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Peripheral sensory information and postural control in children with strabismus
Gait & Posture 65 (2018) 197–202
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Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Full length article
Peripheral sensory information and postural control in children with strabismus☆
T
⁎
Prasath Jayakarana, , Logan Mitchellb,c, Gillian M Johnsona a
School of Physiotherapy, University of Otago, Dunedin, New Zealand Dunedin School of Medicine, University of Otago, Dunedin, New Zealand c Eye Department, Dunedin Hospital, Southern District Health Board, New Zealand b
A R T I C LE I N FO
A B S T R A C T
Keywords: Balance Children Postural control Strabismus Sensory organisation Vision
Background: Sensory feedback from the visual system along with the vestibular and somatosensory systems is essential for the regulation of normal postural control. Children with strabismus and, therefore, with abnormal binocular vision, may have an altered perception of space and use different sets of cues to determine depth perception when compared with children without strabismus. Objective: To explore the postural control of children with and without strabismus, when the three sensory systems are challenged. Method: Forty-six children (21 with strabismus and 25 age-matched controls) aged between 5 and 10 years completed ophthalmic screening and then underwent assessment for postural control, which included Paediatric Balance Scale (PBS) and six conditions of the Sensory Organization Test (SOT). Four primary outcome measures were: PBS summary score, Equilibrium Score (ES), Strategy Score (SS) and Sensory Analysis Score of the SOT. Results: A significant difference (P < 0.05) was observed between the strabismus and non-strabismus group in the PBS and, ES and SS of SOT condition 1. The Sensory Analysis scores were significantly different (P = 0.03) between the groups for ‘Somatosensory’. Simple linear regression analysis suggested that the strabismus condition was significantly (P ≤ 0.02) associated with the PBS and, the ES and SS of condition 1, with a variance of 14.6%, 16.1% and 12.8%, respectively. Subgroup analysis suggested that age was a significant (P ≤ 0.001) correlate for balance scores in non-strabismus group (R2 ranged from 32% to 58.4%), but not for the strabismus group. Significance: Postural control in children with strabismus is not equivalent to that of children without strabismus, when their somatosensory system is challenged. Additionally, the functional balance performance of children with strabismus is lower than their counterparts without strabismus. Collectively, the results suggest that the usual improvement in balance performance with increasing age is observed in children without strabismus but not in children with strabismus.
1. Introduction
in the control of posture [3]. In the early years of child development, appropriate visual input is necessary for establishing the effective integration of the sensory systems and for context-dependent reweighting of all three sensory input [2,4,5]. Strabismus (misalignment of eyes) is a relatively common childhood ophthalmic disorder affecting 2% to 5% of preschool and school-aged children, irrespective of ethnic and geographical differences [6,7]. Childhood strabismus may lead to abnormal development of the visual system, in particular affecting binocularity (being able to fuse an image
Vision, vestibular and the somatosensory systems are three key sensory systems that play a significant role in the regulation of normal postural control [1]. The vestibular system mainly provides information about head position and orientation in space, whereas the somatosensory system is responsible for relaying feedback regarding body position and orientation. The visual system regulates the head and body in visual space [2]. These three sensory systems collectively work together
☆ Preliminary findings of this research was presented as a platform presentation at the Australia and New Zealand Strabismus Society (March, 2016) and the New Zealand Branch of the Royal Australian and New Zealand College of Ophthalmologists (May, 2016). ⁎ Corresponding author at: Centre for Health, Activity and Rehabilitation Research, School of Physiotherapy, University of Otago, 325 Great King Street, Dunedin 9016, New Zealand. E-mail address: [email protected] (P. Jayakaran).
https://doi.org/10.1016/j.gaitpost.2018.07.173 Received 21 February 2018; Received in revised form 14 June 2018; Accepted 17 July 2018 0966-6362/ © 2018 Elsevier B.V. All rights reserved.
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from both eyes to form single vision) and stereopsis (depth perception and ability to see three-dimensionally) [8]. Children with a history of constant strabismus since birth may develop compensatory cortico-visual adaptations such as suppression of visual input from the deviating eye in order to avoid diplopia (double vision) [9,10]. Children with strabismus acquired in later years of life after the visual system has matured (after about the age of 9 years) will usually suffer from diplopia (double vision) with significant functional impacts [11,12]. Investigations into postural control of adults reveal impaired vision of even one eye (with resultant impairment of binocular vision) may be associated with poor postural control in altered sensory conditions [13,14]. Thus, children with strabismus and, therefore abnormal binocular vision may have an altered perception of space and may use different sets of cues to depth perception when compared with children with normal vision [15]. Reportedly, children with strabismus have impaired postural control ability when assessed in eyes open condition while standing on a firm and foam surface [16,17], suggesting that they are more reliant on somatosensory input than their other senses. However, there is a need to further this understanding and explore how the alterations in visual processing associated with strabismus may manifest when demands are placed on the dynamic multi-sensory postural control system. The purpose of this study was to explore postural control of children with strabismus (demonstrating visual suppression from the deviating eye) and of children with normal vision (without strabismus), when the three sensory systems are challenged with a computerised dynamic posturography. It is hypothesised that the measures of postural control and functional measures of balance in children with strabismus are different to that of the children without strabismus, due to the challenges in the organisation of sensory information required for postural control, when the visual, vestibular and somatosensory systems are systematically manipulated.
Fig. 1. The six sensory testing conditions (Sensory Organization Test) of the NeuroCom Smart Equitest®. Image courtesy of Natus Medical Inc.
testing), fusion/binocularity (using Worth four-dot test), and strabismus examination. Only children with definite complete suppression of the deviating eye (as demonstrated by Worth four-dot testing) were included in the experimental group. For the control group, only children demonstrating normal visual acuity (with or without refractive correction), normal binocularity (normal sensory fusion), full stereopsis (100” to Titmus testing or better), and orthotropia for distance and near (with and without refractive correction), were included.
2. Methods 2.1. Study design Cross-sectional observational study design. 2.2. Setting
2.4. Tools and instruments
The study was undertaken at the University of Otago Balance Clinic and the Ophthalmology Outpatient Clinic of Dunedin Hospital.
2.4.1. Sensory Organization Test The Sensory Organization Test (SOT) was administered to all participants using the NeuroCom SMART EquiTest® (version 8.4.0), to evaluate the sensory weighting in postural control. The EquiTest consists of two AMTI force platforms (22.86 cm × 45.72 cm) mounted on a servo-motored base [18]. The EquiTest also included a visual surround screen which was servo-motored. The data were sampled at the default sampling rate of the SMART EquiTest® (100 Hz). The Sensory Organization Test comprised six sensory testing conditions (Fig. 1) standing with eyes open or closed on a fixed or movable platform and visual surround [19]. The sensory system available were systematically manipulated in each testing condition.
