Foot-ankle therapeutic exercise program can improve gait speed in people with diabetic neuropathy: a randomized controlled trial

Renan L Monteiro, Jane S S P Ferreira, Érica Q Silva, Ronaldo H Cruvinel-Júnior, Jady L Veríssimo, Sicco A Bus, Isabel C N Sacco, Renan L Monteiro, Jane S S P Ferreira, Érica Q Silva, Ronaldo H Cruvinel-Júnior, Jady L Veríssimo, Sicco A Bus, Isabel C N Sacco

Abstract

This study sought to determine whether a foot-ankle therapeutic exercise program can improve daily physical activity (i.e. number of steps) and fast and self-selected gait speed in people with diabetic peripheral neuropathy (DPN). In this single-blind randomized controlled trial and intention-to-treat analysis, 78 volunteers with DPN were allocated into a control group, which received usual care, and an intervention group (IG), which received usual care plus a 12-week foot-ankle exercise program. The adherence at 12 weeks rate in the IG was 92.3% (36 participants) and the dropout was 5.1% in the control group (2 participants). The number of steps and self-selected gait speed did not change significantly in either group (p > 0.05), although a 1,365-step difference between groups were observed at 1-year followup. The 12-week foot-ankle therapeutic exercises improved significantly fast-gait speed (primary outcome) (p = 0.020), ankle range of motion (p = 0.048), and vibration perception (secondary outcomes) (p = 0.030), compared with usual-care at 12 weeks. At 24 weeks, the IG showed better quality of life than controls (p = 0.048). At 1-year, fast-gait speed and vibration perception remained higher in the IG versus controls. Overall, the program may be a complementary treatment strategy for improving musculoskeletal and functional deficits related to DPN.Trial registration ClinicalTrials.gov NCT02790931 (06/06/2016).

Conflict of interest statement

The authors declare no competing interests.

© 2022. The Author(s).

Figures

Figure 1
Figure 1
Flowchart of recruitment, assessment, and follow-up process.
Figure 2
Figure 2
Different between intervention group and control group on fast gait speed, quality of life, ankle range of motion and vibration outcomes.

