Is there a link between biological parents' insight into their offspring's schizophrenia and their cognitive functioning, expressed emotion and knowledge about disorder?

    Is there a link between biological parents’ insight into their offspring’s schizophrenia and their cognitive functioning, expressed emotion and knowledge about disorder? Alexandra Macgregor, Joanna Norton, St´ephane Raffard, Delphine Capdevielle PII: DOI: Reference:

S0010-440X(16)30331-5 doi: 10.1016/j.comppsych.2017.02.013 YCOMP 51818

To appear in:

Comprehensive Psychiatry

Please cite this article as: Macgregor Alexandra, Norton Joanna, Raffard St´ephane, Capdevielle Delphine, Is there a link between biological parents’ insight into their offspring’s schizophrenia and their cognitive functioning, expressed emotion and knowledge about disorder?, Comprehensive Psychiatry (2017), doi: 10.1016/j.comppsych.2017.02.013

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ACCEPTED MANUSCRIPT Is there a link between biological parents’ insight into their offspring’s schizophrenia and their

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cognitive functioning, expressed emotion and knowledge about disorder?

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Alexandra Macgregor a, b, *, Joanna Norton b, c, , Stéphane Raffard a, d, , Delphine Capdevielle a,b

University Department of Adult Psychiatry, La Colombière Hospital, Montpelier University

Hospital, Montpellier, France Montpellier University, Montpellier, France

c

INSERM U 1061, La Colombière Hospital, Montpellier, France

d

Epsylon Laboratory, EA4556, Montpellier, France

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b

* corresponding author

University Department of Adult Psychiatry, La Colombière Hospital, Montpelier University

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[email protected]

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Hospital, 39 Avenue Charles Flahault, 34295 Montpellier, Cedex 5, France

ACCEPTED MANUSCRIPT Abstract Background: Recent studies suggest that parents’ awareness of their offspring’s schizophrenia could influence their offspring’s insight. Low patient insight is linked to impairment of specific cognitive abilities, and biological parents of schizophrenia patients

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have impaired capacities in these same domains. However, little is known about what specific socio-demographic, affective or cognitive factors may influence biological parents’

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awareness of their offspring’s disease. Method: Data were drawn from 41 patient-parent dyads. Insight was assessed with a modified version of Amador's Scale to assess Unawareness of Mental Disorders, exploring dimensions of parents’ awareness and attribution of their offspring’s illness and symptoms. Results: Higher educational levels,

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better working memory and executive functioning of parents were associated with better attribution of their offspring’s symptoms to schizophrenia. Conclusions: Parents’ insight

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into their offspring’s schizophrenia is associated with cognitive abilities. This must be taken

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into account when developing family interventions.

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Keywords: schizophrenia; family; cognition; insight

ACCEPTED MANUSCRIPT 1. Introduction Poor insight in schizophrenia patients is of particular concern as it is associated with poor illness outcome [1]. Psychoeducational interventions are recommended as part of routine

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care, in order to try to improve patient disease awareness. However, some literature has associated higher insight levels in schizophrenia patients with higher scores of depression

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or with suicidal behaviour [2]. These controversial results could be explained by selfstigma moderating the association between insight and depression [3]. Self-stigma is the psychological impact at an individual level, of stigmatizing beliefs about mental illness in the general population. It has also been found to mediate the relationship between

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parents’ insight into their adolescents’ mental disorders and their sense of burden or stress [4,5]. Although much literature explores patient factors linked to poor awareness of disease, such as executive functioning [6] and dysfunction of self-reflection networks [7],

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very few studies have explored parental factors associated to patients’ insight. Research supports the view that parents’ perception of their offspring's illness could partially

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influence the way schizophrenia patients recognize their own symptoms and the consequences of their disorder. Indeed, several studies have found associations between

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patient insight and that of their caregivers [8, 9, 10, 11, 12]. Yet specific cognitive abilities

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associated to parental insight remain to date largely unexplored.