2.3. Participants Children aged between 5 and 10 years with constant strabismus (including fully accommodative esotropes who demonstrate constant esotropia when not wearing refractive correction) were recruited for the experimental group (EG) from patients who attended the Ophthalmology Outpatient Clinic of Dunedin Hospital. Age-matched participants for the control group (CG) were recruited from the community via flyers, newspaper advertisements and word-of-mouth. All children were required to be free from any known neurological impairment. Children with a history of delayed milestones, intellectual disability and/or any musculoskeletal injuries to the lower limb in the past six months were excluded from the study. Children with other ocular pathology such as congenital cataract, glaucoma, retinal or optic nerve disease or a history of penetrating/perforating ocular trauma, dense amblyopia (defined as worse than 1.0 LogMAR) were also excluded from the study. A detailed eye examination carried out by a registered orthoptist on all participants in both the experimental and control groups, including measurement of visual acuity using age-appropriate testing methods (with and without correction), stereopsis (using Titmus stereopsis
2.4.2. Paediatric Balance Scale (PBS) The 14-item balance assessment scale designed to be administered by a health care professional was used as the clinical assessment of balance [20]. The 14-items included a range of functional and balance assessment activities such as standing with eyes open or closed with feet apart/close, sit-to-stand and functional reach [20]. Each of the 14-items were scored on a scale of 0–4 where ‘0’ requires moderate to maximal physical assistance and ‘4’ is able to perform the task independently.
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2.5. Outcome measures
Table 1 Demographic details of the participants.
The main outcome measures of SOT were the Equilibrium Score and Strategy Score and, the Sensory Analysis which was derived respectively from the mean scores of the six sensory testing conditions. The Equilibrium Score is a percentage measure of balance where ‘0’ is poor balance and ‘100’ is perfect balance. The Strategy Score is a measure which indicates the strategy employed in achieving the balance, where ‘0’ is pure hip strategy and ‘100’ is pure ankle strategy. The Equilibrium and the Strategy Score of the SOT have been previously used in a paediatric population aged between 3 years 5 months and 16 years and is reported to have acceptable psychometrics [21]. The Sensory Analysis determines the relative balance performance in each sensory testing (visual, vestibular and somatosensory) and was derived from the Equilibrium Scores. The Sensory Analysis ratios were calculated from the following specific pairs of testing conditions: visual = condition 4/ condition 1; vestibular = condition 5/condition 1; somatosensory = condition 2/condition 1. The cumulative score of the PBS gives a maximum score of 56 which indicates better independence in completion of each of the assigned tasks. The PBS has been administered in children as young as 3 years and been determined to have good reliability in children with mild to moderate impairments [22].
Variables
Strabismus (n = 21)
Control (n = 25)
Statistical test¥
Age (in years) Sex (F:M) Height (m) Weight (kg) Body mass index (kg/ m2)
7.2 ± 1.79 7:14 1.2 ± 0.1 26.2 ± 6.7 16.3 ± 2.3
7.6 ± 1.77 13:12 1.3 ± 0.1 26.6 ± 6.4 15.7 ± 1.4
NS NS NS NS NS
¥
Determined by Chi-square or Independent t-test, as appropriate to the comparison; NS: non-significant. Table 2 Clinical characteristics of the children with strabismus (n = 21).
2.6. Procedure The parents/legal guardians of children responding to the call for recruitment were provided with the information sheet and consent form by the Research Administrator. All interested participants completed a preliminary screening questionnaire and underwent full orthoptic examination (visual acuity [unaided and best corrected]; binocular sensory status; ocular alignment and motility; and strabismus diagnosis) to screen for their eligibility to enter into the study. The screening process was conducted by a registered orthoptist at the Ophthalmology Outpatient Clinic, Dunedin Hospital. On a follow-up appointment all children then completed three trials each of the six SOT conditions and the PBS at the School of Physiotherapy Balance Clinic. A research assistant who was blinded to the participants group completed the balance assessment for all children. Ethical approval processes included parental consent and a locality approval was obtained from the Southern District Health Board, Dunedin. Ethical approval for the study was obtained from the University of Otago Human Ethics Committee (Reference # H15/009).
Age
Diagnosis
Alignment
Visual acuity (LogMAR)
Distance angle (prism dioptres)
Previous eye surgery
5 7 7 9 10 8 6 5 8 8 5 10 6 7 10 5 7 8 5 9 6
IET IET IET IET IET IET IET PAET PAET PAET PAET PAET PAET PAET PAET PAET PAET PAET PAET XT XT
Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Exotropia Exotropia
0.2 0.4 0.26 0.46 0.16 0.54 0.16 0.52 0.18 0.16 0.64 0 0.58 0.2 0.3 0 0.66 0.68 0.24 0.5 1
16 25 18 18 35 14 18 8 6 6 14 25 16 14 25 10 14 18 14 12 35
Yes Yes No Yes No No No No No No Yes No No No No No No NA NA No Yes
IET: infantile esotropia; PAET: partial accommodative esotropia; XT: exotropia; NA: data not available.
were not available for balance assessment due to time constraints with other commitments and were finally excluded from the study. Of the control group, all 25 participants completed the ophthalmic screening and PBS, while only 24 participants completed the SOT. One participant elected not to complete the SOT. The demographic details of the study participants are given in Table 1. The clinical characteristics of individual participants in the EG are detailed in Table 2. All participants demonstrated suppression of the deviating eye with two participants having an exotropia and all other participants with an esotropia. The descriptive statistics and the results of the statistical analysis (ttest and simple linear regression) to determine the difference between EG and CG in the outcome measures are shown in Table 3. A significant difference (P < 0.05) was observed between the EG and CG in the PBS score and, in the condition 1 of the SOT (Equilibrium Score and Strategy Score). The Sensory Analysis was only significantly different (P = 0.03) between the groups for the ‘Somatosensory’. The simple linear regression analysis suggested that the strabismus condition was significantly (P ≤ 0.02) associated with the PBS and, the Equilibrium and Strategy Scores of condition 1 with a variance of 14.6%, 16.1% and 12.8%, respectively. The subgroup analysis to determine the effect of participant age on the balance measures with simple linear regression was not significant for the EG (Table 4). However, age was a significant (P ≤ 0.001) correlate of better balance (for all variables) in the CG, with the variability ranging from 32% to 58.4%. The unstandardized β-coefficient ranged
2.7. Data analysis The mean of the three trials of the six SOT conditions and the cumulative score of the PBS was determined and retained for further analysis. The mean and standard deviation were determined for all SOT measures and the PBS. The difference between the groups for all measures were determined using the Independent t-test, with the alpha level set at p < 0.05. Simple linear regression analysis was used to estimate the effect of strabismus (independent variable) on the PBS, Equilibrium Score, Strategy Score and Sensory Analysis. The sub-group analysis to predict the effect of age on PBS, Equilibrium Score, Strategy Score and Sensory Analysis was determined with simple linear regression analysis, independently for the strabismus and control groups. The programme IBM SPSS (Version 24 for Windows) was used for all statistical analysis. 3. Results A total of 46 children, 21 with strabismus and 25 age-matched control children participated in the study. Parents of 25 children with strabismus expressed interest and completed the preliminary screening and ophthalmic examination at the hospital. However, four children 199
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Table 3 Descriptive measures and statistical test results of Sensory Organization Test and Paediatric Balance Score. Variables
Strabismus group (n = 21)
Control group (n = 25)
Statistical significance
Regression analysis
Paediatric Balance Score (0–56)
54.00 ± 2.5
55.5 ± 1.0
t (44) = −2.6; P = 0.017
F (1, 44) = 7.5; P = 0.009; R2 = 14.6%; Unstandardized β = 1.48
Sensory Organization Test (0–100) ES-Condition 1
81.0 ± 14.0
89.4 ± 3.5
t (43) = −2.7; P = 0.013
ES-Condition ES-Condition ES-Condition ES-Condition ES-Condition CS SS-Condition SS-Condition SS-Condition SS-Condition SS-Condition SS-Condition Visual Vestibular Somatosensory
81.5 ± 10.6 80.1 ± 9.7 42.2 ± 20.0 26.1 ± 18.8 28.0 ± 21.6 49.2 ± 13.5 94.0 ± 5.2 94.1 ± 3.8 95.2 ± 2.0 80.6 ± 18.9 72.9 ± 18.7 77.3 ± 15.3 0.5 ± 0.2 0.3 ± 0.2 1.0 ± 0.1
84.6 ± 7.1 83.0 ± 7.2 53.5 ± 21.2 33.9 ± 20.9 32.6 ± 21.8 55.9 ± 13.2 96.7 ± 0.9 95.4 ± 1.4 95.9 ± 1.3 88.0 ± 8.4 78.4 ± 15.2 77.8 ± 15.2 0.6 ± 0.2 0.4 ± 0.2 0.9 ± 0.1
NS NS NS NS NS NS t (43) = −2.7; P = 0.028 NS NS NS NS NS NS NS t (43) = −2.4; P = 0.03
F (1, 43) = 8.2; P = 0.006; R2 = 16.1%; Unstandardized β = 8.48 NS NS NS NS NS NS F (1, 43) = 8.2; P = 0.02; R2 = 12.8%; Unstandardized β = 2.7 NS NS NS NS NS NS NS F (1, 43) = 5.8; P = 0.02; R2 = 12.0%; Unstandardized β = 0.07
2 3 4 5 6 1 2 3 4 5 6
CS: Composite Score; ES: Equilibrium Score; SS: Strategy Score.
