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A light fingertip touch reduces postural sway in children with autism spectrum disorders
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GAIPOS-4570; No. of Pages 4 Gait & Posture xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
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A light fingertip touch reduces postural sway in children with autism spectrum disorders Fu-Chen Chen a,*, Chia-Liang Tsai b,1 a b
Department of Recreational Sport & Health Promotion, National Pingtung University of Science & Technology, Taiwan Institute of Physical Education, Health & Leisure Studies, National Cheng Kung University, Taiwan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 22 April 2015 Received in revised form 3 September 2015 Accepted 15 September 2015
This study examined the effects of a light fingertip touch on postural control in children with autism spectrum disorders (ASD) and typically developing children (TDC). Methods: We recruited 16 children with ASD (age = 11.041 1.275), and 16 TDC (age = 10.966 1.166 years). A force platform measured postural sway in the anteroposterior (AP) and mediolateral (ML) directions under light fingertip touch (LT) and no touch (NT) conditions, with both eyes open (EO) and both eyes closed (EC). As a summary of the experimental conditions, ML sway was significantly greater in the ASD group than in the TDC group. Also, results showed a significant reduction in postural sway in the ML direction in the LT condition compared with the NT condition. These effects applied to both the EO and EC conditions. Lastly, the reduction in ML sway between the NT and LT conditions was significantly greater in the ASD than the TDC group. Conclusion: The effects of a light fingertip touch on reducing postural sway appear more efficient in children with ASD compared with TDC. These findings suggest that a light fingertip touch may be of clinical and practical importance, and provides a useful means of enhancing postural stability in children with ASD. ß 2015 Published by Elsevier B.V.
Keywords: Light touch Postural sway Autism spectrum disorders
1. Introduction Autism spectrum disorder (ASD) is a specific neurodevelopmental disorder with a prevalence estimated at approximately 1– 2% in the school-aged population [1]. Children with ASD are commonly characterized by impairments in communication, social interactions, and recognition of facial expressions [2], as well as difficulties in motor control such as gait, fine motor activities, and control of upright postural sway [3,4]. Whyatt and Craig [5] used the second edition of the Movement Assessment Battery for Children to determine motor skills in children with and without ASD. The greatest area of limitation among autistic children was static balance, highlighting their apparent problems in activities requiring postural control. Minshew et al. [6] measured the duration of one-legged standing with eyes closed, and found that children with Asperger syndrome, a subtype of ASD, maintained
* Corresponding author at: 1, Xuefu Road, Neipu Township, Pingtung County 912, Taiwan. Tel.: +886 87703202; fax: +886 87740536. E-mail addresses: [email protected] (F.-C. Chen), [email protected] (C.-L. Tsai). 1 Address: 1, Daxue Road, East District, Tainan City 701, Taiwan.
one-legged standing for a significantly shorter period than their matched peers, demonstrating the poor control of postural sway in children with ASD. In addition, Molloy et al. [7] used a force platform to examine the excursion of the center of pressure (COP) in children with ASD and typically developing children (TDC). Subjects were examined when standing with two legs on a piece of foam as well as without foam, in both eyes-open (EO) and eyesclosed (EC) conditions. The results indicated a notably greater level of postural sway for all experimental conditions in the ASD group compared with the controls. Additionally, an interaction effect showed that the absence of vision made the differences in the magnitude of postural sway between children with ASD and TDC even more prominent. Kohen-Raz et al. [8] asked individuals with and without ASD to stand on four force plates (one for each toe/ heel) with the aim of assessing the control patterns of postural sway. They found that patterns of postural control in autistic individuals were less likely to change according to age, and were less stable in the control of lateral sway than those in the control group. Based on the diversity of previous study methods and designs, and the consistent trends among their findings, it appears plausible to conclude that autistic children have deficits in the modulation of sway in an upright standing posture. In the current study, the author was particularly interested in how the poor
http://dx.doi.org/10.1016/j.gaitpost.2015.09.012 0966-6362/ß 2015 Published by Elsevier B.V.
Please cite this article in press as: Chen F-C, Tsai C-L. A light fingertip touch reduces postural sway in children with autism spectrum disorders. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.012
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control of sway in the upright posture might be modified in children with ASD, as the fundamental capacity to control posture can greatly affect children’s daily living skills [9], play, and social interactions with others [10]. The effects of light touch on modifying postural control were first reported by Holden et al. [11] in 1994, who found that the amplitude of postural sway in bi-pedal standing significantly decreased in healthy adults while applying light fingertip contact (<1 Newton (N)) on a stable surface. This ‘‘light touch paradigm’’ later became widely employed in populations vulnerable to balance problems. Cunha et al.’s study [12] indicated that applying light contact with a fingertip to a stationary bar significantly reduced postural sway in patients with cerebrovascular accidents in the anterior arterial territory. This stabilizing effect of a light fingertip touch applied in both the EO and EC conditions. More interestingly, Tremblay et al. [13] and Baccini et al.’s [14] studies demonstrated a group light touch interaction, revealing that the effects of light touch on postural stabilization were even more efficient in older adults during both comfortable standing postures (feet naturally apart and weight evenly distributed) and semitandem postures compared with young adults. This interaction effect has been widely reproduced in individuals with Down syndrome [15], unilateral anterior cruciate ligament (ACL) injury [16], and bilateral vestibular loss [17]. Collectively, previous