Social functioning in adults with neurofibromatosis type 1

Research in Developmental Disabilities 34 (2013) 3393–3399

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Research in Developmental Disabilities

Social functioning in adults with neurofibromatosis type 1 Natalie A. Pride a,b,**, Hilda Crawford b, Jonathan. M. Payne a,b, Kathryn N. North a,b,c,* a

The Institute for Neuroscience and Muscle Research, The Children’s Hospital at Westmead, Locked Bag 4001, Westmead, NSW 2145, Australia b Discipline of Paediatrics and Child Health, Faculty of Medicine, The University of Sydney, NSW 2006, Australia c Murdoch Children’s Research Institute, Royal Children’s Hospital, Parkville, VIC 3062, Australia

A R T I C L E I N F O

A B S T R A C T

Article history: Received 13 May 2013 Received in revised form 7 July 2013 Accepted 9 July 2013 Available online 2 August 2013

Neurofibromatosis type 1 (NF1) is a common single-gene disorder characterised by a diverse range of cutaneous, neurological and neoplastic manifestations. It is well recognised that children with NF1 have poor peer interactions and are at risk for deficits in social skills. Few studies, however, have examined social functioning in adults with NF1. We aimed to determine whether adults with NF1 are at greater risk for impairment in social skills and to identify potential risk factors for social skills deficits. We evaluated social skills in 62 adults with NF1 and 39 controls using self-report and observer-report measures of social behaviour. We demonstrate that adults with NF1 exhibit significantly less prosocial behaviour than controls. This deficit was associated with social processing abilities and was more evident in males. The frequency of antisocial behaviour was comparable between the two groups, however was significantly associated with behavioural regulation in the NF1 group. These findings suggest that poor social skills in individuals with NF1 are due to deficits in prosocial behaviour, rather than an increase in antisocial behaviour. This will aid the design of interventions aimed at improving social skills in individuals with NF1. ß 2013 Elsevier Ltd. All rights reserved.

Keywords: Neurofibromatosis type 1 Social skills Cognitive deficits Social cognition

1. Introduction Neurofibromatosis type 1 (NF1) is an autosomal dominant disorder with an estimated frequency of 1 in 2700 births that occurs equally across genders and ethnic groups (Evans et al., 2010). The most common clinical manifestations involve the skin and include cafe´ au lait spots, axillary and groin freckling and cutaneous peripheral neurofibromas. Common complications include central nervous system tumours, scoliosis, and plexiform neurofibromas (Korf, 2002). There is considerable variation in the clinical manifestations of NF1, even within the same family, with some individuals displaying a mild phenotype and others with more severe physical complications. Cognitive deficits are the most common feature of NF1 but are also highly variable between individuals. Intellectual impairment is present in 6–7% of patients (Ferner, Hughes, & Weinman, 1996; Hyman, Shores, & North, 2005), 30–50% satisfy the diagnostic criteria for attention deficit hyperactivity disorder (ADHD) (Hyman et al., 2005; Kayl, Moore, Slopis, Jackson, & Leeds, 2000; Mautner, Kluwe, Thakker, & Leark, 2002; Pride, Payne, & North, 2012), and up to 80% have either learning disability or deficits in executive or visuospatial function (Hofman, Harris, Bryan, & Denckla, 1994; Hyman, Shores, & North, 2006; Hyman et al., 2005; Krab et al., 2008; Pavol et al., 2006). * Corresponding author at: Murdoch Children’s Research Institute, Royal Children’s Hospital, 50 Flemington Road, Parkville, VIC 3062, Australia. Tel.: +61 3 8341 6226; fax: +61 3 9348 1291. ** Corresponding author at: The Institute for Neuroscience and Muscle Research, The Children’s Hospital at Westmead, Locked Bag 4001, Westmead, NSW 2145, Australia. E-mail addresses: [email protected] (N.A. Pride), [email protected] (K.N. North). 0891-4222/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ridd.2013.07.011