Early work on expressed emotions (EE) in families of schizophrenia patients found that those with high EE were less aware of their sick relatives’ illness [13]. Brent et al, also

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found an association between caregivers’ insight and Patient Rejection Scale (PRS) scores [14], reflecting EE levels [9]. In the general population, better knowledge about schizophrenia counterintuitively does not necessarily lead to less social distance or less stigma [15]. On the contrary information campaigns about the disease can lead to increased social distance. Therefore it seems important to explore whether knowledge about schizophrenia in patients’ parents is associated with parental insight their a offspring’s disorder in order to improve family interventions and adjust how information about the disease is presented. Patient insight has been associated with cognitive factors, namely executive functioning and working memory [16]. Given that healthy first-degree relatives of schizophrenia patients also present alterations in these cognitive domains, [17] one might expect to see a link between higher executive functioning scores and better insight scores in schizophrenia patients’ parents. There is further support for this in work on altered self-

ACCEPTED MANUSCRIPT reflection networks in healthy first-degree relatives of schizophrenia patients [18, 19] and in work on associations between parents’ cognitive insight (i.e. an individual’s current ability to examine and question beliefs and interpret experiences [20]) and executive parents’ awareness of their offspring’s schizophrenia.

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functioning [21]. Consequently, cognitive factors could also be involved in biological

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In light of these findings, our objective was to study factors associated with parental insight, more specifically the association between parental insight into their offspring’s schizophrenia and parents’ executive functioning performance, EE as measured by the PRS and knowledge about schizophrenia. Our hypothesis was that better cognitive

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performance, lower EE and better knowledge about schizophrenia would be associated with higher parental insight into their offspring’s illness. We further hypothesized that

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executive functioning and education would both have moderating effects on the relationship between EE and insight, better cognition or higher educational levels

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2. Subjects and Methods

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weakening the association between insight and EE.

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2. 1. Subjects and inclusion procedure

The Montpellier Insight Study recruited 41 patients, aged 18 to 60, with a DSM-IV

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diagnosis of schizophrenia [22]. Details on study design and methods are published elsewhere [8]. Fifty-two of their biological parents accepted to participate, mostly mothers. This data was used when possible. For 7 patients only the father’s data was available. Altogether, 41 patient-parent dyads were used in the analysis. The study was carried out in accordance with the Declaration of Helsinki and informed consent was obtained from all participants.

2. 2. Assessments Parents were assessed by a psychiatrist (AM), blind to patient assessment results except for the PANSS items for which the patients had a score of 3 or more [23], in order to be able to correctly assess insight (awareness of symptoms only assessed if patient sufficiently symptomatic). Each assessment lasted between 2.5 and 3.5 hours, and was conducted in a single session with up to two brief pauses, on parents’ request.

ACCEPTED MANUSCRIPT 2.2.1. Insight Insight into the patients’ current clinical state was assessed with a modified version of the Scale to assess Unawareness of Mental Disorders (SUMD) [24]. The scale is based on Amador’s multidimensional insight model, and has been used extensively throughout

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research on insight in schizophrenia. Five SUMD dimensions were considered in our study:

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 Awareness of mental illness

 Awareness of social consequences of mental illness  Awareness of treatment effect  Awareness of current symptoms

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 Symptom attribution

Each item was scored on a Likert scale of 1 (full awareness / correct attribution) to 5 (no

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awareness / incorrect attribution). Awareness of symptom was explored only if the patient was sufficiently symptomatic (ie. score ≥ 3 on the PANSS). High insight was defined as a score < 3. Psychometric properties of the original patient version of the scale are

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satisfactory with an interrater reliability ranging from 0.68 to 1.00 and internal consistency

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> 0.70 (Cronbach’s alpha) [25].

2.2.2. Cognitive functions

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2.2.2.1. Working memory

The Updating Paradigm [26] requires the participant to recall the last 6 letters of a series of

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6, 8, 10 or 12 letters read out loud. The participant does not know in advance the length of the series, thus obliging him / her to constantly update the last 6 letters memorized. For example, if letters « X, J, T, B, H, D, Z, R » are read out, the participant will update « XJTBHDZR … JTBHDZR…TBHDZR » and finally transcribe « TBHDZR ». The task comprises two series of 16 sequences after 8 practice series. Letters are accounted for only if they are correctly placed.

2.2.2.2 Mental flexibility The Wisconsin Card Sorting Test (WCST) is designed to study mental flexibility and abstraction capacities [27]. The participant is presented with 4 cards with figures, which differ in colour, number or shape. The participant has a deck of similar cards and must sort them into one of the four

piles represented by the four initial cards, according to a

category. The category (colour, number or shape) is not told to the participant, it must be deducted from the examiner’s « yes » or « no » responses to the participants sorting.

ACCEPTED MANUSCRIPT Once the participant successfully sorts ten consecutive cards, the examiner changes the category, without informing the participant. Scores taken into account in our study were

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number of categories successfully completed and perseverative errors.

