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The association between social skills deficits and family history of mood disorder in bipolar I disorder

Abstract

Objective:

To compare social skills and related executive functions among bipolar disorder (BD) patients with a family history of mood disorders (FHMD), BD patients with no FHMD and healthy control (HCs).

Methods:

We evaluated 20 euthymic patients with FHMD, 17 euthymic patients without FHMD, and 31 HCs using the Social Skills Inventory (SSI) and a neuropsychological battery evaluating executive function, inhibitory control, verbal fluency and estimated intelligence.

Results:

Both BD groups had lower SSI scores than controls. Scores for one subfactor of the social skills questionnaire, conversational skills and social performance, were significantly lower among patients with FHMD than among patients without FHMD (p = 0.019). Both groups of BD patients exhibited significant deficits in initiation/inhibition, but only BD patients with FHMD had deficits in verbal fluency, both compared to HC. There were no associations between social skills questionnaire scores and measures of cognitive function.

Conclusion:

Euthymic BD patients have lower social skills and executive function performance than HC. The presence of FHMD among BD patients is specifically associated with deficits in conversational and social performance skills, in addition to deficits in verbal fluency. Both characteristics might be associated with a common genetically determined pathophysiological substrate.

Bipolar disorder; social skills; executive functions; family history


Introduction

Bipolar disorder (BD) is a severe, chronic psychiatric disorder that has a significant negative impact on the lives of patients and families.11. Ketter TA. Diagnostic features, prevalence, and impact of bipolar disorder. J Clin Psychiatry. 2010;71:e14. Increasing evidence suggests that most individuals with BD, even during periods of prolonged remission, present with severe cognitive and functional deficits that result in significant psychosocial impairment, which is mainly characterized by various interpersonal relationship difficulties and reduced work productivity and can result in lost days or even years of work due to impaired daily activity.22. Fagiolini A, Kupfer DJ, Masalehdan A, Scott JA, Houck PR, Frank E. Functional impairment in the remission phase of bipolar disorder. Bipolar Disord. 2005;7:281-5. A lack of social support from relatives and close friends, negative emotions in the family environment, older age and residual depressive symptoms are important predictors of psychosocial impairment in the future.33. Miklowitz DJ. Functional impairment, stress, and psychosocial intervention in bipolar disorder. Curr Psychiatry Rep. 2011;13:504-12.,44. Rosa AR, Reinares M, Franco C, Comes M, Torrent C, Sánchez-Moreno J, et al. Clinical predictors of functional outcome of bipolar patients in remission. Bipolar Disord. 2009;11:401-9. These difficulties probably contribute to making BD patients more socially impaired than those with other affective illnesses.55. Tucci AM, Kerr-Correa F, Dias RS. Social disability of Brazilian mood disorder patients. Braz J Med Biol Res. 2004;37:1713-20.

Recent evidence suggests that part of the psychosocial impairment experienced by BD patients is related to poor social skills.66. Rocca CC, Heuvel Ev, Caetano SC, Lafer B. Facial emotion recognition in bipolar disorder: a critical review. Rev Bras Psiquiatr. 2009;31:171-80. Social skills are defined as behaviors in interpersonal interaction that accurately communicate emotions, feelings, opinions, attitudes, personal rights, and needs.77. Del Prette ZAP, Del Prette A. Avaliação de habilidades sociais: Bases conceituais, instrumentos e procedimentos. In: Del Prette A, Del Prette ZAP, editors. Psicologia das habilidades sociais: diversidade teórica e suas implicações. Petrópolis: Vozes; 2009. p. 187-229. Such behaviors occur in specific situations in which the individual interacts with so-called key social agents, such as colleagues, teachers, and parents. Adequate social functioning promotes positive social outcomes, including acceptance by peers, academic achievement, and professional success.88. Gresham FM. Análise do comportamento aplicadas às habilidades sociais. In: Del Prette A, Del Prette ZAP, editors. Psicologia das habilidades sociais: diversidade teórica e suas implicações. Petrópolis: Vozes; 2009. p. 17-66.

