Early diagnosis of autism: Current status of the Baby and Infant Screen for Children with aUtIsm Traits (BISCUIT-Parts 1, 2, and 3)

Early diagnosis of autism: Current status of the Baby and Infant Screen for Children with aUtIsm Traits (BISCUIT-Parts 1, 2, and 3)

Research in Autism Spectrum Disorders 6 (2012) 1135–1141 Contents lists available at SciVerse ScienceDirect Research in Autism Spectrum Disorders Jo...

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Research in Autism Spectrum Disorders 6 (2012) 1135–1141

Contents lists available at SciVerse ScienceDirect

Research in Autism Spectrum Disorders Journal homepage: http://ees.elsevier.com/RASD/default.asp

Early diagnosis of autism: Current status of the Baby and Infant Screen for Children with aUtIsm Traits (BISCUIT-Parts 1, 2, and 3) Johnny L. Matson *, Kim Tureck Louisiana State University, Baton Rouge, LA 70803, United States

A R T I C L E I N F O

A B S T R A C T

Article history: Received 8 January 2012 Accepted 27 February 2012

The benefits of early intervention for very young children with autism are now well established. Hand and hand with these interventions is the necessity of psychometrically sound diagnostic tools. Not only should these tools be instrumental in differentiating developmentally delayed and other at risk infants. These measures should also be structured to address challenging behaviors and psychopathology. The latter problems cooccur at high rates in infants who evince autism. Being able to identify these behaviors and symptoms, and to monitor the effectiveness of interventions to remediate these problems, is a high priority. The Baby and Infant Screen for Children with aUtIsm Traits (BISCUIT), is designed to address all of the issues listed. At this writing, the BISCUIT has the best psychometrics of any of the early childhood evaluation scales. Over 80 studies have been published to date using the BISCUIT. The purpose of this paper was to review the current status and future research trends using this test battery. ß 2012 Elsevier Ltd. All rights reserved.

Keywords: BISCUIT Autism Commorbity Challenging behaviors

Autism spectrum disorders (referred to as autism going forward in this paper) are lifelong (Ben Itzchak, Lahat, & Zachor, 2011; Gillberg, 2010; Johansson, Gillberg, & Ra˚stam, 2010; Matson & Kozlowski, 2011; Nyde´n et al., 2010; Wing, Gould, & Gillberg, 2011). The condition is generally considered to be neurodevelopmental, but individuals do respond to behavioral interventions (Rivet & Matson, 2011; Weinkauf, Zeug, Anderson, & Ala’i-Rosales, 2011). Among the characteristics which distinguish the condition are deficits in communication and socialization (Clarke et al., 2011; Duffy & Healy, 2011; Fernell & Gillberg, 2010; Gillberg, 2010; Kaland, 2011; Worley, Matson, Sipes, & Kozlowski, 2011). These individuals also evince a number of aberrant behaviors such as stereotypies and repetitive behaviors, which are core features of the disorder (Briegel, Schimek, & Kamp-Becker, 2010; Suzuki, 2011). Other behaviors which are not core features of the disorder are often present. Among these problems are challenging behaviors and co-occurring psychopathology (Bakken et al., 2010; Davis, Fodstad, et al., 2011; Funabiki, Kawagishi, Uwatoko, Yoshimura, & Murai, 2011; Horovitz, Matson, Sipes, Shoemaker, et al., 2011; Lugnega˚rd, Hallerba¨ck, & Gillberg, 2011; Mahan & Matson, 2011; Matson, Belva, Hattier, & Matson, 2011; Matson, Boisjoli, Hess, & Wilkins, 2011; Poppes, van der Putten, & Vlaskamp, 2010; Worley & Matson, 2011). Motor deficits, both fine and gross motor, and cerebral palsy, are also commonly co-occurring conditions (Forti et al., 2011). Because of these core symptoms and co-occurring problems, autism is a condition that requires both early identification and treatment, which continues into adulthood (Fava et al., 2011; Levy & Perry, 2011; Lung, Chiang, Lin, & Shu, 2011; Matson, Rieske, & Tureck, 2011; Meyer, Ingersoll, & Hambrick, 2011).

* Corresponding author at: Department of Psychology, Louisiana State University, Baton Rouge, LA 70803, United States. E-mail address: [email protected] (J.L. Matson). 1750-9467/$ – see front matter ß 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.rasd.2012.02.009

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The purpose of the present study was to provide an update on the current status of the Baby and Infant Screen for Children with aUtIsm Traits (BISCUIT), which is the most heavily researched of the early identification scales. It is the most successful and best established such measure to date.

