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Effects of plantar foot sensitivity manipulation on postural control of young adult and elderly

ABSTRACT

Introduction:

Subjects with sensorial losses present balance deficits. Although such condition is often observed among elderly, there is discussion concerning the dependence on sensorial information for body sway control in the elderly without sensorial losses.

Purpose:

We investigated the effects of foot sensitivity manipulation on postural control during upright standing in young adults and independent elderly (n = 19/group).

Methods:

Plantar sensitivity was evaluated by esthesiometry, and speed of center of pressure shift data during upright posture were evaluated for each foot using a baropodometer while the subjects were standing with eyes open or closed. The young adult group was evaluated for center of pressure in normal conditions and after plantar sensitivity disturbance, by immersing their feet in water and ice.

Results:

Young adults did not show alterations in their center of pressure after sensorial perturbation and presented, even under sensorial perturbation, better postural control than elderly subjects. The elderly showed lower foot sensitivity and greater center of pressure oscillation than young adults.

Conclusion:

Elderly subjects seem to rely more on foot sensitivity for control of body sway than young adults. In the elderly, a clinical intervention to improve foot sensitivity may help in upright posture maintenance.

Keywords:
Postural control; Balance; Center of pressure; Stability; Aging

RESUMO

Introdução:

Pessoas com perdas sensoriais apresentam déficits de equilíbrio. Embora esse quadro seja comum em idosos, ainda se discute o quanto idosos sem doenças que afetam as vias sensoriais dependem dessa informação para controlar oscilações corporais durante o controle da postura.

Objetivo:

Investigar os efeitos da perturbação da sensibilidade plantar sobre o controle da postura ereta em adultos jovens e idosos independentes (n = 19/grupo).

Métodos:

A sensibilidade plantar foi avaliada com estesiômetro e dados de velocidade e deslocamento do centro de pressão durante a postura de pé foram avaliados para cada pé com um baropodômetro, em condições de olhos abertos e fechados. O grupo de adultos jovens foi avaliado quanto ao centro de pressão nas condições normal e pós-perturbação da sensibilidade plantar, pela imersão dos pés em água e gelo.

Resultados:

Adultos não apresentaram alterações no centro de pressão em resposta à perturbação sensorial e tiveram, mesmo na condição de perturbação sensorial, melhor controle postural do que idosos. Idosos apresentaram menor sensibilidade plantar e maior oscilação do centro de pressão do que os adultos jovens.

Conclusão:

Idosos pareceram depender mais da sensibilidade plantar para manter o controle postural do que adultos jovens. Em idosos, intervenções clínicas que melhorem a sensibilidade plantar podem auxiliar na tarefa de manter a postura de pé.

Palavras-chave:
Controle postural; Equilíbrio; Centro de pressão; Estabilidade; Envelhecimento

Introduction

The control of upright posture is a skill required daily and which depends on constant neuromuscular adjustments to keep the center of pressure (CoP) within the stability limits of the supporting base.11 Winter D. Biomechanics and motor control of human movement. 4ª ed. John Wiley & Sons; 1990. p. 370. These adjustments suffer deterioration by the aging process.22 Freitas SM, Wieczorek SA, Marchetti PH, Duarte M. Age-related changes in human postural control of prolonged standing. Gait Posture. 2005;22(4):322-30. One reason for the occurrence of these deficits may be the loss of sensory function or usability of this sensory information. When subjected to situations where proprioceptive functions of the foot and ankle are compromised, young adults have a lower length and area of CoP shift versus elderly subjects, suggesting an improved ability to compensate for sensory loss.33 Ueda LS, Carpes FP. Relação entre sensibilidade plantar e controle postural em jovens e idosos. Rev Bras Cineantropom Desempenho Hum. 2013;15(2):215-24.,44 Schlee G, Sterzing T, Milani TL. Foot sole skin temperature affects plantar foot sensitivity. Clin Neurophysiol. 2009;120(8):1548-611.

