Social skills of children with neurofibromatosis type 1

Transcription

1 Social skills of children with neurofibromatosis type 1 Belinda Barton BA (Hons Psych); Kathryn North* MBBS (Hons) MD FRACP, Head, Neurogenetics Research Unit, The Children s Hospital at Westmead, New South Wales, Australia. *Correspondence to second author at Neurogenetics Research Unit, The Children s Hospital at Westmead, Locked Bag 4001, Westmead, NSW 2145, Australia. kathryn@chw.edu.au Children with neurofibromatosis type 1 (NF1) have difficulties in forming friendships and are often rejected by their peers. Factors that contribute to these negative social outcomes are poorly understood. This study investigated the social skills of children with NF1 and the influence of comorbid conditions, such as attention-deficit hyperactivity disorder (ADHD) and specific learning dfficulties. We assessed and analyzed data from 79 children with NF1 (42 males, 37 females; mean age 11 years 6 months, SD 2 years 4 months) and 46 unaffected siblings (19 males, 27 females; mean age 12 years 1 month, SD 2 years 6 months; age range 8 to 16 years). Social skills were measured with the Social Skills Rating System. Children with NF1 had significantly poorer social outcomes than their unaffected siblings, and significantly poorer social skills in comparison with normative data. The presence of ADHD (in 39% of children with NF1) was the major risk factor for poor social functioning. Children with NF1 and ADHD had the poorest social skills and social outcomes when compared with children with NF1 only or children with NF1 and learning difficulties. These findings dispel the previous assumption that NF1 alone is associated with poor social functioning and has major implications for the development of effective interventions. See end of paper for list of abbreviations. Neurofibromatosis type 1 (NF1) is a genetic disorder that affects about 1 out of every 3000 people and is characterized by developmental defects in neural-crest-derived cells in the central and peripheral nervous system (Friedman 1999, 2002). Common physical features include neurocutaneous stigmata, such as cafe-au-lait spots, neurofibromas, freckling in the axillary or inguinal regions, and Lisch nodules, as well as hamartomatous changes in brain tissue (National Institutes of Health 1988, Gutmann et al. 1997, Friedman 2002). Characteristic cognitive features of the disorder include lower general intelligence, learning difficulties, language deficits, visuospatial deficits, and attention and organization problems (Eliason 1988; Hofman et al. 1994; North et al. 1995, 1997; Cutting et al. 2000; Kayl and Moore 2000). In addition, psychosocial problems commonly occur in children with NF1: they are frequently teased, rejected by their peers, have difficulties in forming friendships, and have fewer friends than their unaffected siblings (Benjamin et al. 1993, North et al. 1995, Dilts et al. 1996, Johnson et al. 1999). These poor social outcomes may reflect deficits in social skills, defined as socially acceptable learnt behaviours considered to be important by others, such as starting a conversation with others or giving a compliment (Gresham 1992, Gresham et al. 2001). Surprisingly, there have been very few studies examining social skills in children with NF1 (Mouridsen and Sorensen 1995, Dilts et al. 1996) and the factors that contribute to poor social outcomes in this patient population, despite the role that social competence plays in the adjustment and well-being of the individual (Gresham et al. 2001). Children with NF1 have a number of risk factors that are associated with a higher frequency of social skills deficits than in the general population (Gresham and MacMillan 1997). A meta-analysis of 152 studies indicated that 75% of children with learning difficulties have poorer social skills than their peers (Kavale and Forness 1996). Children with low academic achievement also have impaired social skills and differ very little from children with learning difficulties in terms of social functioning (Gresham et al. 1996, Gresham and MacMillan 1997). Children with attention-deficit hyperactivity disorder (ADHD; American Psychiatric Association 1994) frequently exhibit impaired social functioning, with approximately 50% having problems with peer relationships (Guevremont and Dumas 1994). Characteristics of ADHD, such as inattention, poor impulse control, poor processing of social cues, and aggressive behaviour, contribute to poor social functioning (Milich and Dodge 1984, Landau and Moore 1991, Crick and Dodge 1994, Erhardt and Hinshaw 1994, Bellanti and Bierman 2000). Children with NF1 are frequently diagnosed with learning difficulties (estimates range from 30 to 65%), low academic achievement, and ADHD (estimates range from 10 to 50%, average about 30%); they also experience internalizing problems (Eliason 1986; Eldridge et al. 1989; Hofman et al. 1994; North et al. 1995, 1997; Dilts et al. 1996; Brewer et al. 1997; Johnson et al. 1999; Kayl and Moore 2000; Mautner et al. 2002). These findings suggest that children with NF1 and a comorbid condition, such as specific learning difficulty, low academic achievement, and/or ADHD, are at an increased risk for social skills deficits. Additionally, expressive and receptive language difficulties experienced by children with NF1 (Mazzocco et al. 1995, North et al. 1995, Dilts et al. 1996) can affect negatively the development of social skills. Also, some children with NF1 can have poor social perception as a result of Developmental Medicine & Child Neurology 2004, 46:

