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Relative importance of vision and proprioception in maintaining standing balance in people with multiple sclerosis
Multiple Sclerosis and Related Disorders 39 (2020) 101901
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Multiple Sclerosis and Related Disorders journal homepage: www.elsevier.com/locate/msard
Original article
Relative importance of vision and proprioception in maintaining standing balance in people with multiple sclerosis
T
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Feng Yanga, , Xinyue Liub a b
Department of Kinesiology and Health, Georgia State University, 125 Decatur St, Suite-137, Atlanta, GA 30303, USA School of Mathematics, Georgia Institute of Technology, Atlanta, USA
A R T I C LE I N FO
A B S T R A C T
Keywords: Romberg's quotient Proprioception quotient Fall prevention Posturography test
Background: Balance impairment is common and a risk factor of falls in people with multiple sclerosis (MS). The purpose of this study was to evaluate the relative importance between vision and proprioception in maintaining standing body balance among individuals with MS compared with healthy individuals. Methods: Thirty people with MS (the mean ± standard deviation of the Patient Determined Disability Steps: 3.62 ± 1.67 out of 8) and 25 healthy adults participated in this cross-sectional study. They underwent a static posturography test, consisting of three sensory feedback conditions: eyes open on a firm surface, eyes closed on a firm surface, and eyes open on a compliant surface. Their standing balance performance, quantified by the 95% confidence ellipse area and the total length of the center of pressure trajectory during each sensory condition, was calculated based on the ground reaction force data. The Romberg's quotient (the ratio of the center of pressure measurements on the firm surface between eyes open and eyes closed conditions) and proprioception quotient (the ratio of the center of pressure measurements with eyes open between firm and compliant standing surfaces) were calculated and compared between groups. Results: Persons with MS demonstrated significantly larger postural sway under all three sensory conditions than their healthy counterparts. The reliance on the vision and proprioception systems in maintaining body balance was greater among people with MS compared to healthy adults. Both groups similarly relied more on the proprioceptive input to keep body balance than on the vision. Conclusions: Like healthy individuals, persons with MS rely more on proprioception to maintain body balance than vision. Our findings could provide preliminary reference for optimizing balance improving programs aimed at person with MS.
1. Introduction Multiple sclerosis (MS) is a progressive autoimmune disease of the central nervous system (CNS) (Campbell et al., 2014). With an average onset age between 20–40 years, one's most productive life segment, MS is the predominant chronic, non-traumatic neurological disorder of young adults and has severe health and socioeconomic consequences (Zwibel, 2009). Standing balance is a fundamental requirement of conducting daily activities. Humans maintain body balance through integrating the uninterrupted signal flow from the vestibular, visual, and proprioceptive systems (Fitzpatrick and McCloskey, 1994). Due to the MS-induced damages throughout the CNS, MS could affect one or more of these signal pathways and impair the capacity to maintain body balance (Cattaneoand Jonsdottir, 2009). Balance deficit is a serious challenge
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Corresponding author. E-mail address: [email protected] (F. Yang).
https://doi.org/10.1016/j.msard.2019.101901 Received 11 September 2019; Accepted 19 December 2019 2211-0348/ © 2019 Elsevier B.V. All rights reserved.
faced by people with MS (Kalron and Achiron, 2013) and impacts about three-quarters of people with MS over the disease course (Prosperini et al., 2010). Balance impairment restricts mobility among persons with MS. Mobility limitations adversely affect the employment, functional independence, social participation, and quality of life in people with MS (Kwiatkowski et al., 2014; Bethoux and Bennett, 2011). The compromised body balance also increases the likelihood of falls (Cameron and Lord, 2010), which can negatively affect this population (Matsuda et al., 2012; Mazumder et al., 2015). Therefore, it is imperative to develop effective interventions for improving body balance among people with MS. As standing balance is dependent upon three sensory systems, improvements in the function and capacity of these systems could ameliorate imbalance. From a practical viewpoint, it is useful to determine the relative importance between these three systems in maintaining the
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standing balance, which can inform the design of effective balance training interventions to target the most critical sensory systems. For example, a previous study reported that a visuo-proprioceptive training program improves body balance among persons with MS (Prosperini et al., 2010). Since this training program involved both visual and proprioceptive components simultaneously, it is impossible to detect which component is more important or effective to improve body balance. Identifying the relative dependency of standing balance on these sensory systems also has theoretical significance because it helps the research community understand the process underlying the control of standing balance in people with MS. However, the relative importance of these systems in keeping body balance in people with MS remains unknown. This may foster less than optimal interventions for balance training in MS and thus an inefficient use of the limited resources in MS rehabilitation. As a first attempt, this study identified the relative importance between visual and proprioceptive systems in maintaining body balance in people with MS compared to age- and gender-matched healthy individuals. Posturographic measurement was used to gauge standing balance under three sensory conditions: eyes open, eyes closed, and standing on a foam pad with eyes open. Body balance, characterized by the 95% confidence sway area and the total length of the center of pressure (COP) trajectory, was calculated. To determine the reliance of body balance on the visual system, we adopted Romberg's quotient as the ratio of the balance measurement on a static surface under eyes closed condition to the eyes open condition (Howcroft et al., 2017). A similar measure, proprioception quotient, was established as the ratio of the balance performance with eyes open between the foam and static surface conditions. This quotient assesses the dependence of body standing balance on the proprioceptive system. As both quotients used the measurement under eyes-open condition as the common reference, the comparison between them should provide insight into the relative importance between visual and proprioceptive systems to maintain body balance. We hypothesized that the reliance on both the visual and proprioceptive systems among people with MS would be greater than the healthy controls in maintaining standing balance. This could be confirmed if both quotients being higher among individuals living with MS than healthy individuals. We further hypothesized that the reliance on the proprioceptive system in maintaining balance is higher than that of the visual system in both persons with MS and healthy individuals. This hypothesis would be supported if the Romberg's quotient is greater than the proprioception quotient in both populations. The findings from this study could shed light on the control strategy of standing balance among people with MS and provide useful reference for designing effective body balance training approaches.