Billot et al.55 Billot M, Handrigan GA, Simoneau M, Corbeil P, Teasdale N. Short term alteration of balance control after a reduction of plantar mechanoreceptor sensation through cooling. Neurosci Lett. 2013;535:40-4. suggest that plantar sensitivity is not a primary function for posture control in adults, since this information can be compensated by other proprioceptive pathways, for example, vision or vestibular system. However, posture control seems to be associated with plantar sensitivity in the elderly, where other systems also have deficits in response to aging, for example, losses in vestibular system function, vision and muscle strength.33 Ueda LS, Carpes FP. Relação entre sensibilidade plantar e controle postural em jovens e idosos. Rev Bras Cineantropom Desempenho Hum. 2013;15(2):215-24. Ducic et al.66 Ducic I, Short KW, Dellon AL. Relationship between loss of pedal sensibility, balance, and falls in patients with peripheral neuropathy. Ann Plast Surg. 2004;52(6):535-610. showed that the reduced plantar sensitivity relates to deficits in postural control of elderly patients with peripheral neuropathy. In addition, plantar sensitivity contributes to the control of plantar pressure during upright posture in the elderly.77 Zhang S, Li L. The differential effects of foot sole sensory on plantar pressure distribution between balance and gait. Gait Posture. 2013;37(4):532-7. This helps to explain the fact that older people sometimes show greater reliance on vision, especially for the control of CoP velocity, than young adults.88 Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM. Measures of postural steadiness: differences between healthy young and elderly adults. IEEE Trans Biomed Eng. 1996;43(9):956-966. However, there is still doubt as to the degree of contribution of this kind of sensory information from the plantar region for the regulation of postural control in healthy elderly.

Experimental studies have developed protocols that reduce temporarily the adult sensory function, for example, the activity of mechanoreceptors, in order to mimic sensory decline of aging and facilitate a comparison between this intact versus impaired afferent resource. One strategy that has proved valid in some studies consists in the immersion of the lower limbs in water and ice, in order to reduce plantar sensitivity, two-point touch discrimination ability, and sensitivity to vibration.99 Stal F, Fransson PA, Magnusson M, Karlberg M. Effects of hypothermic anesthesia of the feet on vibration-induced body sway and adaptation. J Vestib Res. 2003;13(1):39-41.

In this study, our aim was to assess changes in the position of CoP under each foot, which is considered as an indicator of postural control in the elderly and in young adults in normal sensory condition and in response to a sensitivity disturbance. Considering that aging can promote heterogeneous losses in different sensorimotor (cognitive and sensory/perceptual processing) components,1010 Anguera JA, Gazzaley A. Dissociation of motor and sensory inhibition processes in normal aging. Clin Neurophysiol. 2012;123(4):730-40. our hypothesis was that reduced plantar sensitivity would exert different impact for the elderly compared to young adults, because young adults would have the capacity to regulate CoP satisfactorily, even under conditions of disturbance in the sensory characteristics of their feet, indicating that this type of information is more important for the elderly than for young adults.

Materials and methods

Participants

Thirty-eight participants invited from the local community were divided into two groups matched for height and body mass. The group of young adults included 19 subjects with mean (SD) age of 35 (5) years, height of 1.65 (0.08) m, and body mass of 63 (10) kg. The elderly group consisted of 19 independent elderly subjects with mean (SD) age of 79 (6) years, height of 1.55 (0.05) m, and body mass of 68 (9) kg. The group of young adults was evaluated in two conditions: one pre- and the other post-sensory disturbance, making a total of three groups in the final analysis: adults without sensory disturbance, post-sensory disturbance adults, and elderly subjects. All participants signed an informed consent in accordance with the Declaration of Helsinki and this study was approved by the Human Research Ethics Committee of the local institution (opinion 082 011). All participants ought to be in a physical condition to walk and to stand on their own feet with no orthosis or prosthesis; moreover, they should be available to visit the laboratory to be part of the evaluations. Exclusion criteria included the presence of cerebellar disease, plantar skin lesions, lower limb traumatic injury history, neuropathy or inability to perform the proposed tasks.

