Proprioception and vestibular alterations affect postural control in children with mild autism : A pilot study

Individuals diagnosed with Autism Spectrum Disorder (ASD) Background: exhibit some type of motor control impairment, for instance, motor apraxia and history of gross motor delay that could lead to increased risk of fall. This pilot research was designed to assess and characterize static postural stability and create a starting point to better understand and describe postural control in children with mild autism. We measured static postural control with center of pressure (COP) Method: displacement in 10 children with mild autism during eight sensory conditions that challenge and cancel the visual, proprioceptive and vestibular systems. Our results showed that children with autism demonstrated increased Results: postural sway in response to challenges to the proprioceptive and vestibular systems. Therefore, under appropriate, challenging conditions, static Conclusion: postural control instability can be detected in children with mild autism.


Introduction
Autism is a developmental disorder characterized by deficits in language, social skills, environment interaction and motor function development; although the latter has not been thoroughly researched (Mari et al., 2003) (Fournier et al., 2010a).According to the "Diagnostic and Statistical Manual of Mental Disorders" (DSM-IV), classic autism, as well as Asperger's disorder, infantile disintegrative disorder and generalized not specified developmental disorder is now all classified under the Autism Spectrum Disorder (ASD) (American Psychiatric Association, 2013).
Individuals diagnosed with Autism Spectrum Disorder (ASD) have been shown to have deficiencies in motor control such as motor apraxia, clumsiness, reduced ankle movement, history of gross motor delay, and toe-walking (Ming et al., 2007;Teitelbaum et al., 1998).These deficiencies could lead to a risk of falls and lower quality of life in these individuals.Kohen-Raz et al. (1992) found that children with autism have more difficulty maintaining postural control due to the gait pattern (walk on tip-toes) that they exhibit regularly.Also, children with ASD have difficulty in the integration of sensory information.Specifically, deficits may exist in the processing of vestibular and proprioceptive information when compared to children with normal development (Blanche et al., 2012;Fournier et al., 2010b;Shumway-Cook & Woollacott, 2001a).
The literature shows concurrent limitations and consensus in which sensory system specifically alter postural control in children with autism.Nevertheless, problems in motor control may be caused by some deficit in postural control mechanisms (visual, proprioceptive and vestibular systems) or problems in the integration/adaptation of these systems (Blanche et al., 2012;Fournier et al., 2010a;Fournier et al., 2010b;Kern et al., 2007;Kohen-Raz et al., 1992;Molloy et al., 2003;Shumway-Cook & Woollacott, 2001b).
Consequently, it is necessary to study and describe how the sensory systems relate to postural control in children with ASD.The primary purpose of our research project is to identify postural deficiencies that may exist and to describe postural control in children who have autism with the objective to ascertain how these systems react when challenged or altered.Therefore, we hypothesized that when standing still (double legged), children with ASD will exhibit the following: 1) increased sway in one or more of the balance conditions, 2) challenges of the vestibular and proprioceptive systems will increase center of pressure (COP), and sway in a mediolateral (M-L) direction.
The long term goals of this pilot study are to provide the foundation to enhance the understanding of postural control, create new inquiry projects to help comprehend postural control in the different categories of autism and aid in developing targeted interventions for fall prevention in children with autism.

Materials and methods
Parents of children diagnosed with mild ASD who were interested in the study called the number on the recruitment flyer.The PI spoke with the parent to assess whether their child qualified for the study based on the following inclusion and exclusion criteria.The inclusion criteria were: (1) children from 7-12 years of age, male or female, (2) mild ASD diagnosis (as determined by a medical doctor (3) (5) capable of ambulating independently.Exclusion criteria were: (1) children with additional neurological problems, (2) children with visual problems, (3) children unable to tolerate walking or standing barefoot, (4) children who have fallen three or more times in the last three months, and (5) children with vestibular problems.We assessed the vestibular system utilizing the Fukuda Stepping Test (Fukuda, 1959).After hearing the qualifications, if the parent wished to volunteer their child for the study, an appointment was made for them to come to the Biomechanical Laboratory.
Ten children, diagnosed with a mild ASD that fulfilled the inclusion criteria participated in this study (Table 1).This project was conducted in the Biomechanical Laboratory of the Medical Science Campus of the University of Puerto Rico.The recruitment of participants was performed by posting flyers at the University of Puerto Rico, Medical Science Campus and other Centers in the Metropolitan Area.
After parents and children had given written consent, the following steps were followed: (1) A preparatory protocol was performed to familiarize the children with the study protocol, the staff and the children spent 5 minutes watching photos related to the materials, equipment, workplace, and team members.(2) Anthropometric measurements were taken (weight and height) as descriptive measures and to calibrate the pressure mat, MatScan.
(3) The Fukuda test was performed to rule out vestibular system impairment (Fukuda, 1959).

