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Research in Autism Spectrum Disorders 2 (2008) 660–670 http://ees.elsevier.com/RASD/default.asp

Is there a relationship between restricted, repetitive, stereotyped behaviors and interests and abnormal sensory response in children with autism spectrum disorders?
Robin L. Gabriels a,b,*, John A. Agnew a,b, Lucy Jane Miller c, Jane Gralla d, Zhaoxing Pan d, Edward Goldson e, James C. Ledbetter e, Juliet P. Dinkins f, Elizabeth Hooks f
Department of Psychiatry, University of Colorado Denver, United States b Department of Psychiatry, The Children’s Hospital, United States c Sensory Processing Disorder Foundation & Sensory Therapies and Research (STAR) Center, Greenwood Village, CO, United States d Department of Pediatrics, University of Colorado Denver and The Research Institute, The Children’s Hospital, United States e Department of Pediatrics, The Children’s Hospital, United States f School of Professional Psychology, University of Denver, United States Received 27 January 2008; accepted 7 February 2008
a

Abstract This study examined the relation between restricted, repetitive, and stereotyped behaviors and interests (RBs) and sensory responses in a group of 70 children and adolescents diagnosed with an autism spectrum disorder (ASD). Caregivers completed the Repetitive Behavior Scale-Revised (RBS-R) and the Sensory Profile. Controlling for IQ and age, total RBS-R and Sensory Profile scores revealed significant correlations both prior to and after removing overlapping items. Examination of the co-occurrence of RBs and atypical sensory responses in this population suggests a subgroup has consistently high rates of problems in both RBs and sensory processing. In addition, this subgroup has high rates of prescribed psychoactive medications and co-morbid psychiatric diagnoses. The IQ and age of this subgroup did not differ significantly from the rest of the participants. Results are consistent with previous research describing the co-occurrence of RBs and sensory response abnormalities in the ASD population. Further investigation of the subset of individuals with ASD who have high rates of RBs and abnormal sensory responses may lead to a more comprehensive

* Corresponding author at: The Children’s Hospital, 13123 East 16th Avenue, B361, Aurora, CO 80045, United States. Tel.: +1 720 777 3404; fax: +1 720 777 7314. E-mail address: gabriels.robin@tchden.org (R.L. Gabriels). 1750-9467/$ – see front matter # 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.rasd.2008.02.002