Table 1 Demographic information for both the healthy control (HC) and multiple sclerosis (MS) groups. Parameter
HC (n = 25)
MS (n = 30)
p value
Age (years) Female (%) Height (cm) Mass (kg)
50.6 ± 13.3 18 (72.0) 164.9 ± 10.4 75.9 ± 15.4
50.8 ± 14.4 23 (76.7) 164.2 ± 7.7 73.5 ± 14.5
0.958 0.762* 0.795 0.562
Patient Determined Disability Steps for MS: 3.62 ± 1.67. Disease duration for MS: 14.0 ± 10.6 years. ⁎ : Fisher's exact test used.
excluded if they had a neurological disorder, ambulation dysfunction, or previous surgery involving lower extremities or were pregnant. All participants gave written informed consent approved by the Institutional Review Board before participation. 2.2. Posturography test Static posturography assesses postural control which involves responses to gravity and relatively subtle, self-initiated disturbance to body balance (Visser et al., 2008). This assessment is typically achieved by measuring the spontaneous movement of the COP beneath the feet as participants stand on a force plate. In this current study, a 30-second trial was collected in sequence for each of the three following conditions: eyes open on a static surface, eyes closed on the static surface, and eyes open while standing on a block of compliant foam (10-cm thick, Aeromat Fitness Product, CA). Participants were told to hold the body as still as possible under all conditions with feet shoulder width apart and arms resting at the sides in a comfortable position. The ground reaction force during the three trials were acquired by a force plate (AMTI, ORT6-1000) at 600 Hz. During eyes open conditions, participants looked at a fixed point about 4 m in front of them. A 2minute rest was administered between conditions to reduce the possible effect of fatigue on our results. 2.3. Data reduction and analysis Ground reaction force data was low-pass filtered at 25 Hz with a fourth-order Butterworth filter (Pai et al., 2006). The COP trace during each trial was then determined by the filtered ground reaction force (Fig. 1). Based on the determined COP trajectory, the 95% confidence ellipse area (A) which encloses 95% of COP trajectory (Schubert and Kirchner, 2014) and the total COP trajectory length (L) (Howcroft et al., 2017) were calculated (Fig. 1). These two parameters were chosen as they have been widely used in previous studies concerning people with MS (Kalron and Achiron, 2013; Cameron and Lord, 2010). Then, Romberg's quotient (RQ) and proprioception quotient (PQ) were computed corresponding with the conditions of vision removal and proprioception removal according to the two COP measurements (A and L):
2. Materials and methods In this cross-sectional study, people with MS and healthy individuals were assessed for their balance during quiet stance under three sensory conditions: normal, vision removal, and proprioception removal. The reliance of balance control on the visual and proprioceptive systems were then calculated as the Romberg's quotient and proprioception quotient, respectively. The relative importance of visual and proprioceptive systems in maintaining standing balance was evaluated. 2.1. Participants
RQ =
AEC L or EC AEO LEO
PQ =
AFM L or FM AEO LEO
where, EO, EC, and FM respectively represents the sensory conditions of eyes open, eyes closed, and standing on the foam. A quotient value greater than one indicates that the removal of the respective sensory system would worsen the balance performance in comparison with the EO condition, reflecting the reliance on the corresponding sensory feedback system in keeping the upright body posture. The greater the quotient value, the higher the dependence on the respective sensory system. Since both quotients were defined on a common basis – the balance performance during EO condition – the comparison between
Thirty people with MS and 25 healthy adults were recruited (Table 1). To be enrolled into the MS group, participants needed to have a neurologist-confirmed diagnosis of MS; a score of ≤6.5 on the Patient Determined Disease Steps; ability to stand for at least 30 s independently; and no significant relapse within the past eight weeks. Participants must be free from other major general medical or surgical disorders or pregnancy. For healthy individuals, participants were 2
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Fig. 1. Schematic plot of the center of pressure (COP) trajectory under three sensory feedback conditions for both healthy control (HC) and multiple sclerosis (MS) groups. The three conditions include eyes open on a firm surface, eyes closed on a firm surface, and standing on a foam with eyes open. X axis denotes the mediolateral direction and Y represents the anteroposterior direction. The upper panel (subplots: a, b, and c) is for HC under the three conditions and the lower panel (d, e, and f) is for the MS. The area enclosed by the ellipse defines the 95% confidence ellipse area of the COP trajectory in mm2. The distance covered by the whole COP trajectory is the total COP path length in mm.
these two quotients could reflect the relative importance of these two sensory systems (vison vs. proprioception) in sustaining standing posture. A custom Matlab (Mathworks, MA) script was developed to conduct all calculations. 2.4. Statistical analysis Normality of each variable was checked using the Shapiro-Wilk test. If nonnormality was found, a logarithm transform would be executed. Differences in the demographic characteristics between groups were analyzed by a χ2 test for the categorical variable and independent samples t-tests for continuous variables. Independent t-tests were also used to compare the COP sway area and path length between groups under all three sensory conditions. Analyses of variance (ANOVA) with repeated measures was used to compare both quotients between groups (between-subject factor: MS vs. health) and systems (within-subject factor: vision vs. proprioception or RQ vs. PQ). Any significant main or interaction effect was further analyzed by appropriate post-hoc tests. All statistical analyses were performed using SPSS 24.0 (IBM, NY), and a significance level of 0.05 was applied throughout.
Fig. 2. The comparison of the center of pressure a) 95% confidence ellipse area and b) total path length between the healthy control (HC) and multiple sclerosis (MS) groups under three sensory conditions: eyes open (EO), eyes closed (EC), and standing on a foam (FM). Both measurements of the center of pressure are significantly larger among people with MS than in healthy individuals under all three conditions (***: p < 0.001).
3. Results 3.1. Measurements of COP area and length Under all three sensory conditions, both the COP sway area and the total COP path length in the MS group were significantly greater than the ones among healthy individuals (Fig. 2, p < 0.001 for the betweengroup comparison of both measures under three conditions). The average RQ and PQ for both COP measurements in the two groups were greater than one, indicating that the removal of vision or proprioception input increases the measurements of the COP sway area and trace length (Fig. 3).
the healthy controls (p = 0.007 for RQ and p = 0.026 for PQ). Within either group, the PQ was significantly greater than the RQ (p < 0.001 for both groups).