results provide both replication and extension of Holden et al.’s work, demonstrating that light touch is an influential intervention to enhance postural stabilization for clinical populations. Although there has been many empirical studies investigating how light touch modifies postural control in individuals who have difficulties in adjusting posture, there is no research on this effect in children with ASD. Hence, the current study aimed to investigate how the use of light fingertip touch influences the responses of postural sway in children with and without ASD. In addition, research has indicated greater group differences in the control of postural sway when visual information is occluded [7]; therefore, the current study investigated further the effect of light touch in a scenario where upright postural control was challenged by removing vision. We hypothesized that children with and without ASD would reduce postural sway while applying a light fingertip touch to a stable surface in both the EO and EC conditions, and that the light touch effect would be greater in the ASD group compared with the TDC group. 2. Methods Before this study took place, participants and their guardians were informed about the experimental process and signed an informed consent form approved by the Institutional Review Board of Antai Memorial Hospital, Pingtung County, Taiwan. 2.1. Participants Sixteen children with ASD (height = 142.063 8.242 cm, weight = 40.750 7.010 kg) and 16 TDC (height = 144.063 7.937 cm, cm, weight = 41.813 7.485 kg) took part in this study. Participants were recruited using convenience sampling from eleven mainstream primary schools in Pingtung County and Taitung County, Taiwan. The diagnosis of ASDs was based on the DSM-IV-TR [2], and established by a psychologist or psychiatrist in a public hospital, and the severity level of ASD was based on both language comprehension and functioning in the social adaptive skills domain [18]. All participants in the ASD group were mildly autistic, and were enrolled in regular classroom settings with added resource support for reading and/or mathematics. The inclusion criteria were: (1) aged 9–12 years, (2) an overall IQ of at least 80, and (3) being able to understand and follow instructions. The exclusion criteria were: (1) ongoing medication, (2) severe neurological disorders (e.g.,
epilepsy, brain tumor, and cerebral palsy), (3) musculoskeletal conditions affecting postural control (e.g., sprain, and fracture), and (4) severe behavioral problems. A case–control design was employed; therefore, the two groups were matched in gender ratio (eleven males and five females in each group) and age ratio (four individuals in each age band for both groups, ASD = 11.041 1.275 years, TDC = 10.966 1.166 years). All participants were right-handed and had normal or corrected-to-normal vision. 2.2. Apparatus Participants stood on a Kistler force platform (model: 9260AA6, Winterthur, Switzerland) that collected data for COP sway with a sampling rate set at 100 Hz. The signals from the force platform were filtered by a Butterworth low pass filter at 10 Hz. In addition, participants were asked to touch a customized 5 cm 5 cm force plate (LSB 200, Futek Advanced Sensor Technology, Inc., Irvine, CA) (mounted on a tripod) that measured data for touch force in the vertical direction at a sampling rate of 1000 Hz via Labview 2012 (National Instruments, Austin, Texas, USA). We set the threshold for touch force at 1 N. Once the touch force exceeded the threshold, an alarm was triggered and a repeat trial was requested. 2.3. Procedure Participants were instructed to stand quietly and relax for 60 s in each trial, with their feet side-by-side at shoulder width on a force platform. For each participant, we marked the position of both the heel and toe to enable consistent positioning across trials. Participants looked straight ahead at a black circular mark attached on a wall 100 cm away in the EO condition, and kept their eyes shut in the EC condition. Besides, the positions of the arm were different between the no touch (NT) and the light touch (LT) conditions. Arms were relaxed at their sides in the NT condition, while the dominant (right) index fingertip applied light contact to a fixed point on the customized force plate placed laterally at about waist level in the LT condition [14]. The force of the fingertip touch applied to the plate was limited to 1 N in the vertical direction. All participants received three trials for each of the four conditions: (1) EO + NT, (2) EO + LT, (3) EC + NT, and (4) EC + LT, with the order of trials randomly assigned. Each experimental condition was practiced once before formal data collection, and there was a one-minute rest between trials. Two trials were aborted and repeated for a child due to failure to keep touch force within the threshold. Participants were coded to blind an experimenter who collected and analyzed the data. 2.4. Statistics All data were processed using the SPSS 18.0 (SPSS Inc., Chicago, IL, USA). Touch force in the vertical direction was calculated for each LT trial. We quantified the magnitude of postural sway in terms of the standard deviation of COP excursion for both anteroposterior (AP) and mediolateral (ML) directions, as this dependent variable represents the level of postural stabilization [19]. A higher value for postural sway demonstrates a lower level of stabilization, and vice versa. The average values for postural sway from three trials performed in each experimental condition were used for analysis. Data was presented as the mean SD. An independent t-test was used to determine group differences in mean touch force. Separate group (2: ASD and TDC) vision (EO and EC) and touch (NT and LT) repeated measures ANOVAs were performed for postural sway in the AP and ML directions. The effect size was quantified by calculating etasquared (h2). Both group vision and group touch interactions were found; therefore, post hoc comparisons were performed using planned t-tests with Bonferroni corrections to determine whether the
Please cite this article in press as: Chen F-C, Tsai C-L. A light fingertip touch reduces postural sway in children with autism spectrum disorders. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.012
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groups differed in the changes of sway amplitude between the two visual conditions (1) in the NT condition only, and (2) in the LT condition only, as well as between the two touch conditions (3) in the EO condition only, and (4) in the EC condition only. Statistical significance was defined as p < 0.05.
