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Erschienen in: International Journal of Diabetes in Developing Countries 1/2024

12.05.2023 | Original Article

Role of sensory feedback in postural control of the patients with diabetic neuropathy

verfasst von: Alireza Reisi, Alireza Hashemi-Oskouei, Mohammed N. Ashtiani, Farid Bahrpeyma

Erschienen in: International Journal of Diabetes in Developing Countries | Ausgabe 1/2024

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Abstract

Background/Purpose

Impaired balance is prevalent in patients with type II diabetes mellitus (T2DM). The aim of the current study was to evaluate the role of sensory information in these patients.

Methods

Stabilogram-diffusion analysis was utilized to categorize the balance into local and central control modes based on the center of pressure (CoP) data acquired from quiet standing tests of 36 patients with T2DM and 20 healthy individuals. Local control was considered the efforts of muscles to stiffen the joints. Central control was the mode in which sensory information is used. Open- and closed-eye conditions were added to detect other sensory sources during the standing. Traditional linear measures of stability were also calculated for anterior–posterior and mediolateral directions.

Results

Results showed that sway area, pathlength, and maximum velocity of the CoP are higher in the T2DM group (p < 0.001) in open-eye condition, but they did not change in eyes closed (p > 0.158). Both the local and central control mechanisms can cause postural instability in AP direction in patients with T2DM (p < 0.017). Contrarily, diabetes had no effect on the ML direction (p > 0.051). Patients with T2DM had a significant delay (about 225 ms greater than the controls) in the use of sensory information reflected in the AP direction outputs (p < 0.009).