Balance assessment protocol
To assess balance, we used a MatScan TM pressure mat (TekScan, Boston, MA).This mat contains sensors that measure body sway in centimeters (cm), anteriorly (forward), posteriorly (backward) (A-P), or laterally (sideways) (L-R).The mat provides information about the direction and amount of sway as well  1) eyes open (EO MAT) -evaluates visual and vestibular system while the proprioceptive system is challenged and, (2) eyes closed (EC MAT) -removes visual input, evaluates the vestibular system and alters the proprioceptive system.( 3) eyes open while moving the head up and down (EO MAT HUD) -evaluates visual system modifying the input of proprioceptive and vestibular systems, (4) eyes closed while moving the head up and down (EC MAT HUD) -evaluates altered proprioceptive and, vestibular systems in the absence of visual system.

Data analysis
The software used to analyze all the information was the statistical package for the social science version 19 (SPSS).P values <.05 were accepted as statistically significant.This study's focus was to identify postural control deficiency in children diagnosed with mild ASD.We assessed how participants reacted when exposed to a stable and unstable surface and how altered proprioceptive information impacts postural control.We used a ANOVA analyses to compare differences in COP and sways (AP and ML) within the eight balance sensory conditions.A Bonferroni post hoc analysis was used to identify the specific variables or parameters to which significant differences could be attributed.

Results
We recruited ten children diagnosed with mild ASD, eight male and two female with an age average of 8.58.5± 1.433 (anthropometric information are in Table 1).
We compared postural control between firm (stable) and foam (unstable) surface to identify postural instability.In detail, we used eye open on a firm surface test as a baseline and compared to the other three (eyes closed, eyes open head up and down, and eyes closed head up and down) conditions.Likewise, we examined eyes open on foam (unstable) to the other three conditions on the foam.
Results of the comparison of average COP and sway movement under four different conditions (EO, EC, EO HUD, and HUD EC) on a stable surface and the mean excursion of the COP and sways under the same four conditions on an unstable surface are shown in Table 2.In our study, the most significant results were that children showed significantly more oscillations (instability) on the comparison of unstable surface versus the stable condition.