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While a considerable amount of research has focused on the cognitive sequelae of NF1, the psychosocial impact of the disorder has received less attention. Studies of social functioning have typically employed broader behavioural ratings such as the Child Behaviour Checklist (CBCL) and demonstrate that children with NF1 have significantly more social problems (such as loneliness, clinginess, immaturity) than unaffected children (Dilts et al., 1996; Johnson, Saal, Lovell, & Schorry, 1999; Noll et al., 2007). Social skills have been measured more directly in children with NF1 with mixed results. Noll et al. (2007) assessed social behaviour and peer acceptance in children with NF1 and unaffected peers using teacher, peer and self-report on the Revised Class Play instrument. While children with NF1 did not have lower self-ratings, they were perceived by teachers and peers as displaying less leadership behaviour, as more sensitive and isolated, and less well liked than comparison children. In contrast, Barton and North (2004) found no difference in social skills between children with NF1 when compared to unaffected siblings (measured by the Social Skills Rating System) (Barton & North, 2004). There is evidence for elevated symptoms of autism spectrum disorder (ASD) in children with NF1, with recent evidence suggesting that 14–29% of children with NF1 display severe levels of symptomatology that have been associated with a diagnosis of ASD (Garg et al., 2012; Walsh et al., 2012). Despite significant social problems in children with NF1 and evidence that adults with the condition frequently struggle to maintain interpersonal relationships (Ablon, 1996), research into the nature of social functioning in adults with NF1 is limited. The burden of NF1 on social functioning has been highlighted by interviews of adult patients (Ablon, 1996; Benjamin et al., 1993; Hummelvoll & Antonsen, 2013; Samuelsson & Riccardi, 1989); reduced social networks, feelings of loneliness, and more social problems such as social withdrawal, are reported by adults with NF1 as a major concern. Nonetheless, there have been no quantitative studies to date that have examined the social skills of adults with NF1 or the underlying reasons for impaired social functioning. A key issue in this regard is whether adults with NF1 are aware of their deficits; previous studies in children with NF1 have shown that they have limited insight into their social abilities (Barton & North, 2004; Noll et al., 2007). It is also unclear whether comorbidity for cognitive impairment or more severe physical manifestations of the disorder contribute to deficits in social functioning. On this basis, we sought to compare social skills between a sample of adults with NF1 and a sample of unaffected adults using the Social Performance Survey Schedule (SPSS). We hypothesised that social deficits will be a common feature of adulthood NF1 and that adults with NF1 would exhibit poorer awareness of any deficit in social skills. We also aimed to determine how disease severity, demographic and cognitive variables (executive functions, IQ, social processing) relate to social functioning in adults with NF1. 2. Materials and methods 2.1. Participants Adults who satisfied the diagnostic criteria for NF1 based on a National Institutes of Health (NIH) statement (NIH, 1988) were identified from Neurogenetic Clinic databases from hospitals within local urban and suburban regions including Royal North Shore Hospital, Westmead Hospital and The Children’s Hospital at Westmead. Individuals with NF1 were also recruited via an online advertisement on The Children’s Tumour Foundation of Australia website. Medical files were examined to determine eligibility for participation. Exclusion criteria for NF1 patients were as follows: (1) less than 18 years or more than 60 years of age, (2) insufficient understanding of the English language, (3) history of co-existing genetic or neurological condition, (4) abnormal vision or hearing that could not be corrected to normal and (5) unable to complete questionnaires independently. Of the 81 NF1 patients contacted, 14 refused to participate, and five were excluded due to either insufficient language abilities (n = 2), severe psychiatric disturbance i.e. psychosis (n = 1), or insufficient reading abilities to complete the questionnaire (n = 2). Thus, 62 NF1 patients participated in the study. In order to provide a modern comparison group for this study, we recruited 39 unaffected adults between the ages of 18 and 60 from local urban and suburban areas. Participants were recruited from a variety of sources: (1) normal individuals recruited from the wider community via advertisements (n = 22), (2) parents of unaffected children who were controls in a concurrent study examining the cognitive phenotype of toddlers with NF1 (n = 15), (3) parents of children with sporadic NF1 (non-familial) who were seen at the hospital’s Neurogenetic Clinic (n = 2). Control participants were excluded from the study based on the same exclusion criteria used for NF1 patients. Control participants with a reported psychiatric history (e.g. ASD, ADHD, psychiatric disturbance) were additionally excluded. 2.2. NF1 disease severity Clinical severity of NF1 was rated with Riccardi’s severity scale (Riccardi & Kleiner, 1977). Grade 1 indicates that few features of NF1 are present with no compromise of health (e.g. cafe´ au lait spots and freckling only). Grade 2, or mild NF1, indicates physical signs of NF1 that are obvious to others and are a concern, but without significant compromise of health. Grade 3, or moderate NF1, indicates a significant compromise of health but symptoms can be managed reasonably well. Finally, Grade 4, or severe NF1, indicates the presence of serious compromise that is intractable, is managed or treated only with difficulty and is associated with a shortened life span. Severity was assigned retrospectively from patient medical files and interview transcripts. One investigator (N.P.) and a clinical geneticist (both who have extensive experience with the clinical management of NF1 patients), rated severity in 15 of the same NF1 participants to establish inter-rater reliability.