Conclusion

The patients with T2DM had poorer stability due to the delayed use of the sensory information. Diabetic postural stability was not fully provided in comparison with the healthy people even with using the sensory information. Elimination of the visual feedback led to reduced postural balance in these patients.
Literatur
1.
Zurück zum Zitat Tilling LM, Darawil K, Britton M. Falls as a complication of diabetes mellitus in older people. J Diabetes Complicat. 2006;20:158–62.CrossRef Tilling LM, Darawil K, Britton M. Falls as a complication of diabetes mellitus in older people. J Diabetes Complicat. 2006;20:158–62.CrossRef
2.
Zurück zum Zitat Ajimsha M, Paul J, Chithra S. Efficacy of stability trainer in improving balance in type II diabetic patients with distal sensory neuropathy. J Diabetol. 2011;2:7. Ajimsha M, Paul J, Chithra S. Efficacy of stability trainer in improving balance in type II diabetic patients with distal sensory neuropathy. J Diabetol. 2011;2:7.
3.
Zurück zum Zitat Hsu C-R, Chen Y-T, Sheu WH-H. Glycemic variability and diabetes retinopathy: a missing link. J Diabetes Complicat. 2015;29:302–6.CrossRef Hsu C-R, Chen Y-T, Sheu WH-H. Glycemic variability and diabetes retinopathy: a missing link. J Diabetes Complicat. 2015;29:302–6.CrossRef
4.
Zurück zum Zitat Hatef B, Bahrpeyma F, Mohajeri Tehrani MR. The comparison of muscle strength and short-term endurance in the different periods of type 2 diabetes. J Diabetes Metab Disord. 2014;13:1–10.CrossRef Hatef B, Bahrpeyma F, Mohajeri Tehrani MR. The comparison of muscle strength and short-term endurance in the different periods of type 2 diabetes. J Diabetes Metab Disord. 2014;13:1–10.CrossRef
5.
Zurück zum Zitat Najafi B, Horn D, Marclay S, Crews RT, Wu S, Wrobel JS. Assessing postural control and postural control strategy in diabetes patients using innovative and wearable technology. J Diabetes Sci Technol. 2010;4:780–91.PubMedPubMedCentralCrossRef Najafi B, Horn D, Marclay S, Crews RT, Wu S, Wrobel JS. Assessing postural control and postural control strategy in diabetes patients using innovative and wearable technology. J Diabetes Sci Technol. 2010;4:780–91.PubMedPubMedCentralCrossRef
6.
Zurück zum Zitat Vaz MM, Costa GC, Reis JG, Junior WM, de Paula FJA, Abreu DC. Postural control and functional strength in patients with type 2 diabetes mellitus with and without peripheral neuropathy. Arch Phys Med Rehabil. 2013;94:2465–70.PubMedCrossRef Vaz MM, Costa GC, Reis JG, Junior WM, de Paula FJA, Abreu DC. Postural control and functional strength in patients with type 2 diabetes mellitus with and without peripheral neuropathy. Arch Phys Med Rehabil. 2013;94:2465–70.PubMedCrossRef
7.
Zurück zum Zitat Boucher P, Teasdale N, Courtemanche R, Bard C, Fleury M. Postural stability in diabetic polyneuropathy. Diabetes Care. 1995;18:638–45.PubMedCrossRef Boucher P, Teasdale N, Courtemanche R, Bard C, Fleury M. Postural stability in diabetic polyneuropathy. Diabetes Care. 1995;18:638–45.PubMedCrossRef
8.
Zurück zum Zitat Giacomini PG, Bruno E, Monticone G, Di Girolamo S, Magrini A, Parisi L, et al. Postural rearrangement in IDDM patients with peripheral neuropathy. Diabetes Care. 1996;19:372–4.PubMedCrossRef Giacomini PG, Bruno E, Monticone G, Di Girolamo S, Magrini A, Parisi L, et al. Postural rearrangement in IDDM patients with peripheral neuropathy. Diabetes Care. 1996;19:372–4.PubMedCrossRef
9.
Zurück zum Zitat Morrison S, Colberg S, Parson H, Vinik A. Relation between risk of falling and postural sway complexity in diabetes. Gait Posture. 2012;35:662–8.PubMedCrossRef Morrison S, Colberg S, Parson H, Vinik A. Relation between risk of falling and postural sway complexity in diabetes. Gait Posture. 2012;35:662–8.PubMedCrossRef
10.