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(t(30) = 2.171, p = 0.019) (Fig. 2b). No significant effects were found for AP sway. 4. Discussion
Analysis of the kinematic data indicated a significant main effect of group (F(1, 30) = 53.616, p < 0.001, h2 = 0.641), with a larger mean ML sway in children with ASD (0.614 0.343 cm), compared to that of controls (0.335 0.094 cm). A significant main effect of vision (F(1, 30) = 14.345, p = 0.001, h2 = 0.323) was also observed, showing that ML sway was greater in the EC condition (0.556 0.307 cm) compared to the EO condition (0.393 0.241 cm). Lastly, there was a significant group vision interaction (F(1, 30) = 6.977, p = 0.013, h2 = 0.141) that the effect of the absence of vision was more prominent in children with ASD compared with TDC. Post hoc planned comparisons indicated that the ASD group increased COP sway from the EO to the EC conditions by a level greater than that of the TDC group in the NT condition (t(30) = 2.284, p = 0.015) (Fig. 1a), and in the LT condition (t(30) = 2.104, p = 0.022) (Fig. 1b). Regarding our hypotheses, the analysis of postural sway revealed a main effect of touch (F(1, 30) = 18.581, p < 0.001, h2 = 0.382), demonstrating that ML sway was significantly greater in the NT (0.558 0.337 cm) condition than in the LT (0.391 0.196 cm) condition. In addition, there was no vision touch interaction (F(1, 30) = 1.101, p = 0.302, h2 = 0.035), indicating that the effect of light touch in reducing postural sway was independent of vision conditions. Lastly, there was a significant group touch interaction (F(1, 30) = 7.567, p = 0.010, h2 = 0.123) that the effect of a fingertip touch was more prominent in children with ASD compared with TDC. Post hoc planned comparisons indicated that the ASD group reduced COP sway from the LT to the NT conditions by a level greater than that of the TDC group in the EO condition (t(30) = 2.171, p = 0.023) (Fig. 2a), and in the EC condition
This study examined the influence of light fingertip touch on the control of postural sway in children with ASD and TDC while standing with both eyes open and eyes closed. The results indicated that children with ASD swayed more than TDC. Additionally, an increased postural sway occurred when visual information was unavailable, an effect more pronounced in children with ASD than in TDC. More importantly, the new findings from the results were that a light fingertip touch reduced postural sway in children with and without ASD in both EO and EC conditions, and that autistic children benefited more from fingertip touch than TDC. Firstly, the group effect showed that children with ASD had a markedly greater amount of postural sway in the ML direction than TDC. These results were consistent with previous findings [8,20]. In a shoulder-width stance, the sway in the ML direction is mainly modulated by hip strategy, which involves the activation of both abductor and adductor muscles [21,22]. Therefore, the greater amount of ML sway may reflect a deficit, an abnormality, or a less adept ability in the use of hip strategy to maintain balance in children with ASD. In addition, the vision effect showed that removing vision resulted in a significant increase in postural sway compared to quiet standing with eyes open. This was not surprising, as visual information about both body movements and orientation in the environment are deprived in the EC condition. Lastly, the interaction effects of group vision further revealed that the vision effect is more pronounced in children with ASD than in TDC; that is, children with ASD showed more difficulties in maintaining postural balance when visual information was occluded. Molloy et al. [7] found a similar group vision interaction effect, and they suggested an overreliance on visual information to regulate body movements among children with ASD. A more recent study showed that children with ASD displayed impairments in processing proprioceptive input [23]. Thus, it seems rational that children with ASD would display a greater augmentation in postural sway compared with TDC under the condition that a lack of visual input would require individuals to depend more on proprioception. In short, the present results replicated previous studies, indicating poor control of ML sway in children with ASD, especially when vision was restricted.
Fig. 1. Mean ML sway in the EO and the EC conditions for the ASD and the TDC groups. (a) The NT condition only, (b) the LT condition only. Error bar represents standard error. EO, eyes open, EC, eyes closed, NT, no touch, LT, light touch, ASD, children with autism spectrum disorders, TDC, typically developing children. Asterisk symbols report the result of post hoc tests that groups differ in the changes of sway amplitude between the EO and the EC conditions.
Fig. 2. Mean ML sway in the NT and the LT conditions for the ASD and the TDC groups. (a) The EO condition only, (b) the EC condition only. Error bar represents standard error. EO, eyes open, EC, eyes closed, NT, no touch, LT, light touch, ASD, children with autism spectrum disorders, TDC, typically developing children. Asterisk symbols report the result of post hoc tests that groups differ in the changes of sway amplitude between the NT and the LT conditions.
3. Results 3.1. Touch force Mean touch force was 0.314 0.119 N in the ASD group, and 0.283 0.093 N in the TDC group. No difference was found between the ASD and TDC group (t(30) = 0.829, p = 0.414). 3.2. Magnitude of postural sway
Please cite this article in press as: Chen F-C, Tsai C-L. A light fingertip touch reduces postural sway in children with autism spectrum disorders. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.012
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The most remarkable finding to emerge from the current study was that a light fingertip touch is beneficial for postural stability regardless of the presence of visual information in children with ASD, an effect that is more efficient in children with ASD than TDC. Since in the NT condition, the controls had relatively lower sway amplitude that could prevent the light fingertip touch effect on reducing sway, a floor effect for the control group may explain these findings. It is worth mentioning that the interaction effects require cautious interpretation, as the percentage changes in the sway between the two touch conditions were similar for both groups: approximately 29% for the ASD group, and 26% for the TDC group. Further, even though autistic children showed a more pronounced reduction in sway resulted from light fingertip touch, they still swayed more than their control peers did in the NT condition. Earlier studies repeatedly found that individuals with difficulties in the control of postural sway (e.g., the elderly, individuals with Down syndrome, ACL injuries, or vestibular loss) could take greater advantage of the light touch effect than their matched controls in both EO and EC conditions [13–17]. The present study replicated these findings and extended them to children suffering the diagnosis of autism spectrum, disorders. Studies have demonstrated that tactile stimuli from light contact with a fixed point can provide a source of additional information about spatial reference and bodily movements with respect to the vertical, thus leading to a reduction in COP sway in standing [24–26]. Anatomically, slow adaptation receptors (i.e., Merkel’s disks and Ruffini endings) are especially sensitive to slow changes in skin stretch and skin indentation, while fast adaptation receptors (i.e., Meissner and Pacinian corpuscles) are responsible for rapid onset and offset of the ‘‘slip’’ stimulation [27]. The light touch task required participants to maintain a touch force of less than 1 N and to avoid having their fingertips slipping across the plate; therefore, both the slow and fast adaptation receptors should have been involved. Regarding the functioning of tactile sensitivity in children with ASD, Gu¨c¸lu¨ et al. [28] used vibration stimuli at frequencies of 40 Hz and 250 Hz to determine the tactile threshold of slow and fast adaptation receptors, revealing a similar threshold between children with ASD and TDC. Likewise, a recent experiment conducted by Cascio et al. [29] employed a set of ‘‘von Frey’’ filaments to test the threshold for detecting light touch. The experiment did not find any significant differences in light touch sensitivity between autistic individuals and controls. Collectively, previous studies suggest that the function of perceiving light tactile information is intact in children with ASD. Based on these findings, it is plausible to conclude that children with ASD are able to use additional tactile information to enhance postural stabilization. A possible way to put the present findings into practice is to use the light touch contact of fingertips while children with ASD are performing activities with high demands in balancing, such as standing on a foam surface, or walking a beam. For future research to test the clinical applications of a light fingertip touch, it would be essential to investigate how the use of a light fingertip touch could change postural sway responses while the risk of falling is presented to individuals with ASD. Acknowledgements This study was not funded by Ministry of Science and Technology, Taiwan (104-2410-H-020-007). Conflict of interest We declare that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript
entitled, ‘‘A light fingertip touch reduces postural sway in children with autism spectrum disorders’’.
