Autism spectrum disorders (ASDs) are a set of complex neurological conditions of increasing prevalence and community concern. Recent estimates in the United States indicate that 1 in 91 children are affected.1 Core deficits of ASDs limit functioning in social interaction, communication, and daily activity participation.2 Individuals with ASDs typically require significant levels of supervised care, special education resources, and health service.3 Deficits in the motor performance of children with ASDs, although not part of the primary diagnostic criteria, are thought to contribute to the clinical presentation and functional difficulties experienced by these children.4–6 The prevalence of motor deficits in individuals with ASDs varies from 50% to 100%.6–8 Understanding the nature of motor performance differences in young children with an ASD may provide insights into the emergence of the adaptive behavior difficulties associated with these disorders.
Both fine and gross motor performance difficulties have been observed in children with ASDs.4,9–11 Previous researchers have reported motor delays in school-aged children with ASD in manual dexterity, ball skills, balance, and graphomotor skills.4,6,12 In addition, specific deficits affecting motor performance include imitation skills, motor coordination, and postural control.10,13–18 Furthermore, qualitative motor performance differences have been observed in locomotion and motor planning.4,16,19–22 Finally, atypical movements, including repetitive body movements, stereotypical movements, and self-injurious behavior, commonly occur in individuals with ASDs.23–25 Some authors have suggested that motor abnormalities in ASDs may be observable during the first 2 to 3 years of life, but the findings are inconsistent. Recently, a retrospective movement analysis study of the lying patterns of infants aged 0 to 5 months (taken from home videos) revealed significant differences between infants who were later diagnosed with an ASD as compared with those with developmental delay (DD) or typical development.5 Specifically, infants later diagnosed with an ASD were more likely to display lower levels of symmetry in lying.5 Teitelbaum et al completed a retrospective analysis of movement patterns (lying, righting, sitting, crawling, standing, and walking) using a movement analysis system along with still-frame videos of 17 children with ASD compared with 15 controls who were developing typically. They found that movement disturbances were clearly detectable between the ages of 4 and 6 months in children with ASDs, although the type of movement disturbance varied among infants.26 Matson et al found that toddlers (aged 17 to 36 months) with autistic disorder exhibited greater motor skill deficits as compared with toddlers with pervasive developmental disorder not otherwise specified (PDD-NOS) and toddlers who were atypically developing but not on the autism spectrum.27 Finally, Baranek's retrospective video review of infants between 9 and 12 months of age found that infants later diagnosed with an ASD mouthed objects more frequently than infants who were developmentally delayed and infants who were developing typically.28 These authors agree that motor performance in very young children may be useful as an indicator of a possible ASD phenotype.9,26,29,30 In contrast, Ozonoff et al attempted to replicate the above mentioned Teitelbaum et al study, finding no elevated rates of movement abnormalities in infants who were later diagnosed with an ASD. In fact, the movement patterns of the group with ASDs were very similar to the group with typical development. However, their findings did indicate an overall slowed rate of motor development for infants with regressive ASD, nonregressive ASD, and DD as compared with infants developing typically.31 In addition, prospective studies examining motor development at different time periods (6 and 12 months) through standardized assessments did not identify motor differences in individuals with ASDs.32,33
Despite the lack of agreement in the literature regarding the clinical identification of motor differences in children with ASDs, several researchers report abnormalities in brain regions involved in motor function. Specifically, the cerebellum and subcortical white matter of individuals with ASDs have consistently been identified with differences when compared to the typically developing brain.34,35 Debate can be found in the literature as to whether individuals with ASDs experience dysfunction in the mirror neuron system. Mirror neurons are thought to be primarily involved in perception and comprehension of motor activity and have also been linked to higher order cognitive processes such as imitation, language, theory of mind, and empathy.35–38 Mirror neuron activity can be measured utilizing electroencephalographic oscillations of the sensorimotor cortex in the μ frequency (8–13 Hz). Researchers often compare participant's level of μ suppression under 2 conditions: (1) observing a