It has been proposed that the family environment plays an important role in the development of adequate social skills.99. Caballo VE, Irurtia MJ, Salazar IC. Abordagem cognitiva na avaliação e intervenção sobre habilidades sociais. In: Del Prette A, Del Prette ZAP, editors. Psicologia das habilidades sociais: diversidade teórica e suas implicações. Petrópolis: Vozes; 2009. p. 67-107. Among the families of individuals with BD, growing evidence suggests that there is greater conflict, less cohesiveness, and poorer organization when one or more first-degree relatives have a mood disorder.1010. Chang KD, Blasey C, Ketter TA, Steiner H. Family environment of children and adolescents with bipolar parents. Bipolar Disord. 2001;3:73-8.

11. Romero S, Delbello MP, Soutullo CA, Stanford K, Strakowski SM. Family environment in families with versus families without parental bipolar disorder: a preliminary comparison study. Bipolar Disord. 2005;7:617-22.
-1212. Belardinelli C, Hatch JP, Olvera RL, Fonseca M, Caetano SC, Nicoletti M, et al. Family environment patterns in families with bipolar children. J Affect Disord. 2008;107:299-305. Among BD patients, a history of family mood disorders has been associated with greater cognitive impairment, including deficits in verbal memory and executive functioning, specifically in psychomotor processing speed.1313. Antila M, Partonen T, Kieseppa T, Suvisaari J, Eerola M, Lonnqvist J, et al. Cognitive functioning of bipolar I patients and relatives from families with or without schizophrenia or schizoaffective disorder. J Affect Disord. 2009;116:70-9. In addition, there have been several studies addressing social skills training for schizophrenia patients and their families,1414. Girón M, Fernández-Yañez A, Mañá-Alvarenga S, Molina-Habas A, Nolasco A, Gomez-Beneyto M. Efficacy and effectiveness of individual family intervention on social and clinical functioning and family burden in severe schizophrenia: a 2-year randomized controlled study. Psychol Med. 2010;40:73-84. as well as studies evaluating the use of family-focused treatment in adults and adolescents with BD.1515. Lucksted A, McFarlane W, Downing D, Dixon L. Recent developments in family psychoeducation as an evidence-based practice. J Marital Fam Ther. 2012;38:101-21. However, to our knowledge, there have been no studies addressing the question of whether BD patients whose families include another individual with BD have poorer social skills than BD patients whose families do not.

The objective of this study was to evaluate social skills and related executive functions in BD patients with and without a history of mood disorders among first-degree relatives, as well as in a group of control individuals, drawing comparisons between and among the three groups. We hypothesize that BD patients with family history of mood disorders (FHMD) would present lower social skills than BD patients without FHMD and healthy controls. In addition, we sought to explore whether certain aspects of social skills are correlated with cognitive functions, such as executive function, inhibitory control, verbal fluency, and intelligence, an important consideration to further characterize neural substrates that subserve social functioning in BD patients.

Methods

Participants

The study sample consisted of 37 individuals with BD, diagnosed according to DSM-IV criteria, who were treated as outpatients in the Programa de Transtorno Bipolar (PROMAN), Instituto de Psiquiatria, Faculdade de Medicina, Universidade de São Paulo, in the city of São Paulo, Brazil. The inclusion criteria were age over 18 years, having been diagnosed with BD type I (hereafter, BD), as confirmed by the Structured Clinical Interview for DSM-IV Axis I Disorders, Patient Edition (SCID-I/P),1616. First MB, Spitzer RL, Gibbon M, Williams JB. Entrevista clínica estruturada para o DSM-IV – transtorno do eixo I: edição para pacientes (SCID-I/P). New York: New York Biometrics Research; 1997. and having been euthymic for at least 4 weeks. Euthymia was defined as a score < 7 on the 21-item Hamilton Depression Rating Scale and < 7 on the Young Mania Rating Scale, in two consecutive measures with an interval of 4 weeks between the two.1717. Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry. 1960;23:56-62.,1818. Young RC, Biggs JT, Ziegler VE, Meyer DA. A rating scale for mania: reliability, validity, and sensitivity. Br J Psychiatry. 1978;133:429-35. The exclusion criteria were substance use disorder in the last 6 months, a lifetime history of epilepsy or seizures, and having used topiramate or benzodiazepines in the last 2 weeks. FHMD was identified by the Family History Screen.1919. Weissman MM, Markowitz JC, Klerman GL. Comprehensive guide to interpersonal psychotherapy. New York: Basic Books; 2000. Patients were divided into two groups: those with and without FHMD among first-degree relatives (BD-FHMD+ and BD-FHMD-, respectively).We recruited 31 healthy controls (HCs) from the general community with no personal or family history of DSM-IV axis I disorders, as confirmed by the SCID and the Family History Screen.

