Introduction: Peripheral neuropathy is one of the major complications of type II diabetes mellitus. Lower limb proprioceptive impairments due to neuropathy can lead to balance disorders in these patients. The present study aimed to investigate postural stability and neuropathic changes following ankle proprioceptive training in type II diabetic patients with moderate neuropathy.
Materials and Methods: The present study was conducted on 24 type II diabetic patients with moderate neuropathy (9 females and 15 males) aged 40-65 years (with a mean age of 57.25 years). The treatment consisted of ankle proprioceptive training by the balance board and rocker for 10 consecutive days. Balance indices, including Overall Stability Index (OSI), Anterior-Posterior Stability Index (APSI), and Medial-Lateral Stability Index (MLSI), were measured with Biodex system before and after the treatment, as well as two weeks after treatment in two conditions: condition1: Eyes open, head straight, without using trunk, pelvis, thigh, and knee constrained orthosis. Condition 2: Eyes closed, head back (hyperextension), with using trunk, pelvis, thigh, and knee constrained orthosis. Plate-based Biodex stability was fixed at levels 6 and 8 for condition1 and level 8 for condition 2. The severity of neuropathy was assessed using Valk and Michigan questionnaires, as well as light touch sensation. The analysis of variance with repeated measure was used to evaluate alterations in the stability of patients. Furthermore, the correlation of neuropathic changes and stability parameters were assessed by the Pearson correlation coefficients.
Results: Significant improvements were observed in OSI in all tests of condition 1 (Biodex Balance System (BBS) at level 8 (P=0.001) and level 6 (P=0.017), as well as test conditions 2 (level 8; P=0.004). After the treatment, at stability level 8, a significant improvement in the mean values of postural sways in the Anterior-Posterior (AP) direction demonstrated that the ankle strategy was improved in the patients. After the treatment, the scores of the Valk (P=0.02) and Michigan (P=0.001) questionnaires were significantly decreased. After two weeks of follow-up, the observed improvement was maintained in the mean values of balance indices (OSI, APSI) and neuropathy due to treatment.
Conclusion: As evidenced by the obtained results, 10 sessions of targeted ankle proprioceptive training improved stability, neuropathy, and light touch sensation of the foot in type II diabetic patients with moderate neuropathy. Foot somatosensory information is one of the most important causes of balance alterations in these patients
- van Dieren S, Beulens JW, van der Schouw YT, Grobbee DE, Neal B. The global burden of diabetes and its complications: an emerging pandemic. Eur J Cardiovasc Prev Rehabil. 2010;17(Suppl 1):S3-8. doi: 10.1097/01.hjr.0000368191.86614.5a. [PubMed: 20489418].
- Shun CT, Chang YC, Wu HP, Hsieh SC, Lin WM, Lin YH, et al. Skin denervation in type 2 diabetes: correlations with diabetic duration and functional impairments. Brain. 2004;127(Pt 7):1593-605. doi: 10.1093/brain/awh180. [PubMed: 15128619].
- 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(3):213-21. doi: 10.1016/s0168-8227(01)00236-4. [PubMed: 1132309].
- Stevens KN, Lang IA, Guralnik JM, Melzer D. Epidemiology of balance and dizziness in a national population: findings from the English Longitudinal Study of Ageing. Age Ageing. 2008;37(3):300-5. doi: 10.1093/ageing/afn019. [PubMed: 18270246].
- Cimbiz A, Cakir O. Evaluation of balance and physical fitness in diabetic neuropathic patients. J Diabetes Complications. 2005;19(3):160-4. doi: 10.1016/j.jdiacomp.2004.06.005. [PubMed: 1586606].
- Gutierrez EM, Helber MD, Dealva D, Ashton-Miller JA, Richardson JK. Mild diabetic neuropathy affects ankle motor function. Clin Biomech (Bristol, Avon). 2001;16(6):522-8. doi: 10.1016/s0268-0033(01)00034-1. [PubMed: 11427295].
- Centers for Disease Control and Prevention. National diabetes fact sheet. Georgia: Centers for Disease Control and Prevention; 2010.