References [1] Centers for Disease Control and Prevention. Autism spectrum disorders; 2014, Available from http://www.cdc.gov/ncbddd/autism/data.html. [2] American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 4th ed. Washington, DC: American Psychiatric Press; 2000, Text revision. [3] Green D, Charman T, Pickles A, Chandler S, Loucas T, Simonoff E, Baird G. Impairment in movement skills of children with autistic spectrum disorders. Dev Med Child Neurol 2009;51(4):311–6. [4] Ming X, Brimacombe M, Wagner G. Prevalence of motor impairment in autism spectrum disorders. Brain Dev 2007;29(9):565–70. [5] Whyatt CP, Craig CM. Motor skills in children aged 7–10 years, diagnosed with autism spectrum disorder. J Autism Dev Disord 2012;42(9):1799– 809. [6] Minshew NJ, Sung K, Jones BL, Furman JM. Underdevelopment of the postural control system in autism. Neurology 2004;63:2056–61. [7] Molloy CA, Dietrich KN, Bhattacharya A. Postural stability in children with autism spectrum disorder. J Autism Dev Disord 2003;33(6):643–52. [8] Kohen-Raz R, Volkmar FR, Cohen DJ. Postural control in children with autism. J Autism Dev Disord 1992;22(3):419–32. [9] Jasmin E, Couture M, McKinley P, Reid G, Fombonne E, Gisel E. Sensori-motor and daily living skills of preschool children with autism spectrum disorders. J Autism Dev Disord 2009;39(2):231–41. [10] Clearfield MW. Learning to walk changes infants’ social interactions. Infant Behav Dev 2011;34(1):15–25. [11] Holden M, Ventura J, Lackner JR. Stabilization of posture by precision contact of the index finger. J Vestib Res 1994;4(4):285–301. [12] Cunha BP, Alouche SR, Araujo IMG, Freitas SMSF. Individuals with post-stroke hemiparesis are able to use additional sensory information to reduce postural sway. Neurosci Lett 2012;513(1):6–11. [13] Tremblay F, Mireault AC, Dessureault L, Manning H, Seveistrup H. Postural stabilization from fingertip contact: I. Variations in sway attenuation, perceived stability and contact forces with aging. Exp Brain Res 2004;157(3):275– 85. [14] Baccini M, Rinaldi LA, Federighi G, Vannucchi L, Paci M, Mascotti G. Effectiveness of fingertip light contact in reducing postural sway in older people. Age Ageing 2007;36(1):30–5. [15] Gomes MM, Barela JA. Postural control in down syndrome: the use of somatosensory and visual information to attenuate body sway. Motor Control 2007;11(3):224–34. [16] Bonfim TR, Grossi DB, Paccola CAJ, Barela JA. Additional sensory information reduces body sway of individuals with anterior cruciate ligament injury. Neurosci Lett 2008;441(3):257–60. [17] Lackner JR, DiZio P, Jeka JJ, Horak F, Krebs D, Rabin E. Precision contact of the fingertip reduces postural sway of individuals with bilateral vestibular loss. Exp Brain Res 1999;126(4):459–66. [18] Taiwan Executive Yuan Department of Health. Levels of disabilities; 2009, Available from: http://www.doh.gov.tw/CHT2006/DM/DM2_p01.aspx? class_no=211&now_fod_list_no=6753&level_no=3&doc_no=41058. [19] Riley MA, Mitra S, Saunders N, Kiefer AW, Wallot S. The interplay between posture control and memory for spatial locations. Exp Brain Res 2012;217(1):43–52. [20] Memari AH, Ghanouni P, Gharibzadeh S, Eghlidi J, Ziaee A, Moshayedi VP. Postural sway patterns in children with autism spectrum disorder compared with typically developing children. Res Autism Spectr Disord 2013;7(2): 325–32. [21] Winter DA, Prince F, Stergiou P, Powell C. Medial-lateral and anterior-posterior motor responses associated with centre of pressure changes in quiet standing. Neurosci Res Commun 1993;12:141–8. [22] Winter DA, Prince F, Frank JS, Powell C, Zabjek KF. Unified theory regarding A/P and M/L balance in quiet stance. J Neurophysiol 1996;75:2334–43. [23] Blanche EI, Reinoso G, Chang MC, Bodison S. Proprioceptive processing difficulties among children with autism spectrum disorders and developmental disabilities. Am J Occup Ther 2012;66(5):621–4. [24] Jeka JJ, Lackner JR. Fingertip contact influences human postural control. Exp Brain Res 1994;100(3):495–502. [25] Jeka JJ, Lackner JR. The role of haptic cues from rough and slippery surfaces in human postural control. Exp Brain Res 1995;103(2):267–76. [26] Lackner JR, Rabin E, DiZio P. Stabilization of posture by precision touch of the index finger with rigid and flexible filaments. Exp Brain Res 2001;139(4):454– 64. [27] Purves D, Augustine GJ, Fitzpatrick D, Katz LC, LaMantia AS, McNamara JO, Williams SM. Neuroscience. 2nd ed. Sunderland: Sinauer Associates; 2001. [28] Gu¨c¸lu¨ B, Tanidir C, Mukaddes NM, Unal F. Tactile sensitivity of normal and autistic children. Somatosens Mot Res 2007;24(1–2):21–33. [29] Cascio C, McGlone F, Folger S, Tannan V, Baranek G, Pelphrey KA, Essick G. Tactile perception in adults with autism: a multidimensional psychophysical study. J Autism Dev Disord 2008;38(1):127–37.