2 visual perceptual problems; i.e. they do not accurately perceive and interpret social cues, such as facial expressions, body gestures, and tone of voice (Eliason 1986). Physical manifestations and cosmetic disfiguration associated with NF1 might also contribute to poor social outcomes; adults with NF1 have stated that the presence of skin lesions and neurofibromas in childhood, as well as frequent absences from school because of medical complications, made it hard for them to form and maintain friendships (Ablon 1999). The few studies that have examined social outcomes of children with NF1 employed behavioural rating scales and found that children with NF1 have significantly more social problems than their unaffected siblings or typically developing peers (Dilts et al. 1996, Johnson et al. 1999). Yet, the specific nature of these problems has not been examined in detail. Only one study so far has formally examined social skills in children with NF1 (Dilts et al. 1996). Gresham and Elliott (1990), using a validated rating system of social behaviour, found no significant difference for total social skills scores between children with NF1 and their unaffected siblings, although parental ratings of social skills in this study were lower for children with NF1. Parent and teacher ratings from behavioural checklists indicated that children with NF1 had significantly more social problems than their unaffected siblings. However, almost 60% of the NF1 sample recruited by Dilts et al. (1996) had learning difficulties and/or communication disorders, which might have affected social functioning. It is, therefore, unclear whether poor social outcomes in children with NF1 are due to NF1 alone or are secondary to a variety of learning and cognitive deficits. Consistent with the latter proposition is the finding by Church (1993) that adolescents with NF1 and learning difficulties had greater difficulties with friendships than adolescents with NF1 and no learning difficulties. However, the very small number of participants used in that study limited the reliability of the findings. In summary, although children with NF1 commonly experience negative social outcomes, very little is known about the factors that contribute to these poor outcomes. No study has examined the relationship between social skills and social outcomes, and results are conflicting as to whether children with NF1 are as socially competent as their unaffected siblings (Dilts et al. 1996, Johnson et al. 1999). The influence of comorbid conditions, such as learning difficulties, low academic achievement, and/or ADHD, on social skills has not been examined, and it is not known whether only a subgroup of children with NF1 experience poor social functioning. Correlates associated with poor social skills, such as aggression and attention, have also not been investigated. Therefore, the aims of the present study were: (1) to examine the social skills of children with NF1; (2) to obtain different perspectives of social skills via ratings from parents, teachers, and by self-report from the children; (3) to examine the relationship between social skills and social outcomes; (4) to investigate the relationship between social skills, intelligence, achievement, and behaviour; and (5) to examine the influence of comorbid conditions on the social skills of children with NF1. Method PARTICIPANTS The Neurogenetics Clinic at The Children s Hospital at Westmead, New South Wales, Australia caters for families with NF1, primarily those from the Sydney Metropolitan Region. The clinic is financed by the national health scheme and is, thus, available to all socioeconomic groups. Patients are reviewed regularly by a neurologist as part of routine care. Details of clinic reviews and medical information are stored in patients medical records. Siblings of children with NF1 are also assessed clinically at the time of first clinic review of their affected sibling, to exclude a diagnosis of NF1. Children who satisfied the diagnostic criteria for NF1 based on a National Institutes of Health (1988) statement and were aged between 8 and 16 years old were selected from the clinic s database. Medical files were examined to determine eligibility for participation. Eligible children were ascertained sequentially, in terms of when they were first seen in the clinic. Twentyeight children were excluded from the study owing to the presence of central nervous system pathology: epilepsy or history of seizures (n=8); optic gliomas (n=13); possible brain lesions (n=3); hydrocephalus (n=1); hypothalamic tumour (n=1); Arnold Chiari malformation and hydrocephalus (n=1); and absence of corpus callosum (n=1). Two other children were excluded for other medical reasons: acute lymphoblastic leukaemia and B cell non-hodgkin s lymphoma. Of the 102 participants contacted, 19 children with NF1 (15 families) refused to participate (eight gave no reason, four children were not willing to participate, two children were unaware of the diagnosis, two found it too far to travel, two had no transport, and one was leaving the country). A total of 83 children with NF1 and 51 unaffected siblings agreed to participate. However, four children with NF1 were excluded from data analysis for the following reasons: insufficient understanding of the English language (n=2), removal of the child from parental custody (n=1), and moderate intellectual delay (n=1). Unaffected siblings of these children were also excluded because of incomplete data. The final sample consisted of 79 children with NF1 (42 males and 37 females, from 75 families) and 48 unaffected siblings (20 males and 28 females, from 46 families). In addition, 75 of the 79 children with NF1 recruited had magnetic resonance imaging as part of another concurrent study (S Hyman and K North, unpublished data). Children with magnetic resonance T 2 -hyperintensities were not excluded, and no other central nervous pathology was present. For sibling pairs, each child with NF1 was matched only once to their unaffected sibling who was the closest in age. This resulted in 46 sibling pairs for analysis. The clinical severity of NF1 was rated with a modified version of Riccardi s severity scale (Riccardi 1999). Minimal severity indicates that few features of NF1 are present (e.g. café au lait spots and freckling only). Mild severity indicates physical signs of NF1 that are obvious to others and are a concern. Moderate NF1 indicates a significant compromise of health but symptoms can be managed reasonably well. Severe NF1 indicates a serious compromise of health that is difficult to manage and is associated with a shortened life span. Cognitive features were not included in the modified severity scale used. One neurologist with extensive experience in NF1 (KN) assigned all severity ratings. The study was approved by the Ethics Committee at The Children s Hospital at Westmead. PROCEDURE Parents of children with NF1 that satisfied the inclusion criteria were mailed an information sheet about the study. A follow-up phone call was made to answer any questions and ascertain consent. Written informed consent was obtained from chil- 554 Developmental Medicine & Child Neurology 2004, 46:

3 dren s parents/guardians and verbal consent was obtained from children aged 10 years and older. Children were assessed at the Children s Hospital over two morning sessions. Each child was assessed individually and sibling pairs were tested on the same day. The order of test administration for each session was the same for all participants. Psychologists performing the assessments were not blinded to the children s diagnosis of NF1. Children with ADHD were not on stimulant medication during testing. Written informed consent was obtained from the parent to contact the child s teacher and approval was obtained from the relevant school authorities. Teachers were informed about the nature of the study and that the child identified might have NF1 or be an unaffected sibling. MEASURES Socioeconomic status of families Daniel s Scale of Occupational Prestige (Daniel 1983) was used to determine socioeconomic status based on parental occupation. The lowest score (minimum 1) represents high socioeconomic status, whereas a high score (maximum 7) represents low socioeconomic status. When both parents were working, the more prestigious occupation was used. Behavioural and emotional functioning Information on the children s behavioural and emotional functioning was obtained from behavioural ratings from parents and teachers using the Child Behaviour Checklist (CBCL; Achenbach 1991a) and the Teacher s Report Form (TRF; Achenbach 1991b). Because T scores for syndrome scales, adaptive functioning, and competence items are truncated, it is recommended that raw scores be used (Achenbach 1991a). However, to account for age and sex differences and to preserve all the differentiation of scores, raw scores for competence, adaptive functioning, and syndrome scales were converted to z scores based on normative data for that child s sex and age (Achenbach 1991a,b). T scores (mean 50, SD 10) for Total Problem Behaviours, Internalizing, Externalizing Problems, Total Competence, and Total Adaptive Functioning are not truncated and are reported (Achenbach 1991a,b). T scores in the borderline clinical range were included in the clinical range (Achenbach 1991a,b). For Total Problem Behaviours and syndrome scales, high z scores are indicative of poor functioning, whereas for competence and adaptive functioning scales, low scores are indicative of poor functioning. Intellectual ability and academic achievement The Wechsler Intelligence Scale for Children, 3rd edition (Wechsler 1991) was used to assess intellectual functioning of the children. The Wechsler Individual Achievement Test (Wechsler 1992) was used to assess academic achievement. For both measures, standard scores are reported (mean 100, SD 15). Social skills Social skills were assessed with the Social Skills Rating System (SSRS; Gresham and Elliott 1990). The SSRS is a multirater assessment that obtains ratings on the perceived frequency of social behaviour. SSRS ratings were obtained by self-report from the student (SSRS-S), the parent (SSRS-P), and the student s teacher (SSRS-T). Separate SSRS forms are used for primary-age and secondary-age students. The SSRS-S, SSRS-P, and SSRS-T do not all share the same subscales, with only about 37% overlap of items for any two SSRS forms (Gresham and Elliott 1990). Raw subscale scores for each domain range from 0 to 20 and are summed to provide total social skills scores. Raw total scores were then converted into standard scores (mean 100, SD 15), with high standard scores indicative of positive behaviours. Social outcomes Social Problem scores from the CBCL and TRF and Social Competence scores from the CBCL were used as measures of social outcomes. Definition of groups: specific learning difficulties, low academic achievement, and ADHD To examine the influence of learning difficulty, low academic achievement, and ADHD on social functioning, the total NF1 group (n=79) was divided into subgroups based on comorbidity for these conditions. Specific learning difficulties (SLD) are commonly defined as a significant discrepancy between intellectual ability and academic achievement (American Psychiatric Association 1994). However, Kavale and Forness (2000) argue that a significant discrepancy is a necessary but not sufficient criterion for learning difficulties. Therefore, in this study children with a significant discrepancy between ability and achievement (mathematics, reading, and/or spelling) might potentially have SLD. Low academic achievement (LA) was defined as those children whose mathematics, spelling, and/or reading scores in the Wechsler Individual Achievement Test were within or below the borderline range of ability (i.e. a standard score of less than 80; Wechsler 1992). Because there were too few cases for a separate group for SLD and LA, and because some children had both SLD and LA, this group was combined to form the LA/SLD group. The diagnosis of ADHD was based on scores from Conners ADHD/DSM-IV scales (parent and teacher; Conners 1997), performance on the Test of Everyday Attention for Children (Manly et al. 1999), and clinical presentation as part of a concurrent study of this patient cohort (S Hyman and K North, unpublished data). Children with NF1 and ADHD formed the NF1+ADHD group. Children with ADHD frequently have LA and/or SLD (Mayes et al. 2000, Snider et al. 2000). For children with NF1 and ADHD who had LA and/or SLD, ADHD was the overriding classification used. Children with NF1 without ADHD, LA, or SLD formed the NF1-only group. Four children with NF1 and a Full-scale IQ of less than 70, three of whom also had ADHD, were excluded. STATISTICAL ANALYSIS Data were analyzed with SPSS for Windows (version 10). Scores for all measures were examined for missing values, univariate and/or multivariate outliers, fit for normal distribution, and test assumptions. Mean standard scores for the total NF1 group (n=79) were compared with the normative mean by using a onesample t-test or the Wilcoxon one-sample signed-ranks test when scores were asymmetrically distributed. Only total scores for each of the SSRSs, CBCL, and TRF were compared with normative means to reduce the number of comparisons made between experiments. Differences between sibling pairs (n=46) were examined using paired t-tests or the Wilcoxon signed-ranks test when scores were asymmetrically distributed. When several t-tests (multiple comparisons) were Social Skills of Children with Neurofibromatosis Type 1 Belinda Barton and Kathryn North 555