Assessment of plantar sensitivity

Before engaging in the assessment of plantar sensitivity, participants had 10 min of rest, sitting in a chair. The plantar sensitivity was evaluated according to a clinical protocol using a Semmes-Weinstein pressure esthesiometer (Semmes-Weinstein Monofilaments, San Jose, USA).1111 Perry SD. Evaluation of age-related plantar-surface insensitivity and onset age of advanced insensitivity in older adults using vibratory and touch sensation tests. Neurosci Lett. 2006;392(1–2):62-7.,1212 Patel M. Foam posturography: standing on foam is not equivalent to standing with decreased rapidly adapting mechanoreceptive sensation. Exp Brain Res. 2011;208(4):519-25. The esthesiometer consisted of 6 nylon filaments of equal length (Fig. 1A) with varying diameters, able to produce a standardized pressure on the skin surface (considering six values from 0.05 gf to 300 gf) in accordance with calibration and recommendation for use.1313 Holewski JJ, Stess RM, Graf PM, Grunfeld C. Aesthesiometry: quantification of cutaneous pressure sensation in diabetic peripheral neuropathy. J Rehabil Res Dev. 1988;25(2):1-10.

Fig. 1
Illustration of the points where plantar sensitivity was evaluated and the esthesiometer used in the study.

During the assessment, all participants were blindfolded and in a supine position in a quiet and distraction-free environment. All participants were evaluated by the same evaluator. Plantar sensitivity was evaluated in nine different locations of the foot (Fig. 1A) in a randomized order, with an alternation of feet in the evaluation of each participant. Participants indicated in their palm the area where they perceived the tactile stimulus on their feet. All evaluations were performed in the same period of the day. Plantar sensitivity was determined by the initial application of the thin filaments, progressing to the thick filaments until the participant would be able to detect the touch.1414 Feng Y, Schlosser FJ, Sumpio BE. The Semmes Weinstein monofilament examination as a screening tool for diabetic peripheral neuropathy. J Vasc Surg. 2009;50(3):675-682. These touches were performed during 1 second and with two repetitions, so that the filament would take a C-shaped form.

Each filament corresponded to a classification based on their colors, in which green and blue corresponds to a normal sensitivity; violet corresponds to some difficulty of shape and temperature discrimination; red denotes slight loss of a vulnerable to injury, protective sensation; orange denotes a slight loss of protective sensation; pink denotes loss of protective sensation and no response at all.

To determine the sensitivity of the entire foot, the sum of the values for each region was calculated. Thus, the higher the score, the lower the plantar sensitivity.

Postural control assessment

Data acquisition for the evaluation of CoP was made during the standing posture with bipedal support, feet positioned in an abduction of 30° 1515 Azzi NM, Coelho DB, Teixeira LA. Efeito da posição dos pés na recuperação do equilíbrio após perturbação. Anais do V SNA. 2014;1:88-93. with the heels kept 5 cm apart and arms relaxed beside the upper body in two situations: (a) looking toward a fixed point 4 meters ahead and at eye level; (b) with closed eyes.33 Ueda LS, Carpes FP. Relação entre sensibilidade plantar e controle postural em jovens e idosos. Rev Bras Cineantropom Desempenho Hum. 2013;15(2):215-24.

For each visual condition, three attempts of 30 s each were made, the first condition alternating between open and closed eyes in each participant assessed. For all participants, a 30-second interval was observed between attempts. CoP data were collected for each foot with the use of a baropodometer (Tekscan Inc., Boston, MA), with a sampling rate of 100 Hz The following variables were measured: average speed of CoP (CoPsp), anteroposterior (CoPap) and mediolateral (CoPml) amplitude, considering the contact area of each foot with the surface.

Plantar sensitivity disturbance

The plantar sensitivity disturbance protocol was applied only to young adult participants, and aimed to simulate a sensory decrease in foot area – a common finding in the elderly. The disturbance protocol was conducted through hypothermia, similar to the protocol previously used.99 Stal F, Fransson PA, Magnusson M, Karlberg M. Effects of hypothermic anesthesia of the feet on vibration-induced body sway and adaptation. J Vestib Res. 2003;13(1):39-41.,1616 Kunzler MR, Lopes LM, Ueda LS, de Britto MA, Carpes FP. Does skin stimulation compensate impairments in postural control after ankle plantar flexors fatigue? Gait Posture. 2013;37(4):611-615. For the generation of the disturbance in order to obtain the plantar sensorial information, participants completed the protocol in a comfortable sitting position and kept their feet immersed in a container with ice and water, at a controlled temperature between 5 °C and 8 °C for 15 min.33 Ueda LS, Carpes FP. Relação entre sensibilidade plantar e controle postural em jovens e idosos. Rev Bras Cineantropom Desempenho Hum. 2013;15(2):215-24. For the evaluation of CoP after immersion in ice, participants moved immediately from the position described to the standing position on the baropodometer.

