INTRODUCTION
Autism spectrum disorder (ASD) is a neurodevelopmental disorder that is characterized by limitations in social interactions and communication, restricted interest, and stereotyped or repetitive behaviors.1 The term autism spectrum disorder is often used to describe individuals who have been diagnosed with autism disorder (AD), pervasive development disorder not otherwise specified (PDD-NOS), or Asperger syndrome (AS) on the basis of medical and developmental history and clinical observations of behavior (see Table 1 for definitions).2,3 Recent research supported by the Centers for Disease Control and Prevention4 indicates that based on parent report, the incidence of autism is 110 per 10 000, with a higher incidence in males than in females.5
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TABLE 1: Definitions and Abbreviations of Developmental Disorders Identified in the Literature and Associated With Autism
The approach to evaluation and treatment of children with ASD is frequently a multidisciplinary team approach.6 Although the term clumsiness has been used in describing individuals with AS, limitations in motor activity are not considered to be core deficits of individuals with ASD.7,8 Historically, physical therapists have not been involved in the evaluation and treatment process of individuals with ASD; the role of the physical therapist is evolving with regard to both the evaluation and intervention processes. There is an increasing body of literature related to ASD, but evidence regarding physical therapy (PT) and intervention with this population continues to be limited in scope. To best understand PT intervention in children with autism, physical therapists need to assess the effect of motor activity limitations including motor anomalies, delays, or weaknesses on a child's ability to fully participate in daily activities and routines. These deficits in motor activity inform physical therapists' clinical decision making.
The purposes of this review were to summarize current evidence for limitations in motor activity in children with ASD and suggest further areas of research related to PT and autism while considering how PT may benefit children with autism. The term motor activity was selected by the authors in an attempt to capture and describe motor abnormalities, delays, and general motor function of children with ASD.
METHODS
A literature search was carried out using OVID, PubMed, and Google Scholar search engines between January 1, 2009, and October 31, 2009. Seventeen search terms were used in an attempt to best capture the broad range of articles addressing children with autism or related diagnoses, motor activity, and PT (see Figure for search terms). Care was given to be certain that each search yielded all possible evidence in the published literature. The search was then updated during May 2010 using the same strategies with each of the 17 search terms. In all, 90 searches were completed (Figure). Further review of an article was dependent on the appearance of the search terms in the abstract of the article as identified by the first author (Figure). Articles were then graded according to the level of evidence, on the basis of criteria from Sackett et al.9,10 Only articles that were found to be at Sackett levels 1–3B were used for this analysis. Other exclusion criteria included systematic reviews that did not include specific research methods, articles in which the search terms were present in the abstract but did not include analysis of motor function, and articles that were not accessible in English (see Figure).
Fig: Search strategy.
RESULTS
The search strategy and inclusion criteria resulted in a total of 49 articles that were acceptable for this literature review of motor activity in children with ASD. No level 1 articles appropriate for analysis were identified during the search. Two level 2 articles and 47 level 3 articles were identified and included in the analysis. Articles classified as levels 4 and 5 were identified but not used in the literature review. Articles that originally met the inclusion criteria but did not address motor activities as part of study criteria or outcomes also were not included. Review articles that did not include specific methods and inclusion criteria also were excluded from the analysis (see Figure). As is the case with all searches of the literature, additional articles that would meet the search criteria may be found if a new search following the same strategy was conducted today. The search strategy used here yielded all articles meeting inclusion criteria as of May 2010.
Studies that inform health care providers about children with ASD and addressed motor activity were analyzed and reviewed (see Appendix). During the review process, various themes related to the characteristics and concerns related to ASD arose in the literature. The articles were grouped and analyzed on the basis of these themes. The themes were not derived through a specific qualitative methodological approach; rather, they were generated through the work of the first author, and corroborated with the second author, during the process of sorting articles that met the search criteria. Based on recurring similarities in the content of the available literature as reviewed, the following thematic categories emerged: early motor findings, gestures and motor imitation, postural control, and dyspraxia.
Early Motor Findings
Several recent studies sought evidence of motor impairments to provide early motor identification markers and characteristics of ASD. For example, in a study by Provost et al,11 68% of children with ASD who were tested on the Bayley Scales of Infant Development II Motor Scale and 63% of children who were tested on the Peabody Developmental Motor Scales, Second Edition, would have qualified for early intervention services. Landa and Garrett-Mayer12 also prospectively studied 2 groups of infants: 1 group was classified as low-risk for development of autism and the other as high-risk for development of autism. Children were examined with the Mullen Scales of Early Learning at 6, 14, and 24 months. At the 24-month visit, further testing was administered to classify children who had typical development, ASD, or language delay. No differences on the Mullen Scales of Early Learning were found in children with ASD and typical children at 6 months; however, by 14 months, the children with ASD began to demonstrate a slowing in development compared with the other groups. By 24 months, significant differences were found between the group with ASD and the group developing typically in all domains, as well as between the group with ASD and the group with language delay. The children with ASD demonstrated the slowest rate of increase in developmental skills over time.