Please cite this article in press as: Chen F-C, Tsai C-L. A light fingertip touch reduces postural sway in children with autism spectrum disorders. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.012
GAIPOS-4570; No. of Pages 4 Gait & Posture xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
A light fingertip touch reduces postural sway in children with autism spectrum disorders Fu-Chen Chen a,*, Chia-Liang Tsai b,1 a b
Department of Recreational Sport & Health Promotion, National Pingtung University of Science & Technology, Taiwan Institute of Physical Education, Health & Leisure Studies, National Cheng Kung University, Taiwan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 22 April 2015 Received in revised form 3 September 2015 Accepted 15 September 2015
This study examined the effects of a light fingertip touch on postural control in children with autism spectrum disorders (ASD) and typically developing children (TDC). Methods: We recruited 16 children with ASD (age = 11.041 1.275), and 16 TDC (age = 10.966 1.166 years). A force platform measured postural sway in the anteroposterior (AP) and mediolateral (ML) directions under light fingertip touch (LT) and no touch (NT) conditions, with both eyes open (EO) and both eyes closed (EC). As a summary of the experimental conditions, ML sway was significantly greater in the ASD group than in the TDC group. Also, results showed a significant reduction in postural sway in the ML direction in the LT condition compared with the NT condition. These effects applied to both the EO and EC conditions. Lastly, the reduction in ML sway between the NT and LT conditions was significantly greater in the ASD than the TDC group. Conclusion: The effects of a light fingertip touch on reducing postural sway appear more efficient in children with ASD compared with TDC. These findings suggest that a light fingertip touch may be of clinical and practical importance, and provides a useful means of enhancing postural stability in children with ASD. ß 2015 Published by Elsevier B.V.
Keywords: Light touch Postural sway Autism spectrum disorders
1. Introduction Autism spectrum disorder (ASD) is a specific neurodevelopmental disorder with a prevalence estimated at approximately 1– 2% in the school-aged population [1]. Children with ASD are commonly characterized by impairments in communication, social interactions, and recognition of facial expressions [2], as well as difficulties in motor control such as gait, fine motor activities, and control of upright postural sway [3,4]. Whyatt and Craig [5] used the second edition of the Movement Assessment Battery for Children to determine motor skills in children with and without ASD. The greatest area of limitation among autistic children was static balance, highlighting their apparent problems in activities requiring postural control. Minshew et al. [6] measured the duration of one-legged standing with eyes closed, and found that children with Asperger syndrome, a subtype of ASD, maintained
* Corresponding author at: 1, Xuefu Road, Neipu Township, Pingtung County 912, Taiwan. Tel.: +886 87703202; fax: +886 87740536. E-mail addresses: [email protected] (F.-C. Chen), [email protected] (C.-L. Tsai). 1 Address: 1, Daxue Road, East District, Tainan City 701, Taiwan.
one-legged standing for a significantly shorter period than their matched peers, demonstrating the poor control of postural sway in children with ASD. In addition, Molloy et al. [7] used a force platform to examine the excursion of the center of pressure (COP) in children with ASD and typically developing children (TDC). Subjects were examined when standing with two legs on a piece of foam as well as without foam, in both eyes-open (EO) and eyesclosed (EC) conditions. The results indicated a notably greater level of postural sway for all experimental conditions in the ASD group compared with the controls. Additionally, an interaction effect showed that the absence of vision made the differences in the magnitude of postural sway between children with ASD and TDC even more prominent. Kohen-Raz et al. [8] asked individuals with and without ASD to stand on four force plates (one for each toe/ heel) with the aim of assessing the control patterns of postural sway. They found that patterns of postural control in autistic individuals were less likely to change according to age, and were less stable in the control of lateral sway than those in the control group. Based on the diversity of previous study methods and designs, and the consistent trends among their findings, it appears plausible to conclude that autistic children have deficits in the modulation of sway in an upright standing posture. In the current study, the author was particularly interested in how the poor
http://dx.doi.org/10.1016/j.gaitpost.2015.09.012 0966-6362/ß 2015 Published by Elsevier B.V.
Please cite this article in press as: Chen F-C, Tsai C-L. A light fingertip touch reduces postural sway in children with autism spectrum disorders. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.012
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control of sway in the upright posture might be modified in children with ASD, as the fundamental capacity to control posture can greatly affect children’s daily living skills [9], play, and social interactions with others [10]. The effects of light touch on modifying postural control were first reported by Holden et al. [11] in 1994, who found that the amplitude of postural sway in bi-pedal standing significantly decreased in healthy adults while applying light fingertip contact (<1 Newton (N)) on a stable surface. This ‘‘light touch paradigm’’ later became widely employed in populations vulnerable to balance problems. Cunha et al.’s study [12] indicated that applying light contact with a fingertip to a stationary bar significantly reduced postural sway in patients with cerebrovascular accidents in the anterior arterial territory. This stabilizing effect of a light fingertip touch applied in both the EO and EC conditions. More interestingly, Tremblay et al. [13] and Baccini et al.’s [14] studies demonstrated a group light touch interaction, revealing that the effects of light touch on postural stabilization were even more efficient in older adults during both comfortable standing postures (feet naturally apart and weight evenly distributed) and semitandem postures compared with young adults. This interaction effect has been widely reproduced in individuals with Down syndrome [15], unilateral anterior cruciate ligament (ACL) injury [16], and bilateral vestibular loss [17]. Collectively, previous results