3.3. Quotient measurements for COP path length The quotient of the COP path length displayed a significant main effect on the factors of system (p < 0.001) and group (p = 0.016, Fig. 3b). There was no difference associated with the group by system interaction effect (p = 0.872). Both quotients were greater among MS than the healthy control (p = 0.014 for RQ and p = 0.047 for PQ, Fig. 3b). Within both groups, PQ was significantly greater than RQ (p = 0.012 for MS and p < 0.001 for healthy individuals).
3.2. Quotient measurements for COP sway area ANOVA results indicated that the COP sway area-related quotient showed a significant main effect on group (p = 0.015) and system (p < 0.001) but not for the group by system interaction (p = 0.601, Fig. 3a). Post-hoc analyses further indicated that both the RQ and PQ of the COP area among people with MS are significantly greater than in 3
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and limit of stability (Ganesan et al., 2015). To reiterate, balance maintenance is a complex process affected by visual, proprioceptive, and vestibular systems. Any MS-induced deteriorations to these systems (such as the vision impairments (Van Emmerik et al., 2010), proprioception dysfunctions (Citaker et al., 2011), and vestibular problems (Pula et al., 2013)) could result in disturbance of standing balance in people with MS compared to healthy individuals. The results supported our first hypothesis that the removal of either vision or proprioception would lead to more imbalance among people with MS than the healthy controls. Specifically, both the RQ and PQ for the two COP measurements were significantly greater for people with MS than healthy adults (Fig. 3). This signifies that the dependence on both systems in keeping standing balance among MS is greater than in healthy individuals. The three sensory systems responsible for body balance can partially compensate for each other's deterioration. One potential compensation strategy to maintain upright stance is sensory reweighting among the afferent information from these systems (Pasma et al., 2015). The CNS usually prefers reliable sensory input of one sensory system over less reliable information from other sensory systems within a continuous dynamically weighting process. Compared with healthy individuals, people with MS experience disease-induced impairments to the sensory systems. When one sensory input is blocked, people with MS would put more weight on the available sensory systems to maintain body balance than the healthy persons. The increased weight could be indicative of the more reliance on the available sensory systems to keep body balance in people with MS. Our finding that MSinduced impairments lead to increased reliance on the visual and proprioceptive systems among people with MS than in healthy individuals coincides with the finding from a previous study which observed the increased RQ with the advancement in the disability level among people with MS (Kalron, 2017). Postural control, as a closed loop, involves three underlying systems: sensory, nervous, and motor systems. A steady standing body balance requires an adequately rapid transforming of neural information to and from the CNS. As MS could affect each of the three systems, people with MS exhibit more instability and may rely more on the sensory systems to maintain body balance. Specifically, the somatosensory conduction is slower among people with MS than their healthy counterparts (Cameron and Lord, 2010; Cameron et al., 2008). Due to the delayed spinal somatosensory conduction, it is likely that people with MS receive delayed and/or contaminated proprioceptive feedback of postural displacements and thus compensatory postural adjustments are untimely, incorrect, or insufficient, leading to more postural instability among people with MS than in healthy individuals (Cameron and Lord, 2010; Cameron et al., 2008). Evidence indeed suggests that the impaired central processing deficits of sensory information cause instability in people with MS (Cameron and Lord, 2010; Cameron et al., 2008). Another possible contributing factor to the increased reliance in people with MS is the MS-induced demyelination to the motor neuron, that may block or delay the transmission of the potentials along the neuro pathway from the CNS to the motor end units. This could result in consequential inaccuracy in the execution of appropriate motor commands to maintain postural stability (Cattaneoand Jonsdottir, 2009), further adversely affecting the body balance among people with MS. Our finding also aligns with previous studies which documented that postural sway increases more in MS than in healthy controls during altered sensory conditions, such as deprivation of vision and reduction in the proprioception system (Cameron and Lord, 2010). Other common impairments, such as spasticity (Sosnoff et al., 2010), muscle weakness (Citaker et al., 2013), and fatigue (Van Emmerik et al., 2010; Hebert and Corboy, 2013), have been reported to affect postural control among people with MS. Therefore, these factors may associate with the amplified postural instability among people with MS compared with healthy individuals. These functional limitations could also play a role in increasing the reliance
Fig. 3. Comparisons of Romberg's quotient (RQ) and proprioception quotient (PQ) of a) the 95% sway area and b) the total path length of the center of pressure (COP) trace between the healthy control (HC) and multiple sclerosis (MS) groups. RQ was defined as the ratio of the COP measurements without vision to with vision. PQ was the ratio of the COP measurements with eyes open when standing on a compliant surface to the ones on a firm surface. The greater the value of RQ or PQ, the higher the reliance on the vision or proprioception system in keeping body balance. pG: p value for the main factor of group; pS: p value for the main factor of system; and pG×S: p value for the interaction effect of group by system.