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Inter-rater reliability determined by Pearson correlation coefficient was r = 0.81. Sufficient clinical information necessary to score severity was not available in 12 cases. 2.3. Social functioning The Social Performance Survey Schedule (SPSS; Lowe & Cautela, 1978) is a 100 item questionnaire developed to assess antisocial and prosocial behaviour. Participants were required to rate the frequency with which they engage in each of the 100 behaviours on a 5-point (0–4) scale ranging from ‘‘not at all’’ to ‘‘very much’’. Fifty items include behaviours associated with prosocial traits (e.g. warm, sympathetic, sensitive) such as ‘‘uses eye contact when speaking’’, and ‘‘shows interest in what another is saying’’. Fifty items include behaviours associated with antisocial traits (e.g. manipulative, rude, insensitive) such as ‘‘interrupts often’’, ‘‘gets into arguments’’, ‘‘makes embarrassing comments’’. This questionnaire has been used in several populations including students (Lowe, 1985), patients with traumatic brain injury (Long, McDonald, Tate, Togher, & Bornhofen, 2008; Macdonald, Flanagan, Martin, & Saunders, 2004), and patients with psychiatric disturbance (Lowe, 1982). It has a self and observer form, high internal consistency (a = .94) and re-test reliability (r = .87; Lowe & Cautela, 1978) as well as established validity in psychiatric and student populations (Lowe, 1982, 1985). While there is normative data for this scale, it is limited to a 1978 US-based student sample; hence the need to include a ‘‘modern’’ control sample to provide a comparison for current social behaviour. An observer-report version was also administered and completed independently by a significant other (family member/friend). The following scores are produced by this measure; self-reported prosocial behaviour; self-reported antisocial behaviour; observer-reported prosocial behaviour; and observer-reported antisocial behaviour. Scores measuring antisocial behaviour are ‘‘reversed-scored’’, so higher scores on all four scales reflect higher social competence. Scores range from 0 to 200 for each scale and are a summation of the questionnaire items. 2.4. Cognition and social processing A subset of the NF1 (n = 20) and control group (n = 20) underwent cognitive testing. The Wechsler Adult Intelligence Scale Version 3 (WAIS-III) was administered to assess general intelligence (Wechsler, 1997) and a Full-Scale IQ (FSIQ) was generated (M = 100; SD = 15). The Behaviour Rating Inventory of Executive Function – Adult Version (BRIEF-A) was also administered to the NF1 patients who underwent cognitive testing. This self-report scale of executive functions provides two composite index scores; Behavioural Regulation Index (BRI) and Metacognition Index (MI). BRI consists of four subscales (Inhibit, Shift, Emotional Control, Self-Monitor), while MI consists of five subscales (Initiate, Working Memory, Plan/ Organise, Task Monitor, and Organisation of Materials), each generating a T score (M = 50, SD = 10) (Roth, Isquith, & Gioia, 2005). The Emotion Evaluation Test (EET) from The Awareness of Social Inference Test-Form A (TASIT) (Macdonald, Flanagan, Rollins, & Kinch, 2003) was administered to examine social processing. The EET uses 28 professionally enacted video vignettes lasting 20–30 s in which an actor portrays either a positive (happiness, surprise) or a negative (sadness, anger, disgust, fear) emotion. Participants were required to state the emotion portrayed based on response cards which contained each of the emotions in a random order. The EET produced a score that measures the respondents’ ability to identify positive emotions and a score that measures their ability to identify negative emotions. A maximum score of 8 and 16 could be obtained for the positive and negative subscales respectively. 2.5. Procedure Participants were mailed a study information sheet and a follow-up phone call was made to answer any questions about the study. Those who agreed to participate took part in an initial intake interview either at the hospital or at their home. This was to confirm disease severity (for NF1 participants only), and to ascertain a history of psychiatric disturbance or comorbid pathology. Participants were provided with an envelope containing the questionnaires, with a cover letter requesting that the participant and a friend or family member who knows them well complete each questionnaire independently and return in a reply paid envelope. Detailed administration instructions for the questionnaire were included in the package. Cognitive testing was completed at the Children’s Hospital at Westmead by a clinical neuropsychologist (N.P.). Socio-economic status (SES) was measured by the Index of Relative Socio-Economic Advantage and Disadvantage, derived from Australian census data (Australian Bureau of Statistics, 2006). Written informed consent was obtained from all participants prior to enrolment and the study was approved by The Children’s Hospital at Westmead Human Research Ethics Committee (08/CHW/74). 2.6. Statistics Prior to analysis, the variables were screened for violations of the assumptions associated with univariate tests. When appropriate, tests were examined for the presence of outliers, homogeneity of variance–covariance, and multicollinearity. To test our primary hypothesis, analysis of variance (ANOVA) was used to assess group differences on the SPSS scales. Analysis of covariance (ANCOVA) was also used to assess group differences after controlling for demographic variables (age, SES, gender, level of education). To determine awareness of social abilities, a paired t test was used to compare self-ratings versus observer-ratings in each group. To assess our final objective, Pearson correlations were used to assess bivariate relationships