Data analysis

Data were grouped (mean and standard deviation) for each group. Data normality was verified with Shapiro–Wilk test. Plantar sensitivity was compared between right and left feet of young adults using the paired t test; in the elderly, the Wilcoxon test was applied. The independent t test was used to compare groups. To obtain an analysis of asymmetries and the effect of vision on CoP data, for all groups and conditions the Wilcoxon test was used. From CoP measurements, young adults, post-sensory disturbance young adults, and elderly groups were compared by analysis of variance, with the post hoc Bonferroni test. In all tests, a 0.05 significance level was set.

Results

The normality test for sensitivity showed a parametric distribution in young adults for the right (p = 0.064) and left (p = 0.177) leg; and for the elderly, a parametric distribution for the right leg (p = 0.175), and a non-parametric distribution for the left leg (p = 0.018) were observed. The sensitivity data were analyzed only for the right foot, as there were no asymmetries in these observations in young adults [t (18) = –0.529; p = 0.603] and in the elderly [Z = –0.393; p = 0.694]. The plantar sensitivity results showed that young adults had a better sensitivity than the elderly for both feet (Table 1). As to the analysis of CoP (Fig. 2), it was found that the visual deprivation did not change any variable of CoP; furthermore, no asymmetries were observed (Fig. 3). Thus, subsequent comparisons were performed using data of the analysis of trials with eyes open and using data from the right foot.

Table 1
Plantar sensitivity scores (data expressed as mean and standard deviation) in each foot. The sum of all points for each foot represents the sensitivity of the whole foot. Higher values represent worse sensitivity.

Fig. 2
CoP amplitude values in anteroposterior (CoPap) and mediolateral (CoPml) directions, in centimeters, on the left vertical axis, and CoP speed (CoPsp) in millimeters per second (mm/s) on the right vertical axis for each group (n = 19 per group). *It indicates statistically significant difference between groups, confirmed by an analysis of variance with post hoc Bonferroni (p < 0.05).
Fig. 3
Mean (bars) and standard deviation of anteroposterior amplitude of the center of pressure (CoPap) and mediolateral amplitude of the center of pressure (CoPml) in centimeters, and center of pressure shift speed (CoPsp) for each group (n = 19 per group) in millimeters per second (mm/s). The left column (column A) displays values for both feet, where R indicates right foot and L indicates left foot. In the right column (column B), values are presented for visual conditions with open eyes (OE) and closed eyes (CE). For both analysis of comparison between right and left foot, the Wilcoxon test was used, with a significance level of 0.05.

Analyzing the amplitude of CoP shift, a group effect was not observed in the anteroposterior direction [F(2) = 2.348; p = 0.105]. On the other hand, in the assessments of CoP shift in the mediolateral direction, a group effect was observed [F(2) = 5.622; p = 0.006]. The post hoc analysis indicated similarity among young adults versus young adults after sensory disturbance (p = 1.000). However, elderly subjects had greater mediolateral shift of CoP versus young adults (p = 0.017), and young adults after sensory disturbance (p = 0.015).

In the same line, a group effect was observed for CoP speed [F(2) = 7.587; p = 0.001]. The post hoc analysis indicated that the group of young adults after sensory disturbance was not different from the “without sensory disturbance” condition (p = 1.00). However, young adults prior to (p = 0.006) and after (p = 0.003) plantar sensitivity disturbance showed lower values versus the elderly.