Hill. & Farley. Fico. Kiely. Wood. 1993. Volkmar. Kern et al. 2006. 1994). Summers. They also may have seizures (Elia. Adolescents 1. tactile. & Berkson. frequency. and self-injurious behaviors (Bodfish. 2007. & Watson. 1990. ASDs are diagnosed based on a core triad of clinically observable symptoms involving impaired social interaction and communication abilities along with restricted. & McNeill. Gabriels. Cohen. Hill. & Sherman. Autism spectrum disorders. 1995. compulsive or ritualized behaviors.. Poe. 2003). Stone. 2001). Tomchek & Dunn. & Bergonzi. 1994). and proprioceptive domains (Dunn. 2006. a group of disorders that are thought to be related through the sharing of risk genes or pathophysiological mechanisms’’ (Hyman. & Smith. 1997. Yeargin-Allsopp et al. 2005. which is associated with abnormal . David. 2007. 1998. Introduction Autism spectrum disorders (ASD) include Autistic Disorder. such as Obsessive Compulsive Disorder (American Psychiatric Association. 2004). research with this subgroup may have significance for identifying a specific phenotype in ASD. Lainhart. RB features also appear as a part of early typical development. Matson. p. & Kinsbourne. 1977. & Bamburg. 1995). Musumeci. Ivers. Greenspan & Wieder.. 1985). Fein. 1976. 2005. if a specific pattern of RBs distinguishes a unique ASD phenotype from general cognitive disabilities is not known. are present in individuals with other developmental disabilities (Berkson. Hirstein. RB features in individuals with ASD vary in their occurrence.R. 2001. Ornitz. Cuccaro. Children. Gillberg et al. / Research in Autism Spectrum Disorders 2 (2008) 660–670 661 understanding of their clinical picture and improve interventions. Tomchek & Dunn. & Paul. 1978. Bravaccio. & Santosh... & Palermo. 2003. In addition to the core diagnostic features. . 2001. RBs include stereotyped and repetitive body movements and manipulation of object parts. Not Otherwise Specified (American Psychiatric Association. & Shinnar. Atypical sensory response patterns occur in many individuals with autism (Baranek. & Bryson. 2006. Falco. Mulick. Berkson. Specifically.L. circumscribed interests. The term ‘‘spectrum disorders’’ is commonly used to refer to this population and has been defined as ‘‘. Saulnier. Keywords: Repetitive behaviors. . Foster.. Kern et al. Ivers. 2003). Tuchman. 2000). and sleep (Schreck. Additionally. All seven sensory domains may be affected particularly auditory. adaptive behavior (Gabriels. repetitive. & Farley. 2007). Liss. Tecchio et al. # 2008 Elsevier Ltd. & Lewis. 2007) and together all three subtypes are known as Sensory Modulation Disorder. individuals with ASD have a variety of challenges in areas such as cognition (Chakrabarti & Fombonne. WainwrightSharp & Bryson. 2007. 2006. Ornitz. Parker. Symons. Numerous studies report clinical evidence of abnormal responses to sensory stimuli in the ASD population (Baranek. and Pervasive Developmental Disorder.. Rapin. Lewis & Bodfish. & Ramachandran. Schultz & Berkson. and stereotyped behaviors and interests (RBs) (American Psychiatric Association. however. 1999). 2004. 730). Tupa. Leyfer et al. Militerni. Guthrie. 1997. All rights reserved. and are a diagnostic part of other mental disorders. Carcani-Rathwell. under-responsivity and sensory seeking behavior. 1997. Poustka & Lisch. 2003. Gabriels et al. 2002. & Goldson. insistence on sameness of the environment and routines. 1991) and/or co-morbid psychiatric disorders (Bradley. Sverd. Some reports suggest that intellectual ability is highly correlated with both the occurrence and type of RBs in individuals with autism (Bartak & Rutter. 1986. and severity (Bodfish et al. 1994). visual.. Ferri. vestibular. 1993) including over-responsivity. Sensory response. Agnew. Rabe-Hasketh. Asperger’s Disorder. 2000. Thompson & Berkson. Guthrie. Iversen. 2002.

Missiuna. research. a limitation in many previous studies is information specifying the cognitive level of the sample and what the relation is between cognition and sensory response. Thompson & Berkson. Grandin.. Rogers et al. 2003. Willemsen-Swinkels. 1993.. 1976. However. Miller. The mean age of all . Visual over-responsivity and increased RBs were noted with florescent light compared to incandescent lighting in ASD (Colman et al. 2003.. Despite these findings that suggest a direct relation between RBs and abnormal sensory responsiveness in individuals. 1992. Mandich. 1976). Dahlgren & Gillberg. The inconsistent labeling of behavior confounds interpretation of the overlap/discrimination of RBs and sensory response abnormalities. Rutter. Militerni et al.. Dyck. 58 males. the goal was elucidating whether the association is due to item overlap in scales. since intellectual ability has been shown to be related to the expression of RBs (Bartak & Rutter. 2006). Parham. Poustka & Lisch.662 R.. Further studies have shown that ‘‘attractive’’ sensory stimuli are related to reduced stereotyped movements compared to ‘‘aversive’’ sensory stimuli (Gal et al. 2005. aversive responses to tactile stimulation which is not noxious to most people) has been associated with more rigid stereotyped behaviors (e. & Wehner. Similarly high levels of sensory responsiveness are noted in individuals with fragile X syndrome. Gabriels et al. Rogers. Hepburn. Kientz & Dunn. & Macnab. Gal. / Research in Autism Spectrum Disorders 2 (2008) 660–670 arousal. The third goal was examining whether a phenotypic subtype of ASD was suggested with high rates of RBs and abnormal sensory responses. Gabriels et al. The aim of this pilot study was to evaluate whether a relationship existed between RBs and sensory response in children with ASD. 1997. Ornitz et al. the Short Sensory Profile (McIntosh. 1997). & Le Couteur.. Thus certain scales label a behavior as an RB while different scales label the same behavior as sensory. 1989. tactile over-responsivity (i. Frankel. 2006). Watling. 1999) classifies ‘‘touches people and objects’’ as a sensory seeking behavior. Methods 2. 12 females) participated.. Shyu.. Studies have examined specifically this relationship between RBs and sensory response to environmental stimulation in individuals with developmental disabilities and those with autism (Baranek et al. One scale. 2001. and community settings. 2006. & van Engeland. & White. The sample was recruited from clinical. insistence on sameness and repetitive verbalizations) (Baranek et al. 1997. & Freeman. Studies using parent-report scales suggest that children with autism have significantly more abnormal sensory responses than do children with other developmental delays and/or typically developing children (Baranek.e. 1999) classifies the same behavior as a compulsive behavior. 2002.1.L. 1969). & Hagerman. For all research questions methodology used in previous studies was improved upon by measuring and controlling for IQ. Researchers suggests two disparate reasons that individuals with ASD might engage in RBs: (1) to induce a sensory experience and (2) as reaction to sensory stimulation (Liss et al. For example. 1985). the Repetitive Behavior Scale-Revised (Bodfish et al. Ritvo. receptive aphasia. For example. Secondarily. 1994) are used interchangeably with ‘‘sensory seeking’’ behaviors (Liss et al.. Lord. and yet another scale. 2002.g. Wing. Carcani-Rathwell et al. & Passmore. 2002) in children with autism and MR (IQs < 50). 2005. Deitz. research on measurement tools which use both RBs and sensory items is lacking rigor.. Colman. 1998). & Bodfish. 1976. 2. Participants Children with a clinical diagnosis of an ASD (n = 70.. 1997. behavior labeled repetitive movement behaviors in the DSM-IV (American Psychiatric Association. 1995. and deafblindness (Miller. 2001).. Buitelaar. Dekker. 1994. Polatajko. Lord... Matson et al. 1978.