motor task and (2) completing of a motor task. Research has shown that individuals who are developing typically tend to display μ suppression while performing and observing motor tasks, which has been linked to the ability to understand and imitate others.39 Oberman et al measured μ suppression in the sensorimotor cortex under several conditions in individuals with high functioning autism (HFA) and controls who were developing typically. They found that the group with HFA showed significant μ suppression to self-performed hand movements but not to observed hand movements as compared with the group developing typically. These findings support the hypothesis of a dysfunctional mirror neuron system in individuals with HFA.39 These findings, however, have been disputed by Fan et al, who conducted a very similar task, finding both groups (those with ASDs and those developing typically) exhibited stronger μ suppression when watching hand movements as compared to a moving dot.40 In addition, although the group with ASDs showed μ suppression while watching hand movements, they were unable to imitate those movements. This information disputes the broken mirror neuron theory of ASD. In addition, the group with ASDs showed a positive association between amount of μ suppression while watching a motor task and communication abilities, suggesting that μ suppression could be an indicator of symptom severity in ASD.40
Other studies have explored the relationship of motor characteristics in ASD and functional limitations. In one study, gross and fine motor development were assessed in preschool children with ASDs and correlated with scores in adaptive behavior. Significant positive associations were found between delays in fine-motor (r = 0.397, P = .018) and visual-motor performance (r = 0.444, P = .008) and independence in daily living skills such as dressing, grooming, and bathing assessed using the Functional Independence Measure (Wee FIM) for children.41 This association held even after controlling for cognitive level. In another study, oral-motor and manual-motor skills in toddlers (aged 3 to 4 years) with ASDs were found to be predictive of speech fluency.42 Furthermore, both oral- and manual-motor performance could be used to distinguish infants and toddlers with ASDs from those who were developing typically.42 In addition, a study examining the relationship between basic motor skill and dyspraxia in high-functioning children (aged 8 to 14 years) found that praxis performance was a significant predictor of total score on the Autism Diagnosis Observation Schedules-Generic (R2 = 0.237, P = .002),20 which suggests that impaired performance of skilled gestures (including social gestures) is associated with social, communicative, and repetitive behavioral impairments found in individuals with ASDs.20
Motor abnormalities in children with ASDs are documented in the literature. However, the pattern of emergence of these difficulties and their relationship to functional performance are yet to be defined. Further examination of this issue is warranted. Therefore, this study sought to further the characterization of the motor performance of young children with ASDs by describing patterns of motor performance of young children referred to a neurodevelopmental clinic for possible diagnosis of an ASD. The primary aims of this study were to (1) characterize the motor performance of young children (aged 19–41 months) referred to a neurodevelopmental clinic for possible diagnosis of an ASD, (2) compare the motor performance of young children who received a diagnosis of an ASD with those who did not, and (3) describe associations between motor performance and functional limitations in young children diagnosed with an ASD.
The Institutional Review Board at The Ohio State University approved this study.
Participants were drawn from all children evaluated for a possible ASD at a neurodevelopmental clinic at the Nisonger Center for Excellence in Developmental Disabilities program between June 1, 2007, and May 30, 2009. Seventy-six charts were initially reviewed, and participants were included in the study if complete evaluations of motor function using the Bayley Scales of Infant and Toddler Development, Third Edition (BSID-III) were available from their clinic chart and if the children were younger than 43 months. Thirty children (23 male, 7 female; mean age = 31.57 ± 6 months, range = 19–41 months) met this criteria (see Figure). These 30 children were then diagnosed with an ASD (n = 22; 73.3%; autism = 20, HFA = 1, PDD-NOS = 1), given a non-ASD diagnosis (n = 7; 23.3%), or assessed as developing typically (n = 1; 0.03%). Non-ASD diagnoses included global DD (n = 3), developmental language delay (n = 1), hypotonia (n = 1), apraxia of speech (n = 1), and history of hearing loss (n = 1). Children are referred to this clinic from both urban and rural areas surrounding Columbus, Ohio, and represent a range of socioeconomic circumstances. Most children seen at the clinic are Caucasian.
