Diabetic Neuropathy and Gait: A Review

Uazman Alam, David R Riley, Ravinder S Jugdey, Shazli Azmi, Satyan Rajbhandari, Kristiaan D'Août, Rayaz A Malik, Uazman Alam, David R Riley, Ravinder S Jugdey, Shazli Azmi, Satyan Rajbhandari, Kristiaan D'Août, Rayaz A Malik

Abstract

Diabetic peripheral neuropathy (DPN) is a major sequela of diabetes mellitus and may have a detrimental effect on the gait of people with this complication. DPN causes a disruption in the body's sensorimotor system and is believed to affect up to 50% of patients with diabetes mellitus, dependent on the duration of diabetes. It has a major effect on morbidity and mortality. The peripheral nervous system controls the complex series of events in gait through somatic and autonomic functions, careful balancing of eccentric and concentric muscle contractions and a reliance on the sensory information received from the plantar surface. In this literature review focussing on kinetics, kinematics and posture during gait in DPN patients, we have identified an intimate link between DPN and abnormalities in gait and demonstrated an increased risk in falls for older patients with diabetes. As such, we have identified a need for further research on the role of gait abnormalities in the development of diabetic foot ulceration and subsequent amputations.

Keywords: Diabetic neuropathy; Gait; Kinematics; Kinetics; Plantar pressure; Posture; Ulceration.

References

    1. Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010;33(10):2285–2293.
    1. Shaw J, Zimmet P. The epidemiology of diabetic neuropathy. Diabetes Rev. 1999;7:245–252.
    1. Skljarevski V, Malik RA. Clinical diagnosis of diabetic neuropathy. In: Veves A, Malik RA, editors. Diabetic neuropathy: clinical management. 2. Totowa: Humana Press; 2007.
    1. Boulton AJ. The diabetic foot: from art to science. The 18th Camillo Golgi lecture. Diabetologia. 2004;47(8):1343–1353.
    1. Timsina LR, Willetts JL, Brennan MJ, Marucci-Wellman H, Lombardi DA, Courtney TK, et al. Circumstances of fall-related injuries by age and gender among community-dwelling adults in the United States. PLoS One. 2017;12(5):e0176561.
    1. Pop-Busui R, Boulton AJM, Feldman EL, Bril V, Freeman R, Malik RA, et al. Diabetic neuropathy: a position statement by the American Diabetes Association. Diabetes Care. 2017;40(1):136–154.
    1. Malik RA. Current and future strategies for the management of diabetic neuropathy. Treat Endocrinol. 2003;2(6):389–400.
    1. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54(6):1615–1625.
    1. Malik RA. The pathology of human diabetic neuropathy. Diabetes. 1997;46:50–53.
    1. Malik RA, Veves A, Walker D, Siddique I, Lye RH, Schady W, et al. Sural nerve fibre pathology in diabetic patients with mild neuropathy: relationship to pain, quantitative sensory testing and peripheral nerve electrophysiology. Acta Neuropathol. 2001;101(4):367–374.
    1. Ward JD, Tesfaye S. Pathogenesis of human diabetic neuropathy. In: Pickup J, Williams G, editors. Textbook of diabetes. Oxford: Blackwell Science; 1997. pp. 49.1–49.19.
    1. Boulton AJM, Vinik AI, Arezzo JC, Bril V, Feldman EL, Freeman R, et al. Diabetic neuropathies: a statement by the American Diabetes Association. Diabetes Care. 2005;28(4):956–962.
    1. Nathan DM. The diabetes control and complications trial/epidemiology of diabetes interventions and complications study at 30 years: overview. Diabetes Care. 2014;37(1):9–16.
    1. Dyck PJ, Kratz KM, Karnes JL, Litchy WJ, Klein R, Pach JM, et al. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology. 1993;43(4):817–824.
    1. Harris M, Eastman R, Cowie C. Symptoms of sensory neuropathy in adults with NIDDM in the US population. Diabetes Care. 1993;16(11):1446–1452.