2.2.2.3 Problem resolution

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The Behavioural Assessment of Dysexecutive Syndrome (BADS) is a battery of 6 ecological tests exploring dysexecutive syndrome (mental flexibility, problem solving, planning, judgment and behavioral regulation) which has frequently been used in research

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on schizophrenia. We used a simplified 5 test version, validated by Wilson et al. [28].

2.2.3. Expressed emotion (EE)

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EE was assessed in parents by a self-administered questionnaire, the PRS. Parents scored the frequency with which they felt certain emotions or adopted certain attitudes towards their offspring on a Likert scale from 1 (always) to 7 (never).

Of the 24

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statements, some are negative such as « I don’t expect much from X » some are positive, such as « I enjoy being with X ». Higher scores reveal more rejecting attitudes. The PRS

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score has been linked to relapse and to the Camberwell Family Interview assessment of EE, recognized as a gold standard for EE assessment [14]. Based upon a sample of 133

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outpatients diagnosed with schizophrenia and their family members, the scale demonstrates a moderately high reliability (?? = 0.78) and test-retest correlation (r = 0.72).

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The questionnaire was translated into French for the purpose of the Montpellier Insight Study by a team of experienced bilingual medical translators .

2.2.4. Knowledge about schizophrenia Knowledge about schizophrenia was explored with the French translation of the Knowledge About Schizophrenia Test (KAST), which covers the origins of schizophrenia; its symptoms and treatment in 18 multiple-choice questions. In a population of 441 people of which 77 family members of schizophrenia patients, it demonstrated good internal consistency, reliability (reliability coefficient KR-20 of 0.82) and construct validity. For 39 family members, scores were directly correlated with scores on the concurrent criterion measure, the Knowledge of Schizophrenia true/false questionnaire developed for caregivers (r=0.48; p<0,01) [29, 30]. Again, the questionnaire was translated into French for the purpose of the study.

ACCEPTED MANUSCRIPT 2. 3. Statistical analysis The sample is described using percentages for categorical variables and the median and range for continuous variables with skewed distributions. Normality was tested using the Shapiro-Wilk test. Spearman’s correlation coefficient was used to examine correlations

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between continuous non-normal variables.

Insight was analyzed as a binary variable comparing high insight (score<3) to low insight.

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Associations between insight and socio-demographic and cognitive functions as well as expressed emotions were examined using logistic regression analysis. Independent variables were entered as continuous variables, after testing the linearity of their relationship with insight. Only the number of categories completed on the WCST was

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defined as a binary variable (<6 versus >6) as 75% of patients had a score of 6. For symptom attribution, interactions were tested between variables significantly associated

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with insight only, that is, education level and working memory and BADS IQ, respectively. Statistical analyses were performed with SAS version 9.4 (SAS Institute. Inc. Cary. North-

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Carolina).

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3. Results

Patient and parent characteristics are described in Table 1.

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A large majority of parents had high insight (score < 3) for the first three SUMD dimensions (90 to 97%). Given the very low numbers in the poor insight categories, we

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were not able to explore factors associated with insight for these dimensions. Of parents with high awareness of symptoms and/or high symptom attribution (n=38/41), 63.2% had high insight in both dimensions: 18.4% on symptom awareness only and 18.4% on symptom attribution only. Table 2 shows associations between parent factors and parental insight for the last two SUMD dimensions: symptom awareness and attribution. None of the studied variables were significantly associated with parents’ awareness of their offspring’s symptoms. For parental symptom attribution, higher scores on the BADS (98 [79-123] vs 80.5 [58-117] p=0.01), better working memory (24 [12-33.5] vs 18.8 [12.5-22] p=0.008) and higher educational level (14 [9-18] vs 10 [5-16] p=0.01) were all associated with high insight. Given the strong co-linearity between these three variables (between educational level and working memory: r=0.59 p=0.0001; between education level and BADS IQ: r=0.44 p=0.005; between working memory and BADS IQ: r=0.43 p=0.007), they were not entered simultaneously into a multivariate logistic regression model.

ACCEPTED MANUSCRIPT Interactions between educational level and working memory, and between educational level and BADS IQ on insight were not significant.

4. Discussion

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Our study is the first to show an association between parents’ attribution of their offspring's symptoms and cognitive performance in two domains: working memory and executive

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functioning. Brent et al. did not find an association between caregiver insight and working memory scores with a similar test, despite all caregivers being first-degree biological relatives [9]. This could be due to Brent’s smaller sample size (14 caregivers) or to the younger age in the caregiver group (42.3 years) thus reducing the chance of cognitive

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dysfunction. Our results support previous findings from the Montpellier Insight Study, namely that the cognitive insight of schizophrenia patients’ biological parents was

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associated with executive functioning [21]. Both of these results support the introduction of cognitive remediation techniques in family interventions.