The study protocol was approved by the research ethics committee of the Universidade de São Paulo. All study procedures were carried out in accordance with the Declaration of Helsinki, and all participants gave written informed consent.

Instruments

Social skills

To assess social skills, we used the Social Skills Inventory (SSI), a 38-item self-report questionnaire that evaluates how social skills are expressed in an array of different settings, including family, school, work, and everyday situations. The SSI was developed and validated for use in Brazil by Del Prette.2020. Del Prette, ZAP, Del Prette A. Inventário de habilidades sociais: manual de aplicação, apuração e interpretação. São Paulo: Casa do Psicólogo; 2001. It consists of five subscales, referred to as subfactors: self-assertion in coping with risk (subfactor 1); self-assertion in expressing positive feelings (subfactor 2); conversational skills and social performance (subfactor 3); self-exposure to strangers and new situations (subfactor 4); and self-control of aggression in adverse situations (subfactor 5). Lower scores on this instrument indicate impaired social skills.2020. Del Prette, ZAP, Del Prette A. Inventário de habilidades sociais: manual de aplicação, apuração e interpretação. São Paulo: Casa do Psicólogo; 2001.

Neurocognition

Neurocognitive assessment was conducted using the following instruments: the Hayling test, a battery of cognitive tests that evaluates the relationship between the timing of decision making and the conscious decision taken2121. Burgess PW, Shallice T. The Hayling and Brixton tests. Test manual. Bury St Edmunds: Thames Valley Test Company; 1997.; the Stroop test, which assesses selective attention, mental flexibility, and inhibitory control2222. Spreen O, Strauss E. Stroop test. In: Spreen O, Strauss E. A compendium of neuropsychological tests. New York: Oxford University; 1998. p. 213-8.; the FAS Verbal Fluency Test, which evaluates letter fluency, planning, organization, and sustained attention2323. Spreen O, Strauss E. Controlled oral word association (FAS). In: Spreen O, Strauss E. A compendium of neuropsychological tests. New York: Oxford University; 1998. p. 447-64.; and the Wechsler Abbreviated Scale of Intelligence, which allows the intelligence quotient (IQ) to be estimated.2424. Wechsler D. Wechsler abbreviated scale of intelligence (WASI). San Antonio: Harcourt Brace E Company; 1999.

Statistical analysis

We used the chi-square and Kruskal-Wallis tests to compare the groups’ demographic and clinical characteristics, as well as social skills and neurocognitive variables. For the variables identified as significant in the Kruskal-Wallis comparison, we performed pairwise comparisons with the Mann-Whitney test. To identify bivariate correlations between social skills and neurocognitive variables within each group, we used Spearman’s correlation coefficient. For total or subfactor SSI scores in which an association with FHMD was found, we used logistic regression to predict which variables would be most strongly associated with a given score. Statistical analyses were conducted using SPSS version 14.0. A p-value < 0.05 was considered statistically significant.

Results

There were no significant differences among the three groups in terms of age, sex, or estimated IQ. There was a statistically significant difference among the groups in education level, expressed as years of schooling (p = 0.022). The BD-FHMD+ and BD-FHMD- groups were comparable in terms of clinical characteristics (Table 1).

