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The effect of aging on vertical postural control during the forward and backward shift of the center of pressure
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The effect of aging on vertical postural control during the forward and backward shift of the center of pressure Satoshi Kasahara a,*, Hiroshi Saito a, Tsubasa Anjiki b, Hitomi Osanai c a
Department of Rehabilitation Sciences, Faculty of Health Sciences, Hokkaido University, Sapporo, Japan Department of Rehabilitation, Hatsudai Rehabilitation Hospital, Tokyo, Japan c Department of Rehabilitation, Kasai Shoikai Hospital, Tokyo, Japan b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 16 December 2014 Received in revised form 15 July 2015 Accepted 22 July 2015
Preventing fall-related injuries is becoming a priority as the world population ages. This study’s purpose was to examine the effect of aging on vertical postural control in the community-dwelling elderly. Thirty-six elderly individuals and twenty-two healthy young adults were asked to shift their centers of pressure (COPs) as far as possible while standing. The COP position, angle of each lower leg joint, and postural muscle activities were measured using a force plate, three-dimensional motion analyzer, and electromyogram, respectively. The vertical position of the center of mass (COM) was also measured to assess the change in vertical postural control. The backward COP shift in the elderly group was significantly smaller than that in the young group, and both the forward and backward COM shifts were significantly smaller in elders relative to those in youths. The COM position in the elderly group during the backward COP shift was also significantly lower than that in the young group. Knee and ankle joint movements differed between the two groups during the backward COP shift. Factor analysis indicated that dorsal and ventral muscle groups were involved in the COP shift. Specifically, the relationship between the biceps femoris muscle and the voluntary COP shift was reinforced in the elderly group. These findings suggest that the vertical postural strategy changes in the elderly during the backward COP shift. ß 2015 Published by Elsevier B.V.
Keywords: Aging Vertical postural control Postural strategy Muscle synergy Center of mass
1. Introduction Falls are the most serious cause of hip and wrist fractures and head injuries among the elderly [1]. Major factors contributing to falls among the elderly are the reduced physiological capacity that occurs with aging and decreased balance [2–4]. Furthermore, the risk of falls among the elderly is affected by the interactions of the organism, environment, and task [5]. More than 30% of community-dwelling elderly people and those in long-term care facilities report at least one indoor fall per year [1], with 10–15% of these falls resulting in significant injury [6]. The most common problem among the elderly is reported to be incorrect transfer or weightshifting performed by the individual (i.e., self-paced) [1]. A smooth shift of the center of pressure (COP) and center of mass (COM) is essential for transferring or shifting body weight
* Corresponding author at: Department of Rehabilitation Sciences, Faculty of Health Sciences, Hokkaido University, West 5, North 12, Kita-ku, Sapporo 060-0812, Japan. Tel.: +81 11 706 3391; fax: +81 11 706 3391. E-mail address: [email protected] (S. Kasahara).
during activities of daily living, and analyses of such shifts have often been used in previous studies [7–10]. In terms of balance ability, the elderly have been reported to show smaller maximum displacement [7] and greater reaction and movement times [8] during a voluntary COP shift when compared to those in the young. COP has been measured and analyzed in the anterior-posterior (A/P) and/or medial-lateral (M/L) directions, because COP movement is performed two-dimensionally within the base of support [9]. Although researchers have focused on the A/P and/or M/L directions with respect to the COM in relation to the COP [10], the actual COM has three-dimensional (3-D) motion, because the vertical direction is added to these directions. Recent studies have reported that higher COM positions decreased postural stability and lower COM positions improved standing stability [9,10]; thus 3-D postural control requires vertical changes as well as A/P and M/L changes. However, to our knowledge, no study has attempted to clarify postural control further in humans during the erect stance through examining the COM in the vertical dimension. In this study, we aimed to evaluate the effect of aging on vertical postural control by investigating the COM in the vertical direction during a task involving a self-paced dynamic shift in the COP. We
http://dx.doi.org/10.1016/j.gaitpost.2015.07.056 0966-6362/ß 2015 Published by Elsevier B.V.
Please cite this article in press as: Kasahara S, et al. The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.07.056
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anticipated that the vertical position of the COM would differ between elderly and young individuals because of differences in the adopted postural strategy [3,4]. Additionally, we hypothesized that changes in the vertical postural strategy as a consequence of aging would be related to activity in the postural muscles, which specifically control the knee joint and thereby movement in the vertical axis [11].
2. Methods 2.1. Participants Twenty-two healthy young adults (Y-Group: 13 women and 9 men; mean age, 20.6 1.0 years) and 36 healthy elderly adults (E-Group: 36 men; mean age, 69.5 3.2 years) participated. The body characteristics in both groups were similar (Table 1). Young participants were randomly selected from among college students who volunteered to participate in this study. Elderly participants >65 years old with no history of any neurological or orthopedic diseases or ophthalmologic conditions that could contribute to movement dysfunction were randomly selected from among communitydwelling elderly who had registered with the employment agency. None had had a history of falls for at least 6 months before enrollment in the study or took any medication that could affect balance [12]. All study participants provided written informed consent to participate, and the procedures were approved by the ethics committee of Hokkaido University School of Medicine (no. 11-03). 2.2. Experimental tasks Participants stood with bare feet and their legs shoulder-width apart on a force plate (Kistler, Type 9286A, Switzerland) with their arms crossed in front of their chests. Visual feedback information about the COP position was provided to participants from a computer monitor, and the start position of the COP was located 5.0 cm in front of the middle of the line joining both medial malleoluses to ensure a backward motion range. After the examiner checked the steady state of the COP within 1 cm of the start position, the power to the monitor was turned off, and each trial was started. Participants performed the three tasks of: (1) maintaining a static stance; (2) shifting to the maximum forward COP position; and (3) shifting to the maximum backward COP position [13]. Participants were instructed to shift the COP as far as possible and not to raise their toes or heels and to stably maintain their COP position. Participants were given no instruction regarding the use of leg joints in order to avoid a bias in postural strategy. Each task was performed 3 times in a random order, with sufficient rest between tasks to prevent fatigue. 2.3. Data acquisition and processing Force and muscle activity data were digitized at a frequency of 1 kHz by an NI Compact DAQ (National Instruments, Austin, TX,
Table 1 Descriptive statistics of the participants according to age. YG (n = 22)
Age (year) Height (cm) Weight (kg) BMI (kg/m2)
EG (n = 36)
Mean SD
Range
Mean SD
Range
20.6 1.0 165.9 8.9 58.4 9.5 21.1 2.1
20–24 152–181 44–75 17.6–25.3
69.5 3.2* 163.9 5.2 62.8 5.2 23.4 2.4
65–78 153–172 49–85 19.3–28.7
YG: young group, EG: elderly group, BMI: body mass index, SD: standard deviation * p < 0.05 between the YG and EG groups.
USA), and the COP position was subsequently calculated with force data using a customized program (Labview 2009; National Instruments, Austin, TX, USA). Surface electromyography (EMG) data were collected using the Delsys EMG system (Bagnoli-2EMG System; DELSYS, Boston, MA). Activity was recorded for each of the following 6 postural muscles according to previous studies [2,3,11,12]: the rectus abdominis (RA), erector spinae (ES), rectus femoris (RF), biceps femoris (BF), tibialis anterior (TA), and gastrocnemius (GAS) muscles. EMG sensors were attached to the belly of the target muscle, and reference electrodes were attached to the iliac crest, the head of the fibula, and the lateral malleolus [2,3,11,12]. A 3-D motion analysis system with 6 cameras at a sampling rate of 100 Hz was used to compute the angles of the hip, knee, and ankle joints and the position of the COM (Motion Analysis Corporation, Santa Rosa, CA, USA). Reflective markers were attached based on the anatomical landmark locations used by Winter [14]. All markers were located bilaterally, except for those at the top, front, and back of the head; the acromion process; the angulus inferior scapulae; and the sacrum. Positive values of calculated joint angles show flexion and dorsal flexion, and negative values show extension and plantar flexion. All off-line data processing was performed with the customized Matlab program (Mathworks, Natick, MA, USA). COP and COM data were low-pass filtered with a zero-lag, second-order Butterworth filter with a cut-off frequency of 10 Hz. The distance from the start position to the maximum COP and COM positions in either the anterior or posterior direction was subsequently measured for each task. The A/P displacement of the COP and the COM was normalized by dividing it by the length of each participant’s foot [14]. Vertical displacement was calculated by subtracting the start position of the COM from the COM position during the maximum COP shift and subsequently normalized by each participant’s height. Surface EMG data were rectified and band-pass filtered from 10 to 500 Hz using a fourth-order Butterworth filter. The magnitude of muscle activity was evaluated using the mean amplitude of each muscle’s activity in maintaining a stable COP after the completion of a COP shift. The change in each joint angle was calculated by subtracting the value obtained during the static stance from the joint angle at each maximum COP shift. 2.4. Statistical analysis All statistical analyses were performed using PASW Statistics 18 (SPSS Inc., Chicago, IL). All data are shown as the mean and standard deviation of the three trials for each task in each group. An analysis of variance (ANOVA) was used to examine the interactive effects of age and movement direction. If a significant interaction was identified, the simple main effect was further analyzed with a post-hoc paired t-test with Bonferroni corrections. A p value <0.05 was considered statistically significant. The effect sizes from the ANOVA are expressed as eta-squared (h2) values, and the effect sizes for differences in the means are expressed as Cohen’s d values [15]. After performing the ANOVA for muscle activities among tasks in each group, we conducted an exploratory factor analysis with the principal factor method to identify the factor structure of the muscle activities for postural strategy during the COP shift. An optimal factor solution was determined based on eigenvalues of >1.0 [16], and on an examination of the scree plot using all 6 muscle activities. For the optimal factor solution, principal axis factoring with varimax rotation and Kaiser’s normalization were used to determine the latent variables that best explained the observed variability in each EMG. After the rotation, any variable that significantly loaded on more than one factor (with an absolute value >0.4) was identified and removed [17].
Please cite this article in press as: Kasahara S, et al. The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.07.056
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3. Results 3.1. Comparison of COP and COM between Elderly and Young Participants The ANOVA showed a significant interactive effect (age direcdirection) for COP displacement (F(1, 112) = 7.36, p < 0.01, h2 = 0.04). The backward COP displacement of the E-group was 28.9% lower than that of the Y-group (p < 0.01, Fig. 1a). In the E-group, the backward displacement was significantly smaller (a decrease of 30%) than the forward displacement (p < 0.01).
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There was a significant interactive effect (age task) for COM A/P displacement (F(2, 168) = 14.65, p < 0.01, h2 = 0.04). The COM A/P displacement in the E-group during both the forward and backward COP shift was significantly smaller than that in the Y-group (p < 0.01, Fig. 1b). In the E-group, COM amplitude during the backward COP shift was significantly smaller than that during the forward COP shift (p < 0.01). For vertical COM displacement, there was a significant interactive effect (age direction) (F(1, 112) = 7.19, p < 0.01, h2 = 0.09). The posthoc test showed that vertical COM displacement in the E-group during the backward COP shift was significantly lower than that in the Y-group (p < 0.01, Fig. 1c). On the other hand, the COM was lower in both groups during the forward COP shift, and there was no significant difference between the two groups. In the E-group, the amplitude of the COM during the backward COP shift was significantly greater than that during the forward COP shift (p < 0.05). 3.2. Joints involved in the postural strategy of elderly participants The ANOVA results showed that there was a significant interaction (age task joint site) for the change of joint angle (F(2, 336) = 5.73, p < 0.01, h2 = 0.02). The post-hoc test revealed that plantar flexion in the ankle joint in the E-group tended to be greater than that in the Y-group (p = 0.052, Fig. 2a) during the forward COP shift and that during the backward COP shift, the dorsal flexion in the ankle joint was significantly greater in the E-group compared with the Y-group (p < 0.05, Fig. 2b). For the backward COP shift, the ankle joint of the elderly group performed the opposite motion relative to that of the younger group (Fig. 2c). Moreover, flexion of the knee joint in the E-group was significantly greater compared to that in the Y-group during the backward COP shift (p < 0.05, Fig. 2b). 3.3. Identification of muscles involved in the shift in postural strategy The ANOVA revealed significant differences in muscle activities between the different tasks in both groups (Fig. 3). The activities of the ventral and dorsal muscles were significantly increased during the backward and forward COP shifts, respectively (both p < 0.01, Fig. 3a and b). The factor analysis results are shown in Table 2. The analyses of the scree plot revealed two factors with eigenvalues of >1 in both groups. For the Y-group, the first factor (38.4%) and second factor (30.5%) accounted for 68.9% of the variance. For the E-group, the first factor (35.4%) and second factor (21.0%) accounted for 56.4% of the variance. Based on the resulting loading coefficients of the rotated solution, the first factor differed between groups (Table 2). The first and second factors in the Y-group were the ventral and dorsal muscle groups, respectively. In the E-group, the BF in the dorsal muscles was detected as the first factor, while the ventral muscle group was detected as the second factor. 4. Discussion
Fig. 1. Comparison of the maximum COP shift (a), anteroposterior COM displacement (b), and vertical COM displacement (c) between the elderly and young groups during each COP shift. The error bars represent standard deviations. *p < 0.01 between groups. COP, center of pressure; COM, center of mass.
Previous investigations of postural control have primarily focused on the A/P or M/L directions. The purpose of this study was to examine the effect of aging on vertical postural control through vertical movement of the COM, and furthermore to relate the vertical postural strategy to muscle synergy in the elderly. Our findings, with respect to the lowered COM position and the change in postural muscle activity, suggest that vertical postural control is influenced by aging. As the COP shift decreases with age, a deficit is particularly observed in the posterior direction [13]. The elderly tend to rely more on visual input for postural control since somatosensory input becomes less reliable with age [18]. As a compensatory
Please cite this article in press as: Kasahara S, et al. The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.07.056
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Fig. 2. Comparison of changes in the hip, knee, and ankle angles during each COP-shift task between the elderly (EG) and young (YG) groups, as assessed with respect to a static standing position. Positive values on the y-axis represent changes in flexion/dorsal flexion, and negative values represent changes in extension/plantar flexion. *p < 0.01 between groups. (c) is a visual summary and comparison of movement strategies between groups and between directions during COP shift. COP, center of pressure.
change, vison is known to help maintain postural stability, especially when another sensory system is compromised in the elderly [19,20]. Although participants’ vision was not blocked (e.g., with a blindfold) in this study, participants only received visual information from the field in front of them; there was no information from behind, which may have contributed to a fear of falling backward in older people [21]. In the present study, the results of the COM were the same as those of the COP shift,
suggesting that COM and COP are closely linked during quiet standing [10]. On the other hand, the vertical position of the COM in the elderly group was significantly lower during the backward COP shift compared to that in the young group. A lower COM position has been shown to decrease the mean velocity of the COP and the root mean square as a parameter of postural sway during quiet standing [9,10] and could contribute to postural stabilization of elders from the view of the stability of a rigid body
Please cite this article in press as: Kasahara S, et al. The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.07.056
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Fig. 3. Muscle activities during each COP-shift task. F, forward COP shift; C, static stance; B, backward COP shift. The EMG scale is in arbitrary units. *p < 0.01 between tasks. COP, center of pressure; EMG, electromyography.
[10]. However, although a lower COM can achieve stabilization during standing, a disadvantage is a loss of mobility. Therefore, the vertical COM may indicate a trade-off in stability and mobility. In general, three strategies are used to achieve postural control during standing [22]. Postural control in the A/P and M/L directions during standing is performed by the ankle strategy
and the hip strategy, respectively [14]. The third strategy is the suspensory strategy, which employs the flexing of the leg joints to lower the COM toward the base of support [22]. This strategy is often observed during a strong disturbance on the moving platform and the knee is added to the postural control involving the hip and the ankle to stabilize the standing posture [23,24].
Table 2 Factor loading of the factor analysis in each group. YG
EG
Factor 1
Factor 2
1. Ventral muscles rectus abdominis m. rectus femoris m. tibialis anterior m.
0.708 0.750 0.757
0.066 0.068 0.204
2. Dorsal muscles erector spinae m. biceps femoris m. gastrocnemius m.
0.151 0.106 0.087
0.621 0.853 0.639
h2
h2
Factor 1
Factor 2
0.505 0.568 0.614
0.007 0.163 0.164
0.579 0.648 0.586
0.335 0.447 0.370
0.408 0.739 0.416
0.333 0.937 0.383
0.020 0.117 0.270
0.111 0.891 0.220
Loadings over the absolute value of 0.4 are shown in bold. h2: communality, YG: young group, EG: elderly group.
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The knee joint is located between the hip and the ankle and interacts with both hip and ankle joints in a multi-segmental control strategy [24]. However, the role of the knee has not been the focus of investigation, based on the supposition that knee joint motion is negligible in a voluntary task during the upright stance [14,18]. Although the joint angle of the knee was small in the present study, the knee joint of the elderly group showed more flexion during the backward COP shift as compared to that of the young group. Additionally, a significant downward displacement of the COM was observed in the elderly group but not the young group during the backward COP. Based on our findings, we speculate that the suspensory strategy contributes to lowering the COM for stabilizing posture during the backward COP shift in the elderly and that the knee becomes functional in vertical postural control (Fig. 2c). Naturally, the application of the knee in the suspensory strategy would relate to the differing utilization of the ankle joint. Our electromyogram results are in agreement with previous findings on the activation patterns of ventral and dorsal postural muscles in the A/P direction by a disturbance [11] or voluntary sway [25]. Another finding in this study was that the BF was a noticeable factor in the elderly participants. Biarticular muscles such as the BF may be related to both postural strategy and antigravity control [11,22,26,27] adopted during standing among the aging. Postural control becomes complex because, following displacement of the body from its vertical alignment during a forward or backward COP shift, the force of gravity accelerates body motion progression [11]. The hamstrings over the hip and knee joints in elderly individuals were suggested to participate actively as part of an additional compensatory activity for effectively controlling the COP [26]. Another possible explanation for BF participation could be aging-associated posterior muscle chain stiffness [28,29]. Although it is difficult to identify the factor underlying increased EMG signals, changes in leg muscle activity in elders suggest the exception from the muscle synergy observed in youths. This study had several limitations, the first of which is the difference in sex distribution between groups. Second, activities of the deep muscles were not measured; however, aging has been found to have a smaller effect on these muscles as compared to superficial ones [30]. Therefore, we investigated the superficial activity of postural muscles using surface electromyograms. Third, this study did not examine the COP shift in the M/L direction. Hence, it is possible that muscle activation changes according to motor direction. However, even if the COP or COM shift were to occur in the M/L direction, the downward vertical postural strategy would still be helpful for postural stabilization. Fourth, other characteristics of aging related to balance (e.g., sensation, muscle strength, joint stiffness, cognition, etc.) were not measured. Therefore, further study is required to understand effects of aging on postural control in elderly individuals.
5. Conclusions We have shown here that balance in the elderly is reduced relative to that in younger individuals. In particular, backward postural control shifted to a postural strategy that lowered the COM in the vertical direction to stabilize the standing posture for self-paced perturbation. Two muscle synergies (i.e., ventral and dorsal) were identified in both the elderly and young participants during the voluntary COP-shift task. Moreover, in the elderly individuals, the BF was found to be an important postural muscle. These findings indicate that vertical postural control, namely antigravity control, is influenced by aging along with A/P control.
Author contributions Conception and design of the study: SK. Acquisition and analysis of data: SK, TA, HO. Drafting and revising the manuscript: SK, HS. All the authors approve of the final version of this manuscript for publication. Acknowledgments This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sport, Science and Technology of Japan (21700518 and 24500566). The sponsor had no role 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.
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The effect of aging on vertical postural control during the forward and backward shift of the center of pressure Satoshi Kasahara a,*, Hiroshi Saito a, Tsubasa Anjiki b, Hitomi Osanai c a
Department of Rehabilitation Sciences, Faculty of Health Sciences, Hokkaido University, Sapporo, Japan Department of Rehabilitation, Hatsudai Rehabilitation Hospital, Tokyo, Japan c Department of Rehabilitation, Kasai Shoikai Hospital, Tokyo, Japan b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 16 December 2014 Received in revised form 15 July 2015 Accepted 22 July 2015
Preventing fall-related injuries is becoming a priority as the world population ages. This study’s purpose was to examine the effect of aging on vertical postural control in the community-dwelling elderly. Thirty-six elderly individuals and twenty-two healthy young adults were asked to shift their centers of pressure (COPs) as far as possible while standing. The COP position, angle of each lower leg joint, and postural muscle activities were measured using a force plate, three-dimensional motion analyzer, and electromyogram, respectively. The vertical position of the center of mass (COM) was also measured to assess the change in vertical postural control. The backward COP shift in the elderly group was significantly smaller than that in the young group, and both the forward and backward COM shifts were significantly smaller in elders relative to those in youths. The COM position in the elderly group during the backward COP shift was also significantly lower than that in the young group. Knee and ankle joint movements differed between the two groups during the backward COP shift. Factor analysis indicated that dorsal and ventral muscle groups were involved in the COP shift. Specifically, the relationship between the biceps femoris muscle and the voluntary COP shift was reinforced in the elderly group. These findings suggest that the vertical postural strategy changes in the elderly during the backward COP shift. ß 2015 Published by Elsevier B.V.
Keywords: Aging Vertical postural control Postural strategy Muscle synergy Center of mass
1. Introduction Falls are the most serious cause of hip and wrist fractures and head injuries among the elderly [1]. Major factors contributing to falls among the elderly are the reduced physiological capacity that occurs with aging and decreased balance [2–4]. Furthermore, the risk of falls among the elderly is affected by the interactions of the organism, environment, and task [5]. More than 30% of community-dwelling elderly people and those in long-term care facilities report at least one indoor fall per year [1], with 10–15% of these falls resulting in significant injury [6]. The most common problem among the elderly is reported to be incorrect transfer or weightshifting performed by the individual (i.e., self-paced) [1]. A smooth shift of the center of pressure (COP) and center of mass (COM) is essential for transferring or shifting body weight
* Corresponding author at: Department of Rehabilitation Sciences, Faculty of Health Sciences, Hokkaido University, West 5, North 12, Kita-ku, Sapporo 060-0812, Japan. Tel.: +81 11 706 3391; fax: +81 11 706 3391. E-mail address: [email protected] (S. Kasahara).
during activities of daily living, and analyses of such shifts have often been used in previous studies [7–10]. In terms of balance ability, the elderly have been reported to show smaller maximum displacement [7] and greater reaction and movement times [8] during a voluntary COP shift when compared to those in the young. COP has been measured and analyzed in the anterior-posterior (A/P) and/or medial-lateral (M/L) directions, because COP movement is performed two-dimensionally within the base of support [9]. Although researchers have focused on the A/P and/or M/L directions with respect to the COM in relation to the COP [10], the actual COM has three-dimensional (3-D) motion, because the vertical direction is added to these directions. Recent studies have reported that higher COM positions decreased postural stability and lower COM positions improved standing stability [9,10]; thus 3-D postural control requires vertical changes as well as A/P and M/L changes. However, to our knowledge, no study has attempted to clarify postural control further in humans during the erect stance through examining the COM in the vertical dimension. In this study, we aimed to evaluate the effect of aging on vertical postural control by investigating the COM in the vertical direction during a task involving a self-paced dynamic shift in the COP. We
http://dx.doi.org/10.1016/j.gaitpost.2015.07.056 0966-6362/ß 2015 Published by Elsevier B.V.
Please cite this article in press as: Kasahara S, et al. The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.07.056
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anticipated that the vertical position of the COM would differ between elderly and young individuals because of differences in the adopted postural strategy [3,4]. Additionally, we hypothesized that changes in the vertical postural strategy as a consequence of aging would be related to activity in the postural muscles, which specifically control the knee joint and thereby movement in the vertical axis [11].
2. Methods 2.1. Participants Twenty-two healthy young adults (Y-Group: 13 women and 9 men; mean age, 20.6 1.0 years) and 36 healthy elderly adults (E-Group: 36 men; mean age, 69.5 3.2 years) participated. The body characteristics in both groups were similar (Table 1). Young participants were randomly selected from among college students who volunteered to participate in this study. Elderly participants >65 years old with no history of any neurological or orthopedic diseases or ophthalmologic conditions that could contribute to movement dysfunction were randomly selected from among communitydwelling elderly who had registered with the employment agency. None had had a history of falls for at least 6 months before enrollment in the study or took any medication that could affect balance [12]. All study participants provided written informed consent to participate, and the procedures were approved by the ethics committee of Hokkaido University School of Medicine (no. 11-03). 2.2. Experimental tasks Participants stood with bare feet and their legs shoulder-width apart on a force plate (Kistler, Type 9286A, Switzerland) with their arms crossed in front of their chests. Visual feedback information about the COP position was provided to participants from a computer monitor, and the start position of the COP was located 5.0 cm in front of the middle of the line joining both medial malleoluses to ensure a backward motion range. After the examiner checked the steady state of the COP within 1 cm of the start position, the power to the monitor was turned off, and each trial was started. Participants performed the three tasks of: (1) maintaining a static stance; (2) shifting to the maximum forward COP position; and (3) shifting to the maximum backward COP position [13]. Participants were instructed to shift the COP as far as possible and not to raise their toes or heels and to stably maintain their COP position. Participants were given no instruction regarding the use of leg joints in order to avoid a bias in postural strategy. Each task was performed 3 times in a random order, with sufficient rest between tasks to prevent fatigue. 2.3. Data acquisition and processing Force and muscle activity data were digitized at a frequency of 1 kHz by an NI Compact DAQ (National Instruments, Austin, TX,
Table 1 Descriptive statistics of the participants according to age. YG (n = 22)
Age (year) Height (cm) Weight (kg) BMI (kg/m2)
EG (n = 36)
Mean SD
Range
Mean SD
Range
20.6 1.0 165.9 8.9 58.4 9.5 21.1 2.1
20–24 152–181 44–75 17.6–25.3
69.5 3.2* 163.9 5.2 62.8 5.2 23.4 2.4
65–78 153–172 49–85 19.3–28.7
YG: young group, EG: elderly group, BMI: body mass index, SD: standard deviation * p < 0.05 between the YG and EG groups.
USA), and the COP position was subsequently calculated with force data using a customized program (Labview 2009; National Instruments, Austin, TX, USA). Surface electromyography (EMG) data were collected using the Delsys EMG system (Bagnoli-2EMG System; DELSYS, Boston, MA). Activity was recorded for each of the following 6 postural muscles according to previous studies [2,3,11,12]: the rectus abdominis (RA), erector spinae (ES), rectus femoris (RF), biceps femoris (BF), tibialis anterior (TA), and gastrocnemius (GAS) muscles. EMG sensors were attached to the belly of the target muscle, and reference electrodes were attached to the iliac crest, the head of the fibula, and the lateral malleolus [2,3,11,12]. A 3-D motion analysis system with 6 cameras at a sampling rate of 100 Hz was used to compute the angles of the hip, knee, and ankle joints and the position of the COM (Motion Analysis Corporation, Santa Rosa, CA, USA). Reflective markers were attached based on the anatomical landmark locations used by Winter [14]. All markers were located bilaterally, except for those at the top, front, and back of the head; the acromion process; the angulus inferior scapulae; and the sacrum. Positive values of calculated joint angles show flexion and dorsal flexion, and negative values show extension and plantar flexion. All off-line data processing was performed with the customized Matlab program (Mathworks, Natick, MA, USA). COP and COM data were low-pass filtered with a zero-lag, second-order Butterworth filter with a cut-off frequency of 10 Hz. The distance from the start position to the maximum COP and COM positions in either the anterior or posterior direction was subsequently measured for each task. The A/P displacement of the COP and the COM was normalized by dividing it by the length of each participant’s foot [14]. Vertical displacement was calculated by subtracting the start position of the COM from the COM position during the maximum COP shift and subsequently normalized by each participant’s height. Surface EMG data were rectified and band-pass filtered from 10 to 500 Hz using a fourth-order Butterworth filter. The magnitude of muscle activity was evaluated using the mean amplitude of each muscle’s activity in maintaining a stable COP after the completion of a COP shift. The change in each joint angle was calculated by subtracting the value obtained during the static stance from the joint angle at each maximum COP shift. 2.4. Statistical analysis All statistical analyses were performed using PASW Statistics 18 (SPSS Inc., Chicago, IL). All data are shown as the mean and standard deviation of the three trials for each task in each group. An analysis of variance (ANOVA) was used to examine the interactive effects of age and movement direction. If a significant interaction was identified, the simple main effect was further analyzed with a post-hoc paired t-test with Bonferroni corrections. A p value <0.05 was considered statistically significant. The effect sizes from the ANOVA are expressed as eta-squared (h2) values, and the effect sizes for differences in the means are expressed as Cohen’s d values [15]. After performing the ANOVA for muscle activities among tasks in each group, we conducted an exploratory factor analysis with the principal factor method to identify the factor structure of the muscle activities for postural strategy during the COP shift. An optimal factor solution was determined based on eigenvalues of >1.0 [16], and on an examination of the scree plot using all 6 muscle activities. For the optimal factor solution, principal axis factoring with varimax rotation and Kaiser’s normalization were used to determine the latent variables that best explained the observed variability in each EMG. After the rotation, any variable that significantly loaded on more than one factor (with an absolute value >0.4) was identified and removed [17].
Please cite this article in press as: Kasahara S, et al. The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.07.056
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3. Results 3.1. Comparison of COP and COM between Elderly and Young Participants The ANOVA showed a significant interactive effect (age direcdirection) for COP displacement (F(1, 112) = 7.36, p < 0.01, h2 = 0.04). The backward COP displacement of the E-group was 28.9% lower than that of the Y-group (p < 0.01, Fig. 1a). In the E-group, the backward displacement was significantly smaller (a decrease of 30%) than the forward displacement (p < 0.01).
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There was a significant interactive effect (age task) for COM A/P displacement (F(2, 168) = 14.65, p < 0.01, h2 = 0.04). The COM A/P displacement in the E-group during both the forward and backward COP shift was significantly smaller than that in the Y-group (p < 0.01, Fig. 1b). In the E-group, COM amplitude during the backward COP shift was significantly smaller than that during the forward COP shift (p < 0.01). For vertical COM displacement, there was a significant interactive effect (age direction) (F(1, 112) = 7.19, p < 0.01, h2 = 0.09). The posthoc test showed that vertical COM displacement in the E-group during the backward COP shift was significantly lower than that in the Y-group (p < 0.01, Fig. 1c). On the other hand, the COM was lower in both groups during the forward COP shift, and there was no significant difference between the two groups. In the E-group, the amplitude of the COM during the backward COP shift was significantly greater than that during the forward COP shift (p < 0.05). 3.2. Joints involved in the postural strategy of elderly participants The ANOVA results showed that there was a significant interaction (age task joint site) for the change of joint angle (F(2, 336) = 5.73, p < 0.01, h2 = 0.02). The post-hoc test revealed that plantar flexion in the ankle joint in the E-group tended to be greater than that in the Y-group (p = 0.052, Fig. 2a) during the forward COP shift and that during the backward COP shift, the dorsal flexion in the ankle joint was significantly greater in the E-group compared with the Y-group (p < 0.05, Fig. 2b). For the backward COP shift, the ankle joint of the elderly group performed the opposite motion relative to that of the younger group (Fig. 2c). Moreover, flexion of the knee joint in the E-group was significantly greater compared to that in the Y-group during the backward COP shift (p < 0.05, Fig. 2b). 3.3. Identification of muscles involved in the shift in postural strategy The ANOVA revealed significant differences in muscle activities between the different tasks in both groups (Fig. 3). The activities of the ventral and dorsal muscles were significantly increased during the backward and forward COP shifts, respectively (both p < 0.01, Fig. 3a and b). The factor analysis results are shown in Table 2. The analyses of the scree plot revealed two factors with eigenvalues of >1 in both groups. For the Y-group, the first factor (38.4%) and second factor (30.5%) accounted for 68.9% of the variance. For the E-group, the first factor (35.4%) and second factor (21.0%) accounted for 56.4% of the variance. Based on the resulting loading coefficients of the rotated solution, the first factor differed between groups (Table 2). The first and second factors in the Y-group were the ventral and dorsal muscle groups, respectively. In the E-group, the BF in the dorsal muscles was detected as the first factor, while the ventral muscle group was detected as the second factor. 4. Discussion
Fig. 1. Comparison of the maximum COP shift (a), anteroposterior COM displacement (b), and vertical COM displacement (c) between the elderly and young groups during each COP shift. The error bars represent standard deviations. *p < 0.01 between groups. COP, center of pressure; COM, center of mass.
Previous investigations of postural control have primarily focused on the A/P or M/L directions. The purpose of this study was to examine the effect of aging on vertical postural control through vertical movement of the COM, and furthermore to relate the vertical postural strategy to muscle synergy in the elderly. Our findings, with respect to the lowered COM position and the change in postural muscle activity, suggest that vertical postural control is influenced by aging. As the COP shift decreases with age, a deficit is particularly observed in the posterior direction [13]. The elderly tend to rely more on visual input for postural control since somatosensory input becomes less reliable with age [18]. As a compensatory
Please cite this article in press as: Kasahara S, et al. The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.07.056
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Fig. 2. Comparison of changes in the hip, knee, and ankle angles during each COP-shift task between the elderly (EG) and young (YG) groups, as assessed with respect to a static standing position. Positive values on the y-axis represent changes in flexion/dorsal flexion, and negative values represent changes in extension/plantar flexion. *p < 0.01 between groups. (c) is a visual summary and comparison of movement strategies between groups and between directions during COP shift. COP, center of pressure.
change, vison is known to help maintain postural stability, especially when another sensory system is compromised in the elderly [19,20]. Although participants’ vision was not blocked (e.g., with a blindfold) in this study, participants only received visual information from the field in front of them; there was no information from behind, which may have contributed to a fear of falling backward in older people [21]. In the present study, the results of the COM were the same as those of the COP shift,
suggesting that COM and COP are closely linked during quiet standing [10]. On the other hand, the vertical position of the COM in the elderly group was significantly lower during the backward COP shift compared to that in the young group. A lower COM position has been shown to decrease the mean velocity of the COP and the root mean square as a parameter of postural sway during quiet standing [9,10] and could contribute to postural stabilization of elders from the view of the stability of a rigid body
Please cite this article in press as: Kasahara S, et al. The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.07.056
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Fig. 3. Muscle activities during each COP-shift task. F, forward COP shift; C, static stance; B, backward COP shift. The EMG scale is in arbitrary units. *p < 0.01 between tasks. COP, center of pressure; EMG, electromyography.
[10]. However, although a lower COM can achieve stabilization during standing, a disadvantage is a loss of mobility. Therefore, the vertical COM may indicate a trade-off in stability and mobility. In general, three strategies are used to achieve postural control during standing [22]. Postural control in the A/P and M/L directions during standing is performed by the ankle strategy
and the hip strategy, respectively [14]. The third strategy is the suspensory strategy, which employs the flexing of the leg joints to lower the COM toward the base of support [22]. This strategy is often observed during a strong disturbance on the moving platform and the knee is added to the postural control involving the hip and the ankle to stabilize the standing posture [23,24].
Table 2 Factor loading of the factor analysis in each group. YG
EG
Factor 1
Factor 2
1. Ventral muscles rectus abdominis m. rectus femoris m. tibialis anterior m.
0.708 0.750 0.757
0.066 0.068 0.204
2. Dorsal muscles erector spinae m. biceps femoris m. gastrocnemius m.
0.151 0.106 0.087
0.621 0.853 0.639
h2
h2
Factor 1
Factor 2
0.505 0.568 0.614
0.007 0.163 0.164
0.579 0.648 0.586
0.335 0.447 0.370
0.408 0.739 0.416
0.333 0.937 0.383
0.020 0.117 0.270
0.111 0.891 0.220
Loadings over the absolute value of 0.4 are shown in bold. h2: communality, YG: young group, EG: elderly group.
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The knee joint is located between the hip and the ankle and interacts with both hip and ankle joints in a multi-segmental control strategy [24]. However, the role of the knee has not been the focus of investigation, based on the supposition that knee joint motion is negligible in a voluntary task during the upright stance [14,18]. Although the joint angle of the knee was small in the present study, the knee joint of the elderly group showed more flexion during the backward COP shift as compared to that of the young group. Additionally, a significant downward displacement of the COM was observed in the elderly group but not the young group during the backward COP. Based on our findings, we speculate that the suspensory strategy contributes to lowering the COM for stabilizing posture during the backward COP shift in the elderly and that the knee becomes functional in vertical postural control (Fig. 2c). Naturally, the application of the knee in the suspensory strategy would relate to the differing utilization of the ankle joint. Our electromyogram results are in agreement with previous findings on the activation patterns of ventral and dorsal postural muscles in the A/P direction by a disturbance [11] or voluntary sway [25]. Another finding in this study was that the BF was a noticeable factor in the elderly participants. Biarticular muscles such as the BF may be related to both postural strategy and antigravity control [11,22,26,27] adopted during standing among the aging. Postural control becomes complex because, following displacement of the body from its vertical alignment during a forward or backward COP shift, the force of gravity accelerates body motion progression [11]. The hamstrings over the hip and knee joints in elderly individuals were suggested to participate actively as part of an additional compensatory activity for effectively controlling the COP [26]. Another possible explanation for BF participation could be aging-associated posterior muscle chain stiffness [28,29]. Although it is difficult to identify the factor underlying increased EMG signals, changes in leg muscle activity in elders suggest the exception from the muscle synergy observed in youths. This study had several limitations, the first of which is the difference in sex distribution between groups. Second, activities of the deep muscles were not measured; however, aging has been found to have a smaller effect on these muscles as compared to superficial ones [30]. Therefore, we investigated the superficial activity of postural muscles using surface electromyograms. Third, this study did not examine the COP shift in the M/L direction. Hence, it is possible that muscle activation changes according to motor direction. However, even if the COP or COM shift were to occur in the M/L direction, the downward vertical postural strategy would still be helpful for postural stabilization. Fourth, other characteristics of aging related to balance (e.g., sensation, muscle strength, joint stiffness, cognition, etc.) were not measured. Therefore, further study is required to understand effects of aging on postural control in elderly individuals.
5. Conclusions We have shown here that balance in the elderly is reduced relative to that in younger individuals. In particular, backward postural control shifted to a postural strategy that lowered the COM in the vertical direction to stabilize the standing posture for self-paced perturbation. Two muscle synergies (i.e., ventral and dorsal) were identified in both the elderly and young participants during the voluntary COP-shift task. Moreover, in the elderly individuals, the BF was found to be an important postural muscle. These findings indicate that vertical postural control, namely antigravity control, is influenced by aging along with A/P control.
Author contributions Conception and design of the study: SK. Acquisition and analysis of data: SK, TA, HO. Drafting and revising the manuscript: SK, HS. All the authors approve of the final version of this manuscript for publication. Acknowledgments This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sport, Science and Technology of Japan (21700518 and 24500566). The sponsor had no role 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.
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Please cite this article in press as: Kasahara S, et al. The effect of aging on vertical postural control during the forward and backward shift of the center of pressure. Gait Posture (2015), http://dx.doi.org/10.1016/j.gaitpost.2015.07.056