4 conducted, the Holm procedure (a modified Bonferroni procedure) was applied to control the error rate between families (Aickin and Gensler 1996, Levin 1996). McNemar s χ 2 was used to examine whether proportions differed between sibling pairs for sex, macrocephaly, ADHD, and borderline/clinical behaviour on the CBCL. Raw subscale scores for primary-age and secondary-age versions of each SSRS were combined because the factor structure of the subscales for each version is identical. In addition, mean differences in raw subscale scores for primary and secondary students are very small (Gresham and Elliott 1990). To determine whether sibling pairs differed on raw social skills subscales, a multivariate matched-pairs analysis was conducted with a difference score between sibling pairs being calculated for each subscale. The multivariate analysis tests whether the difference variables (considered jointly) differ significantly from the zero vector (Stevens 1996, Tatsuoka 1971). Exact F ratios reported are based on Hotelling s T 2. Total social skills scores from the SSRS-S, SSRS-P, and SSRS-T for sibling pairs were analyzed separately with paired t-tests. The relationship between social skills, intelligence, achievement, behaviour, and social outcomes was examined using Pearson s product moment or Spearman s rho correlations, with the coefficient of determination reported for some variables. To examine the differences in social skills between children with NF1 and a comorbid condition and those without, a one-way analysis of variance (ANOVA) was conducted with post-hoc testing using the Tukey Kramer test because sample sizes were not equal. All statistical tests and correlations were two-tailed. To control for Type I error rate, correlations were evaluated at 0.01 level of significance. COMPLETION RATE FOR MEASURES Total NF1 group All parents completed the CBCL and the SSRS-P. For teacher ratings, three parents (two of whom had an unaffected child in the study) did not give permission to contact their child s school and indicated that they had not informed the school that their child had NF1. One adolescent with NF1 had just left school and begun employment, so the SSRS-S was completed but the SSRS-T was not. A total of 75 teachers were contacted to complete questionnaires. Five teachers did not return the TRF or the SSRS-T, three teachers returned the SSRS-T only, and two teachers returned the TRF only. This resulted in a total of 67 completed TRFs and 68 completed SSRS-T forms. Sibling pairs Data were available for all sibling pairs for the CBCL and SSRS-P. One unaffected child did not attend school and was taught at home by the parents; the SSRS-S, SSRS-T, and TRF were, therefore, not completed for this child because these forms contain items that relate to the school environment. For teacher questionnaires, the parents of two sibling pairs did not give permission to contact their children s school (as in the total NF1 group). One set of parents gave permission to contact the school for their child with NF1, but did not give permission to contact the school of the unaffected child. Of the teachers contacted for 42 sibling pairs, teachers did not return any forms for one sibling pair. In addition, the TRF was not returned for two sibling pairs, one child with NF1, and four unaffected siblings. TRF scores were available for 34 sibling pairs. The SSRS-T was not completed for two children with NF1 and one unaffected sibling, resulting in SSRS-T scores for 38 sibling pairs. Results Demographic details for the total NF1 group, the NF1 paired group, and unaffected siblings are shown in Table I. Mean age difference between sibling pairs was 2 years 8 months (SD 1 year 3 months). There were 22 same-sex pairs and 24 different-sex pairs. There was no significant difference between the NF1 paired group and unaffected siblings for age or sex (χ 2 [1,46]=2.04, p=0.152; Table I). As expected, there Table I: Demographic details, mean IQ, and achievement scores for total NF1 group, NF1 paired group, and unaffected siblings Variable Total NF1 NF1 paired Unaffected siblings t(45) p (n=79) (n=46) (n=46) Age, mean (SD) y:m 11:6 (2:4) 11:5 (2:5) 12:1 (2:6) Socioeconomic status, mean (SD) 4.27 (1.18) 4.25 (1.15) Sex, n (%) Male 42 (53) 27 (59) 19 (41) Female 37 (47) 19 (41) 27 (59) Macrocephaly a, n (%) Yes 42 (53) 22 (48) 7 (15) No 37 (47) 24 (52) 39 (85) IQ, mean (SD) Verbal IQ (14.34) b (16.30) (13.11) c 4.45 < Performance IQ (12.68) b (14.39) (13.22) c 4.04 < Full-scale IQ (12.97) b (15.02) (12.88) c 4.87 < Academic Achievement, mean (SD) Reading (13.26) b (15.21) (12.57) c 6.09 < Spelling (13.81) b (16.06) (14.79) c 5.84 < Maths Reasoning (13.76) b (15.77) (15.53) c 5.23 < Listening Comprehension (12.29) b (13.88) (13.11) c a Greater than 97th centile; b significant difference from normative data (Holm p<0.05); c significant differences between sibling pairs (Holm p<0.05). NF1, neurofibromatosis type Developmental Medicine & Child Neurology 2004, 46:

5 was a significant difference between the NF1 paired group and unaffected siblings for the presence of macrocephaly (>97th centile), with macrocephaly being more common in the NF1 group (χ 2 [1,46]=9.33, p=0.001; Table I). For the total NF1 group, the disorder was sporadic in 50 (63%) children, and familial in the remaining 29 (37%) children. Severity ratings indicated that 23 (29%) children had minimal NF1, 38 (48%) had mild, 12 (15%) had moderate, and six (8%) had severe NF1. For the NF1 paired group, in 14 (30%) children the disorder was familial and in 32 (70%) children it was sporadic; 11 (24%) children had minimal NF1, 24 (52%) had mild, seven (15%) had moderate, and four (9%) had severe NF1. Responses from 79 parents indicated that 12 (15%) children with NF1 had a pre-existing diagnosis of ADHD; four of these children were on stimulant medication. On the basis of the DSM-IV criteria (American Psychiatric Association 1994) for ADHD, 31 of the 79 (39%) children