- Francia P, Gulisano M, Anichini R, Seghieri G. Diabetic foot and exercise therapy: step by step the role of rigid posture and biomechanics treatment. Cur Diabetes Rev. 2014;10(2): 86-99. doi: 10.2174/1573399810666140507112536. [PubMed: 24807636].
- Andreassen CS, Jakobsen J, Andersen H. Muscle weakness: a progressive late complication in diabetic distal symmetric polyneuropathy. Diabetes. 2006;55(3):806-12. doi: 10.2337/diabetes.55.03.06.db05-1237. [PubMed: 16505247].
- Fahmy IM, Ramzy GM, Salem NA, Ahmed GM, Mohammed AA. Balance disturbance in patients with diabetic sensory polyneuropathy. Egypt J Neurol Psych Neurosurg. 2014;51(1):21-9.
- Salsabili H, Bahrpeyma F, Forogh B, Rajabali S. Dynamic stability training improves standing balance control in neuropathic patients with type 2 diabetes. J Rehabil Res Dev. 2011;48(7):775-86. doi: 10.1682/jrrd.2010.08.0160. [PubMed: 21938664].
- Dobretosv M, Romanovsky D, Stimers J. Early diabetic neuropathy: triggers and mechanisms. World J Gastroenterol. 2007;13(2):175-91. doi: 10.3748/wjg.v13.i2.175. [PubMed: 17226897].
- Bloem BR, Allum JH, Carpenter MG, Honegger F. Is lower leg proprioception essential for triggering human automatic postural responses? Exp Brain Res. 2000;130(3):375-91. doi: 10.1007/s002219900259. [PubMed: 10706436].
- Moslemi-Haghighi F, Ghafarinejad F, Hemmati L, Saadat Z, Oorangi Z, Torabi S, et al. Evaluation of ankle joint proprioception and balance in patients with type 2 diabetes and healthy subjects. J Rehabil Sci Res. 2015;2(1):17-9. doi: 10.30476/JRSR.2015.41068.
- Horak FB, Nashner LM, Diener HC. Postural strategies associated with somatosensory and vestibular loss. Exp Brain Res. 1990;82(1):167-77. doi: 10.1007/BF00230848. [PubMed: 2257901].
- Akbari M, Jafari H, Moshashaee A, Forugh B. Do diabetic neuropathy patients benefit from balance training? J Rehabil Res Dev. 2012;49(2):333-8. doi: 10.1682/jrrd.2010.10.0197. [PubMed: 22773533].
- Chong RK, Ambrose A, Carzoli J, Hardison L, Jacobson B. Source of improvement in balance control after a training program for ankle proprioception. Percept Mot Skills. 2001;92(1):265-72. doi: 10.2466/pms.2001.92.1.265. [PubMed: 11322594].
- Kruse RL, Lemaster JW, Madsen RW. Fall and balance outcomes after an intervention to promote leg strength, balance, and walking in people with diabetic peripheral neuropathy: “feet first” randomized controlled trial. Phys Ther. 2010;90(11):1568-79. doi: 10.2522/ptj.20090362. [PubMed: 20798179].
- Allet L, Armand S, de Bie RA, Golay A, Monnin D, Aminian K, Staal JB, et al. The gait and balance of patients with diabetes can be improved: a randomised controlled trial. Diabetologia. 2010;53(3):458-66. doi: 10.1007/s00125-009-1592-4. [PubMed: 19921145].
- Najafi B, Bharara M, Talal TK, Armstrong DG. Advances in balance assessment and balance training for diabetes. Diabetes Manage. 2012;2(4):293-308. doi: 10.2217/dmt.12.38.
- El-Wishy A, Elsayed E. Effect of proprioceptive training program on balance in patients with diabetic neuropathy: a controlled randomized study. Bull Facul Physical Ther. 2012;17(2):1-8.
- Corriveau H, Prince F, Hebert R, Raiche M, Tessier D, Maheux P, et al. Evaluation of postural stability in elderly with diabetic neuropathy. Diabetes Care. 2000;23(8):1187–91. doi: 10.2337/diacare.23.8.1187. [PubMed: 10937520].
- Rao S, Riskowski J, Hannan MT. Musculoskeletal conditions of the foot and ankle: assessments and treatment options. Best Pract Res Clin Rheumatol. 2012;26(3):345-68. doi: 10.1016/j.berh.2012.05.009. [PubMed: 22867931].
- Santos AA, Bertato FT, Montebelo MI, Guirro E. Effect of proprioceptive training among diabetic women. Braz J Physical Ther. 2008;12(3):183-7. doi: 10.1590/S1413-35552008000300005.
- Sartor CD, Hasue RH, Cacciari LP, Butugan MK, Watari R, Pássaro AC, et al. Effects of strengthening, stretching and functional training on foot function in patients with diabetic neuropathy: results of a randomized controlled trial. BMC Musculoskelet Dis. 2014;15:137-13. doi: 10.1186/1471-2474-15-137. [PubMed: 24767584].
- Salek S, Bahrpeyma F, Mohajeri-Tehrani MR. Intermittent pneumatic compression therapy improves functional and dynamic balance and neuropathy severity in neuropathic patients with type 2 diabetes. Int J Diabetes Dev Ctries. 2015;35(3):439-48. doi: 10.1007/s13410-015-0378-0.
- Shah A, Parthasarathi D, Sarkar D, Saha CG. A comparative study of body mass index (BMI) in diabetic and nondiabetic in Nepalese population. Kathmandu Univ Med J. 2006;4(1):4-10. [PubMed: 18603858].
- Valk GD, Grootenhuis PA, Bouter LM, Bertelsmann FW. Complaints of neuropathy related to the clinical and neurophysiological assessment of nerve function in patients with diabetes mellitus. Diabetes Res Clin Pract. 1994;26(1):29-34. doi: 10.1016/0168-8227(94)90136-8. [PubMed: 7875047].
- Son J, Ashton-Miller JA, Richardson JK. Do ankle orthoses improve ankle proprioceptive thresholds or unipedal balance in older persons with peripheral neuropathy? Am J Phys Med Rehabil. 2010;89(5):369-75. doi: 10.1097/PHM.0b013e3181d89861. [PubMed: 20407302].
- Kutty NAM, Majida NA. Effects of multisensory training on balance and gait in persons with type 2 diabetes: a randomised controlled trial. Disabil CBR Inclusive Dev. 2013;24(2):79-91. doi: 10.5463/DCID.v24i2.206.
- Moghtaderi A, Bakhshipour A, Rashidi H. Validation of Michigan neuropathy screening instrument for diabetic peripheral neuropathy. Clin Neurol Neurosurg. 2006;108(5):477-81. doi: 10.1016/j.clineuro.2005.08.003. [PubMed: 16150538].
- Timar B, Timar R, Gaiță L, Oancea C, Levai C, Lungeanu D. The impact of diabetic neuropathy on balance and on the risk of falls in patients with type 2 diabetes mellitus: a cross-sectional study. PLoS One. 2016;11(4):e0154654. doi: 10.1371/journal.pone.0154654. [PubMed: 27119372].
- Valk GD, Grootenhuis PA, van Eijk JT, Bouter LM, Bertelsmann FW. Methods for assessing diabetic polyneuropathy: validity and reproducibility of the measurement of sensory symptom severity and nerve function tests. Diabetes Res Clin Pract. 2000;47(2):87-95. doi: 10.1016/s0168-8227(99)00111-4. [PubMed: 10670907].
- Herman WH, Pop-Busui R, Braffett BH, Martin CL, Cleary PA, Albers JW, et al. Use of the Michigan neuropathy screening instrument as a measure of distal symmetrical peripheral neuropathy in Type 1 diabetes: results from the diabetes control and complications trial/epidemiology of diabetes interventions and complications. Diabet Med. 2012;29(7):937-44. doi: 10.1111/j.1464-5491.2012.03644.x. [PubMed: 22417277].
- Armstrong DG, Lavery LA, Vela SA, Quebedeaux TL, Fleischli JG. Choosing a practical screening instrument to identify patients at risk for diabetic foot ulceration. Arch Intern Med. 1998;158(3):289-92. doi: 10.1001/archinte.158.3.289. [PubMed: 9472210].