Table 1
Demographic and clinical characteristics of patients with bipolar I disorder, with and without a family history of mood disorders among first-degree relatives, and healthy controls

Table 2 shows the results for social skills and cognitive tests. There was a significant difference among the groups for total SSI score (p = 0.002), as well as for conversational skills and social performance (p < 0.001), self-exposure to strangers and new situations (p < 0.001), and self-control of aggression in adverse situations (p = 0.029). Compared with the HC group, the BD-FHMD+ and BD-FHMD- groups presented significantly lower total SSI scores (p = 0.002 and p = 0.005, respectively), lower conversational skills and social performance (p < 0.001 and p = 0.008, respectively), and lower self-exposure to strangers and new situations (p < 0.001 and p = 0.004, respectively). For self-control of aggression in adverse situations, the BD-FHMD+ group scored significantly lower than the HC group (p = 0.007), although there was no significant difference between the BD-FHMD- and HC (p = 0.76). The BD-FHMD+ group presented significantly lower scores for conversational skills and social performance than the BD-FHMD- group (p = 0.014). However, there was no significant difference between the two BD groups for self-exposure to strangers and new situations (p = 0.26), self-control of aggression in adverse situations (p = 0.10), or total SSI score (p = 0.78).

Table 2
Cognitive variables of patients with bipolar I disorder, with and without a family history of mood disorders among first-degree relatives, and healthy controls

There were statistically significant differences among the groups in terms of mean scores on the Stroop test card 1 (p = 0.023) and the FAS Verbal Fluency Test (p = 0.011), although not in mean scores on parts A and B of the Hayling test (p = 0.069 and p = 0.109, respectively) or on Stroop test cards 2 and 3 (p = 0.086 and p = 0.230, respectively). Pairwise comparison showed that mean scores on Stroop test card 1 were significantly higher in the BD-FHMD- group than in the HC group (p = 0.010). There was no statistical difference between the BD-FHMD+ and BD-FHMD- groups (p = 0.724) or between the BD-FHMD+ and HC groups (p = 0.056). For FAS verbal fluency scores, pairwise comparison showed that the BD-FHMD+ group had significantly lower scores than the HC group (p = 0.002). There were no statistical differences between the BD-FHMD+ and BD-FHMD- groups or between the BD-FHMD- and HC groups (p > 0.13 for both).

Exploratory analyses of correlations between conversational skills and social performance and other cognitive variables showed that, within the BD-FHMD- group, the conversational skills and social performance score correlated negatively with FAS verbal fluency errors (r = -0.63, p = 0.008). Within the BD-FHMD+ and HC groups, there were no significant correlations between conversational skills and social performance and any other cognitive variable. Correlations between the other SSI subfactors and all cognitive variables were not significant.

Linear regression analyses with conversational skills and social performance as the dependent variable, and gender, years of schooling, social phobia, age at illness onset, FAS verbal fluency errors, and FHMD as explanatory variables, showed that only FHMD could predict conversational skills and social performance. Conversation skills and social performance scores decreased by 35.54 (95% confidence interval 6.281-64.802, p = 0.019) with FHMD. Linear regression analyses with the other SSI subfactors revealed that no variable predicted the performance of those subfactors.

Discussion

In this study, we found that euthymic BD patients, with or without FHMD, exhibit significantly poorer social skills than HC, as assessed by a self-report questionnaire. This difference seems driven by difficulties in conversational skills and social performance, and in self-exposure to strangers and new situations, as suggested by significant differences in SSI subscales that evaluate those social skills dimensions. FHMD is associated with an important effect on conversational skills and social performance, as demonstrated by the finding that BD patients with FHMD scored lower on this factor than BD patients without FHMD. Regarding the neurocognitive assessment, we found that both groups of BD patients scored lower than HC in initiation/inhibition measures on the Stroop Card 1 subtest, and that there was an association between FHMD and lower cognitive function only in verbal fluency. The poor performance of BD patients in total social skills scores is consistent with previous studies.2525. Goldstein TR, Miklowitz DJ, Mullen KL. Social skills knowledge and performance among adolescents with bipolar disorder. Bipolar Disord. 2006;8:350-61.