The objective would be to

reduce healthy first-degree relatives’ cognitive biases and thus improve their cognitive

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insight but also their capacity to correctly attribute patients’ symptoms to schizophrenia. None of the factors we studied were associated to parents' awareness of symptoms. This

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could be due to high insight scores in this dimension among our parent group. This result is also in favour of different cognitive processes underlying awareness and attribution, thus

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supporting the multidimensional model of insight [31].

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Contrary to Brent’s study, we did not show a significant association between parental insight and parents’ critical attitudes assessed with the PRS, even though median PRS scores were similar in the two studies. This may be due to the higher levels of parental insight in our study, or due to the fact that not all the parents in our study had caregiver status. Indeed, parents with less contact with their ill offspring could have less rejecting attitudes due to distance, yet still have low insight into the disease. Furthermore, the gold standard for assessment of EE is the Camberwell Family Interview. The use of a selfreport measure with the PRS could lead to inaccurate exploring of the relationship between insight and EE in patients’ parents. Nonetheless we have demonstrated elsewhere that parental attitudes are associated to patient insight thus supporting the need for family interventions. By reducing EE levels among parents, family interventions can improve disease outcome as well as patient-parent relationships and patients’ disease awareness [8, 32].

ACCEPTED MANUSCRIPT Contrary to our hypothesis, parental knowledge about schizophrenia was not associated with parental insight. This could partially be due to high KAST scores and lack of variability, the median being at 16 out of 18. High levels of knowledge may be secondary to participation bias in our study as the questionnaire was originally tested in a sample of

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57 family members of schizophrenia patients with a mean score of 10.9 out of 18 [29]. Also, as increasing information about the disease is not sufficient to reduce stigma in the

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general population [15], better knowledge may not be sufficient to improve awareness or attribution capacities in a group of parents. This supports current recommendations stating more is expected of family interventions than merely providing facts and figures about the

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disease.

As mentioned in the introduction, care must be taken when patient insight improves,

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because many studies have associated better awareness of disorder to higher depression or higher risk of suicide [2]. Nonetheless, moderator variables of this association such as self-stigma, can be explored and addressed, in order to sufficiently support patients going

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through the process of increasing their awareness of their schizophrenia. The same should be said for parents and their insight into offspring’s disease: if better insight has been

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associated to greater stress or sense of burden, these issues can nonetheless be explored and taken into account during family interventions [4,5]. Altogether, improving patient and

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parental insight appears as an essential step on the pathway to positive disease outcome.

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Our study has several limitations, namely patients and parents who accepted to participate had to have sufficiently good insight in order to do so, thus explaining the very high rates of parental insight in the first three SUMD dimensions. This prevented us from studying factors associated to these domains. Furthermore, our modified parent version of the SUMD was not tested prior to the study. However it has been used previously in research on parent insight into offspring’s schizophrenia and performed well [9, 12]. Despite firstdegree relatives of schizophrenia patients having an increased risk of psychosis [33], the absence of psychotic disorders in the parent group in our study meant we were not able to study the impact of family history of psychosis or parental psychopathology on insight. The lack of parental psychopathology in our parent group is no doubt due to participation bias. Finally, our sample size is relatively small and further studies are warranted for results to be replicated in a larger group of first-degree biological relatives.

ACCEPTED MANUSCRIPT 5. Conclusions The Montpellier Insight Study is the first to explore, in a group of 41 biological parents, factors associated to insight into their offspring’s schizophrenia. Just as insight in patients is associated to cognitive functioning, it appears that parents’ capacity to correctly attribute

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their offspring's symptoms to disease, is higher among those with better cognitive performance and higher educational levels. These results are of major importance when

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discussing patients’ care with their relatives or when trying to improve patient insight via family interventions. Indeed, cognitive remediation techniques could enhance such programs in an attempt to overcome parents’ difficulties in correctly attributing patients’

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symptoms to their schizophrenia.

Ethical standards

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The study was approved by the French ethics committee and was carried out in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. All participants gave their informed consent prior to their inclusion in

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the study. Conflicts of interest

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Acknowledgments

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The authors declare that they do not have any conflicts of interest.

The authors would like to thank all the patients and their parents who participated in the

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Montpellier Insight Study. The authors also thank Montpellier University Hospital who financed the project.

Role of funding source This study was financed by Montpellier University Hospital who otherwise had no role in the recruitment of patients, the data collection, analysis or publication.

