Neuroscience Letters 562 (2014) 60–62

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Leg skin stimulation can be a strategy to improve postural control in the elderly Liane M. Lopes a , Letícia S. Ueda a , Marcos R. Kunzler a , Morgana A. de Britto a , Felipe P. Carpes a,b,∗ a b

Laboratory of Neuromechanics, Center for Health Sciences, Federal University of Pampa, Uruguaiana, RS, Brazil Laboratory of Biomechanics, Faculty of Physical Education, Federal University of Santa Maria, Santa Maria, RS, Brazil

h i g h l i g h t s • We tested the effects of skin stimulation on the postural control of elderly. • Skin stimulation in the Achilles tendon region was effective to improve postural control in the elderly. • These results are promising as the protocol we tested can be a low cost strategy when dealing with aged subjects.

a r t i c l e

i n f o

Article history: Received 10 June 2013 Received in revised form 12 December 2013 Accepted 12 January 2014 Keywords: Proprioception Stability Center of pressure Sensorimotor stimulation Aging Falling

a b s t r a c t Previous studies suggested that skin stimulation by using medical tape glued to the skin over the Achilles tendon can improve postural control in young adults. Such strategy can be valuable if helping to improve postural control in the elderly. Here, we tested the effects of skin stimulation on the postural control of elderly while standing barefoot. Twenty-two voluntary elderly had postural control assessed under different conditions of skin stimulation. Center of pressure was monitored while they stood quietly barefoot on a force plate during standing with and without medical tape glued to the skin over the Achilles tendon. There were effects of skin stimulation for anteroposterior amplitude of center of pressure displacement, mediolateral amplitude of center of pressure displacement, and area of the ellipse for 95% of center of pressure data (P < .05). These results are promising considering that skin stimulation by using medical tape is feasible even for low incoming subjects and possible to self manage for improvements in postural control. © 2014 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Thedon et al. [1] presented instigating results suggesting that degraded postural performance after ankle flexors muscle fatigue in young adults might be compensated by skin stimulation using straps of tape attached to the leg skin. Interestingly, the authors suggested that the proprioceptive inputs from leg skin would not contribute to postural control in a baseline condition (without fatigue). Recently, it was found that skin stimulation using medical tape improved postural control in health adults especially before fatigue of ankle flexor muscles [2]. When ankle flexor muscles were fatigued, the amplitude of center of pressure in anteroposterior direction was the unique variable improved by tape stimulation.

∗ Corresponding author at: Federal University of Pampa, Laboratory of Neuromechanics, BR 472 km 592 - PO Box 118 - ZIP 97500-970, Uruguaiana, RS, Brazil. Tel.: +55 55 3413 4321; fax: +55 55 3414 1484. E-mail address: [email protected] (F.P. Carpes). 0304-3940/$ – see front matter © 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2014.01.020

The application of skin stimulation for improvement of postural control has clinical and practical relevance. Considering the acute effects observed in the previous studies mentioned [1,2], the skin stimulation in the elderly could help to improve postural control during a physiotherapy session involving upright postures or even during daily life activities requiring standing. Of note, no previous study addressed this strategy of skin stimulation for elderly. While foot manipulation is efficient to improve postural control of elderly when visual information is also manipulated [3], the use of tape stimulation might be possible to use even when the presence of a therapist is unavailable. Indeed, the stimulation provided by the tape could facilitate to reach cutaneous discharge threshold [4] in a different way of those braces and bandages that limit joint motion [5]. Here, we investigated the effects of skin stimulation on the postural control of elderly standing barefoot. Based in previous results [1,2] we hypothesized that the tape stimulation can improve the postural control in the elderly during quiet standing.

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Fig. 1. Mean and standard deviation data of center of pressure (CoP) during quiet standing in the no-tape and tape condition in the elderly. CoP AMPap, amplitude of CoP in the anteroposterior direction; CoP AMPml, amplitude of CoP in the mediolateral direction; CoP area, area of ellipse including 95% of CoP data; CoP velocity, resultant translational velocity of CoP; *indicates statistical significant difference between the no-tape and tape conditions (P < .05).

2. Material and methods

2.4. Assessment of postural control

2.1. Participants

The postural control was quantified by analysis of center of pressure (CoP) traces during quiet upright standing. Subjects stood barefoot on a biomechanical 3-D force plate (OR6 2000, Advanced Mechanical Technology, Inc., Watertown, MA, USA) embedded at the level of the laboratory floor, calibrated according to the manufacturer recommendations and placed in the center of a quiet room without auditory distractions. Subjects were barefoot to minimize any influence of shoes or socks on modulation of leg muscle involved in both gait and postural control [7]. Subjects had their foot position standardized at 15◦ with sagittal midline and heels positioned 10 cm apart each other and arms resting along the trunk. The trials lasted 30 s with a 30 s interval between them [8]. During the trials subjects stood with eyes closed to avoid influence of visual input [9] since it would be difficult to quantify the participation of visual input combined to the sensorial stimulation [10,11]. Ground reaction forces and moments were recorded at 100 Hz. CoP variables analyzed were: ellipse area involving 95% of data (CoP area), mean velocity (CoP velocity) and amplitude displacement in both directions (AMPap and AMPml, for anteroposterior and mediolateral directions, respectively, computed by the difference between maximal and minimum values obtained for each direction) [12].