References

    1. Kluding PM, Bareiss SK, Hastings M, Marcus RL, Sinacore DR, Mueller MJ, et al. Physical training and activity in people with diabetic peripheral neuropathy: Paradigm shift. Phys. Ther. 2017;97:31–43.
    1. van Sloten TT, Savelberg HHCM, Duimel-Peeters IGP, Meijer K, Henry RMA, Stehouwer CDA, et al. Peripheral neuropathy, decreased muscle strength and obesity are strongly associated with walking in persons with type 2 diabetes without manifest mobility limitations. Diabetes Res. Clin. Pract. 2011;91:32–39. doi: 10.1016/j.diabres.2010.09.030.
    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;74:299–308. doi: 10.1093/ptj/74.4.299.
    1. Tuttle LJ, Sinacore DR, Cade WT, Mueller MJ. Lower physical activity is associated with higher intermuscular adipose tissue in people with type 2 diabetes and peripheral neuropathy. Phys. Ther. 2011;91:923–930. doi: 10.2522/ptj.20100329.
    1. van Schie CHM. Neuropathy: Mobility and quality of life. Diabetes/Metab. Res. Rev. 2008 doi: 10.1002/dmrr.856.
    1. Rao S, Saltzman C, Yack HJ. Ankle ROM and stiffness measured at rest and during gait in individuals with and without diabetic sensory neuropathy. Gait Posture. 2006;24:295–301. doi: 10.1016/j.gaitpost.2005.10.004.
    1. Cieza A, Causey K, Kamenov K, Hanson SW, Chatterji S, Vos T. Global estimates of the need for rehabilitation based on the Global Burden of Disease study 2019: A systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2020;396:2006–2017. doi: 10.1016/S0140-6736(20)32340-0.
    1. van Netten JJ, Sacco ICN, Lavery LA, Monteiro-Soares M, Rasmussen A, Raspovic A, et al. Treatment of modifiable risk factors for foot ulceration in persons with diabetes: A systematic review. Diabetes Metab. Res. Rev. 2020;36:1–19. doi: 10.1002/dmrr.3271.
    1. Orkin AM, Gill PJ, Ghersi D, Campbell L, Sugarman J, Emsley R, et al. Guidelines for reporting trial protocols and completed trials modified due to the COVID-19 pandemic and other extenuating circumstances the CONSERVE 2021 statement supplemental content clinical review & education JAMA|special communication. JAMA. 2021;326:257–265. doi: 10.1001/jama.2021.9941.
    1. Gutierrez EM, Helber MD, Dealva D, Ashton-Miller JA, Richardson JK. Mild diabetic neuropathy affects ankle motor function. Clin. Biomech. 2001;16:522–528. doi: 10.1016/S0268-0033(01)00034-1.
    1. Ferreira JSSP, Panighel JP, Silva ÉQ, Monteiro RL, Cruvinel Júnior RH, Sacco ICN. Foot function and strength of patients with diabetes grouped by ulcer risk classification (IWGDF) Diabetol. Metab. Syndrome. 2019 doi: 10.1186/s13098-019-0487-x.
    1. Henderson AD, Johnson AW, Rasmussen LG, Peine WP, Symons SH, Scoresby KA, et al. Early-stage diabetic neuropathy reduces foot strength and intrinsic but not extrinsic foot muscle size. J. Diabetes Res. 2020 doi: 10.1155/2020/9536362.
    1. Buchner DM, Larson EB, Wagner EH, Koepsell TD, de Lateur BJ. Evidence for a non-linear relationship between leg strength and gait speed. Age Ageing. 1996;25:386–391. doi: 10.1093/ageing/25.5.386.
    1. Hausdorff J, Rios D, Edelberg H. Gait variability and fall risk in community-living older adults: A 1-year prospective study. Arch. Phys. Med. Rehabil. 2001;82:1050–1056. doi: 10.1053/APMR.2001.24893.
    1. Studenski S, Perera S, Patel K, Rosano C, Faulkner K, Inzitari M, et al. Gait speed and survival in older adults. JAMA. 2011;305:50–58. doi: 10.1001/jama.2010.1923.
    1. White DK, Neogi T, Nevitt MC, Peloquin CE, Zhu Y, Boudreau RM, et al. Trajectories of gait speed predict mortality in well-functioning older adults: The health, aging and body composition study. J. Gerontol. A Biol. Sci. Med. Sci. 2013;68:456–464. doi: 10.1093/gerona/gls197.