SSRIs.8 (min: 3. 1981. yet comprehensive survey of the entire spectrum of RBs clinically observed and referred to in the DSM-IV (American Psychiatric Association. 0 years (range: 3. consisting of six distinct subscales (Stereotyped Behavior. max: 19.L.0–19. Sameness Behavior and Restricted Behavior). which identified the puberty status of their child based on Tanner’s criteria (Tanner.4. opioid agonists and alpha adrenergic agonists. 1997).. and (b) diagnostic data to confirm a DSM-IV (American Psychiatric Association.g. 1990) (average full scale IQ = 81.2. In this sample. 2003). The RBS-R is a brief (<15 min to complete).4 Æ 26. Instrumentation 2. max: 138) 48 14 8 . caregivers responded to a screening. where 0 indicates the behavior does not occur and 3 indicates the behavior does occur and is a severe problem. Inclusion criteria were: (a) documentation of participants’ full scale IQ (within 41 months of study entry). stimulants. Routine Behavior. Compulsive Behavior. Murray. / Research in Autism Spectrum Disorders 2 (2008) 660–670 663 participants in this study was 10.9% Caucasian Yes: 30. the Bayley Scales of Infant Development (Bayley. Thirty (43%) of the 70 participants were diagnosed with co-morbid psychiatric disorders including mood disorders.1 (range 25–138). Table 1 Demographic characteristics of participants N = 70 Mean age (years) Gender Ethnicity Co-morbid psychiatric diagnoses Puberty Psychoactive medications Mean IQ Diagnosis Autistic Disorder Asperger’s Disorder PDD-NOS 10. 1989. the Kaufman-ABC (Kaufman & Kaufman. including atypical antipsychotics. In addition.4 (min: 25.2. and sleep disorders. anxiety disorders. 1994) diagnostic description of Autistic Disorder. Self-injurious Behavior. Thirty-one (44%) of the 70 participants were identified as pubescent by their caregivers. 1993). 2. 1999) is an empirically derived 43-item caregiver report of the full spectrum of RBs. 1962) (e. Subject demographics are summarized in Table 1.R. no: 39 Yes: 42. Gabriels et al.8 Æ 4. attention deficit disorders. It showed discriminant validity in adults. mood stabilizers. 1991. and the Differential Abilities Scales (Elliott. 1994) clinical diagnosis of an ASD. the five Tanner stages were divided into two groupings: Group 1 (prepubescent) and Group 2: all other Tanner stages 2–5 (pubescent). physically observable pubertal maturation features such as genital and pubic hair in boys and breast and pubic hair in girls.7) Male: 58. Forty-two of the 70 participants (60%) were taking psychotropic medications at the time of the study. no: 40 Yes: 31.7 years) and the average IQ was 81. IQ tests review included the Wechsler Intelligence Scales (Wechsler. female: 12 82. 1997. ranging from 25 to 138). 1995). psychotic disorders. no: 28 81. Repetitive Behavior Scale-Revised (RBS-R) The RBS-R (Bodfish et al. & Pearson.0. the Leiter International Performance Scale-R (Roid & Miller. 1983).. the Mullen Scales of Early Learning (Mullen.1. Parents or caregivers rate 43 behaviors on a scale of 0–3.

3. 2003) was used for data analysis.664 R.2. 2. p < 0. To determine whether frequent/severe RBs or sensory processing abnormalities were affected by the use of psychotropic medication.. 2. The developers of this measure have collected data with children with ASD ages 3–17 years (Dunn. controlling for age and IQ. 2000). Item responses occur on a five point Likert-rating scale from 1 (always occurs) to 5 (never occurs). See Table 2 for a list of these specific items. Auditory. Procedure The study was approved by the Institutional Review Board and caregivers participated in informed consent to review participants’ medical records to obtain demographic.001) with the complete sample. One caregiver for each participant completed both the RBS-R and the Sensory Profile based on the participant’s behavior in the past month. 1999). confirming a strong relation among the items. 2. Touch.. a sum of six domain scores (i. Participants’ current age. Several items on the RBS-R overlap with items on the Sensory Processing domain of the Sensory Profile.2. The Sensory Profile provides two sets of standard scores depending on how the items are clustered: (1) domain scores (Sensory Processing. This reduced the critical p value to p < 0.05.4. For the analyses. Vestibular.001).5 for Windows (SPSS. To address the primary aim of characterizing the relation between RBs and abnormal sensory response. a multivariate analysis of variance (MANOVA) was performed. with dependent factors of total RBS-R score and total Sensory Processing domain score. Sensory Profile (Caregiver Questionnaire) The Sensory Profile (Dunn. Visual.007 to achieve an uncorrected alpha of p < 0. Multisensory and Oral Sensory Processing. Behavior and Emotional Response) and (2) factor scores (nine empirically derived factors). diagnostic. Sensory Modulation. and IQ information. Normative data for the Sensory Profile were obtained from 1037 typically developing children ages 3–10 years. and medications were provided by caregivers. This study used the Sensory Processing score. a partial correlation between RBS-R Total Score and the Sensory Processing domain score was calculated.L.65 ( p < 0.2. alpha was set at 0.2. The correlation between the overlapping items from the RBS-R and the Sensory Processing domain of the Sensory Profile was À0. standard caregiver questionnaire of the effect of sensory processing on the child’s ability to function in daily life.e. 1999) is a 125-item. Participants were excluded if no standardized IQ results were available.61. . / Research in Autism Spectrum Disorders 2 (2008) 660–670 distinguishing participants with autism and MR from non-autistic participants with MR in the overall RBS severity score (Bodfish et al. Three additional items in the remaining five RBS-R subscales were also dropped. 3.05 and a Bonferroni correction for multiple significance tests for the correlation analysis was applied. the redundant items from the RBS-R were deleted from the analysis including the complete Stereotyped Behavior Subscale of the RBS-R. puberty status. To assure that the relation between the scales was not affected by item overlap. 30-min. Gabriels et al. Results A significant correlation was found between the RBS-R Total Score and the Sensory Processing domain score (Pearson’s r = À0. Analytical procedure Statistical Package for the Social Sciences version 11.