In another study, Esposito et al13 retrospectively examined videotapes of 3 groups of infants aged 12 to 21 weeks: those diagnosed with ASD, those with developmental delays not associated with ASD, and children with typical development. These researchers found that the group with ASD had significantly less static and dynamic symmetry in the supine position than the other groups. Teitelbaum et al14 also suggested that motor abnormalities, including asymmetrical movement patterns, are present at birth in children with ASD and may aid in the early identification of ASD. On the basis of video analysis, Baraneck15 suggested that symptoms of autism, including sensory-motor symptoms, might be present and identifiable between 9 and 12 months of age. In another study, Dewrang and Sandberg16 used retrospective parent reports to compare individuals with AS with a group of young adults who were developing typically. They found that during the first 2 years of life, individuals with AS demonstrated impaired imitation, increased clumsiness, and poor coordination. These findings suggest that evaluation of motor activity may play a role in early prediction of ASD.
In contrast, Ozonoff et al17 reported that infants who are later diagnosed with ASD do not demonstrate an increased number of movement abnormalities or a lack of protective reactions when compared with a group of children who are developing typically. They did, however, find a slower rate of development in reaching mature motor patterns. In addition, they suggested that more comprehensive motor evaluations might be useful in early detection of autism. In another study by Loh et al,18 stereotyped behaviors and postures found in children with ASD were similar to those in the comparison group. These authors also suggested that more sensitive testing might be required to identify motor impairments.
Gestures and Motor Imitation
The ability to use gestures and motor imitation relies on motor activity to communicate with others. Interestingly, children with ASD have difficulty with communication as well as difficulty using motor activity (eg, gestures and imitation) as forms of communication to support social interaction. Motor imitation has been identified as a significant impairment in previous literature on individuals with ASD, particularly in relation to social communication.19–21 In a literature review by Williams et al,22 the authors suggested that imitation impairments are present in children with ASD and are more apparent in younger age groups (below the age of 4 years) when compared with other children.
Stone et al21 suggested that imitation impairments in children with ASD are due to a delay in acquiring imitation skills, rather than disordered sequencing. Although some improvement may be seen between the ages of 2 and 3 years, this delay was apparent in young children, as well as in preschool-aged children.22,23 In another study, Rogers et al20 found that children with ASD have impaired imitation skills on sequential imitation tasks when compared with a group of children with developmental delays. No support was found for a relationship between imitation impairment and play skills, language skills, or dyspraxia in children with ASD. In a more recent study, Rogers et al24 noted that during a simple task, children with autism fail more imitation tasks than a group of children with developmental delays and a group of children who were developing typically. These findings were especially meaningful in children with autism who were younger than 14 months. In the older age group (older than 30 months), children with regressive type autism continued to fail more tasks, especially nonfunctional imitation tasks.
Other researchers have suggested a possible link between imitation impairments and the presence of motor activity abnormalities. For example, Van Vuchelen et al25 reported the presence of an imitation impairment, especially in nonmeaningful gestures, in children with ASD who have low-functioning autism and high-functioning autism (HFA). They also found increased impairment on motor testing. Green et al26 also found an association between motor and imitation scores, with lower and more variable scores in children with AS than in children with specific developmental delays of motor function. Spatiotemporal errors were more common in the group with AS. In a study by Mostofsky et al,27 children with ASD had more imitation errors on the Florida Apraxia Screening Test than children who were developing typically. Spatial errors were the most common in both groups. In the groups with ASD, errors were increased when gesturing on command and imitation, rather than tool use. Notably, no significant difference was found in the number of total errors between individuals diagnosed with HFA and those with AS.
In another study, Smith and Bryson28 found that children with ASD have increased difficulty performing and naming both meaningful and nonmeaningful gestures but no difficulty understanding or identifying gestures. The authors suggested that these impairments might be related to dyspraxia.28 Dewey et al29 also found that when compared with children with both developmental coordination disorder (DCD) and attention-deficit/hyperactive disorder (ADHD), DCD only, or ADHD only, children with ASD have significantly lower motor and gestural performance scores. Although this may be related to praxis, these authors suggested that it might also be related to altered neural substrates or language deficits.