4. Discussion Balance impairment is a serious concern facing people with MS. The literature has documented increased COP movements during stance among even minimally impaired people with MS (Karst et al., 2005) and the COP movements keep increasing with the disease progression (Kalron, 2017). The balance deficits among people with MS could be because of the MS-induced impairments to the three sensory systems for maintaining body balance. To design optimal balance improvement training programs, it is essential to identify the reliance of body balance on the sensory systems. By using the quotients as a novel tool, this study examined the relative importance between the visual and proprioceptive systems in maintaining standing balance among people with MS in comparison with their healthy counterparts. Our overall results indicate that the reliance on either vision or proprioception to maintain balance is greater among people with MS than the healthy individuals. Furthermore, the proprioceptive input is more important in keeping body's balance than the visual system in both people with MS and healthy adults. We found that people with MS display more standing instability in comparison with their healthy counterparts under all three sensory conditions, evidenced by the increased COP sway area and the prolonged COP trajectory length (Fig. 2). The large COP activity may reflect the ineffectiveness of postural control among people with MS. Our finding is coincident with the ones from previous studies. For example, prior studies documented that people with MS show greater COP sway area, higher median sway velocity, and larger COP excursion on both mediolateral and anteroposterior directions than healthy individuals (Huisinga et al., 2012; Ganesan et al., 2015; Fling et al., 2014). Consistent with the findings based on posturography tests, people with MS were also reported to have poor performance during clinical balance assessments, such as Berg Balance Scale test (Learmonth et al., 2012), Tinetti performance-oriented mobility assessment (SilkwoodSherer and Warmbier, 2007), trunk movement (Findling et al., 2011), 4
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rehabilitation focused only on improving motor strategies (Cattaneoet al., 2007). Second, as indicated by our results and others’ (Fling et al., 2014; Rougier et al., 2007), proprioception is more important than vision in maintaining body balance in people with MS, it may be beneficial to direct attention to improve the proprioception functions in MS rehabilitation. The balance impairments among persons with MS could be addressed with approaches that augment proprioceptive input, including sensory facilitation techniques using supplementary tactile input and supportive devices that provide additional proprioceptive input to both the lower and upper extremities (Cameron and Lord, 2010). For example, supplementary tactile input created by kinesiology tape applied to the skin of calves (Cortesi et al., 2011), textured insoles (Kalron et al., 2015), and light fingertip touch on a stationary surface (Kanekar et al., 2013), has shown effects in improving standing balance among people with MS. In clinical settings, additional proprioceptive information could also be provided to persons with MS through other simple sources, such as elastic bandages, ankle braces, or shoes with high heel collars (Cameron et al., 2013). A recent study reported a 63% prevalence of accidental falls in people with MS, and the risk of falling increased when the proprioception declines with an odds ratio of 2.5 (Nilsagard et al., 2009). From this connection, a specific program focusing on proprioceptive training may be a key component to improve balance and thus reduce fall incidences among people with MS. Our study has limitations. First, only two of the three sensory systems responsible for body balance are included in this study. It remains unknow how the vestibular system impacts body balance with reference to other two systems. Second, results regarding people with MS should be interpreted with the caution that impairments in the participants tested in our study were relatively mild and results may translate differently to those with more progressive and/or advanced stages of MS. Further studies are needed to address these limitations. Overall, the present study revealed that the reliance of maintaining body balance on the proprioceptive and visual systems is greater among people with MS than in healthy individuals. Further, our finding highlighted the greater importance of the proprioceptive system compared with visual system in keeping body balance among both populations. Our findings could provide insight into postural control among people with MS and guidance for establishing effective balance training strategies.
on the visual and proprioceptive systems to preserve body balance among people with MS than their healthy counterparts. The results verified the second hypothesis that the reliance on the proprioceptive input is greater than on the visual system in maintaining upright standing. This notion was evidenced by the significantly greater PQ compared with RQ for both COP measurements among the two populations. The disease of MS seems not to affect the relative importance between vision and proprioception in maintaining balance with reference to the healthy individuals. As stated before, the CNS places more weight on the information of one reliable sensory system than information of other less reliable sensory systems. Studies suggested that proprioceptive information is the most critical sensory mechanism for the control of postural balance (Dietz et al., 1992). A study, that compared balance control between various sensory feedback conditions, estimated that proprioceptive system contributes up to 69% of body sway in a stance position (Lord et al., 1991). Restrictions of the proprioceptive and visual systems would impact the process of postural balance control differently. In detail, reduced proprioceptive input could exert more influence on body balance than impairment of the visual input, explaining the greater PQ than RQ and thus the higher reliance on the proprioceptive input in maintaining body balance than the visual input. Our results reinforced the conclusion from a past study which stated that the instability is largely the result of deficits in proprioceptive input among people with MS (Rougier et al., 2007). When one is standing without holding onto anything, the body's only contact is with the ground on the plantar side of the feet. The cutaneous sensation of the soles becomes a critical pathway to sense and transmit afferent information to the CNS to maintain the erect stance. It was shown that sensitivity of the cutaneous receptors of the foot sole is related to and predicts static standing balance in people with MS (Citaker et al., 2011). Another study suspected that people with MS may purposely adopt an asymmetrical posture between body sides to enhance the proprioceptive input on their stronger limb in order to maintain a relatively stable upright stance (Kalron and Achiron, 2013). When standing on compliant foam, this functional capacity of sensing afferent information is compromised. The visual system may not effectively and sufficiently compensate the consequence of the restricted proprioceptive input. Hence, the static standing stability will be significantly affected. On the other hand, when visual input is eliminated, individuals could more effectively compensate with the information supplied from the proprioceptive system. This could be another explanation of the greater reliance of body balance on proprioceptive input than the visual input. Another contribution of this study was the development of PQ, defined as the ratio of the balance performance between intact and limited proprioceptive input conditions. Such a definition is very similar to RQ. As RQ quantifies the reliance of body balance maintenance on visual input, PQ illustrates the dependence of body balance on proprioceptive information. We based the quotients of RQ and PQ on the same reference (i.e., the COP measurements with eyes open on a static surface). By comparing these two quotients, the relative importance between the visual and proprioceptive systems on standing balance could be determined. Such a process may detect the relative role of vision and proprioception systems in maintaining body balance. To verify the accuracy of our calculation of RQ, we have compared its value between the current study (sway area: 2.43 ± 2.23; path length: 1.79 ± 0.66) and a previous one (area: 2.10–2.48; length: 1.82–1.91 for mild to moderate MS) which involved more than 500 people with MS (Kalron, 2017). The similar values between studies endorse our calculation and indicate that our sample could be representative of people mildly to moderately affected by MS. Our findings may be clinically meaningful for the design and implementation of balance training programs for people with MS. First, the sensory information is important to maintain body balance. Balance rehabilitation to improve sensory as well as motor components may improve body balance and reduce falls more effectively than balance