Discussion
The purpose of our study was to identify postural control deficiency, compare how participants react when exposed to a stable and unstable surface, and to describe how each system responds when altered.We identified postural instability and the systems that might be responsible for these alterations in these children with mild autism.Therefore, we discussed our findings in the following working hypothesis.
Hypothesis: children with ASD will exhibit altered postural instability in one or more of the balance conditions.Under stable and unstable conditions, we identified postural instability on unstable condition.Similar to Molloy and colleagues ( 2003) we found that children with ASD exhibited increased oscillations when standing on the foam, or unstable surface, compared to a stable platform, thus showing postural alterations (Molloy et al., 2003).Therefore, our hypothesis is accepted.
Participants showed increased COP excursion (postural instability) on the stable surface under EC HUD condition (when the proprioceptive is the only unaltered system, however not significant at this point.It is possible that the proprioceptive system could not compensate correctly when the input of the visual was canceled, and when altering the vestibular input, to maintain postural control. During stable surface under all conditions, AP oscillations predominated.Usually, this is expected because human oscillations occur in AP axis due to knee and ankle joints, similar to an inverted pendulum, thus allowing slight medio-lateral movements (Shumway-Cook & Woollacott, 2001b).However, when these oscillations exceed the stability limits, it might be due to weakness in the muscles of the lower extremities or delay of the integration or adaptation of the proprioceptive system (Shumway-Cook & Woollacott, 2001b).
Postural control on an unstable surface shows that our participants exhibit greater COP excursion during the EO MAT HUD and EC MAT HUD condition.This condition was designed to evaluate the role of the visual system input.Therefore, we believe that the visual system was not capable helping to maintain proper balance when the vestibular and proprioceptive were stimulated.However, we believe that the visual system was not affected; it is just not enough to compensate for the other two tested systems.While the participants moved their heads up and down (in a coordinated fashion), they were requested to gaze at a fixed point during the entire task.Because of their low capability of concentration, it was not possible for these children to stare at a fixed point during the whole task.Our participants (when challenging the proprioceptive system) exhibited a trend of movements to the right and anterior directions showing further instability in each one of the tests.Similarly, when altering the visual and vestibular inputs, it was observed a tendency to move anterior and to the right.These results lead us to believe that proprioceptive input in children with autism could interfere with the ability of this system to send the correct information to maintain proper postural stability.(Blanche et al., 2012;Fournier et al., 2010b;Hansson et al., 2010;Shumway-Cook & Woollacott, 2001b).Contrary to a stable surface, ML oscillations predominated under all conditions on the unstable surface (Table 2).One possible explanation for this event may be that the alteration of the proprioceptive system is responsible for the adjustment of the activation of the musculature of the trunk, thus causing instability in the ML direction (Blanche et al., 2012;Fournier et al., 2010b;Hansson et al., 2010).Another possible justification might be related to balance control in the ML direction, mainly occurring due to weakness at the hip and trunk areas.Therefore, we believe that weakness in the trunk and hip muscles and deficits in weight bearing distribution might cause an increase in ML oscillations (O'sullivan, 2007;Shumway-Cook & Woollacott, 2001b).
In conclusion, children with mild autism spectrum disorder showed postural instability on the stable and unstable surfaces.
Our study established that these children exhibited an increase in oscillations both for the AP and ML directions; however, the direction varied depending on what systems were altered.Thus, under controlled test conditions, children with autism exhibit diminished postural control or postural instability due to vestibular and proprioceptive alteration and postural instability in an ML direction.If applicable, is the statistical analysis and its interpretation appropriate?I cannot comment.A qualified statistician is required.

Are all the source data underlying the results available to ensure full reproducibility? Yes
Are the conclusions drawn adequately supported by the results?Partly No competing interests were disclosed.

Competing Interests:
Referee Expertise: Biomechanics, Quantitative posturagraphy Gait assessment, bone fragility quantification, effect of low level toxic chemicals on motor functions I have read this submission.I believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.
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Table 1 . Demographic and Anthropometric Information of Participants.
The data collected with the pressure mat, center of pressure (cm 2 ) and sway (cm), was analyzed with Tekscan Sway Analysis Module (SAM) software designed for this purpose.This test was used to determine the effectiveness of an individual's ability to use different sensory stimuli to examine the balancing of the body while standing under different conditions.The MatScan has an intra-rater reliability of .96-1.0 (Zammit et al., 2010).
Total 10 35.11 ± 8.67 8.5 ± 1.431.38 ± 0.10 kg: kilogram; m: meter; SD: standard deviation as area or center of pressure (COP).tem and alters vestibular input, (4) eyes closed while moving the head up and down (EC HUD) -evaluates the effect of removing visual information, and the vestibular input being altered.The subjects then performed the same four tasks, this time standing on an unstable platform (high quality closed cell foam 19 inches long x 15 inches width x 2.25 inches) with the purpose of altering the proprioceptive input and increasing dependence on the visual and vestibular systems.(

Table 2 . Mean and Standard Deviation of COP and AP & ML sways of the Stable and Unstable Surfaces Comparisons. TESTS Mean ± SD
(Rosario et al., 2018)rol pressure data Pressure data collected was CoP, center of Pressure displacement in centimeters squared and sways.Antero-posterior (AP) and laterally sideways data was measured in centimeters.All measurements were collected during the 8 sensory balance conditions.Eyes open, eyes closed, eyes open head movements and eyes closed head movements.Same as the previous test were analyzed, however on standing on a foam/unstable surface.10.5256/f1000research.14179.d197064(Rosarioet al., 2018)