26. de Almeida Rocca CC, de Macedo-Soares MB, Gorenstein C, Tamada RS, Issler CK, Dias RS, et al. Social dysfunction in bipolar disorder: pilot study. Aust N Z J Psychiatry. 2008;42:686-92.

27. Depp CA, Mausbach BT, Harvey PD, Bowie CR, Wolyniec PS, Thornquist MH, et al. Social competence and observer-rated social functioning in bipolar disorder. Bipolar Disord. 2010;12:843-50.
-2828. Martini T, Czepielewski LS, Fijtman A, Sodré L, Wollenhaupt-Aguiar B, Pereira CS, et al. Bipolar disorder affects behavior and social skills on the Internet. PLoS One. 2013;8:e79673. This deficit is present in patients with a normal theoretical knowledge of social skills but have difficulty in processing emotional cues in social circumstances.2525. Goldstein TR, Miklowitz DJ, Mullen KL. Social skills knowledge and performance among adolescents with bipolar disorder. Bipolar Disord. 2006;8:350-61.,2626. de Almeida Rocca CC, de Macedo-Soares MB, Gorenstein C, Tamada RS, Issler CK, Dias RS, et al. Social dysfunction in bipolar disorder: pilot study. Aust N Z J Psychiatry. 2008;42:686-92. It is possible that BD patients have difficulties reading the emotional signs present in social situations, which are essential components of social interaction. In fact, different aspects of emotional processing have been found to be altered even in euthymic BD patients, such as facial emotion recognition,66. Rocca CC, Heuvel Ev, Caetano SC, Lafer B. Facial emotion recognition in bipolar disorder: a critical review. Rev Bras Psiquiatr. 2009;31:171-80.,2929. de Brito Ferreira Fernandes F, Gigante AD, Berutti M, Amaral JA, de Almeida KM, de Almeida Rocca CC, et al. Facial emotion recognition in euthymic patients with bipolar disorder and their unaffected first-degree relatives. Compr Psychiatry. 2016;68:18-23.,3030. Vierck E, Porter RJ, Joyce PR. Facial recognition deficits as a potential endophenotype in bipolar disorder. Psychiatry Res. 2015;230:102-7. prosodic processing3131. Van Rheenen TE, Rossell SL. Phenomenological predictors of psychosocial function in bipolar disorder: is there evidence that social cognitive and emotion regulation abnormalities contribute? Aust N Z J Psychiatry. 2014;48:26-35. and affective responsiveness.3232. Seidel EM, Habel U, Finkelmeyer A, Hasmann A, Dobmeier M, Derntl B. Risk or resilience? Empathic abilities in patients with bipolar disorders and their first-degree relatives. J Psychiatr Res. 2012;46:382-8.

Another interpretation of this finding could involve the presence of certain psychological characteristics, which have been found associated with BD, such as low self-esteem,3333. Pope M, Dudley R, Scott J. Determinants of social functioning in bipolar disorder. Bipolar Disord. 2007;9:38-44. perfectionism, and need for approval,3434. Scott J, Stanton B, Garland A, Ferrier IN. Cognitive vulnerability in patients with bipolar disorder. Psychol Med. 2000;30:467-72. which could contribute, at least theoretically, to poor social performance.

We found that FHMD had a specific effect on social skills, especially conversational skills and social performance, as measured by the conversational skills and social performance subfactor of the SSI questionnaire. FHMD has been associated with certain clinical BD characteristics related to disease severity, such as younger age at onset, psychosis, predominant polarity, substance abuse, hospitalizations, suicidal behavior, and level of functioning.3535. Leboyer M, Bellivier F, Nosten-Bertrand M, Jouvent R, Pauls D, Mallet J. Psychiatric genetics: search for phenotypes. Trends Neurosci. 1998;21:102-5.

36. Schulze TG, Hedeker D, Zandi P, Rietschel M, McMahon FJ. What is familial about familial bipolar disorder? Resemblance among relatives across a broad spectrum of phenotypic characteristics. Arch Gen Psychiatry. 2006;63:1368-76.
-3737. Berutti M, Dias RS, Pereira VA, Lafer B, Nery FG. Association between history of suicide attempts and family functioning in bipolar disorder. J Affect Disord. 2016;192:28-33. Furthermore, families affected by BD demonstrate fewer positive and productive strategies, such as positive affect and conflict resolution,3838. Miklowitz DJ. The role of the family in the course and treatment of bipolar disorder. Curr Dir Psychol Sci. 2007;16:192-6. which could not only hinder problem resolution but also impair family relationships and communications. Families in which both parents have a mood disorder have been shown to present worse general functioning and problem resolution than those in which only one or neither parent is affected.3939. Du Rocher Schudlich TD, Youngstrom EA, Calabrese JR, Findling RL. The role of family functioning in bipolar disorder in families. J Abnorm Child Psychol. 2008;36:849-63. Among the families of BD patients, there is also evidence of greater conflict, less cohesiveness, and poorer organization when other family members have a history of mood disorders than when they do not.1010. Chang KD, Blasey C, Ketter TA, Steiner H. Family environment of children and adolescents with bipolar parents. Bipolar Disord. 2001;3:73-8.

11. Romero S, Delbello MP, Soutullo CA, Stanford K, Strakowski SM. Family environment in families with versus families without parental bipolar disorder: a preliminary comparison study. Bipolar Disord. 2005;7:617-22.
-1212. Belardinelli C, Hatch JP, Olvera RL, Fonseca M, Caetano SC, Nicoletti M, et al. Family environment patterns in families with bipolar children. J Affect Disord. 2008;107:299-305. Taken together, these findings suggest that a family history of BD is associated with more clinical signs of BD severity and greater family dysfunction. Thus, the lower conversation skills and social performance we found in BD patients with FHMD could be interpreted in two ways. The first is that clinical severity, family dysfunction and poor capacity for conversation are all manifestations of a common pathophysiological substrate that is genetically determined and contributes to these impairments. The second is that a dysfunctional family environment plays a determinant role, damaging normal social skills development in these patients. However, further studies are necessary to better understand the interplay of these variables.

The initiation/inhibition deficits found in both groups of euthymic BD patients are consistent with previous studies.4040. Yatham LN, Torres IJ, Malhi GS, Frangou S, Glahn DC, Bearden CE, et al. The international society for bipolar disorders-battery for assessment of neurocognition (ISBD-BANC). Bipolar Disord. 2010;12:351-63. In our study, this characteristic was not associated with familial BD, since we found no difference between BD groups. On the other hand, of both groups of patients, only those with a family history of BD had verbal fluency deficits according to the FAS test. The fact that patients with FHMD also had more conversation and social performance problems suggests that both characteristics belong to a group of highly heritable phenotypic features. Finally, we found no association between measures of executive functioning, inhibitory control, verbal fluency, or IQ and scores on the SSI questionnaire. This association was expected due to evidence that behaviors requiring interpersonal interaction must rely on adequate executive functioning. As demonstrated by McClure et al. and Shamay-Tsoory et al.,4141. McClure EB, Treland JE, Snow J, Schmajuk M, Dickstein DP, Towbin KE, et al. Deficits in social cognition and response flexibility in pediatric bipolar disorder. Am J Psychiatry. 2005;162:1644-51.,4242. Shamay-Tsoory S, Harari H, Szepsenwol O, Levkovitz Y. Neuropsychological evidence of impaired cognitive empathy in euthymic bipolar disorder. J Neuropsychiatry Clin Neurosci. 2009;21:59-67. adaptive social interaction requires the ability to engage in flexible thinking and to monitor, recognize, and respond to unexpected or contradictory situations (executive functioning); to respond rapidly to demands (processing speed); to inhibit irrelevant responses (inhibitory control); and to produce effective communication (verbal fluency). However, these were exploratory analyses, and the study was not powered to investigate such associations. The small sample size might have contributed to these negative findings, and hence, future studies with larger sample sizes could investigate the associations between social skills and executive functioning.