Zurück zum Zitat Dixit S, Maiya A, Shasthry B, Kumaran DS, Guddattu V. Postural sway in diabetic peripheral neuropathy among Indian elderly. Indian J Med Res. 2015;142:713.PubMedPubMedCentralCrossRef Dixit S, Maiya A, Shasthry B, Kumaran DS, Guddattu V. Postural sway in diabetic peripheral neuropathy among Indian elderly. Indian J Med Res. 2015;142:713.PubMedPubMedCentralCrossRef
11.
Zurück zum Zitat Mustapa A, Justine M, Mohd Mustafah N, Jamil N, Manaf H. Postural control and gait performance in the diabetic peripheral neuropathy: a systematic review. Biomed Res Int. 2016;2016:9305025.PubMedPubMedCentralCrossRef Mustapa A, Justine M, Mohd Mustafah N, Jamil N, Manaf H. Postural control and gait performance in the diabetic peripheral neuropathy: a systematic review. Biomed Res Int. 2016;2016:9305025.PubMedPubMedCentralCrossRef
12.
Zurück zum Zitat DiLiberto FE, Nawoczenski DA, Tome J, McKeon PO. Use of time-to-boundary to assess postural instability and predict functional mobility in people with diabetes mellitus and peripheral neuropathy. Gait Posture. 2021;83:141–6.PubMedCrossRef DiLiberto FE, Nawoczenski DA, Tome J, McKeon PO. Use of time-to-boundary to assess postural instability and predict functional mobility in people with diabetes mellitus and peripheral neuropathy. Gait Posture. 2021;83:141–6.PubMedCrossRef
13.
Zurück zum Zitat Wong E, Backholer K, Gearon E, Harding J, Freak-Poli R, Stevenson C, et al. Diabetes and risk of physical disability in adults: a systematic review and meta-analysis. Lancet Diabetes Endocrinol. 2013;1:106–14.PubMedCrossRef Wong E, Backholer K, Gearon E, Harding J, Freak-Poli R, Stevenson C, et al. Diabetes and risk of physical disability in adults: a systematic review and meta-analysis. Lancet Diabetes Endocrinol. 2013;1:106–14.PubMedCrossRef
14.
Zurück zum Zitat Wardlaw JM, Smith C, Dichgans M. Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. The Lancet Neurology. 2013;12:483–97.PubMedCrossRef Wardlaw JM, Smith C, Dichgans M. Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. The Lancet Neurology. 2013;12:483–97.PubMedCrossRef
15.
Zurück zum Zitat Hughes TM, Ryan CM, Aizenstein HJ, Nunley K, Gianaros PJ, Miller R, et al. Frontal gray matter atrophy in middle aged adults with type 1 diabetes is independent of cardiovascular risk factors and diabetes complications. J Diabetes Complicat. 2013;27:558–64.CrossRef Hughes TM, Ryan CM, Aizenstein HJ, Nunley K, Gianaros PJ, Miller R, et al. Frontal gray matter atrophy in middle aged adults with type 1 diabetes is independent of cardiovascular risk factors and diabetes complications. J Diabetes Complicat. 2013;27:558–64.CrossRef
16.
Zurück zum Zitat Erus G, Battapady H, Zhang T, Lovato J, Miller ME, Williamson JD, et al. Spatial patterns of structural brain changes in type 2 diabetic patients and their longitudinal progression with intensive control of blood glucose. Diabetes Care. 2015;38:97–104.PubMedCrossRef Erus G, Battapady H, Zhang T, Lovato J, Miller ME, Williamson JD, et al. Spatial patterns of structural brain changes in type 2 diabetic patients and their longitudinal progression with intensive control of blood glucose. Diabetes Care. 2015;38:97–104.PubMedCrossRef
17.
Zurück zum Zitat Stranahan AM, Norman ED, Lee K, Cutler RG, Telljohann RS, Egan JM, et al. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus. 2008;18:1085–8.PubMedPubMedCentralCrossRef Stranahan AM, Norman ED, Lee K, Cutler RG, Telljohann RS, Egan JM, et al. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus. 2008;18:1085–8.PubMedPubMedCentralCrossRef
18.
Zurück zum Zitat Cui Y, Jiao Y, Chen Y-C, Wang K, Gao B, Wen S, et al. Altered spontaneous brain activity in type 2 diabetes: a resting-state functional MRI study. Diabetes. 2014;63:749–60.PubMedCrossRef Cui Y, Jiao Y, Chen Y-C, Wang K, Gao B, Wen S, et al. Altered spontaneous brain activity in type 2 diabetes: a resting-state functional MRI study. Diabetes. 2014;63:749–60.PubMedCrossRef
19.
