Abstract
This prospective study of the FIRST WORDS® Project examined restricted and repetitive behaviors in a sample of 55 toddlers at a mean age of 20 months who were later diagnosed with autism spectrum disorder. Restricted and repetitive behaviors were coded using the Repetitive Movement and Restricted Interest Scales in two video-recorded observation methods–structured sampling procedures in a clinic and naturalistic everyday activities at home. Measures of restricted and repetitive behaviors were higher in the clinic setting than in the home observation, especially for behaviors involving object use. Repetitive movements with objects in the clinic predicted nonverbal developmental scores and Autism Diagnostic Observation Schedule social affect scores at later follow-up. In contrast, repetitive movements with objects at home significantly predicted later Autism Diagnostic Observation Schedule restricted and repetitive behaviors scores. These results support the utility of the Repetitive Movement and Restricted Interest Scales to detect restricted and repetitive behaviors in toddlers and suggest that observations of restricted and repetitive behaviors in clinic and home settings may provide unique and important diagnostic information for improving early detection of autism spectrum disorder.
Introduction
The proposed criteria of the fifth edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM -5; American Psychiatric Association [APA], 2011) include restricted repetitive patterns of behavior, interests, or activities as a core diagnostic domain of autism spectrum disorders (ASD; APA, 2000, 2011), along with persistent deficits in social communication and social interaction. The diagnostic criteria require at least two of the following restricted repetitive behaviors (RRB): (1) repetitive or stereotyped speech or movements with the body or objects, (2) excessive insistence on sameness or adherence to ritualized patterns or routines, (3) restricted or fixated interests unusual in intensity or focus, and (4) unusual sensory interests or hyporesponsivity and/or hyperresponsivity to sensory stimuli. Most of the evidence documenting RRB as a diagnostic domain of ASD in children below the age of 2 years has been collected in clinical settings (Kim and Lord, 2010; Loh et al., 2007; Morgan et al., 2008; Ozonoff et al., 2008; Watt et al., 2008; Wetherby et al., 2004). While a limited number of studies examined RRB in early home videos of children later diagnosed with ASD (Baranek, 1999; Osterling and Dawson, 1994; Osterling et al., 2002), no studies to date have observed RRB in both clinical and home settings using a prospective sample of very young children with ASD.
The National Research Council (NRC, 2001) recommended that children with ASD begin receiving intensive intervention as early as possible to maximize treatment outcomes, preferably before the age of 3 years. Better screening for ASD at younger ages will lead to earlier identification and therefore earlier enrollment in intervention (NRC, 2001; Wetherby et al., 2004). The setting of a behavioral screening and assessment may have an impact on which child behaviors will be observed. Factors such as the child’s familiarity with social partners, the structure of activities, and the novelty of objects could affect the manifestation of early signs of ASD in young children. Because of these factors, the NRC (2001) emphasized the importance of screening and assessment of ASD across settings. Completing screenings and assessments in the home as well as the clinic may be useful for observing a child’s behaviors in both familiar and novel contexts.
The presence of RRB in young children with ASD
Little consensus exists in the literature regarding the utility of RRB in the diagnosis of ASD in very young children. Several studies have shown that the presence of RRB did not distinguish children with and without ASD before the age of 3 years using parent report measures and clinical assessments (Lord, 1995; Moore and Goodson, 2003; Stone et al., 1999; Ventola et al., 2006). More recent studies using direct observations of toddlers in the second year of life have shown that RRB can be observed in very young children with ASD, supporting the utility of RRB as a core diagnostic feature (Kim and Lord, 2010; Loh et al., 2007; MacDonald et al., 2007; Morgan et al., 2008; Ozonoff et al., 2008; Watt et al., 2008; Wetherby et al., 2004). Possible reasons for this discrepancy include differences in method and type of RRB measured.
