Brief Report: Early Social Communication Behaviors in the Younger Siblings of Children with Autism

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1 Journal of Autism and Developmental Disorders, Vol. 35, No. 5, October 2005 (Ó 2005) DOI: /s Brief Report: Early Social Communication Behaviors in the Younger Siblings of Children with Autism Wendy A. Goldberg, 1,4 Kelly L. Jarvis, 1 Kathryn Osann, 2 Tracy M. Laulhere, 1 Carol Straub, 1 Erin Thomas, 1 Pauline Filipek, 3 and M. Anne Spence 3 The early social and communicative development of very young siblings of children with autism spectrum disorder (ASD) is the focus of the current study. Three groups of children were included: (1) young children diagnosed with ASD, (2) younger siblings in families with a somewhat older child with ASD, and (3) young typically developing children. All children participated in a videotaped, structured interactional procedure called the Early Social Communication Scales (ESCS; [Mundy & Hogan, 1996, A Preliminary Manual for the Abridged Early Social Communication Scales (ESCS) Unpublished manual, University of Miami]). Very young siblings were compared to young children with a diagnosed autism spectrum disorder and to a group of young typically developing children. Results indicated that, on three of four of the ESCS subscales, the social communicative behaviors of the younger siblings differed from those of the typically developing children but not from the behaviors displayed by the ASD group. Genetic vulnerability for ASD among siblings and characteristics of family interaction may explain the level of impairment observed in the very young siblings of children with autism spectrum disorders. KEY WORDS: Autism; siblings; social; communication; joint attention. INTRODUCTION 1 Department of Psychology and Social Behavior, University of California, Irvine, CA, USA. 2 Department of Medicine, University of California Irvine Medical Center, USA. 3 Department of Pediatrics, University of California Irvine Medical Center, USA. 4 Correspondence should be addressed to: Wendy A. Goldberg, Department of Psychology and Social Behavior, University of California, 3375 SE II, Irvine, CA 92697, USA; wagoldbe@uci.edu It is now widely accepted that autism disorder (AD), characterized by deficits in language, joint attention, and social communicative behaviors beginning in early childhood, is a product of underlying genetic liability, with broad heterogeneity among those affected (Rutter, 2000; Szatmari, Jones, Zwaigenbaum, & MacLean, 1998). Actual candidate genes and genomic regions are being evaluated for their potential role in autism (see Gutkucht, 2001 for a review), suggesting shared genes as a primary explanatory factor. Evidence of a genetic basis is provided by the co-occurrence of autism within relatives, the familial aggregation of autism with other deficits, and the association of autism with other genetic disorders (Folstein & Piven, 1991). For example, research from our larger project has found a 100% concordance rate for autism disorder with MZ twins and a 33% concordance rate with DZ twins (Thomas et al., 2001). When the spectrum is broadened, a number of twin and family studies point to the co-occurrence of autism, Asperger s, PDD-NOS, and CDD within sibships, bolstering support for a genetic liability to autism (Bailey et al., 1995; Bolton et al., 1994; Folstein & Rutter, 1977; LeCouteur et al., 1996; /05/ /0 Ó 2005 Springer ScienceþBusiness Media, Inc.

