Advertisement

The relationship of one-leg standing time with peripheral nerve function and clinical neuropathy in patients with type 2 diabetes

  • Kazuhiro Sugimoto
  • Takehiko Hoshino
  • Akira Tamura
  • Toshiro Yamazaki
  • Susumu Suzuki
  • Takuro Shimbo
Original Article
  • 106 Downloads

Abstract

Objective

This study aimed at exploring physical fitness including postural stability in relation to peripheral nerve function and clinical neuropathy in patients with type 2 diabetes across a wide range of ages.

Methods

We analyzed data collected from 139 patients with type 2 diabetes aged between 19 and 81 years, which included the peripheral nerve conduction parameters and coefficient of variation for normal R–R intervals (CVRR) at rest and during deep breathing. The results of neurological examinations to diagnose probable and confirmed diabetic neuropathies based on the minimal criteria proposed by the Toronto diabetic neuropathy expert group and a battery of physical fitness tests including one-leg standing time with eyes open were also assessed. Multiple linear and logistic regressions were used to estimate the relationships of the physical fitness measures with the parameters of peripheral and cardiac autonomic nerve functions and clinical neuropathies, respectively. Receiver operating characteristic curves were generated to depict the relation between sensitivity and specificity of one-leg standing time for probable and confirmed neuropathies.

Results

After adjustment for age and other potential confounders, one-leg standing time correlated with peripheral and cardiac autonomic nerve functions as well as with probable and confirmed neuropathies. The one-leg standing time of 23 s was found to be 66 and 63% sensitive and 81 and 77% specific for diagnosing probable and confirmed neuropathies, respectively.

Conclusions

Short one-leg standing time was associated with peripheral and cardiac autonomic nerve dysfunction and clinical neuropathy in patients with type 2 diabetes, independent of age.

Keywords

Physical fitness Postural stability Nerve conduction Heart rate variability Diabetic neuropathy 

Notes

Acknowledgements

The authors gratefully acknowledge the contribution of Izumi Furukawa, Masanori Chiba and Yukinori Arakawa for data collection and analysis.

Author Contributions

KS contributed to the study design, data collection, analysis, interpretation, writing and approving the manuscript. TH, AT and TY contributed to data collection and final approval of the manuscript. SS and TS contributed to reviewing the draft and final approval of the manuscript.

Compliance with ethical standards

Conflicts of interest

The authors have nothing to declare.

Human rights statement and informed consent

All analyses were conducted with the approval of the Ethical Committee of the Ohta Nishinouchi Hospital (approval no. N/A, approval date: 30 July 2014) and in accordance with the Helsinki Declaration of 1964 and later versions. No informed consent was given because existing data were retrieved and analyzed anonymously.