    1. Orlando G, Reeves ND, Boulton AJM, Ireland A, Federici G, Federici A, et al. Sedentary behaviour is an independent predictor of diabetic foot ulcer development: An 8-year prospective study. Diabetes Res. Clin. Practice. 2021 doi: 10.1016/j.diabres.2021.108877.
    1. Taveggia G, Villafañe JH, Vavassori F, Lecchi C, Borboni A, Negrini S. Multimodal treatment of distal sensorimotor polyneuropathy in diabetic patients: A randomized clinical trial. J. Manipulative Physiol. Ther. 2014;37:242–252. doi: 10.1016/j.jmpt.2013.09.007.
    1. Hardy SE, Perera S, Roumani YF, Chandler JM, Studenski SA. Improvement in usual gait speed predicts better survival in older adults. J. Am. Geriatr. Soc. 2007;55:1727–1734. doi: 10.1111/j.1532-5415.2007.01413.x.
    1. Coleman CI, Sobieraj DM, Marinucci LN. Minimally important clinical difference of the Timed 25-Foot Walk Test: Results from a randomized controlled trial in patients with multiple sclerosis. Curr. Med. Res. Opin. 2012;28:49–56. doi: 10.1185/03007995.2011.639752.
    1. Melese H, Alamer A, Temesgen MH, Kahsay G. Effectiveness of exercise therapy on gait function in diabetic peripheral neuropathy patients: A systematic review of randomized controlled trials. Diabetes Metab. Syndrome Obesity Targets Ther. 2020;13:2753–2764. doi: 10.2147/DMSO.S261175.
    1. Stensvold D, Viken H, Steinshamn SL, Dalen H, Støylen A, Loennechen JP, et al. Effect of exercise training for five years on all cause mortality in older adults-the Generation 100 study: Randomised controlled trial. BMJ. 2020 doi: 10.1136/bmj.m3485.
    1. Lopez JPR, Sabag A, Juan MM, Rezende LFM, Pastor-Valero M. Do vigorous-intensity and moderate-intensity physical activities reduce mortality to the same extent? A systematic review and meta-analysis. BMJ Open Sport Exercise Med. 2020 doi: 10.1136/BMJSEM-2020-000775.
    1. Tryon WW. Activity Measurement in Psychology and Medicine. Springer Science & Business Media; 1991.
    1. 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. Disord. 2014;15:1–13. doi: 10.1186/1471-2474-15-137.
    1. Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, et al. Exercise and type 2 diabetes: The American College of Sports Medicine and the American Diabetes Association: Joint position statement. Diabetes Care. 2010;3:3. doi: 10.2337/dc10-9990.
    1. Shephard RJ. Limits to the measurement of habitual physical activity by questionnaires. Br. J. Sports Med. 2003;37:197–206. doi: 10.1136/bjsm.37.3.197.
    1. Prince SA, Adamo KB, Hamel ME, Hardt J, Connor Gorber S, Tremblay M. A comparison of direct versus self-report measures for assessing physical activity in adults: A systematic review. Int. J. Behav. Nutr. Phys. Activity. 2008 doi: 10.1186/1479-5868-5-56.
    1. Bus SA, Lavery LA, Monteiro-Soares M, Rasmussen A, Raspovic A, Sacco ICN, et al. Guidelines on the prevention of foot ulcers in persons with diabetes (IWGDF 2019 update) Diabetes/Metab. Res. Rev. 2020 doi: 10.1002/dmrr.3269.
    1. Grewal GS, Schwenk M, Lee-Eng J, Parvaneh S, Bharara M, Menzies RA, et al. Sensor-based interactive balance training with visual joint movement feedback for improving postural stability in diabetics with peripheral neuropathy: A randomized controlled trial. Gerontology. 2015;61:567–574. doi: 10.1159/000371846.
    1. Mueller MJ, Tuttle LJ, Lemaster JW, Strube MJ, McGill JB, Hastings MK, et al. Weight-bearing versus nonweight-bearing exercise for persons with diabetes and peripheral neuropathy: A randomized controlled trial. Arch. Phys. Med. Rehabil. 2013;94:829–838. doi: 10.1016/j.apmr.2012.12.015.