Discussion

Trying to simulate in young adults the losses in plantar sensitivity experienced by the elderly, we conducted a sensitivity disturbance protocol for plantar sensitivity in young adults. Although this same sensory disturbance protocol has generated changes in plantar sensitivity of adults in a previous study,33 Ueda LS, Carpes FP. Relação entre sensibilidade plantar e controle postural em jovens e idosos. Rev Bras Cineantropom Desempenho Hum. 2013;15(2):215-24.,99 Stal F, Fransson PA, Magnusson M, Karlberg M. Effects of hypothermic anesthesia of the feet on vibration-induced body sway and adaptation. J Vestib Res. 2003;13(1):39-41. the impact of this acute disturbance cannot be regarded as equivalent to that experienced by the elderly, in whom these deficits are present in a continuous and progressive manner.1111 Perry SD. Evaluation of age-related plantar-surface insensitivity and onset age of advanced insensitivity in older adults using vibratory and touch sensation tests. Neurosci Lett. 2006;392(1–2):62-7. However, this is not a specific limitation of our study, but of all studies which seek to investigate this type of question. In addition, differences can also depend on the ability of adults to use information coming from other afferent pathways, possibly the vestibular system, to control CoP.1717 Yasuda T, Nakagawa T, Inoue H, Iwamoto M, Inokuchi A. The role of the labyrinth, proprioception and plantar mechanosensors in the maintenance of an upright posture. Eur Arch Otorhinolaryngol. 1999;256(1):27-32.

There was no asymmetry between the feet with respect to the sensitivity or the oscillation of CoP, which indicates that the evaluated participants showed no influence of functional lateralization in a simple task such as the proposed protocol. Deprivation of visual information and the change in plantar sensitivity did not lead to changes in postural control standards measured in young adults. Nevertheless, some literature findings indicate that individuals of all ages depend on the plantar sensitivity to maintain balance in the standing posture, and old age leads to an increased body sway.1818 Lord SR, Ward JA. Age-associated differences in sensori-motor function and balance in community dwelling women. Age Ageing. 1994;23(6):452-60. Ueda et al.33 Ueda LS, Carpes FP. Relação entre sensibilidade plantar e controle postural em jovens e idosos. Rev Bras Cineantropom Desempenho Hum. 2013;15(2):215-24. found an increase in anteroposterior shift of CoP of the whole body in the elderly, compared to young adults, and our evaluation of CoP for each foot showed that the mediolateral amplitude of CoP is greater in older subjects than in young adults (with or without sensory disturbance). This result is relevant, since the measurement of the mediolateral amplitude is important for predicting the risk of falls in the elderly population1919 Brauer S, Burns Y, Galley P. Lateral reach: a clinical measure of medio-lateral postural stability. Physiother Res Int. 1999;4(2):81-8.; thus, our result is an indicator of vulnerability to falls in elderly patients with compromised plantar sensitivity. The same happened with CoP velocity, which remained higher in elderly versus young adults before and after sensory disturbance, meaning a worse performance in controlling the standing posture. This variable is described by Hewson et al.2020 Hewson DJ, Singh NK, Snoussi H, Duchene J. Classification of elderly as fallers and non-fallers using Centre of Pressure velocity. IEEE Trans Biomed Eng. 2010;2010:3678-81. as being useful in the classification of elderly people with and without risk of falls. Again, we find a variable that can indicate the negative influence of reduced sensitivity on the stability of the elderly.

Our results corroborate the findings of a recent study2121 Billot M, Handrigan GA, Simoneau M, Teasdale N. Reduced plantar sole sensitivity induces balance control modifications to compensate ankle tendon vibration and vision deprivation. Physiother Res Int. 2014;25(1):155-60. that also found no increase in CoP shifts when visual information was not available, or with disturbance of the sensitivity of adult feet.2222 Hafstrom A, Fransson PA, Karlberg M, Ledin T, Magnusson M. Visual influence on postural control, with and without visual motion feedback. Acta Otolaryngol. 2002;122(4):392-9. This recent study has shown that sole cooling does not alter the balance control either with or without vision information available. In our study, even when visual information was unavailable and the sensory plantar information was disturbed, young adults continued to have better postural control than the elderly. This can be explained by the possibility that, for adults, decreases in the temperature of the plantar area induce a readjustment in the use of sensory information, in the search for preservation of postural control in the face of the experienced deficits, with special attention to other afferent pathways, such as vestibular information.2121 Billot M, Handrigan GA, Simoneau M, Teasdale N. Reduced plantar sole sensitivity induces balance control modifications to compensate ankle tendon vibration and vision deprivation. Physiother Res Int. 2014;25(1):155-60.