Children referred to the neurodevelopmental clinic during the time of the study underwent an arena-style multidisciplinary evaluation including physical and occupational therapy, speech language pathology, developmental pediatrics, and nutrition. Diagnosis of an ASD was made using Diagnostic and Statistical Manual of Mental Disorders (Fourth Edition) criteria and clinical impression by the developmental pediatrician after interviewing the family, observation of the child, and consultation with the interdisciplinary team.
The BSID-III was administered routinely as part of this evaluation by 2 to 3 members of the team (typically physical, occupational, and speech therapists). Scoring and interpretation of the individual domains of the BSID-III were completed by each discipline according to their expertise. Generally, an occupational therapy team member was responsible for scoring and interpreting the fine motor domain, a physical therapy team member was responsible for scoring and interpreting the gross motor domain, and a speech pathology team member was responsible for scoring and interpreting the language and cognitive domains. The BSID-III adaptive behavior and social-emotional questionnaires were completed by parents under the direction of a member of the interdisciplinary team during the clinic appointment. The clinic is staffed by experienced clinical and administrative faculty and graduate level trainees from the therapy, medical, and psychology disciplines.
The BSID-III record forms are completed by team members at the time of the evaluation and filed in each child's individual clinic chart by the clinic coordinator. A retrospective chart review of medical records for 76 children evaluated for possible ASD diagnosis was performed. Two members of the research team (the first author and a student assistant) reviewed the medical charts of all eligible children. Thirty children met the inclusion criteria, having complete fine and gross motor domains from the BSID-III. The following data were obtained from each file: date of birth, date of evaluation, age at evaluation, diagnosis given at the end of the clinic evaluation, and BSID-III raw, scaled, growth equivalent, developmental age (DA), and composite scores. For the fine and gross motor domains of the BSID-III, item scores were also obtained for each participant where available.
The BSID-III43 is designed to assesses overall development in the motor (gross and fine), language (receptive and expressive), cognition, adaptive behavior, and social-emotional domains. Administration is generally completed in 40 to 50 minutes. The BSID-III is the preferred tool by many clinicians for evaluation of general development in young children aged 1 to 42 months.44,45 Scores are compared with a large normative dataset to derive scaled scores, composite scores, DA, and percentiles.
Composite scores are standard scores that can be derived for the cognitive, language, and motor scales with a mean of 100 and standard deviation of 15. Scaled scores can be obtained for the gross and fine motor, receptive and expressive language, and cognitive subtests and have a mean of 10 and a standard deviation of 3. The BSID-III was standardized on 1700 children across 17 age groups (1 to 42 months of age) with 100 children in each age group. This sample is reported to be representative of the 2000 US Bureau of Census population survey data in reference to parent education, ethnicity, and geographic region. Initially, the sample only included children who were developing typically, but later children with behavioral, cognitive, and physical issues were added to account for 10% of the sample.43 Reliability and validity is established for the BSID-III. Numerous studies demonstrate high to moderate scores on both reliability and validity of this assessment.46 In addition, the BSID-III has concurrent validity with a variety of other pediatric assessment tools in addition to high intra- and interrater reliability. The BSID-III cognitive scale was significantly positively correlated with the Vineland II among a group 125 toddlers with ASDs. In addition, in that same study, the BSID-III cognitive scale was negatively correlated with Autism Diagnostic Observation Schedule (ADOS) scores.47 The BSID-III effectively discriminates between children with DD and children who are developing typically. The BSID-III is a potentially useful tool for measuring motor characteristics in young children with the possible diagnosis of an ASD.
Descriptive analyses were conducted initially to determine the motor performance, adaptive behavior, social and communication skills, and cognitive level of participants. Comparative analyses (including paired sample t tests) were then used to distinguish differences in motor performance between children based on diagnosis and cognitive/language level. A Pearson product-moment correlation analysis was applied to determine associations between motor function and adaptive behavior in participants diagnosed with an ASD. SPSS version 17.0 was used for statistical analyses.48
Motor Characteristics of the Referred Sample
Developmental characteristics of the participants included in this study are presented in Table 1. Participants diagnosed with an ASD tended to experience more significant delay in the cognitive (t = −2.84, df = 27, P = .008) and language developmental domains (receptive: t = −2.03, df = 26, P = .05; expressive: t = −1.91, df = 26, P = .07) than did those who did not receive an ASD diagnosis. No significant differences were noted between the participants diagnosed with an ASD and those who were not diagnosed with an ASD on the other developmental characteristics assessed.