    1. Francia P, Anichini R, de Bellis A, Seghieri G, Lazzeri R, Paternostro F, et al. Diabetic foot prevention: The role of exercise therapy in the treatment of limited joint mobility, muscle weakness and reduced gait speed. Ital. J. Anat. Embryol. 2015;120:21–32. doi: 10.13128/IJAE-16470.
    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;53:458–466. doi: 10.1007/s00125-009-1592-4.
    1. 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;90:1568–1579. doi: 10.2522/ptj.20090362.
    1. Lázaro-Martínez J, Aragón-Sánchez F, Beneit-Montesinos J, González-Jurado M, Morales EG, Hernández DM. Foot biomechanics in patients with diabetes mellitus: Doubts regarding the relationship between neuropathy, foot motion, and deformities. J. Am. Podiatr. Med. Assoc. 2011;101:208–214. doi: 10.7547/1010208.
    1. Monteiro-Soares M, Boyko EJ, Ribeiro J, Ribeiro I, Dinis-Ribeiro M. Predictive factors for diabetic foot ulceration: A systematic review. Diabetes Metab. Res. Rev. 2012;28:574–600. doi: 10.1002/dmrr.2319.
    1. Cerrahoglu L, Koşan U, Sirin TC, Ulusoy A. Range of motion and plantar pressure evaluation for the effects of self-care foot exercises on diabetic patients with and without neuropathy. J. Am. Podiatr. Med. Assoc. 2016;106:189–200. doi: 10.7547/14-095.
    1. Kanchanasamut W, Pensri P. Effects of weight-bearing exercise on a mini-trampoline on foot mobility, plantar pressure and sensation of diabetic neuropathic feet; a preliminary study. Diabetic Foot Ankle. 2017;8:1–10. doi: 10.1080/2000625X.2017.1287239.
    1. Dijs H, Roofthooft J, Driessens M, de Bock P, Jacobs C, van Acker K. Effect of physical therapy on limited joint mobility in the diabetic foot. A pilot study. J. Am. Podiatr. Med. Assoc. 2000;90:126–132. doi: 10.7547/87507315-90-3-126.
    1. Chatchawan UA, Eungpinichpong WB, de Plandee P, Yamauchi J, Chatchawan U. Effects of Thai foot massage on balance performance in diabetic patients with peripheral neuropathy: A randomized parallel-controlled trial HUMAN STUDY. Med. Sci. Monit. Basic Res. 2015;21:68–75. doi: 10.12659/MSMBR.894163.
    1. Zippenfennig C, Drechsel TJ, Monteiro RL, Sacco ICN, Milani TL. The mechanoreceptor’s role in plantar skin changes in individuals with diabetes mellitus. J. Clin. Med. 2021;10:2537. doi: 10.3390/jcm10122537.
    1. Cooper MA, Kluding PM, Wright DE. Emerging relationships between exercise, sensory nerves, and neuropathic pain. Front. Neurosci. 2016 doi: 10.3389/fnins.2016.00372.
    1. Bobinski F, Martins DF, Bratti T, Mazzardo-Martins L, Winkelmann-Duarte EC, Guglielmo LGA, et al. Neuroprotective and neuroregenerative effects of low-intensity aerobic exercise on sciatic nerve crush injury in mice. Neuroscience. 2011;194:337–348. doi: 10.1016/j.neuroscience.2011.07.075.
    1. Balducci S, Iacobellis G, Parisi L, di Biase N, Calandriello E, Leonetti F, et al. Exercise training can modify the natural history of diabetic peripheral neuropathy. J. Diabetes Complicat. 2006;20:216–223. doi: 10.1016/j.jdiacomp.2005.07.005.
    1. Cai H, Li G, Zhang P, Xu D, Chen L. Effect of exercise on the quality of life in type 2 diabetes mellitus: A systematic review. Qual. Life Res. 2016;26:515–530. doi: 10.1007/S11136-016-1481-5.
    1. Ahn S, Song R. Effects of tai chi exercise on glucose control, neuropathy scores, balance, and quality of life in patients with type 2 diabetes and neuropathy. J. Altern. Complement. Med. 2012;18:1172–1178. doi: 10.1089/acm.2011.0690.
    1. Ausili D, Bulgheroni M, Ballatore P, Specchia C, Ajdini A, Bezze S, et al. Self-care, quality of life and clinical outcomes of type 2 diabetes patients: An observational cross-sectional study. Acta Diabetol. 2017;54:1001–1008. doi: 10.1007/S00592-017-1035-5.