References

  1. 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;43:817–24.CrossRefPubMedGoogle Scholar
  2. 2.
    Bongaerts BW, Rathmann W, Heier M, Kowall B, Herder C, Stockl D, et al. Older subjects with diabetes and prediabetes are frequently unaware of having distal sensorimotor polyneuropathy: the KORA F4 study. Diabetes Care. 2013;36:1141–6.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Singleton JR, Smith AG, Bromberg MB. Increased prevalence of impaired glucose tolerance in patients with painful sensory neuropathy. Diabetes Care. 2001;24:1448–53.CrossRefPubMedGoogle Scholar
  4. 4.
    Sumner CJ, Sheth S, Griffin JW, Cornblath DR, Polydefkis M. The spectrum of neuropathy in diabetes and impaired glucose tolerance. Neurology. 2003;60:108–11.CrossRefPubMedGoogle Scholar
  5. 5.
    Khoshnoodi MA, Truelove S, Burakgazi A, Hoke A, Mammen AL, Polydefkis M. Longitudinal assessment of small fiber neuropathy: evidence of a non-length-dependent distal axonopathy. JAMA Neurol. 2016;73:684–90.CrossRefPubMedGoogle Scholar
  6. 6.
    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;20:216–23.CrossRefPubMedGoogle Scholar
  7. 7.
    Kluding PM, Pasnoor M, Singh R, Jernigan S, Farmer K, Rucker J, et al. The effect of exercise on neuropathic symptoms, nerve function, and cutaneous innervation in people with diabetic peripheral neuropathy. J Diabetes Complicat. 2012;26:424–9.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Dixit S, Maiya AG, Shastry BA. Effect of aerobic exercise on peripheral nerve functions of population with diabetic peripheral neuropathy in type 2 diabetes: a single blind, parallel group randomized controlled trial. J Diabetes Complicat. 2014;28:332–9.CrossRefPubMedGoogle Scholar
  9. 9.
    Lee DC, Sui X, Church TS, Lee IM, Blair SN. Associations of cardiorespiratory fitness and obesity with risks of impaired fasting glucose and type 2 diabetes in men. Diabetes Care. 2009;32:257–62.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Wei M, Gibbons LW, Mitchell TL, Kampert JB, Lee CD, Blair SN. The association between cardiorespiratory fitness and impaired fasting glucose and type 2 diabetes mellitus in men. Ann Intern Med. 1999;130:89–96.CrossRefPubMedGoogle Scholar
  11. 11.
    Chow LS, Odegaard AO, Bosch TA, Bantle AE, Wang Q, Hughes J, et al. Twenty year fitness trends in young adults and incidence of prediabetes and diabetes: the CARDIA study. Diabetologia. 2016.Google Scholar
  12. 12.
    Resnick HE, Vinik AI, Schwartz AV, Leveille SG, Brancati FL, Balfour J, et al. Independent effects of peripheral nerve dysfunction on lower-extremity physical function in old age: the Women’s Health and Aging Study. Diabetes Care. 2000;23:1642–7.CrossRefPubMedGoogle Scholar
  13. 13.
    Strotmeyer ES, de Rekeneire N, Schwartz AV, Faulkner KA, Resnick HE, Goodpaster BH, et al. The relationship of reduced peripheral nerve function and diabetes with physical performance in older white and black adults: the Health, Aging, and Body Composition (Health ABC) study. Diabetes Care. 2008;31:1767–72.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Fujinuma H, Abe R, Yamazaki T, Seino H, Kikuchi H, Hoshino T, et al. Effect of exercise training on doses of oral agents and insulin. Diabetes Care. 1999;22:1754–5.CrossRefPubMedGoogle Scholar
  15. 15.
    Park SW, Goodpaster BH, Strotmeyer ES, de Rekeneire N, Harris TB, Schwartz AV, et al. Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes. 2006;55:1813–8.CrossRefPubMedGoogle Scholar
  16. 16.
    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;33:2285–93.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Moghtaderi A, Bakhshipour A, Rashidi H. Validation of Michigan neuropathy screening instrument for diabetic peripheral neuropathy. Clin Neurol Neurosurg. 2006;108:477–81.CrossRefPubMedGoogle Scholar
  18. 18.
    Handa N, Matsumoto M, Maeda H, Hougaku H, Ogawa S, Fukunaga R, et al. Ultrasonic evaluation of early carotid atherosclerosis. Stroke. 1990;21:1567–72.CrossRefPubMedGoogle Scholar
  19. 19.
    Ziegler D, Papanas N, Vinik AI, Shaw JE. Epidemiology of polyneuropathy in diabetes and prediabetes. Handb Clin Neurol. 2014;126:3–22.CrossRefPubMedGoogle Scholar