Yasuda et al.1717 Yasuda T, Nakagawa T, Inoue H, Iwamoto M, Inokuchi A. The role of the labyrinth, proprioception and plantar mechanosensors in the maintenance of an upright posture. Eur Arch Otorhinolaryngol. 1999;256(1):27-32. point out that the major mechanism contributing to the control of orthostatic posture is the vestibular system. Knowing that this system is impaired with advancing age,2323 Matheson AJ, Darlington CL, Smith PF. Dizziness in the elderly and age-related degeneration of the vestibular system. NZ J Psychol. 1999;28(1):10-16. it can be inferred that adults get better postural control values that the elderly because, even with the deprivation of vision and in a scenario of plantar sensitivity disturbance, the young adults maintained a body adjustment system in better condition. On the other hand, knowing that vestibular problems are one of the most common causes of dizziness and imbalance in the elderly,2424 Iwasaki S, Yamasoba T. Dizziness and imbalance in the elderly: age-related decline in the vestibular system. Aging Disease. 2015;6(1):38-47. and considering that the loss of plantar sensitivity in elderly people is related to the greater fluctuation of the CoP, it may be suggested that interventions that aim to maintain or reduce losses in plantar sensitivity can help maintaining postural balance to compensate for compromises in CoP under the acute effect of the disturbance. We did not evaluate post-hypothermia sensitivity because studies show that the effect of the immersion of the feet in water and ice on postural control can be compensated for shortly after the end of the immersion.99 Stal F, Fransson PA, Magnusson M, Karlberg M. Effects of hypothermic anesthesia of the feet on vibration-induced body sway and adaptation. J Vestib Res. 2003;13(1):39-41. An evaluation of sensitivity after immersion in water and ice would require a time that would cancel the effects of sensory change sought by our group. On the other hand, other studies were published indicating that this type of protocol is effective for plantar sensitivity disturbance.1212 Patel M. Foam posturography: standing on foam is not equivalent to standing with decreased rapidly adapting mechanoreceptive sensation. Exp Brain Res. 2011;208(4):519-25.,2525 Douglas M, Bivens S, Pesterfield J, Clemson N, Castle W, Sole G, et al. Immediate effects of cryotherapy on static and dynamic balance. Int J Sports Phys Ther. 2013;8(1):9-14. In our study, we considered the measurement of CoP in each foot, because the determination of plantar sensitivity is done on each foot. While this may not be a limitation in our discussion, our procedure still leaves room for an investigation that also monitor the shift of the center of gravity, allowing a broader view of postural stability in response to disturbances in plantar sensitivity.

Conclusion

The elderly and young adults differ in relation to their dependence on plantar sensitivity in order to maintain the upright posture, on the basis of CoP measures, wherein the plantar sensory information appears more important for the elderly. It is possible that clinical interventions that improve the plantar sensitivity in the elderly can contribute to improve the control of orthostatic posture.

  • Funding
    FAPERGS (process 1013100).