1. Psychometrics Before a new test can be used to explore characteristics of the disorder in question, basic psychometrics must be established. Reliability, validity, establishing the factor structure of the measure, cut-offs, and norms are all needed to insure a viable instrument (Matson & Sipes, 2010). The first study on the BISCUIT established the reliability of all three parts of the test battery: (1) core symptoms of autism and PDD-NOS, (2) comorbid psychopathology, and (3) challenging behaviors. The authors evaluated test data on 276 children who were 17 to 37 months of age (M = 26.83 months, SD = 5.27 months) (Matson, Wilkins, et al., 2009). A subset of items from all three tests had robust reliability. Methods included removing items with very low endorsements, followed by analyzing individual item correlations and internal reliability (internal consistency). The next step in establishing the psychometrics of the BISCUIT involved a series of validity studies. Matson, Wilkins, and Fodstad (2011) reported on the convergent and divergent validity of the BISCUIT Part 1 in a sample of 1007 children 17–37 months of age. BISCUIT scores converged with the Modified Checklist for Autism in Toddlers (M-CHAT) and the Personal–Social domain from the Battelle Developmental Inventory (Second Edition, BDI-2). (Deficits in social and communication skills are core features of the disorder.) Divergent validity was demonstrated by low correlations with the Adaptive and Motor domains of the BDI-2. Sensitivity and specificity have also been established for the BISCUIT (Matson, Wilkins, et al., 2009). In this study, 1007 children ages 17–37 months were diagnosed with autism, PDD-NOS, or with no diagnosis by a licensed clinical psychologist using data from the M-CHAT, DSM-IV-TR, and BDI-2. Independent reliability of 99% agreement was established with a second Ph.D. level clinical psychologist who independently diagnosed 97 children using the same methods. From this sample, 178 were diagnosed with autism, 152 were diagnosed with PDD-NOS, and 677 received no diagnosis. Chi-square analyses were run on all items of the BISCUIT. Every item significantly differentiated children with an Autism Spectrum Disorder (ASD). Cutoff scores for autism and Pervasive Developmental Disorder-Not Otherwise Specified (PDD-NOS) were empirically established, and then children in defined categories were compared to clinically derived diagnoses. The M-CHAT produced a sensitivity of 74.1, specificity of 87.5, and correct classification rate of 83.0, while the BISCUIT values were 93.4 for sensitivity, 86.6 for specificity, and 88.8 for correct classification. The results above were refined and expanded upon in a second study. Matson, Fodstad, and Dempsey (2009) tested 1957 infants 17–37 months of age. Study 1 produced results similar to those noted above on the BISCUIT, and additionally a subset of items was found to distinguish between persons with an ASD versus those without this diagnosis. Study 2 compared children diagnosed with autism to children diagnosed with PDD-NOS. (The no diagnosis group was excluded.) The purpose of the study was to confirm that the BISCUIT was sufficiently sensitive to distinguish between these two highly prevalent ASDs. This hypothesis was answered in the affirmative. The notion of using a few items from the scale to identify children with ASD has also been explored. LoVullo and Matson (2012) tested 2168 at risk infants, 17–37 months of age. They employed Discriminant Functional Analysis (DFA) and Receiver Operating Characteristics (ROC) analysis. A 5 item scoring algorithm with comparable diagnostic accuracy to the entire BISCUIT-Part 1 was established. Matson, Fodstad, et al. (2009) also showed that autism or PDD-NOS could be differentiated from each other. The authors suggested that a few items could be used as a screener, with the entire scale being administered to children identified as at risk. The additional items help further establish the diagnosis, and also provide a rich source of information for treatment planning and for evaluating treatment effectiveness (by administering the BISCUIT battery post intervention). The BISCUIT has also been factor analyzed. Matson, Boisjoli, et al. (2011) employed 1287 children 12–37 months of age. The exploratory factor analysis produced a three factor solution that mirrored the triad of core ASD symptoms; communication, socialization, and stereotyped repetitive behaviors. All three factors yielded higher scores for those with an ASD diagnosis versus those children without an ASD diagnosis. For Part 2 of the BISCUIT 270 infants with autism or PDD-NOS were studied (Matson, Boisjoli, et al., 2011). A five factor solution was found: tantrum/conduct, inattention/impulsivity, avoidance behavior, anxiety/repetitive behavior, and eating/sleeping problems. Part 3 of the BISCUIT has also been factor analyzed. Matson, Boisjoli, Rojahn, and Hess (2009) evaluated 270 infants 17–37 months old. A three factor solution emerged and conceptually fit a priori established factors: (1) aggressive/disruptive behavior, (2) stereotypic behavior, and (3) self-injurious behavior. Cutoffs and norms have also been reported. Earlier in this section, the cut-offs and norms for Part 1 of the BISCUIT were noted. Cut-offs and norms have also been reported for Parts 2 and 3. For Part 2, the psychopathology comorbidity scale, 309 children with and ASD diagnosis participated in establishing the cut-offs and norms (Matson, Fodstad, Mahan, & Sevin, 2009). Then 460 children, with and without an ASD were compared on all five factors of the BISCUIT-Part 2; tantrum, conduct behavior, inattention/impulsive, avoidant behavior, anxiety/repetitive behavior, and eating problems. Children with an ASD had higher scores on all five factors, compared to children without a diagnosis of ASD. Cut-offs for total and subtest scores for the BISCUIT-Part 3 was reported for 312 children diagnosed with an ASD (Rojahn et al., 2009). A second study on norms and cut-offs scores used a larger sample (644 children) with developmental delays