2 658 Goldberg et al. Maclean et al., 1999; Zwaigenbaum et al., 2000). A greater prevalence of autism spectrum disorders (ASD) has been reported among non-twin siblings than would be expected given rates in the general population (Ritvo et al., 1989; Smalley, 1997). In a sample of school-aged children (4 16 years old), the siblings of children with autism were reported to have more behavior problems and fewer prosocial behaviors than children in normative samples (Hastings, 2003a, b). However, there is not unequivocal support for differences between siblings of affected children and typically developing children; a recent review attributes inconsistencies across studies to use of different comparison groups and a focus on different outcome measures with siblings of varying ages (Yirmiya, Shaked, & Erel, 2001). These researchers also determined via meta-analysis that there are insufficient data from which to conclude that siblings of children with autism are more impaired than siblings of children with other diagnoses when the outcomes are other than autism. Of interest in the current study is whether impaired functioning in joint attention and social communicative domains during very early development characterizes younger siblings of young children with a known autism spectrum disorder. This is the first study that we know of to focus on very young diagnosed children and their younger, prediagnostic siblings. Primary symptomatology of autism disorder, apart from language delays, involves deficits in joint attention and social communicative behaviors. Deficits in social reciprocity and social communication or pragmatics have been identified as part of the symptom-based genetic research in autism (Klin, Jones, Schultz, Volkmar, & Cohen, 2002). A widely used measure to assess these domains is the Early Social Communication Scales (ESCS; Mundy & Hogan, 1996). In one study, Mundy, Sigman, and Kasari (1990) found children with AD to exhibit fewer gestural joint attention skills than mentally retarded children, after controlling for language level, mental age, and IQ. Additionally, children with AD have shown significantly less positive affect toward an adult tester during joint attention situations than both mentally retarded and typically developing children (Kasari, Sigman, Mundy, & Yirmiya, 1990). Children with autism fail to orient to both social and nonsocial stimuli, with greater impairment for social stimuli such as name calling than for sounds emanating from objects (Dawson, Meltzoff, Osterling, Rinaldi, & Brown, 1998; Toth et al., 2001). The Current Study Early detection of the symptoms of autism during infancy is gaining momentum in the pediatric community (American Academy of Neurology, 2000). However, the gold standards for diagnosis the ADI-R (Lord, Rutter, & LeCouteur, 1994) and the ADOS-G (Lord et al., 1989) are most commonly used with children who are at least 2 or 3 years of age. The current study uses the ESCS to examine young children s functioning in the domains of joint attention and social communication. Our intent was not to render a diagnosis, as the ESCS is not a diagnostic instrument. We tested the hypothesis that the social and communication behaviors of untested, clinically undiagnosed, very young siblings in families with an older sibling diagnosed with ASD would differ significantly from the behaviors of young typically developing children. METHOD Sample The study sample was drawn from a larger sample of families who were participants in a federally funded study of autism disorder in children at a large university medical center. Young children who qualified for ESCS administration (under 3 years) were included in this study. The study sample consisted of 25 children, 17 boys and 8 girls. Of the sample, 68% was Caucasian, 16% Hispanic, 8% Asian, and 8% mixed or unknown ethnicity. The sample was divided into three groups: (1) 8 children with ASD (5 AD, 3 PDD-NOS; all boys); (2) 8 untested younger siblings of children with ASD (4 boys); and (3) 9 typically developing children from families without ASD (5 boys). In the ASD group, there was one only child, one set of twins, two second borns, and three third or later borns. As newborns, one child later diagnosed with ASD had been in an incubator and another had early feeding problems; one control child also had a significant birth event (NICU). Of the younger siblings, three were second borns, and five were third born or later. Seven of the nine children in the control group were second born, one was an only child, and one was a third born. The ASD group had a mean age of 29.9 months (range = ); the younger siblings had a mean age of 17.1 months (range = ); and the average age of the typically developing children was 15.3 months (range = ). IQ was assessed in

3 Younger Siblings of Children with Autism 659 the ASD group as part of their assessment battery (IQ testing was not conducted with the non-asd children); two of the older, higher functioning children were able to take the Stanford-Binet IV and their full-scale scores ranged from 88 to 102 with a mean of 95. Four of the ASD children were given the Mullen (1995); full-scale scores ranged from 49 to 70, with a mean of 60. Measures The target sample of children who were recruited as part of the larger study was administered the Autistic Diagnostic Interview-Revised (ADI-R; Lord, Rutter, & LeCouteur, 1994) and the Autism Diagnostic Observation Schedule-Generic (ADOS-G; Lord et al., 1989). Control children were screened for participation using the Childhood Autism Rating Scale (CARS; Schopler, Reichler, DeVellis, & Dely 1980). Autism Diagnostic Interview-Revised (ADI-R; Lord et al., 1994). This assessment is a standardized, semi-structured interview, approximately 90 min long, conducted with caregivers of children with autism disorder. It includes questions about the child s family, schooling, developmental history, and behaviors commonly associated with autism disorder (i.e., domains such as verbal and non-verbal communication, reciprocal social interaction, repetitive or stereotyped activities or behaviors). The interview