non-linear approach in the dynamic systems model to facilitate smooth goal-directed movements [23]. The sensory integration process is key in the effective control of posture [24] and a number of previous investigations have proposed that impairment in one of the three sensory systems either affects overall postural control and/or require necessary compensatory adaptation from other sensory systems [25–28]. The somatosensory and vestibular systems primarily perceive and interpret the motion within the body [27,28]. The visual input however provides spatial orientation and facilitates interaction with the environment, to accommodate for the real-time dynamic environmental changes [2,26,29]. The current study explored postural control of children with strabismus in dynamic sensory conditions as well as its functional dimensions (PBS). The study identified a significant difference between children with and without strabismus in condition 1 (normal standing when all sensory input is available), but no difference in any of the other sensory testing conditions. The Equilibrium Scores of condition 2 were not statistically different between the groups. The values obtained for Equilibrium Scores of conditions 1 and 2 in children with strabismus were similar; while the children without strabismus demonstrated higher scores in condition 1 than condition 2. It was also observed that the children without strabismus are likely to score at least 8.48 points more than children with strabismus, in the Equilibrium Score of condition 1. Collectively, the findings suggest that children with strabismus depend on the somatosensory input even when the visual input was available. The ‘Somatosensory’ scores of the Sensory Analysis and the regression analysis to predict strabismus condition further supports the
from 0.35 (for PBS) to 7.76 (condition 5 of the SOT). 4. Discussion The purpose of this cross-sectional study was to explore the relative weighting of the key sensory systems underpinning postural control in children with strabismus. It was found that there is a difference between the children with and without strabismus in the clinical balance assessment (PBS) and, condition 1 of the Sensory Organization Test. It was also found that the age of the child did not affect the measures of postural control in children with strabismus, whereas in children without strabismus their scores improved with increased age. Although postural control in children with strabismus has not been investigated thoroughly, several recent investigations conclude that postural control ability in eyes open conditions is generally impaired in children with strabismus [16,17]. The findings of the current study is partly in agreement with these previous reports. While previous studies have explored postural control in children with strabismus in eyes open with the subjects placed on firm and foam surfaces [16,17], this study used a suite of testing conditions purposely designed to evaluate the visual, somatosensory and vestibular systems’ influence on postural control. Nevertheless, it is acknowledged that in our study a comfortable stance on the force platform was adopted rather than the Romberg and tandem stance positions that were used in previous studies [16,17]. However, these latter positions were incorporated within the functional assessment (PBS items 8 and 9). Postural control system is seen as a continuum which may use a
Table 4 Linear regression analysis to determine the influence of age (independent variable) on Paediatric Balance Score and Sensory Organization Test measures. Within strabismus group R ; Unstandardized β Paediatric Balance Sore Sensory Organization Test ES-Condition 1 ES-Condition 2 ES-Condition 3 ES-Condition 4 ES-Condition 5 ES-Condition 6
Within control group R2; Unstandardized β
F-value; Predictor P-value
NS
42.5%; 0.35
F (1,23) = 16.99; P < 0.000
NS NS NS NS NS NS
36.5%; 58.4%; 42.3%; 39.8%; 40.5%; 32.0%;
F F F F F F
2
F-value; Predictor P-value
ES: Equilibrium score; NS: non-significant. 200
1.25 3.13 2.70 7.73 7.76 7.11
(1,23) = 12.63; (1,23) = 30.94; (1,23) = 16.12; (1,23) = 14.56; (1,23) = 14.96; (1,23) = 10.33;
P = 0.002 P < 0.000 P = 0.001 P = 0.001 P = 0.001 P = 0.004
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performance seen in children without strabismus with increasing age is lacking in children with strabismus.
hypothesis of dependency on somatosensory input in children with strabismus. Functional balance (goal-directed movements) as measured by the PBS was significantly different between the children with and without strabismus. The PBS included a range of functional tasks such as standing eyes open/closed, tandem position, turning and reaching. Although the mean cumulative score of children without strabismus was close to that of the children with strabismus, the differences observed between the groups perhaps point to the difficulties in undertaking goal-directed movements. Lions et al explored the tandem stance and Romberg stance on a force platform and reported that children with strabismus demonstrate higher sway when compared with the control group [16]. The PBS included some of these positional stance tasks and therefore the differences observed in the cumulative score may be attributed to the nature of the tasks. An active sensory-motor system is essential for optimal development of balance and function, although the associated sensory systems may develop at a slower rate than the hierarchically lower automated motor processes [21]. In the current study, the subgroup analysis examining the effect of age suggested that the postural control (PBS and Equilibrium Scores for all conditions) improves with age in children without strabismus. It is estimated that for increase in one year of age, the Equilibrium Scores will increase from 1.25 (condition 1) to 7.7 (condition 5). However, the effect of age was not significant in children with strabismus in our cohort. This suggests that the postural control in children with strabismus may not change with age. While this speculation needs to be verified with longitudinal studies, a more recent review on individuals with visual impairment concluded that the improved function of other sensory systems (proprioception and vestibular) may not contribute to better postural control and function [30].