Zurück zum Zitat Wang C-X, Fu K-L, Liu H-J, Xing F, Zhang S-Y. Spontaneous brain activity in type 2 diabetics revealed by amplitude of low-frequency fluctuations and its association with diabetic vascular disease: a resting-state FMRI study. PLoS ONE. 2014;9: e108883.PubMedPubMedCentralCrossRef Wang C-X, Fu K-L, Liu H-J, Xing F, Zhang S-Y. Spontaneous brain activity in type 2 diabetics revealed by amplitude of low-frequency fluctuations and its association with diabetic vascular disease: a resting-state FMRI study. PLoS ONE. 2014;9: e108883.PubMedPubMedCentralCrossRef
20.
Zurück zum Zitat Peng J, Qu H, Peng J, Luo T-Y, Lv F-J, Wang Z-N, et al. Abnormal spontaneous brain activity in type 2 diabetes with and without microangiopathy revealed by regional homogeneity. Eur J Radiol. 2016;85:607–15.PubMedCrossRef Peng J, Qu H, Peng J, Luo T-Y, Lv F-J, Wang Z-N, et al. Abnormal spontaneous brain activity in type 2 diabetes with and without microangiopathy revealed by regional homogeneity. Eur J Radiol. 2016;85:607–15.PubMedCrossRef
22.
Zurück zum Zitat Centomo H, Termoz N, Savoie S, Beliveau L, Prince F. Postural control following a self-initiated reaching task in type 2 diabetic patients and age-matched controls. Gait Posture. 2007;25:509–14.PubMedCrossRef Centomo H, Termoz N, Savoie S, Beliveau L, Prince F. Postural control following a self-initiated reaching task in type 2 diabetic patients and age-matched controls. Gait Posture. 2007;25:509–14.PubMedCrossRef
23.
Zurück zum Zitat Allet L, Armand S, de Bie RA, Pataky Z, Aminian K, Herrmann FR, et al. Gait alterations of diabetic patients while walking on different surfaces. Gait Posture. 2009;29:488–93.PubMedCrossRef Allet L, Armand S, de Bie RA, Pataky Z, Aminian K, Herrmann FR, et al. Gait alterations of diabetic patients while walking on different surfaces. Gait Posture. 2009;29:488–93.PubMedCrossRef
24.
Zurück zum Zitat Collins JJ, De Luca CJ. Open-loop and closed-loop control of posture: a random-walk analysis of center-of-pressure trajectories. Exp Brain Res. 1993;95:308–18.PubMedCrossRef Collins JJ, De Luca CJ. Open-loop and closed-loop control of posture: a random-walk analysis of center-of-pressure trajectories. Exp Brain Res. 1993;95:308–18.PubMedCrossRef
25.
Zurück zum Zitat Toosizadeh N, Mohler J, Armstrong DG, Talal TK, Najafi B. The influence of diabetic peripheral neuropathy on local postural muscle and central sensory feedback balance control. PLoS ONE. 2015;10: e0135255.PubMedPubMedCentralCrossRef Toosizadeh N, Mohler J, Armstrong DG, Talal TK, Najafi B. The influence of diabetic peripheral neuropathy on local postural muscle and central sensory feedback balance control. PLoS ONE. 2015;10: e0135255.PubMedPubMedCentralCrossRef
26.
Zurück zum Zitat Ashtiani MN, Azghani M-R. Open-and closed-loop responses of joint mechanisms in perturbed stance under visual and cognitive interference. Biomed Signal Process Control. 2018;42:1–8.CrossRef Ashtiani MN, Azghani M-R. Open-and closed-loop responses of joint mechanisms in perturbed stance under visual and cognitive interference. Biomed Signal Process Control. 2018;42:1–8.CrossRef
27.
Zurück zum Zitat Mitchell SL, Collin J, De Luca CJ, Burrows A, Lipsitz LA. Open-loop and closed-loop postural control mechanisms in Parkinson’s disease: increased mediolateral activity during quiet standing. Neurosci Lett. 1995;197:133–6.PubMedCrossRef Mitchell SL, Collin J, De Luca CJ, Burrows A, Lipsitz LA. Open-loop and closed-loop postural control mechanisms in Parkinson’s disease: increased mediolateral activity during quiet standing. Neurosci Lett. 1995;197:133–6.PubMedCrossRef
28.
Zurück zum Zitat Kurz I, Oddsson L, Melzer I. Characteristics of balance control in older persons who fall with injury–a prospective study. J Electromyogr Kinesiol. 2013;23:814–9.PubMedCrossRef Kurz I, Oddsson L, Melzer I. Characteristics of balance control in older persons who fall with injury–a prospective study. J Electromyogr Kinesiol. 2013;23:814–9.PubMedCrossRef
