a mean age of 42.3 years ranging between 17 and 84 years. They were classified into three groups of patients: patients with NSA (n=76, 19.7%), patients with SAS (n=222, 57.7%), and patients with comorbid SAD (n=87, 22.6%). The SAD group was divided according to the severity of SAD into mild SAD manifested in 19.5% (n=17), moderate SAD in 29.9% (n=26), marked SAD in 24.1% (n=21), severe SAD in 14.9% (n=13), and very severe SAD in 11.6% (n=10).
The SAD group was relatively younger [mean 38.4±standard deviation (SD) 12.8] than the SAS group (mean 43.9±SD 14.3) and the difference was statistically significant (P<0.05). Thirty-seven (27.7%) female patients developed SAD compared with 48 (19.7%) among male patients (P<0.05). Education years were found to be significantly longer (mean 11.6±SD 4.3) in the SAD group compared with SAS (mean 10.2±SD 4.6). Other sociodemographic and economic factors showed no significant differences among the three groups; NSA, SAS, and SAD, namely residence (including origin of birth whether rural or urban), socioeconomic class, marital status, order of birth, occupation, religion, or consanguinity.
More patients with SAD (27.5%) were recruited from the outpatients than inpatients (19.4%). SAS and/or SAD were less reported among the group of patients with schizophrenia with a history of psychiatric illness (17.5%) than those without a history of psychiatric illness (81.2%). Patients subjected to ECT, either in the past or present, developed SAD in a less frequent rate than those who were not subjected to ECT. Current copsychiatric illness and a family history of psychiatric illness have no effect on SA (Table 1). With regard to the current treatment, only antidepressant intake (n=15; 19.7%) was significantly associated with a lower risk of SA development whether SAD (n=20; 9.0%) or SAS (n=9; 10.3%) (P=0.037).
Undifferentiated and paranoid schizophrenia reported the highest rates of SAD compared with the other types of schizophrenia, but the difference was not statistically significant. The duration of illness was not related to the incidence of SA (either symptoms or disorder) among the studied group of patients with schizophrenia. As regards the course of the disease, patients with complete remission reported the lowest rate of SA compared with the other courses of the disease (Table 2).
Both fear and avoidance subscale score of LSAS were significantly higher among patients with schizophrenia with SAD compared with those with SAS (P<0.05) (Table 3).
Positive and Negative subscales of PANSS and the general subscale showed a significant decrease trend from SAD to SAS to NSA groups. The total score of PANSS showed the same trend that was statistically significant (Table 4).
The negative subscale of PANSS was more correlated with the total score of LSAS (r=0.397) than the positive subscale (r=0.217) in the whole group of patients with schizophrenia with TSA (both symptoms and disorder), although both are significant. Negative and Positive PANSS subscale scores were not significantly correlated with either the total LSAS score or any of its subscale score among the group of patients with SAD. The general subscale of PANSS was significantly positively correlated with fear and the total score of LSAS, although the Spearman's correlation coefficient was less than 0.4. In the SAS group of patients, a significant positive correlation was evident with the fear subscale score of LSAS and general, positive, and negative subscales of PANSS, although the spearman coefficient was less than 0.4 (Table 5).
Somatic concern, mannerisms/posturing, unusual thought content, disorientation, poor attention, and poor impulse control are general psychopathological symptoms that didnot differentiate significantly between the SAD and SAS groups. Although other general psychopathological symptoms differentiate significantly (P<0.05), they include anxiety, guilt, tension, depression, motor retardation, uncooperativeness, lack of judgment and insight, disorientation of volition, and preoccupation. Only delusions (P<0.05) among the positive psychotic symptoms could differentiate significantly between SAD and SAS. Negative psychotic symptoms differentiate significantly between SAD and SAS (P<0.05), except for stereotyped thinking.
On comparing among mild, moderate, and severe SAD (all patients scored on LSAS ≥65), only the general psychopathological symptom subscale score could differentiate significantly among the three groups (mean 42.8, 35.8, and 47.1, respectively), and the disturbance of volition was the only symptom that showed a significant trend through the three groups of SAD (mild, moderate, and severe) being positive in 23.5% of the mild group, 44.0% in the moderate group, and 60.0% in the severe group (P=0.033).
The type of patient complaint showed no relation with the severity of SA in terms of sleep disturbance, denial, noncompliance, delusions, violence/aggression, somatic symptoms, negative symptoms, mood symptoms, catatonic symptoms, hallucination symptoms, bizarre behavior, obsessive–compulsive symptoms, anxiety, or cognitive symptoms. As regards relative's complaints, delusions and mood changes were significantly associated with SAD (P<0.05).
Logistic regression analysis for the identification of independent risk determinants of TSA showed sex (female), being an outpatient, and a negative history of ECT as independent risk factors for social anxiety in schizophrenia (Tables 6, 7).
Quantitative analysis of our results will give clues for several issues. (i) The extent of prevalence of social anxiety in schizophrenia. (ii) The types of social anxiety in schizophrenia and the percentage of each. In contrast, qualitative analysis also gave information about (i) the differences in the characteristics of patients with NSA and those with social anxiety. (ii) Criteria differentiating patients with NSA from patients with SAS and patients with SAD. (iii) The correlation between psychotic symptoms and anxiety symptoms. (iv) The detrimental factors of social anxiety developed in schizophrenia.
In our sample, 80.3% of patients with schizophrenia hadsocial anxiety (TSA, both symptoms and disorder) and only 19.7% did not develop social anxiety (NSA). Three categories were identified and arranged in the order of prevalence as follows: the first category is SAS in 57.7%, the second category is SAD in 22.6%, and the third category is NSA in 19.7%. This means that social anxiety is a common symptom in schizophrenia , which could mountain to the threshold of comorbid disorder (SAD) in approximately one fifth of patients (22.6%). As such, it is very important that we must get a true picture of its relationship with psychosis .
On comparing our results, we must consider the multiple factors interfering with proper assessment and appreciation of anxiety disorders, particularly social anxiety, in patients with schizophrenia , because of heterogeneity among definitions of symptoms, rating instruments usedfor diagnosis , impact of sociocultural factors on appreciation of social anxiety, differences in subject recruitment , and different pathogenesis of the SAS that could be either spontaneous, intermittent, in direct response to psychotic symptoms, and/or as a side effect of antipsychotic medications, besides the cutoff point defined for discriminating symptoms from disorder. Despite all these considerations, most of the studies carried out in this domain confirmed the high prevalence of social anxiety in patients with schizophrenia, such as those by Halperin et al. , Pini et al. , Muller et al. , and Birchwood et al. . Even in the first episode psychosis, Michail and Birchwood  reported that 25% of their patients with schizophrenia were diagnosed with the International Classification of Diseases–10 criteria as having SAD, and a further 11.6% reported severe difficulties in social encounters.
In this study, three independent risk factors for social anxiety in schizophrenia were identified: sex (female), being an outpatient, and no history of ECT. This raised the concept of closeness between SAS in both schizophrenia and SAD. This concept was confirmed before in the study carried out by Pallanti et al. .
Social anxiety in our sample of patients with schizophrenia increased with undifferentiated and paranoid types of schizophrenia and negative psychotic symptoms, decreased with antidepressant intake and complete remission, and not affected by the duration of schizophrenic illness and the type of the patient's complaint. In contrast, other researchers, such as Lysaker and Salyer  found that,social anxiety increased with greater hallucinations, social withdrawal, depression, hopelessness, better insight, poorer function, higher rate of suicide attempts, and a history of substance abuse. This diversity of risk factors reported in the different studies may be an indication that, social anxiety in schizophrenia is not simply an epiphenomenon of psychotic symptoms, and it has more than one causal pathway.
Some researchers have already started to suspect a possible overlap between social anxiety and paranoia, especially delusions,  and the construction of ideas ofreference (IOR). However, it was unclear whether itisa byproduct of persecutory thinking or not . Socialanxiety and IOR are close to each other conceptually and in their presentations. Both are prodromal signs and schizotypal features [33,34], and may manifest as increased selfconsciousness, fear, and avoidance in certain social situations, with the patients being aware of the excessive nature of such feelings. More subtle differences between the two may be noticed with more careful questioning (e.g. IOR seldom involves anticipation anxiety). It is doubted whether existing scales or diagnostic instruments have enough sensitivity to tell that they are apart. It is only after the potential contamination is safely ruled out by IOR, can we start to confidently investigate comorbid social anxiety and its relationship with psychosis .
The effect of current treatment of schizophrenia on social anxiety was discussed, in which the prevalence of social anxiety was affected by the use of psychotropic drugs. The study carried out by Pallanti et al.  reported the emergence of SAD in schizophrenia after 14.83±3.07 weeks of clozapine treatment (range, 9–20 weeks). None of the patients had a history of SAS. All the patients were treated with fluoxetine and 8/12 responded, defined as a greater than or equal to 35% reduction in the LSAS score. This is in agreement with our results, in which social anxiety decreased with antidepressant use. In this study, we did not identify the name of the drug; only the psychotropic group was identified. There was no significant difference between the TSA group and NSA group regarding the group of antipsychotics.
Comorbidity is an important area of work in psychosis. Apart from the clinical implications, it provides clues tothe pathological mechanisms underpinning psychosis. This may particularly be the case for social anxiety, which has been noted as a candidate end phenotype for psychosis . In our study, we compared among the three identified categories: SAS, SAD, and NSA. Patients with schizophrenia with SAD (22.6%) are significantly more likely to be female patients, younger in age, highly educated, being outpatients, not exposed to ECT, and presented with delusions and mood changes as per relatives' complaints. SAD comorbid with schizophrenia tends to be severe in degree ; severe SAD (50.0%) was more common than moderate (29.9%) and mild disorders (19.5%).
Other data on comorbid SAD and schizophrenia have shown that patients with SAD are significantly less likely to be married and more likely to live alone, have higher negative symptoms, more often have a flat affect, and seem to have an earlier onset of psychosis. In addition, it was reported that, patients with schizophrenia with SAD had a higher lifetime rate of suicide attempts, greater lethality of suicide attempts, more past substance/alcohol abuse disorder, lower social adjustment, and lower overall quality of life [7,38].
Results to date have also been confusing about the relationship between social anxiety and schizophrenic symptoms, with studies pointing to all kinds of directions as to the association with positive symptoms, negative symptoms, or both, or neither . It was found that positive symptoms correlated with increased self reports of social anxiety, and that negative symptoms correlated with specific behaviors related to social anxiety during an unstructured role-play. The social anxiety was associated with increased isolation and was thought to be related to social skill deficits . There was a significant correlation between the score of the LSAS ‘fear’ and PANSS positive subscales. Avoidance scores were higher among patients with negative signs . In contrast, social anxiety in psychosis was not related to the positive symptoms of PANSS, including suspiciousness/persecution . In addition, Sherman  found that scores onthe LSAS remained stable over a period of several months, and were not correlated with positive, negative, or total psychotic symptoms.
The same confusion applies to the relationship between social anxiety and the severity of schizophrenia. Some researchers reported a tendency for patients with comorbid social phobia to have a higher severity PANSS total score , with strong negative association between scores on the social anxiety scale and functional status, emotional well being, measures of quality of life, and lower self esteem . Other researchers found no differences in negative and positive symptom rates between patients with schizophrenia with and without SAD [7,41].
In our sample, the relationship between social anxiety and positive and negative symptoms in schizophrenia wasinvestigated, and it was different among the different categories of social anxiety as follows: in the group of social anxiety as a whole (TSA=SAD+SAS), all the subscales of LSAS was positively correlated with all PANSS scores especially the negative symptoms subscale; in the group of SAD, all the subscales of LSAS is correlated with only the general psychopathology subscale of PANSS; and in the group of SAS, only the fear subscale score of LSAS was correlated with all scores ofPANSS. However, some observations may contradict the positive relationship between social anxiety and the severity of the schizophrenic illness. These observations were: (i) patients with NSA were characterized by having a higher rate of history of psychiatric illness than those with TSA; (ii) duration of schizophrenia, parental consanguinity, and family history of psychiatric illness had no effect on social anxiety; and (iii) social anxiety was more frequent in outpatients with no history of ECT and in patients with complete remission.
On PANSS, general psychopathology symptoms were the most powerful in differentiating SAD from SAS, followed by negative symptoms (except for stereotyped thinking) and then, delusions. All the differentiating symptoms on the general subscale (anxiety, guilt feelings, tension, depression, motor retardation, uncooperativeness, lack of judgment and insight, disturbance of volition, and preoccupation) are characterized by having mood rather than psychotic nature. In addition, the general psychopathology symptoms, especially disturbance of volition, were the only PANSS symptom subscale differentiating the grade of severity of SAD (mild, moderate, and severe).
Social anxiety is highly prevalent in schizophrenia despite the multiple factors interfering with proper assessment. Subthreshold SAS are more common than SAD, which tends to be severe in patients with schizophrenia. The independent risk factors for social anxiety in schizophrenia are sex (female), being an outpatient, and a negative history of ECT. The prevalence of social anxiety in schizophrenia is affected by the type of schizophrenia, type of psychotic symptoms, type of psychotropic drug used, and the course of schizophrenia. It is not affected either by the duration of schizophrenia or the type of the patient's complaint. However, this affection depends on the severity of social anxiety, either symptoms or disorder.
These conclusions confirmed that social anxiety in schizophrenia is not simply an epiphenomenon of psychotic symptoms, and it has more than one causal pathway. Its need for specific operational guidelines to be treated and incorporated as a separate symptom dimension in patients with schizophrenia should be highlighted. Besides, it raises the need for adding routine screening for social anxiety to the protocol of schizophrenia management as an essential step.
The authors have no conflict of interest.
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Keywords:© 2011 Institute of Psychiatry, Ain Shams University
analysis; anxiety; qualitative; quantitative; schizophrenia; social