Conflict of interest None. Funding The study was supported by the Maurice and Phyllis Paykel Trust, Auckland, New Zealand. [grant No.: 11140001 QLX]. Acknowledgements The authors acknowledge the help of Research Assistant (Dr Aleksandra Mącznik) and Dr Marina Moss, School of Physiotherapy, University of Otago. The orthoptists (Jill Beaton and Rachael Grierson, Southern District Health Board) are also thanked for their assistance in undertaking the ophthalmic screening of the participants. References [1] A. Shumway-Cook, M. Woollacott, Normal postural control, Motor Control: Theory and Practical Applications, Lippincott Williams & Wilkins, Maryland, USA, 2012, pp. 161–193. [2] R. Chiba, K. Takakusaki, J. Ota, A. Yozu, N. Haga, Human upright posture control models based on multisensory inputs; in fast and slow dynamics, Neurosci. Res. 104 (2016) 96–104. [3] C. Maurer, T. Mergner, B. Bolha, F. Hlavacka, Vestibular, visual, and somatosensory contributions to human control of upright stance, Neurosci. Lett. 281 (2000) 99–102. [4] A. Shumway-Cook, M. Woollacott, Development of postural control, Motor Control: Theory and Practical Applications, Lippincott Williams & Wilkins, Maryland, USA, 2012, pp. 195–222. [5] S.L. Westcott, L.P. Lowes, P.K. Richardson, Evaluation of postural stability in children: current theories and assessment tools, Phys. Ther. 77 (1997) 629–645. [6] K.A. Garvey, V. Dobson, D.H. Messer, J.M. Miller, E.M. Harvey, Prevalence of strabismus among preschool, kindergarten, and first-grade Tohono O’odham children, Optometry 81 (2010) 194–199. [7] A. Simpson, C. Kirkland, P.A. Silva, Vision and eye problems in seven year olds: a report from the Dunedin Multidisciplinary Health and Development Research Unit, N.Z. Med. J. 97 (1984) 445–449. [8] C. Lions, L. Colleville, E. Bui-Quoc, M.P. Bucci, Importance of visual inputs quality for postural stability in strabismic children, Neurosci. Lett. 617 (2016) 127–133. [9] A.L. Rosenbaum, A.P. Santiago, Clinical Strabismus Management, Saunders, Philadelphia, London, 1999. [10] C. Gaertner, C. Creux, M.A. Espinasse-Berrod, C. Orssaud, J.L. Dufier, Z. Kapoula, Postural control in nonamblyopic children with early-onset strabismus, Invest. Ophthalmol. Vis. Sci. 54 (2013) 529–536. [11] J.R. Economides, D.L. Adams, J.C. Horton, Perception via the deviated eye in strabismus, J. Neurosci. 32 (2012) 10286–10295. [12] J.R. Economides, D.L. Adams, J.C. Horton, Variability of ocular deviation in strabismus, JAMA Ophthalmol. 134 (2016) 63–69. [13] A. Przekoracka-Krawczyk, P. Nawrot, M. Czaińska, K.P. Michalak, Impaired body balance control in adults with strabismus, Vis. Res. 98 (2014) 35–45. [14] N. Teasdale, G.E. Stelmach, A. Breunig, H.J. Meeuwsen, Age differences in visual sensory integration, Exp. Brain Res. 85 (1991) 691–696. [15] D.L. Gallahue, J.C. Ozmun, J. Goodway, Understanding motor Development: Infants, Children, Adolescents, Adults, 7th ed., McGraw-Hil, New York, 2012. [16] C. Lions, E. Bui Quoc, S. Wiener-Vacher, M.P. Bucci, Postural control in strabismic children: importance of proprioceptive information, Front. Physiol. 5 (2014) 156. [17] C. Lions, E. Bui-Quoc, M.P. Bucci, Postural control in strabismic children versus non strabismic age-matched children, Graefe’s Arch. Clin. Exp. Ophthalmol. 251 (2013) 2219–2225. [18] NeuroCom, Balance Manager Systems Clinical Operations Guide, NeuroCom International, Inc., Seattle, WA, 2014. [19] G.P. Jacobson, C.W. Newman, J.M. Kartush, Handbook of Balance Function Testing, Mosby Year Book, 1993. [20] M.R. Franjoine, J.S. Gunther, M.J. Taylor, Pediatric balance scale: a modified version of the berg balance scale for the school-age child with mild to moderate motor impairment, Pediatr. Phys. Ther. 15 (2003) 114–128. [21] R. Steindl, K. Kunz, A. Schrott-Fischer, A.W. Scholtz, Effect of age and sex on maturation of sensory systems and balance control, Dev. Med. Child Neurol. 48 (2006) 477–482. [22] J. Zylka, U. Lach, I. Rutkowska, Functional balance assessment with pediatric balance scale in girls with visual impairment, Pediatr. Phys. Ther. 25 (2013) 460–466. [23] R.J. Peterka, Sensorimotor integration in human postural control, J. Neurophysiol.
4.1. Strengths and limitations The relative contribution of the sensory systems to postural control in children under 10 years has not been thoroughly investigated and the findings add to the body of evidence in this population. The study included a modest sample size and was of cross-sectional design hence findings have to be interpreted with due caution. Future investigations with a longitudinal study design and a larger sample size are required to confirm the results of this current investigation. Although blinded to the participants’ groups, the research assistant performing the balance and postural assessments may have been able to detect which children demonstrated strabismus, potentially leading to some bias, especially for the more subjective PBS. However, as the research assistant was not ophthalmically-trained or experienced in any way, the mild-moderate strabismus angles demonstrated by our EG (only 5/21 having a deviation greater than 20 prism dioptres) makes it unlikely the research assistant would have been aware of their deviations to a ‘casual’ glance. Finally, most children with strabismus in this study had a diagnosis of infantile esotropia or partially accommodative esotropia (the most common childhood causes of strabismus), while only two had exotropia. The suppression scotoma in childhood esotropia extends from the fovea to the disc, whereas in exotropia the entire temporal retina is suppressed. Thus these data do not allow us to comment on possible differences in balance behaviour between these two types of suppression scotoma. It should also be noted that the study included children who may have had a previous strabismus surgery, but yet with suppression from their deviating eye. 5. Conclusion The difference in sensory processing associated with postural control in children with strabismus is limited to only one of the six testing conditions; however, it also manifests in lower functional balance performance when compared to the corresponding scores of children without strabismus. Also, the usual improvement in balance 201
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input in the control of human posture, Gait Posture 3 (1995) 115–122. [28] G.G. Mary, P.T. Alpert, C. Chad, L. Margaret, K. Susan, Postural balance in young adults: the role of visual, vestibular and somatosensory systems, J. Am. Acad. Nurse Pract. 24 (2012) 375–381. [29] M.G. Wade, G. Jones, The role of vision and spatial orientation in the maintenance of posture, Phys. Ther. 77 (1997) 619–628. [30] R.B. Parreira, L.A.C. Grecco, C.S. Oliveira, Postural control in blind individuals: a systematic review, Gait Posture 57 (2017) 161–167.