To be included in the study subjects should not be involved in regular physical training program for the last 3 months, they should be free of acute or chronic injury of lower extremity, vestibular problems, restrict joint range of motion and foot deformities that might impair independent gait. Exclusion criteria involved use of any medication that could generate dizziness, somnolence, as well as use of drugs or alcohol dependence. Partial or total blind subjects were not included in the sample. Twenty two subjects (5 men) volunteered for the study. They were (mean ±SD) aged 76.9 ± 5.2 years old, body mass 72.5 ± 11.11 kg, height 1.61 ± 0.09 m, and body mass index 27.99 ± 3.87 kg/m2 . All of them signed a consent approved by the local institutional ethics committee (IRB#10.037.09-008/2011).

2.2. Experimental design Subjects stood quiet barefoot. All the trials were performed with the eyes closed, with and without bilateral stimulation of the skin over Achilles tendon region. All the subjects were assessed in the morning to avoid any influence of time of day on postural control [6]. Subjects performed three trials without stimulation and three trials with the stimulation. However, half of the sample was evaluated first with the skin stimulation and the other half without the stimulation. It was done in attempt to avoid any effect of first condition tested. During all the trials the signals of ground reaction forces and moments were sampled. All the procedures developed in this study were in accordance with the Helsinki Declaration.

2.3. Skin stimulation The skin stimulation was conducted using medical adhesive tape (3M, Transpore, 3M, USA) glued directly in the shaved skin. The tape dimension was 10 cm by 2.5 cm applied on skin over both Achilles tendons in the longitudinal direction from the calcaneus tuberosity without any compression or skin stretch [1]. For each subject a new piece of tape was used, always positioned at the same place by the same experimenter.

2.5. Statistical analysis Data normality was verified by Shapiro-Wilk. The equality of variances was tested using Levene’s test. CoP data were compared between trials with (tape condition) without (no-tape condition) tape glued to the skin by means of paired Student t-tests. Effect sizes were computed for each comparison. Significance level was set at 0.05 for all data analysis.

3. Results CoP data showed a consistent significant improvement in postural control of the elderly during tape stimulation (Fig. 1). The use of tape decreased AMPap [t(21) = 2.349; P = 0.029; ES = 0.30], AMPml [t(21) = 2.370; P = 0.027; ES = 0.50] and COP area [t(21) = 2.302;

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P = 0.032; ES = 0.43]. COP velocity was not influenced by tape stimulation [t(21) = 1.825; P = 0.082; ES = 0.15]. 4. Discussion It was recently suggested that attention should be directed toward the contribution of the proprioceptive system to postural control in older adults [13]. In especial, strategies with low cost and that permit the self management or familiar care could contribute for those subjects that may not have access to the professional care. In this regard, skin stimulation was discussed as a strategy to improve postural control of young subjects [1,2]. The goal of our study was to evaluate the effects of skin stimulation, which use a very accessible strategy, on postural control in the elderly. Our results confirmed our hypothesis of skin stimulation by attaching a strap of medical tape over the Achilles tendon might improve postural control in the elderly during quiet standing with eyes closed. This effect may have relationship with cutaneous reflexes and stimulation of muscles crossing ankle joint. Our results are promising considering that skin stimulation by using medical tape is feasible even for low incoming subjects. Furthermore, it is a strategy possible for self-management, and further studies are required to fully address the role and impacts of this strategy of skin stimulation when looking to reduce the risk of falling in the elderly. Bent and Lowrey [14] recently demonstrate that single cutaneous afferents in the foot (dorsum region) affect muscle activity in the upper extremity. The statement concerning that skin on the foot and ankle can contribute to the modulation of interlimb muscles in distant innervations territories [14] that can influence postural control, are in line with our results from skin stimulation using medical tape. Manipulation of the foot and ankle by a therapist improves postural control in the elderly [3]. Here, we showed that the skin stimulation by using medical tape glued to the skin over the Achilles tendon improves postural control in the elderly. Foot and ankle manipulation may require participation of a therapist. In other hand, the use of tape glued to the skin in the lower leg, specifically at Achilles tendon regions as we showed here, is more likely possible to self manage or familiar care of the elderly. This is especially important if considering low incoming regions. The efficiency of skin stimulation by using medical tape glued to leg skin to improve postural control recently suggested for young subjects [1,2] was here confirmed also for elderly. The manipulation of somatosensory information by vibration applied to the plantar cutaneous-muscular regions and Achilles tendon during quiet stance changed center of mass and center of pressure displacements [15]. The sensory stimulation provides references for the central nervous system to sustain the upright posture and improves postural control [15]. The tape stimulation can contribute to increase sensory input for movement detection, by delivering sensorial input close to the ankle [16]. The effect can be similar to those observed by applying braces and bandages, which had positive effects for postural control [5]. However, the use of tape does not affect joint range of motion in the same extent of braces and bandages. Regarding the nature of the skin stimulation, we consider that it is most likely possible that cyclical stretch of the skin in connection with the low ankle oscillations (even if oscillation is very small) contributes more than pressure exerted by the tape on the skin. This rationale comes from studies considering hand’s proprioception [4]. In a research done with taping of the ankle, the authors suggested that the skin connection of the plantar surface and ankle achieved with the tape may provide cutaneous sensory cues, giving