More recently, Ben-Sasson et al30 examined gestural representations in 3 groups of children: children with HFA, children with language impairment, and children who are developing typically. The authors concluded that children with HFA have increased difficulty with gestural representations, which they suggest may be related to a motor planning deficit. There appeared to be decreased quality of gesture performance as well as a discrepancy between gestures and verbal descriptions, when compared with the other 2 groups. The authors hypothesized that performing motor actions might be more difficult when the task is combined with verbal description. This may be related to a lack of integration between motor and language. Ben-Sasson et al30 suggest that individuals with ASD may benefit from further testing to examine motor planning and sequencing.
Postural Control
Postural control requires a level of stability necessary prior to executing additional motor skills or activities. Without this control, motor activity may be limited to more static positions. Individuals with autism tend to have decreased postural control.31,32 Minshew et al31 found that individuals with autism have decreased postural stability, particularly in circumstances where there is sensory conflict. Compared to a group of children who were developing typically and adults, development of postural stability appeared to be delayed in children with autism. Postural stability did not appear to improve in individuals with autism until the age of 12 years. At the age of 15 years, the group that was developing typically appeared to have a plateau in postural stability; however, this same level of control was not achieved in the group with ASD. Based on the data from a bimanual lift task by Schmitz et al,32 children with ASD rely on reactive postural control rather than on the typical anticipatory postural control seen in the comparison group when performing lifting tasks.
In another study, Kohen-Raz et al33 examined postural stability in various standing positions between a group of children with ASD and a group of children who were developing typically. Children with ASD demonstrated increased sway, abnormal weight distribution, and the absence of typical ankle strategies in standing. A “paradoxical stress response” was noted in individuals with autism, indicated by an increase in postural stability in stressful conditions (defined as removal of vision). In a follow-up study, Molloy et al34 also found that children with ASD had significantly more sway in standing than a comparison group of children who are developing typically. Instead of a “paradoxical stress response,” they found that children with ASD experienced a larger increase in sway when visual input was removed and somatosensory input modified, indicating that children with ASD rely on visual input for balance. This finding points to impaired processing abilities with sensory conflict in individuals with ASD. Molloy et al34 argued that the presence of a paradoxical response found in the Kohen-Raz et al33 study might have been the result of additional visual and auditory input used in their methods. Further support for impaired postural control in children with ASD was provided by Fournier et al,35 who reported that children with ASD have increased postural sway in quiet stance without manipulation of sensory input as well as altered center of pressure shifts during gait initiation.
Dyspraxia
Quality of movement may be altered in children with ASD, and dyspraxia has been noted when comparing children with ASD with children who are developing typically. Motor delay and motor variability have also been noted and described in some studies and refuted in others. Although motor abnormalities were noted in individuals who were first described with AS,8 these limitations have not been consistently identified in individuals with ASD. While no level 1 research supporting the presence of limitations in motor activities was found, several lower-level studies indicate that impairments in motor activity may be common in children with ASD. Researchers have sought to distinguish differences across individuals with ASD, as well as to compare those with ASD with individuals who are developing typically or have other developmental concerns.
Manjiviona and Prior36 found limits in motor activity and function in children with HFA and AS. Ghaziuddin and Butler37 noted that children with autism, AS, and PDD-NOS have motor impairments. Statistically significant differences were found only between those with AS and those with AD (children with AD were noted to be more clumsy) as measured by the Bruinink-Oseretsky Test of Motor Proficiency. Individuals diagnosed with AD had higher levels of motor activity impairment, while those with AS demonstrated less impairment on gross motor, fine motor, and total battery scores. A strong correlation existed between intelligence quotient (IQ) scores and test results. When adjusted for level of intelligence, no significant difference remained between groups. Green et al38 found a similar correlation between IQ and motor scores in individuals with ASD, indicating that motor impairments might be related to IQ level. Current research has demonstrated that there is no significant difference in level of motor impairments among children with AS, AD, or PDD-NOS; however, there is a trend toward higher cognitive limitations correlated to lower motor scores.
Several researchers have suggested that when compared with a comparison group developing typically, children with ASD have dyspraxia. Mostofsky et al27 suggested that based on the Florida Apraxia Screening test, motor imitation may be linked to dyspraxia, particularly to a delay in spatial mapping. Dzuik et al39 proposed that dyspraxia may be separate from other motor skills in children with ASD and may be strongly correlated to the core deficits associated with autism.1 According to Dowell et al,40 praxis score was correlated with the Autism Diagnostic Observation Schedule score, also suggesting that dyspraxia may be a core symptom of ASD. In addition, Dowell et al40 reported that children with ASD have slower timed movements and score significantly lower on postural knowledge testing.