88 (2002) 1097–1118. [24] F.B. Horak, Postural orientation and equilibrium: what do we need to know about neural control of balance to prevent falls? Age Ageing 35 (2006) ii7–ii11. [25] F.B. Horak, L.M. Nashner, H.C. Diener, Postural strategies associated with somatosensory and vestibular loss, Exp. Brain Res. 82 (1990) 167–177. [26] W. Paulus, A. Straube, T.H. Brandt, Visual postural performance after loss of somatosensory and vestibular function, J. Neurol. Neurosurg. Psychiatry 50 (1987) 1542. [27] G.G. Simoneau, J.S. Ulbrecht, J.A. Derr, P.R. Cavanagh, Role of somatosensory
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Contents lists available at ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Full length article
Peripheral sensory information and postural control in children with strabismus☆
T
⁎
Prasath Jayakarana, , Logan Mitchellb,c, Gillian M Johnsona a
School of Physiotherapy, University of Otago, Dunedin, New Zealand Dunedin School of Medicine, University of Otago, Dunedin, New Zealand c Eye Department, Dunedin Hospital, Southern District Health Board, New Zealand b
A R T I C LE I N FO
A B S T R A C T
Keywords: Balance Children Postural control Strabismus Sensory organisation Vision
Background: Sensory feedback from the visual system along with the vestibular and somatosensory systems is essential for the regulation of normal postural control. Children with strabismus and, therefore, with abnormal binocular vision, may have an altered perception of space and use different sets of cues to determine depth perception when compared with children without strabismus. Objective: To explore the postural control of children with and without strabismus, when the three sensory systems are challenged. Method: Forty-six children (21 with strabismus and 25 age-matched controls) aged between 5 and 10 years completed ophthalmic screening and then underwent assessment for postural control, which included Paediatric Balance Scale (PBS) and six conditions of the Sensory Organization Test (SOT). Four primary outcome measures were: PBS summary score, Equilibrium Score (ES), Strategy Score (SS) and Sensory Analysis Score of the SOT. Results: A significant difference (P < 0.05) was observed between the strabismus and non-strabismus group in the PBS and, ES and SS of SOT condition 1. The Sensory Analysis scores were significantly different (P = 0.03) between the groups for ‘Somatosensory’. Simple linear regression analysis suggested that the strabismus condition was significantly (P ≤ 0.02) associated with the PBS and, the ES and SS of condition 1, with a variance of 14.6%, 16.1% and 12.8%, respectively. Subgroup analysis suggested that age was a significant (P ≤ 0.001) correlate for balance scores in non-strabismus group (R2 ranged from 32% to 58.4%), but not for the strabismus group. Significance: Postural control in children with strabismus is not equivalent to that of children without strabismus, when their somatosensory system is challenged. Additionally, the functional balance performance of children with strabismus is lower than their counterparts without strabismus. Collectively, the results suggest that the usual improvement in balance performance with increasing age is observed in children without strabismus but not in children with strabismus.
1. Introduction
in the control of posture [3]. In the early years of child development, appropriate visual input is necessary for establishing the effective integration of the sensory systems and for context-dependent reweighting of all three sensory input [2,4,5]. Strabismus (misalignment of eyes) is a relatively common childhood ophthalmic disorder affecting 2% to 5% of preschool and school-aged children, irrespective of ethnic and geographical differences [6,7]. Childhood strabismus may lead to abnormal development of the visual system, in particular affecting binocularity (being able to fuse an image
Vision, vestibular and the somatosensory systems are three key sensory systems that play a significant role in the regulation of normal postural control [1]. The vestibular system mainly provides information about head position and orientation in space, whereas the somatosensory system is responsible for relaying feedback regarding body position and orientation. The visual system regulates the head and body in visual space [2]. These three sensory systems collectively work together
☆ Preliminary findings of this research was presented as a platform presentation at the Australia and New Zealand Strabismus Society (March, 2016) and the New Zealand Branch of the Royal Australian and New Zealand College of Ophthalmologists (May, 2016). ⁎ Corresponding author at: Centre for Health, Activity and Rehabilitation Research, School of Physiotherapy, University of Otago, 325 Great King Street, Dunedin 9016, New Zealand. E-mail address: [email protected] (P. Jayakaran).
https://doi.org/10.1016/j.gaitpost.2018.07.173 Received 21 February 2018; Received in revised form 14 June 2018; Accepted 17 July 2018 0966-6362/ © 2018 Elsevier B.V. All rights reserved.
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from both eyes to form single vision) and stereopsis (depth perception and ability to see three-dimensionally) [8]. Children with a history of constant strabismus since birth may develop compensatory cortico-visual adaptations such as suppression of visual input from the deviating eye in order to avoid diplopia (double vision) [9,10]. Children with strabismus acquired in later years of life after the visual system has matured (after about the age of 9 years) will usually suffer from diplopia (double vision) with significant functional impacts [11,12]. Investigations into postural control of adults reveal impaired vision of even one eye (with resultant impairment of binocular vision) may be associated with poor postural control in altered sensory conditions [13,14]. Thus, children with strabismus and, therefore abnormal binocular vision may have an altered perception of space and may use different sets of cues to depth perception when compared with children with normal vision [15]. Reportedly, children with strabismus have impaired postural control ability when assessed in eyes open condition while standing on a firm and foam surface [16,17], suggesting that they are more reliant on somatosensory input than their other senses. However, there is a need to further this understanding and explore how the alterations in visual processing associated with strabismus may manifest when demands are placed on the dynamic multi-sensory postural control system. The purpose of this study was to explore postural control of children with strabismus (demonstrating visual suppression from the deviating eye) and of children with normal vision (without strabismus), when the three sensory systems are challenged with a computerised dynamic posturography. It is hypothesised that the measures of postural control and functional measures of balance in children with strabismus are different to that of the children without strabismus, due to the challenges in the organisation of sensory information required for postural control, when the visual, vestibular and somatosensory systems are systematically manipulated.
Fig. 1. The six sensory testing conditions (Sensory Organization Test) of the NeuroCom Smart Equitest®. Image courtesy of Natus Medical Inc.
testing), fusion/binocularity (using Worth four-dot test), and strabismus examination. Only children with definite complete suppression of the deviating eye (as demonstrated by Worth four-dot testing) were included in the experimental group. For the control group, only children demonstrating normal visual acuity (with or without refractive correction), normal binocularity (normal sensory fusion), full stereopsis (100” to Titmus testing or better), and orthotropia for distance and near (with and without refractive correction), were included.
2. Methods 2.1. Study design Cross-sectional observational study design. 2.2. Setting
2.4. Tools and instruments
The study was undertaken at the University of Otago Balance Clinic and the Ophthalmology Outpatient Clinic of Dunedin Hospital.
2.4.1. Sensory Organization Test The Sensory Organization Test (SOT) was administered to all participants using the NeuroCom SMART EquiTest® (version 8.4.0), to evaluate the sensory weighting in postural control. The EquiTest consists of two AMTI force platforms (22.86 cm × 45.72 cm) mounted on a servo-motored base [18]. The EquiTest also included a visual surround screen which was servo-motored. The data were sampled at the default sampling rate of the SMART EquiTest® (100 Hz). The Sensory Organization Test comprised six sensory testing conditions (Fig. 1) standing with eyes open or closed on a fixed or movable platform and visual surround [19]. The sensory system available were systematically manipulated in each testing condition.
