Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Contents lists available at ScienceDirect

Psychiatry Research journal homepage: www.elsevier.com/locate/psychres

Emotional perception and theory of mind in first episode psychosis: The role of obsessive–compulsive symptomatology Evangelos Ntouros a, Vasilios P. Bozikas b,n, Christina Andreou c, Dimitris Kourbetis a, Grigoris Lavrentiadis d, George Garyfallos d a

Psychiatric Clinic of 424 Military Hospital of Thessaloniki, Greece 1st Department of Psychiatry, Aristotle University of Thessaloniki, General Hospital “Papageorgiou”, Ring Road Thessaloniki, N. Efkarpia, 54603 Thessaloniki, Greece c Department of Psychiatry and Psychotherapy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany d 2nd Department of Psychiatry, Aristotle University of Thessaloniki, Thessaloniki, Greece b

art ic l e i nf o

a b s t r a c t

Article history: Received 1 August 2013 Received in revised form 12 July 2014 Accepted 24 July 2014

The aim of the present study was to investigate the effects of comorbid obsessive–compulsive symptoms on emotional perception and theory of mind (ToM) in patients with first-episode psychosis. Participants were 65 patients with non-affective first episode psychosis (FEP) and 47 healthy controls. The patient group was divided into two subgroups, those with (FEPþ ; n ¼ 38) and those without obsessive– compulsive symptomatology (FEP ; n ¼ 27). Emotion perception and ToM were assessed with the Perception of Social Inference Test. Severity of psychotic and obsessive–compulsive symptoms was assessed with the Positive and Negative Syndrome Scale (PANSS) and the Yale-Brown Obsessive– Compulsive Scale (Y-BOCS), respectively. Deficits in emotion recognition and theory of mind were confirmed in patients with non-affective first-episode psychosis compared to healthy controls. In patients, comorbidity with obsessive–compulsive symptoms was associated with worse performance on certain aspects of social cognition (ToM 2nd order) compared to FEP  patients. Our findings of impaired emotion perception and ToM in patients with first-episode psychosis support the hypothesis that deficits are already present at illness onset. Presence of OCS appears to have further deleterious effects on social cognition, suggesting that these patients may belong to a schizo-obsessive subtype of schizophrenia characterized by more extensive neurobiological impairment. & 2014 Elsevier Ireland Ltd. All rights reserved.

Keywords: Emotion perception Theory of mind First episode psychosis Obsessive–compulsive disorder

1. Introduction With a prevalence rate of up to 64% (Buckley et al., 2009), obsessive–compulsive symptoms (OCS) are a very common comorbidity in patients with schizophrenia, while the fully developed syndrome of obsessive–compulsive disorder (OCD) occurs in approximately one in eight patients (7.0–17.1%), (Achim et al., 2011). Prevalence rates of OCS and OCD in patients with firstepisode psychosis (FEP) are similarly high (Poyurovsky et al., 1999; De Haan et al., 2013), suggesting that these symptoms are already present at illness onset. As these figures clearly diverge from the established prevalence of OCD in the community which does not exceed 1.5–3%, (Fullana et al., 2009), there has been growing interest into the causes and implications of this comorbidity, especially in the past two decades.

n

Corresponding author. Tel.: þ 30 2313323151; fax: þ30 2310991577. E-mail address: [email protected] (V.P. Bozikas).

In general, schizophrenia with comorbid OCD or OCS is associated with more severe psychopathology and functional deficits (Devulapalli et al., 2008). Previous studies have associated obsessive–compulsive comorbidity in schizophrenia with increased symptom severity (Cunill et al., 2009). Moreover, the symptomatic and functional outcome of this subgroup of patients is significantly poorer, with more hospitalizations and functional impairment (Hwang et al., 2000), as well as more frequent suicide attempts (Sevincok et al., 2007). Regarding basic neuropsychological functions, findings are more disparate. However, here too, patients with OCS/OCD appear to exhibit greater impairments than those without, especially with regard to abstraction ability and executive functioning (for a recent review, see Lysaker and Whitney (2009)). A cognitive domain that has so far remained, to the best of our knowledge, relatively unexplored in first episode psychosis patients is the effect of OCS/OCD in social cognition. Only one study explored the role of obsessive–compulsive symptomatology in social cognition in chronic patients with schizophrenia (Whitton and Henry, 2013). The term social cognition refers to a variety of mental processes associated with the perception, interpretation and

http://dx.doi.org/10.1016/j.psychres.2014.07.058 0165-1781/& 2014 Elsevier Ireland Ltd. All rights reserved.

Please cite this article as: Ntouros, E., et al., Emotional perception and theory of mind in first episode psychosis: The role of obsessive– compulsive symptomatology. Psychiatry Research (2014), http://dx.doi.org/10.1016/j.psychres.2014.07.058i

E. Ntouros et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

2

response to stimuli pertinent to social interaction (Green et al., 2008; Bell et al., 2010; Chung et al., 2010). In patients with schizophrenia, there is significant evidence that various aspects of social cognition are impaired (Green et al., 2008), the most extensively investigated ones being theory of mind (ToM), i.e. the capacity to infer intentions, dispositions and beliefs of others (Biedermann et al., 2012), and affect perception, i.e. the ability to accurately perceive, interpret and process emotional facial expressions or prosody (Adolphs et al., 2002). Impairments in these functions are a very prominent and consistent finding in patients with schizophrenia (Edwards et al., 2002; Brune, 2005; Harrington et al., 2005; Sprong et al., 2007; Bora et al., 2009; Kohler et al., 2010; Savla et al., 2013). Social cognitive impairments are already present before the onset of the illness (Dworkin et al., 1993; Davidson et al., 1999; Schiffman et al., 2004; Addington et al., 2008; Gibson et al., 2010), and are stable over time (Addington et al., 2006; Penn et al., 2008; Green et al., 2012), independent of clinical fluctuations (Addington and Addington, 2008) and pharmacological treatment (Mueser et al., 1996; Salem et al., 1996; Wolwer et al., 1996; Addington et al., 2008; Hempel et al., 2010; Kohler et al., 2010). They are also present in unaffected relatives of patients with schizophrenia and individuals at ultra-high risk for psychosis (Bora and Pantelis, 2013) and thus appear to constitute a trait marker of the illness. Importantly, several aspects of social cognition have shown a robust association with the functional outcome of schizophrenia (Couture et al., 2006; Bell et al., 2009). According to the above findings, it appears undeniable that social cognition is of paramount significance in early schizophrenia. The aim of the present study was to investigate the association of OCS/OCD with social cognition in patients with a first episode of a schizophrenia spectrum psychosis. Based on previous findings, we formed two hypotheses: (a) social cognition deficits are present at the time of illness onset for all patients; and (b) the presence of OCS/OCD symptoms would aggravate these deficits. Our second hypothesis is mainly based on the results of studies showing that obsessive–compulsive symptomatology contributes to poorer non-social cognitive function and that non-social cognitive function is closely related to social cognition (Lysaker and Whitney, 2009).

controls, additional exclusion criteria were a history of any axis I mental disorder, treatment with any psychiatric medication and the presence of a first-degree relative diagnosed with psychosis. Participants were screened for the presence of exclusion criteria by means of a semi-structured interview conducted by one of the authors. Seventeen patients were diagnosed with schizophrenia, 11 with brief psychotic disorder, 27 with schizophreniform disorder and 10 with psychotic disorder not otherwise specified. All patients were receiving antipsychotic medication at the time of the study (atypical antipsychotic monotherapy n¼ 58; typical antipsychotic monotherapy n ¼3; combination treatment with atypical and typical antipsychotics n¼1; and combination of two atypical antipsychotics n¼ 3). However, no patient had been in antipsychotic medication treatment for longer than 12 weeks at the time of assessment. Antipsychotic doses were converted to equivalent dosages of chlorpromazine (Woods, 2003). Anticholinergic agents were being administered to 12 patients and benzodiazepines to three patients. Finally, six patients were receiving antidepressants additionally to their antipsychotic medication. 2.2. Psychopathological assessment We assessed symptom severity in patients with the Greek version (Lykouras et al., 1997) of the Positive and Negative Syndrome Scale (PANSS), (Kay et al., 1987). The assessment was conducted with use of the Greek version of the Structured Clinical Interview for the PANSS (Lykouras et al., 1997). Scores of positive, negative, cognitive, excitement and depressive symptoms according to the five-factor model of schizophrenia were calculated based on a Greek validation study of the PANSS (Lykouras et al., 2000). 2.3. Social cognition assessment For the present study we used the Perception of Social Inference Test (PESIT), (Kosmidis et al., 2008), which was developed for the Greek population based on The Awareness of Social Inference Test (TASIT), (McDonald et al., 2003). The PESIT consists of three subtests: Facial Affect Recognition, Social Inference-Minimal (SI-M) and Social Inference-Enriched (SI-E). The Facial Affect Recognition subtest assesses basic emotion perception. Stimuli are short videos of an actor who speaks out a sentence while expressing one of seven basic emotions: sadness, anger, happiness, disgust, surprise, fear, and neutral. The subtest comprises 21 videos (three for each emotion), which are presented in randomized order. One point is given for each correct response. Stimuli for the SI-M and SI-E subtests are videotaped scenarios played by two actors. In the SI-M, participants view a series of 10 brief scenarios of social interaction. After presentation of each scenario, participants are asked to evaluate i) the speaker's emotional state among six complex emotions such as disappointment, satisfaction or rage (complex emotion perception), ii) the meaning of the speaker's remark and his/her beliefs (ToM 1st order question) and iii) the speakers belief about the message the listener got from his/her remark (ToM 2nd order question). Example of SI-M scenario

2. Method 2.1. Participants We recruited 65 patients with non-affective first episode psychosis (FEP), (52 men and 13 women) and 47 healthy controls (HC), (31 men and 16 women). The patient group was divided into two subgroups, those with (FEP þ; n¼ 38; 28 men and 10 women) and those without obsessive–compulsive symptomatology (FEP  ; n¼ 27; 24 men and 3 women). Patients were recruited from two psychiatric clinics (424 Army General Hospital and 2nd Psychiatric Clinic, Aristotle University) while healthy controls were recruited from the community through word-ofmouth. The study was approved by the Ethics Committee of the Aristotle University of Thessaloniki, and written informed consent was obtained from all participants. All patients met DSM-IV criteria for Schizophrenia and other Psychotic Disorders (American Psychiatric Association, 1994). Diagnosis was confirmed with the Greek version (translation–adaptation to the Greek language by S. Beratis) of the Mini-International Neuropsychiatric Interview (4.4) (MINI) (Sheehan et al., 1998). Obsessive–compulsive symptomatology was evaluated with the Yale-Brown Obsessive–Compulsive Scale (Y-BOCS), (Goodman et al., 1989). Patients with a score of zero on the Y-BOCS were included in the FEP group, while all other patients composed the FEPþ group following a dimensional perspective also used in most of relevant studies (Niendam et al., 2009; Meijer et al., 2013). The latter group included six patients who fulfilled DSM-IV criteria for a comorbid diagnosis of OCD; due to the small number of these patients, no further analysis was conducted on these patients as a separate subgroup. Patients were assessed after clinical stabilization, shortly before or shortly after discharge. Exclusion criteria were the following: non-native speakers of the Greek language, a history of neurological or developmental disorders, substance abuse in the past 6 months prior to participation in the study, as well as any co-morbid medical disorder which might compromise cognitive performance. In healthy

Actor A: Have you asked the teacher everything you wanted? Actor B: Yes, and he has explained me everything… (expressed ironically) For each question, 0–2 points are administered according to the degree of proximity with the correct response (0 ¼wrong, 1¼ partially correct and 2¼correct). In the SI-E subtest, participants are requested to view four brief scenarios; comprehension is assessed by four questions, the first three identical to those of the SI-M, and an additional question concerning the intention of one of the two actors. The SI-E differs from the SI-M in that more cues (a prologue that reveals the actor's thoughts) are provided in addition to paralinguistic features. Example of SI-E scenario Actor A is speaking on the telephone with a friend of hers saying that she doesn't like the car that Actor B bought. She ends the conversation when Actor B enters the room. The following dialog takes place: Actor B: So what do you think about my new car? Actor A: I find it great, I can't wait to take a ride with it! (expressed in a enthusiastic tone) The PESIT yields four subscores: (a) Basic Emotion Perception (BEP) consisting of the score on the Facial Affect Perception subtest (maximum score: 21); (b) Complex Emotion Perception (CEP), calculated as the sum of points on the first question in SI-M and SI-E (maximum score: 28); (c) 1st order ToM (ToM1), which consists in the sum of points on the second question in SI-M and SI-E (maximum score: 28); and (d) 2nd order ToM (ToM2), reflecting performance on the 3rd and 4th questions of the SI-M and SI-E (maximum score: 36). The PESIT has a very high internal consistency for the total score (Cronbach's α ¼ 0.866), and high for each of the four subscores (α ¼ 0.800, 0.755, 0.762 and 0.807 for BEP, CEP, ToM 1st order and ToM 2nd order, respectively). Internal

Please cite this article as: Ntouros, E., et al., Emotional perception and theory of mind in first episode psychosis: The role of obsessive– compulsive symptomatology. Psychiatry Research (2014), http://dx.doi.org/10.1016/j.psychres.2014.07.058i

E. Ntouros et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎ consistency among the seven different emotions is moderate (Cronbach's 0.640), (Aretouli, 2008).

α¼

3

not differ from each other on any of the factors measured by PANSS (p4 0.05 for all comparisons).

2.4. Statistical analyses

3.1. Group comparisons of PESIT performance

Data were expressed as the mean 7 standard deviation (S.D.) for continuous variables and percentages for categorical variables. The measured variables were not distributed normally across our three research groups (as assessed with the Kolmogorov–Smirnov test), so appropriate non-parametric statistics were employed for between-group comparisons. PESIT performance was compared among the three groups (controls, FEPþ , FEP  ) with group as the only between-subjects factor and BEP, CEP, ToM1 and ToM2 scores as the dependent variables using the Kruskal–Wallis test. The same procedure was followed to investigate the between group differences in every basic emotion separately. Correlations among PESIT scores and psychosis severity indices (scores on the five PANSS Factors: Positive Factor, Negative Factor, Cognitive Factor, Excitement Factor and Depression Factor) were investigated by means of Spearman's r for each patient group separately. Because of the large number of variables, the Holm– Bonferroni correction was applied with the target p set at 0.0025 (0.05:20). Moreover, correlations between PESIT and Y-BOCS scores were also investigated in FEP þ with the target p set at 0.05. All statistical analyses were performed using SPSS 21.0.

PESIT performance scores for each subtest are presented in Table 2. Between-subject tests revealed significant differences between the HC group and the patient groups for all PESIT subtests (p o0.001). Between-group tests indicated that healthy controls scored significantly higher on BEP and CEP subtests compared to both patient groups, who did not differ from each other. Controls exhibited significantly higher scores than both patient groups in ToM1 and ToM2 subtests as well; here, however, the two patient groups differed from each other in ToM2 subtest performance (p¼0.015), with the FEPþ group being significantly more impaired than the FEP group. Regarding BEP scores for each emotion separately, the overall effect of group is again significant and the results are presented in Table 3. The Kruskal–Wallis test suggested that there were statistically significant differences among the three groups in all basic emotions except for Disgust. Between-group comparisons with the Mann–Whitney statistic revealed that both FEP þ and FEP  groups had significantly lower values when compared to controls in Happiness, Sadness, Fear, Anger and Neutral. Surprisingly, only the FEP  group demonstrated lower values compared to controls. No statistically significant differences were noted between FEP þ and FEP  groups in any basic emotion.

3. Results Sociodemographic and clinical characteristics of participants are presented in Table 1. There were no significant differences among groups in terms of age [F(2,109) ¼0.33, p ¼0.7], years of education [F(2,109) ¼0.46, p ¼ 0.6], or gender [χ2(2) ¼4.71, p¼ 0.1]. Moreover, the two patient groups did not differ from each other on any of the factors measured by PANSS (p4 0.05 for all comparisons) or mean doses of antipsychotics in chlorpromazine equivalents [t(63) ¼0.22, p¼ 0.82]. Moreover, the two patient groups did Table 1 Demographic and clinical characteristics of the three groups.

Age (years) Education (years) PANSS total score Positive Factor Negative Factor Cognitive Factor Excitement Factor Depression Factor Y-BOCS total score Mean doses of antipsychotics

FEP þ (n¼ 38) mean (S.D.)

FEP  (n¼ 27) mean (S.D.)

HC (n¼ 47) mean (S.D.)

26.42 12.65 73.37 15.36 14.05 12.42 9.52 8.05 9.86 556.06

26.33 (4.51) 12.70 (1.89) 69.93 (14.99) 13.81 (3.88) 15.25 (3.87) 10.92 (3.02) 9.70 (3.78) 7.44 (2.00) – 538.09 (67.32)

25.45 (6.52) 12.98 (1.32) – – – – – – –

(6.33) (1.84) (14.23) (4.18) (5.03) (4.26) (2.85) (2.26) (5.43) (48.09)

FEPþ : patients with obsessive–compulsive symptoms; FEP  : patients without obsessive–compulsive symptoms; HC: healthy controls; PANSS: Positive and Negative Syndrome Scale; Y-BOCS: Yale-Brown Obsessive Compulsive Scale; and Mean doses of antipsychotics in chlorpromazine equivalents.

3.2. Correlations between social cognition and symptoms All correlations were calculated using the non-parametric Spearman's r. Although there were several significant correlations within the two research groups, direct comparisons revealed that after correcting for multiple testing only three significant correlations (p o0.0025) remained. These were negative correlations between BEP and Negative PANSS Factor in the FEP þ group, and between ToM 2nd order and two PANSS Factors (Positive and Excitement) in the FEP  group. All results and statistically significant correlations (displayed in bold) are presented in Table 4. Y-BOCS scores did not correlate significantly with PANSS Factors (r ranged from  0.114 to 0.180).

4. Discussion The findings of the present study have confirmed our assumption of deficits in emotion recognition and theory of mind in patients with non-affective first-episode psychosis compared to healthy controls. Comorbidity with OCS or OCD was associated with worse performance of patients on certain aspects of social cognition, notably in 2nd order theory of mind. To the best of our

Table 2 Perception of Social Inference Test scores of the three groups.

BEP CEP ToM1 ToM2

FEP þ (n¼ 38) mean (S.D.)

FEP  (n¼ 27) mean (S.D.)

HC (n¼ 47) mean (S.D.)

Kruskal–Wallis χ2

p

Between-group test

16.18 17.74 22.13 24.39

16.04 18.19 24.26 27.89

18.85 24.06 27.36 34.21

37.984 50.358 57.743 73.504

o 0.001 o 0.001 o 0.001 o 0.001

HC4 FEP ¼FEP þ HC4 FEP ¼FEP þ HC4 FEP ¼FEP þ HC4 FEP 4FEPþ

(2.93) (4.69) (4.69) (6.09)

(2.31) (3.71) (2.14) (4.37)

(1.31) (2.80) (1.12) (1.74)

FEPþ : patients with obsessive–compulsive symptoms; FEP  : patients without obsessive–compulsive symptoms; and HC: healthy controls. BEP score: Basic Emotion Perception; CEP score: Complex Emotion Perception; ToM1: theory of mind 1st order; and ToM2: theory of mind 2nd order.

Please cite this article as: Ntouros, E., et al., Emotional perception and theory of mind in first episode psychosis: The role of obsessive– compulsive symptomatology. Psychiatry Research (2014), http://dx.doi.org/10.1016/j.psychres.2014.07.058i

E. Ntouros et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

4

Table 3 Perception of Social Inference Test scores (Basic Emotions) of the three groups.

BEP Emotions Happiness Sadness Disgust Surprise Fear Anger Neutral

FEP þ (n¼ 38) Mean (S.D.)

FEP  (n¼ 27) Mean (S.D.)

HC (n¼47) Mean (S.D.)

Kruskal–Wallis χ2

p

Between-group test

2.13 1.82 2.58 2.39 2.11 2.76 2.39

2.07 1.81 2.63 2.04 2.15 2.78 2.56

2.64 2.36 2.79 2.57 2.57 3.00 2.91

12,887 10,917 2,699 7,918 8,060 11,462 17,494

0.002 0.004 0.259 0.019 0.018 0.003 o 0.001

HC 4FEP  ¼ FEPþ HC 4FEP  ¼ FEPþ

(0.78) (0.95) (0.72) (0.72) (0.95) (0.49) (0.75)

(0.83) (0.79) (0.69) (0.85) (0.82) (0.42) (0.75)

(0.49) (0.82) (0.51) (0.58) (0.65) (0.00) (0.35)

HC 4FEP  ; HC¼FEP þ HC ¼ FEP ¼FEP þ HC 4FEP  ¼ FEPþ HC4FEP  ¼ FEPþ

FEPþ : patients with obsessive–compulsive symptoms; FEP  : patients without obsessive–compulsive symptoms; HC: healthy controls; and BEP score: Basic Emotion Perception.

Table 4 Correlations (Spearman's r) between PANSS subscores and social cognition performance in FEPþ and FEP patients. Significant correlations (p o 0.0025, corrected for multiple testing) are displayed in bold. PANSS factors Positive

Negative

Cognitive

Excitement

Depression

FEP þ BEP CEP ToM1 ToM2

0.040 0.042  0.027 0.098

 0.509 0.198 0.065  0.036

 0.405  0.195  0.284  0.208

 0.084  0.170  0.132  0.158

 0.186 0.174 0.284 0.260

FEP  BEP CEP ToM1 ToM2

 0.490  0.361  0.300  0.578

 0.077 0.033  0.043  0.334

 0.357  0.393  0.282  0.517

 0.422  0.432  0.276  0.564

 0.470 0.118  0.250  0.286

FEPþ : patients with obsessive–compulsive symptoms; FEP  : patients without obsessive–compulsive symptoms; BEP score: Basic Emotion Perception; CEP score: Complex Emotion Perception; ToM1: theory of mind 1st order; ToM2: theory of mind 2nd order.

knowledge, this is the first study to address this topic in first episode psychosis patients. Regarding basic and complex emotion perception, both patient groups presented significant impairments compared to those of controls. This finding is in line with those of a multitude of studies on facial and vocal affect recognition in patients with first-episode schizophrenia (Edwards et al., 2001; Kucharska-Pietura et al., 2005; Amminger et al., 2012) and ultra-high risk individuals (Amminger et al., 2012), as well as with the conclusions of a recent meta-analysis of studies on facial emotion perception in patients with schizophrenia (Kohler et al., 2010). Overall, these findings indicate the relevance of emotion decoding deficits in psychosis. FEP  and FEP þ patients performed equally in basic and complex emotion perception with regard to the overall score and, largely, to individual emotions. These results are similar to those of a recent study that found no difference in facial affect recognition between two groups of patients with recent-onset schizophrenia spectrum disorders with and without a social anxiety diagnosis (Achim et al., 2013). They are also comparable to the results by Whitton and Henry (2013), who reported similar facial affect recognition performance in chronic schizophrenic patients with OCS compared to schizophrenic patients without comorbid OCS. Performance profiles were quite different in the case of ToM. The finding that both patient groups exhibited deficits compared to those of healthy controls is consistent with reports of impaired ToM both in patients with schizophrenia in general (Sprong et al.,

2007; Bora et al., 2009; Savla et al., 2013), and with a first psychotic episode in particular (Bora and Pantelis, 2013). However, 2nd order ToM was differentially affected in the two patient groups, as patients with comorbid OCS/OCD symptoms were significantly more impaired than those without. This result corroborates the view that these patients might belong to a discrete, schizo-obsessive subtype of schizophrenia characterized by more extensive neurobiological impairment (Bottas et al., 2005). For example, schizophrenia patients with OCS perform worse than those without OCS on some neuropsychological tasks, including measures of memory and executive functioning (Hwang et al., 2000), as well as attentional set-shifting (Patel et al., 2010) – although see also Meijer et al. (2013) for opposite results. And conversely, it has been suggested that OCD patients with poor insight may represent a distinct neuropsychological subgroup of OCD, possibly reflecting a transition point on a continuum between OCD and schizophrenia with regard to neuropsychological features (Tumkaya et al., 2009). A previous study in patients with recent-onset schizophrenia and comorbid social anxiety disorder showed common mentalizing deficits (Achim et al., 2013). Previous studies have reported social cognition deficits to be a significant predictor of functional outcome in patients with schizophrenia (Couture et al., 2006; Bell et al., 2009). Importantly, social cognition deficits appear to be more strongly associated with impaired community functioning than basic neuropsychological impairments, with the strongest associations being observed for ToM (Fett et al., 2011). Thus, differences in ToM capacity might partially explain findings of worse functional outcomes in patients with the “schizo-obsessive” type of schizophrenia (Poyurovsky et al., 2001; Whitney et al., 2004). Further studies are warranted to test this hypothesis. In the present study, there were only three significant correlations between social cognition performance and symptom severity in either patient group. The first one was a significant correlation of BEP score with the Negative Factor of PANSS in the FEP þ group, and is consistent with the suggestion that a limitation in the range of emotions that patients are able to perceive is associated with emotional blunting and anhedonia (Phillips and Seidman, 2008). The other two statistically significant correlations were between ToM 2nd order and two PANSS Factors (Positive and Excitement) in the FEP  group. This is partly in line with the results of a metaanalysis reporting that, although all symptom subgroups were significantly associated with ToM deficits in a group of patients with schizophrenia, patients with behavioral symptoms of disorganization exhibited the most severe impairments compared to all other subgroups (Sprong et al., 2007). In general, the association between various symptom dimensions of psychosis with social cognition parameters is in itself one of the most notoriously unstable findings in the literature. Discrepancies are due to

Please cite this article as: Ntouros, E., et al., Emotional perception and theory of mind in first episode psychosis: The role of obsessive– compulsive symptomatology. Psychiatry Research (2014), http://dx.doi.org/10.1016/j.psychres.2014.07.058i

E. Ntouros et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

differences regarding the phase of the illness (acute exacerbation vs. stabilization vs. remission) or patient populations (inpatients vs. outpatients), but also to differences in psychopathological assessment methods. A limitation of the present study consists in the fact that it only included stable patients around the time of hospital discharge. At that time, most patients met PANSS criteria for symptom remission as defined by the Remission in Schizophrenia Working Group (Andreasen et al., 2005), but without fulfilling the 6-month time criterion of remission. This, along with the cross-sectional nature of the study, precludes strong conclusions on whether our finding of impaired ToM represents a trait feature of schizophrenia with comorbid OCS/OCD. In summary, our findings of impaired emotion perception and ToM in first-episode psychotic patients support the notion that these deficits are already present at illness onset. Furthermore, comorbidity with OCS/OCD in non-affective psychosis appears to be associated with larger impairments in ToM 2nd order. Given the reported significance of social cognition deficits for psychosocial functioning in patients with psychosis, further studies are warranted to investigate whether ToM deficits attribute to worse functional outcomes in particular with comorbid obsessive– compulsive symptomatology.

References Achim, A.M., Maziade, M., Raymond, E., Olivier, D., Merette, C., Roy, M.A., 2011. How prevalent are anxiety disorders in schizophrenia? A meta-analysis and critical review on a significant association. Schizophrenia Bulletin 37, 811–821. Achim, A.M., Ouellet, R., Lavoie, M.A., Vallieres, C., Jackson, P.L., Roy, M.A., 2013. Impact of social anxiety on social cognition and functioning in patients with recent-onset schizophrenia spectrum disorders. Schizophrenia Research 145, 75–81. Addington, J., Saeedi, H., Addington, D., 2006. Influence of social perception and social knowledge on cognitive and social functioning in early psychosis. British Journal of Psychiatry 189, 373–378. Addington, J., Addington, D., 2008. Social and cognitive functioning in psychosis. Schizophrenia Research 99, 176–181. Addington, J., Penn, D., Woods, S.W., Addington, D., Perkins, D.O., 2008. Facial affect recognition in individuals at clinical high risk for psychosis. British Journal of Psychiatry 192, 67–68. Adolphs, R., Baron-Cohen, S., Tranel, D., 2002. Impaired recognition of social emotions following amygdala damage. Journal of Cognitive Neuroscience 14, 1264–1274. American Psychiatric Association, 1994. Diagnostic and Statistical Manual of Mental Disorders, 4th ed. American Psychiatric Association, Washington, DC. Amminger, G.P., Schafer, M.R., Klier, C.M., Schlogelhofer, M., Mossaheb, N., Thompson, A., Bechdolf, A., Allott, K., McGorry, P.D., Nelson, B., 2012. Facial and vocal affect perception in people at ultra-high risk of psychosis, first-episode schizophrenia and healthy controls. Early Intervention in Psychiatry 6, 450–454. Andreasen, N.C., Carpenter Jr., W.T., Kane, J.M., Lasser, R.A., Marder, S.R., Weinberger, D.R., 2005. Remission in schizophrenia: proposed criteria and rationale for consensus. American Journal of Psychiatry 162, 441–449. Aretouli, E., 2008. Social Cognition (SC) and Executive Functions in Patients With Frontal Variant Frontotemporal Dementia. Department of Psychology, Aristotle University of Thessaloniki, Thessaloniki. Bell, M., Tsang, H.W., Greig, T.C., Bryson, G.J., 2009. Neurocognition, social cognition, perceived social discomfort, and vocational outcomes in schizophrenia. Schizophrenia Bulletin 35, 738–747. Bell, M.D., Fiszdon, J.M., Greig, T.C., Wexler, B.E., 2010. Social attribution testmultiple choice (SAT-MC) in schizophrenia: comparison with community sample and relationship to neurocognitive, social cognitive and symptom measures. Schizophrenia Research 122, 164–171. Biedermann, F., Frajo-Apor, B., Hofer, A., 2012. Theory of mind and its relevance in schizophrenia. Current Opinion in Psychiatry 25, 71–75. Bora, E., Yucel, M., Pantelis, C., 2009. Theory of mind impairment in schizophrenia: meta-analysis. Schizophrenia Research 109, 1–9. Bora, E., Pantelis, C., 2013. Theory of mind impairments in first-episode psychosis, individuals at ultra-high risk for psychosis and in first-degree relatives of schizophrenia: systematic review and meta-analysis. Schizophrenia Research 144, 31–36. Bottas, A., Cooke, R.G., Richter, M.A., 2005. Comorbidity and pathophysiology of obsessive-compulsive disorder in schizophrenia: is there evidence for a schizoobsessive subtype of schizophrenia? Journal of Psychiatry and Neuroscience 30, 187–193.

5

Brune, M., 2005. “Theory of mind” in schizophrenia: a review of the literature. Schizophrenia Bulletin 31, 21–42. Buckley, P.F., Miller, B.J., Lehrer, D.S., Castle, D.J., 2009. Psychiatric comorbidities and schizophrenia. Schizophrenia Bulletin 35, 383–402. Chung, Y.S., Mathews, J.R., Barch, D.M., 2010. The effect of context processing on different aspects of social cognition in schizophrenia. Schizophrenia Bulletin 37, 1048–1056. Couture, S.M., Penn, D.L., Roberts, D.L., 2006. The functional significance of social cognition in schizophrenia: a review. Schizophrenia Bulletin 32 (1), S44–S63. Cunill, R., Castells, X., Simeon, D., 2009. Relationships between obsessivecompulsive symptomatology and severity of psychosis in schizophrenia: a systematic review and meta-analysis. Journal of Clinical Psychiatry 70, 70–82. Davidson, M., Reichenberg, A., Rabinowitz, J., Weiser, M., Kaplan, Z., Mark, M., 1999. Behavioral and intellectual markers for schizophrenia in apparently healthy male adolescents. American Journal of Psychiatry 156, 1328–1335. De Haan, L., Sterk, B., Wouters, L., Linszen, D.H., 2013. The 5-year course of obsessive-compulsive symptoms and obsessive-compulsive disorder in firstepisode schizophrenia and related disorders. Schizophrenia Bulletin 39, 151–160. Devulapalli, K.K., Welge, J.A., Nasrallah, H.A., 2008. Temporal sequence of clinical manifestation in schizophrenia with co-morbid OCD: review and metaanalysis. Psychiatry Research 161, 105–108. Dworkin, R.H., Cornblatt, B.A., Friedmann, R., Kaplansky, L.M., Lewis, J.A., Rinaldi, A., Shilliday, C., Erlenmeyer-Kimling, L., 1993. Childhood precursors of affective vs. social deficits in adolescents at risk for schizophrenia. Schizophrenia Bulletin 19, 563–577. Edwards, J., Pattison, P.E., Jackson, H.J., Wales, R.J., 2001. Facial affect and affective prosody recognition in first-episode schizophrenia. Schizophrenia Research 48, 235–253. Edwards, J., Jackson, H.J., Pattison, P.E., 2002. Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clinical Psychology Review 22, 789–832. Fett, A.K., Viechtbauer, W., Dominguez, M.D., Penn, D.L., van Os, J., Krabbendam, L., 2011. The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: a meta-analysis. Neuroscience and Biobehavioral Reviews 35, 573–588. Fullana, M.A., Mataix-Cols, D., Caspi, A., Harrington, H., Grisham, J.R., Moffitt, T.E., Poulton, R., 2009. Obsessions and compulsions in the community: prevalence, interference, help-seeking, developmental stability, and co-occurring psychiatric conditions. American Journal of Psychiatry 166, 329–336. Gibson, C.M., Penn, D.L., Prinstein, M.J., Perkins, D.O., Belger, A., 2010. Social skill and social cognition in adolescents at genetic risk for psychosis. Schizophrenia Research 122, 179–184. Goodman, W.K., Price, L.H., Rasmussen, S.A., Mazure, C., Fleischmann, R.L., Hill, C.L., Heninger, G.R., Charney, D.S., 1989. The Yale-Brown Obsessive Compulsive Scale. I. Development, use, and reliability. Archives of General Psychiatry 46, 1006–1011. Green, M.F., Penn, D.L., Bentall, R., Carpenter, W.T., Gaebel, W., Gur, R.C., Kring, A.M., Park, S., Silverstein, S.M., Heinssen, R., 2008. Social cognition in schizophrenia: an NIMH workshop on definitions, assessment, and research opportunities. Schizophrenia Bulletin 34, 1211–1220. Green, M.F., Bearden, C.E., Cannon, T.D., Fiske, A.P., Hellemann, G.S., Horan, W.P., Kee, K., Kern, R.S., Lee, J., Sergi, M.J., Subotnik, K.L., Sugar, C.A., Ventura, J., Yee, C. M., Nuechterlein, K.H., 2012. Social cognition in schizophrenia, Part 1: performance across phase of illness. Schizophrenia Bulletin 38, 854–864. Harrington, L., Siegert, R.J., McClure, J., 2005. Theory of mind in schizophrenia: a critical review. Cognitive Neuropsychiatry 10, 249–286. Hempel, R.J., Dekker, J.A., van Beveren, N.J., Tulen, J.H., Hengeveld, M.W., 2010. The effect of antipsychotic medication on facial affect recognition in schizophrenia: a review. Psychiatry Research 178, 1–9. Hwang, M.Y., Morgan, J.E., Losconzcy, M.F., 2000. Clinical and neuropsychological profiles of obsessive-compulsive schizophrenia: a pilot study. Journal of Neuropsychiatry and Clinical Neurosciences 12, 91–94. Kay, S.R., Fiszbein, A., Opler, L.A., 1987. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276. Kohler, C.G., Walker, J.B., Martin, E.A., Healey, K.M., Moberg, P.J., 2010. Facial emotion perception in schizophrenia: a meta-analytic review. Schizophrenia Bulletin 36, 1009–1019. Kosmidis, M.H., Aretouli, E., Bozikas, V.P., Giannakou, M., Ioannidis, P., 2008. Studying social cognition in patients with schizophrenia and patients with frontotemporal dementia: theory of mind and the perception of sarcasm. Behavioral Neurology 19, 65–69. Kucharska-Pietura, K., David, A.S., Masiak, M., Phillips, M.L., 2005. Perception of facial and vocal affect by people with schizophrenia in early and late stages of illness. British Journal of Psychiatry 187, 523–528. Lykouras, L., Botsis, A., Oulis, P., 1997. Positive and Negative Syndrome Scale. Translation–Validity–Reliability. Tsiveriotis Ed, Athens. Lykouras, L., Oulis, P., Psarros, K., Daskalopoulou, E., Botsis, A., Christodoulou, G.N., Stefanis, C., 2000. Five-factor model of schizophrenic psychopathology: how valid is it? European Archives of Psychiatry and Clinical Neuroscience 250, 93–100. Lysaker, P.H., Whitney, K.A., 2009. Obsessive-compulsive symptoms in schizophrenia: prevalence, correlates and treatment. Expert Review of Neurotherapeutics 9, 99–107. McDonald, S., Flanagan, S., Rollins, J., Kinch, J., 2003. TASIT: a new clinical tool for assessing social perception after traumatic brain injury. Journal of Head Trauma Rehabilitation 18, 219–238.

