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      Postural stability and visual impairment: Assessing balance in children with strabismus and amblyopia

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          Abstract

          Background

          Vision plays an important role in controlling posture and balance in children. Reduced postural control has been reported in children with strabismus, but little has been reported specifically in amblyopia.

          Objective

          To investigate whether children with amblyopia have reduced balance compared to both children with strabismus without amblyopia and healthy controls.

          Study design and methods

          In this cross-sectional study, a total of 56 patients and healthy controls were recruited from the Ophthalmology and Otolaryngology Clinics at The Hospital for Sick Children, Toronto. Participants were divided into three groups: (1) 18 with unilateral amblyopia (strabismic amblyopia or mixed mechanism); (2) 16 with strabismus only without amblyopia; and (3) 22 visually-normal controls. The primary outcome was the balance performance as measured by the balance subtest of the Bruininks-Oseretsky Test of Motor Proficiency 2 [BOT2].

          Results

          The age and gender-adjusted BOT2 balance scores were significantly reduced in the amblyopia group (mean score 9.0 ± 3.1 SD) and the strabismus without amblyopia group (mean score 8.6 ± 2.4 SD) compared to visually normal controls (mean score 18.9 ± 4.2) (p<0.0001), but no statistical difference was demonstrated between the two patient groups (p = 0.907). Further subgroup analysis of the strabismus only group did not reveal a statistically significant difference in performance on BOT2 balance score between strabismus only patients with good stereopsis 60 sec or better (BOT2 mean score 9.8±3.0 SD) to patients with 3000 sec or no stereopsis (BOT2 mean score 7.9±1.7) (p = 0.144).

          Conclusion

          Our findings suggest that normal vision plays an important role in the development and maintenance of balance control. When normal binocular vision is disrupted in childhood in strabismus and/or amblyopia, not only is the vision affected, but balance is also reduced. Our results indicate that the presence of even mild binocular discordance/dysfunction (patients with intermittent strabismus and good stereopsis) may lead to postural instability.

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          Most cited references45

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          Adapting reflexes controlling the human posture.

          Doubt about the role of stretch reflexes in movement and posture control has remained in part because the questions of reflex "usefulness" and the postural "set" have not been adequately considered in the design of experimental paradigms. The intent of this study was to discover the stabilizing role of stretch reflexes acting upon the ankle musculature while human subjects performed stance tasks requiring several different postural "sets". Task specific differences of reflex function were investigated by experiments in which the role of stretch reflexes to stabilize sway doing stance could be altered to be useful, of no use, or inappropriate. Because the system has available a number of alternate inputs to posture (e.g., vestibular and visual), stretch reflex responses were in themselves not necessary to prevent a loss of balance. Nevertheless, 5 out of 12 subjects in this study used long-latency (120 msec) stretch reflexes to help reduce postural sway. Following an unexpected change in the usefulness of stretch reflexes, the 5 subjects progressively altered reflex gain during the succeeding 3-5 trials. Adaptive changes in gain were always in the sense to reduce sway, and therefore could be attenuating or facilitating the reflex response. Comparing subjects using the reflex with those not during so, stretch reflex control resulted in less swaying when the task conditions were unchanging. However, the 5 subjects using reflex controls oftentimes swayed more during the first 3-5 trials after a change, when inappropriate responses were elicited. Four patients with clinically diagnosed cerebellar deficits were studied briefly. Among the stance tasks, their performance was similar to normal in some and significantly poorer in others. Their most significant deficit appeared to be the inability to adapt long-latency reflex gain following changes in the stance task. The study concludes with a discussion of the role of stretch reflexes within a hierarchy of controls ranging from muscle stiffness up to centrally initiated responses.
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            Effect of age and sex on maturation of sensory systems and balance control.