    1. Kuo AD, Donelan JM. Dynamic principles of gait and their clinical implications. Phys Ther. 2010;90(2):157–174.
    1. Hendrickson J, Patterson KK, Inness EL, McIlroy WE, Mansfield A. Relationship between asymmetry of quiet standing balance control and walking post-stroke. Gait Posture. 2014;39(1):177–181.
    1. Marigold DS, Eng JJ, Tokuno CD, Donnelly CA. Contribution of muscle strength and integration of afferent input to postural instability in persons with stroke. Neurorehabil Neural Repair. 2004;18(4):222–229.
    1. Tyson SF, Hanley M, Chillala J, Selley A, Tallis RC. Balance disability after stroke. Phys Ther. 2006;86(1):30–38.
    1. Alfuth M, Rosenbaum D. Effects of changes in plantar sensory feedback on human gait characteristics: a systematic review. Footwear Sci. 2012;4(1):1–22.
    1. Kavounoudias A, Roll R, Roll JP. The plantar sole is a ‘dynamometric map’ for human balance control. Neuroreport. 1998;9(14):3247–3252.
    1. Winter DA. Biomechanics of normal and pathological gait: implications for understanding human locomotor control. J Mot Behav. 1989;21(4):337–355.
    1. Whittle MW. Clinical gait analysis: a review. Hum Mov Sci. 1996;15(3):369–387.
    1. Aruin AS. Enhancing anticipatory postural adjustments: a novel approach to balance rehabilitation. J Nov Physiother. 2016;6(2):e144.
    1. Takakusaki K. Functional neuroanatomy for posture and gait control. J Mov Disord. 2017;10(1):1–17.
    1. Jones LA. Perception of force and weight: theory and research. Psychol Bull. 1986;100(1):29–42.
    1. Abraira VE, Ginty DD. The sensory neurons of touch. Neuron. 2013;79(4):618–639.
    1. Burgess PR, Perl ER. Cutaneous mechanoreceptors and nociceptors. In: Iggo A, editor. Somatosensory system. Berlin: Springer; 1973. pp. 29–78.
    1. Almurdhi MM, Brown SJ, Bowling FL, Boulton AJM, Jeziorska M, Malik RA, et al. Altered walking strategy and increased unsteadiness in participants with impaired glucose tolerance and type 2 diabetes relates to small-fibre neuropathy but not vitamin D deficiency. Diabet Med. 2017;34(6):839–845.
    1. Petrofsky J, Lee S, Macnider M, Navarro E. Autonomic, endothelial function and the analysis of gait in patients with type 1 and type 2 diabetes. Acta Diabetol. 2005;42(1):7–15.
    1. Sacco IC, Amadio AC. A study of biomechanical parameters in gait analysis and sensitive chronaxie of diabetic neuropathic patients. Clin Biomech (Bristol, Avon) 2000;15(3):196–202.
    1. Menz HB, Lord SR, St George R, Fitzpatrick RC. Walking stability and sensorimotor function in older people with diabetic peripheral neuropathy. Arch Phys Med Rehabil. 2004;85(2):245–252.
    1. Arvanitakis Z, Wilson RS, Schneider JA, Bienias JL, Evans DA, Bennett DA. Diabetes mellitus and progression of rigidity and gait disturbance in older persons. Neurology. 2004;63(6):996–1001.
    1. Vileikyte L, Leventhal H, Gonzalez JS, Peyrot M, Rubin RR, Ulbrecht JS, et al. Diabetic peripheral neuropathy and depressive symptoms. Diabetes Care. 2005;28(10):2378–2383.
    1. Brach JS, Talkowski JB, Strotmeyer ES, Newman AB. Diabetes mellitus and gait dysfunction: possible explanatory factors. Phys Ther. 2008;88(11):1365–1374.
    1. Cavanagh PR, Derr JA, Ulbrecht JS, Maser RE, Orchard TJ. Problems with gait and posture in neuropathic patients with insulin-dependent diabetes mellitus. Diabet Med. 1992;9(5):469–474.