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Table 1 Demographic details for NF1 and control groups. Variable

NF1

Control

Age, mean (SD) y:m Sex, n (%) Male Female Education, n (%) Less than high school gradate High school graduate Some post-secondary education University graduate and beyond Socio-economic Scale, mean (SD) Disease severity, mean (SD)

29:5 (7:1)

32.9 (8:1)

29 (47) 33 (53)

15 (38) 24 (62)

12 (19) 15 (24) 21 (34) 14 (23) 6.3 (3.11) 2.36 (0.79)

1 (3) 11 (28) 11 (28) 16 (41) 6.9 (3.31)

between SPSS scores and cognitive, disease and demographic variables. Analyses were considered exploratory and alpha set at .05. 3. Results 3.1. Demographic variables Demographic details for the NF1 and control groups are shown in Table 1. The ratio of males to females in the two groups did not differ significantly, x2 = 0.67, df = 1, p = .412. SES was also not found to be significantly different between groups (t(99) = .88, p = .38). The NF1 group, however, received less formal education than the control group x2 = 8.38, df = 3, p = .039 and were younger (t(99) = 2.58, p = .011). The relationship of the observer (observer status) in the NF1 cohort differed to relationships in the normative sample, x2 = 13.64, df = 2, p  0.001. In the NF1 cohort the majority of observers rating the participant were partners (31; 50%), followed by parents (25; 40%), and friends (6; 10%). In the normative sample, the majority of observer raters were partners (20; 56%), followed by friends (12; 33%), and parents (4; 11%). In order to check whether observer status affected SPSS scores, we used one-way (between groups) ANOVAS to compare observer status for each of the four SPSS scales. These analyses were performed in each group separately using an alpha level of .05 to determine significant group effects. There were no differences between observer status for any of the scales, indicating the relationship of the observer to the NF1 participant did not influence their ratings (all, p > .05). 3.2. Social functioning Mean SPSS performance of the NF1 and control group as well as the rate of impairment are detailed in Table 2. Observerreported prosocial behaviour was significantly lower in the NF1 group than the control group (F(1, 96) = 21.87, p < .001); a difference that remained after gender, age, SES and education were entered as covariates (F(4, 93) = 16.97, p < .001). There was no group differences in self-reported prosocial behaviour (F(1, 99) = .91, p = .345), self-reported antisocial behaviour (F(1, 99) = 3.26, p = .075), or observer-reported antisocial behaviour (F(1, 96) = 1.10, p = .297). There was a significant difference in observer-reported prosocial behaviour between genders in the NF1 group (F(2, 60) = 6.46, p = .014) with males with NF1 rated significantly worse than females. This gender difference was not present in the control group (F(2, 34) = 1.89, p = .179). To determine the participant’s awareness of their social abilities, a paired t test was used to compare self-reported versus observer-reported scores in each group. While adults with NF1 rated themselves as displaying significantly more prosocial behaviour than observer ratings (t = 2.2, p = .030), the opposite pattern was found in control participants, where participants

Table 2 Social Performance Survey Schedule (SPSS) raw scores for the NF1 and control group. SPSS scale

Self-reported prosocial Self-reported antisocial Observer-reported prosocial Observer-reported antisocial

Adults with NF1 (n = 62)

Controls (n = 39)

M (SD)

%  1 SD

M (SD)

%  1 SD

125.0 (26.5) 159.03 (19.2) 113.89 (30.7)** 158.74 (27.5)

34 15 48 21

131.72 (18.1) 154.78 (16.0) 142.89 (27.7)a 164.0 (23.2)a

10 15 19 21

Mean (M) and standard deviation (SD) of SPSS raw scores. The percentage of participants who scored more than one standard deviation below the control mean is also provided for each group. a Four adults did not complete this scale. ** p < 0.01.

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Table 3 Cognitive and social processing scores for the NF1 and control group. Variable

NF1 (n = 20)

Control (n = 20)

% of NF1 adults 1 SD < mean

Full-Scale IQ BRIEF-A, M(SD) BRI MI TASIT EETb Positive emotions Negative emotions

98.68 (16.44)

108.43 (10.69)

21.1

56.26 (10.95) 60.65 (11.36) 6.72 (1.32) 14.12 (.96)

52.6 55.0 7.56 (.70) 14.67 (.97)

27.8a 22.2a

Mean (M) and standard deviation (SD) of standardised cognitive and raw social processing scores. The percentage of NF1 participants who scored more than one standard deviation below the normative mean is also provided. BRIEF-A: Behaviour Rating Inventory of Executive Function Adult Self-Report Version; BRI: Behaviour Regulation Index; MI: Metacognition Index; TASIT EET: The Awareness of Social Inference Test Emotion Evaluation Test. a % impairment based on control group mean average and standard deviation. b Two participants from each group did not complete this test.