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(with and without ASD) (Matson, Fodstad, Mahan, & Rojahn, 2010). In this study, the authors also note that aggressive/ destructive acts were the most common problems, and they could be readily identified in these very young children. 2. Diagnosis The big issue in the area of diagnosis is early detection (Matson, Rieske, et al., 2011). This process can be made more difficult when children are very young, because skill sets which help differentiate those persons with or without ASD have not fully emerged. Additionally, intellectual disability (ID) can present with symptoms that mimic ASD, further confusing the diagnostic picture (Rojahn & Matson, 2010). Finally, communication disorders may appear similar for one or two of the three triads, particularly at young ages, and these must be taken into account when differentially diagnosing ASD (Matson & Neal, 2010). What we do know, however, is that this disorder and its associated behavioral symptoms can be identified at an early age, and that these symptoms are stable over time (Matson & Horovitz, 2010; Worley, Matson, Mahan, Kozlowski, & Neal, 2011). The major exception to this finding is that a subset of children develop relatively normally, then regress with the development of numerous ASD symptoms at roughly 20–24 months of age (Matson, Wilkins, & Fodstad, 2010). Efforts to shape and sharpen diagnostic efforts for very young children have been enhanced by parent reports of first concerns. Horovitz, Matson, and Sipes (2011b) assessed 1393 toddlers. They noted clear and more pronounced deficits in socialization, non-verbal communication, and repetitive behavior in children with ASD than for children with other types of developmental disabilities. These findings were then replicated with the overall subscale scores of the BISCUIT (Horovitz et al., 2011b). These deficits occur on a number of parameters. For example, while communication problems appear at an early age for developmentally delayed children in general, they are apparent at the youngest ages for those infants with ASD (Horovitz, Matson, & Sipes, 2011c; Kozlowski, Matson, Horovitz, Worley, & Neal, 2011). Finally, more severe core symptoms of ASD are related to co-occurring conditions such as psychopathology (Matson, Mahan, et al., 2011). The BISCUIT has excellent sensitivity and specificity. It has proven useful in differentiating an ASD from other developmental problems such as hearing impairments and more general atypical development (Worley, Matson, & Kozlowski, 2011). Additionally, the BISCUIT has proven to have higher sensitivity and specificity than other well-established early diagnosis/screening measures (Kozlowski, Matson, Worley, Sipes, & Horovitz, 2012). 3. Prevalence and core symptoms The BISCUIT has been used to help establish rates of ASD in infants at risk for developmental delays. Worley, Matson, and Kozlowski (2011) assessed 2027 children 17–37 months of age. As anticipated, rates of ASD were higher for this at risk group compared to a general population of older children, which is how most prevalence data has been reported. However, male to female ratios were lower than in previous studies, 1.16 to 1. A number of other interesting papers have emerged with this age group. For example, communication levels of 168 toddlers with challenging behaviors have been studied (Matson, Boisjoli, & Mahan, 2009). Lower levels of expressive and receptive communication were correlated with more aggressive, disruptive, and self-injurious behavior. These deficits in communication along with social deficits are evident at a very early age (Fodstad, Matson, Hess, & Neal, 2009). Hattier and Matson (2012) evaluated 591 toddlers 17–37 months old with autism, PDD-NOS, or no ASD. Communication impairments were evaluated with the BISCUIT and the BDI-2. Deficits were greatest for children with autism, followed by PDD-NOS. Deficits were greater for overall score than for specific items (Horovitz & Matson, 2010). Communication deficits were the mildest for children at risk for developmental disabilities, but without a diagnosis of ASD. These communication deficits can also compound other problems such as anxiety symptoms (Davis et al., 2012). More severe symptoms were found to be related to greater levels of inattention and impulsivity. Hattier, Matson, May, and Whiting (in press) further noted that repetitive/restrictive behaviors were more common in children with ASD versus cerebral palsy (CP). Interaction effects are evident between multiple skill areas as well. Thus, not only do children with autism evince greater problems with communication and social behaviors than persons with CP, they also experience more fine and gross motor problems (Sipes, Matson, & Horovitz, 2011). Similarly, the co-occurrence of CP with autism resulted in more communication deficits compared to autism alone (Hattier, Matson, & Kozlowski, 2012). However, the combinations of these problems appears to be particularly debilitating since children with CP alone had fewer communication deficits than children with Down Syndrome or children with a history of seizures based on results of the BISCUIT (Hattier, Matson, Sipes, & Turygin, 2011). 4. Relationship to other problems and disorders A substantial number of studies have been published which look at challenging behaviors (CB) using Parts 1 and 3 of the BISCUIT. Stereotypic behaviors, for example, were highest for persons with the most severe autism symptoms (Matson, Dempsey, & Fodstad, 2009). Developmental quotient has also been demonstrated to be a factor in severity of CB. Medeiros, Kozlowski, Beighley, Rojahn, and Matson (2012) studied 1509 infants 17–36 months of age. They found that atypically developing infants with no specific diagnosis evinced fewer CB with higher developmental quotient, while children with autism showed greater CB with higher developmental quotients. Hattier, Matson, Belva, and Horovitz (2011) evaluated 2131 toddlers 17–37 months old (633 with an ASD and 1498 with atypical development but no diagnosed ASD). Children with an ASD evinced greater numbers of CB and were also more likely

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to display multiple CBs. These trends in CB are evident even when CB are divided into age cohorts of 12–18, 19–25, 26–32, and 33–39 months of age (Fodstad, Rojahn, & Matson, in press). Similarly, lower levels of adult interaction and peer interactions have been found to be associated with higher levels of stereotypic behavior, aggression, destruction, and selfinjurious behavior (Matson, Neal, Fodstad, & Hess, 2010). Tantrums and conduct problems are more prevalent when autistic symptoms are more severe (Sipes, Matson, Horovitz, & Shoemaker, 2011). However, children with autism, Down syndrome, general developmental delay, prematurity, cerebral palsy, and seizure disorders did not differ by group (Sipes, Rojahn, Turygin, Matson, & Tureck, 2011). Additionally, CB for these very young children with ASD did not differ by gender (Kozlowski & Matson, 2012). Gender differences were absent on Part 3 of the BISCUIT for 17–37 month olds with cerebral palsy, Down syndrome, or seizure disorder. Comorbid psychopathology is also a common problem among persons with autism (Smith & Matson, 2010). An interaction effect between comorbid symptoms of psychopathology and CB among small children with ASD has also been studied. Children who scored high on avoidance and tantrum/conduct problems had more aggressive/destructive behaviors, self-injurious behaviors, and stereotypies. High levels of inattention/impulsivity were also related to a range of CB, while high rates of anxiety/repetitive behavior only covaried with stereotypies in the CB category (Matson, Mahan, Fodstad, Hess, & Neal, 2010). Anxiety and CB have also been found to co-occur in high rates on the BISCUIT for 17–37 month old (Matson, Mahan, et al., 2011). These trends continue across the lifespan (Davis, Hess, Moree, et al., 2011). Information on psychopathology among very young children with ASD is scant (Matson, Hess, & Boisjoli, 2010). However, the BISCUIT is providing some useful insights in this area. For example, all types of comorbid psychopathology measured by the BISCUIT Part 2 are more pronounced in atypically developing children with an ASD versus those who do not have an ASD (Matson, Hess, et al., 2010). Additionally, Matson, Hess, et al. (2010) evaluated 324 infants and toddlers who had no ASD diagnosis or who were diagnosed with autism or PDD-NOS. Tantrum/conduct problems, inattention/impulsivity, and eating/ sleeping problems were most common and serious for children diagnosed with autism, followed by those diagnosed with PDD-NOS. Children at risk for developmental disabilities, but without an ASD had the fewest symptoms of comorbid psychopathology. Fodstad, Rojahn, and Matson (2010) replicated these findings. Furthermore, they broke children into groups by age (12–18, 19–24, 25–31, and 32–39 months of age). Comorbid psychopathology symptoms increased with age. Many of these symptoms tended to be largely associated with autism. For example, developmental quotient had little effect on symptoms of inattention and impulsivity, while symptoms of autism did affect those behaviors (Matson, Mahan, Hess, & Fodstad, 2010). Matson, Worley, Neal, Mahan, and Fodstad (2010) studied 240 toddlers 17–37 months of age who were diagnosed with ASD. They found that those toddlers with fewer symptoms of ASD and inattention/impulsivity had significantly fewer deficits in social skills. A series of studies have also found a strong relationship between anxiety and ASD in this very young population using the BISCUIT. Anxiety and avoidance symptoms were found to be more prevalent among infants and toddlers with autism or PDDNOS compared to typically developing infants without an ASD (Davis, Fodstad, et al., 2011). Second, these symptoms are present at a very early age and persist across the lifespan (Davis, Hess, Moree, et al., 2011). Communication, one of the core deficits of autism also covaries with ASD and anxiety. Davis, Moree, et al. (2011) found that anxiety decreased as communication deficits increased. And, this trend was more pronounced for infants and toddlers with autism compared to children with PDD-NOS or no ASD diagnosis. Both receptive and expressive skills are affected by anxiety in these children (Davis et al., 2012). Moreover, infants and toddlers with greater numbers of anxiety symptoms had significantly lower developmental quotients as measured on the BDI-2 (Davis, Hess, Matthews, et al., 2011). 5. Comorbid physical problems A number of studies have been published looking at a variety of physical conditions often co-occurring with an ASD. For example, seizures co-occur at high rates among persons with ASD. Matson, Neal, Hess, Mahan, and Fodstad (2010) noted that when both of these disorders co-occured, deficits in adaptive, personal-social, communication, motor and cognitive skills were greater than when either problem occurred alone. ASD also appears to have a significant effect on developmental milestones with greater severity of autism resulting in more delays in fine and gross motor skills. This result was observed in a sample of 1044 infants and toddlers aged 17–37 months who were at risk for developmental delays (Matson, Mahan, Kozlowski, & Shoemaker, 2010). These findings are similar to those reported by Matson, Mahan, Fodstad, et al. (2010), who noted that children with autism evinced more fine and gross motor deficits than atypically developing infants and toddlers. However, the differences between fine and gross motor skills did not differ within groups. Other factors found to co-occur with autism are low birth weight, premature birth, birth defects, and obesity (Matson, Matson, & Beighley, 2011). 6. Demographic variables Studies have been conducted establishing demographic factors that are associated with autism. The preponderance of evidence suggests that males are much more likely to evince autism across the lifespan (Rivet & Matson, 2011). Several studies have been conducted to look at gender difference with the BISCUIT. For example, the age of first concern for autism was significantly younger in girls than boys (Horovitz, Matson, Turygin, & Beighley, 2012). Second, externalizing and internalizing CB did not differ by gender for 17–37 months old, but children with ASD, regardless of sex were more likely to

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evince CB than children without ASD (Kozlowski, Matson, & Rieske, 2012). It was also noted that African Americans evince more CB than Caucasians (Horovitz, Matson, Rieske, Kozlowski, & Sipes, 2011). Finally, on the triad of impairments (communication, socialization, and repetitive/restrictive behaviors), only restrictive behaviors differed. Females had significantly fewer endorsements than males (Sipes, Matson, Worley, & Kozlowski, 2011). Additionally, psychiatric symptoms did not differ by gender in these very young children (Worley & Matson, 2011). Thus, gender differences on ASD are evident only during some periods of life (Horovitz, Matson, & Sipes, 2011c). It is important to add that symptom endorsements differ between mothers and fathers (Matson, Hess, Kozlowski, & Neal, 2011). Finally, children with a biological family member with ASD were compared to infants and toddlers with no family member diagnosed with ASD using the BISCUIT (Kozlowski, Matson, & Worley, 2012). A larger percentage of children with an ASD had a biological relative with the condition compared to the group of atypically developing children. However, symptom expression for ASD did not differ depending on whether there was or was not a relative with ASD.

7. Conclusions The BISCUIT at this point is an extensively studied measure of ASD for young children. The psychometrics of this test battery have been studied in a number of papers and are well established. Additionally, the test has proven useful in assisting in diagnosis and evaluation of a variety of characteristics of infants and toddlers with ASD. One of the most striking findings in the aggregate is that many characteristics of the disorder, and the co-morbid conditions that accompany them, are present very early in life. Without effective intervention these problems are also highly persistent and durable. The assumption that the child will ‘‘grow’’ out of these problems is not tenable. Further research with the BISCUIT is underway. Among the most interesting developments is a 15 nation study using the scaling system for early detection and diagnosis. Statewide and countrywide systems are in place or being put in place for early screening and diagnosis of ASD. 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