- Simoneau GG, Ulbrecht JS, Derr JA, Becker MB, Cavanagh PR. Postural instability in patients with diabetic sensory neuropathy. Diabetes Care. 1994;17(12):1411-21. doi: 10.2337/diacare.17.12.1411. [PubMed: 7882810].
- Brandt Th, Krafczyk S, Malsbenden I. Postural imbalance with head extension: improvement by training as a model for ataxia therapy. Ann N Y Acad Sci. 1981;374:636-49. doi: 10.1111/j.1749-6632.1981.tb30907.x. [PubMed: 6978651].
- Colberg SR, Sigal RJ, Yardley JE, Riddell MC, Dunstan DW, Dempsey PC, et al. Physical activity/exercise and diabetes: a position statement the American diabetes association. Diabetes Care. 2016;39(11):2065-79. doi: 10.2337/dc16-1728. [PubMed: 27926890].
- Guney H, Kafa N. Is there any loss of ankle proprioception in diabetic patients without neuropathy. Isokinetics Exer Sci. 2013;21(4):317-23. doi: 10.3233/IES-130503.
- Aruin AS. Enhancing anticipatory postural adjustments: a novel approach to balance rehabilitation. J Nov Physiother. 2016;6(2):e144. doi: 10.4172/2165-7025.1000e144. [PubMed: 27335705].
- Hiroyuki S, Uchiyama Y, Kakurai S. Specific effects of balance and gait exercises on physical function among the frail elderly. Clin Rehabil. 2003;17(5):472-9. doi: 10.1191/0269215503cr638oa. [PubMed: 12952151].
- Ko S, Simonsick E, Deshpande N, Ferrucci L. Sex-specific age associations of ankle proprioception test performance in older adults: results from the Baltimore Longitudinal Study of Aging. Age Ageing. 2015;44(3):485-90. doi: 10.1093/ageing/afv005. [PubMed: 25637144].
- Kiers H, Brumagne S, van Dieën J, van der Wees P, Vanhees L. Ankle proprioception is not targeted by exercises on an unstable surface. Eur J Appl Physiol. 2012;112(4):1577-85. doi: 10.1007/s00421-011-2124-8. [PubMed: 21858665].
- Fortaleza AC, Chagas EF, Ferreira DM, Mantovani AM, Barela JA, Chagas EF, et al. Postural control and functional balance in individuals with diabetic peripheral neuropathy. Rev Bras Cineantropometria Desempenho Humano. 2013;15(3):305-14. doi: 10.5007/1980-0037.2013v15n3p305.
- Brown SJ, Handsaker JC, Bowling FL, Boulton AJ, Reeves ND. Diabetic peripheral neuropathy compromises balance during daily activities. Diabetes Care. 2015;36(6):1116-22. doi: 10.2337/dc14-1982. [PubMed: 25765355].
- Hamada SM, Debrky HM. Monitoring of motor function affection and postural sway in patients with type 2 diabetes mellitus. Egyp J Ear Nose Throat Allied Sci. 2014;15(3):241-5. doi: 10.1016/j.ejenta.2014.05.006.
- Dixit S, Maiya A, Shasthry BA, Kumaran DS, Guddattu V. Postural sway in diabetic peripheral neuropathy among Indian elderly. Indian J Med Res. 2015;142(6):713-20. doi: 10.4103/0971-5916.174562. [PubMed: 26831420].
- Bloem BR, Allum JH, Carpenter MG, Honegger F. Is lower leg proprioception essential for triggering human automatic postural responses? Exp Brain Res. 2000;130(3):375–91. doi: 10.1007/s002219900259. [PubMed: 10706436].
- Simmons RW, Richardson C. The effects of muscle activation on postural stability in diabetes mellitus patients with cutaneous sensory deficit in the foot. Diabetes Res Clin Pract. 2001;53(1):25-32. doi: 10.1016/s0168-8227(01)00231-5. [PubMed: 11378210].
- Kim H. Effect of age and peripheral neuropathy on responses to an unexpected underfoot perturbation during gait. [Doctoral Dissertation]. Michigan: University of Michigan Library; 2012.