provide both replication and extension of Holden et al.’s work, demonstrating that light touch is an influential intervention to enhance postural stabilization for clinical populations. Although there has been many empirical studies investigating how light touch modifies postural control in individuals who have difficulties in adjusting posture, there is no research on this effect in children with ASD. Hence, the current study aimed to investigate how the use of light fingertip touch influences the responses of postural sway in children with and without ASD. In addition, research has indicated greater group differences in the control of postural sway when visual information is occluded [7]; therefore, the current study investigated further the effect of light touch in a scenario where upright postural control was challenged by removing vision. We hypothesized that children with and without ASD would reduce postural sway while applying a light fingertip touch to a stable surface in both the EO and EC conditions, and that the light touch effect would be greater in the ASD group compared with the TDC group. 2. Methods Before this study took place, participants and their guardians were informed about the experimental process and signed an informed consent form approved by the Institutional Review Board of Antai Memorial Hospital, Pingtung County, Taiwan. 2.1. Participants Sixteen children with ASD (height = 142.063 8.242 cm, weight = 40.750 7.010 kg) and 16 TDC (height = 144.063 7.937 cm, cm, weight = 41.813 7.485 kg) took part in this study. Participants were recruited using convenience sampling from eleven mainstream primary schools in Pingtung County and Taitung County, Taiwan. The diagnosis of ASDs was based on the DSM-IV-TR [2], and established by a psychologist or psychiatrist in a public hospital, and the severity level of ASD was based on both language comprehension and functioning in the social adaptive skills domain [18]. All participants in the ASD group were mildly autistic, and were enrolled in regular classroom settings with added resource support for reading and/or mathematics. The inclusion criteria were: (1) aged 9–12 years, (2) an overall IQ of at least 80, and (3) being able to understand and follow instructions. The exclusion criteria were: (1) ongoing medication, (2) severe neurological disorders (e.g.,
epilepsy, brain tumor, and cerebral palsy), (3) musculoskeletal conditions affecting postural control (e.g., sprain, and fracture), and (4) severe behavioral problems. A case–control design was employed; therefore, the two groups were matched in gender ratio (eleven males and five females in each group) and age ratio (four individuals in each age band for both groups, ASD = 11.041 1.275 years, TDC = 10.966 1.166 years). All participants were right-handed and had normal or corrected-to-normal vision. 2.2. Apparatus Participants stood on a Kistler force platform (model: 9260AA6, Winterthur, Switzerland) that collected data for COP sway with a sampling rate set at 100 Hz. The signals from the force platform were filtered by a Butterworth low pass filter at 10 Hz. In addition, participants were asked to touch a customized 5 cm 5 cm force plate (LSB 200, Futek Advanced Sensor Technology, Inc., Irvine, CA) (mounted on a tripod) that measured data for touch force in the vertical direction at a sampling rate of 1000 Hz via Labview 2012 (National Instruments, Austin, Texas, USA). We set the threshold for touch force at 1 N. Once the touch force exceeded the threshold, an alarm was triggered and a repeat trial was requested. 2.3. Procedure Participants were instructed to stand quietly and relax for 60 s in each trial, with their feet side-by-side at shoulder width on a force platform. For each participant, we marked the position of both the heel and toe to enable consistent positioning across trials. Participants looked straight ahead at a black circular mark attached on a wall 100 cm away in the EO condition, and kept their eyes shut in the EC condition. Besides, the positions of the arm were different between the no touch (NT) and the light touch (LT) conditions. Arms were relaxed at their sides in the NT condition, while the dominant (right) index fingertip applied light contact to a fixed point on the customized force plate placed laterally at about waist level in the LT condition [14]. The force of the fingertip touch applied to the plate was limited to 1 N in the vertical direction. All participants received three trials for each of the four conditions: (1) EO + NT, (2) EO + LT, (3) EC + NT, and (4) EC + LT, with the order of trials randomly assigned. Each experimental condition was practiced once before formal data collection, and there was a one-minute rest between trials. Two trials were aborted and repeated for a child due to failure to keep touch force within the threshold. Participants were coded to blind an experimenter who collected and analyzed the data. 2.4. Statistics All data were processed using the SPSS 18.0 (SPSS Inc., Chicago, IL, USA). Touch force in the vertical direction was calculated for each LT trial. We quantified the magnitude of postural sway in terms of the standard deviation of COP excursion for both anteroposterior (AP) and mediolateral (ML) directions, as this dependent variable represents the level of postural stabilization [19]. A higher value for postural sway demonstrates a lower level of stabilization, and vice versa. The average values for postural sway from three trials performed in each experimental condition were used for analysis. Data was presented as the mean SD. An independent t-test was used to determine group differences in mean touch force. Separate group (2: ASD and TDC) vision (EO and EC) and touch (NT and LT) repeated measures ANOVAs were performed for postural sway in the AP and ML directions. The effect size was quantified by calculating etasquared (h2). Both group vision and group touch interactions were found; therefore, post hoc comparisons were performed using planned t-tests with Bonferroni corrections to determine whether the
Please cite this article in press as: Chen F-C, Tsai C-L. A light fingertip touch reduces postural sway in children with autism spectrum disorders. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.012
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groups differed in the changes of sway amplitude between the two visual conditions (1) in the NT condition only, and (2) in the LT condition only, as well as between the two touch conditions (3) in the EO condition only, and (4) in the EC condition only. Statistical significance was defined as p < 0.05.