reported significantly less prosocial behaviour compared to observer ratings (t = 2.4, p = .025). Self and observer-reported antisocial behaviour did not differ significantly in the NF1 group (t = .02, p = .98). For controls, observer-reported antisocial behaviour was significantly lower compared to self-reported antisocial behaviour (t = 3.2, p = 0.03). 3.3. Cognition and social processing Table 3 shows the descriptive statistics for the cognitive and social processing measures, as well as the percentage of participants scoring more than one standard deviation below the normative mean for each test. The mean FSIQ was in the average range for each group, although significantly lower in the NF1 group than controls (t(38) = 2.24, p = .031). In terms of BRIEF-A performance, the Metacognition Index (BRIEF-A MI) T score was more than one standard deviation from the normative mean in more than half (55%) of the NF1 participants who completed this measure, suggesting a high rate of impairment in this group. A high rate of impairment (50%) was also observed on the Behavioural Regulation Index (BRIEF-A BRI) in those with NF1. On the EET, the NF1 group were significantly worse at identifying positive emotions than the control group (t(34) = 2.7, p = .024). There was no significant difference between groups in their ability to identify negative emotions (t(34) = 1.73, p = .94). 3.4. Disease severity Disease severity ratings were completed for 50 adults. Scores ranged from 1 to 4. The mean clinical severity of the NF1 group was 2.36 (SD = .79); similar to severity levels reported in other adult NF1 cohorts (Wolkenstein et al., 2009). There was no significant difference in disease severity found between males (mean = 2.5, SD = .78) and females (mean = 2.2, SD = .78) with NF1 (F(1, 48) = 1.10, p = .30). 3.5. Relationship between social, cognitive and demographic variables A significant relationship emerged between age and self-reported prosocial behaviour in the NF1 group (r = .03, p = .011), suggesting older adults with NF1 rate themselves more poorly than younger adults. A lower SES status was also found to be associated with more frequent self-reported antisocial behaviour in the NF1 group (r = .07, p = .049). Level of education, disease severity, and FSIQ scores were not associated with SPSS scores (Table 4). BRI scores were significantly correlated with self-reported antisocial behaviour. Specifically, adults with NF1 who rated themselves as more antisocial also demonstrated more severe deficits in executive functions (r = .58, p = .012). In terms of social processing (EET), poorer recognition of negative emotions was associated with less frequent self-reported prosocial behaviour in the NF1 group (r = .57, p = .014). This association was not evident in the control group (r = .18, p = .467). 4. Discussion Poor social skills are common in children with NF1 and this study confirms that these problems continue into adulthood. Adults with NF1 were perceived by family members/friends as experiencing deficits in their social skills. While the frequency of antisocial behaviour did not differ significantly between groups, we found that adults with NF1 were perceived as demonstrating less prosocial behaviour than unaffected adults, with almost half of adults with NF1 (48%) rated within the impaired range. Interestingly, this problem was more pronounced in males, supporting findings from a qualitative study in which 32 females and 19 male adults with NF1 were interviewed on their attitudes and lifestyle (Ablon, 1996). Ablon reported that while less than a quarter of female participants in her study were single, a large proportion (more than half) of the male cohort were single and had ‘‘retreated from social life early on’’. Women with comparable severity from this previous adult cohort did not seem to have the same level of social difficulties as males.

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Table 4 Correlation coefficients between SPSS scores and cognitive, disease and demographic variables for the NF1 group. Variable Age Education Disease severity SES FSIQ BRIEF-A BRI BRIEF-A MI EET positive EET negative

Self-reported prosocial .32 .07 .07 .07 .08 .20 .29 .29 .05

**

Self-reported antisocial .01 .06 .09 .27* .01 .58* .15 .25 .02

Observer-reported prosocial .14 .11 .12 .07 .45 .27 .25 .07 .57*

Observer-reported antisocial .12 .01 .07 .19 .19 .28 .27 .03 .05

SES: Socio-economic Scale; FSIQ: Full Scale IQ; BRIEF-A: Behaviour Rating Inventory of Executive Function Adult Self Report. BRI: Behaviour Regulation Index; MI: Metacognition Index; EET: Emotion Evaluation Test. Lower scores on BRIEF-A indicate better performance. * p < .05. ** p < .01.