2.3. Participants Children aged between 5 and 10 years with constant strabismus (including fully accommodative esotropes who demonstrate constant esotropia when not wearing refractive correction) were recruited for the experimental group (EG) from patients who attended the Ophthalmology Outpatient Clinic of Dunedin Hospital. Age-matched participants for the control group (CG) were recruited from the community via flyers, newspaper advertisements and word-of-mouth. All children were required to be free from any known neurological impairment. Children with a history of delayed milestones, intellectual disability and/or any musculoskeletal injuries to the lower limb in the past six months were excluded from the study. Children with other ocular pathology such as congenital cataract, glaucoma, retinal or optic nerve disease or a history of penetrating/perforating ocular trauma, dense amblyopia (defined as worse than 1.0 LogMAR) were also excluded from the study. A detailed eye examination carried out by a registered orthoptist on all participants in both the experimental and control groups, including measurement of visual acuity using age-appropriate testing methods (with and without correction), stereopsis (using Titmus stereopsis
2.4.2. Paediatric Balance Scale (PBS) The 14-item balance assessment scale designed to be administered by a health care professional was used as the clinical assessment of balance [20]. The 14-items included a range of functional and balance assessment activities such as standing with eyes open or closed with feet apart/close, sit-to-stand and functional reach [20]. Each of the 14-items were scored on a scale of 0–4 where ‘0’ requires moderate to maximal physical assistance and ‘4’ is able to perform the task independently.
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2.5. Outcome measures
Table 1 Demographic details of the participants.
The main outcome measures of SOT were the Equilibrium Score and Strategy Score and, the Sensory Analysis which was derived respectively from the mean scores of the six sensory testing conditions. The Equilibrium Score is a percentage measure of balance where ‘0’ is poor balance and ‘100’ is perfect balance. The Strategy Score is a measure which indicates the strategy employed in achieving the balance, where ‘0’ is pure hip strategy and ‘100’ is pure ankle strategy. The Equilibrium and the Strategy Score of the SOT have been previously used in a paediatric population aged between 3 years 5 months and 16 years and is reported to have acceptable psychometrics [21]. The Sensory Analysis determines the relative balance performance in each sensory testing (visual, vestibular and somatosensory) and was derived from the Equilibrium Scores. The Sensory Analysis ratios were calculated from the following specific pairs of testing conditions: visual = condition 4/ condition 1; vestibular = condition 5/condition 1; somatosensory = condition 2/condition 1. The cumulative score of the PBS gives a maximum score of 56 which indicates better independence in completion of each of the assigned tasks. The PBS has been administered in children as young as 3 years and been determined to have good reliability in children with mild to moderate impairments [22].
Variables
Strabismus (n = 21)
Control (n = 25)
Statistical test¥
Age (in years) Sex (F:M) Height (m) Weight (kg) Body mass index (kg/ m2)
7.2 ± 1.79 7:14 1.2 ± 0.1 26.2 ± 6.7 16.3 ± 2.3
7.6 ± 1.77 13:12 1.3 ± 0.1 26.6 ± 6.4 15.7 ± 1.4
NS NS NS NS NS
¥
Determined by Chi-square or Independent t-test, as appropriate to the comparison; NS: non-significant. Table 2 Clinical characteristics of the children with strabismus (n = 21).
2.6. Procedure The parents/legal guardians of children responding to the call for recruitment were provided with the information sheet and consent form by the Research Administrator. All interested participants completed a preliminary screening questionnaire and underwent full orthoptic examination (visual acuity [unaided and best corrected]; binocular sensory status; ocular alignment and motility; and strabismus diagnosis) to screen for their eligibility to enter into the study. The screening process was conducted by a registered orthoptist at the Ophthalmology Outpatient Clinic, Dunedin Hospital. On a follow-up appointment all children then completed three trials each of the six SOT conditions and the PBS at the School of Physiotherapy Balance Clinic. A research assistant who was blinded to the participants group completed the balance assessment for all children. Ethical approval processes included parental consent and a locality approval was obtained from the Southern District Health Board, Dunedin. Ethical approval for the study was obtained from the University of Otago Human Ethics Committee (Reference # H15/009).
Age
Diagnosis
Alignment
Visual acuity (LogMAR)
Distance angle (prism dioptres)
Previous eye surgery
5 7 7 9 10 8 6 5 8 8 5 10 6 7 10 5 7 8 5 9 6
IET IET IET IET IET IET IET PAET PAET PAET PAET PAET PAET PAET PAET PAET PAET PAET PAET XT XT
Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Esotropia Exotropia Exotropia
0.2 0.4 0.26 0.46 0.16 0.54 0.16 0.52 0.18 0.16 0.64 0 0.58 0.2 0.3 0 0.66 0.68 0.24 0.5 1
16 25 18 18 35 14 18 8 6 6 14 25 16 14 25 10 14 18 14 12 35
Yes Yes No Yes No No No No No No Yes No No No No No No NA NA No Yes
IET: infantile esotropia; PAET: partial accommodative esotropia; XT: exotropia; NA: data not available.
were not available for balance assessment due to time constraints with other commitments and were finally excluded from the study. Of the control group, all 25 participants completed the ophthalmic screening and PBS, while only 24 participants completed the SOT. One participant elected not to complete the SOT. The demographic details of the study participants are given in Table 1. The clinical characteristics of individual participants in the EG are detailed in Table 2. All participants demonstrated suppression of the deviating eye with two participants having an exotropia and all other participants with an esotropia. The descriptive statistics and the results of the statistical analysis (ttest and simple linear regression) to determine the difference between EG and CG in the outcome measures are shown in Table 3. A significant difference (P < 0.05) was observed between the EG and CG in the PBS score and, in the condition 1 of the SOT (Equilibrium Score and Strategy Score). The Sensory Analysis was only significantly different (P = 0.03) between the groups for the ‘Somatosensory’. The simple linear regression analysis suggested that the strabismus condition was significantly (P ≤ 0.02) associated with the PBS and, the Equilibrium and Strategy Scores of condition 1 with a variance of 14.6%, 16.1% and 12.8%, respectively. The subgroup analysis to determine the effect of participant age on the balance measures with simple linear regression was not significant for the EG (Table 4). However, age was a significant (P ≤ 0.001) correlate of better balance (for all variables) in the CG, with the variability ranging from 32% to 58.4%. The unstandardized β-coefficient ranged
2.7. Data analysis The mean of the three trials of the six SOT conditions and the cumulative score of the PBS was determined and retained for further analysis. The mean and standard deviation were determined for all SOT measures and the PBS. The difference between the groups for all measures were determined using the Independent t-test, with the alpha level set at p < 0.05. Simple linear regression analysis was used to estimate the effect of strabismus (independent variable) on the PBS, Equilibrium Score, Strategy Score and Sensory Analysis. The sub-group analysis to predict the effect of age on PBS, Equilibrium Score, Strategy Score and Sensory Analysis was determined with simple linear regression analysis, independently for the strabismus and control groups. The programme IBM SPSS (Version 24 for Windows) was used for all statistical analysis. 3. Results A total of 46 children, 21 with strabismus and 25 age-matched control children participated in the study. Parents of 25 children with strabismus expressed interest and completed the preliminary screening and ophthalmic examination at the hospital. However, four children 199
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Table 3 Descriptive measures and statistical test results of Sensory Organization Test and Paediatric Balance Score. Variables
Strabismus group (n = 21)
Control group (n = 25)
Statistical significance
Regression analysis
Paediatric Balance Score (0–56)
54.00 ± 2.5
55.5 ± 1.0
t (44) = −2.6; P = 0.017
F (1, 44) = 7.5; P = 0.009; R2 = 14.6%; Unstandardized β = 1.48
Sensory Organization Test (0–100) ES-Condition 1
81.0 ± 14.0
89.4 ± 3.5
t (43) = −2.7; P = 0.013
ES-Condition ES-Condition ES-Condition ES-Condition ES-Condition CS SS-Condition SS-Condition SS-Condition SS-Condition SS-Condition SS-Condition Visual Vestibular Somatosensory
81.5 ± 10.6 80.1 ± 9.7 42.2 ± 20.0 26.1 ± 18.8 28.0 ± 21.6 49.2 ± 13.5 94.0 ± 5.2 94.1 ± 3.8 95.2 ± 2.0 80.6 ± 18.9 72.9 ± 18.7 77.3 ± 15.3 0.5 ± 0.2 0.3 ± 0.2 1.0 ± 0.1
84.6 ± 7.1 83.0 ± 7.2 53.5 ± 21.2 33.9 ± 20.9 32.6 ± 21.8 55.9 ± 13.2 96.7 ± 0.9 95.4 ± 1.4 95.9 ± 1.3 88.0 ± 8.4 78.4 ± 15.2 77.8 ± 15.2 0.6 ± 0.2 0.4 ± 0.2 0.9 ± 0.1
NS NS NS NS NS NS t (43) = −2.7; P = 0.028 NS NS NS NS NS NS NS t (43) = −2.4; P = 0.03
F (1, 43) = 8.2; P = 0.006; R2 = 16.1%; Unstandardized β = 8.48 NS NS NS NS NS NS F (1, 43) = 8.2; P = 0.02; R2 = 12.8%; Unstandardized β = 2.7 NS NS NS NS NS NS NS F (1, 43) = 5.8; P = 0.02; R2 = 12.0%; Unstandardized β = 0.07
2 3 4 5 6 1 2 3 4 5 6
CS: Composite Score; ES: Equilibrium Score; SS: Strategy Score.