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(t(30) = 2.171, p = 0.019) (Fig. 2b). No significant effects were found for AP sway. 4. Discussion
Analysis of the kinematic data indicated a significant main effect of group (F(1, 30) = 53.616, p < 0.001, h2 = 0.641), with a larger mean ML sway in children with ASD (0.614 0.343 cm), compared to that of controls (0.335 0.094 cm). A significant main effect of vision (F(1, 30) = 14.345, p = 0.001, h2 = 0.323) was also observed, showing that ML sway was greater in the EC condition (0.556 0.307 cm) compared to the EO condition (0.393 0.241 cm). Lastly, there was a significant group vision interaction (F(1, 30) = 6.977, p = 0.013, h2 = 0.141) that the effect of the absence of vision was more prominent in children with ASD compared with TDC. Post hoc planned comparisons indicated that the ASD group increased COP sway from the EO to the EC conditions by a level greater than that of the TDC group in the NT condition (t(30) = 2.284, p = 0.015) (Fig. 1a), and in the LT condition (t(30) = 2.104, p = 0.022) (Fig. 1b). Regarding our hypotheses, the analysis of postural sway revealed a main effect of touch (F(1, 30) = 18.581, p < 0.001, h2 = 0.382), demonstrating that ML sway was significantly greater in the NT (0.558 0.337 cm) condition than in the LT (0.391 0.196 cm) condition. In addition, there was no vision touch interaction (F(1, 30) = 1.101, p = 0.302, h2 = 0.035), indicating that the effect of light touch in reducing postural sway was independent of vision conditions. Lastly, there was a significant group touch interaction (F(1, 30) = 7.567, p = 0.010, h2 = 0.123) that the effect of a fingertip touch was more prominent in children with ASD compared with TDC. Post hoc planned comparisons indicated that the ASD group reduced COP sway from the LT to the NT conditions by a level greater than that of the TDC group in the EO condition (t(30) = 2.171, p = 0.023) (Fig. 2a), and in the EC condition
This study examined the influence of light fingertip touch on the control of postural sway in children with ASD and TDC while standing with both eyes open and eyes closed. The results indicated that children with ASD swayed more than TDC. Additionally, an increased postural sway occurred when visual information was unavailable, an effect more pronounced in children with ASD than in TDC. More importantly, the new findings from the results were that a light fingertip touch reduced postural sway in children with and without ASD in both EO and EC conditions, and that autistic children benefited more from fingertip touch than TDC. Firstly, the group effect showed that children with ASD had a markedly greater amount of postural sway in the ML direction than TDC. These results were consistent with previous findings [8,20]. In a shoulder-width stance, the sway in the ML direction is mainly modulated by hip strategy, which involves the activation of both abductor and adductor muscles [21,22]. Therefore, the greater amount of ML sway may reflect a deficit, an abnormality, or a less adept ability in the use of hip strategy to maintain balance in children with ASD. In addition, the vision effect showed that removing vision resulted in a significant increase in postural sway compared to quiet standing with eyes open. This was not surprising, as visual information about both body movements and orientation in the environment are deprived in the EC condition. Lastly, the interaction effects of group vision further revealed that the vision effect is more pronounced in children with ASD than in TDC; that is, children with ASD showed more difficulties in maintaining postural balance when visual information was occluded. Molloy et al. [7] found a similar group vision interaction effect, and they suggested an overreliance on visual information to regulate body movements among children with ASD. A more recent study showed that children with ASD displayed impairments in processing proprioceptive input [23]. Thus, it seems rational that children with ASD would display a greater augmentation in postural sway compared with TDC under the condition that a lack of visual input would require individuals to depend more on proprioception. In short, the present results replicated previous studies, indicating poor control of ML sway in children with ASD, especially when vision was restricted.
Fig. 1. Mean ML sway in the EO and the EC conditions for the ASD and the TDC groups. (a) The NT condition only, (b) the LT condition only. Error bar represents standard error. EO, eyes open, EC, eyes closed, NT, no touch, LT, light touch, ASD, children with autism spectrum disorders, TDC, typically developing children. Asterisk symbols report the result of post hoc tests that groups differ in the changes of sway amplitude between the EO and the EC conditions.
Fig. 2. Mean ML sway in the NT and the LT conditions for the ASD and the TDC groups. (a) The EO condition only, (b) the EC condition only. Error bar represents standard error. EO, eyes open, EC, eyes closed, NT, no touch, LT, light touch, ASD, children with autism spectrum disorders, TDC, typically developing children. Asterisk symbols report the result of post hoc tests that groups differ in the changes of sway amplitude between the NT and the LT conditions.
3. Results 3.1. Touch force Mean touch force was 0.314 0.119 N in the ASD group, and 0.283 0.093 N in the TDC group. No difference was found between the ASD and TDC group (t(30) = 0.829, p = 0.414). 3.2. Magnitude of postural sway
Please cite this article in press as: Chen F-C, Tsai C-L. A light fingertip touch reduces postural sway in children with autism spectrum disorders. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.012
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The most remarkable finding to emerge from the current study was that a light fingertip touch is beneficial for postural stability regardless of the presence of visual information in children with ASD, an effect that is more efficient in children with ASD than TDC. Since in the NT condition, the controls had relatively lower sway amplitude that could prevent the light fingertip touch effect on reducing sway, a floor effect for the control group may explain these findings. It is worth mentioning that the interaction effects require cautious interpretation, as the percentage changes in the sway between the two touch conditions were similar for both groups: approximately 29% for the ASD group, and 26% for the TDC group. Further, even though autistic children showed a more pronounced reduction in sway resulted from light fingertip touch, they still swayed more than their control peers did in the NT condition. Earlier studies repeatedly found that individuals with difficulties in the control of postural sway (e.g., the elderly, individuals with Down syndrome, ACL injuries, or vestibular loss) could take greater advantage of the light touch effect than their matched controls in both EO and EC conditions [13–17]. The present study replicated these findings and extended them to children suffering the diagnosis of autism spectrum, disorders. Studies have demonstrated that tactile stimuli from light contact with a fixed point can provide a source of additional information about spatial reference and bodily movements with respect to the vertical, thus leading to a reduction in COP sway in standing [24–26]. Anatomically, slow adaptation receptors (i.e., Merkel’s disks and Ruffini endings) are especially sensitive to slow changes in skin stretch and skin indentation, while fast adaptation receptors (i.e., Meissner and Pacinian corpuscles) are responsible for rapid onset and offset of the ‘‘slip’’ stimulation [27]. The light touch task required participants to maintain a touch force of less than 1 N and to avoid having their fingertips slipping across the plate; therefore, both the slow and fast adaptation receptors should have been involved. Regarding the functioning of tactile sensitivity in children with ASD, Gu¨c¸lu¨ et al. [28] used vibration stimuli at frequencies of 40 Hz and 250 Hz to determine the tactile threshold of slow and fast adaptation receptors, revealing a similar threshold between children with ASD and TDC. Likewise, a recent experiment conducted by Cascio et al. [29] employed a set of ‘‘von Frey’’ filaments to test the threshold for detecting light touch. The experiment did not find any significant differences in light touch sensitivity between autistic individuals and controls. Collectively, previous studies suggest that the function of perceiving light tactile information is intact in children with ASD. Based on these findings, it is plausible to conclude that children with ASD are able to use additional tactile information to enhance postural stabilization. A possible way to put the present findings into practice is to use the light touch contact of fingertips while children with ASD are performing activities with high demands in balancing, such as standing on a foam surface, or walking a beam. For future research to test the clinical applications of a light fingertip touch, it would be essential to investigate how the use of a light fingertip touch could change postural sway responses while the risk of falling is presented to individuals with ASD. Acknowledgements This study was not funded by Ministry of Science and Technology, Taiwan (104-2410-H-020-007). Conflict of interest We declare that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript
entitled, ‘‘A light fingertip touch reduces postural sway in children with autism spectrum disorders’’.