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ACCEPTED MANUSCRIPT Table 1. Socio-demographic and clinical characteristics of study population

40 18 18 8 8

0 0 6 0 10

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Insight assessment: high insight (score<3) Awareness of illness Awareness of treatment effect Awareness of social consequences Awareness of symptoms Attribution of symptoms Cognitive assessment: Updating score (median [min-max]) WCST (median [min-max]) Nb of categories completed Nb of perseverative errors % of perseverative errors BADS score (median [min-max]) Parent factors: KAST score (median [min-max]) PRS total score (median [min-max]) Parent personal history of axis I disorder : Psychotic disorder Mood disorder Anxious disorder

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Parents N = 41 n % 7 17.1 39 58 [43-75] 39 12 [5-18] 18 43.9 7 17.1

600 [60-3500] 20 [5-120] 43.9 19.5 19.5

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Sex (male) Age (years) (median [min-max]) Education (years) (median [min-max]) Family situation (single) Living alone Duration of illness(years) (median [min-max]) Psychotropic treatment : Chlorpromazine eq (mg) (median [min-max]) Diazepam eq (mg) (median [min-max]) Benzodiazepine Corrector Antidepressant PANSS (median [min- max]) Positive symptom subscale Negative symptom subscale General psychopathology subscale Total score Cannabis abuse/dependency Alcohol abuse Specific psycho-educational intervention Days of contact/month (median [min-max])

Patients N= 41 n % 34 82.9 39 29 [20-53] 39 11 [8-17] 41 100 19 46.3 41 10 [1-34]

0 0 14.6 0 24.4

14 [7-31] 17 [7-33] 35 [23-55] 67 [43-99] 19.5 4.9 39.0

15 [1-31]

41 41 41 41 41

61.0 68.3 56.1 51.2 46.3

41 41 41 41 41

97.6 97.6 90.2 75.6 75.6

37

23.8 [6-37]

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22 [12-33.5]

39 39 39 39

6 [1-6] 10 [3-65] 11.1 [4.3-50.8] 86 [43-124]

39 6 [3-6] 39 10 [3-37] 39 10.4 [4.3-28.9] 39 98 [58-123]

41 40 20 0 17 6

16 [8-18] 58 [36-121] 48.8 0 41.5 14.6

PANSS : Positive and Negative Symptom Scale ; KAST : Knowledge about Schizophrenia Test ;

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PRS : Parent Rejection Scale ; WCST : Wisconsin Card Sorting Test ; BADS Behavioural Assessment of Dysexecutive Syndrome (IQ equivalent)

ACCEPTED MANUSCRIPT Table 2. Associations between parents’ socio-demographic, clinical and cognitive factors and parents' symptom awareness and attribution levels Awareness of symptoms

median [min-max]

median [min-max]

58.5 [50-66]

57 [43-75]

13 [9-16]

12 [5-18]

Parents’ socio demographic factors Age

High insight (N=31)

median [min-max]

median [min-max]

0.78

58.5 [43-69]

58 [46-75]

0.32

0.75

10 [5-16]

14 [9-18]

0.01

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Years of education

Low insight (N=10)

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High insight (N=31)

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Low insight (N=10)

Symptom attribution

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Clinical factors

15.5 [8-17]

16 [8-18]

0.65

14 [8-18]

16 [8-18]

0.11

Expressed Emotion (PRS)

58 [36-88]

58 [36-121]

0.77

58.5 [36-74]

58 [36-121]

0.32

23 [19.8-33.5]

22 [12-31.3]

0.45

18.8 [12.522]

50.0

80.7

0.10

70.0

74.2

0.79

WCST: Number of perseverative errors

12 [5-37]

9 [3-36]

0.24

21 [3-36]

7 [4-37]

0.04

WCST: Percentage of perseverative errors

14.3 [6.828.9]

10.3 [4.328.6]

0.35

19.3 [4.328.6]

8.6 [5.928.9]

0.05

93 [73-117]

98 [58-123]

0.75

80.5 [58117]

98 [79-123]

0.01

CE

Updating score

PT

Parent’s cognitive functions

ED

Knowledge about schizophrenia (KAST)

AC

WCST: Number of categories completed (>6) (%)

BADS IQ equivalent

24 [12-33.5] 0.008

* from logistic regression analysis Note: High insight = score < 3 KAST = Knowledge about Schizophrenia Test; PRS = Patient Rejection Scale ; WCST = Wisconsin Card Sorting Test ; BADS = Behavioural Assessment of Dysexecutive Syndrome