    1. Richardson JK, Ching C, Hurvitz EA. The relationship between electromyographically documented peripheral neuropathy and falls. J Am Geriatr Soc. 1992;40(10):1008–1012.
    1. Blake AJ, Morgan K, Bendall MJ, Dallosso H, Ebrahim SB, Arie TH, et al. Falls by elderly people at home: prevalence and associated factors. Age Ageing. 1988;17(6):365–372.
    1. Brown SJ, Handsaker JC, Bowling FL, Boulton AJ, Reeves ND. Diabetic peripheral neuropathy compromises balance during daily activities. Diabetes Care. 2015;38(6):1116–1122.
    1. Gandevia SC, Burke D. Does the nervous system depend on kinesthetic information to control natural limb movements? In: Cordo P, Harnad S, editors. Movement control. Cambridge: Cambridge University Press; 1994. pp. 12–30.
    1. Ferber R, Osternig LR, Woollacott MH, Wasielewski NJ, Lee JH. Reactive balance adjustments to unexpected perturbations during human walking. Gait Posture. 2002;16(3):238–248.
    1. Lalli P, Chan A, Garven A, Midha N, Chan C, Brady S, et al. Increased gait variability in diabetes mellitus patients with neuropathic pain. J Diabetes Complicat. 2013;27(3):248–254.
    1. Karmakar S, Rashidian H, Chan C, Liu C, Toth C. Investigating the role of neuropathic pain relief in decreasing gait variability in diabetes mellitus patients with neuropathic pain: a randomized, double-blind crossover trial. J Neuroeng Rehabil. 2014;11:125.
    1. Dingwell JB, Cavanagh PR. Increased variability of continuous overground walking in neuropathic patients is only indirectly related to sensory loss. Gait Posture. 2001;14(1):1–10.
    1. Dingwell JB, Cusumano JP, Cavanagh PR, Sternad D. Local dynamic stability versus kinematic variability of continuous overground and treadmill walking. J Biomech Eng. 2000;123(1):27–32.
    1. Studenski S, Perera S, Patel K, et al. Gait speed and survival in older adults. JAMA. 2011;305(1):50–58.
    1. Forsblom CM, Sane T, Groop PH, Totterman KJ, Kallio M, Saloranta C, et al. Risk factors for mortality in type II (non-insulin-dependent) diabetes: evidence of a role for neuropathy and a protective effect of HLA-DR4. Diabetologia. 1998;41(11):1253–1262.
    1. Wang H, Ramakrishnan A, Fletcher S, Prochownik EV. A quantitative, surface plasmon resonance-based approach to evaluating DNA binding by the c-Myc oncoprotein and its disruption by small molecule inhibitors. J Biol Methods. 2015;2(2):e18.
    1. Andersen H. Motor dysfunction in diabetes. Diabetes Metab Res Rev. 2012;28(Suppl 1):89–92.
    1. van Deursen R. Mechanical loading and off-loading of the plantar surface of the diabetic foot. Clin Infect Dis. 2004;01(39 Suppl 2):S87–S91.
    1. Pham H, Armstrong DG, Harvey C, Harkless LB, Giurini JM, Veves A. Screening techniques to identify people at high risk for diabetic foot ulceration: a prospective multicenter trial. Diabetes Care. 2000;23(5):606–611.
    1. Frykberg RG, Lavery LA, Pham H, Harvey C, Harkless L, Veves A. Role of neuropathy and high foot pressures in diabetic foot ulceration. Diabetes Care. 1998;21:1714.
    1. Fernando ME, Crowther RG, Lazzarini PA, Sangla KS, Buttner P, Golledge J. Gait parameters of people with diabetes-related neuropathic plantar foot ulcers. Clin Biomech. 2016;37:98–107.
    1. Hazari A, Maiya AG, Shivashankara KN, Agouris I, Monteiro A, Jadhav R, et al. Kinetics and kinematics of diabetic foot in type 2 diabetes mellitus with and without peripheral neuropathy: a systematic review and meta-analysis. Springerplus. 2016;5(1):1819.