Motor DA and difference scores (chronological age – developmental age) were calculated for fine and gross motor domains. On average, the fine motor DA for the referred sample was 23.4 months, with a range of 11 to 42 months. The average fine motor difference score was 8.17 months. This difference was higher for participants with an ASD (ASD = 8.59 months, non-ASD = 7.00 months) but did not reach significance levels (P = .57).
Similarly, gross motor DA for the referred sample was delayed when compared to chronological age (mean gross motor DA = 25.50 months, range = 16–42 months). The average gross motor difference score was 6.06 months. Mean differences were higher in the participants with an ASD (ASD = 6.36 months, non-ASD = 5.25 months) but did not reach significance levels (P = .70).
Overall, children referred to a neurodevelopmental clinic for possible diagnosis of an ASD experienced moderate-level fine and gross motor delays ranging 6 to 8 months. In addition, scaled scores were 1.5 points lower for fine motor skills compared with gross motor skills. Young children who went on to meet criteria for a diagnosis of an ASD tended to have greater delays in both the fine and gross motor domains, although these were not found to be statistically different from the children with a non-ASD diagnosis.
Given the trend in the previous analysis for participants with ASDs to experience greater fine and gross motor delays, further comparative analyses were used to examine possible qualitative differences in motor function in children with and without ASDs in our sample. Item data from the fine and gross motor subtests of the BSID-III were obtained and compared between groups using a paired sample design. Participants who did not meet criteria for an ASD diagnosis were each paired with a participant who was diagnosed with an ASD. Initially matches were made on the basis of gender and cognitive age. When a close match could not be found based on these criteria, language composite score was used to determine the final match. Using these criteria, 6 close matches were possible. Table 2 displays the gender, age, cognitive, and language characteristics of each pair.
A 2-step item analysis was conducted on a subsample of 6 matched pairs (n = 12). First, pass rates (percentages) were calculated for the participants with and without ASD for each item in the gross motor and fine motor domains. Items on the BSID-III are scored pass (1) or fail (0), according to established criteria reported in the administration manual. In the gross motor section, a difference in pass rate was found for more than 1 child (30%) on the following items: jumps from bottom step, kicks ball, walks forward on a path, walks up stairs alone with both feet on each step/alternating feet, jumps forward, walks backward close to path, stops from a full run, and walks on tip toes. In the fine motor section, a difference in pass rate was found for more than 1 child (30%) on the following items: places 10 pellets in 20 seconds, takes connecting blocks apart, imitates horizontal stroke, stacks 6 blocks, builds train, wall, bridge with block, strings blocks, tactile discrimination of shapes, and cuts paper. Second, groups of items that appeared to be passed at different rates between groups were identified through visual inspection of the data. These groups of items were then submitted to paired sample t test or chi square analysis to ascertain significant differences between diagnostic groups. There were no differences between groups with ASD and groups without ASD.
Association of Motor Performance With Functional Limitations in ASD
Fine and gross motor DAs and difference scores from children in our sample diagnosed with ASD (n = 22) were subjected to Pearson product-moment correlation analysis with adaptive behavior (Generalized Adaptive Composite) and social-emotional (composite) scores (Table 3). Not all participants with ASD had completed adaptive behavior and social-emotional questionnaires. The following analyses were conducted on samples of n = 14 (adaptive behavior) and n = 13 (social-emotional). Correlation coefficients (r), significance values (P), and the coefficients of determination (R2) are reported. Gliner et al suggest that Pearson r values of ± 0.5 indicate strong associations, values of ± 0.3 indicate medium strength associations, and values of ± 0.1 indicate weak associations.49 Several moderate-level, although not statistically significant, associations are apparent between motor performance and adaptive and social-emotional function in this sample. It is likely that our sample size was insufficient to detect statistically significant associations between these variables. Our result, however, does reveal trends in association of clinical significance. Gross motor DA explains 17% of the variance in adaptive behavior (R2 = 0.17; r = 0.41, P = .14). Furthermore, the gross motor difference score explains 15% of the variance in social-emotional function (R2 = 0.15; r = −0.39, P = .19) and 20% of the variance in adaptive behavior (R2 = 0.20; r = −0.45, P = .11). This suggests that as the discrepancy between chronological age and gross motor DA widens, social-emotional function and adaptive behavior become more compromised. Fine motor DA was not observed to be strongly associated with adaptive behavior or social-emotional function. The fine motor difference score, however, explained 18% of the variance in social-emotional function (r2 = 0.18; r = −0.42, P = .16). As the discrepancy between chronological age and fine motor age widens, social-emotional function worsens. In a secondary finding, adaptive behavior was strongly associated with gender in our sample (r = 0.86, P = .01). Specifically, girls were rated as having greater skills in adaptive behavior than boys.