            Maintenance of postural balance requires an active sensorimotor control system. Current data are limited and sometimes conflicting regarding the influence of the proprioceptive, visual, and vestibular afferent systems on posture control in children. This study investigated the development of sensory organization according to each sensory component in relation to age and sex. A total of 140 children (70 males, 70 females; mean age 10y [SD 4y]; age range 3y 5mo-16y 2mo) and 20 adults (10 males, 10 females; mean age 30y 6mo [SD 8y 4mo]; age range 17y 2mo-49y 1mo) were examined using the Sensory Organization Test. Participants were tested in three visual conditions (eyes open, blindfolded, and sway-referenced visual enclosure) while standing on either a fixed or a sway-referenced force platform. Mean equilibrium scores for the six balance conditions showed rapid increases and maturation ceiling levels for age-related development of the sensorimotor control system. Proprioceptive function seemed to mature at 3 to 4 years of age. Visual and vestibular afferent systems reached adult level at 15 to 16 years of age, revealing differences between young males and females. Characterizing balance impairments can contribute to the diagnostic evaluation of neuromotor disorders.
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              Visual stabilization of posture. Physiological stimulus characteristics and clinical aspects.

              Visual stabilization of posture is critically dependent on stimulus characteristics as well as on the performance of the visual system. The purpose of the present investigation was to obtain quantitative data in man by means of posturography of fore-aft and lateral body sway in relation to different visual stimulus characteristics. Visual acuity, when decreased logarithmically, causes a linearly increasing postural instability, twice as prominent for fore-aft than for lateral sway. Any measurable visual contribution for fore-aft sway ceases with an acuity lower than 0.03 and for lateral sway with an acuity lower than 0.01. The central area of the visual field as compared with the peripheral retina dominates postural control. The foveal region exhibits a powerful contribution, in particular for lateral sway. A partial but significant visual stabilization is preserved with a visual input rate between 1 to 4 Hz flicker frequency. As soon as continuous motion perception becomes involved with frequencies higher than 4 Hz, visual stabilization gradually improves with a saturation at frequencies higher than 16 Hz. Lateral body sway activity and eye-object distance are linearly related: body sway decreases with increasing distance corresponding to the linear decrease of net retinal displacement with increasing eye-object distance. Aspects of 'afferent' and 'efferent' visual motion perception, which involve fore-aft and lateral body sway differently, are evaluated. The clinical relevance is demonstrated in patients with oculomotor disturbances. The results are discussed with respect to the variety of related clinical disorders, which involve reduction in visual acuity, field defects, accommodation disturbances and ocular oscillations.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: Writing – original draft
                Role: ConceptualizationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                18 October 2018
                2018
                : 13
                : 10
                : e0205857
                Affiliations
                [1 ] Department of Ophthalmology and Vision Sciences, The Hospital for Sick Children, Toronto, Canada
                [2 ] Department of Ophthalmology, Tel Aviv Sourasky Medical Center, affiliated to the Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
                [3 ] Eye Movement and Vision Neuroscience Laboratory, The Hospital for Sick Children, Toronto, Canada
                [4 ] Department of Otolaryngology–Head and Neck Surgery, The Hospital for Sick Children, Toronto, Canada
                [5 ] Archie's Cochlear Implant Laboratory, Cochlear Implant Program and Communication Disorders, The Hospital for Sick Children, Toronto, Canada
                Moorfields Eye Hospital NHS Foundation Trust, UNITED KINGDOM
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-2757-7996
                Article
                PONE-D-18-20159
                10.1371/journal.pone.0205857
                6193669
                30335817
                9aa90a60-32f3-41c6-b438-25996d9f2d4b
                © 2018 Zipori et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 7 July 2018
                : 2 October 2018
                Page count
                Figures: 4, Tables: 4, Pages: 18
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Head
                Eyes
                Medicine and Health Sciences
                Anatomy
                Head
                Eyes
                Biology and Life Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Anatomy
                Ocular System
                Eyes
                Biology and Life Sciences
                Neuroscience
                Cognitive Science
                Cognitive Neuroscience
                Motor Reactions
                Postural Control
                Biology and Life Sciences
                Neuroscience
                Cognitive Neuroscience
                Motor Reactions
                Postural Control
                Medicine and Health Sciences
                Geriatrics
                Balance and Falls
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Vision
                Social Sciences
                Psychology
                Sensory Perception
                Vision
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Visual Acuity
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Vision
                Visual Acuity
                Social Sciences
                Psychology
                Sensory Perception
                Vision
                Visual Acuity
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Binocular Vision
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                Psychology
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                Vision
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                Social Sciences
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                Vision
                Binocular Vision
                Medicine and Health Sciences
                Surgical and Invasive Medical Procedures
                People and Places
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