Glazebrook et al41 noted that individuals with ASD are able to use advance information; however, more time is required to plan movements. Glazebrook et al42 and Nazzarali et al43 noted that individuals with ASD required more time to plan and execute goal-directed movements. Rinehart et al44 also noted a slower preparation time in children with HFA and AS when compared with a cohort developing typically. This was further supported in another study by Rinehart et al,45 where children with HFA demonstrated increased preparation time compared with a cohort developing typically, and children with AS demonstrated a trend toward a motor preparation deficit. On the basis of an analysis of goal-directed gait, Vernazza-Martin et al46 suggested that when compared with a typical comparison group, children with ASD have impaired motor planning and execution. Whereas differences in motor planning are present in some individuals with ASD, the alterations in patterns are unclear. Hughes47 suggested that individuals with autism demonstrate difficulty executing simple goal-directed motor tasks that might be related to sequencing, vision, or consequence prediction.
Staples and Reid48 compared a group of children diagnosed with ASD to 3 groups developing typically. The 3 typical groups were matched with children in the group with ASD by chronological age, cognitive development, or movement skill development. They found that children with ASD have significantly poorer motor scores than children who are developing typically and who are chronologically age matched and cognitively age matched. Specifically, children with ASD had difficulty with bilateral coordination and performed at a similar motor level as children approximately of half their chronological age. The authors suggested that by late childhood, motor skills in children with ASD are significantly delayed.
Jansiewicz et al49 noted that boys with HFA and AS have increased difficulty with balance, gait, and dysrhythmia with timed hand and foot movements. In another study, Weimer et al50 examined tests of apraxia and basic motor function in a group of children and young adults with AS and a comparison group. The authors found that deficits were present on tests of apraxia, especially on measures where visual input was removed, suggesting reliance on vision with a proprioceptive impairment. In addition, Freitag et al51 reported that when compared with a group developing typically, individuals with HFA and AS are “strongly impaired” in dynamic balance and diadochokinesis, and integration between sensory and motor input may be also impaired. They also noted a positive association of motor scores to the level of social withdrawal.
In a study by Fuentes et al,52 the authors found that when compared with a group of children who were developing typically, children with ASD had significantly poorer motor and writing scores overall. More specifically, scores were decreased on gait, stance, and timed movement activities. Poor gross motor skills were correlated with poor handwriting scores. They hypothesized that if therapies address overall motor control, handwriting scores would improve as a result of increased ability to control and manipulate arm movements. In contrast, van Swieten et al53 sought to differentiate between motor and executive planning abilities in 3 groups of children and adults: a group with ASD, a group with DCD, and a group with typical development. Based on what the authors suggested to be a pure motor planning test, no difference was found between the group with typical development and the group with ASD.
Miyahara et al54 found high rates of motor delay in 2 groups of children: a group of children with AS and a group of children with a learning disability. A significant difference was found between groups for manual dexterity scores. The children with AS had a trend toward poorer ball skills, which, the authors hypothesized, might be related to the type of preferred play.
No difference in motor profile was found between children with ASD who were chronologically age matched and children with other developmental delays.55 The authors did, however, note that scores of children with ASD were more variable than those with developmental delays. In another study by Provost et al,11 the authors evaluated 3 groups of children—children with ASD, developmental delays, and developmental concerns—on the basis of results from the Bayley Scales of Infant Development. In this study, none of the children in the group with ASD tested within normal limits, and at least 68% of these children would have qualified for early intervention services based on a delay of 25% or more. Motor scores of children with ASD did not differ when compared with children with developmental delay. These results suggest that there is a limitation in motor function in children with ASD. Further research is needed to identify the specific type of dysfunction.
Matson et al56 also noted gross and fine motor impairments in toddlers with AD when compared with toddlers with atypical development between 18 and 36 months of age. No significant differences were found between toddlers with PDD-NOS and children who are developing typically. The authors suggested that motor impairments are present at a young age and benefit may be obtained from early intervention. In another study, children with ASD were compared with children with specific speech and language disorders and a comparison group of children who were developing typically. The children with speech disorders had lower scores on all gross and fine motor domains except coordination, whereas children with autism had significantly poorer scores on all fine and gross motor scores (including balance), except oral motor and coordination.57 Morin and Reid58 noted that although individuals with autism have poor motor performance, they can obtain higher balance scores than those with intellectual delay. Balance in individuals with ASD may be decreased; however, continued research is necessary to identify the severity and the pattern of deficit.