  20. 20.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Vinik A. The approach to the management of the patient with neuropathic pain. J Clin Endocrinol Metab. 2010;95:4802–11.CrossRefPubMedGoogle Scholar
  22. 22.
    Bonnet C, Carello C, Turvey MT. Diabetes and postural stability: review and hypotheses. J Mot Behav. 2009;41:172–90.CrossRefPubMedGoogle Scholar
  23. 23.
    D’Silva LJ, Lin J, Staecker H, Whitney SL, Kluding PM. Impact of diabetic complications on balance and falls: contribution of the vestibular system. Phys Ther. 2016;96:400–9.CrossRefPubMedGoogle Scholar
  24. 24.
    Simoneau GG, Ulbrecht JS, Derr JA, Becker MB, Cavanagh PR. Postural instability in patients with diabetic sensory neuropathy. Diabetes Care. 1994;17:1411–21.CrossRefPubMedGoogle Scholar
  25. 25.
    Hewston P, Deshpande N. Falls and balance impairments in older adults with type 2 diabetes: thinking beyond diabetic peripheral neuropathy. Can J Diabetes. 2016;40:6–9.CrossRefPubMedGoogle Scholar
  26. 26.
    Wearing SC, Hennig EM, Byrne NM, Steele JR, Hills AP. The biomechanics of restricted movement in adult obesity. Obes Rev. 2006;7:13–24.CrossRefPubMedGoogle Scholar
  27. 27.
    Andersen H. Motor dysfunction in diabetes. Diabetes Metab Res Rev. 2012;28(Suppl 1):89–92.CrossRefPubMedGoogle Scholar
  28. 28.
    Hartog LC, Schrijnders D, Landman GWD, Groenier K, Kleefstra N, Bilo HJG, et al. Is orthostatic hypotension related to falling? A meta-analysis of individual patient data of prospective observational studies. Age Ageing. 2017;46:568–75.CrossRefPubMedGoogle Scholar
  29. 29.
    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.CrossRefPubMedGoogle Scholar
  30. 30.
    Verma AK, Garg A, Xu D, Bruner M, Fazel-Rezai R, Blaber AP, et al. Skeletal muscle pump drives control of cardiovascular and postural systems. Sci Rep. 2017;7:45301.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Freeman R, Wieling W, Axelrod FB, Benditt DG, Benarroch E, Biaggioni I, et al. Consensus statement on the definition of orthostatic hypotension, neurally mediated syncope and the postural tachycardia syndrome. Clin Auton Res. 2011;21:69–72.CrossRefPubMedGoogle Scholar
  32. 32.
    Gibbons CH, Schmidt P, Biaggioni I, Frazier-Mills C, Freeman R, Isaacson S, et al. The recommendations of a consensus panel for the screening, diagnosis, and treatment of neurogenic orthostatic hypotension and associated supine hypertension. J Neurol. 2017;264:1567–82.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Smith AG, Russell J, Feldman EL, Goldstein J, Peltier A, Smith S, et al. Lifestyle intervention for pre-diabetic neuropathy. Diabetes Care. 2006;29:1294–9.CrossRefPubMedGoogle Scholar
  34. 34.
    Singleton JR, Marcus RL, Lessard MK, Jackson JE, Smith AG. Supervised exercise improves cutaneous reinnervation capacity in metabolic syndrome patients. Ann Neurol. 2015;77:146–53.CrossRefPubMedGoogle Scholar
  35. 35.
    Bhati P, Shenoy S, Hussain ME. Exercise training and cardiac autonomic function in type 2 diabetes mellitus: a systematic review. Diabetes Metab Syndr. 2017.Google Scholar
  36. 36.
    Morrison S, Colberg SR, Parson HK, Vinik AI. Exercise improves gait, reaction time and postural stability in older adults with type 2 diabetes and neuropathy. J Diabetes Complicat. 2014;28:715–22.CrossRefPubMedGoogle Scholar
  37. 37.
    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;53:458–66.CrossRefPubMedGoogle Scholar
  38. 38.
    Kim B, Feldman EL. Insulin resistance in the nervous system. Trends Endocrinol Metab. 2012;23:133–41.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Japan Diabetes Society 2018

Authors and Affiliations

  • Kazuhiro Sugimoto
    • 1
  • Takehiko Hoshino
    • 2
  • Akira Tamura
    • 1
  • Toshiro Yamazaki
    • 1
  • Susumu Suzuki
    • 1
  • Takuro Shimbo
    • 3
  1. 1.Diabetes CenterOhta Nishinouchi HospitalKoriyamaJapan
  2. 2.Department of Physical Training and ScienceOhta Nishinouchi HospitalKoriyamaJapan
  3. 3.Ohta Nishinouchi HospitalKoriyamaJapan

Personalised recommendations