A few prospective studies of younger siblings at risk for ASD have documented RRB in infants. Some of these findings include atypical patterns of object exploration (Ozonoff et al., 2008); sensory oriented behaviors, such as dangling beads in front of the eyes in a self-stimulatory manner (Zwaigenbaum et al., 2005); increased visual attention to nonsocial stimuli (Bhat et al., 2010); and difficulty in disengaging visual attention from objects (Zwaigenbaum et al., 2005). Difficulty shifting visual attention, also referred to as “sticky attention,” may be an early precursor to restricted or fixated interests on unusual objects. These studies suggest that RRB can be observed even in the first and second years of life, and that further research is needed examining RRB in younger samples.
The majority of studies examining RRB using direct observation have observed these behaviors in a clinical setting. Several studies have documented the early signs of ASD in naturalistic settings using retrospective home video samples collected from the parents or other caregivers before their child was suspected of having ASD. Baranek (1999) observed signs of ASD in 10-min samples of early home videos of children at 9–12 months of age. While RRB were observed in all participants regardless of diagnostic status, these behaviors did not differentiate children with ASD from children with other developmental disorders (DDs) or typically developing (TD) children. Using videotapes of first birthday celebrations, Osterling and Dawson (1994) identified behaviors that differentiated children with ASD from TD children. Behaviors in the area of social communication were most likely to successfully distinguish children with ASD from TD children, with looking at face classifying 77% of the participants. While the authors did not look at RRB alone, they found group differences in “ASD-specific behaviors,” including RRB, such as self-stimulatory behavior and covering ears as well as the social communication item “failing to orient to name.” A follow-up study of home videotapes reported significantly higher rates of repetitive motor actions in 12-month-old children with ASD than TD children but did not find significant differences between children with ASD and children with other DDs (Osterling et al., 2002).
Thorsen et al. (2008) compared ASD features in home videotapes of 24-month-old children with ASD in different contexts—birthday parties and home observations not during the child’s birthday party. They found that social communication behaviors and use of eye contact differed across the contexts, with the behaviors coded from the nonbirthday observations being more predictive of later functioning. While this study provides evidence for the importance of context when measuring behaviors associated with ASD, the authors did not examine the presence of RRB in this sample.
Relationship between RRB and developmental outcomes and ASD symptoms
In addition to the disagreements in the literature regarding the presence of RRB as a diagnostic marker in young children with ASD, little consensus exists regarding the relationship between RRB below 3 years of age and later measures of developmental functioning and ASD symptoms. Several studies have reported no link between RRB and developmental measures (Lord and Pickles, 1996; Mooney et al., 2006), while recent studies have found relationships between these variables. In a large study using the Autism Diagnostic Interview–Revised (ADI-R; Lord et al., 1994) for 830 children with ASD between the ages of 15 months and 11 years, Bishop et al. (2006) found that the correlation between nonverbal intelligence and RRB became stronger with age. Using detailed video coding software to code RRB, Watt et al. (2008) observed significant negative correlations between repetitive movements with objects (RMO) and developmental level both in the second year and at age 3. In the same sample, Morgan et al. (2008) observed a significant correlation between the composite score of repetitive movements of the body and RMO and outcomes in the fourth year. Specifically, RRB were related to nonverbal and verbal developmental quotients (DQs) measured by the Mullen Scales of Early Learning (MSEL; Mullen, 1995) and the RRB algorithm score of the Autism Diagnostic Observation Schedule (ADOS). Other studies have also found a relationship between observational measures of RRB and the ADOS. For example, Ozonoff et al. (2008) observed a significant correlation between the frequency of object spinning and unusual visual exploration at 12 months and ADOS algorithm scores at 36 months.
Purpose
This study examined RRB in 55 toddlers later diagnosed with ASD late in the second year of life using video from two sampling contexts—structured observations using systematic structured sampling procedures in a clinic setting and naturalistic observations in the home. The study addressed two specific research questions about toddlers with ASD: (1) what is the relationship between RRB in clinic observations compared to home observations and (2) what is the relationship between RRB in clinic and home observations compared to (a) concurrent measures of social communication and (b) later measures of cognitive development and autism symptoms?