29.
Zurück zum Zitat Safi K, Hutin E, Mohammed S, Albertsen IM, Delechelle E, Amirat Y, et al. Human static postures analysis using empirical mode decomposition. 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC): IEEE; 2016. p. 3765–8. Safi K, Hutin E, Mohammed S, Albertsen IM, Delechelle E, Amirat Y, et al. Human static postures analysis using empirical mode decomposition. 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC): IEEE; 2016. p. 3765–8.
30.
Zurück zum Zitat Wuehr M, Pradhan C, Novozhilov S, Krafczyk S, Brandt T, Jahn K, et al. Inadequate interaction between open-and closed-loop postural control in phobic postural vertigo. J Neurol. 2013;260:1314–23.PubMedCrossRef Wuehr M, Pradhan C, Novozhilov S, Krafczyk S, Brandt T, Jahn K, et al. Inadequate interaction between open-and closed-loop postural control in phobic postural vertigo. J Neurol. 2013;260:1314–23.PubMedCrossRef
31.
Zurück zum Zitat Nardone A, Schieppati M. Group II spindle fibres and afferent control of stance. Clues from diabetic neuropathy. Clin Neurophysiol. 2004;115:779–89.PubMedCrossRef Nardone A, Schieppati M. Group II spindle fibres and afferent control of stance. Clues from diabetic neuropathy. Clin Neurophysiol. 2004;115:779–89.PubMedCrossRef
32.
Zurück zum Zitat Nardone A, Grasso M, Schieppati M. Balance control in peripheral neuropathy: are patients equally unstable under static and dynamic conditions? Gait Posture. 2006;23:364–73.PubMedCrossRef Nardone A, Grasso M, Schieppati M. Balance control in peripheral neuropathy: are patients equally unstable under static and dynamic conditions? Gait Posture. 2006;23:364–73.PubMedCrossRef
33.
Zurück zum Zitat Simmons RW, Richardson C, Pozos R. Postural stability of diabetic patients with and without cutaneous sensory deficit in the foot. Diabetes Res Clin Pract. 1997;36:153–60.PubMedCrossRef Simmons RW, Richardson C, Pozos R. Postural stability of diabetic patients with and without cutaneous sensory deficit in the foot. Diabetes Res Clin Pract. 1997;36:153–60.PubMedCrossRef
34.
Zurück zum Zitat Yamamoto R, Kinoshita T, Momoki T, Arai T, Okamura A, Hirao K, et al. Postural sway and diabetic peripheral neuropathy. Diabetes Res Clin Pract. 2001;52:213–21.PubMedCrossRef Yamamoto R, Kinoshita T, Momoki T, Arai T, Okamura A, Hirao K, et al. Postural sway and diabetic peripheral neuropathy. Diabetes Res Clin Pract. 2001;52:213–21.PubMedCrossRef
35.
Zurück zum Zitat Simoneau GG, Ulbrecht JS, Derr JA, Cavanagh PR. Role of somatosensory input in the control of human posture. Gait Posture. 1995;3:115–22.CrossRef Simoneau GG, Ulbrecht JS, Derr JA, Cavanagh PR. Role of somatosensory input in the control of human posture. Gait Posture. 1995;3:115–22.CrossRef
36.
Zurück zum Zitat Cavanagh PR, Simoneau GG, Ulbrecht JS. Ulceration, unsteadiness, and uncertainty: the biomechanical consequences of diabetes mellitus. J Biomech. 1993;26:23–40.PubMedCrossRef Cavanagh PR, Simoneau GG, Ulbrecht JS. Ulceration, unsteadiness, and uncertainty: the biomechanical consequences of diabetes mellitus. J Biomech. 1993;26:23–40.PubMedCrossRef
37.
Zurück zum Zitat Abbruzzese G, Schenone A, Scramuzza G, Caponnetto C, Gasparetto B, Adezati L, et al. Impairment of central motor conduction in diabetic patients. Electroencephalogr Clin Neurophysiol/Evoked Potentials Sect. 1993;89:335–40.CrossRef Abbruzzese G, Schenone A, Scramuzza G, Caponnetto C, Gasparetto B, Adezati L, et al. Impairment of central motor conduction in diabetic patients. Electroencephalogr Clin Neurophysiol/Evoked Potentials Sect. 1993;89:335–40.CrossRef
38.