a better sense of position and orientation to the subjects [17]. It also may help to understand why applying straps of tape with different orientation and crossing the ankle joint limiting degrees of freedom leaded to improvement of postural control even after fatigue [9]. It is important to note that the tape improved postural control in the elderly during a baseline condition were subjects standing without any perturbation other than the fact they were eyes closed. One limitation of our study was the impossibility to use microneurography to show increase or decrease in the sensory activation of plantar receptors or skin receptors during the protocols. In summary, the skin stimulation by using medical tape glued over the Achilles’ tendon region contributes for improvement of postural control in the elderly most likely due to increase in sensory input for movement detection by delivering sensorial input close to the ankle. Acknowledgement This research was partially supported by process 476163/20102 CNPq grant to FPC and FAPERGS student fellowship to MAB. The authors declare they have any conflict of interesting regarding the content of this paper. References [1] T. Thedon, K. Mandrick, M. Foissac, D. Mottet, S. Perrey, Degraded postural performance after muscle fatigue can be compensated by skin stimulation, Gait Posture 33 (2011) 686–689. [2] M.R. Kunzler, L.M. Lopes, L.S. Ueda, M.A. de Britto, F.P. Carpes, Does skin stimulation compensate impairments in postural control after ankle plantar flexors fatigue? Gait Posture 37 (2013) 611–614. [3] J. Vaillant, N. Vuillerme, A. Janvey, F. Louis, R. Braujou, R. Juvin, V. Nougier, Effect of manipulation of the feet and ankles on postural control in elderly adults, Brain Res. Bull. 75 (2008) 18–22. [4] D.F. Collins, K.M. Refshauge, G. Todd, S.C. Gandevia, Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee, J. Neurophysiol. 94 (2005) 1699–1706. [5] K.L. Bennell, P.A. Goldie, The differential effects of external ankle support on postural control, J. Orthop. Sports. Phys. Ther. 20 (1994) 287–295. [6] M.G. Jorgensen, M.S. Rathleff, U. Laessoe, P. Caserotti, O.B. Nielsen, P. Aagaard, Time-of-day influences postural balance in older adults, Gait Posture 35 (2012) 653–657. [7] B.M. Van Wezel, F.A. Ottenhoff, J. Duysens, Dynamic control of location-specific information in tactile cutaneous reflexes from the foot during human walking, J. Neurosci. 17 (1997) 3804–3814. [8] E.T. Hsiao-Wecksler, K. Katdare, J. Matson, W. Liu, L.A. Lipsitz, J.J. Collins, Predicting the dynamic postural control response from quiet-stance behavior in elderly adults, J. Biomech. 36 (2003) 1327–1333. [9] P. Hlavackova, D. Pradon, N. Vuillerme, Control of bipedal posture following localised muscle fatigue of the plantar-flexors and finger-flexors, Eur. J. Appl. Physiol. 112 (2012) 789–793. [10] H.G. Palm, J. Strobel, G. Achatz, F. von Luebken, B. Friemert, The role and interaction of visual and auditory afferents in postural stability, Gait Posture 30 (2009) 328–333. [11] N. Sarabon, J. Rosker, S. Loefler, H. Kern, The effect of vision elimination during quiet stance tasks with different feet positions, Gait Posture 13 (2013), http://dx.doi.org/10.1016/j.gaitpost.2013.03.005. [12] T.E. Prieto, J.B. Myklebust, R.G. Hoffmann, E.G. Lovett, B.M. Myklebust, Measures of postural steadiness: differences between healthy young and elderly adults, IEEE Trans. Biomed. Eng. 43 (1996) 956–966. [13] D.R. Toledo, J.A. Barela, Sensory and motor differences between young and older adults: somatosensory contribution to postural control, Braz. J. Physiother. 14 (2010) 267–275. [14] L.R. Bent, C.R. Lowrey, Single low threshold afferents innervating the skin of the human foot modulate ongoing muscle activity in the upper limbs, J. Neurophysiol. 109 (2013) 1614–1625. [15] C. Thompson, M. Belanger, J. Fung, Effects of plantar cutaneo-muscular and tendon vibration on posture and balance during quiet and perturbed stance, Hum. Mov. Sci. 30 (2011) 153–171. [16] H.B. Menz, S.R. Lord, R.C. Fitzpatrick, A tactile stimulus applied to the leg improves postural stability in young, old and neuropathic subjects, Neurosci. Lett. 406 (2006) 23–26. [17] S. Robbins, E. Waked, R. Rappel, Ankle taping improves proprioception before and after exercise in young men, Br. J. Sports Med. 29 (1995) 242–247.

Leg skin stimulation can be a strategy to improve postural control in the elderly.

Previous studies suggested that skin stimulation by using medical tape glued to the skin over the Achilles tendon can improve postural control in youn...
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