Overall, young children referred to an ASD clinic demonstrated poor fine and gross motor performance on the BSID-III. Our study has 3 main findings based on our objectives.
First, the motor performance of young children (19–41 months) referred to a neurodevelopment clinic for possible diagnosis of an ASD can be characterized as delayed. Specifically, the motor characteristics of the referred sample, comparison between groups with ASD and without ASD, and item analysis controlling for cognition resulted in similarly delayed motor performance on the BSID-III. These results could suggest that referring physicians may be using poor motor skills as a factor in referral to an ASD clinic. The argument is strengthened as many of the participants in our sample were preverbal and language and cognitive delay were likely not the primary or only concern in referral. These findings are consistent with previous work by Provost who reported delayed motor skills on the BSID-II and Peabody in children 21 to 41 months with an ASD diagnosis and those with a DD diagnosis.4 Together, these findings lend support to the idea that fine and gross motor delays in young children may be considered a characteristic of the early emergence of an ASD.
However, we were not able to distinguish differences in motor characteristics between children with ASDs and those with DD using the BSID-III. Our approach was similar to those that have used the BSID-II in young children with ASDs and developmental disability.4,9,50 Although differences between groups with ASD and without ASD did not reach statistical significance, pass rate variances appeared to be clustered around items requiring dynamic balance (eg, stair climbing, walks on tiptoes, and kicks ball) and visual-motor integration (eg, block building and form copying). Other studies that have used video-based movement analysis and specific motion capture tools, such as biomechanical analysis, have, however, identified specific motor characteristics of children and adults with ASDs including abnormal movement patterns during reaching and grasping29 and walking.16,51–53 It is likely that common clinical measures such as the BSID-III may need to be combined with more sensitive measures of motor coordination such as biomechanical measures to further discriminate between specific motor characteristics of ASDs and DD. Comprehensive evaluation of motor patterns using clinical and biomechanical tools in infants and toddlers may open a window into earlier diagnosis of this complex disorder, which is typically not diagnosed until 3 years of age.
Second, calculated DAs on the BSID-III for the group with ASD suggest that fine and gross motor delays are in the range of 6 to 8 months. In children under 40 months of age, we feel a skill delay of this range should be considered clinically significant and worthy of focused intervention. Clinical convention in the management of young children with ASDs, however, tends to minimize the importance of motor delays as they are often considered an area of relative strength. This may be related to the use of scaled scores rather than “months delay” as a basis for determining eligibility for services. In our study, median scaled scores in gross and fine motor skills for the group with ASD were 8 and 6, respectively. A scaled score of 8 on the BSID-III generally equates to performance at the low end of normal limits, which would not qualify the child for services in these areas. The use of standardized assessments to guide decisions regarding service eligibility has been a topic of previous discussion.54 Provost et al found in studying the concurrent validity of the BSID-II and Peabody-II in children with DDs, that there was poor agreement between the tools. These authors cautioned against the use of these tools alone for determining service eligibility. In addition, Anderson et al examined babies born extremely preterm and at term using the BSID-III and found that both groups had mean scores close to the normative mean. Furthermore, the proportion of children with DD was extremely underestimated, and children in the control group (with typical development) had mean scores that were higher than expected.55 On the basis of the results of our study, we would recommend that difference scores (chronological age – developmental age) and scaled scores on the BSID-III be used in addition to clinical impression to determine whether motor delays are clinically significant.