non-linear approach in the dynamic systems model to facilitate smooth goal-directed movements [23]. The sensory integration process is key in the effective control of posture [24] and a number of previous investigations have proposed that impairment in one of the three sensory systems either affects overall postural control and/or require necessary compensatory adaptation from other sensory systems [25–28]. The somatosensory and vestibular systems primarily perceive and interpret the motion within the body [27,28]. The visual input however provides spatial orientation and facilitates interaction with the environment, to accommodate for the real-time dynamic environmental changes [2,26,29]. The current study explored postural control of children with strabismus in dynamic sensory conditions as well as its functional dimensions (PBS). The study identified a significant difference between children with and without strabismus in condition 1 (normal standing when all sensory input is available), but no difference in any of the other sensory testing conditions. The Equilibrium Scores of condition 2 were not statistically different between the groups. The values obtained for Equilibrium Scores of conditions 1 and 2 in children with strabismus were similar; while the children without strabismus demonstrated higher scores in condition 1 than condition 2. It was also observed that the children without strabismus are likely to score at least 8.48 points more than children with strabismus, in the Equilibrium Score of condition 1. Collectively, the findings suggest that children with strabismus depend on the somatosensory input even when the visual input was available. The ‘Somatosensory’ scores of the Sensory Analysis and the regression analysis to predict strabismus condition further supports the
from 0.35 (for PBS) to 7.76 (condition 5 of the SOT). 4. Discussion The purpose of this cross-sectional study was to explore the relative weighting of the key sensory systems underpinning postural control in children with strabismus. It was found that there is a difference between the children with and without strabismus in the clinical balance assessment (PBS) and, condition 1 of the Sensory Organization Test. It was also found that the age of the child did not affect the measures of postural control in children with strabismus, whereas in children without strabismus their scores improved with increased age. Although postural control in children with strabismus has not been investigated thoroughly, several recent investigations conclude that postural control ability in eyes open conditions is generally impaired in children with strabismus [16,17]. The findings of the current study is partly in agreement with these previous reports. While previous studies have explored postural control in children with strabismus in eyes open with the subjects placed on firm and foam surfaces [16,17], this study used a suite of testing conditions purposely designed to evaluate the visual, somatosensory and vestibular systems’ influence on postural control. Nevertheless, it is acknowledged that in our study a comfortable stance on the force platform was adopted rather than the Romberg and tandem stance positions that were used in previous studies [16,17]. However, these latter positions were incorporated within the functional assessment (PBS items 8 and 9). Postural control system is seen as a continuum which may use a
Table 4 Linear regression analysis to determine the influence of age (independent variable) on Paediatric Balance Score and Sensory Organization Test measures. Within strabismus group R ; Unstandardized β Paediatric Balance Sore Sensory Organization Test ES-Condition 1 ES-Condition 2 ES-Condition 3 ES-Condition 4 ES-Condition 5 ES-Condition 6
Within control group R2; Unstandardized β
F-value; Predictor P-value
NS
42.5%; 0.35
F (1,23) = 16.99; P < 0.000
NS NS NS NS NS NS
36.5%; 58.4%; 42.3%; 39.8%; 40.5%; 32.0%;
F F F F F F
2
F-value; Predictor P-value
ES: Equilibrium score; NS: non-significant. 200
1.25 3.13 2.70 7.73 7.76 7.11
(1,23) = 12.63; (1,23) = 30.94; (1,23) = 16.12; (1,23) = 14.56; (1,23) = 14.96; (1,23) = 10.33;
P = 0.002 P < 0.000 P = 0.001 P = 0.001 P = 0.001 P = 0.004
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performance seen in children without strabismus with increasing age is lacking in children with strabismus.
hypothesis of dependency on somatosensory input in children with strabismus. Functional balance (goal-directed movements) as measured by the PBS was significantly different between the children with and without strabismus. The PBS included a range of functional tasks such as standing eyes open/closed, tandem position, turning and reaching. Although the mean cumulative score of children without strabismus was close to that of the children with strabismus, the differences observed between the groups perhaps point to the difficulties in undertaking goal-directed movements. Lions et al explored the tandem stance and Romberg stance on a force platform and reported that children with strabismus demonstrate higher sway when compared with the control group [16]. The PBS included some of these positional stance tasks and therefore the differences observed in the cumulative score may be attributed to the nature of the tasks. An active sensory-motor system is essential for optimal development of balance and function, although the associated sensory systems may develop at a slower rate than the hierarchically lower automated motor processes [21]. In the current study, the subgroup analysis examining the effect of age suggested that the postural control (PBS and Equilibrium Scores for all conditions) improves with age in children without strabismus. It is estimated that for increase in one year of age, the Equilibrium Scores will increase from 1.25 (condition 1) to 7.7 (condition 5). However, the effect of age was not significant in children with strabismus in our cohort. This suggests that the postural control in children with strabismus may not change with age. While this speculation needs to be verified with longitudinal studies, a more recent review on individuals with visual impairment concluded that the improved function of other sensory systems (proprioception and vestibular) may not contribute to better postural control and function [30].