84). Rocks unconsciously 24/25. 1. Touches people and objects 61.001). / Research in Autism Spectrum Disorders 2 (2008) 660–670 Table 2 Overlapping measurement items RBS-R item 1. Need to touch.75. Body rocking.09) and inclusion of full scale IQ did not affect the model ( p = 0.) . lets objects fall 6. Rubs or scratches out a spot that have been touched 40/41/45. 1) and the upper quartile (‘‘High RB’’ subgroup. Unusual need to touch certain toys.L. Fig. Covers eyes.07).53. Twirls/spins self frequently 41. Turns in circles. on Full Scale IQ score (t = 0. p = 0. p < 0. surfaces or textures 15. Rolls head. No significant differences between the High RB and Low RB subgroups on age (t = 0. turns head 3. twiddles or slaps or throws objects. covers ears. Gabriels et al. Sensory Profile Total Score and RBS-R Total Score. whirls. Strongly prefers eating or drinking certain things Sensory Profile Item 665 27. The effect of psychoactive medication was non-significant ( p = 0. Spins or twirls objects.53. Shows strong preference for certain tastes A new analysis with overlapping RBS-R items deleted identified a significant correlation between this shortened RBS-R Total Score and the Sensory Processing domain score of the Sensory Profile (Pearson’s r = À0.21. The data were then examined to explore the presence of a phenotypic subgroup within ASD who has both high RBs and atypical sensory responses. tap or rub items. jumps 5. (Grey shading in lower right quadrant highlights High RB group. p < 0.001) with the complete sample. Holds hands over ears 39. a MANOVA was conducted with full scale IQ as a covariate. nods head. claps hands. shakes hand or arm 4. smells or sniffs items 12. This finding remained relatively unchanged when age and IQ were controlled by partial correlations (r = À0. surfaces or people 23. Seeks all kinds of movement (fidgets) 26. body swaying 2. RBS-R Total Score !44) compared to the lower three quartiles (‘‘Low RB’’ subgroup) using unpaired t-tests and x2. Rubs or scratches self 22. Covers eyes or squints. Flaps hand.46). Seeks all kinds of movement (fidgets) 24/25. 2. p = 0. To determine the impact of taking psychoactive medications on the shortened RBS-R Total Score and Sensory Processing domain score of the Sensory Profile. The sample was divided into quartiles based on the RBS-R Total Score (with overlapping items deleted) (see Fig.R.

001) with the High RB subgroup demonstrating significantly more abnormal sensory responses.666 R.03 0. in a group of 70 participants with ASD.03).16). p = 0. the High RB and Low RB subgroups showed significant differences on the Sensory Processing domain of the Sensory Profile Sensory (t = 4. A chart review of the sensory response problems in the High RB subgroup revealed a variety of issues including over. Colman et al.04 or on puberty status (x2 = 2.7% Statistical value t = 0.96 (min: 2. max: 319) 49. it seems logical that the Sensory Processing domain total scores are atypical in the High RB .75 t = 0.01 x2 = 4. Given the correlation between the RBS-R and the Sensory Processing domain score of the Sensory Profile. 1998). and vestibular stimulation. 4. and treat.29 t = 4. The demographic data related to this subgroup suggests that they are more difficult to understand. 2002.24 (min: 44. under. p = 0. more than half of whom had Bipolar Disorder. However. but that the High RB subgroup did have a significantly higher percentage of participants taking psychoactive medications (x2 = 4.13 (min: 3. max: 138) 24.21 t = 11.8% High RB subgroup (n = 17) 10. max: 95) 212.16 0.4% 64.16) was found.92 x2 = 2. auditory.67) 81. / Research in Autism Spectrum Disorders 2 (2008) 660–670 Table 3 Characteristics of High RB and Low RB subgroups Low RB subgroup (n = 53) Mean age (years) Mean IQ RBS-R Total Score Sensory Profile Total Score Puberty Psychoactive medications Co-morbid psychiatric diagnoses 10. Using a x2 test.L. Finally. as assessed by the RBS-R Total Score and abnormal sensory responses. p = 0. 1976. Discussion This study demonstrated a significant relationship between frequent/severe RBs.73) 80. it was shown that the High RB subgroup did not differ significantly from the Low RB group in terms of puberty status (x2 = 2.24 (min: 168. as assessed by the Sensory Processing domain of the Sensory Profile.38 p value 0. After removing overlapping items from the RBS-R. tactile. 1997.01. See Table 3 for a description of these two subgroups. 82% in the High RB group compared to 53% in the Low RB subgroup. 1992.67 x2 = 4.1% 52. max: 43) 249. Of particular interest was the suggestion that a subgroup might exist within ASD with high rates of RBs and abnormal sensory responses regardless of age and IQ.13 (min: 207. Co-morbid psychiatric diagnosis were also significantly higher in the High RB subgroup (x2 = 4.8% 35. max: 110) 62.4% 82.99. diagnose.29 (min: 38. oral. max: 19..04) with 64% of the High RB group compared to only 36% of the Low RB group demonstrating additional diagnoses. These findings concur with findings from previous smaller studies (Baranek et al.92.67.84 <0.001 0. Examination of the co-morbid diagnoses in the High RB group revealed 59% has a mood disorder. and sensory seeking behaviors in relation to visual. reflected by more psychoactive medications. particularly Bipolar Disorder and other mood disorders..46 0.01. Gabriels et al. max: 244) 29. Grandin.63. p = 0. Willemsen-Swinkels et al.02 (min: 2.. Gal et al. p < 0..001 <0. diagnosis after age 6 years and more co-morbid psychiatric diagnoses. which suggests that the relation is not an artifact of item overlap in the dependent measures. 52% of the participants in the High RB subgroup were not diagnosed with an ASD until at least age six and some were not diagnosed until 18 years of age. a significant association remained.38.81 (min: 25. controlling for age and IQ. max: 17.