Third, active management of motor delays in young children with ASDs may be particularly important in light of our third finding that suggested that these delays are related to adaptive and social-emotional limitations. We found a trend for an association between gross motor skill and functional difficulties in children diagnosed with an ASD. The mechanism of this relationship was not revealed in our study, but a number of theories can be postulated on the basis of the literature. First, fine and gross motor deficits affect participation in social activities (playgroups, gym, playground interactions, etc).56 Not only does participation in these activities lead to higher quality of life and healthier lifestyles, but for children with ASDs, participation provides an important context for the ongoing development of social interaction skills, a core deficit of the disorder. It is possible that motor limitations further compound the social communication deficits experienced by children with an ASD by reducing opportunities to engage with peers who may serve as models. Second, the success of some of the interactions of young children with ASDs with their peers may have a relationship to how well they are able to perform fundamental motor and play skills. In this scenario, the unique motor difficulties experienced by young children with ASDs may disrupt the pattern, timing, and flexibility of their movement, thereby affecting both their responses to social situations and the manner in which their social communications are interpreted by others.20 Finally, delays in fine and gross motor skills in a young developing child are likely to directly impede acquisition of independence in motor-based self-care and other adaptive skills leading to reduced performance in these areas.
This study was subject to the limitations of designs using retrospective chart audits as the method of data collection. First, we had limited control of the consistency with which the BSID-III was administered to participants. Although the clinic from which the data were collected was staffed consistently during the data collection period with experienced clinical faculty, as a training clinic, students were often involved in the administration of the evaluations. This resulted in the possibility of variation in the administration of test tasks and errors in scoring. Second, we were only able to include 30 of a possible 76 participants based on age of the child and completion of BSID-III data. Smaller subsets of this sample were used in additional analyses to compare group differences and examine adaptive behavior and social-emotional function. Although these numbers are comparable with previous reports in the literature, it is likely that our study lacked sufficient power to allow detection of statistically significant differences and associations in the data. Our capacity to draw conclusions regarding associations between motor performance and functional abilities from this study, therefore, is limited. Group differences were not detected and none of the associations reported achieved statistical significance despite being of moderate strength. Furthermore, it is likely that our sample of children with ASDs was varied in terms of autism severity. Although the majority of the sample was diagnosed with autism, 1 participant was identified as “high functioning autism” and another with PDD-NOS. Motor features may vary between different subdiagnostic groups.
Despite these limitations, our study has provided the basis for further understanding of the motor difficulties experienced by children with ASDs and highlighted the need for ongoing examination of the emergence of these delays and their relationship to core deficits of the disorder. While our results did not achieve statistical significance, trends were revealed that might be meaningful in clinical decision making.
On the basis of our study and others, we have the following recommendations for future research examining the motor characteristics of individuals with ASDs. First, possible mechanisms for motor impairment in ASD should be investigated in larger samples of children with ASDs with the concurrent application of clinical, neurophysiologic, and biomechanical measures. Motor performance should be compared with controls who are developing typically and controls with DD without an ASD and by ASD diagnostic subcategory.
Characterization of the motor difficulties experienced in young children with ASDs should be continued in larger scale studies. These studies should explore possible qualitative differences in motor impairment between ASD and DD by using a cognitive age-matched design. Clinical measures such as the BSID-III should be used in combination with research measures that assess motor fluency, balance, and visual-motor coordination.
The emergence of motor difficulties in early childhood in infants at risk for ASDs should be examined in a prospective cohort study that tracks the development of motor skills from birth to the point of an ASD diagnosis. The motor delay during infancy of high-risk populations, such as siblings with autism, preterm birth, and/or neonatal seizures, should be examined to aid in earlier identification of ASDs and guide early intervention.
The authors acknowledge the contributions of Sara O'Rourke, Lindsay Daniels, and Susan White.
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autism spectrum disorder; child; developmental delay; infant; psychomotor skills