    1. Fernando M, Crowther R, Lazzarini P, Sangla K, Cunningham M, Buttner P, et al. Biomechanical characteristics of peripheral diabetic neuropathy: a systematic review and meta-analysis of findings from the gait cycle, muscle activity and dynamic barefoot plantar pressure. Clin Biomech (Bristol, Avon) 2013;28(8):831–845.
    1. Sacco ICN, Hamamoto AN, Gomes AA, Onodera AN, Hirata RP, Hennig EM. Role of ankle mobility in foot rollover during gait in individuals with diabetic neuropathy. Clin Biomech. 2009;24(8):687–692.
    1. DiLiberto FE, Tome J, Baumhauer JF, Houck J, Nawoczenski DA. Individual metatarsal and forefoot kinematics during walking in people with diabetes mellitus and peripheral neuropathy. Gait Posture. 2015;42(4):435–441.
    1. Raspovic A. Gait characteristics of people with diabetes-related peripheral neuropathy, with and without a history of ulceration. Gait Posture. 2013;38(4):723–728.
    1. Turner DE, Helliwell PS, Burton AK, Woodburn J. The relationship between passive range of motion and range of motion during gait and plantar pressure measurements. Diabet Med. 2007;24(11):1240–1246.
    1. Buzzi UH, Stergiou N, Kurz MJ, Hageman PA, Heidel J. Nonlinear dynamics indicates aging affects variability during gait. Clin Biomech (Bristol, Avon) 2003;18(5):435–443.
    1. Gomes AA, Onodera AN, Otuzi ME, Pripas D, Mezzarane RA, Sacco IC. Electromyography and kinematic changes of gait cycle at different cadences in diabetic neuropathic individuals. Muscle Nerve. 2011;44(2):258–268.
    1. Yavuzer G, Yetkin I, Toruner FB, Koca N, Bolukbasi N. Gait deviations of patients with diabetes mellitus: looking beyond peripheral neuropathy. Eura Medicophys. 2006;42(2):127–133.
    1. Mustapa A, Justine M, Mustafah NM, Manaf H. The effect of diabetic peripheral neuropathy on ground reaction forces during straight walking in stroke survivors. Rehabil Res Pract. 2017;2017:9.
    1. Savelberg HH, Schaper NC, Willems PJ, de Lange TL, Meijer K. Redistribution of joint moments is associated with changed plantar pressure in diabetic polyneuropathy. BMC Musculoskelet Disord. 2009;03(10):16.
    1. Sacco IC, Picon AP, Macedo DO, Butugan MK, Watari R, Sartor CD. Alterations in the lower limb joint moments precede the peripheral neuropathy diagnosis in diabetes patients. Diabetes Technol Ther. 2015;17(6):405–412.
    1. DiLiberto FE, Tome J, Baumhauer JF, Quinn JR, Houck J, Nawoczenski DA. Multi-joint foot kinetics during walking in people with diabetes mellitus and peripheral neuropathy. J Biomech. 2015;48(13):3679–3684.
    1. Rao S, Saltzman CL, Yack HJ. Relationships between segmental foot mobility and plantar loading in individuals with and without diabetes and neuropathy. Gait Posture. 2010;31(2):251–255.
    1. Savelberg HH, Schaper NC, Willems PJ, de Lange TL, Meijer K. Redistribution of joint moments is associated with changed plantar pressure in diabetic polyneuropathy. BMC Musculoskelet Disord. 2009;10(1):16.
    1. Umegaki H. Sarcopenia and diabetes: hyperglycemia is a risk factor for age-associated muscle mass and functional reduction. J Diabetes Investig. 2015;6(6):623–624.
    1. Jang HC. Sarcopenia, frailty, and diabetes in older adults. Diabetes Metab J. 2016;40(3):182–189.
    1. Mueller MJ, Minor SD, Sahrmann SA, Schaaf JA, Strube MJ. Differences in the gait characteristics of patients with diabetes and peripheral neuropathy compared with age-matched controls. Phys Ther. 1994;74:299.
    1. Andersen H, Gadeberg PC, Brock B, Jakobsen J. Muscular atrophy in diabetic neuropathy: a stereological magnetic resonance imaging study. Diabetologia. 1997;40(9):1062–1069.