Method
Participants
This study included 55 participants who were recruited from the FIRST WORDS® Project, a prospective longitudinal study. All participants included in the current study received a best-estimate diagnosis of ASD at 3 years of age from a multidisciplinary clinical team, which included a speech–language pathologist and psychologist. Children completed a diagnostic evaluation consisting of the ADOS, Social Communication Questionnaire (Rutter et al., 2003), Vineland Adaptive Behavior Scales (VABS; Sparrow et al., 1984), MSEL (Mullen, 1995), a home observation, and a developmental history. Best-estimate diagnoses were made based on information gathered using the fourth edition of DSM (DSM-IV; APA, 2000) diagnostic criteria. This comprehensive assessment battery allowed the team to accurately distinguish children with ASD from children with other disorders or developmental delays.
Children who met the following criteria were included in the current study: (1) completed Communication and Symbolic Behavior Scales (CSBS) behavior sample (Wetherby and Prizant, 2002) between ages 15 and 24 months, (2) completed a video-recorded home observation within 3 months of the CSBS documenting child behaviors during everyday activities, and (3) received a diagnosis of ASD based on the diagnostic evaluation completed between 30 and 42 months of age. Of the 55 participants who met these criteria, only 1 participant was also included in the study reported by Morgan et al. (2008). See Tables 1 and 2 for participant demographic and developmental characteristics. All of the measures used to characterize the sample are included in Table 2. All of these measures except the VABS were also used in the analyses of this study to address the research questions. None of the participants were enrolled in intervention research prior to the time of their CSBS or home observation.
Summary of participant demographics (N = 55).
Summary of developmental characteristics (N = 55).
CSBS: Communication and Symbolic Behavior Scales; MSEL: Mullen Scales of Early Learning; VABS: Vineland Adaptive Behavior Scales; ADOS: Autism Diagnostic Observation Schedule; SS: standard score; DQ: developmental quotient; SA: social affect; RRB: restricted repetitive behaviors; SD: standard deviation.
SSs based on a M of 10 and SD of 3.
SSs based on a M of 100 and SD of 15.
Measures in the second year of life
CSBS behavior sample
The CSBS behavior sample provides a standardized sampling context in which infants and toddlers between the ages of 9 and 24 months interact with a clinician and a caregiver. The behavior sample uses a standard set of systematic temptations and procedures that were developed to encourage spontaneous social and communicative behaviors. Children are seated at a table and presented with a series of 12 communication opportunities, including a wind-up toy, bubbles, balloon, jar with food, books, and a feeding and cooking set for playing. The administration of the behavior sample lasts for approximately 20–30 min. The behavior sample was video-recorded and scored using standard procedures of the CSBS by trained examiners blind to the child’s diagnosis. This scoring provides three composite scores in social, speech, and symbolic domains. The social composite measures emotion and eye gaze, communication, and gestures. The speech composite measures sounds and words. The symbolic composite measures language comprehension and object use in play. This standard scoring demonstrates good internal consistency and test–retest stability based on norming of a national sample (Wetherby and Prizant, 2002). Research has also indicated that the CSBS provides good predictive validity with language outcomes at 2 and 3 years of age (Wetherby et al., 2002, 2003).
Home observation
A naturalistic home observation of the children and their parents was video-recorded for about an hour during a variety of everyday activities (e.g. play with toys, play without toys, snack, sharing books, caregiving, and family chores). Instructions were provided to parents, including descriptions and examples of each activity category. Parents were asked to select activities from at least three different activity categories and to engage their child for an hour. Parents were instructed to participate in the activity with their child as they typically would and to encourage spontaneous communication and interaction. The parent and child, along with other family members, if present, engaged in these naturalistic activities using only their own toys and materials. A trained videographer video-recorded the observation without talking to or interacting with the child or caregivers during the recording.
Repetitive Movement and Restricted Interest Scales
All of the archival video-recordings of both the CSBS behavior samples and the home observations were coded using the Repetitive Movement and Restricted Interest Scales (RMRIS; Wetherby et al., 2011). The RMRIS was developed from the Repetitive and Stereotyped Movement Scales: Companion to the CSBS (Morgan et al., 2008) by adding scales on restricted interest to measure behaviors across the RRB categories proposed in the DSM-V. Coding definitions for the items used in this study are presented in Table 3. Trained coders rated all of the CSBS behavior samples and home observations for participants in the current study using the RMRIS. During the CSBS video-recordings, a maximum of four instances of each RRB were coded per activity, for a total of 32 possible coding opportunities for each item. In the home videos, a modified partial-interval coding scheme (Merrell, 2003) was used in which each RRB was coded up to four times per 3-min interval, with total opportunities depending on video length. Scoring procedures were patterned after the CSBS in order to create a measure of RRB that would be clinically feasible and not overinflate RRB when these behaviors occur many times in a few activities. In order to directly compare RMRIS items across contexts of varying lengths, scores were totaled for each behavior and a proportion score was calculated by dividing the number of RRB observed by the number of coding opportunities.
RMRIS coding definitions.
RMRIS: Repetitive Movement and Restricted Interest Scales.
Coders were trained and reached reliability when they completed 25 training videos of children not participating in this study with generalizability (g) coefficients for all items of at least .60. Interobserver reliability was calculated for 30 randomly selected video-recordings (15 from each context) of 26 participants (27% of the data). In order to account for source and magnitude variance of scorer rating and child behaviors, g intraclass correlation coefficients were calculated. For adequate interrater reliability, g coefficients should be .60 or higher (Mitchell, 1979). For this sample, g coefficients ranged from .63 to .85 with a mean g coefficient of .76. Interobserver reliability was also calculated for each context; the mean g was .78 (range = .50–.89) for the CSBS and .78 (range = .49–1.00) for the home. Dysregulation over object removal in the CSBS and clutching objects in the home were the only items with a g coefficient less than .60. However, these coefficients should be interpreted cautiously given the low number of videos from each context.
Archival standardized measures at 30–42 months
MSEL
The MSEL was completed for all participants as a measure of cognitive functioning. This measure is appropriate for children aged 1–68 months, and assesses children’s abilities in five domains: gross motor, fine motor, visual reception, receptive language, and expressive language. Because gross motor skills are only assessed for children less than 24 months of age, these scores were not included for this sample. DQs were calculated to more fully characterize individual variation for verbal and nonverbal abilities by dividing the child’s age equivalent score by their chronological age and then multiplying by 100. The receptive and expressive age equivalents were averaged to obtain a verbal DQ (VDQ), and the fine motor and visual reception age equivalents were averaged to obtain a nonverbal DQ (NVDQ).
ADOS
The ADOS (Lord et al., 2002) is a standardized assessment of the features of ASD, including social communication and play or use of materials. The ADOS uses a semistructured interaction between a child and clinician to create opportunities for observing signs of ASD and yield scores in the domains of social affect (SA), RRB, and a total combined algorithm score (Gotham et al., 2007). Diagnostic classifications of nonspectrum, autism spectrum, and autism are based upon the total algorithm score.
Results
Comparison of RRB in clinic and home observations
Preliminary descriptive analyses indicate considerable variability across measures of RRB. For the total RRB measure in the CSBS, the skewness = 1.41 and kurtosis = 2.35. In the home, skewness = 0.75 and kurtosis = 0.08. Skewness values for individual items in either context range from 0.86 to 5.60 and kurtosis values range from 0.51 to 36.02. However, according to Maxwell and Delaney (2004), analysis of variance (ANOVA) statistics are robust to violations of normality. Descriptive data for the RMRIS items are reported in Table 4.
Descriptive statistics for RMRIS, reported as percentages of behaviors per coding opportunities (N = 55).
RMRIS: Repetitive Movement and Restricted Interest Scales; CSBS: Communication and Symbolic Behavior Scales; SD: standard deviation.
To examine differences in the proportion of RRB in the CSBS behavior samples and home observations, a within-subject ANOVA was performed for the RRB totals in the CSBS and home observation contexts. The RRB total coded in the CSBS (M = 43.9, standard deviation (SD) = 27.7) was significantly higher than the RRB total in the home observation (M = 25.1, SD = 16.9), F(1,54) = 26.09, p < .001, d = 1.49. Exploratory analyses were performed for individual RRB items to compare across contexts and are reported in Table 5. Significant between-context differences were observed between RMO in the CSBS (M = 13.8, SD = 14.0) and in the home observation (M = 3.9, SD = 4.6), F(1,54) = 26.08, p < .001, d = .79. The participants demonstrated significantly more clutching in the CSBS (M = 3.9, SD = 11.7) than in the home observation (M = 0.7, SD = 1.7), F(1,54) = 4.19, p = .045, d = .36, but this relationship is limited by the poor interrater reliability for this item. In addition, higher measures of sticky attention were observed in the CSBS (M = 7.0, SD = 6.4) than in the home observation (M = 0.8, SD = 1.3), F(1,54) = 59.34, p < .001, d = 1.52. No other significant differences were observed between contexts.