The present study has some limitations. The cross-sectional study design prevented us from drawing any causal inferences from the associations reported here. In addition, social skills were evaluated with a self-report instrument, which could be a source of bias related to how patients view their own social performance. Moreover, although the SSI has been validated for the Brazilian population, this is the first study to apply this instrument to individuals with BD, which raises questions about the validity of the instrument in this population as opposed to a more performance-based assessment. Furthermore, since we did not control for multiple comparisons, these findings should be considered as exploratory. The strengths of our study include the fact that the social skills were assessed using a standardized inventory validated for use in Brazil. This is relevant because social skills are significantly influenced by the culture of a given country.

In conclusion, euthymic BD patients with FHMD presented poorer social skills in specific areas, particularly conversational skills and social performance, than those without it. This impairment might be influenced by deficits in emotion processing, which has been shown to be altered in many BD studies. Because these social skills difficulties can affect an individual’s quality of life, further studies are needed to investigate how FHMD affects the social skills of BD patients.

We believe that there is a real need for neuropsychological interventions aimed at improving the effectiveness of social skills in BD patients. In addition, our findings suggest that BD patients belonging to families in which more than one member is affected by BD can be considered a subgroup to be targeted separately within the proposed intervention, since such patients present greater cognitive and social deficits.

References

  • 1
    Ketter TA. Diagnostic features, prevalence, and impact of bipolar disorder. J Clin Psychiatry. 2010;71:e14.
  • 2
    Fagiolini A, Kupfer DJ, Masalehdan A, Scott JA, Houck PR, Frank E. Functional impairment in the remission phase of bipolar disorder. Bipolar Disord. 2005;7:281-5.
  • 3
    Miklowitz DJ. Functional impairment, stress, and psychosocial intervention in bipolar disorder. Curr Psychiatry Rep. 2011;13:504-12.
  • 4
    Rosa AR, Reinares M, Franco C, Comes M, Torrent C, Sánchez-Moreno J, et al. Clinical predictors of functional outcome of bipolar patients in remission. Bipolar Disord. 2009;11:401-9.
  • 5
    Tucci AM, Kerr-Correa F, Dias RS. Social disability of Brazilian mood disorder patients. Braz J Med Biol Res. 2004;37:1713-20.
  • 6
    Rocca CC, Heuvel Ev, Caetano SC, Lafer B. Facial emotion recognition in bipolar disorder: a critical review. Rev Bras Psiquiatr. 2009;31:171-80.
  • 7
    Del Prette ZAP, Del Prette A. Avaliação de habilidades sociais: Bases conceituais, instrumentos e procedimentos. In: Del Prette A, Del Prette ZAP, editors. Psicologia das habilidades sociais: diversidade teórica e suas implicações. Petrópolis: Vozes; 2009. p. 187-229.
  • 8
    Gresham FM. Análise do comportamento aplicadas às habilidades sociais. In: Del Prette A, Del Prette ZAP, editors. Psicologia das habilidades sociais: diversidade teórica e suas implicações. Petrópolis: Vozes; 2009. p. 17-66.
  • 9
    Caballo VE, Irurtia MJ, Salazar IC. Abordagem cognitiva na avaliação e intervenção sobre habilidades sociais. In: Del Prette A, Del Prette ZAP, editors. Psicologia das habilidades sociais: diversidade teórica e suas implicações. Petrópolis: Vozes; 2009. p. 67-107.
  • 10
