Skip to main content
SpringerLink
Log in

An exploratory study of relationship between lower-limb muscle mass and diabetic polyneuropathy in patients with type 2 diabetes

  • Research article
  • Published:
Journal of Diabetes & Metabolic Disorders Aims and scope Submit manuscript

Abstract

Purpose

This exploratory study compared the lower-limb muscle mass (thigh muscle mass [TMM] and lower-leg muscle mass [LLMM]) in type 2 diabetic patients with and without diabetic polyneuropathy (DPN).

Methods

A total of 130 patients with type 2 diabetes, hospitalized for glycemic control, were enrolled in this cross-sectional study. TMM and LLMM were measured using the bioelectrical impedance method. The muscle mass value was normalized by the bodyweight, and the total muscle mass was calculated by combining the muscle mass on the left and right (%TMM and %LLMM). DPN was evaluated according to the Japanese criteria. Anthropometric parameters, blood pressure, laboratory data, exercise habits, medication, related index of diabetes, and diabetic complications were analyzed.

Results

Sixty patients, comprising of 32 males (47.8%) and 28 females (44.4%) with type 2 diabetes (46.2%), had DPN. The %TTM and %LLMM were significantly lower in type 2 diabetic patients with DPN than in those without DPN. Multiple regression analysis identified DPN, age, and hemoglobin A1c (HbA1c) as the determinants of %TMM, and DPN and HbA1c were identified as the determinants of %LLMM in type 2 diabetic patients.

Discussion

The %TMM and %LLMM were significantly decreased in type 2 diabetic patients with DPN. DPN was found to be the strongest determinant of %TMM and %LLMM. Preventing and improving DPN, through active physical therapy, may increase the muscle mass of the lower limbs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. DeFronzo RA. The triumvirate: beta-cell, muscle, liver. a collusion responsible for NIDDM. Diabetes. 1988;37:667–87.

    Article  CAS  Google Scholar 

  2. Gregg EW, Mangione CM, Cauley JA, Thompson TJ, Schwartz AV, Ensrud KE, et al. Diabetes and incidence of functional disability in older women. Diabetes Care. 2002;25:61–7.

    Article  Google Scholar 

  3. Araki A, Nakano T, Oba K, Ito C, Mori S, Ishibashi S, et al. Low well-being, cognitive impairment and visual impairment associated with functional disabilities in elderly Japanese patients with diabetes mellitus. Geriatr Gerontol Int. 2004. https://doi.org/10.1111/j.1447-0594.2003.00108.x.

  4. Park SW, Goodpaster BH, Strotmeyer ES, Kuller LH, Broudeau R, Kammerer C, et al. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care. 2007;30:1507–12.

    Article  Google Scholar 

  5. Schwartz AV, Hillier TA, Sellmeyer DE, Resnick HE, Gregg E, Ensrud KE, et al. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care. 2002;25:1749–54.

    Article  Google Scholar 

  6. Strotmeyer ES, Cauley JA, Schwartz AV, Nevitt MC, Resnick HE, Bauer DC, et al. Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. Arch Intern Med. 2005;165:1612–7.

    Article  Google Scholar 

  7. Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755–63.

    Article  CAS  Google Scholar 

  8. Atkins JL, Whincup PH, Morris RW, Lennon LT, Papacosta O, Wannamethee SG. Sarcopenic obesity and risk of cardiovascular disease and mortality: a population-based cohort study of older men. J Am Geriatr Soc. 2014. https://doi.org/10.1111/jgs.12652.

  9. Tanimoto Y, Watanabe M, Sun W, Sugiura Y, Hayashida I, Kusabiraki T, et al. Sarcopenia and falls in community-dwelling elderly subjects in Japan: defining sarcopenia according to criteria of the European Working Group on Sarcopenia in Older People. Arch Gerontol Geriatr. 2014. https://doi.org/10.1016/j.archger.2014.04.016.

  10. Ryall JG, Schertzer JD, Lynch GS. Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontology. 2008. https://doi.org/10.1007/s10522-008-9131-0.

  11. Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci. 2005;60:324–33.

    Article  Google Scholar 

  12. Hamasaki H. Lower extremity skeletal muscle mass, but not upper extremity skeletal muscle mass, is inversely associated with hospitalization in patients with type 2 diabetes. J Diabetes Res. 2017. https://doi.org/10.1155/2017/2303467.

  13. Ohara N, Minami I, Bouchi R, Izumiyama H, Hashimoto K, Yoshimoto T, et al. Loss of skeletal muscle mass and its predictors in type 2 diabetes patients under a multifaceted treatment approach. Diabetol Int. 2017;8:366–74. https://doi.org/10.1007/s13340-017-0325-z.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Marzetti E, Calvani R, Tosato M, Cesari M, Di Bari M, Cherubini A, et al. Sarcopenia: an overview. Aging Clin Exp Res. 2017. https://doi.org/10.1007/s40520-016-0704-5.

  15. Tajiri Y, Kato T, Nakayama H, Yamada K. Reduction of skeletal muscle, especially in lower limbs, in Japan type 2 diabetic patients with insulin resistance and cardiovascular risk factors. Metab Syndr Relat Disord. 2010;8:137–42.

    Article  CAS  Google Scholar 

  16. Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care. 2009;32:1993–7.

    Article  Google Scholar 

  17. Andersen H, Gadeberg PC, Brock B, Jakobsen J. Muscular atrophy in diabetic neuropathy: a stereological magnetic resonance imaging study. Diabetologia. 1997;40:1062–9.

    Article  CAS  Google Scholar 

  18. 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. https://doi.org/10.2337/dc15-0995.