REFERENCES

  • 1
    Winter D. Biomechanics and motor control of human movement. 4ª ed. John Wiley & Sons; 1990. p. 370.
  • 2
    Freitas SM, Wieczorek SA, Marchetti PH, Duarte M. Age-related changes in human postural control of prolonged standing. Gait Posture. 2005;22(4):322-30.
  • 3
    Ueda LS, Carpes FP. Relação entre sensibilidade plantar e controle postural em jovens e idosos. Rev Bras Cineantropom Desempenho Hum. 2013;15(2):215-24.
  • 4
    Schlee G, Sterzing T, Milani TL. Foot sole skin temperature affects plantar foot sensitivity. Clin Neurophysiol. 2009;120(8):1548-611.
  • 5
    Billot M, Handrigan GA, Simoneau M, Corbeil P, Teasdale N. Short term alteration of balance control after a reduction of plantar mechanoreceptor sensation through cooling. Neurosci Lett. 2013;535:40-4.
  • 6
    Ducic I, Short KW, Dellon AL. Relationship between loss of pedal sensibility, balance, and falls in patients with peripheral neuropathy. Ann Plast Surg. 2004;52(6):535-610.
  • 7
    Zhang S, Li L. The differential effects of foot sole sensory on plantar pressure distribution between balance and gait. Gait Posture. 2013;37(4):532-7.
  • 8
    Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM. Measures of postural steadiness: differences between healthy young and elderly adults. IEEE Trans Biomed Eng. 1996;43(9):956-966.
  • 9
    Stal F, Fransson PA, Magnusson M, Karlberg M. Effects of hypothermic anesthesia of the feet on vibration-induced body sway and adaptation. J Vestib Res. 2003;13(1):39-41.
  • 10
    Anguera JA, Gazzaley A. Dissociation of motor and sensory inhibition processes in normal aging. Clin Neurophysiol. 2012;123(4):730-40.
  • 11
    Perry SD. Evaluation of age-related plantar-surface insensitivity and onset age of advanced insensitivity in older adults using vibratory and touch sensation tests. Neurosci Lett. 2006;392(1–2):62-7.
  • 12
    Patel M. Foam posturography: standing on foam is not equivalent to standing with decreased rapidly adapting mechanoreceptive sensation. Exp Brain Res. 2011;208(4):519-25.
  • 13
    Holewski JJ, Stess RM, Graf PM, Grunfeld C. Aesthesiometry: quantification of cutaneous pressure sensation in diabetic peripheral neuropathy. J Rehabil Res Dev. 1988;25(2):1-10.
  • 14
    Feng Y, Schlosser FJ, Sumpio BE. The Semmes Weinstein monofilament examination as a screening tool for diabetic peripheral neuropathy. J Vasc Surg. 2009;50(3):675-682.
  • 15
    Azzi NM, Coelho DB, Teixeira LA. Efeito da posição dos pés na recuperação do equilíbrio após perturbação. Anais do V SNA. 2014;1:88-93.
  • 16
    Kunzler MR, Lopes LM, Ueda LS, de Britto MA, Carpes FP. Does skin stimulation compensate impairments in postural control after ankle plantar flexors fatigue? Gait Posture. 2013;37(4):611-615.
  • 17
    Yasuda T, Nakagawa T, Inoue H, Iwamoto M, Inokuchi A. The role of the labyrinth, proprioception and plantar mechanosensors in the maintenance of an upright posture. Eur Arch Otorhinolaryngol. 1999;256(1):27-32.
  • 18
    Lord SR, Ward JA. Age-associated differences in sensori-motor function and balance in community dwelling women. Age Ageing. 1994;23(6):452-60.
  • 19
    Brauer S, Burns Y, Galley P. Lateral reach: a clinical measure of medio-lateral postural stability. Physiother Res Int. 1999;4(2):81-8.
  • 20
    Hewson DJ, Singh NK, Snoussi H, Duchene J. Classification of elderly as fallers and non-fallers using Centre of Pressure velocity. IEEE Trans Biomed Eng. 2010;2010:3678-81.
  • 21
    Billot M, Handrigan GA, Simoneau M, Teasdale N. Reduced plantar sole sensitivity induces balance control modifications to compensate ankle tendon vibration and vision deprivation. Physiother Res Int. 2014;25(1):155-60.
  • 22
    Hafstrom A, Fransson PA, Karlberg M, Ledin T, Magnusson M. Visual influence on postural control, with and without visual motion feedback. Acta Otolaryngol. 2002;122(4):392-9.
  • 23
    Matheson AJ, Darlington CL, Smith PF. Dizziness in the elderly and age-related degeneration of the vestibular system. NZ J Psychol. 1999;28(1):10-16.
  • 24
    Iwasaki S, Yamasoba T. Dizziness and imbalance in the elderly: age-related decline in the vestibular system. Aging Disease. 2015;6(1):38-47.
  • 25
    Douglas M, Bivens S, Pesterfield J, Clemson N, Castle W, Sole G, et al. Immediate effects of cryotherapy on static and dynamic balance. Int J Sports Phys Ther. 2013;8(1):9-14.

Publication Dates

  • Publication in this collection
    Jan-Feb 2017

History

  • Received
    25 Aug 2015
  • Accepted
    24 Nov 2015
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