Consistent with our hypothesis as well as findings from paediatric studies (Barton & North, 2007; Noll et al., 2007), adults with NF1 demonstrated reduced awareness of deficits in social skills. Significantly less prosocial behaviour and a higher rate of impairment in this area were reported by family members and friends of adults with NF1 compared to self-reports. The opposite pattern was seen in control participants. This finding may have implications for future interventions aimed at improving the expression of prosocial behaviour in NF1. In other clinical populations (e.g. traumatic brain injury, dementia), awareness of deficits is a strong predictor of social-functional abilities because the use and nature of compensatory strategies aimed at improving behaviour depend on level of awareness (Crossen et al., 1989; Starkstein, Chemerinski, Sabe, & Kuzis, 1997). The level of awareness a participant has of their own social abilities should be considered when selecting compensatory strategies and interventions for future clinical trials aimed at improving social skills in NF1. It is unclear what factors are contributing to poor social skills in adults with NF1 or why this deficit is more prevalent in males. Given that NF1 is a progressive condition commonly resulting in disfiguring cutaneous features that increase with age (Friedman & Birch, 1997), greater overall disease severity might therefore be expected to be associated with social functioning, especially in adulthood. We, however, did not find a significant association. This is in contrast to studies in paediatric samples which have reported a link between social problems and greater disease severity in terms of neurological involvement (CNS involvement, cognition, and attention deficit hyperactivity disorder) (Barton & North, 2004; Noll et al., 2007). Alternatively, social deficits in NF1 may be directly related to impairments in the cognitive processes that underlie social behaviour. Studies involving disorders characterised by social dysfunction (e.g. ASD, schizophrenia, traumatic brain injury), have shown that impairments in attention and executive functions explain a significant proportion of variance of social skills in these patients (Addington & Addington, 1999; Godfrey & Shum, 2000; Penn, Mueser, Spaulding, Hope, & Reed, 1995). Consistent with this, we found a significant association between executive functions and social skills in adults with NF1. Specifically, adults with more severe deficits in behavioural regulation exhibited more frequent antisocial behaviour. Interestingly, the presence of ADHD, a disorder characterised by behavioural regulation deficits, has been found to be an important risk factor for poor social skills and outcomes in children with NF1 (Barton & North, 2004). These findings suggest that behavioural regulation may play a key role in successful social interactions in NF1. At the same time, emerging literature has identified social cognition, i.e. the ability to receive and process social information, as a key mechanism underlying social functioning in normal and clinical populations (Baron-Cohen, 2000; Kagan, 1984; Kipps, Nestor, Acosta-Cabronero, Arnold, & Hodges, 2009; Macdonald et al., 2003; Sparks, McDonald, Lino, O’Donnell, & Green, 2010). Two recent studies have also found social cognitive deficits, in particular the recognition of angry and fearful facial expressions, in children and adults with NF1 (Huijbregts, Jahja, De Sonneville, De Breij, & Swaab-Barneveld, 2010; Pride, Korgaonkar, Barton, Payne, & North, in press). This is important, given we found a significant relationship between the frequency of prosocial behaviour and facial expression recognition in our study. Collectively, these findings suggest that impairments in behavioural regulation and social processing may impact the social competence of adults with NF1 and that interventions targeting such cognitive deficits may help reduce behavioural and social problems in NF1. 5. Conclusions Our study helps characterise the impact of NF1 on the social functioning of adults with NF1. These findings can be used to guide the development of future treatment interventions targeting social deficits in this population; a particularly important target given links between impoverished social skills and poor social outcomes, such as social participation, peer relationships, self-esteem and quality of life (Brooks, Campsie, Symington, Beattie, & McKinlay, 1986; Matson & Swiezy, 1994; Oddy, Humphrey, & Uttley, 1978; Tate, 1991). References Ablon, J. (1996). Gender response to neurofibromatosis 1. Social Science and Medicine, 42(1), 99–109.