References [1] Centers for Disease Control and Prevention. Autism spectrum disorders; 2014, Available from http://www.cdc.gov/ncbddd/autism/data.html. [2] American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 4th ed. Washington, DC: American Psychiatric Press; 2000, Text revision. [3] Green D, Charman T, Pickles A, Chandler S, Loucas T, Simonoff E, Baird G. Impairment in movement skills of children with autistic spectrum disorders. Dev Med Child Neurol 2009;51(4):311–6. [4] Ming X, Brimacombe M, Wagner G. Prevalence of motor impairment in autism spectrum disorders. Brain Dev 2007;29(9):565–70. [5] Whyatt CP, Craig CM. Motor skills in children aged 7–10 years, diagnosed with autism spectrum disorder. J Autism Dev Disord 2012;42(9):1799– 809. [6] Minshew NJ, Sung K, Jones BL, Furman JM. Underdevelopment of the postural control system in autism. Neurology 2004;63:2056–61. [7] Molloy CA, Dietrich KN, Bhattacharya A. Postural stability in children with autism spectrum disorder. J Autism Dev Disord 2003;33(6):643–52. [8] Kohen-Raz R, Volkmar FR, Cohen DJ. Postural control in children with autism. J Autism Dev Disord 1992;22(3):419–32. [9] Jasmin E, Couture M, McKinley P, Reid G, Fombonne E, Gisel E. Sensori-motor and daily living skills of preschool children with autism spectrum disorders. J Autism Dev Disord 2009;39(2):231–41. [10] Clearfield MW. Learning to walk changes infants’ social interactions. Infant Behav Dev 2011;34(1):15–25. [11] Holden M, Ventura J, Lackner JR. Stabilization of posture by precision contact of the index finger. J Vestib Res 1994;4(4):285–301. [12] Cunha BP, Alouche SR, Araujo IMG, Freitas SMSF. Individuals with post-stroke hemiparesis are able to use additional sensory information to reduce postural sway. Neurosci Lett 2012;513(1):6–11. [13] Tremblay F, Mireault AC, Dessureault L, Manning H, Seveistrup H. Postural stabilization from fingertip contact: I. Variations in sway attenuation, perceived stability and contact forces with aging. Exp Brain Res 2004;157(3):275– 85. [14] Baccini M, Rinaldi LA, Federighi G, Vannucchi L, Paci M, Mascotti G. Effectiveness of fingertip light contact in reducing postural sway in older people. Age Ageing 2007;36(1):30–5. [15] Gomes MM, Barela JA. Postural control in down syndrome: the use of somatosensory and visual information to attenuate body sway. Motor Control 2007;11(3):224–34. [16] Bonfim TR, Grossi DB, Paccola CAJ, Barela JA. Additional sensory information reduces body sway of individuals with anterior cruciate ligament injury. Neurosci Lett 2008;441(3):257–60. [17] Lackner JR, DiZio P, Jeka JJ, Horak F, Krebs D, Rabin E. Precision contact of the fingertip reduces postural sway of individuals with bilateral vestibular loss. Exp Brain Res 1999;126(4):459–66. [18] Taiwan Executive Yuan Department of Health. Levels of disabilities; 2009, Available from: http://www.doh.gov.tw/CHT2006/DM/DM2_p01.aspx? class_no=211&now_fod_list_no=6753&level_no=3&doc_no=41058. [19] Riley MA, Mitra S, Saunders N, Kiefer AW, Wallot S. The interplay between posture control and memory for spatial locations. Exp Brain Res 2012;217(1):43–52. [20] Memari AH, Ghanouni P, Gharibzadeh S, Eghlidi J, Ziaee A, Moshayedi VP. Postural sway patterns in children with autism spectrum disorder compared with typically developing children. Res Autism Spectr Disord 2013;7(2): 325–32. [21] Winter DA, Prince F, Stergiou P, Powell C. Medial-lateral and anterior-posterior motor responses associated with centre of pressure changes in quiet standing. Neurosci Res Commun 1993;12:141–8. [22] Winter DA, Prince F, Frank JS, Powell C, Zabjek KF. Unified theory regarding A/P and M/L balance in quiet stance. J Neurophysiol 1996;75:2334–43. [23] Blanche EI, Reinoso G, Chang MC, Bodison S. Proprioceptive processing difficulties among children with autism spectrum disorders and developmental disabilities. Am J Occup Ther 2012;66(5):621–4. [24] Jeka JJ, Lackner JR. Fingertip contact influences human postural control. Exp Brain Res 1994;100(3):495–502. [25] Jeka JJ, Lackner JR. The role of haptic cues from rough and slippery surfaces in human postural control. Exp Brain Res 1995;103(2):267–76. [26] Lackner JR, Rabin E, DiZio P. Stabilization of posture by precision touch of the index finger with rigid and flexible filaments. Exp Brain Res 2001;139(4):454– 64. [27] Purves D, Augustine GJ, Fitzpatrick D, Katz LC, LaMantia AS, McNamara JO, Williams SM. Neuroscience. 2nd ed. Sunderland: Sinauer Associates; 2001. [28] Gu¨c¸lu¨ B, Tanidir C, Mukaddes NM, Unal F. Tactile sensitivity of normal and autistic children. Somatosens Mot Res 2007;24(1–2):21–33. [29] Cascio C, McGlone F, Folger S, Tannan V, Baranek G, Pelphrey KA, Essick G. Tactile perception in adults with autism: a multidimensional psychophysical study. J Autism Dev Disord 2008;38(1):127–37.
Please cite this article in press as: Chen F-C, Tsai C-L. A light fingertip touch reduces postural sway in children with autism spectrum disorders. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.09.012