R. 4. G. IQ..L. Future studies should also collect reports of RBs and sensory response abnormalities from more than one caregiver including teachers. T.. This study was funded by The Children’s Hospital Research Institute. . IV).. L. (pp.831–861). & Bodfish. (2005b). W. combined with a larger sample size. Eds. 51. This research may be significant for better understanding the genetic etiology of ASD. and Bridget Bax. American Psychiatric Association. American Journal of Occupational Therapy. David. Poe. puberty status. G. Foster. would permit more definitive conclusions. Vol. (1994). T. L. Acknowledgements We are grateful to the families and children who participated in this study.. However.. individuals with autism may be under responsive to pain sensation and cause self-injury by insisting on engaging in repetitive behaviors such as head banging or biting themselves (Gal et al. Assessment. 1 suggests that participants in the Low RB subgroup have more heterogeneous Sensory Processing domain scores than persons in the High RB subgroup. Future directions This study suggests more frequent/severe RBs and atypical sensory responses are associated. Sensory Experiences Questionnaire: Discriminating sensory features in young children with autism. some participants in the Low RB subgroup have minimal abnormal sensory responses.. a subgroup with ASD who have high RBs and high atypical sensory responses appears to exist. In Volkmar.C. include standardized clinical observations of RBs and abnormal sensory response. J. and medication use. Specifically. 2007).2. and if possible. . Baranek. However. 3rd ed.. OTR. J. 2. interventions. This. & Cohen. 4. G. Gabriels et al. for their assistance with this study. F. Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) (Vol. A. 591–601. Tactile defensiveness and stereotyped behaviors. (1997). L. R. D. G. F. & Watson. & Berkson. Paul. 91–95. G. T. Baranek. the scatter plot in Fig. This subgroup may benefit from more comprehensive assessment to identify the presence of additional co-morbidities and/or sensory response abnormalities. D. M. B..1. D. causality cannot be inferred from these correlation findings. D.. Klin... developmental delays. and typical development. Limitations of the present study The findings of this pilot study are limited by the fact that the RB and sensory response measurements were based only on caregiver report measures. For example. Handbook of autism and pervasive developmental disorders. thus informing clinical interventions leading to a more comprehensive understanding of the clinical picture. Though this observation is limited by a relatively small sample size. R. and policy. Replication studies are needed to support or refute the findings with a larger ASD sample controlling for age... L. We would also like to thank Katherine Holt. Sensory and motor features in autism: Assessment and intervention. W. J. / Research in Autism Spectrum Disorders 2 (2008) 660–670 667 subgroup. Finally. Washington. further research examining whether these two characteristics within autism constitute a consistent phenotypic subgroup is indicated. Parham. References American Psychiatric Association. 47(6). Collecting RB and sensory response information from several different reporters across environments would provide a more comprehensive picture of these features. Stone.A. as was done in this study. (2005a). Baranek. Journal of Child Psychology and Psychiatry.

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