with NF1 were classified as having ADHD (S Hyman and K North, unpublished data); this group included all 12 children with a pre-existing diagnosis of ADHD. Of the 31 children with NF1 and ADHD, 20 were diagnosed as ADHD-Combined, 10 as ADHD-Inattentive, and one as ADHD-Hyperactive. For sibling pairs, parental responses indicated that seven (15%) children with NF1 (four on stimulant medication) and three (7%) unaffected siblings (one on stimulant medication) had a pre-existing diagnosis of ADHD. Fourteen (30%) children with NF1 and six (13%) unaffected siblings were classified as ADHD (S Hyman and K North, unpublished data), with four sibling pairs concordant for ADHD. Of the unaffected siblings, four children were diagnosed as ADHD-Combined, one child as ADHD- Inattentive and one child as ADHD-Hyperactive. ADHD was significantly more common in children with NF1 than in their unaffected siblings (χ 2 [1,46]=4.08, p=0.039). INTELLIGENCE AND ACADEMIC ACHIEVEMENT Children with NF1 had significantly lower mean Verbal IQ, Performance IQ, and Full-scale IQ scores in comparison with normative data (t[78]= 4.93, p<0.0001; t[78]= 6.12, p<0.0001; and t[78]= 6.33, p< respectively). Similarly, children with NF1 had significantly lower mean Verbal, Performance, and Full-scale IQ scores than their unaffected siblings (Table I). Mean scores for reading, spelling, mathematics, and listening comprehension for the total NF1 group (Table I) were significantly lower than the normative mean (t[78]= 5.29, p<0.0001; t[78]= 5.33, p<0.0001; t[78]= 3.90, p<0.0001; and t[78]= 2.92, p=0.005 respectively). Similarly, children with NF1 had significantly poorer academic achievement than their unaffected siblings (Table I). For sibling pairs, 12 (26%) children with NF1 and four (9%) unaffected siblings had SLD in mathematics, reading, and/or spelling. BEHAVIOURAL/EMOTIONAL FUNCTIONING AND SOCIAL OUTCOMES The CBCL and TRF profiles for the total NF1 group, the NF1 paired group, and their unaffected siblings are shown in Table II. In comparison with normative CBCL data, the total NF1 group had significantly more Total Problem Behaviours, Internalizing and Externalizing Problems and poorer Total Competence (s[79]=1012.5, p<0.0001; t[78]=5.47, p<0.0001; t[78]=2.14, p=0.035 and s[78] = , p< respectively). Examination of z syndrome scores for the total NF1 group indicated that parents rated somatic, social, and attention problems as the most significant problem areas for children with NF1. CBCL T scores indicated that about 40% of children with NF1 had Table II: Mean CBCL and TRF scores for total NF1, NF1 paired group, and unaffected siblings CBCL/TRF scales Child Behavior Checklist (Achenbach 1991a) Teachers Report Form (Achenbach 1991b) Total NF1 NF1 paired Unaffected siblings Total NF1 NF1 paired Unaffected siblings (n=79) (n =46) (n=46) (n=67) (n=34) (n=34) Problem Behaviours (T) Total Problems (12.13) a (12.60) (12.42) b (9.71) a (9.77) (9.50) Internalizing (11.59) a (11.68) (11.85) (9.67) a (9.58) (9.47) Externalizing (12.44) a (12.98) (10.85) (9.24) (8.64) (8.56) Syndrome (z) Withdrawn 0.39 (1.19) 0.42 (1.19) 0.24 (1.21) 0.38 (1.11) 0.46 (1.16) 0.01 (0.80) Somatic Complaints 1.18 (1.42) 1.10 (1.35) 0.32 (1.17) b 0.12 (0.87) 0.16 (0.87) 0.30 (0.29) Anxious/Depressed 0.69 (1.31) 0.65 (1.36) 0.53 (1.57) 0.57 (1.34) 0.53 (1.27) 0.00 (0.85) Social Problems 1.53 (1.64) 1.37 (1.80) 0.11 (1.09) b 0.91 (1.55) 0.71 (1.41) 0.03 (0.97) Thought Problems 0.73 (1.51) 0.78 (1.65) 0.09 (0.71) b 0.06 (0.96) 0.17 (1.16) 0.02 (0.83) Attention Problems 1.48 (1.49) 1.32 (1.59) 0.13 (0.87) b 0.66 (1.26) 0.53 (1.10) 0.01 (0.97) Delinquent Behaviour 0.40 (1.40) 0.52 (1.57) 0.24 (1.07) 0.26 (0.69) 0.21 (0.83) 0.20 (0.69) Aggressive Behaviour 0.40 (1.34) 0.49 (1.44) 0.14 (1.20) 0.03 (0.88) 0.01 (0.90) 0.13 (0.86) CBCL Competence (z) Activities 0.71 (1.03) 0.67 (1.05) 0.15 (0.88) b Social 0.88 (1.11) 0.88 (1.24) 0.31 (1.13) b School 1.82 (1.27) c 1.02 (1.16) 0.07 (0.95) b Total Competence (T) (9.00) c (9.84) (8.82) b Total Adaptive Functioning (T) (7.16) a (7.60) (6.82) Academic Performance (z) 0.76 (0.84) 0.63 (0.89) 0.28 (0.86) Results are means (SD). a Significant difference from normative data (Holm p<0.05); b significant differences between sibling pairs (Holm p<0.05); c n=78. NF1, neurofibromatosis type 1. Social Skills of Children with Neurofibromatosis Type 1 Belinda Barton and Kathryn North 557

6 Social (31/79) and/or Attention (33/79) Problems in the borderline/clinical range. Interestingly, 34% (27/79) of children with NF1 had both Social and Attention Problems in the borderline/clinical range. About 25% (20/79) of the total NF1 group had Social Competence Problems in the borderline/clinical range. For sibling pairs, parents rated children with NF1 as having significantly more Total Problem Behaviours (t[45]=3.20, p=0.0030), Somatic Complaints (z= 3.10, p=0.002), Social Problems (z= 4.17, p<0.0001), Thought Problems (z= 3.42, p=0.0001), and Attention Problems (z= 4.53, p<0.0001) than their unaffected siblings. As observed in the total NF1 group, almost 40% (18/46) of the NF1 paired group had Social Problems in the borderline/clinical range. There was a significant difference between sibling pairs in the proportion of Social Problems in the borderline/clinical range (χ 2 (1,46) =9.33, p=0.001). A total of 25 sibling pairs were concordant for Social Problems not in the borderline/clinical range. For 18 discordant pairs, the child with NF1 had Social Problems in the borderline/clinical range whereas the unaffected sibling did not, and for the remaining three discordant pairs the unaffected sibling had Social Problems in the borderline/clinical range. Children with NF1 were significantly less competent socially (t[45]= 3.00, p=0.004) and at school (z= 3.84, p<0.0001), less active, and less skilled in sporting and non-sporting activities (t[45]= 5.13, p<0.0001) than their unaffected siblings. About 28% (13/46) of children with NF1 and 11% (5/46) of unaffected siblings had Social Competence Problems in the borderline/clinical range. Only two sibling pairs were concordant for Social Competence Problems in the borderline/clinical range. Overall, children with NF1 were significantly less competent than their unaffected siblings (t[45]= 6.08, p<0.0001). There was no other significant