Conflict of interest None. Funding The study was supported by the Maurice and Phyllis Paykel Trust, Auckland, New Zealand. [grant No.: 11140001 QLX]. Acknowledgements The authors acknowledge the help of Research Assistant (Dr Aleksandra Mącznik) and Dr Marina Moss, School of Physiotherapy, University of Otago. The orthoptists (Jill Beaton and Rachael Grierson, Southern District Health Board) are also thanked for their assistance in undertaking the ophthalmic screening of the participants. References [1] A. Shumway-Cook, M. Woollacott, Normal postural control, Motor Control: Theory and Practical Applications, Lippincott Williams & Wilkins, Maryland, USA, 2012, pp. 161–193. [2] R. Chiba, K. Takakusaki, J. Ota, A. Yozu, N. Haga, Human upright posture control models based on multisensory inputs; in fast and slow dynamics, Neurosci. Res. 104 (2016) 96–104. [3] C. Maurer, T. Mergner, B. Bolha, F. Hlavacka, Vestibular, visual, and somatosensory contributions to human control of upright stance, Neurosci. Lett. 281 (2000) 99–102. [4] A. Shumway-Cook, M. Woollacott, Development of postural control, Motor Control: Theory and Practical Applications, Lippincott Williams & Wilkins, Maryland, USA, 2012, pp. 195–222. [5] S.L. Westcott, L.P. Lowes, P.K. Richardson, Evaluation of postural stability in children: current theories and assessment tools, Phys. Ther. 77 (1997) 629–645. [6] K.A. Garvey, V. Dobson, D.H. Messer, J.M. Miller, E.M. Harvey, Prevalence of strabismus among preschool, kindergarten, and first-grade Tohono O’odham children, Optometry 81 (2010) 194–199. [7] A. Simpson, C. Kirkland, P.A. Silva, Vision and eye problems in seven year olds: a report from the Dunedin Multidisciplinary Health and Development Research Unit, N.Z. Med. J. 97 (1984) 445–449. [8] C. Lions, L. Colleville, E. Bui-Quoc, M.P. Bucci, Importance of visual inputs quality for postural stability in strabismic children, Neurosci. Lett. 617 (2016) 127–133. [9] A.L. Rosenbaum, A.P. Santiago, Clinical Strabismus Management, Saunders, Philadelphia, London, 1999. [10] C. Gaertner, C. Creux, M.A. Espinasse-Berrod, C. Orssaud, J.L. Dufier, Z. Kapoula, Postural control in nonamblyopic children with early-onset strabismus, Invest. Ophthalmol. Vis. Sci. 54 (2013) 529–536. [11] J.R. Economides, D.L. Adams, J.C. Horton, Perception via the deviated eye in strabismus, J. Neurosci. 32 (2012) 10286–10295. [12] J.R. Economides, D.L. Adams, J.C. Horton, Variability of ocular deviation in strabismus, JAMA Ophthalmol. 134 (2016) 63–69. [13] A. Przekoracka-Krawczyk, P. Nawrot, M. Czaińska, K.P. Michalak, Impaired body balance control in adults with strabismus, Vis. Res. 98 (2014) 35–45. [14] N. Teasdale, G.E. Stelmach, A. Breunig, H.J. Meeuwsen, Age differences in visual sensory integration, Exp. Brain Res. 85 (1991) 691–696. [15] D.L. Gallahue, J.C. Ozmun, J. Goodway, Understanding motor Development: Infants, Children, Adolescents, Adults, 7th ed., McGraw-Hil, New York, 2012. [16] C. Lions, E. Bui Quoc, S. Wiener-Vacher, M.P. Bucci, Postural control in strabismic children: importance of proprioceptive information, Front. Physiol. 5 (2014) 156. [17] C. Lions, E. Bui-Quoc, M.P. Bucci, Postural control in strabismic children versus non strabismic age-matched children, Graefe’s Arch. Clin. Exp. Ophthalmol. 251 (2013) 2219–2225. [18] NeuroCom, Balance Manager Systems Clinical Operations Guide, NeuroCom International, Inc., Seattle, WA, 2014. [19] G.P. Jacobson, C.W. Newman, J.M. Kartush, Handbook of Balance Function Testing, Mosby Year Book, 1993. [20] M.R. Franjoine, J.S. Gunther, M.J. Taylor, Pediatric balance scale: a modified version of the berg balance scale for the school-age child with mild to moderate motor impairment, Pediatr. Phys. Ther. 15 (2003) 114–128. [21] R. Steindl, K. Kunz, A. Schrott-Fischer, A.W. Scholtz, Effect of age and sex on maturation of sensory systems and balance control, Dev. Med. Child Neurol. 48 (2006) 477–482. [22] J. Zylka, U. Lach, I. Rutkowska, Functional balance assessment with pediatric balance scale in girls with visual impairment, Pediatr. Phys. Ther. 25 (2013) 460–466. [23] R.J. Peterka, Sensorimotor integration in human postural control, J. Neurophysiol.
4.1. Strengths and limitations The relative contribution of the sensory systems to postural control in children under 10 years has not been thoroughly investigated and the findings add to the body of evidence in this population. The study included a modest sample size and was of cross-sectional design hence findings have to be interpreted with due caution. Future investigations with a longitudinal study design and a larger sample size are required to confirm the results of this current investigation. Although blinded to the participants’ groups, the research assistant performing the balance and postural assessments may have been able to detect which children demonstrated strabismus, potentially leading to some bias, especially for the more subjective PBS. However, as the research assistant was not ophthalmically-trained or experienced in any way, the mild-moderate strabismus angles demonstrated by our EG (only 5/21 having a deviation greater than 20 prism dioptres) makes it unlikely the research assistant would have been aware of their deviations to a ‘casual’ glance. Finally, most children with strabismus in this study had a diagnosis of infantile esotropia or partially accommodative esotropia (the most common childhood causes of strabismus), while only two had exotropia. The suppression scotoma in childhood esotropia extends from the fovea to the disc, whereas in exotropia the entire temporal retina is suppressed. Thus these data do not allow us to comment on possible differences in balance behaviour between these two types of suppression scotoma. It should also be noted that the study included children who may have had a previous strabismus surgery, but yet with suppression from their deviating eye. 5. Conclusion The difference in sensory processing associated with postural control in children with strabismus is limited to only one of the six testing conditions; however, it also manifests in lower functional balance performance when compared to the corresponding scores of children without strabismus. Also, the usual improvement in balance 201
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input in the control of human posture, Gait Posture 3 (1995) 115–122. [28] G.G. Mary, P.T. Alpert, C. Chad, L. Margaret, K. Susan, Postural balance in young adults: the role of visual, vestibular and somatosensory systems, J. Am. Acad. Nurse Pract. 24 (2012) 375–381. [29] M.G. Wade, G. Jones, The role of vision and spatial orientation in the maintenance of posture, Phys. Ther. 77 (1997) 619–628. [30] R.B. Parreira, L.A.C. Grecco, C.S. Oliveira, Postural control in blind individuals: a systematic review, Gait Posture 57 (2017) 161–167.
88 (2002) 1097–1118. [24] F.B. Horak, Postural orientation and equilibrium: what do we need to know about neural control of balance to prevent falls? Age Ageing 35 (2006) ii7–ii11. [25] F.B. Horak, L.M. Nashner, H.C. Diener, Postural strategies associated with somatosensory and vestibular loss, Exp. Brain Res. 82 (1990) 167–177. [26] W. Paulus, A. Straube, T.H. Brandt, Visual postural performance after loss of somatosensory and vestibular function, J. Neurol. Neurosurg. Psychiatry 50 (1987) 1542. [27] G.G. Simoneau, J.S. Ulbrecht, J.A. Derr, P.R. Cavanagh, Role of somatosensory
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