Zurück zum Zitat Moglia A, Arrigo A, Maurelli M, Alfonsi E, Bodini A, Lozza A, et al. Central motor conduction after magnetic stimulation in diabetes. Ital J Neurol Sci. 1998;19:10–4.PubMedCrossRef Moglia A, Arrigo A, Maurelli M, Alfonsi E, Bodini A, Lozza A, et al. Central motor conduction after magnetic stimulation in diabetes. Ital J Neurol Sci. 1998;19:10–4.PubMedCrossRef
39.
Zurück zum Zitat Muramatsu K, Ikutomo M, Tamaki T, Shimo S, Niwa M. Effect of streptozotocin-induced diabetes on motor representations in the motor cortex and corticospinal tract in rats. Brain Res. 2018;1680:115–26.PubMedCrossRef Muramatsu K, Ikutomo M, Tamaki T, Shimo S, Niwa M. Effect of streptozotocin-induced diabetes on motor representations in the motor cortex and corticospinal tract in rats. Brain Res. 2018;1680:115–26.PubMedCrossRef
40.
Zurück zum Zitat Almeida S, Riddell M, Cafarelli E. Slower conduction velocity and motor unit discharge frequency are associated with muscle fatigue during isometric exercise in type 1 diabetes mellitus. Muscle Nerve. 2008;37:231–40.PubMedCrossRef Almeida S, Riddell M, Cafarelli E. Slower conduction velocity and motor unit discharge frequency are associated with muscle fatigue during isometric exercise in type 1 diabetes mellitus. Muscle Nerve. 2008;37:231–40.PubMedCrossRef
41.
Zurück zum Zitat Ferris JK, Inglis JT, Madden KM, Boyd LA. Brain and body: a review of central nervous system contributions to movement impairments in diabetes. Diabetes. 2020;69:3–11.PubMedCrossRef Ferris JK, Inglis JT, Madden KM, Boyd LA. Brain and body: a review of central nervous system contributions to movement impairments in diabetes. Diabetes. 2020;69:3–11.PubMedCrossRef
43.
Zurück zum Zitat Andersen H, Nielsen S, Mogensen CE, Jakobsen J. Muscle strength in type 2 diabetes. Diabetes. 2004;53:1543–8.PubMedCrossRef Andersen H, Nielsen S, Mogensen CE, Jakobsen J. Muscle strength in type 2 diabetes. Diabetes. 2004;53:1543–8.PubMedCrossRef
44.
Zurück zum Zitat Ferreira JP, Sartor CD, Leal AM, Sacco IC, Sato TO, Ribeiro IL, et al. The effect of peripheral neuropathy on lower limb muscle strength in diabetic individuals. Clin Biomech. 2017;43:67–73.CrossRef Ferreira JP, Sartor CD, Leal AM, Sacco IC, Sato TO, Ribeiro IL, et al. The effect of peripheral neuropathy on lower limb muscle strength in diabetic individuals. Clin Biomech. 2017;43:67–73.CrossRef
45.
Zurück zum Zitat Peterson MD, Zhang P, Choksi P, Markides KS, Al SS. Muscle weakness thresholds for prediction of diabetes in adults. Sports Med. 2016;46:619–28.PubMedPubMedCentralCrossRef Peterson MD, Zhang P, Choksi P, Markides KS, Al SS. Muscle weakness thresholds for prediction of diabetes in adults. Sports Med. 2016;46:619–28.PubMedPubMedCentralCrossRef
46.
Zurück zum Zitat Oh TJ, Kang S, Lee J-E, Moon JH, Choi SH, Lim S, et al. Association between deterioration in muscle strength and peripheral neuropathy in people with diabetes. J Diabetes Complicat. 2019;33:598–601.CrossRef Oh TJ, Kang S, Lee J-E, Moon JH, Choi SH, Lim S, et al. Association between deterioration in muscle strength and peripheral neuropathy in people with diabetes. J Diabetes Complicat. 2019;33:598–601.CrossRef
47.
Zurück zum Zitat Collins J, De Luca C, Burrows A, Lipsitz L. Age-related changes in open-loop and closed-loop postural control mechanisms. Exp Brain Res. 1995;104:480–92.PubMedCrossRef Collins J, De Luca C, Burrows A, Lipsitz L. Age-related changes in open-loop and closed-loop postural control mechanisms. Exp Brain Res. 1995;104:480–92.PubMedCrossRef
48.
Zurück zum Zitat Van Deursen RWM, Sanchez MM, Ulbrecht JS, Cavanagh PR. The role of muscle spindles in ankle movement perception in human subjects with diabetic neuropathy. Exp Brain Res. 1998;120:1–8.PubMedCrossRef Van Deursen RWM, Sanchez MM, Ulbrecht JS, Cavanagh PR. The role of muscle spindles in ankle movement perception in human subjects with diabetic neuropathy. Exp Brain Res. 1998;120:1–8.PubMedCrossRef
49.