Please cite this article as: Ntouros, E., et al., Emotional perception and theory of mind in first episode psychosis: The role of obsessive– compulsive symptomatology. Psychiatry Research (2014), http://dx.doi.org/10.1016/j.psychres.2014.07.058i

6

E. Ntouros et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Meijer, J.H., Swets, M., Keeman, S., Nieman, D.H., Meijer, C.J., 2013. Is a schizoobsessive subtype associated with cognitive impairment? Results from a large cross-sectional study in patients with psychosis and their unaffected relatives. Journal of Nervous and Mental Disease 201, 30–35. Mueser, K.T., Doonan, R., Penn, D.L., Blanchard, J.J., Bellack, A.S., Nishith, P., DeLeon, J., 1996. Emotion recognition and social competence in chronic schizophrenia. Journal of Abnormal Psychology 105, 271–275. Niendam, T.A., Berzak, J., Cannon, T.D., Bearden, C.E., 2009. Obsessive compulsive symptoms in the psychosis prodrome: correlates of clinical and functional outcome. Schizophrenia Research 108, 170–175. Patel, D.D., Laws, K.R., Padhi, A., Farrow, J.M., Mukhopadhaya, K., Krishnaiah, R., Fineberg, N.A., 2010. The neuropsychology of the schizo-obsessive subtype of schizophrenia: a new analysis. Psychological Medicine 40, 921–933. Penn, D.L., Sanna, L.J., Roberts, D.L., 2008. Social cognition in schizophrenia: an overview. Schizophrenia Bulletin 34, 408–411. Phillips, L.K., Seidman, L.J., 2008. Emotion processing in persons at risk for schizophrenia. Schizophrenia Bulletin 34, 888–903. Poyurovsky, M., Fuchs, C., Weizman, A., 1999. Obsessive-compulsive disorder in patients with first-episode schizophrenia. American Journal of Psychiatry 156, 1998–2000. Poyurovsky, M., Hramenkov, S., Isakov, V., Rauchverger, B., Modai, I., Schneidman, M., Fuchs, C., Weizman, A., 2001. Obsessive-compulsive disorder in hospitalized patients with chronic schizophrenia. Psychiatry Research 102, 49–57. Salem, J.E., Kring, A.M., Kerr, S.L., 1996. More evidence for generalized poor performance in facial emotion perception in schizophrenia. Journal of Abnormal Psychology 105, 480–483. Savla, G.N., Vella, L., Armstrong, C.C., Penn, D.L., Twamley, E.W., 2013. Deficits in domains of social cognition in schizophrenia: a meta-analysis of the empirical evidence. Schizophrenia Bulletin 39, 979–992.

Schiffman, J., Lam, C.W., Jiwatram, T., Ekstrom, M., Sorensen, H., Mednick, S., 2004. Perspective-taking deficits in people with schizophrenia spectrum disorders: a prospective investigation. Psychological Medicine 34, 1581–1586. Sevincok, L., Akoglu, A., Kokcu, F., 2007. Suicidality in schizophrenic patients with and without obsessive-compulsive disorder. Schizophrenia Research 90, 198–202. Sheehan, D.V., Lecrubier, Y., Sheehan, K.H., Amorim, P., Janavs, J., Weiller, E., Hergueta, T., Baker, R., Dunbar, G.C., 1998. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59, 22–33. Sprong, M., Schothorst, P., Vos, E., Hox, J., van Engeland, H., 2007. Theory of mind in schizophrenia: meta-analysis. British Journal of Psychiatry 191, 5–13. Tumkaya, S., Karadag, F., Oguzhanoglu, N.K., Tekkanat, C., Varma, G., Ozdel, O., Atesci, F., 2009. Schizophrenia with obsessive-compulsive disorder and obsessive-compulsive disorder with poor insight: a neuropsychological comparison. Psychiatry Research 165, 38–46. Whitney, K.A., Fastenau, P.S., Evans, J.D., Lysaker, P.H., 2004. Comparative neuropsychological function in obsessive-compulsive disorder and schizophrenia with and without obsessive-compulsive symptoms. Schizophrenia Research 69, 75–83. Whitton, A.E., Henry, J.D., 2013. The relationship between sub-clinical obsessivecompulsive symptoms and social cognition in chronic schizophrenia. British Journal of Clinical Psychology 52, 115–128. Wolwer, W., Streit, M., Polzer, U., Gaebel, W., 1996. Facial affect recognition in the course of schizophrenia. European Archives of Psychiatry and Clinical Neurosciences 246, 165–170. Woods, S.W., 2003. Chlorpromazine equivalent doses for the newer atypical antipsychotics. The Journal of Clinical Psychiatry 64, 663–667.

Please cite this article as: Ntouros, E., et al., Emotional perception and theory of mind in first episode psychosis: The role of obsessive– compulsive symptomatology. Psychiatry Research (2014), http://dx.doi.org/10.1016/j.psychres.2014.07.058i