Funding This study was partially supported by the National Multiple Sclerosis Society and Georgia State University Neuroscience Institute. The funding sources have no roles in study design, in the collection, analysis and interpretation of data, in the writing of the report, and in the decision to submit the article for publication. Declaration of Competing Interest None. Acknowledgments The authors thank Maria Sanchez and Edson Estrada for assistance in data collection and processing; and Jennifer Lees for editing. The authors also thank Rebekah Buehler for her initial contribution to this manuscript. References Campbell, J.D., Ghushchyan, V., McQueen, R.B., Cahoon-Metzger, S., Livingston, T., Vollmer, T., et al., 2014. Burden of multiple sclerosis on direct, indirect costs and quality of life; National US estimates. Mult. Scler. Relat. Disord. 3, 227–236. Zwibel, H.L., 2009. Contribution of impaired mobility and general symptoms to the
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Multiple Sclerosis and Related Disorders journal homepage: www.elsevier.com/locate/msard
Original article
Relative importance of vision and proprioception in maintaining standing balance in people with multiple sclerosis
T
⁎
Feng Yanga, , Xinyue Liub a b
Department of Kinesiology and Health, Georgia State University, 125 Decatur St, Suite-137, Atlanta, GA 30303, USA School of Mathematics, Georgia Institute of Technology, Atlanta, USA
A R T I C LE I N FO
A B S T R A C T
Keywords: Romberg's quotient Proprioception quotient Fall prevention Posturography test
Background: Balance impairment is common and a risk factor of falls in people with multiple sclerosis (MS). The purpose of this study was to evaluate the relative importance between vision and proprioception in maintaining standing body balance among individuals with MS compared with healthy individuals. Methods: Thirty people with MS (the mean ± standard deviation of the Patient Determined Disability Steps: 3.62 ± 1.67 out of 8) and 25 healthy adults participated in this cross-sectional study. They underwent a static posturography test, consisting of three sensory feedback conditions: eyes open on a firm surface, eyes closed on a firm surface, and eyes open on a compliant surface. Their standing balance performance, quantified by the 95% confidence ellipse area and the total length of the center of pressure trajectory during each sensory condition, was calculated based on the ground reaction force data. The Romberg's quotient (the ratio of the center of pressure measurements on the firm surface between eyes open and eyes closed conditions) and proprioception quotient (the ratio of the center of pressure measurements with eyes open between firm and compliant standing surfaces) were calculated and compared between groups. Results: Persons with MS demonstrated significantly larger postural sway under all three sensory conditions than their healthy counterparts. The reliance on the vision and proprioception systems in maintaining body balance was greater among people with MS compared to healthy adults. Both groups similarly relied more on the proprioceptive input to keep body balance than on the vision. Conclusions: Like healthy individuals, persons with MS rely more on proprioception to maintain body balance than vision. Our findings could provide preliminary reference for optimizing balance improving programs aimed at person with MS.
1. Introduction Multiple sclerosis (MS) is a progressive autoimmune disease of the central nervous system (CNS) (Campbell et al., 2014). With an average onset age between 20–40 years, one's most productive life segment, MS is the predominant chronic, non-traumatic neurological disorder of young adults and has severe health and socioeconomic consequences (Zwibel, 2009). Standing balance is a fundamental requirement of conducting daily activities. Humans maintain body balance through integrating the uninterrupted signal flow from the vestibular, visual, and proprioceptive systems (Fitzpatrick and McCloskey, 1994). Due to the MS-induced damages throughout the CNS, MS could affect one or more of these signal pathways and impair the capacity to maintain body balance (Cattaneoand Jonsdottir, 2009). Balance deficit is a serious challenge
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Corresponding author. E-mail address: [email protected] (F. Yang).
https://doi.org/10.1016/j.msard.2019.101901 Received 11 September 2019; Accepted 19 December 2019 2211-0348/ © 2019 Elsevier B.V. All rights reserved.
faced by people with MS (Kalron and Achiron, 2013) and impacts about three-quarters of people with MS over the disease course (Prosperini et al., 2010). Balance impairment restricts mobility among persons with MS. Mobility limitations adversely affect the employment, functional independence, social participation, and quality of life in people with MS (Kwiatkowski et al., 2014; Bethoux and Bennett, 2011). The compromised body balance also increases the likelihood of falls (Cameron and Lord, 2010), which can negatively affect this population (Matsuda et al., 2012; Mazumder et al., 2015). Therefore, it is imperative to develop effective interventions for improving body balance among people with MS. As standing balance is dependent upon three sensory systems, improvements in the function and capacity of these systems could ameliorate imbalance. From a practical viewpoint, it is useful to determine the relative importance between these three systems in maintaining the
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standing balance, which can inform the design of effective balance training interventions to target the most critical sensory systems. For example, a previous study reported that a visuo-proprioceptive training program improves body balance among persons with MS (Prosperini et al., 2010). Since this training program involved both visual and proprioceptive components simultaneously, it is impossible to detect which component is more important or effective to improve body balance. Identifying the relative dependency of standing balance on these sensory systems also has theoretical significance because it helps the research community understand the process underlying the control of standing balance in people with MS. However, the relative importance of these systems in keeping body balance in people with MS remains unknown. This may foster less than optimal interventions for balance training in MS and thus an inefficient use of the limited resources in MS rehabilitation. As a first attempt, this study identified the relative importance between visual and proprioceptive systems in maintaining body balance in people with MS compared to age- and gender-matched healthy individuals. Posturographic measurement was used to gauge standing balance under three sensory conditions: eyes open, eyes closed, and standing on a foam pad with eyes open. Body balance, characterized by the 95% confidence sway area and the total length of the center of pressure (COP) trajectory, was calculated. To determine the reliance of body balance on the visual system, we adopted Romberg's quotient as the ratio of the balance measurement on a static surface under eyes closed condition to the eyes open condition (Howcroft et al., 2017). A similar measure, proprioception quotient, was established as the ratio of the balance performance with eyes open between the foam and static surface conditions. This quotient assesses the dependence of body standing balance on the proprioceptive system. As both quotients used the measurement under eyes-open condition as the common reference, the comparison between them should provide insight into the relative importance between visual and proprioceptive systems to maintain body balance. We hypothesized that the reliance on both the visual and proprioceptive systems among people with MS would be greater than the healthy controls in maintaining standing balance. This could be confirmed if both quotients being higher among individuals living with MS than healthy individuals. We further hypothesized that the reliance on the proprioceptive system in maintaining balance is higher than that of the visual system in both persons with MS and healthy individuals. This hypothesis would be supported if the Romberg's quotient is greater than the proprioception quotient in both populations. The findings from this study could shed light on the control strategy of standing balance among people with MS and provide useful reference for designing effective body balance training approaches.
Table 1 Demographic information for both the healthy control (HC) and multiple sclerosis (MS) groups. Parameter
HC (n = 25)
MS (n = 30)
p value
Age (years) Female (%) Height (cm) Mass (kg)
50.6 ± 13.3 18 (72.0) 164.9 ± 10.4 75.9 ± 15.4
50.8 ± 14.4 23 (76.7) 164.2 ± 7.7 73.5 ± 14.5
0.958 0.762* 0.795 0.562
Patient Determined Disability Steps for MS: 3.62 ± 1.67. Disease duration for MS: 14.0 ± 10.6 years. ⁎ : Fisher's exact test used.
excluded if they had a neurological disorder, ambulation dysfunction, or previous surgery involving lower extremities or were pregnant. All participants gave written informed consent approved by the Institutional Review Board before participation. 2.2. Posturography test Static posturography assesses postural control which involves responses to gravity and relatively subtle, self-initiated disturbance to body balance (Visser et al., 2008). This assessment is typically achieved by measuring the spontaneous movement of the COP beneath the feet as participants stand on a force plate. In this current study, a 30-second trial was collected in sequence for each of the three following conditions: eyes open on a static surface, eyes closed on the static surface, and eyes open while standing on a block of compliant foam (10-cm thick, Aeromat Fitness Product, CA). Participants were told to hold the body as still as possible under all conditions with feet shoulder width apart and arms resting at the sides in a comfortable position. The ground reaction force during the three trials were acquired by a force plate (AMTI, ORT6-1000) at 600 Hz. During eyes open conditions, participants looked at a fixed point about 4 m in front of them. A 2minute rest was administered between conditions to reduce the possible effect of fatigue on our results. 2.3. Data reduction and analysis Ground reaction force data was low-pass filtered at 25 Hz with a fourth-order Butterworth filter (Pai et al., 2006). The COP trace during each trial was then determined by the filtered ground reaction force (Fig. 1). Based on the determined COP trajectory, the 95% confidence ellipse area (A) which encloses 95% of COP trajectory (Schubert and Kirchner, 2014) and the total COP trajectory length (L) (Howcroft et al., 2017) were calculated (Fig. 1). These two parameters were chosen as they have been widely used in previous studies concerning people with MS (Kalron and Achiron, 2013; Cameron and Lord, 2010). Then, Romberg's quotient (RQ) and proprioception quotient (PQ) were computed corresponding with the conditions of vision removal and proprioception removal according to the two COP measurements (A and L):
2. Materials and methods In this cross-sectional study, people with MS and healthy individuals were assessed for their balance during quiet stance under three sensory conditions: normal, vision removal, and proprioception removal. The reliance of balance control on the visual and proprioceptive systems were then calculated as the Romberg's quotient and proprioception quotient, respectively. The relative importance of visual and proprioceptive systems in maintaining standing balance was evaluated. 2.1. Participants
RQ =
AEC L or EC AEO LEO
PQ =
AFM L or FM AEO LEO
where, EO, EC, and FM respectively represents the sensory conditions of eyes open, eyes closed, and standing on the foam. A quotient value greater than one indicates that the removal of the respective sensory system would worsen the balance performance in comparison with the EO condition, reflecting the reliance on the corresponding sensory feedback system in keeping the upright body posture. The greater the quotient value, the higher the dependence on the respective sensory system. Since both quotients were defined on a common basis – the balance performance during EO condition – the comparison between
Thirty people with MS and 25 healthy adults were recruited (Table 1). To be enrolled into the MS group, participants needed to have a neurologist-confirmed diagnosis of MS; a score of ≤6.5 on the Patient Determined Disease Steps; ability to stand for at least 30 s independently; and no significant relapse within the past eight weeks. Participants must be free from other major general medical or surgical disorders or pregnancy. For healthy individuals, participants were 2
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Fig. 1. Schematic plot of the center of pressure (COP) trajectory under three sensory feedback conditions for both healthy control (HC) and multiple sclerosis (MS) groups. The three conditions include eyes open on a firm surface, eyes closed on a firm surface, and standing on a foam with eyes open. X axis denotes the mediolateral direction and Y represents the anteroposterior direction. The upper panel (subplots: a, b, and c) is for HC under the three conditions and the lower panel (d, e, and f) is for the MS. The area enclosed by the ellipse defines the 95% confidence ellipse area of the COP trajectory in mm2. The distance covered by the whole COP trajectory is the total COP path length in mm.
these two quotients could reflect the relative importance of these two sensory systems (vison vs. proprioception) in sustaining standing posture. A custom Matlab (Mathworks, MA) script was developed to conduct all calculations. 2.4. Statistical analysis Normality of each variable was checked using the Shapiro-Wilk test. If nonnormality was found, a logarithm transform would be executed. Differences in the demographic characteristics between groups were analyzed by a χ2 test for the categorical variable and independent samples t-tests for continuous variables. Independent t-tests were also used to compare the COP sway area and path length between groups under all three sensory conditions. Analyses of variance (ANOVA) with repeated measures was used to compare both quotients between groups (between-subject factor: MS vs. health) and systems (within-subject factor: vision vs. proprioception or RQ vs. PQ). Any significant main or interaction effect was further analyzed by appropriate post-hoc tests. All statistical analyses were performed using SPSS 24.0 (IBM, NY), and a significance level of 0.05 was applied throughout.
Fig. 2. The comparison of the center of pressure a) 95% confidence ellipse area and b) total path length between the healthy control (HC) and multiple sclerosis (MS) groups under three sensory conditions: eyes open (EO), eyes closed (EC), and standing on a foam (FM). Both measurements of the center of pressure are significantly larger among people with MS than in healthy individuals under all three conditions (***: p < 0.001).
3. Results 3.1. Measurements of COP area and length Under all three sensory conditions, both the COP sway area and the total COP path length in the MS group were significantly greater than the ones among healthy individuals (Fig. 2, p < 0.001 for the betweengroup comparison of both measures under three conditions). The average RQ and PQ for both COP measurements in the two groups were greater than one, indicating that the removal of vision or proprioception input increases the measurements of the COP sway area and trace length (Fig. 3).
the healthy controls (p = 0.007 for RQ and p = 0.026 for PQ). Within either group, the PQ was significantly greater than the RQ (p < 0.001 for both groups).
3.3. Quotient measurements for COP path length The quotient of the COP path length displayed a significant main effect on the factors of system (p < 0.001) and group (p = 0.016, Fig. 3b). There was no difference associated with the group by system interaction effect (p = 0.872). Both quotients were greater among MS than the healthy control (p = 0.014 for RQ and p = 0.047 for PQ, Fig. 3b). Within both groups, PQ was significantly greater than RQ (p = 0.012 for MS and p < 0.001 for healthy individuals).
3.2. Quotient measurements for COP sway area ANOVA results indicated that the COP sway area-related quotient showed a significant main effect on group (p = 0.015) and system (p < 0.001) but not for the group by system interaction (p = 0.601, Fig. 3a). Post-hoc analyses further indicated that both the RQ and PQ of the COP area among people with MS are significantly greater than in 3
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and limit of stability (Ganesan et al., 2015). To reiterate, balance maintenance is a complex process affected by visual, proprioceptive, and vestibular systems. Any MS-induced deteriorations to these systems (such as the vision impairments (Van Emmerik et al., 2010), proprioception dysfunctions (Citaker et al., 2011), and vestibular problems (Pula et al., 2013)) could result in disturbance of standing balance in people with MS compared to healthy individuals. The results supported our first hypothesis that the removal of either vision or proprioception would lead to more imbalance among people with MS than the healthy controls. Specifically, both the RQ and PQ for the two COP measurements were significantly greater for people with MS than healthy adults (Fig. 3). This signifies that the dependence on both systems in keeping standing balance among MS is greater than in healthy individuals. The three sensory systems responsible for body balance can partially compensate for each other's deterioration. One potential compensation strategy to maintain upright stance is sensory reweighting among the afferent information from these systems (Pasma et al., 2015). The CNS usually prefers reliable sensory input of one sensory system over less reliable information from other sensory systems within a continuous dynamically weighting process. Compared with healthy individuals, people with MS experience disease-induced impairments to the sensory systems. When one sensory input is blocked, people with MS would put more weight on the available sensory systems to maintain body balance than the healthy persons. The increased weight could be indicative of the more reliance on the available sensory systems to keep body balance in people with MS. Our finding that MSinduced impairments lead to increased reliance on the visual and proprioceptive systems among people with MS than in healthy individuals coincides with the finding from a previous study which observed the increased RQ with the advancement in the disability level among people with MS (Kalron, 2017). Postural control, as a closed loop, involves three underlying systems: sensory, nervous, and motor systems. A steady standing body balance requires an adequately rapid transforming of neural information to and from the CNS. As MS could affect each of the three systems, people with MS exhibit more instability and may rely more on the sensory systems to maintain body balance. Specifically, the somatosensory conduction is slower among people with MS than their healthy counterparts (Cameron and Lord, 2010; Cameron et al., 2008). Due to the delayed spinal somatosensory conduction, it is likely that people with MS receive delayed and/or contaminated proprioceptive feedback of postural displacements and thus compensatory postural adjustments are untimely, incorrect, or insufficient, leading to more postural instability among people with MS than in healthy individuals (Cameron and Lord, 2010; Cameron et al., 2008). Evidence indeed suggests that the impaired central processing deficits of sensory information cause instability in people with MS (Cameron and Lord, 2010; Cameron et al., 2008). Another possible contributing factor to the increased reliance in people with MS is the MS-induced demyelination to the motor neuron, that may block or delay the transmission of the potentials along the neuro pathway from the CNS to the motor end units. This could result in consequential inaccuracy in the execution of appropriate motor commands to maintain postural stability (Cattaneoand Jonsdottir, 2009), further adversely affecting the body balance among people with MS. Our finding also aligns with previous studies which documented that postural sway increases more in MS than in healthy controls during altered sensory conditions, such as deprivation of vision and reduction in the proprioception system (Cameron and Lord, 2010). Other common impairments, such as spasticity (Sosnoff et al., 2010), muscle weakness (Citaker et al., 2013), and fatigue (Van Emmerik et al., 2010; Hebert and Corboy, 2013), have been reported to affect postural control among people with MS. Therefore, these factors may associate with the amplified postural instability among people with MS compared with healthy individuals. These functional limitations could also play a role in increasing the reliance
Fig. 3. Comparisons of Romberg's quotient (RQ) and proprioception quotient (PQ) of a) the 95% sway area and b) the total path length of the center of pressure (COP) trace between the healthy control (HC) and multiple sclerosis (MS) groups. RQ was defined as the ratio of the COP measurements without vision to with vision. PQ was the ratio of the COP measurements with eyes open when standing on a compliant surface to the ones on a firm surface. The greater the value of RQ or PQ, the higher the reliance on the vision or proprioception system in keeping body balance. pG: p value for the main factor of group; pS: p value for the main factor of system; and pG×S: p value for the interaction effect of group by system.
4. Discussion Balance impairment is a serious concern facing people with MS. The literature has documented increased COP movements during stance among even minimally impaired people with MS (Karst et al., 2005) and the COP movements keep increasing with the disease progression (Kalron, 2017). The balance deficits among people with MS could be because of the MS-induced impairments to the three sensory systems for maintaining body balance. To design optimal balance improvement training programs, it is essential to identify the reliance of body balance on the sensory systems. By using the quotients as a novel tool, this study examined the relative importance between the visual and proprioceptive systems in maintaining standing balance among people with MS in comparison with their healthy counterparts. Our overall results indicate that the reliance on either vision or proprioception to maintain balance is greater among people with MS than the healthy individuals. Furthermore, the proprioceptive input is more important in keeping body's balance than the visual system in both people with MS and healthy adults. We found that people with MS display more standing instability in comparison with their healthy counterparts under all three sensory conditions, evidenced by the increased COP sway area and the prolonged COP trajectory length (Fig. 2). The large COP activity may reflect the ineffectiveness of postural control among people with MS. Our finding is coincident with the ones from previous studies. For example, prior studies documented that people with MS show greater COP sway area, higher median sway velocity, and larger COP excursion on both mediolateral and anteroposterior directions than healthy individuals (Huisinga et al., 2012; Ganesan et al., 2015; Fling et al., 2014). Consistent with the findings based on posturography tests, people with MS were also reported to have poor performance during clinical balance assessments, such as Berg Balance Scale test (Learmonth et al., 2012), Tinetti performance-oriented mobility assessment (SilkwoodSherer and Warmbier, 2007), trunk movement (Findling et al., 2011), 4
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rehabilitation focused only on improving motor strategies (Cattaneoet al., 2007). Second, as indicated by our results and others’ (Fling et al., 2014; Rougier et al., 2007), proprioception is more important than vision in maintaining body balance in people with MS, it may be beneficial to direct attention to improve the proprioception functions in MS rehabilitation. The balance impairments among persons with MS could be addressed with approaches that augment proprioceptive input, including sensory facilitation techniques using supplementary tactile input and supportive devices that provide additional proprioceptive input to both the lower and upper extremities (Cameron and Lord, 2010). For example, supplementary tactile input created by kinesiology tape applied to the skin of calves (Cortesi et al., 2011), textured insoles (Kalron et al., 2015), and light fingertip touch on a stationary surface (Kanekar et al., 2013), has shown effects in improving standing balance among people with MS. In clinical settings, additional proprioceptive information could also be provided to persons with MS through other simple sources, such as elastic bandages, ankle braces, or shoes with high heel collars (Cameron et al., 2013). A recent study reported a 63% prevalence of accidental falls in people with MS, and the risk of falling increased when the proprioception declines with an odds ratio of 2.5 (Nilsagard et al., 2009). From this connection, a specific program focusing on proprioceptive training may be a key component to improve balance and thus reduce fall incidences among people with MS. Our study has limitations. First, only two of the three sensory systems responsible for body balance are included in this study. It remains unknow how the vestibular system impacts body balance with reference to other two systems. Second, results regarding people with MS should be interpreted with the caution that impairments in the participants tested in our study were relatively mild and results may translate differently to those with more progressive and/or advanced stages of MS. Further studies are needed to address these limitations. Overall, the present study revealed that the reliance of maintaining body balance on the proprioceptive and visual systems is greater among people with MS than in healthy individuals. Further, our finding highlighted the greater importance of the proprioceptive system compared with visual system in keeping body balance among both populations. Our findings could provide insight into postural control among people with MS and guidance for establishing effective balance training strategies.
on the visual and proprioceptive systems to preserve body balance among people with MS than their healthy counterparts. The results verified the second hypothesis that the reliance on the proprioceptive input is greater than on the visual system in maintaining upright standing. This notion was evidenced by the significantly greater PQ compared with RQ for both COP measurements among the two populations. The disease of MS seems not to affect the relative importance between vision and proprioception in maintaining balance with reference to the healthy individuals. As stated before, the CNS places more weight on the information of one reliable sensory system than information of other less reliable sensory systems. Studies suggested that proprioceptive information is the most critical sensory mechanism for the control of postural balance (Dietz et al., 1992). A study, that compared balance control between various sensory feedback conditions, estimated that proprioceptive system contributes up to 69% of body sway in a stance position (Lord et al., 1991). Restrictions of the proprioceptive and visual systems would impact the process of postural balance control differently. In detail, reduced proprioceptive input could exert more influence on body balance than impairment of the visual input, explaining the greater PQ than RQ and thus the higher reliance on the proprioceptive input in maintaining body balance than the visual input. Our results reinforced the conclusion from a past study which stated that the instability is largely the result of deficits in proprioceptive input among people with MS (Rougier et al., 2007). When one is standing without holding onto anything, the body's only contact is with the ground on the plantar side of the feet. The cutaneous sensation of the soles becomes a critical pathway to sense and transmit afferent information to the CNS to maintain the erect stance. It was shown that sensitivity of the cutaneous receptors of the foot sole is related to and predicts static standing balance in people with MS (Citaker et al., 2011). Another study suspected that people with MS may purposely adopt an asymmetrical posture between body sides to enhance the proprioceptive input on their stronger limb in order to maintain a relatively stable upright stance (Kalron and Achiron, 2013). When standing on compliant foam, this functional capacity of sensing afferent information is compromised. The visual system may not effectively and sufficiently compensate the consequence of the restricted proprioceptive input. Hence, the static standing stability will be significantly affected. On the other hand, when visual input is eliminated, individuals could more effectively compensate with the information supplied from the proprioceptive system. This could be another explanation of the greater reliance of body balance on proprioceptive input than the visual input. Another contribution of this study was the development of PQ, defined as the ratio of the balance performance between intact and limited proprioceptive input conditions. Such a definition is very similar to RQ. As RQ quantifies the reliance of body balance maintenance on visual input, PQ illustrates the dependence of body balance on proprioceptive information. We based the quotients of RQ and PQ on the same reference (i.e., the COP measurements with eyes open on a static surface). By comparing these two quotients, the relative importance between the visual and proprioceptive systems on standing balance could be determined. Such a process may detect the relative role of vision and proprioception systems in maintaining body balance. To verify the accuracy of our calculation of RQ, we have compared its value between the current study (sway area: 2.43 ± 2.23; path length: 1.79 ± 0.66) and a previous one (area: 2.10–2.48; length: 1.82–1.91 for mild to moderate MS) which involved more than 500 people with MS (Kalron, 2017). The similar values between studies endorse our calculation and indicate that our sample could be representative of people mildly to moderately affected by MS. Our findings may be clinically meaningful for the design and implementation of balance training programs for people with MS. First, the sensory information is important to maintain body balance. Balance rehabilitation to improve sensory as well as motor components may improve body balance and reduce falls more effectively than balance
Funding This study was partially supported by the National Multiple Sclerosis Society and Georgia State University Neuroscience Institute. The funding sources have no roles in study design, in the collection, analysis and interpretation of data, in the writing of the report, and in the decision to submit the article for publication. Declaration of Competing Interest None. Acknowledgments The authors thank Maria Sanchez and Edson Estrada for assistance in data collection and processing; and Jennifer Lees for editing. The authors also thank Rebekah Buehler for her initial contribution to this manuscript. References Campbell, J.D., Ghushchyan, V., McQueen, R.B., Cahoon-Metzger, S., Livingston, T., Vollmer, T., et al., 2014. Burden of multiple sclerosis on direct, indirect costs and quality of life; National US estimates. Mult. Scler. Relat. Disord. 3, 227–236. Zwibel, H.L., 2009. Contribution of impaired mobility and general symptoms to the
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