Zurück zum Zitat Muller KA, Ryals JM, Feldman EL, Wright DE. Abnormal muscle spindle innervation and large-fiber neuropathy in diabetic mice. Diabetes. 2008;57:1693–701.PubMedCrossRef Muller KA, Ryals JM, Feldman EL, Wright DE. Abnormal muscle spindle innervation and large-fiber neuropathy in diabetic mice. Diabetes. 2008;57:1693–701.PubMedCrossRef
50.
Zurück zum Zitat Yahya A, Kluding P, Pasnoor M, Wick J, Liu W, Dos Santos M. The impact of diabetic peripheral neuropathy on pinch proprioception. Exp Brain Res. 2019;237:3165–74.PubMedCrossRef Yahya A, Kluding P, Pasnoor M, Wick J, Liu W, Dos Santos M. The impact of diabetic peripheral neuropathy on pinch proprioception. Exp Brain Res. 2019;237:3165–74.PubMedCrossRef
51.
Zurück zum Zitat IJzerman TH, Schaper NC, Melai T, Meijer K, Willems PJ, Savelberg HH. Lower extremity muscle strength is reduced in people with type 2 diabetes, with and without polyneuropathy, and is associated with impaired mobility and reduced quality of life. Diabetes Res Clin Pract. 2012;95:345–51.PubMedCrossRef IJzerman TH, Schaper NC, Melai T, Meijer K, Willems PJ, Savelberg HH. Lower extremity muscle strength is reduced in people with type 2 diabetes, with and without polyneuropathy, and is associated with impaired mobility and reduced quality of life. Diabetes Res Clin Pract. 2012;95:345–51.PubMedCrossRef
52.
Zurück zum Zitat Orlando G, Balducci S, Bazzucchi I, Pugliese G, Sacchetti M. Neuromuscular dysfunction in type 2 diabetes: underlying mechanisms and effect of resistance training. Diabetes Metab Res Rev. 2016;32:40–50.PubMedCrossRef Orlando G, Balducci S, Bazzucchi I, Pugliese G, Sacchetti M. Neuromuscular dysfunction in type 2 diabetes: underlying mechanisms and effect of resistance training. Diabetes Metab Res Rev. 2016;32:40–50.PubMedCrossRef
53.
Zurück zum Zitat Mégrot F, Bardy BG, Dietrich G. Dimensionality and the dynamics of human unstable equilibrium. J Mot Behav. 2002;34:323–8.PubMedCrossRef Mégrot F, Bardy BG, Dietrich G. Dimensionality and the dynamics of human unstable equilibrium. J Mot Behav. 2002;34:323–8.PubMedCrossRef
54.
Zurück zum Zitat Ashtiani MN, Azghani MR. Nonlinear dynamics analysis of the human balance control subjected to physical and sensory perturbations. Acta Neurobiologiae Experimentalis. 2017;77:168–75.PubMedCrossRef Ashtiani MN, Azghani MR. Nonlinear dynamics analysis of the human balance control subjected to physical and sensory perturbations. Acta Neurobiologiae Experimentalis. 2017;77:168–75.PubMedCrossRef
55.
Zurück zum Zitat Mbongo F, Qu’hen C, Vidal P, Huy PTB, De Waele C. Role of vestibular input in triggering and modulating postural responses in unilateral and bilateral vestibular loss patients. Audiol Neurotol. 2009;14:130–8.CrossRef Mbongo F, Qu’hen C, Vidal P, Huy PTB, De Waele C. Role of vestibular input in triggering and modulating postural responses in unilateral and bilateral vestibular loss patients. Audiol Neurotol. 2009;14:130–8.CrossRef
56.
Zurück zum Zitat Santos SM, da Silva RA, Terra MB, Almeida IA, De Melo LB, Ferraz HB. Balance versus resistance training on postural control in patients with Parkinson’s disease: a randomized controlled trial. Eur J Phys Rehabil Med. 2016;53:173–83.PubMed Santos SM, da Silva RA, Terra MB, Almeida IA, De Melo LB, Ferraz HB. Balance versus resistance training on postural control in patients with Parkinson’s disease: a randomized controlled trial. Eur J Phys Rehabil Med. 2016;53:173–83.PubMed
Metadaten
Titel
Role of sensory feedback in postural control of the patients with diabetic neuropathy
verfasst von
Alireza Reisi
Alireza Hashemi-Oskouei
Mohammed N. Ashtiani
Farid Bahrpeyma
Publikationsdatum
12.05.2023
Verlag
Springer India
Erschienen in
International Journal of Diabetes in Developing Countries / Ausgabe 1/2024
Print ISSN: 0973-3930
Elektronische ISSN: 1998-3832
DOI
https://doi.org/10.1007/s13410-023-01200-9

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