  19. Tajima N, Noda M, Origasa H, Noto H, Yabe D, Fujita Y, et al. Evidence-based practice guideline for the treatment for diabetes in Japan 2013. Diabetol Int. 2015;6:151–87.

    Article  Google Scholar 

  20. Miyatani M, Kanehisa H, Masuo Y, Ito M, Fukunaga T. Validity of estimating limb muscle volume by bioelectrical impedance. J Appl Physiol. 2001;91:386–94.

    Article  CAS  Google Scholar 

  21. Yasuda H, Sanada M, Kitada K, Terashima T, Kim H, Sakaue Y, et al. Rationale and usefulness of newly devised abbreviated diagnostic criteria and staging for diabetic polyneuropathy. Diabetes Res Clin Pract. 2007;77:S178–83.

    Article  CAS  Google Scholar 

  22. Kataoka H, Miyatake N, Kitayama N, Murao S, Kohi F, Tanaka S. Relationship of toe pinch force to other muscle strength parameters in men with type 2 diabetes. Environ Health Prev Med. 2016;21:179–85. https://doi.org/10.1007/s12199-016-0512-8.

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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.

    Article  Google Scholar 

  24. Allet L, Armand S, Golay A, Monnin D, de Bie RA, de Bruin ED. Gait characteristic of diabetic patients: a systematic review. Diabetes Metab Res Rev. 2008. https://doi.org/10.1002/dmrr.809.

  25. Botelho MC, Conde MG, Rebelo Braz NM. Functional aspects in ageing adults with diabetic neuropathy. A Review. Curr Diabetes Rev. 2015;12:114–9.

    Article  Google Scholar 

  26. Andersen H, Nielsen S, Mogensen CE, Jakobsen J. Muscle strength in type 2 diabetes. Diabetes. 2004. https://doi.org/10.2337/diabetes.53.6.1543.

  27. Hirata Y, Nomura K, Senga Y, Okada Y, Kobayashi K, Okamoto S, et al. Hyperglycemia induces skeletal muscle atrophy via a WWP1/KLF15 axis. JCI Insight. 2019. https://doi.org/10.1172/jci.insight.124952.

  28. Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care. 2009. https://doi.org/10.2337/dc09-0264.

  29. Kim TN, Park MS, Yang SJ, Yoo HJ, Kang HJ, Song W, et al. Prevalance and determinant factors or sarcopenia in patients with type 2 diabetes: the Korean Sarcopenic Obesity Study (KSOS). Diabetes Care. 2010. https://doi.org/10.2337/dc09-2310.

  30. Anbalagan VP, Venkataraman V, Pradeepa R, Deepa M, Anjana RM, Mohan V. The prevalence of presarcopenia in Asian Indian individuals with and without type 2 diabetes. Diabetes Technol Ther. 2013. https://doi.org/10.1089/dia.2013.0068.

  31. Lee SJ, Auyeung TW, Leung J, Kwok T, Leung PC, Woo J. The effect of diabetes mellitus on age-associated lean mass loss in 3153 older adults. Diabet Med. 2010. https://doi.org/10.1111/j.1464-5491.

  32. 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.

    Article  CAS  Google Scholar 

  33. Dunstan DW, Daly RM, Owen N, Jolley D, De Courten M, Shaw J, et al. High-intensity resistance training improves glycemic control in older patients with type 2 diabetes. Diabetes Care. 2002;25:1729–36.

    Article  Google Scholar 

  34. Mavros Y, Kay S, Anderberg KA, Baker MK, Wang Y, Zhao R, et al. Changes in insulin resistance and HbA1c are related to exercise mediated changes in body composition in older adults with type 2 diabetes: interim outcomes from the GREAT2DO trial. Diabetes Care. 2013. https://doi.org/10.2337/dc12-2196.

  35. Castaneda C, Layne JE, Munoz-Orians L, Gordon PL, Walsmith J, Foldvari M, et al. A randomized control trial of resistance exercise training to improve glycemic control in older adults with type 2 diabetes. Diabetes Care. 2002;25:2335–41.

    Article  Google Scholar 

  36. Schwingshackl L, Missbach B, Dias S, König J, Hoffmann G. Impact of different training modalities on glycemic control and blood lipids in patients with type 2 diabetes: a systematic review and network meta-analysis. Diabetologia. 2014. https://doi.org/10.1007/s00125-014-3303-z.

  37. 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.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physical Therapy, Okayama Institute for Medical and Technical Sciences, 3-2-18, Daiku, Kitaku, Okayama-city, Okayama, 700-0913, Japan

    Hiroaki Kataoka

  2. Rehabilitation Center, KKR Takamatsu Hospital, Takamatsu, Kagawa, Japan

    Hiroaki Kataoka & Naomi Kitayama

  3. Department of Hygiene, Faculty of Medicine, Kagawa University, Takamatsu, Kagawa, Japan

    Hiroaki Kataoka & Nobuyuki Miyatake

  4. Department of Diabetes and Endocrinology, KKR Takamatsu Hospital, Takamatsu, Kagawa, Japan

    Satoshi Murao

  5. Department of Physical Therapy, Faculty of Health and Welfare, Prefectural University of Hiroshima, Hiroshima, Japan

    Satoshi Tanaka

Authors
  1. Hiroaki Kataoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nobuyuki Miyatake
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naomi Kitayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Satoshi Murao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Satoshi Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroaki Kataoka.

Ethics declarations

Declaration of interest

All authors declare no financial support or relationships that could pose a conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kataoka, H., Miyatake, N., Kitayama, N. et al. An exploratory study of relationship between lower-limb muscle mass and diabetic polyneuropathy in patients with type 2 diabetes. J Diabetes Metab Disord 19, 281–287 (2020). https://doi.org/10.1007/s40200-020-00505-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40200-020-00505-4

Keywords

Search

Navigation