    1. Testa M, Rossettini G. Enhance placebo, avoid nocebo: How contextual factors affect physiotherapy outcomes. Man. Ther. 2016;24:65–74. doi: 10.1016/j.math.2016.04.006.
    1. Monteiro RL, Ferreira JSSP, Silva ÉQ, Donini A, Cruvinel-Júnior RH, Verissímo JL, et al. Feasibility and preliminary efficacy of a foot-ankle exercise program aiming to improve foot-ankle functionality and gait biomechanics in people with diabetic neuropathy: A randomized controlled trial. Sensors (Switzerland) 2020;20:1–18. doi: 10.3390/s20185129.
    1. Monteiro RL, Sartor CD, Ferreira JSSP, Dantas MGB, Bus SA, Sacco ICN. Protocol for evaluating the effects of a foot-ankle therapeutic exercise program on daily activity, foot-ankle functionality, and biomechanics in people with diabetic polyneuropathy: A randomized controlled trial. BMC Musculoskelet. Disord. 2018;19:1–12. doi: 10.1186/s12891-018-2323-0.
    1. Faul F, Erdfelder E, Lang A-G, Buchner A. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods. 2007;39:175–191. doi: 10.3758/BF03193146.
    1. Eggenberger P, Theill N, Holenstein S, Schumacher V, de Bruin ED. Multicomponent physical exercise with simultaneous cognitive training to enhance dual-task walking of older adults: A secondary analysis of a 6-month randomized controlled trial with I-year follow-up. Clin. Interv. Aging. 2015;10:1711–1732. doi: 10.2147/CIA.S91997.
    1. Bohannon R, Glenney S. Minimal clinically important difference for change in comfortable gait speed of adults with pathology: A systematic review. J. Eval. Clin. Pract. 2014;20:295–300. doi: 10.1111/JEP.12158.
    1. Watari R, Sartor CD, Picon AP, Butugan MK, Amorim CF, Ortega NR, et al. Effect of diabetic neuropathy severity classified by a fuzzy model in muscle dynamics during gait. J. Neuroeng. Rehabil. 2014 doi: 10.1186/1743-0003-11-11.
    1. Fragala MS, Cadore EL, Dorgo S, Izquierdo M, Kraemer WJ, Peterson MD, et al. Resistance training for older adults: Position statement from the national strength and conditioning association. J. Strength Cond. Res. 2019;33:2019–2052. doi: 10.1519/JSC.0000000000003230.
    1. Boulton AJM, Armstrong DG, Albert SF, Frykberg RG, Hellman R, Kirkman MS, et al. Comprehensive foot examination and risk assessment. Diabetes Care. 2008;31:1679–1685. doi: 10.2337/dc08-9021.
    1. Jeng C, Michelson J, Mizel M. Sensory thresholds of normal human feet. Foot Ankle Int. 2000;21:501–504. doi: 10.1177/107110070002100609.
    1. Perkins BA, Olaleye D, Zinman B, Bril V. Simple screening tests for peripheral neuropathy in the diabetes clinic. Diabetes Care. 2001;24:250–256. doi: 10.2337/diacare.24.2.250.
    1. Mickle KJ, Caputi P, Potter JM, Steele JR. Efficacy of a progressive resistance exercise program to increase toe flexor strength in older people. Clin. Biomech. 2016;40:14–19. doi: 10.1016/j.clinbiomech.2016.10.005.
    1. Sartor CD, Oliveira MD, Campos V, Ferreira JSSP, Sacco ICN. Cross-cultural adaptation and measurement properties of the Brazilian Version of the Michigan Neuropathy Screening Instrument. Braz. J. Phys. Ther. 2018;22:222–230. doi: 10.1016/j.bjpt.2017.10.004.
    1. Santos M, Cintra MA, Monteiro AL, Santos B, Gusmão-Filho F, Andrade MV, et al. Brazilian valuation of EQ-5D-3L health states: Results from a saturation study. Med. Decis. Making. 2016;36:253–263. doi: 10.1177/0272989X15613521.
    1. Ferreira AFB, Laurindo IMM, Rodrigues PT, Ferraz MB, Kowalski SC, Tanaka C. Brazilian version of the foot health status questionnaire (FHSQ-BR): Cross-cultural adaptation and evaluation of measurement properties. Clinics. 2008;63:595–600. doi: 10.1590/S1807-59322008000500005.
    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;32:84–98. doi: 10.1002/DMRR.2701.

Source: PubMed

3
Subscribe