© 2014 John Wiley & Sons A/S.
Scand J Med Sci Sports 2014: ••: ••–•• doi: 10.1111/sms.12256
Published by John Wiley & Sons Ltd
Regular physical activity reduces the effects of Achilles tendon vibration on postural control for older women J. Maitre1,2, I. Serres1, L. Lhuisset1, J. Bois1, Y. Gasnier3, T. Paillard1 1
Laboratoire Activité Physique, Performance et Santé, EA 4445, Département STAPS, Université de Pau et des Pays de l’Adour, Tarbes, France, 2Office Départemental des Sports des Hautes-Pyrénées, Tarbes, France, 3Centre Hospitalier de Bigorre, Vic en Bigorre, France Corresponding author: Julien Maitre, PhD, Laboratoire Activité Physique, Performance et Santé, EA 4445, Université de Pau et des Pays de l’Adour, Département STAPS, ZA Bastillac Sud, 65000 Tarbes, France. Tel: 33(0)562566100, Fax: 33(0)562566110, E-mail: [email protected] Accepted for publication 22 April 2014
The aim was to determine in what extent physical activity influences postural control when visual, vestibular, and/or proprioceptive systems are disrupted. Two groups of healthy older women: an active group (74.0 ± 3.8 years) who practiced physical activities and a sedentary group (74.7 ± 6.3 years) who did not, underwent 12 postural conditions consisted in altering information emanating from sensory systems by means of sensory manipulations (i.e., eyes closed, cervical collar, tendon vibration, electromyostimulation, galvanic vestibular stimulation, foam surface). The center of foot pressure velocity was
recorded on a force platform. Results indicate that the sensory manipulations altered postural control. The sedentary group was more disturbed than the active group by the use of tendon vibration. There was no clear difference between the two groups in the other conditions. This study suggests that the practice of physical activities is beneficial as a means of limiting the effects of tendon vibration on postural control through a better use of the not manipulated sensory systems and/or a more efficient reweighting to proprioceptive information from regions unaffected by the tendon vibration.
The ability to maintain balance implies the efficiency of the sensory, integrating, and motor systems (Massion, 1994; Peterka, 2002). The effects of aging affect this efficiency and can increase the risk of falls and fallrelated injuries (Lord & Sturnieks, 2005; Sturnieks et al., 2008). Falls can lead to hospitalization and mark the beginning of dependency (Bradley, 2011). Instead, physical activities improve balance abilities (Perrin et al., 1999; Howe et al., 2007). The repetition of specific movements of the body segments and body as a whole, resulting from the practice of physical activities, induces adaptations of the postural control mechanism through a better use of sensory information and motor output (Gauchard et al., 1999, 2001, 2003; Paillard et al., 2004; Ribeiro & Oliveira, 2007). Several studies have tried to quantify the impact of regular physical and/or sports activities on the postural control mechanism through the use of external perturbations altering information emanating from some sensory systems (Hu & Woollacott, 1994; Perrin et al., 1999; Hue et al., 2004; Tsang et al., 2004). It has been demonstrated that external perturbations result in compensatory postural strategies (Horak & Nashner, 1986) and sensory reweighting (Oie et al., 2002) which enable balance disturbance to be counteracted or limited. Thus, it is possible to detect the extent to which an older subject is able
to improve his or her postural performance (e.g., postural stability) and strategy (involvement of different neural loops) in disturbing condition after a period of physical practice. Yet, the effects of physical activities on postural control studied by creating external perturbations have been only partially analyzed in older subjects (Hu & Woollacott, 1994; Perrin et al., 1999; Hue et al., 2004; Tsang et al., 2004). No study has analyzed the effects of physical activities on all of the sensory systems in the same protocol which would enable precise identification of the main sensory adaptations induced. In order to assess postural adaptations, the technique of sensory manipulation (Balter et al., 2004; Fransson et al., 2004; Hue et al., 2004; Paillard et al., 2007) (e.g., vibration, electromyostimulation, or vestibular galvanic stimulation) can be used as external perturbation that alters information emanating from one sensory system (referred to in this article as the “manipulated” sensory system). Furthermore, different sensory manipulations may also be combined to leave only one sensory system unmanipulated (referred to in this article as the “nonmanipulated” sensory system). Hence, the aim of this study was to determine the influence of physical activities on different neural loops involved in postural control through the use of sensory manipulations in healthy older subjects. We hypothesized that regular physical
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Maitre et al. activities may improve the use of some sensory channels more than the use of others. Moreover, some studies have reported differences between men and women population in postural control (Era et al., 2006; Kim et al., 2010, 2012a,b). Hence, to exclude the influence of an eventual gender effect, we have voluntary chosen to focus only on women subjects in this study. Materials and methods Participants Thirty-four healthy women, all above the age of 64 and shown to be free from any cognitive, neurological, motor, and metabolic disorders after medical examination, participated in the study. They were divided into two groups: one group of 17 active subjects (the active group) and one group of 17 sedentary subjects (the sedentary group). Age and anthropometrical data are presented in Table 1. This experimental procedure received the approval of the local committee for the protection of human subjects and all subjects gave informed consent. After interviewing each subject, we included, in the active group, persons who have regularly practiced physical activity (at least 3 h per week) in a sports club (e.g., gym, walking, dancing, aquarobics) for at least 3 years. We included, in the sedentary group, persons who have not practiced physical activity (either at home or in a sports club), apart from daily tasks, for at least 3 years. All the subjects lived independently at home. Exclusion criteria included a documented postural control disorder or a medical condition that might affect postural control, a neurological or a musculoskeletal impairment, or current injury making the subjects unable to participate. Thus, we excluded persons who were not able to walk without a walking stick and who were in a nursing home. Concerning the medical examination criteria, we excluded persons in the following categories: those who had suffered hip, knee, or ankle traumatism in the previous 2 years, or lesion of the foot skin support surface, or ankylosis of the large lower limb joints (hip, knee, ankle); those who had disabling low vision, despite a correction, or suffered from chronic respiratory insufficiency requiring treatment with oxygen therapy; those undergoing medical treatment (bronchodilators, beta-blockers, corticosteroid, neuroleptics); those with cardiovascular disease (coronary artery disease, myocardial infarction, congestive heart failure, permanent or paroxysmal heart rhythm disturbances, poorly controlled hypertension); or neurological deficit; or disorders of higher functions, tone, sensitivity, and balance. The subjects were questioned as to whether abnormal cutaneous sensations were experienced. The cutaneous sensations under the feet were screened with a pencil. Concerning vestibular function, the subjects were questioned about history of vertigo and abnormal ocular nystagmus was screened.
Experimental protocol The experiment examined possible postural modifications when sensory systems were altered by means of one sensory Table 1. Active and sedentary groups’ age, anthropometrical data, and physical activity status [mean (SD) median]
Age (year) Height (cm) Weight (kg) Foot size (cm) Physical activity Past physical activity
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Active group
Sedentary group
74.0 (3.8) 73.4 156.6 (4.2) 155.0 63.2 (6.9) 65.0 25.6 (0.8) 26.0 ≥ 3 hours per week For at least 3 years
74.7 (6.3) 73.7 155.8 (5.7) 155.0 62.4 (9.0) 62.0 25.3 (0.7) 25.3 None None
manipulation, or several sensory manipulations. Sensory manipulations were used to alter one sensory system (referred to as the “manipulated condition”) or all sensory systems except one (referred to as the “non-manipulated condition”). Each subject underwent 14 different conditions, each lasting 20 s and separated by 2 min. To avoid the training effect, one trial was carried out to adapt the subjects to the exercise prior to the recording. Two reference conditions were measured with eyes open on the force platform (see section on postural control). The initial measure, at the beginning of the protocol, was REF1. The final measure at the end of the protocol was REF2 (after the completion of 12 challenging postural conditions). REF1 and REF2 were compared to ensure that there was no fatigue effect on the procedure, which could alter postural measurement. The 12 conditions’ order was partially counterbalanced. These conditions were randomized for each subject in the same group and compared with REF1. The main objective of the 12 other conditions was to manipulate or modify proprioceptive and/or exteroceptive information. To avoid initial transients and anticipation behavior being recorded at the onset of the sensory disturbance, each sensory manipulation was set up in a range of 5 s before the recording of postural sway data.
Manipulated sensory conditions Sensory manipulations were used to alter or modulate afferences emanating from specific sensory receptors of the visual, vestibular, proprioceptive, and plantar cutaneous sensory systems in order to evaluate their postural modifications on a force platform in the following conditions (when only one specific sensory receptor was manipulated all others were available): • Eyes closed (EC): Subjects were instructed to keep their eyes closed. The aim was to eliminate the contribution of visual information in postural regulation (Edwards, 1946). • Foam surface (Foam): Subjects were instructed to stand on a foam surface (15 mm, 70 kg/m3) (TG700, Domyos®, Villeneuve d’Ascq, France) placed on the force platform. The aim was to alter the contribution of cutaneous information in postural regulation (Chiang & Wu, 1997). • Cervical collar (CCollar): Subjects were instructed to wear a rigid cervical collar (C3, Thuasne®, Levallois-Perret, France). The aim was to render jointly liable the head with the trunk to limit information from the cervical joints (Paillard et al., 2007). • Electromyostimulation (ES): Electromyostimulation was applied on the gastrocnemius medialis and lateralis muscles, and the vastus medialis and lateralis muscles of both legs with a current stimulator (Rehab 4 Pro, Cefar™, Malmö, Sweden). One electrode (50 × 90 mm) (Sport-elec®, Luxembourg, Luxembourg) was placed over the motor point on each of the four muscles with a biphasic symmetric square wave (continuous pulse 350 μs, 15 mA, 80 Hz). The aim was to disturb the myotatic proprioceptive information (Hoffman & Koceja, 1997; Paillard et al., 2007). • Tendon vibration (TV): Vibration was continuously applied to the Achilles tendons of both legs by means of inertial vibrators (VB 115, Techno Concept™, Céreste, France) secured with elastic bands. Vibration frequency was set at 40 Hz and the amplitude was 0.85 mm. The aim was to modulate Ia afferences (Roll & Vedel, 1982; Roll et al., 1989). • Galvanic vestibular stimulation (GVS): A 1 mA transmastoidal galvanic vestibular stimulation was delivered by a constant-current stimulator (Galvadyn 2, Electronic Conseil, Gallargues le Montueux, France) through two disposable electrodes (T-Tracet, Contrôle-Graphique, BrieComte-Robert, France). The aim was to induce an asymmetry of vestibular activity (Wardman & Fitzpatrick, 2002). The electrodes were placed over each mastoid process, for a
Physical activity and postural control binaural bipolar design. The current was applied continuously without polarity shifts. To avoid any local noxious sensation, an anesthetic gel was applied onto each mastoid process. Subjects were measured in two different polarity conditions: • GVSAnode right: anode placed on the right mastoid process and cathode placed on the left mastoid process. • GVSAnode left: anode placed on the left mastoid process and cathode placed on the right mastoid process.
were separately compared with the REF1 condition using the paired-samples Wilcoxon–Mann–Whitney test. To determine if there were differences between the two groups, all the parameters were compared for the active and the sedentary groups, using the non-parametric Wilcoxon–Mann–Whitney test: anthropometric data (age, weight, height, foot size) and COP velocity on the X and Y axes with their absolute increase. Results were considered significant at the level of 5%.
Results Combined sensory manipulation conditions A combination of sensory manipulations was used to alter all the proprioceptive information: • Proprioceptive information manipulated (Proprio manip): CCollar + ES + TV A combination of sensory manipulations was used to alter all the sensory systems except one: • Vestibular information not manipulated (Vestibular nonmanip): EC + Foam + ES + TV + CCollar • Proprioceptive information not manipulated (Proprio nonmanip): EC + GVS + Foam • Cutaneous information not manipulated (Cutaneous nonmanip): EC + CCollar + ES + TV + GVS • Visual information not manipulated (Vision non-manip): Foam + CCollar + ES + TV + GVS For the non-manipulated conditions, where GVS was used, the laterality of the anodal electrode was randomized.
Postural control The postural responses were measured by the force platform with three strain gauges (Techno Concept™, 40 Hz frequency, 12 bit A/D conversion). All subjects stood barefoot on the force platform with their arms next to their body. They were instructed to remain as motionless as possible, with their eyes fixed on a target (4 cm2) 1.5 m in front of them at the height of their eyes. The subjects were placed according to precise marks. Their legs were straight and their feet formed a 30° angle relative to each other (intermalleolar distance of 9 cm). Posturowin software (Techno Concept™) calculated and recorded the center of foot pressure (COP) for giving its spatiotemporal parameters. The COP velocity can be viewed as a parameter evaluating the postural control, the smaller the COP velocity the better the postural control (Caron et al., 2000). It can be detailed on the mediolateral axis in COPX velocity (mm/s1) and on the anterior–posterior axis in COPY velocity (mm/s1). The absolute increases between REF1 and the other conditions were calculated for all the parameters: Absolute increase = Manipulated – REF1
Statistical analysis Statistical analyses were performed with R statistical software (Ihaka & Gentleman, 1996). Two main directions were followed for the analysis: firstly, change for each subject between REF1 condition and each condition and, secondly, the effect of physical activity. As the prerequisites for the use of parametric tests (normality, homoscedasticity) were not present for all the parameters, non-parametric statistics were used. To determine whether there were differences between REF1 and the other conditions, all the parameters describing body sways for the manipulated, combined manipulated, and REF2 conditions
Means and standard deviation are presented with the medians in each table. Age and anthropometrical data are presented in Table 1. The parameters describing body sway relating to the manipulated and the combined sensory manipulation conditions are presented in Tables 2 and 3, respectively. Age and anthropometrical data There was no significant difference between the active and sedentary groups. Postural control parameters There was no difference between the initial condition (REF1) and the final condition (REF2) for both groups for the parameters describing body sway. Hence, no fatigue effect was detected at the end of the protocol. All the sensory manipulations altered postural control in both groups compared with the initial reference condition (REF1), except for the sedentary group in the ES condition (Tables 2 and 3). Moreover, the postural control was more disturbed for the sedentary group than for the active group in the TV condition (Table 2). Concerning the proprio manip condition, the statistical analysis revealed tendencies indicating that the absolute increases of the COPX velocity and the COPY velocity were greater for the sedentary group than the active group. Moreover, there is a tendency indicating that the COPY velocity was higher for the sedentary group than the active group. Discussion This study showed that all the manipulated and the combined sensory manipulations disturbed postural control in older subjects. Moreover, regular physical activities seem to enhance the old subjects’ ability to withstand postural disturbance. The main finding indicated that in the TV condition, the postural control was more disturbed for the sedentary group than for the active group. Otherwise, concerning the proprio manip condition, the postural disturbance tends to be more important for the sedentary group than the active group. However, concerning the other combined sensory manipulations (vestibular non-manip, proprio non-manip, cutaneous non-manip, vision non-manip), the postural control was equally disturbed for both groups.
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Maitre et al. Table 2. Active and sedentary groups’ COP velocity on the X (mediolateral direction) and Y (anteroposterior direction) axes and their absolute increases [mean (SD) median], in reference and manipulated conditions
Active group
REF1 REF2 EC Foam CCollar ES TV GVSAnode right GVSAnode left
COPVX COPVY COPVX COPVY COPVX COPVY COPVX COPVY COPVX COPY COPVX COPVY COPVX COPVY COPVX COPVY COPVX COPVY
4.5 (1.4) 4.3 6.9 (2.4) 6.1 4.3 (1.2) 4.0 7.4 (1.8) 6.9 5.3 (1.8) 5.6† 9.6 (3.4) 8.4† 6.2 (1.4) 6.0† 11.1 (2.3) 10.7† 4.6 (1.6) 4.3 8.0 (1.9) 8.0† 4.6 (1.7) 4.2 8.0 (2.7) 7.6† 8.9 (2.2) 9.0† 14.1 (4.6) 13.0† 4.7 (1.2) 4.8† 8.3 (2.2) 8.7† 4.6 (1.5) 4.2 7.9 (2.9) 6.5†
Sedentary group
4.0 (1.2) 3.7 7.5 (2.7) 7.3 4.0 (1.2) 3.8 7.6 (2.8) 7.4 4.8 (1.7) 4.4† 9.9 (3.4) 9.5† 6.4 (2.6) 5.7† 12.7 (5.0) 11.4† 4.5 (1.3) 4.0 9.1 (3.1) 9.1† 4.2 (1.4) 3.9 8.4 (3.2) 8.0 11.2 (4.2) 10.4† [P = 0.08] 23.0 (11.0) 19.8†* 5.2 (4.4) 3.8 9.0 (3.9) 8.3† 4.7 (4.1) 3.5 9.5 (4.5) 9.0†
Absolute increase Active group
Sedentary group
−0.1 (1.2) −0.0 0.5 (1.4) 0.3 0.9 (1.6) 0.6 2.6 (2.3) 2.3 1.8 (1.5) 1.8 4.1 (2.9) 3.9 0.2 (1.4) 0.1 1.1 (1.7) 1.0 0.1 (1.2) 0.5 1.1 (1.7) 0.8 4.4 (2.1) 4.0 7.2 (3.9) 6.5 0.2 (1.3) 0.1 1.4 (2.3) 0.7 0.1 (1.1) 0.2 1.0 (1.5) 0.7
−0.1 (1.1) 0.2 0.1 (1.9) 0.0 0.8 (1.2) 0.9 2.4 (2.3) 2.1 2.4 (2.0) 2.2 5.2 (3.6) 5.1 0.4 (1.0) 0.5 1.6 (1.7) 1.9 0.2 (1.2) 0.4 0.9 (2.3) 0.7 7.2 (3.4) 6.6* 15.4 (9.3) 12.7* 1.2 (3.9) 0.1 1.5 (3.1) 1.3 0.7 (3.7) 0.2 1.9 (3.3) 1.2
The median level significance differences are included in the table at the level of 5%. *Significant group difference. The P values of the group difference tendencies are included in the table at the level of 10%. † Significant condition difference with REF1. COPVX, COPX velocity (mm/s1); COPVY, COPY velocity (mm/s1); CCollar, cervical collar; EC, eyes closed; Foam, stand up on a foam surface; ES, electromyostimulation; GVS, galvanic vestibular stimulation; REF, reference condition (stand up on a firm surface with eyes open); REF1, initial condition; REF2, final condition; TV, Achilles tendinous vibration.
Table 3. Active and sedentary groups’ COP velocity on the X (mediolateral direction) and Y (anteroposterior direction) axes and their absolute increases [mean (SD) median], in reference and combined sensory manipulation conditions
Active group
Sedentary group
Absolute increase Active group
REF1
COPVX 4.5 (1.4) 4.3 COPVY 6.9 (2.4) 6.1 Combined sensory manipulations to alter proprioception Proprio manip COPVX 8.8 (1.9) 8.4† 14.7 (3.6) 14.3†
4.0 (1.2) 3.7 7.5 (2.7) 7.3 11.1 (4.4) 9.6†
21.3 (10.5) 18.9† [P = 0.07] Combined sensory manipulations to alter all sensory systems except one Vestibular non-manip COPVX 12.7 (4.5) 13.1† 16.7 (12.1) 13.3† COPVY 22.5 (7.4) 22.8† 24.9 (10.2) 23.3† Proprio non-manip COPVX 8.7 (2.6) 9.1† 8.6 (4.8) 6.6† COPVY 15.2 (4.8) 15.0† 15.4 (7.5) 12.1† Cutaneous non-manip COPVX 14.9 (6.6) 13.7† 16.1 (12.5) 12.6† COPVY 25.5 (7.7) 26.6† 26.9 (11.2) 30.4† Vision non-manip COPVX 11.1 (5.6) 10.4† 11.4 (6.3) 9.9† † COPVY 18.4 (6.0) 19.2 22.9 (10.2) 21.7† COPVY
Sedentary group
4.4 (1.5) 4.3 7.8 (3.7) 7.8 8.2 (4.0) 7.5 15.6 (6.6) 14.4 4.2 (2.5) 4.0 8.3 (4.6) 7.1 10.4 (6.2) 9.0 18.6 (7.9) 16.7 6.6 (5.1) 6.4 11.5 (6.4) 11.2
7.1 (3.8) 5.7 [P = 0.06] 13.8 (9.4) 11.8 [P = 0.06] 12.7 (11.6) 9.7 17.4 (9.2) 15.0 4.5 (4.1) 3.6 7.9 (5.6) 5.7 12.0 (12.0) 8.7 19.4 (10.0) 21.0 7.4 (5.6) 6.3 15.4 (8.7) 13.2
The median significance differences are included in the table at the level of 5%. The P values of the group difference tendencies are included in the table at the level of 10%. † Significant condition difference with REF1. COPVX, COPX velocity (mm/s1); COPVY, COPY velocity (mm/s1); Cutaneous non-manip, eyes closed + cervical collar + electromyostimulation + Achilles tendinous vibration + galvanic vestibular stimulation; Proprio manip, cervical collar + electromyostimulation + Achilles tendinous vibration; Proprio non-manip, eyes closed + foam surface + galvanic vestibular stimulation; REF1, reference condition (stand up on a firm surface with eyes open); Vestibular non-manip, eyes closed + foam surface + cervical collar + electromyostimulation + Achilles tendinous vibration; Vision non-manip, foam surface + cervical collar + electromyostimulation + Achilles tendinous vibration + galvanic vestibular stimulation.
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Physical activity and postural control Results show that when proprioceptive information from the legs was disturbed in the TV condition, the postural control was more disturbed for the sedentary group than for the active group (absolute increase of the COPX and COPY velocity). Two reasons could explain this phenomenon. Firstly, this could be related to an inability, in the case of the sedentary group, to use other sensory inputs to withstand the sensory manipulation, in contrast to the active group. Secondly, this could be related to a more efficient reweighting to proprioceptive information from regions unaffected by the tendon vibration for the active group than the inactive group. It is well known that aging affects the efficiency of the postural control systems (Sturnieks et al., 2008). However, it has been shown that repetitive stimulations of sensory systems induced by regular practice of physical and/or sports activities limit the involution, or enhance the efficiency, of different neural loops involved in postural regulation (Gauchard et al., 1999, 2001, 2003; Perrin et al., 1999; Paillard et al., 2005a,b; Ribeiro & Oliveira, 2007). In this study, when proprioception was altered (TV condition), subjects might have been compelled to rely more on other sensory inputs (e.g., visual and vestibular) to maintain postural stability. As the active group benefits from the effects of physical activities, unlike the sedentary group, it would enable it to compensate for the proprioceptive disruption by means of a more efficient use of the non-disrupted sensory inputs. Moreover, as suggested by Brumagne et al. (2004), subjects could have refocused proprioceptive control of balance away from the area manipulated by means of tendon vibration. It could be argued that the active group demonstrates a more efficient reweighting to proprioceptive information from regions unaffected by the tendon vibration than the inactive group. Furthermore, no clear difference was found between the two groups in the other conditions. One can suggest that either the conditions were not challenging enough or, conversely, they were too challenging to induce differences between the two groups. Indeed, the CCollar condition altered postural control for the active and the sedentary groups but no differences were highlighted between the both groups. According to Kelly et al. (2002), wearing a cervical collar might limit sensory input from the neck and consequently impair balance abilities. However, some studies (Karlberg et al., 1991; Burl et al., 1992; Bohne et al., 2013) have showed that wearing a cervical collar does not disturb postural control in quiet stance. Three factors could influence the impact of wearing a cervical collar. Firstly, the nature of the cervical collar exerts a different degree of restriction on neck motion. A rigid collar reduces neck movements more than a soft collar (Whitcroft et al., 2011). Secondly, the tightening of the cervical collar can act on the neck motion restriction. Thirdly, the duration for the wearing of the collar may induce habituation effects. In this study, the aim was to limit neck motion only for 20 s by the use of a rigid cervical collar. Hence, the tightening
and the nature of the cervical collar might have limited neck motions enough efficiently to induce postural effects. Also, the habituation effects that would compensate postural alteration may not have occurred because the exposure time was too short. Nevertheless, these postural effects would not be disruptive enough to induce differences between the two groups. In the ES condition, statistical analysis showed that postural control was altered for the active group (COPY velocity) but not for the sedentary group. However, the active group was not more disturbed than the sedentary groups (no difference on the absolute increase of the COPY velocity). Hence, the effects produced by the ES condition were similar on both groups. Although Paillard et al. (2007) have shown that ES (with a current intensity of 25 mA) disturbs postural control in young subjects who regularly practiced sports, the effects of ES may be quite limited for older subjects. To ensure the transmission of the artificial electrical signal, the integrity of the peripheral nervous system is necessary (Bouman & Shaffer, 1957). It is well known that aging alters the peripheral nervous system (Aagaard et al., 2010; Jang & Van Remmen, 2011) and results in a degeneration of the neuromuscular junction and abnormal axon thinning. It is likely that the peripheral nervous system involution reduced the ES effects on postural control, especially as the electrical intensity used was considerably lower (the current intensity used was 15 mA) than in the study carried out by Paillard et al. (2007). Thus, no difference could be seen between the two groups. Concerning the foam condition, postural control was disturbed for both groups. However, no difference was found between the active and the sedentary groups. Conversely, Hue et al. (2004) showed that regular physical activity improves postural control in foam floor condition. In the study by Hue et al. (2004), the foam rubber was thicker (60 mm) and had lower density (53 kg/m3) than in the present study. Because the foam used was thinner than in the previous study, subjects might have had closer contact with the rigid surface beneath the foam. Hence, plantar cutaneous sensory information could have been more accurate and corrective body movements were more effective (Patel et al., 2008), thereby limiting postural disturbance. Thus, the methodological difference between study by Hue et al. (2004) and the present study may imply that, in this study, the task was not sufficiently challenging to induce difference between the two groups. Caution should be taken when analyzing postural control with a foam surface, because foam properties may influence the recorded body sway and the task difficulty (Patel et al., 2008). Concerning the GVS conditions, current stimulation of 1 mA would not be strong enough to generate any difference between the two older groups, especially as visual information was available. Moreover, it must also be considered that visual information was available in all these previous sensory manipulation conditions. Vision
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Maitre et al. is an important source of information, which enables the subjects to compensate the influence of sensory manipulations (Britton et al., 1993; Abrahamova & Hlavacka, 2008). Hence, the availability of visual information in these sensory manipulation conditions could have limited the differences. In fact, Foam, ES, CCollar, and GVS conditions would be tasks that were insufficiently challenging to provoke postural differences between the active and the sedentary groups. In addition, removing visual information (EC condition) may not have induced a sensory alteration that was disruptive enough to induce differences between the two groups. An imposed optic stimulation induced by a moving room (Prioli et al., 2005) could be a more appropriate stimulus than the EC condition. Conversely, combined sensory manipulations (proprio manip, vestibular non-manip, proprio non-manip, cutaneous non-manip, and vision non-manip conditions) created tasks that were too challenging to engender significant differences between the two groups. It is well known that the disturbance of several sensory systems alters postural control more than that of only one sensory system (Simoneau et al., 1995). However, in the present study, when proprioceptive information was manipulated in the TV condition, the sedentary group was more disturbed than the active group. Nevertheless, when proprioceptive information was challenged slightly more than in the TV condition by adding the cervical collar and by using ES (proprio manip condition), the postural disturbance only tends to be more important for the sedentary group than the active group. One can suggest that beyond a given challenging threshold, multiple sensory manipulations make sensory reweighting excessively difficult and/or not sufficiently efficient to limit postural disturbance, even for the active group. Furthermore, it would be argued that the small size of the samples led to reduce sensitivity in samples assessment and would constitute an explanation for the statistically non-significant results. Otherwise, all the subjects did not practice the same physical activity (e.g., gym, walking, dancing, aquarobics) and the different physical activities do not act upon postural control at the same level, which could constitute a limitation of the study. In conclusion, the regular physical activities have positive effects on the ability to limit the effects of tendon
vibration on postural control. When proprioceptive information was disturbed, the ability to use the not manipulated sensory systems and/or the ability to reweight to proprioceptive information from regions unaffected by the tendon vibration were greater for the active group than the sedentary group. Furthermore, it is interesting to note that under multiple sensory input alterations, no significant differences could be demonstrated between the two groups. This could imply that beyond a given challenging threshold, multiple sensory manipulations make sensory reweighting excessively difficult and/or not sufficiently efficient to limit postural disturbance, regardless of the level of physical activity of the women subjects. Perspectives The current study highlights the benefits induced by regular physical activity on postural control. To extend this study, it would be interesting to identify which physical activity and intensity of practice are the most beneficial to postural control through the use of this protocol, particularly for older subjects. Indeed, balance disorders are common in older people. Aging largely impairs postural control and may contribute to increase the risk of falling. Identifying appropriate physical activity to improve postural control in older people would enable clinician to improve prevention and rehabilitation programs. Key words: Postural control, age, physical activity, sensory manipulation, vibration, women.
Conflicts of interest: The authors report no conflict of interest. Acknowledgements The authors thank all the participants for their helpful cooperation.
Funding The investigation was supported by grants from the Association Nationale de la Recherche et de la Technologie and the Conseil Général des Hautes Pyrénées.
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Scand J Med Sci Sports 2014: ••: ••–•• doi: 10.1111/sms.12256
Published by John Wiley & Sons Ltd
Regular physical activity reduces the effects of Achilles tendon vibration on postural control for older women J. Maitre1,2, I. Serres1, L. Lhuisset1, J. Bois1, Y. Gasnier3, T. Paillard1 1
Laboratoire Activité Physique, Performance et Santé, EA 4445, Département STAPS, Université de Pau et des Pays de l’Adour, Tarbes, France, 2Office Départemental des Sports des Hautes-Pyrénées, Tarbes, France, 3Centre Hospitalier de Bigorre, Vic en Bigorre, France Corresponding author: Julien Maitre, PhD, Laboratoire Activité Physique, Performance et Santé, EA 4445, Université de Pau et des Pays de l’Adour, Département STAPS, ZA Bastillac Sud, 65000 Tarbes, France. Tel: 33(0)562566100, Fax: 33(0)562566110, E-mail: [email protected] Accepted for publication 22 April 2014
The aim was to determine in what extent physical activity influences postural control when visual, vestibular, and/or proprioceptive systems are disrupted. Two groups of healthy older women: an active group (74.0 ± 3.8 years) who practiced physical activities and a sedentary group (74.7 ± 6.3 years) who did not, underwent 12 postural conditions consisted in altering information emanating from sensory systems by means of sensory manipulations (i.e., eyes closed, cervical collar, tendon vibration, electromyostimulation, galvanic vestibular stimulation, foam surface). The center of foot pressure velocity was
recorded on a force platform. Results indicate that the sensory manipulations altered postural control. The sedentary group was more disturbed than the active group by the use of tendon vibration. There was no clear difference between the two groups in the other conditions. This study suggests that the practice of physical activities is beneficial as a means of limiting the effects of tendon vibration on postural control through a better use of the not manipulated sensory systems and/or a more efficient reweighting to proprioceptive information from regions unaffected by the tendon vibration.
The ability to maintain balance implies the efficiency of the sensory, integrating, and motor systems (Massion, 1994; Peterka, 2002). The effects of aging affect this efficiency and can increase the risk of falls and fallrelated injuries (Lord & Sturnieks, 2005; Sturnieks et al., 2008). Falls can lead to hospitalization and mark the beginning of dependency (Bradley, 2011). Instead, physical activities improve balance abilities (Perrin et al., 1999; Howe et al., 2007). The repetition of specific movements of the body segments and body as a whole, resulting from the practice of physical activities, induces adaptations of the postural control mechanism through a better use of sensory information and motor output (Gauchard et al., 1999, 2001, 2003; Paillard et al., 2004; Ribeiro & Oliveira, 2007). Several studies have tried to quantify the impact of regular physical and/or sports activities on the postural control mechanism through the use of external perturbations altering information emanating from some sensory systems (Hu & Woollacott, 1994; Perrin et al., 1999; Hue et al., 2004; Tsang et al., 2004). It has been demonstrated that external perturbations result in compensatory postural strategies (Horak & Nashner, 1986) and sensory reweighting (Oie et al., 2002) which enable balance disturbance to be counteracted or limited. Thus, it is possible to detect the extent to which an older subject is able
to improve his or her postural performance (e.g., postural stability) and strategy (involvement of different neural loops) in disturbing condition after a period of physical practice. Yet, the effects of physical activities on postural control studied by creating external perturbations have been only partially analyzed in older subjects (Hu & Woollacott, 1994; Perrin et al., 1999; Hue et al., 2004; Tsang et al., 2004). No study has analyzed the effects of physical activities on all of the sensory systems in the same protocol which would enable precise identification of the main sensory adaptations induced. In order to assess postural adaptations, the technique of sensory manipulation (Balter et al., 2004; Fransson et al., 2004; Hue et al., 2004; Paillard et al., 2007) (e.g., vibration, electromyostimulation, or vestibular galvanic stimulation) can be used as external perturbation that alters information emanating from one sensory system (referred to in this article as the “manipulated” sensory system). Furthermore, different sensory manipulations may also be combined to leave only one sensory system unmanipulated (referred to in this article as the “nonmanipulated” sensory system). Hence, the aim of this study was to determine the influence of physical activities on different neural loops involved in postural control through the use of sensory manipulations in healthy older subjects. We hypothesized that regular physical
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Maitre et al. activities may improve the use of some sensory channels more than the use of others. Moreover, some studies have reported differences between men and women population in postural control (Era et al., 2006; Kim et al., 2010, 2012a,b). Hence, to exclude the influence of an eventual gender effect, we have voluntary chosen to focus only on women subjects in this study. Materials and methods Participants Thirty-four healthy women, all above the age of 64 and shown to be free from any cognitive, neurological, motor, and metabolic disorders after medical examination, participated in the study. They were divided into two groups: one group of 17 active subjects (the active group) and one group of 17 sedentary subjects (the sedentary group). Age and anthropometrical data are presented in Table 1. This experimental procedure received the approval of the local committee for the protection of human subjects and all subjects gave informed consent. After interviewing each subject, we included, in the active group, persons who have regularly practiced physical activity (at least 3 h per week) in a sports club (e.g., gym, walking, dancing, aquarobics) for at least 3 years. We included, in the sedentary group, persons who have not practiced physical activity (either at home or in a sports club), apart from daily tasks, for at least 3 years. All the subjects lived independently at home. Exclusion criteria included a documented postural control disorder or a medical condition that might affect postural control, a neurological or a musculoskeletal impairment, or current injury making the subjects unable to participate. Thus, we excluded persons who were not able to walk without a walking stick and who were in a nursing home. Concerning the medical examination criteria, we excluded persons in the following categories: those who had suffered hip, knee, or ankle traumatism in the previous 2 years, or lesion of the foot skin support surface, or ankylosis of the large lower limb joints (hip, knee, ankle); those who had disabling low vision, despite a correction, or suffered from chronic respiratory insufficiency requiring treatment with oxygen therapy; those undergoing medical treatment (bronchodilators, beta-blockers, corticosteroid, neuroleptics); those with cardiovascular disease (coronary artery disease, myocardial infarction, congestive heart failure, permanent or paroxysmal heart rhythm disturbances, poorly controlled hypertension); or neurological deficit; or disorders of higher functions, tone, sensitivity, and balance. The subjects were questioned as to whether abnormal cutaneous sensations were experienced. The cutaneous sensations under the feet were screened with a pencil. Concerning vestibular function, the subjects were questioned about history of vertigo and abnormal ocular nystagmus was screened.
Experimental protocol The experiment examined possible postural modifications when sensory systems were altered by means of one sensory Table 1. Active and sedentary groups’ age, anthropometrical data, and physical activity status [mean (SD) median]
Age (year) Height (cm) Weight (kg) Foot size (cm) Physical activity Past physical activity
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Active group
Sedentary group
74.0 (3.8) 73.4 156.6 (4.2) 155.0 63.2 (6.9) 65.0 25.6 (0.8) 26.0 ≥ 3 hours per week For at least 3 years
74.7 (6.3) 73.7 155.8 (5.7) 155.0 62.4 (9.0) 62.0 25.3 (0.7) 25.3 None None
manipulation, or several sensory manipulations. Sensory manipulations were used to alter one sensory system (referred to as the “manipulated condition”) or all sensory systems except one (referred to as the “non-manipulated condition”). Each subject underwent 14 different conditions, each lasting 20 s and separated by 2 min. To avoid the training effect, one trial was carried out to adapt the subjects to the exercise prior to the recording. Two reference conditions were measured with eyes open on the force platform (see section on postural control). The initial measure, at the beginning of the protocol, was REF1. The final measure at the end of the protocol was REF2 (after the completion of 12 challenging postural conditions). REF1 and REF2 were compared to ensure that there was no fatigue effect on the procedure, which could alter postural measurement. The 12 conditions’ order was partially counterbalanced. These conditions were randomized for each subject in the same group and compared with REF1. The main objective of the 12 other conditions was to manipulate or modify proprioceptive and/or exteroceptive information. To avoid initial transients and anticipation behavior being recorded at the onset of the sensory disturbance, each sensory manipulation was set up in a range of 5 s before the recording of postural sway data.
Manipulated sensory conditions Sensory manipulations were used to alter or modulate afferences emanating from specific sensory receptors of the visual, vestibular, proprioceptive, and plantar cutaneous sensory systems in order to evaluate their postural modifications on a force platform in the following conditions (when only one specific sensory receptor was manipulated all others were available): • Eyes closed (EC): Subjects were instructed to keep their eyes closed. The aim was to eliminate the contribution of visual information in postural regulation (Edwards, 1946). • Foam surface (Foam): Subjects were instructed to stand on a foam surface (15 mm, 70 kg/m3) (TG700, Domyos®, Villeneuve d’Ascq, France) placed on the force platform. The aim was to alter the contribution of cutaneous information in postural regulation (Chiang & Wu, 1997). • Cervical collar (CCollar): Subjects were instructed to wear a rigid cervical collar (C3, Thuasne®, Levallois-Perret, France). The aim was to render jointly liable the head with the trunk to limit information from the cervical joints (Paillard et al., 2007). • Electromyostimulation (ES): Electromyostimulation was applied on the gastrocnemius medialis and lateralis muscles, and the vastus medialis and lateralis muscles of both legs with a current stimulator (Rehab 4 Pro, Cefar™, Malmö, Sweden). One electrode (50 × 90 mm) (Sport-elec®, Luxembourg, Luxembourg) was placed over the motor point on each of the four muscles with a biphasic symmetric square wave (continuous pulse 350 μs, 15 mA, 80 Hz). The aim was to disturb the myotatic proprioceptive information (Hoffman & Koceja, 1997; Paillard et al., 2007). • Tendon vibration (TV): Vibration was continuously applied to the Achilles tendons of both legs by means of inertial vibrators (VB 115, Techno Concept™, Céreste, France) secured with elastic bands. Vibration frequency was set at 40 Hz and the amplitude was 0.85 mm. The aim was to modulate Ia afferences (Roll & Vedel, 1982; Roll et al., 1989). • Galvanic vestibular stimulation (GVS): A 1 mA transmastoidal galvanic vestibular stimulation was delivered by a constant-current stimulator (Galvadyn 2, Electronic Conseil, Gallargues le Montueux, France) through two disposable electrodes (T-Tracet, Contrôle-Graphique, BrieComte-Robert, France). The aim was to induce an asymmetry of vestibular activity (Wardman & Fitzpatrick, 2002). The electrodes were placed over each mastoid process, for a
Physical activity and postural control binaural bipolar design. The current was applied continuously without polarity shifts. To avoid any local noxious sensation, an anesthetic gel was applied onto each mastoid process. Subjects were measured in two different polarity conditions: • GVSAnode right: anode placed on the right mastoid process and cathode placed on the left mastoid process. • GVSAnode left: anode placed on the left mastoid process and cathode placed on the right mastoid process.
were separately compared with the REF1 condition using the paired-samples Wilcoxon–Mann–Whitney test. To determine if there were differences between the two groups, all the parameters were compared for the active and the sedentary groups, using the non-parametric Wilcoxon–Mann–Whitney test: anthropometric data (age, weight, height, foot size) and COP velocity on the X and Y axes with their absolute increase. Results were considered significant at the level of 5%.
Results Combined sensory manipulation conditions A combination of sensory manipulations was used to alter all the proprioceptive information: • Proprioceptive information manipulated (Proprio manip): CCollar + ES + TV A combination of sensory manipulations was used to alter all the sensory systems except one: • Vestibular information not manipulated (Vestibular nonmanip): EC + Foam + ES + TV + CCollar • Proprioceptive information not manipulated (Proprio nonmanip): EC + GVS + Foam • Cutaneous information not manipulated (Cutaneous nonmanip): EC + CCollar + ES + TV + GVS • Visual information not manipulated (Vision non-manip): Foam + CCollar + ES + TV + GVS For the non-manipulated conditions, where GVS was used, the laterality of the anodal electrode was randomized.
Postural control The postural responses were measured by the force platform with three strain gauges (Techno Concept™, 40 Hz frequency, 12 bit A/D conversion). All subjects stood barefoot on the force platform with their arms next to their body. They were instructed to remain as motionless as possible, with their eyes fixed on a target (4 cm2) 1.5 m in front of them at the height of their eyes. The subjects were placed according to precise marks. Their legs were straight and their feet formed a 30° angle relative to each other (intermalleolar distance of 9 cm). Posturowin software (Techno Concept™) calculated and recorded the center of foot pressure (COP) for giving its spatiotemporal parameters. The COP velocity can be viewed as a parameter evaluating the postural control, the smaller the COP velocity the better the postural control (Caron et al., 2000). It can be detailed on the mediolateral axis in COPX velocity (mm/s1) and on the anterior–posterior axis in COPY velocity (mm/s1). The absolute increases between REF1 and the other conditions were calculated for all the parameters: Absolute increase = Manipulated – REF1
Statistical analysis Statistical analyses were performed with R statistical software (Ihaka & Gentleman, 1996). Two main directions were followed for the analysis: firstly, change for each subject between REF1 condition and each condition and, secondly, the effect of physical activity. As the prerequisites for the use of parametric tests (normality, homoscedasticity) were not present for all the parameters, non-parametric statistics were used. To determine whether there were differences between REF1 and the other conditions, all the parameters describing body sways for the manipulated, combined manipulated, and REF2 conditions
Means and standard deviation are presented with the medians in each table. Age and anthropometrical data are presented in Table 1. The parameters describing body sway relating to the manipulated and the combined sensory manipulation conditions are presented in Tables 2 and 3, respectively. Age and anthropometrical data There was no significant difference between the active and sedentary groups. Postural control parameters There was no difference between the initial condition (REF1) and the final condition (REF2) for both groups for the parameters describing body sway. Hence, no fatigue effect was detected at the end of the protocol. All the sensory manipulations altered postural control in both groups compared with the initial reference condition (REF1), except for the sedentary group in the ES condition (Tables 2 and 3). Moreover, the postural control was more disturbed for the sedentary group than for the active group in the TV condition (Table 2). Concerning the proprio manip condition, the statistical analysis revealed tendencies indicating that the absolute increases of the COPX velocity and the COPY velocity were greater for the sedentary group than the active group. Moreover, there is a tendency indicating that the COPY velocity was higher for the sedentary group than the active group. Discussion This study showed that all the manipulated and the combined sensory manipulations disturbed postural control in older subjects. Moreover, regular physical activities seem to enhance the old subjects’ ability to withstand postural disturbance. The main finding indicated that in the TV condition, the postural control was more disturbed for the sedentary group than for the active group. Otherwise, concerning the proprio manip condition, the postural disturbance tends to be more important for the sedentary group than the active group. However, concerning the other combined sensory manipulations (vestibular non-manip, proprio non-manip, cutaneous non-manip, vision non-manip), the postural control was equally disturbed for both groups.
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Maitre et al. Table 2. Active and sedentary groups’ COP velocity on the X (mediolateral direction) and Y (anteroposterior direction) axes and their absolute increases [mean (SD) median], in reference and manipulated conditions
Active group
REF1 REF2 EC Foam CCollar ES TV GVSAnode right GVSAnode left
COPVX COPVY COPVX COPVY COPVX COPVY COPVX COPVY COPVX COPY COPVX COPVY COPVX COPVY COPVX COPVY COPVX COPVY
4.5 (1.4) 4.3 6.9 (2.4) 6.1 4.3 (1.2) 4.0 7.4 (1.8) 6.9 5.3 (1.8) 5.6† 9.6 (3.4) 8.4† 6.2 (1.4) 6.0† 11.1 (2.3) 10.7† 4.6 (1.6) 4.3 8.0 (1.9) 8.0† 4.6 (1.7) 4.2 8.0 (2.7) 7.6† 8.9 (2.2) 9.0† 14.1 (4.6) 13.0† 4.7 (1.2) 4.8† 8.3 (2.2) 8.7† 4.6 (1.5) 4.2 7.9 (2.9) 6.5†
Sedentary group
4.0 (1.2) 3.7 7.5 (2.7) 7.3 4.0 (1.2) 3.8 7.6 (2.8) 7.4 4.8 (1.7) 4.4† 9.9 (3.4) 9.5† 6.4 (2.6) 5.7† 12.7 (5.0) 11.4† 4.5 (1.3) 4.0 9.1 (3.1) 9.1† 4.2 (1.4) 3.9 8.4 (3.2) 8.0 11.2 (4.2) 10.4† [P = 0.08] 23.0 (11.0) 19.8†* 5.2 (4.4) 3.8 9.0 (3.9) 8.3† 4.7 (4.1) 3.5 9.5 (4.5) 9.0†
Absolute increase Active group
Sedentary group
−0.1 (1.2) −0.0 0.5 (1.4) 0.3 0.9 (1.6) 0.6 2.6 (2.3) 2.3 1.8 (1.5) 1.8 4.1 (2.9) 3.9 0.2 (1.4) 0.1 1.1 (1.7) 1.0 0.1 (1.2) 0.5 1.1 (1.7) 0.8 4.4 (2.1) 4.0 7.2 (3.9) 6.5 0.2 (1.3) 0.1 1.4 (2.3) 0.7 0.1 (1.1) 0.2 1.0 (1.5) 0.7
−0.1 (1.1) 0.2 0.1 (1.9) 0.0 0.8 (1.2) 0.9 2.4 (2.3) 2.1 2.4 (2.0) 2.2 5.2 (3.6) 5.1 0.4 (1.0) 0.5 1.6 (1.7) 1.9 0.2 (1.2) 0.4 0.9 (2.3) 0.7 7.2 (3.4) 6.6* 15.4 (9.3) 12.7* 1.2 (3.9) 0.1 1.5 (3.1) 1.3 0.7 (3.7) 0.2 1.9 (3.3) 1.2
The median level significance differences are included in the table at the level of 5%. *Significant group difference. The P values of the group difference tendencies are included in the table at the level of 10%. † Significant condition difference with REF1. COPVX, COPX velocity (mm/s1); COPVY, COPY velocity (mm/s1); CCollar, cervical collar; EC, eyes closed; Foam, stand up on a foam surface; ES, electromyostimulation; GVS, galvanic vestibular stimulation; REF, reference condition (stand up on a firm surface with eyes open); REF1, initial condition; REF2, final condition; TV, Achilles tendinous vibration.
Table 3. Active and sedentary groups’ COP velocity on the X (mediolateral direction) and Y (anteroposterior direction) axes and their absolute increases [mean (SD) median], in reference and combined sensory manipulation conditions
Active group
Sedentary group
Absolute increase Active group
REF1
COPVX 4.5 (1.4) 4.3 COPVY 6.9 (2.4) 6.1 Combined sensory manipulations to alter proprioception Proprio manip COPVX 8.8 (1.9) 8.4† 14.7 (3.6) 14.3†
4.0 (1.2) 3.7 7.5 (2.7) 7.3 11.1 (4.4) 9.6†
21.3 (10.5) 18.9† [P = 0.07] Combined sensory manipulations to alter all sensory systems except one Vestibular non-manip COPVX 12.7 (4.5) 13.1† 16.7 (12.1) 13.3† COPVY 22.5 (7.4) 22.8† 24.9 (10.2) 23.3† Proprio non-manip COPVX 8.7 (2.6) 9.1† 8.6 (4.8) 6.6† COPVY 15.2 (4.8) 15.0† 15.4 (7.5) 12.1† Cutaneous non-manip COPVX 14.9 (6.6) 13.7† 16.1 (12.5) 12.6† COPVY 25.5 (7.7) 26.6† 26.9 (11.2) 30.4† Vision non-manip COPVX 11.1 (5.6) 10.4† 11.4 (6.3) 9.9† † COPVY 18.4 (6.0) 19.2 22.9 (10.2) 21.7† COPVY
Sedentary group
4.4 (1.5) 4.3 7.8 (3.7) 7.8 8.2 (4.0) 7.5 15.6 (6.6) 14.4 4.2 (2.5) 4.0 8.3 (4.6) 7.1 10.4 (6.2) 9.0 18.6 (7.9) 16.7 6.6 (5.1) 6.4 11.5 (6.4) 11.2
7.1 (3.8) 5.7 [P = 0.06] 13.8 (9.4) 11.8 [P = 0.06] 12.7 (11.6) 9.7 17.4 (9.2) 15.0 4.5 (4.1) 3.6 7.9 (5.6) 5.7 12.0 (12.0) 8.7 19.4 (10.0) 21.0 7.4 (5.6) 6.3 15.4 (8.7) 13.2
The median significance differences are included in the table at the level of 5%. The P values of the group difference tendencies are included in the table at the level of 10%. † Significant condition difference with REF1. COPVX, COPX velocity (mm/s1); COPVY, COPY velocity (mm/s1); Cutaneous non-manip, eyes closed + cervical collar + electromyostimulation + Achilles tendinous vibration + galvanic vestibular stimulation; Proprio manip, cervical collar + electromyostimulation + Achilles tendinous vibration; Proprio non-manip, eyes closed + foam surface + galvanic vestibular stimulation; REF1, reference condition (stand up on a firm surface with eyes open); Vestibular non-manip, eyes closed + foam surface + cervical collar + electromyostimulation + Achilles tendinous vibration; Vision non-manip, foam surface + cervical collar + electromyostimulation + Achilles tendinous vibration + galvanic vestibular stimulation.
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Physical activity and postural control Results show that when proprioceptive information from the legs was disturbed in the TV condition, the postural control was more disturbed for the sedentary group than for the active group (absolute increase of the COPX and COPY velocity). Two reasons could explain this phenomenon. Firstly, this could be related to an inability, in the case of the sedentary group, to use other sensory inputs to withstand the sensory manipulation, in contrast to the active group. Secondly, this could be related to a more efficient reweighting to proprioceptive information from regions unaffected by the tendon vibration for the active group than the inactive group. It is well known that aging affects the efficiency of the postural control systems (Sturnieks et al., 2008). However, it has been shown that repetitive stimulations of sensory systems induced by regular practice of physical and/or sports activities limit the involution, or enhance the efficiency, of different neural loops involved in postural regulation (Gauchard et al., 1999, 2001, 2003; Perrin et al., 1999; Paillard et al., 2005a,b; Ribeiro & Oliveira, 2007). In this study, when proprioception was altered (TV condition), subjects might have been compelled to rely more on other sensory inputs (e.g., visual and vestibular) to maintain postural stability. As the active group benefits from the effects of physical activities, unlike the sedentary group, it would enable it to compensate for the proprioceptive disruption by means of a more efficient use of the non-disrupted sensory inputs. Moreover, as suggested by Brumagne et al. (2004), subjects could have refocused proprioceptive control of balance away from the area manipulated by means of tendon vibration. It could be argued that the active group demonstrates a more efficient reweighting to proprioceptive information from regions unaffected by the tendon vibration than the inactive group. Furthermore, no clear difference was found between the two groups in the other conditions. One can suggest that either the conditions were not challenging enough or, conversely, they were too challenging to induce differences between the two groups. Indeed, the CCollar condition altered postural control for the active and the sedentary groups but no differences were highlighted between the both groups. According to Kelly et al. (2002), wearing a cervical collar might limit sensory input from the neck and consequently impair balance abilities. However, some studies (Karlberg et al., 1991; Burl et al., 1992; Bohne et al., 2013) have showed that wearing a cervical collar does not disturb postural control in quiet stance. Three factors could influence the impact of wearing a cervical collar. Firstly, the nature of the cervical collar exerts a different degree of restriction on neck motion. A rigid collar reduces neck movements more than a soft collar (Whitcroft et al., 2011). Secondly, the tightening of the cervical collar can act on the neck motion restriction. Thirdly, the duration for the wearing of the collar may induce habituation effects. In this study, the aim was to limit neck motion only for 20 s by the use of a rigid cervical collar. Hence, the tightening
and the nature of the cervical collar might have limited neck motions enough efficiently to induce postural effects. Also, the habituation effects that would compensate postural alteration may not have occurred because the exposure time was too short. Nevertheless, these postural effects would not be disruptive enough to induce differences between the two groups. In the ES condition, statistical analysis showed that postural control was altered for the active group (COPY velocity) but not for the sedentary group. However, the active group was not more disturbed than the sedentary groups (no difference on the absolute increase of the COPY velocity). Hence, the effects produced by the ES condition were similar on both groups. Although Paillard et al. (2007) have shown that ES (with a current intensity of 25 mA) disturbs postural control in young subjects who regularly practiced sports, the effects of ES may be quite limited for older subjects. To ensure the transmission of the artificial electrical signal, the integrity of the peripheral nervous system is necessary (Bouman & Shaffer, 1957). It is well known that aging alters the peripheral nervous system (Aagaard et al., 2010; Jang & Van Remmen, 2011) and results in a degeneration of the neuromuscular junction and abnormal axon thinning. It is likely that the peripheral nervous system involution reduced the ES effects on postural control, especially as the electrical intensity used was considerably lower (the current intensity used was 15 mA) than in the study carried out by Paillard et al. (2007). Thus, no difference could be seen between the two groups. Concerning the foam condition, postural control was disturbed for both groups. However, no difference was found between the active and the sedentary groups. Conversely, Hue et al. (2004) showed that regular physical activity improves postural control in foam floor condition. In the study by Hue et al. (2004), the foam rubber was thicker (60 mm) and had lower density (53 kg/m3) than in the present study. Because the foam used was thinner than in the previous study, subjects might have had closer contact with the rigid surface beneath the foam. Hence, plantar cutaneous sensory information could have been more accurate and corrective body movements were more effective (Patel et al., 2008), thereby limiting postural disturbance. Thus, the methodological difference between study by Hue et al. (2004) and the present study may imply that, in this study, the task was not sufficiently challenging to induce difference between the two groups. Caution should be taken when analyzing postural control with a foam surface, because foam properties may influence the recorded body sway and the task difficulty (Patel et al., 2008). Concerning the GVS conditions, current stimulation of 1 mA would not be strong enough to generate any difference between the two older groups, especially as visual information was available. Moreover, it must also be considered that visual information was available in all these previous sensory manipulation conditions. Vision
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Maitre et al. is an important source of information, which enables the subjects to compensate the influence of sensory manipulations (Britton et al., 1993; Abrahamova & Hlavacka, 2008). Hence, the availability of visual information in these sensory manipulation conditions could have limited the differences. In fact, Foam, ES, CCollar, and GVS conditions would be tasks that were insufficiently challenging to provoke postural differences between the active and the sedentary groups. In addition, removing visual information (EC condition) may not have induced a sensory alteration that was disruptive enough to induce differences between the two groups. An imposed optic stimulation induced by a moving room (Prioli et al., 2005) could be a more appropriate stimulus than the EC condition. Conversely, combined sensory manipulations (proprio manip, vestibular non-manip, proprio non-manip, cutaneous non-manip, and vision non-manip conditions) created tasks that were too challenging to engender significant differences between the two groups. It is well known that the disturbance of several sensory systems alters postural control more than that of only one sensory system (Simoneau et al., 1995). However, in the present study, when proprioceptive information was manipulated in the TV condition, the sedentary group was more disturbed than the active group. Nevertheless, when proprioceptive information was challenged slightly more than in the TV condition by adding the cervical collar and by using ES (proprio manip condition), the postural disturbance only tends to be more important for the sedentary group than the active group. One can suggest that beyond a given challenging threshold, multiple sensory manipulations make sensory reweighting excessively difficult and/or not sufficiently efficient to limit postural disturbance, even for the active group. Furthermore, it would be argued that the small size of the samples led to reduce sensitivity in samples assessment and would constitute an explanation for the statistically non-significant results. Otherwise, all the subjects did not practice the same physical activity (e.g., gym, walking, dancing, aquarobics) and the different physical activities do not act upon postural control at the same level, which could constitute a limitation of the study. In conclusion, the regular physical activities have positive effects on the ability to limit the effects of tendon
vibration on postural control. When proprioceptive information was disturbed, the ability to use the not manipulated sensory systems and/or the ability to reweight to proprioceptive information from regions unaffected by the tendon vibration were greater for the active group than the sedentary group. Furthermore, it is interesting to note that under multiple sensory input alterations, no significant differences could be demonstrated between the two groups. This could imply that beyond a given challenging threshold, multiple sensory manipulations make sensory reweighting excessively difficult and/or not sufficiently efficient to limit postural disturbance, regardless of the level of physical activity of the women subjects. Perspectives The current study highlights the benefits induced by regular physical activity on postural control. To extend this study, it would be interesting to identify which physical activity and intensity of practice are the most beneficial to postural control through the use of this protocol, particularly for older subjects. Indeed, balance disorders are common in older people. Aging largely impairs postural control and may contribute to increase the risk of falling. Identifying appropriate physical activity to improve postural control in older people would enable clinician to improve prevention and rehabilitation programs. Key words: Postural control, age, physical activity, sensory manipulation, vibration, women.
Conflicts of interest: The authors report no conflict of interest. Acknowledgements The authors thank all the participants for their helpful cooperation.
Funding The investigation was supported by grants from the Association Nationale de la Recherche et de la Technologie and the Conseil Général des Hautes Pyrénées.
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