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Addington, J., & Addington, D. (1999). Neurocognitive and social functioning in schizophrenia. Schizophrenia Bulletin, 25, 173–183. Australian Bureau of Statistics. (2006). Index of Relative Socio-economic Advantage and Disadvantage (Table 2) Retrieved from: http://www.abs.gov.au/AUSSTATS/ [email protected]/DetailsPage/2033.0.55.0012006. Baron-Cohen, S. (2000). Theory of mind and autism: A fifteen year review. In S. Baron-Cohen, H. Tager-Flusberg, & D. J. Cohen (Eds.), Understanding other minds (2nd ed.). New York: Oxford University Press. Barton, B., & North, K. (2004). Social skills of children with neurofibromatosis type 1. Developmental Medicine and Child Neurology, 46(8), 553–563. Barton, B., & North, K. (2007). The self-concept of children and adolescents with neurofibromatosis type 1. Child: Care, Health and Development, 33(4), 401–408. Benjamin, C. M., Colley, A., Donnai, D., Kingston, H., Harris, R., & Kerzin-Storrar, L. (1993). Neurofibromatosis type 1 (NF1): Knowledge, experience, and reproductive decisions of affected patients and families. Journal of Medical Genetics, 30, 567–574. Brooks, N., Campsie, L., Symington, C., Beattie, A., & McKinlay, W. (1986). The five year outcome of severe blunt head injury: A relative’s view. Journal of Neurology, Neurosurgery, and Psychiatry, 49(7), 764–770. Crossen, B., Barco, P. P., Bolesta, M. M., Cooper, P. V., Werts, D., & Brobeck, T. C. (1989). Awareness and compensation in postacute head injury rehabilitation. Journal of Head Trauma Rehabilitation, 4, 46–54. Dilts, C. V., Carey, J. C., Kircher, J. C., Hoffman, R. O., Creel, D., Ward, K., et al. (1996). Children and adolescents with neurofibromatosis 1: A behavioural phenotype. Journal of Developmental and Behavioural Paediatrics, 17(4), 229–239. Evans, D. G., Howard, E., Giblin, C., Clancy, T., Spencer, H., Huson, S. M., et al. (2010). Birth incidence and prevalence of tumour-prone syndromes: Estimates from a UK family register service. American Journal of Medical Genetics, Part A, 152A, 327–332. Ferner, R. E., Hughes, R. A., & Weinman, J. (1996). Intellectual impairment in neurofibromatosis 1. Journal of the Neurological Sciences, 138(1–2), 125–133. Friedman, J. M., & Birch, P. H. (1997). Type 1 neurofibromatosis: A descriptive analysis of the disorder in 1728 patients. American Journal of Medical Genetics, 70, 138–143. Garg, S., Lehtonen, A., Huson, S. M., Emsley, R., Trump, D., Evans, D. G., et al. (2012). Autism and other psychiatric comorbidity in neurofibromatosis type 1: Evidence from a population-based study. Developmental Medicine and Child Neurology, 55(2), 139–145. Godfrey, H. P. D., & Shum, D. (2000). Executive functioning and the application of social skills following traumatic brain injury. Aphasiology, 14(4), 433–444. Hofman, K. J., Harris, E. L., Bryan, R. N., & Denckla, M. B. (1994). Neurofibromatosis type 1: The cognitive phenotype. Journal of Paediatrics, 124(4), S1–S8. Huijbregts, S., Jahja, R., De Sonneville, L., De Breij, S., & Swaab-Barneveld, H. (2010). Social information processing in children and adolescents with neurofibromatosis type 1. Developmental Medicine and Child Neurology, 52(7), 620–625. Hummelvoll, G., & Antonsen, K. M. (2013). Young adults’ experience of living with neurofibromatosis type 1. Journal of Genetic Counseling, 22(2), 188–199. Hyman, S. L., Shores, A., & North, K. (2005). The nature and frequency of cognitive deficits in children with neurofibromatosis type 1. Neurology, 65(7), 1037–1044. Hyman, S. L., Shores, E. A., & North, K. (2006). Learning disabilities in children with neurofibromatosis type 1: Subtypes, cognitive profile, and attention-deficithyperactivity disorder. Developmental Medicine and Child Neurology, 48(12), 973–977. Johnson, N. S., Saal, H. M., Lovell, A. M., & Schorry, E. K. (1999). Social and emotional problems in children with neurofibromatosis type 1: Evidence and proposed interventions. Journal of Paediatrics, 134(6), 767–772. Kagan, C. (1984). Social problem solving and social skills training. British Journal of Clinical Psychology, 23, 161–173. Kayl, A. E., Moore, B. D., Slopis, J. M., Jackson, E. F., & Leeds, N. E. (2000). Quantitative morphology of the corpus callosum in children with neurofibromatosis and attention-deficit hyperactivity disorder. Journal of Child Neurology, 15, 90–95. Kipps, C. M., Nestor, P. J., Acosta-Cabronero, J., Arnold, R., & Hodges, J. R. (2009). Understanding social dysfunction in the behavioural variant of frontotemporal dementia: The role of emotion and sarcasm processing. Brain, 132, 592–603. Korf, B. R. (2002). Clinical features and pathobiology of neurofibromatosis 1. Journal of Child Neurology, 17(8), 573–577. Krab, L. C., Aarsen, F. K., de