Although impaired motor skills and function are not a core deficit of ASD, they are considered a core deficit of DCD and ADHD.1 In a study by Dewey et al,29 the authors found that when tested on the Bruinink-Oseretsky Test of Motor Proficiency (short form) and a gestural performance test, children with ASD had significantly lower scores than children with DCD, ADHD, or ADHD and DCD. This supports the presence of difficulty with motor activity in children with ASD. This finding was further supported by Pan et al,59 who found that children with ASD performed significantly lower on motor tests than children with ADHD and children who are developing typically. Specific limitations were noted on tests of locomotion and object manipulation. They suggested that poor motor performance might be a sign of autism, with poor skills being related to a lack of social skills as well as lack of motivation to practice. The authors encouraged clinicians to screen for motor impairments as poor motor skills were found to be correlated with poor self-esteem, increased anxiety, and decreased social function.
In a rare study with an all-female sample, Kopp et al60 compared several groups of girls: girls who were developing typically, girls with ASD, and girls with ADHD. They found that a large percentage of girls with ASD also fit the diagnosis for DCD, especially those in the preschool-aged group. Predictors of poor motor scores included younger age, presence and severity of ASD symptoms, and low IQ. Poor motor scores were related to poor activities of daily living and physical education participation.
DISCUSSION
Based on this review of literature, evidence is emerging that supports the identification of impaired motor activity in children who have the diagnosis of autism. Although impaired motor activity is not included in the diagnosis, impaired motor activity appears to be an observable trend. The ability to understand and address the entire clinical picture of the child, including all areas of function, becomes an essential component of any intervention plan. The majority of current evidence does support the presence of motor activity abnormalities prior to 2 years of age in children who are later diagnosed with ASD that persists into early childhood. As children are being diagnosed earlier with ASD and receiving early intervention services, physical therapists should consistently be part of the team addressing all the needs of the child.
Although we still have much to learn about the timing of motor development and the patterns of motor activity in children with ASD, evidence supports the presence of specific difficulties related to motor activity in individuals with ASD. The link between imitation and motor activity is still unclear; however, research indicates that there are limitations in motor imitation in children with ASD. Questions still remain as to whether restrictions in social behavior limit imitation, or whether limitations in motor activity restrict social participation and adversely affect imitation. The presence of postural instability is also supported in the literature. Decreased postural stability can significantly limit participation in activities since the simplest of movements require complex control61,62 and further research is needed to examine the severity, cause, and functional outcomes related to postural control. The literature also lends support to difficulty with motor planning in children with ASD.
Limitations in motor activity in children with ASD might decrease the opportunity for social interactions and learning opportunities. Although limited research related to interventions for motor activity impairments in children with ASD was found, Travers et al63 did address motor-linked implicit learning in children with ASD. In a study comparing a group of individuals with HFA, ASD, and a group developing typically, Travers et al63 reported that for simple tasks, motor-linked implicit learning might be intact in children with ASD, which might influence therapeutic approach.
Motor activity delays have been observed in infants and toddlers with autism and may affect future motor development. As with all developmental delays, early identification leading to the initiation of early service delivery might have a positive benefit on motor skills and long-term disability in individuals diagnosed with ASD.64,65 Since children with ASD are ambulatory, they previously would not have been thought to benefit from PT. Physical therapists need to consider how to address these impairments in motor activity within the child's daily routines.
Although the results of this literature review do indicate that motor activity impairments may be present in children with ASD, there are limitations to this analysis. An updated literature search may provide increased evidence supporting motor activity impairments as well as provide documentation for intervention strategies for children with ASD. No consistent measure was used in each of the reviewed studies, which limits generalization of the findings.
CONCLUSION
Although there may be limitations in motor activity present in children with ASD, much research is still needed to identify the age at which these limitations in motor activity are present and to what extent they differ from children who are developing typically. As with many other diagnoses, lack of evidence has not prohibited the PT profession from forging ahead with new research and ongoing intervention. Future research is necessary to identify to what extent functional activities are limited in children with ASD. Research is also necessary to determine the underlying causes as well as the most appropriate interventions. As physical therapists move toward consistent use of the ICF,66 it may be useful to implement interventions and research their efficacy based on activity limitation and participation restrictions rather than solely by impairment and disability. Physical therapists can and should play a unique role in promoting functionally based intervention strategies to enhance motor activity and improve function in children with ASD.
ACKNOWLEDGMENT
The authors thank Stephanie Lyle, PT, DPT, for her early contributions to this work.
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APPENDIX
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
Brief Summary of Each Article Revieweda