systematically asks about impairments in these domains, obtaining detailed descriptions of behaviors to inform a diagnosis of autism and related disorders. Autism Diagnostic Observation Schedule-Generic (ADOS-G; Lord et al., 1989). This assessment is a standardized, semi-structured observation of the child, lasting approximately min. The examiner engages the child in activities designed to elicit social and communicative behaviors through presentation of toys/objects and opportunities for interaction. The measure consists of four modules, one of which is selected depending on the child s level of expressive language, and assesses social interaction, communication, play, and imagination. Childhood Autism Rating Scale (CARS; Schopler et al., 1980). This assessment is a 15-item behavior rating scale that was designed to identify children with autism. Seven-point rating scales indicate the degree to which the child s behavior deviates from an age-appropriate norm. Although it lacks DSM-IV specificity, it is widely used and found to be a reliable screening instrument. Scores between 15 and 30 represent typical, non-autism levels of functioning. In this study, the CARS was used only to rule out autism in the control sample; it was not used as a screen for autism since the more detailed ADI-R and ADOS-G were available. Early Social Communication Scales (ESCS; Mundy & Hogan, 1996). The abridged version of the ESCS was used to measure nonverbal communication skills in young children. The ESCS has reliably detected functional impairments in children with autism and developmental delays (Mundy, Sigman, & Kasari, 1990). It is a 20-minute structured, videotaped interaction used to assess skills that typically develop between the ages of 8 and 30 months. The ESCS targets three domains: social interaction (e.g., appeals for toy, turn-taking), joint attention (e.g., points, alternating gazes), and behavioral regulation (i.e., child s behaviors when toy ceased to function or was placed out of his/her reach). Four subscales representing these domains were used in this study (missing data precluded inclusion of a 5th subscale): Responds to Social Interaction (total frequency of behaviors such as eye contact, reach, and vocalization, in response to tester s social interaction or bid); Responds to Joint Attention (percent of trials in which child correctly turns eyes or head in direction of tester s point), Initiates Joint Attention (total frequency of all joint attention bids, including eye contact, pointing and showing), and Requesting Behaviors (also known as Initiates Behavioral Regulation, Mundy & Hogan, 1996; total frequency of requesting bids such as eye contact, reach, give object, and point). Requesting behaviors differ from joint attention behaviors in that the former have more of an imperative or instrumental function, rather than the social-sharing function that is characteristic of joint attention behaviors (Mundy & Hogan, 1996). Communicative bids in the social interaction category refer to objects less than in requesting or joint attention categories and rely more on face-to-face interactions in which objects are not the focus (Mundy & Hogan, 1996). Procedure Children who were recruited as part of the larger project received a full battery of neuropsychological and educational testing. Parents of all children were asked to complete the CARS (Schopler et al., 1980) as part of the intake process. Typically developing children were recruited from a community volunteer sample; CARS scores for these children ranged from 15 to 19.5, which is well below the cutoff and

4 660 Goldberg et al. consistent with non-autism. Each child who participated in the ESCS study was videotaped interacting with a trained experimenter, who attempted to engage the child in various play situations. Sessions lasted 18 min on average, and the mother remained near the child throughout the session. Sessions were somewhat longer for the controls than for the other two groups. Following training in coding procedures, two undergraduate research assistants independently coded each ESCS session. Coders and examiners were blind to the child s group status. Percent agreement between raters averaged 82.2%. Agreement was defined as +/) one tally on subscales that involved frequency counts. Discrepancies were resolved through group discussion and review of tapes to reach consensus. RESULTS Overall, the social and communication behaviors of the younger siblings resembled the ASD children more than the typically developing young children. The Kruskal Wallis test, which is the non-parametric equivalent of analysis of variance, indicated a significant difference between the groups on three of the four subscales: Responds to Social Interaction, Initiates Joint Attention, and Requesting Behaviors. The rank sum scores of the younger siblings fell consistently between the scores of the typically developing children and the ASD children. In pairwise comparisons, the young siblings performance on the ESCS sometimes differed significantly from the typically developing children, but the scores of the younger siblings did not significantly differ from the scores of the ASD children. As an added check on the normalcy of our control sample of young, typically developing children, we compared our control sample s scores to normative data reported in Mundy and Gomes (1998). One-sample t-tests were conducted between the mean scores for three of ESCS scale scores (IJA, RJA, RB) for the 24 normally developing infants who were included in the two experiments reported in Mundy and Gomes (1998). The preponderance of non-significant findings points to the comparability of our control data with the data reported in Mundy and Gomes (1998). Results for each of the subscales are presented below and are depicted in Fig. 1 a d. Following these results, in order to provide insight into the heterogeneity of scores within groups, individual data are presented for the children in the study. Individual scores on the ESCS subscales are represented graphically in Fig. 2 a d. Fig. 1. Group differences in rank scores on ESCS subscales.