group difference for any other CBCL scale shown in Table II (Holm p>0.05). Teachers ratings for Total Problem Behaviours and Internalizing Problems for the total NF1 group were significantly above the normative mean (t[66]=4.15, p< and t[66]=4.69, p<0.0001, respectively), indicating that children with NF1 exhibited more problem behaviours in these domains. In addition, children with NF1 had significantly poorer Total Adaptive Functioning and Academic Performance in comparison with normative data (t[66]= 7.46, p< and t[66]= 4.03, p< respectively). The prevalence of Social and Attention Problems in the borderline/clinical range was lower for teacher ratings (18% [12/67] and 16% [11/67] respectively) than for parental ratings. There was no significant difference between children with NF1 and their unaffected siblings for any of the TRF scales (Holm p>0.05) shown in Table II. SOCIAL SKILLS Mean standard scores for total social skills for children with NF1 as rated by parents and teachers were significantly below the normative mean (mean [SD] [16.66], t[78]= 2.28, p=0.025, and mean [SD] [14.30], t[67]= 2.18, p=0.033 respectively). In contrast, mean social skills scores as selfrated by students were significantly above the normative mean (mean [SD] [16.60], t[78]=2.57, p=0.012). Table III: Social skills and outcomes by clinical variables of NF1 Variable Familial Sporadic Minimal/Mild Moderate/Severe (n=29) (n=50) (n=61) (n=18) Social Skills Student (16.23) (16.93) (15.69) (15.86) Parent (18.26) (15.85) (16.13) Teacher (12.22) a (15.64) b (14.2) (15.18) Social Outcomes (z) Social Problems c 1.34 (1.65) 1.63 (1.64) 1.47 (1.65) 1.70 (1.64) Social Competence d 1.08 (1.20) 0.76 (1.05) 0.89 (1.06) 0.84 (1.30) Results are mean (SD). a n=27; b n=41; c high scores indicate poor functioning; d low scores indicate poor functioning. NF1, neurofibromatosis type 1. Table IV: Mean (SD) scores for SSRS-S, SSRS-P, and SSRS-T subscales and total social skills for NF1 paired group and unaffected siblings Social skills Student (SSRS-S) Parent (SSRS-P) Teacher (SSRS-T) NF1 paired Unaffected siblings NF1 paired Unaffected siblings NF1 paired Unaffected siblings (n=45) (n=45) (n=46) (n=46) (n=38) (n=38) Subscales Cooperation (2.69) (3.05) (3.89) (3.56) (3.59) (3.34) Assertion (3.79) (3.03) (3.76) (3.70) (4.74) (3.50) Responsibility (3.32) (3.32) Empathy (3.30) (3.06) Self-Control (3.29) (3.51) (4.37) (3.32) (4.05) (3.44) Total Social skills (15.98) (14.56) (16.72) (16.14) (13.84) (11.87) SSRS-S/-P/-T, Social Skills Rating System-Student/-Parent/-Teacher (Gresham and Elliot 1990); NF1, neurofibromatosis type Developmental Medicine & Child Neurology 2004, 46:

7 There were minimal differences of about two points or less in mean social skills scores between children with familial NF1 and those with sporadic NF1 (Table III). Because there were too few children with severe NF1, severity classifications were combined into two classifications: minimal/mild and moderate/severe. Social skills and social outcomes scores for children with minimal/mild NF1 or moderate/severe NF1 are shown in Table III. There was a mean difference of less than 0.5 between the two severity groups in social skills (as rated by parents and teachers) and social outcomes. For self-ratings made by children, an independent t-test indicated that children with moderate/severe NF1 had significantly poorer social skills than children with minimal/mild NF1 (t[77]=3.14, p=0.002). Mean SSRS-S, SSRS-P, and SSRS-T scores for raw subscales and total social skills for the NF1 paired group and their unaffected siblings are shown in Table IV. Multivariate analysis of difference scores indicated that there was no significant difference between sibling pairs for SSRS-S subscales (Hotelling s T 2 =0.22, F[4,41]=2.25, p=0.080, d=0.18), for SSRS-P subscales (Hotelling s T 2 =0.17, F[4, 42]=1.83, p=0.140, d=0.15) or for SSRS-T subscales (Hotelling s T 2 =0.20, F[3,35]=2.25, p=0.087, d=0.17). There was no significant difference between sibling pairs for total social skills as rated by students, parents, or teachers (t[44]= 0.22, p=0.828; t[45]= 1.81, p=0.077; t[37]= 1.63, p=0.111 respectively). CORRELATES OF SOCIAL SKILLS Social skills scores (parent and teacher) were correlated with respective ratings of social outcomes and behavioural correlates of social skills (Table V). For both the NF1 paired group and their unaffected siblings, better social skills were significantly associated with fewer social problems and better social competence (Table V). For the NF1 group, about 40% of the variability in Social Problems and Social Competence could be predicted from the variability in social skills (as rated by parents). For unaffected siblings, this relationship was weaker; in this group only about 20% of the variability in Social Problems and Social Competence can be predicted from the variability in social skills. High scores for Attention, Aggressive, Internalizing, and Externalizing Problems were significantly associated with poorer social skills for both groups (Table V). Social skills were not significantly correlated with Full-scale or Verbal IQ or academic achievement for the NF1 paired group or their unaffected siblings (Table VI). SOCIAL SKILLS OF CHILDREN WITH NF1 AND A COMORBID CONDITION There were 28 children with NF1+ADHD, 17 children with NF1+LA/SLD, and 30 children with NF1 only. Mean Full-scale IQ, achievement, and total social skills scores for each group are shown in Table VI. The NF1+LA/SLD group had the lowest mean Full-scale IQ and achievement scores of all groups. Parental ratings indicated that the NF1+ADHD group had the Table V: Correlations between parent and teacher rated social skills and social outcomes and behaviour for NF1 paired group and unaffected siblings CBCL/TRF Scale Social skills NF1 Paired Unaffected siblings Parent Teacher Parent Teacher (n=46) (n=32) (n=46) (n=32) Social Problems (z) 0.66 a 0.50 a,b 0.43 a 0.65 a,b Attention Problems(z) 0.61 a 0.51 a,b 0.36 c 0.75 a,b Aggressive Behaviour (z) 0.65 a a 0.41 b,c Internalizing Problems (T) 0.49 a 0.50 a 0.43 a 0.59 a,b Externalizing Problems (T) 0.65 a 0.26 b 0.54 a 0.44 b,c Social Competence (z) 0.63 a 0.48 a a Correlation is significant at 0.01 (two-tailed); b Spearman s rho; c correlation is significant at 0.05 (two-tailed). CBCL, Child Behavior Checklist; TRF, Teacher Report Form (Achenbach 1991a,b). Table VI: Correlations between social skills, Full-scale IQ (FSIQ), Verbal IQ (VIQ), and academic achievement for NF1 paired group and unaffected siblings Measure FSIQ VIQ Reading Spelling Maths Listening Comprehension NF1 paired Total Social Skills Student (n=45) Parents (n=46) Teachers (n=38) 0.38 a a Unaffected siblings Total Social Skills Student (n=45) Parents (n=46) Teachers (n=38) a Correlation is significant at 0.05 (two-tailed). Social Skills of Children with Neurofibromatosis Type 1 Belinda Barton and Kathryn North 559

8 poorest Social Competence and the most Attention Problems, Aggressive Behaviour, Social Problems, and Internalizing and Externalizing Problems of the three groups (Table VII). Attention and Social Problem scores for the NF1+ADHD group were more than 2SD above the mean, indicative of significant problems. There was a significant difference between the three groups for total SSRS-P social skills (F[2,72]=4.93, p=0.010). Parental ratings indicated that children with NF1+ADHD had significantly poorer social skills than the NF1+LA/SLD and NF1-only groups (p=0.024 and p=0.027 respectively). There was no significant difference between the NF1+LA/SLD and NF1 only groups for social skills as rated by parents (p=0.903). There was no significant difference between the groups for social skills as rated by teachers (F(2,62)=1.61, p=0.208). However, teachers rated the NF1+ADHD group has having the poorest social skills of the three groups. There was a significant difference between groups for total social skills as self-rated by children (F[2,72]=4.25, p=0.018). The NF1-only group had significantly better social skills than the NF1+ADHD group (p=0.019). The NF1+LA/SLD group was not significantly different from the NF1+ADHD or the NF1- only group (p=0.888 and p=0.135 respectively). Interestingly, 40% (12/30) of the NF1-only group had total SSRS-S scores greater than 1SD from the mean (greater than the 85th centile), indicating that these students rated themselves as having very good social skills. About 29% (8/28) of the NF1+ADHD group and 12% (2/17) of the NF1+LA/SLD group had total SSRS-S scores greater than 1SD from the mean. Additionally, for each of the three groups, children with NF1 who rated themselves as having very good social skills tended to be younger children. Mean age of the NF1-only children with SSRS-S scores greater than the 85th centile was 9 years 9 months (SD 2 years) and for children with SSRS-S scores less than or equal to the 85th centile mean age was 11 years 5 months (SD 2 years 3 months). Discussion In this study, the social skills of children with NF1 did not differ significantly from their unaffected siblings, for total social skills or for particular aspects of social behaviour, such as cooperativeness and assertiveness. These results were consistent across multiple sources obtained from parents, teachers, and self-ratings made by children. Our findings for total social skills scores for sibling pairs are comparable to those reported by Dilts et al. (1996). When compared with normative data, the total NF1 group (n=79) had significantly poorer social skills as rated by parents and teachers. Although the mean difference between social skills scores (parent and teacher ratings) of the total NF1 group and normative data was similar to that observed between sibling pairs, it is most likely that the results for the total NF1 group were significant as a result of the larger sample size and increased power. As reported by others (Dilts et al. 1996, Johnson et al. 1999), we found that children with NF1 had significantly poorer social outcomes than their unaffected siblings, with almost 40% of children with NF1 having Social Problems in the borderline/clinical range. Interestingly, one-third of the total NF1 group had both Social and Attention Problems in the borderline/clinical range. As proposed by Gresham et al. (2001), we found that social skills were predictive of social outcomes. For the NF1 paired group and their unaffected siblings, better social skills (as rated by parents and teachers) were associated with fewer problem behaviours and better social competence. IQ and academic achievement were not significantly associated with social skills ratings. The relationship between social Table VII: Ages, Full-scale IQ, academic achievement, CBCL, and total social skills scores for NF1+ADHD, NF1+LA/SLD, and NF1-only groups Variable NF1+ADHD NF1+LA/SLD NF1 only (n=28) (n=17) (n=30) Age, y:m 12:0 (2:4) 11:8 (2:3) 10:9 (2:3) Full-scale IQ (11.44) (11.77) (12.11) Achievement Reading (10.31) (10.66) (12.01) Spelling (11.86) (9.96) (13.58) Maths reasoning (12.34) (11.90) (12.52) CBCL (z scores) Social Competence 1.01 (1.20) 0.81 (1.30) 0.68 (0.85) Social Problems 2.12 (1.44) 0.78 (1.46) 1.18 (1.56) Attention Problems 2.42 (0.87) 0.75 (1.23) 0.74 (1.41) Aggressive Behaviour 0.73 (1.13) 0.28 (1.27) 0.16 (1.20) Internalizing 1.21 (1.34) 0.56 (1.17) 0.73 (1.50) Externalizing 0.79 (1.14) 0.31 (1.29) 0.14 (1.26) Total Social Skills Parent (15.43) a,b (15.22) (16.10) Student (20.15) (12.62) (12.96) c Teacher (13.47) d (10.06) e (15.73) f Results are means (SDs). a NF1+ADHD<NF1+LA/SLD; b NF1+ADHD<NF1 only; c NF1 only>nf1+adhd; d n=24; e n=15; f n=26. NF1, neurofibromatosis type 1; ADHD, attention-deficit hyperactivity disorder; LA, low academic achievement; SLD, specific learning difficulty; CBCL, Child Behavior Checklist (Achenbach 1991a). 560 Developmental Medicine & Child Neurology 2004, 46:

9 skills and achievement was lower than correlations previously reported (r=0.20 to 0.60; Gresham 1992). Although the correlations may be influenced to some degree by the measures used, our findings do not support a significant relationship between social behaviour and academic achievement, nor the proposition that social skills deficits are a consequence of academic deficits (Gresham 1992). The presence of ADHD was the major risk factor for poor social skills in children with NF1. Of the three NF1 groups examined, the NF1+ADHD group had the poorest performance for social skills, social competence, and social problems. Mautner et al. (2002) also found that children with NF1 and ADHD had significantly more social problems than children with NF1. This result is not surprising because ADHD is a disorder that is characterized by impaired social functioning, inattentiveness, impulsiveness, and hyperactivity (American Psychiatric Association 1994). These findings dispel the previous assumption that NF1 on its own is associated with poor social performance. Social skills are behaviours that are taught and learnt by observing others, such as parents, so it is plausible that children with NF1 might learn inappropriate social behaviours from a parent with NF1. Social skills and social outcome scores of children with the familial and sporadic forms of NF1 were not significantly different. It seems, therefore, that having a parent with NF1 does not affect the social functioning of the child. Social skills scores from parents and teachers did not differ when grouped by severity of NF1; however, self-ratings from children indicated that children with moderate/severe NF1 had poorer social skills than children with minimal/mild NF1. There is no established theory that accounts for the social skills deficits observed in children with ADHD (Nixon 2001). Aggressive behaviour has been considered to be one of the most significant characteristics associated with ADHD that might contribute to poor social functioning (Hinshaw 1992, Dumas 1998). However, only three children in the NF1+ ADHD group had aggression problems in the borderline/clinical range, suggesting that aggressive behaviour was not characteristic of this group. Other factors associated with poor social functioning in children with ADHD include poor communication skills, less responsiveness to social cues, pragmatic language deficits, and performance deficits (Milich and Dodge 1984, Landau and Milich 1988, Camarata and Gibson 1999, Maedgen and Carlson 2000). Additionally, competing or interfering problem behaviours, such as impulsivity and internalizing problems, might prevent the acquisition or hinder the performance of appropriate social behaviour (Gresham and MacMillan 1997). The NF1+ADHD group had the most problem behaviours in our cohort and it is possible that these behaviours, in particular attention problems, interfered with the acquisition and/or performance of accepted social behaviour. A high percentage of children with learning difficulties or low academic achievement have poor social skills (Haager and Vaughn 1995, Kavale and Forness 1996, Gresham et al. 1996, Most and Greenbank 2000). The NF1+LA/SLD group did not differ from the NF1-only group for social skills. However, because not all children with learning difficulties or low academic achievement experience social difficulties, it might be that our sample was too small to detect differences between the NF1+LA/SLD group and the NF1-only group. The NF1+ADHD group included some children who also had learning difficulties and/or low academic achievement children with comorbid conditions, such as ADHD and learning difficulties, tend to have more social problems than children with a single diagnosis (Landau and Moore 1991, Hall et al. 1999, Semrud-Clikeman and Schafer 2000). Interestingly, student ratings of social skills were not in agreement with parent or teacher ratings. Children with NF1 indicated that they had significantly better social skills than normative data. Additionally, student ratings indicated that the NF1-only group had significantly better social skills than the NF1+ADHD group. Children with NF1 who rated their social skills as very good (greater than 85th centile) were younger children, and the NF1-only group had the lowest mean age of the three groups. It is possible that younger children overestimate their abilities because they do not possess the cognitive ability to organize their self-perceptions, make comparative judgements, and incorporate feedback from others (Silon and Harter 1985, Harter 1999, Barton and North 2002). Our finding that comorbidity for ADHD is the major risk factor for poor social functioning, poor social skills, poor social competence, and problem behaviours in children with NF1 has major implications for the development of successful interventions. Further studies are needed to clarify whether the pattern of social functioning is the same for children with NF1 and different subtypes of ADHD, and to determine whether other common neuropsychological deficits seen in the NF1 population (e.g. visual perceptual problems and executive deficits) contribute to poor social outcomes. Because many of the symptoms and social problems of ADHD continue into adolescence (Bagwell et al. 2001), the development of effective interventions is imperative to improve the long-term outcomes of these children. Although stimulant medication for the treatment of ADHD might improve peer interactions by ameliorating the core symptoms of ADHD and reducing the frequency of inappropriate aversive or social behaviour (Landau and Moore 1991, Swanson et al. 1993), medication alone is not adequate for the treatment of social skills deficits (Landau and Moore 1991, Pfiffner et al. 2000, Bagwell et al. 2001). It is more likely that a multimodal approach that incorporates stimulant medication and social skills training (with generalization techniques) that targets the specific social skills deficits of the child are needed (Gresham 1997, Pfiffner et al. 2000, Gresham et al. 2001). The development of these interventions is a challenge for future research. DOI: /S Accepted for publication 9th February Acknowledgements We thank Shelley Hyman for assistance with the assessment of children. This research, under award number DAMD , was supported by the Department of Defense Neurofibromatosis Research Program, which is managed by the US Army Medical Research and Material Command. This research was also supported by The National Neurofibromatosis Foundation Inc., New York. References Ablon J. (1999) Living With Genetic Disorder: The Impact of Neurofibromatosis 1. Westport, CT: Auburn House. Achenbach TM. (1991a) Manual for the Child Behavior Checklist/4 18 and 1991 Profile. Burlington, VT: University of Vermont Department of Psychiatry. Achenbach TM. (1991b) Manual for the Teacher s Report Form and 1991 Profile. Burlington, VT: University of Vermont Department of Psychiatry. Social Skills of Children with Neurofibromatosis Type 1 Belinda Barton and Kathryn North 561