    Chang KD, Blasey C, Ketter TA, Steiner H. Family environment of children and adolescents with bipolar parents. Bipolar Disord. 2001;3:73-8.
  • 11
    Romero S, Delbello MP, Soutullo CA, Stanford K, Strakowski SM. Family environment in families with versus families without parental bipolar disorder: a preliminary comparison study. Bipolar Disord. 2005;7:617-22.
  • 12
    Belardinelli C, Hatch JP, Olvera RL, Fonseca M, Caetano SC, Nicoletti M, et al. Family environment patterns in families with bipolar children. J Affect Disord. 2008;107:299-305.
  • 13
    Antila M, Partonen T, Kieseppa T, Suvisaari J, Eerola M, Lonnqvist J, et al. Cognitive functioning of bipolar I patients and relatives from families with or without schizophrenia or schizoaffective disorder. J Affect Disord. 2009;116:70-9.
  • 14
    Girón M, Fernández-Yañez A, Mañá-Alvarenga S, Molina-Habas A, Nolasco A, Gomez-Beneyto M. Efficacy and effectiveness of individual family intervention on social and clinical functioning and family burden in severe schizophrenia: a 2-year randomized controlled study. Psychol Med. 2010;40:73-84.
  • 15
    Lucksted A, McFarlane W, Downing D, Dixon L. Recent developments in family psychoeducation as an evidence-based practice. J Marital Fam Ther. 2012;38:101-21.
  • 16
    First MB, Spitzer RL, Gibbon M, Williams JB. Entrevista clínica estruturada para o DSM-IV – transtorno do eixo I: edição para pacientes (SCID-I/P). New York: New York Biometrics Research; 1997.
  • 17
    Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry. 1960;23:56-62.
  • 18
    Young RC, Biggs JT, Ziegler VE, Meyer DA. A rating scale for mania: reliability, validity, and sensitivity. Br J Psychiatry. 1978;133:429-35.
  • 19
    Weissman MM, Markowitz JC, Klerman GL. Comprehensive guide to interpersonal psychotherapy. New York: Basic Books; 2000.
  • 20
    Del Prette, ZAP, Del Prette A. Inventário de habilidades sociais: manual de aplicação, apuração e interpretação. São Paulo: Casa do Psicólogo; 2001.
  • 21
    Burgess PW, Shallice T. The Hayling and Brixton tests. Test manual. Bury St Edmunds: Thames Valley Test Company; 1997.
  • 22
    Spreen O, Strauss E. Stroop test. In: Spreen O, Strauss E. A compendium of neuropsychological tests. New York: Oxford University; 1998. p. 213-8.
  • 23
    Spreen O, Strauss E. Controlled oral word association (FAS). In: Spreen O, Strauss E. A compendium of neuropsychological tests. New York: Oxford University; 1998. p. 447-64.
  • 24
    Wechsler D. Wechsler abbreviated scale of intelligence (WASI). San Antonio: Harcourt Brace E Company; 1999.
  • 25
    Goldstein TR, Miklowitz DJ, Mullen KL. Social skills knowledge and performance among adolescents with bipolar disorder. Bipolar Disord. 2006;8:350-61.
  • 26
    de Almeida Rocca CC, de Macedo-Soares MB, Gorenstein C, Tamada RS, Issler CK, Dias RS, et al. Social dysfunction in bipolar disorder: pilot study. Aust N Z J Psychiatry. 2008;42:686-92.
  • 27
    Depp CA, Mausbach BT, Harvey PD, Bowie CR, Wolyniec PS, Thornquist MH, et al. Social competence and observer-rated social functioning in bipolar disorder. Bipolar Disord. 2010;12:843-50.
  • 28
    Martini T, Czepielewski LS, Fijtman A, Sodré L, Wollenhaupt-Aguiar B, Pereira CS, et al. Bipolar disorder affects behavior and social skills on the Internet. PLoS One. 2013;8:e79673.
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Publication Dates

  • Publication in this collection
    26 Mar 2018
  • Date of issue
    Jul-Sep 2018

History

  • Received
    23 Apr 2017
  • Accepted
    28 July 2017
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