5 Younger Siblings of Children with Autism 661 Group Differences Responds to Social Interaction The groups differed in their level of response to social interaction initiated by the tester, Kruskal Walllis Test Statistic (df = 2) = 13.24, p <.001. In follow-up pairwise tests with adjustments for multiple comparisons, the typically developing children (rank sum = 179) showed significantly more frequent eye contact, gestures, and turn-taking in response to the tester than the ASD children (rank sum = 60; zstat = 3.49, p <.05) and the younger siblings (rank sum = 86, zstat = 2.57, p <.05). ASD children did not differ significantly from the younger siblings. See Fig. 1a for a graphic depiction. Initiates Joint Attention The groups differed in their use of nonverbal behaviors to initiate shared experiences of objects or events with the tester, Kruskal-Wallis Test Statistic (df = 2) = 13.81, p <.001. Examining the pattern of scores, the typically developing children (rank sum = ) engaged in more shared eye contact, pointing and showing behaviors than the younger siblings (rank sum = 99.00), who in turn initiated more joint attention behaviors than the ASD children (rank sum = 50.50). The pairwise comparison between the control sample and ASD children was significant (zstat = 13.19, p <.05). ASD children did not differ significantly from the younger siblings. Fig. 1b displays these data. Responds to Joint Attention Although the group differences in the percent of trials in which the children followed the tester s line of regard and points were not significant, Kruskal Wallis Test Statistic (df = 2) = 3.10, ns, the rank sums followed the expected pattern. That is, the rank sum for the younger siblings (116) was between that of the typically developing children (134) and the ASD children (75). These data are depicted in Fig. 1c. Requesting Behaviors (Initiates Behavioral Regulation) The groups differed in the total frequency of requesting bids, when, for example, a toy stopped a 16 c 20 RSI Individual Rank Scores ASD Control Young Sib GENDER Male Female IJA Individual Rank Scores ASD Control Young Sib GENDER Male Female b 120 d 40 RJA Individual Rank Scores ASD Control Young Sib GENDER Male Female RB Individual Rank Scores ASD Control Young Sib GENDER Male Female Fig. 2. Individual rank scores on ESCS subscales.

6 662 Goldberg et al. working or was out of reach, Kruskal Wallis Test Statistic (df = 2) = p <.01. Significant differences were found between the scores of the typically developing children (rank sum = 170) and younger siblings (rank sum = 83, zstat = 2.39, p <.05) and the children with ASD (rank sum = 72, zstat = 2.77, p <.05). ASD children did not differ significantly from the younger siblings. These data are displayed in Fig. 1d. Individual Data Inspection of plots of individual scores on the subscales provides additional descriptive information (see Fig. 2 a d). For two of the subscales in particular (Responds to Social Interaction and Requesting Behaviors) that showed significant group differences between the control group and the ASD and younger siblings, but not between the ASD and younger siblings groups, the plots were confirming: Dispersion of raw scores for the younger siblings and ASD children were quite similar and were distinct from the controls. On the Initiates Joint Attention subscale, some younger siblings had low frequency scores like the ASD children and some scored similarly to the controls. The individual plots also support the non-significant group differences for Responds to Joint Attention. The graphic representation also indicates that, across the three groups, males often obtained the lowest frequency scores. DISCUSSION Results of this study suggest that very young children in a family with an older child with ASD are at risk for atypical development themselves. In three of four domains, the behaviors of the three groups differed significantly. In particular, the social interaction, joint attention, and requesting behaviors of the younger siblings differed significantly from typically developing children. Pairwise contrasts indicated that the younger siblings behavior in responses to social interaction bids, initiations of joint attention, and requesting behaviors was distinct from the behaviors displayed by young typically developing children, but did not differ significantly from their affected siblings. Our findings are consistent with reports of impaired prosocial behavior among other samples of children with autism (e.g., Mundy et al., 1990) and the school-aged younger siblings of children with autism (Hastings, 2003a). The ESCS was again confirmed as a useful tool for discriminating the nonverbal communicative skills of very young children and underscored social and joint attention deficits as characteristics of autism spectrum disorders. Strengths of the study include the very young ages of the siblings and the comparison of younger siblings of children with ASD to both children with ASD and typically developing children who themselves were younger siblings of typically developing children (one control group child was an only child). Indeed, a recent meta-analysis called for more studies with siblings of typically developing children because of the relative dearth of studies with this comparison group (Yirmiya et al., 2001). When the current study findings are coupled with other research (e.g., Bailey et al., 1995; Bolton et al., 1994; LeCouteur et al., 1996; Maclean et al., 1999; Zwaigenbaum et al., 2000), it is apparent that the younger siblings of children with ASD are not suitable candidates for control groups that presume typical development. Descriptive statistics indicated that our younger siblings are a heterogeneous group in terms of their performance on different subscales and their performance is frequently below that of typical children. Given previous research on the concurrence of autism and related disorders among family members, we expect that some of these toddlers will meet criteria for ASD when they are old enough to be tested reliably with the ADI-R and ADOS-G. In these instances, the ESCS may be detecting affected siblings early on and we may be witnessing a shared genetic etiology that is evident in certain impairments at an early age. Indeed, the very early age itself suggests genetic underpinnings. Other younger siblings may later display subthreshold social communicative impairments the broad phenotype or lesser variant of autism (LeCouteur et al., 1996; Zwaigenbaum et al., 2000), and others may not be affected at all. Although gender would be expected to be related to the broader phenotype, with males more affected, in our small sample, systematic gender differences among the younger siblings were not evidenced. However, across groups, the lowest frequencies often were obtained by males. The most parsimonious explanation for the finding of lower frequencies of various social and communicative behaviors among younger siblings of affected children points to the broad phenotype of autism spectrum disorders. Given the complexity of the autism phenotype, genetic vulnerability may be compounded by environmental factors such as atypical patterns of family interaction in families with

7 Younger Siblings of Children with Autism 663 children with autism. Research points to adverse affects on parental well-being due to the pressures of rearing a child with autism (Lainhart, 1999) and negative associations between maternal stress and child behavior (Hastings, 2003b). The increased anxiety and tenseness found among parents of children with autism has been interpreted as speaking at once to the genetic liability to autism and to the burden of rearing a child with autism (Murphy et al., 2000). As Rutter (2002) observed, even with the traits that are the most strongly genetically influenced, environmental effects are far from trivial (p. 3). As familial and other environmental factors are considered in future research on the vulnerability of younger siblings, the bi-directionality of influences needs to be considered. Profoundly atypical social experiences in the first year of life may negatively affect specific neuropsychological as well as brain processes, rather than just the converse (Klin, Schultz, & Cohen, 2000). Research on neurological processes involved in joint attention development among normal infants suggest that not only are disturbances in social orienting and joint attention symptomatic of autism, but early experiences may drive aspects of postnatal brain development and play a role in the etiology of the disorder (Mundy & Neal, 2001). The results from the current study point to the fruitfulness of further research with the very young siblings of children with autism. Our findings require replication, of course, and raise certain perplexing methodological issues. One issue is the choice of comparison groups. Appropriate use of comparison groups i.e., siblings of children with Down syndrome or another specific chromosomal disorder, siblings of children with learning disabilities, and siblings of children with psychiatric disorders such as schizophrenia can help disentangle genetic risk and environmental effects (Yirmiya et al., 2001). Age matching between younger siblings and their older, affected siblings is, by definition, impossible. The comparison group of affected children, i.e., children who are known to have autism or a related disorder, had to be old enough to test using currently available diagnostic tools. Another agerelated issue is the reliability of IQ assessment. Scales such as the Stanford-Binet may not detect developmental delays in children under six (Saylor, Boyce, Peagler, & Callahan, 2000). In this study, we only used the Mullen and Stanford-Binet for descriptive purposes. Finally, the ESCS provides a window into the social and communicative skills of very young children, but it is not intended to be a diagnostic instrument. We found that a child who is low in one domain (e.g., responds to social interaction) could be high in another (e.g., initiates joint attention). At this point, it is difficult to predict which very young siblings will be on the spectrum, but longitudinal follow-up and full testing are warranted when the children are older. ACKNOWLEDGEMENTS This study was supported by a grant from the National Institute of Child Health and Human Development (NICHD); Contract grant number: HD (M.A. Spence, Principal Investigator). Special thanks to: Lee Mays, Pam Flodman, Makiko Tanabe, Michelle Yang, Julie Endres, Jennifer Ferrouge at UC Irvine, and Michael Siller at UCLA. Portions of this manuscript were presented in a poster at the April 2002 meeting of the Western Psychological Association, Irvine, California. 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