Goede-Bolder, A., Catsman-Berrevoets, C. E., Arts, W. F., Moll, H. A., et al. (2008). Impact of neurofibromatosis type 1 on school performance [Research Support, Non-U.S. Gov’t]. Journal of Child Neurology, 23(9), 1002–1010. Long, E., McDonald, S., Tate, S., Togher, L., & Bornhofen, C. (2008). Assessing social skills in people with very severe traumatic brain injury: Validity of the Social Performance Survey Schedule (SPSS). Brain Impairment, 9(3), 274–281. Lowe, M. R. (1982). Validity of the positive behavior subscale of the social performance schedule in a psychaitric population. Psychological Reports, 50, 83–87. Lowe, M. R. (1985). Psychometric evaluation of the social performance survey schedule: Reliability and validity of the positive behaviour subscale. Behaviour Modification, 9, 193–210. Lowe, M. R., & Cautela, J. R. (1978). A self-report measure of social skills. Behaviour Therapy, 9, 535–544. Macdonald, S., Flanagan, S., Martin, I., & Saunders, C. (2004). The ecological validity of TASIT: A test of social perception. Neuropsychological Rehabilitation, 14, 285–302. Macdonald, S., Flanagan, S., Rollins, J., & Kinch, J. (2003). A new clinical tool for assessing social perception after traumatic brain injury. Journal of Head Trauma Rehabilitation, 18(3), 219–239. Matson, J. L., & Swiezy, N. (1994). Social skills with autistic children. In J. L. Matson (Ed.), Autism in children and adults: Etiology, assessment and intervention (pp. 241–260). Pacific Grove, CA: Brooks/Coles. Mautner, V. F., Kluwe, L., Thakker, S. D., & Leark, R. A. (2002). Treatment of ADHD in neurofibromatosis type 1. Developmental Medicine and Child Neurology, 44, 164–170. National Institutes of Health. (1988). Neurofibromatosis Conference Statement, National Institutes of Health Consensus Development Conference (1988). Archives of Neurology, 45, 575–578. Noll, R. B., Reiter-Purtill, J., Moore, B. D., Schorry, E. K., Lovell, A. M., Vannatta, K., et al. (2007). Social, emotional, and behavioural functioning of children with NF1. American Journal of Medical Genetics, Part A, 143A(19), 2261–2273. Oddy, M., Humphrey, M., & Uttley, D. (1978). Subjective impairment and social recovery after closed head injury. Journal of Neurology, Neurosurgery, and Psychiatry, 41, 611–616. Pavol, M., Hiscock, M., Massman, P., Moore, B., III, Foorman, B., & Meyers, C. (2006). Neuropsychological function in adults with von Recklinghausen’s neurofibromatosis. Developmental Neuropsychology, 29(3), 509–526. Penn, D. L., Mueser, K. T., Spaulding, W., Hope, D. A., & Reed, D. (1995). Information processing and social competence in chronic schizophrenia. Schizophrenia Bulletin, 21, 269–281. Pride, N. A., Korgaonkar, M. S., Barton, B., Payne, J. P., & North, K. N. (2013). The genetic and neuroanatomical basis of social dysfunction – Lessons from neurofibromatosis type 1. Human Brain Mapping (in press). Pride, N. A., Payne, J. M., & North, N. K. (2012). The impact of ADHD on the cognitive and academic functioning of children with NF1. Developmental Neuropsychology, 37, 590–600. Riccardi, V., & Kleiner, B. (1977). Neurofibromatosis: A neoplastic birth defect with two age peaks of severe problems. Birth Defects Original Article Series, 13, 131–138. Roth, R. M., Isquith, P. K., & Gioia, G. A. (2005). Florida Patent No.: P.A. Resources. Samuelsson, B., & Riccardi, V. (1989). Neurofibromatosis in Gothenburg, Sweden. III: Psychiatric and social aspects. Neurofibromatosis, 2, 84–106. Sparks, A., McDonald, S., Lino, B., O’Donnell, M., & Green, M. J. (2010). Social cognition, empathy, and functional outcome in schizophrenia. Schizophrenia Research, 122, 172–178. Starkstein, S. E., Chemerinski, E., Sabe, L., & Kuzis, G. (1997). Prospective longitudinal study of depression and anosognosia in Alzheimer’s disease. British Journal of Psychiatry, 171, 47–52. Tate, R. L. (1991). Impairments after severe blunt head injury: Their consequences for rehabilitation and psychosocial reintegration. Paper presented at the Brain Impairment: Advances in applied research. Proceedings of the 15th Annual Conference of the Australian Society for the Study of Brain Impairment. Walsh, K., Valez, J., Kardel, P., Imas, D., Muenke, M., Packer, R., et al. (2012). Autism spectrum disorder (ASD) symptomatology in a neurofibromatosis type 1 (NF1) population. Developmental Medicine and Child Neurology, 55(2), 131–138. Wechsler, D. (1997). Wechsler Adult Intelligence Scale-3rd Edition (WAIS-III). San Antonio, TX: Harcourt Assessment. Wolkenstein, P., Rodriguez, D., Ferkal, S., Gravier, H., Buret, V., Algans, N., et al. (2009). Impact of neurofibromatosis 1 upon quality of life in childhood: A crosssectional study of 79 cases. British Journal of Dermatology, 160(4), 844–848.