    1. Andersen H, Gjerstad MD. Atrophy of foot muscles: a measure of diabetic neuropathy. Diabetes Care. 2004;27:2382.
    1. Andersen H, Gadeberg PC, Brock B, Jakobsen J. Muscular atrophy in diabetic neuropathy: a stereological magnetic resonance imaging study. Diabetologia. 1997;40:1062.
    1. Bus SA, Yang QX, Wang JH, Smith MB, Wunderlich R, Cavanagh PR. Intrinsic muscle atrophy and toe deformity in the diabetic neuropathic foot. A magnetic resonance imaging study. Diabetes Care. 2002;25(8):1444–1450.
    1. Andreassen CS, Jakobsen J, Ringgaard S, Ejskjaer N, Andersen H. Accelerated atrophy of lower leg and foot muscles—a follow-up study of long-term diabetic polyneuropathy using magnetic resonance imaging (MRI) Diabetologia. 2009;52(6):1182–1191.
    1. Almurdhi MM, Reeves ND, Bowling FL, Boulton AJ, Jeziorska M, Malik RA. Reduced lower-limb muscle strength and volume in patients with type 2 diabetes in relation to neuropathy, intramuscular fat, and vitamin D levels. Diabetes Care. 2016;39(3):441–447.
    1. Allen MD, Kimpinski K, Doherty TJ, Rice CL. Decreased muscle endurance associated with diabetic neuropathy may be attributed partially to neuromuscular transmission failure. J Appl Physiol. 2015;118(8):1014–1022.
    1. Allen MD, Major B, Kimpinski K, Doherty TJ, Rice CL. Skeletal muscle morphology and contractile function in relation to muscle denervation in diabetic neuropathy. J Appl Physiol. 2014;116(5):545–552.
    1. Fernando ME, Crowther RG, Pappas E, Lazzarini PA, Cunningham M, Sangla KS, et al. Plantar pressure in diabetic peripheral neuropathy patients with active foot ulceration, previous ulceration and no history of ulceration: a meta-analysis of observational studies. PLoS One. 2014;9(6):e99050.
    1. Tang UH, Zugner R, Lisovskaja V, Karlsson J, Hagberg K, Tranberg R. Foot deformities, function in the lower extremities, and plantar pressure in patients with diabetes at high risk to develop foot ulcers. Diabet Foot Ankle. 2015;6:27593.
    1. Lavery LA, Armstrong DG, Vela SA, Quebedeaux TL, Fleischli JG. Practical criteria for screening patients at high risk for diabetic foot ulceration. Arch Intern Med. 1998;158(2):157–162.
    1. Crawford F, Anandan C, Chappell FM, Murray GD, Price JF, Sheikh A, et al. Protocol for a systematic review and individual patient data meta-analysis of prognostic factors of foot ulceration in people with diabetes: the international research collaboration for the prediction of diabetic foot ulcerations (PODUS) BMC Med Res Methodol. 2013;15(13):22.
    1. Fernando M, Crowther R, Lazzarini P, Sangla K, Cunningham M, Buttner P, et al. Biomechanical characteristics of peripheral diabetic neuropathy: a systematic review and meta-analysis of findings from the gait cycle, muscle activity and dynamic barefoot plantar pressure. Clin Biomech. 2013;28(8):831–845.
    1. Akashi PMH, Sacco ICN, Watari R, Hennig E. The effect of diabetic neuropathy and previous foot ulceration in EMG and ground reaction forces during gait. Clin Biomech. 2008;23(5):584–592.
    1. Sacco ICN, Akashi PMH, Hennig EM. A comparison of lower limb EMG and ground reaction forces between barefoot and shod gait in participants with diabetic neuropathic and healthy controls. BMC Musculoskelet Disord. 2010;11:24.
    1. Savelberg HH, Schaper NC, Meijer K. The vertical component of the ground reaction force does not reflect horizontal braking or acceleration per se. Clin Biomech (Bristol, Avon) 2009;24(6):527–528.