Within-subject analysis of variance comparing RMRIS scores in the CSBS and home observation (N = 55).
RMRIS: Repetitive Movement and Restricted Interest Scales; CSBS: Communication and Symbolic Behavior Scales.
To further examine the relationship between each of the RMRIS items in the CSBS and home observation, bivariate correlations were calculated (see Table 6). Significant moderate correlations were observed between measures in the CSBS and in the home observation on total RRB, r(55) = .327, p = .015; repetitive movements of body, r(55) = .337, p = .012; and sticky attention, r(55) = .442, p = .001. No other significant correlations were observed between individual items.
Pearson’s product–moment correlations between RMRIS in the CSBS and home observation (N = 55).
RMRIS: Repetitive Movement and Restricted Interest Scales; CSBS: Communication and Symbolic Behavior Scales.
p < .05, **p < .01.
Relationships between RRB and concurrent measures of communication
Concurrent bivariate correlations were examined between RRB measures and CSBS standard scores (SSs) for the social communication composites. Small to moderate significant negative correlations were observed between RMO in the CSBS and CSBS Social Composite, r(55) = −.306, p = .025; Symbolic Composite, r(55) = −.453, p = .001; and total SS, r(55) = −.411, p = .002. In the home observations, significant correlations were observed between excessive interests and CSBS Social Composite, r(55) = −.302, p = .026, and Speech Composite, r(55) = −.273, p = .046.
Relationships between RRB and later measures of cognitive development and autism symptoms
Predictive bivariate correlations examining the relations between RRB in the CSBS and home observation with later cognitive development are reported in Table 7. A large significant negative correlation was observed between RMO in the CSBS and NVDQ, r(55) = −.506, p < .001, but not between any of the RRB measures in the home and NVDQ.
Pearson’s product–moment correlations between RMRIS in the CSBS and home observation and outcome measures (N = 55).
CSBS: Communication and Symbolic Behavior Scales; MSEL: Mullen Scales of Early Learning; VABS: Vineland Adaptive Behavior Scales; ADOS: Autism Diagnostic Observation Schedule; SS: standard score; DQ: developmental quotient; VDQ: verbal DQ: NVDQ: nonverbal DQ; SA: social affect; RRB: restricted repetitive behaviors; RMRIS: Repetitive Movement and Restricted Interest Scales.
p < .05, **p < .01.
To examine the relationship between RRB in the CSBS and home observations and later measures of autism symptoms, bivariate correlations were calculated using the subscores of the RMRIS and ADOS composite scores. Significant correlations were observed between RMO in the CSBS and ADOS SA algorithm scores, r(55) = .331, p = .014, and RMO in the home and ADOS RRB scores, r(55) = .494, p < .001.
Multiple regression analyses were conducted to determine the shared and unique contributions of RMO in the CSBS and home observations, using ADOS SA and RRB scores as outcome variables. These behaviors predicted 10.9% of the variance in ADOS SA scores, R = .331, and only RMO in the CSBS predicted significant unique variance, β = 0.330, t = 2.509, p = .015, sr2 = .107. RMO in the CSBS and home predicted 24.5% of the variance in ADOS RRB scores, R = .495; only RMO in the home predicted significant unique variance, β = 0.489, t = 4.038, p < .001, sr2 = .236.
Discussion
This study examined RRB in a sample of toddlers later diagnosed with ASD across clinic and home contexts. Significantly higher measures of RRB were observed in the CSBS clinical samples than in the home videos. The CSBS behavior sample uses structured probes with objects to encourage social and communicative behaviors, so children have repeated presentations of a variety of objects during this assessment. The opportunities for object use in the home varied greatly, as the home observation provided a naturalistic view of the child’s everyday activities and routines. Because of differences in contexts, which likely influenced the availability of specific objects, it is not surprising that RRB measures were higher in the CSBS. The specific items that were observed significantly more included RMO, clutching, and sticky attention. These three items require the presence of objects to be coded, and both clutching and sticky attention were frequently coded during transitions between objects or activities, which happen at a high rate during the CSBS.
When predicting developmental outcomes (M = 27.15 months) and autism symptoms (M = 31.56 months) in the third year from RRB measured in the second year of life (CSBS M = 19.81; home video M = 20.27), a significant relationship was observed for RMO in the CSBS and later nonverbal developmental outcomes and social communication skills as measured by the ADOS SA composite. While several studies using only parent report measures reported a lack of relationship between RRB and developmental outcome (Lord and Pickles, 1996; Mooney et al., 2006), these results support previous studies that also have directly observed this relationship (Bishop et al., 2006; Morgan et al., 2008). In contrast, measures of RMO in the home predicted ADOS RRB scores. One possible explanation for this latter relationship may be the structure of the ADOS and the home observation. The ADOS is structured to follow the child’s lead and create a supportive environment that facilitates the observation of ASD symptoms as well as the child’s communicative abilities. The rates of RRB observed during this measure may be more similar to the home observations at a younger age as opposed to the adult-directed presentation of objects in the CSBS. These findings support measuring RRB across contexts, since using objects repetitively in the CSBS uniquely predicted later SA while this same behavior in the home predicted later RRB.
Using a precursor to the RMRIS, Morgan et al. (2008) observed that children with ASD displayed significantly higher rates and inventories of repetitive movements of the body and with objects than children with other DDs or TD children during the CSBS. While the current study is limited by the inclusion of only participants with ASD, it supports these results using an almost new sample and adds to these results by examining behaviors observed in the home. Further research is needed to determine whether use of the RMRIS in the home can be used to differentiate children with ASD from TD children and children with other DDs. Because it was beyond the scope of this study to examine factors in the home observations that may affect RRB, future research should determine how the presence of objects or types of activities in the home affects the rate or type of RRB.
These results could have possible clinical implications for the types of assessments and observations used to detect and diagnose ASD in very young children. While social communication deficits have been reported consistently in toddlers with ASD and across contexts (Osterling and Dawson, 1994; Wetherby et al., 2004), there are more discrepancies in the reports of repetitive behaviors at this age (e.g. Watt et al., 2008; Werner and Dawson, 2005). RRB have not previously been observed across contexts to determine whether these behaviors are topographically similar, but the results of this study suggest that the context in which RRB are observed may play an important role in the frequency and occurrence of these behaviors. This study suggests that use of the RMRIS during the CSBS could serve as a more sensitive tool for early detection but that RRB measured in both contexts contributed to predictions of later outcomes. This predictive relationship highlights the value of examining RRB at this young age. These findings suggest that, in young toddlers, engaging in frequent RRB limits opportunities for social interaction, and there may be a cascading effect of RRB on development. That is, the social environment of children with ASD who exhibit high rates of RRB is impacted, resulting in observed effects on developmental outcomes and autism symptoms. The ability to detect RRB in both home and clinic contexts provides additional diagnostic information that may improve early detection of ASD.
Footnotes
Acknowledgements
The authors would like to thank the families who gave their time to participate in this project, the FIRST WORDS® Project staff for their assistance in screening and evaluation, and Victoria Cox and Justin Bragg for their assistance with data coding.
Declaration of conflicting interests
Amy M Wetherby is coauthor of and receives royalties for the CSBS. Sheri Stronach has no conflict of interest to declare.
Funding
This research was supported in part by the Eunice Kennedy Shriver National Institute of Child Health and Human Development grant R01HD065272, the National Institute on Deafness and Other Communication Disorders grant R01DC007462, and the Centers for Disease Control and Prevention Cooperative Agreement U01DD000304 awarded to Amy M. Wetherby. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NICHD, NIDCD, the NIH, or the CDC.