    1. Wrobel JS, Najafi B. Diabetic foot biomechanics and gait dysfunction. J Diabetes Sci Technol. 2010;4(4):833–845.
    1. Cavanagh PR, Bus SA. Off-loading the diabetic foot for ulcer prevention and healing. J Vasc Surg. 2010;52(3 Supplement):37S–43S.
    1. Wu SC, Driver VR, Wrobel JS, Armstrong DG. Foot ulcers in the diabetic patient, prevention and treatment. Vasc Health and Risk Manag. 2007;3(1):65–76.
    1. Chantelau E, Onvlee GJ. Charcot foot in diabetes: farewell to the neurotrophic theory. Horm Metab Res. 2006;38(6):361–367.
    1. Rogers LC, Frykberg RG, Armstrong DG, Boulton AJ, Edmonds M, Van GH, et al. The Charcot foot in diabetes. Diabetes Care. 2011;34(9):2123–2129.
    1. Uccioli L, Sinistro A, Almerighi C, Ciaprini C, Cavazza A, Giurato L, et al. Proinflammatory modulation of the surface and cytokine phenotype of monocytes in patients with acute Charcot foot. Diabetes Care. 2010;33(2):350–355.
    1. Wukich DK, Raspovic KM, Hobizal KB, Sadoskas D. Surgical management of Charcot neuroarthropathy of the ankle and hindfoot in patients with diabetes. Diabetes Metab Res Rev. 2016;32(Suppl 1):292–296.
    1. Illgner U, Podella M, Rummler M, Wuhr J, Busch HG, Wetz HH. Reconstructive surgery for Charcot foot. Long-term 5-year outcome. Orthopade. 2009;38(12):1180–1186.
    1. Christensen TM, Bulow J, Simonsen L, Holstein PE, Svendsen OL. Bone mineral density in diabetes mellitus patients with and without a Charcot foot. Clin Physiol Funct Imaging. 2010;30(2):130–134.
    1. Ergen FB, Sanverdi SE, Oznur A. Charcot foot in diabetes and an update on imaging. Diabet Foot Ankle. 2013;4:21884.
    1. Bus SA, Valk GD, van Deursen RW, Armstrong DG, Caravaggi C, Hlaváček P, et al. The effectiveness of footwear and offloading interventions to prevent and heal foot ulcers and reduce plantar pressure in diabetes: a systematic review. Diabetes Metab Res Rev. 2008;24(S1):S162–S180.
    1. Allet L, Armand S, de Bie RA, Golay A, Monnin D, Aminian K, et al. The gait and balance of patients with diabetes can be improved: a randomised controlled trial. Diabetologia. 2010;53(3):458–466.
    1. Francia P, Gulisano M, Anichini R, Seghieri G. Diabetic foot and exercise therapy: step by step the role of rigid posture and biomechanics treatment. Curr Diabetes Rev. 2014;10(2):86–99.
    1. Taveggia G, Villafane JH, Vavassori F, Lecchi C, Borboni A, Negrini S. Multimodal treatment of distal sensorimotor polyneuropathy in diabetic patients: a randomized clinical trial. J Manip Physiol Ther. 2014;37(4):242–252.
    1. Morrison S, Colberg SR, Mariano M, Parson HK, Vinik AI. Balance training reduces falls risk in older individuals with type 2 diabetes. Diabetes Care. 2010;33(4):748–750.
    1. van Netten JJ, Price PE, Lavery LA, Monteiro-Soares M, Rasmussen A, Jubiz Y, et al. Prevention of foot ulcers in the at-risk patient with diabetes: a systematic review. Diabetes Metab Res Rev. 2016;32(Suppl 1):84–98.
    1. Kashefsky H, Marston W. Total contact casting combined with human fibroblast-derived dermal tissue in 15 DFU patients. J Wound Care. 2012;21(5):236.
    1. Ko M, Hughes L, Lewis H. Walking speed and peak plantar pressure distribution during barefoot walking in persons with diabetes. Physiother Res Int. 2012;17(1):29–35.

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner