The impact of diabetic polyneuropathy on toe grip strength in patients with type 2 diabetes mellitus: a cross-sectional study

1. 2. 3. Conclusion

The results of this study suggest that age, T2DM, and DPN

should be considered factors related to TGS in clinical practice. These factors should be considered when providing fall

prevention, foot care, and rehabilitation for patients with

T2DM.

Acknowledgements The authors thank the study participants, physicians of the Department of Diabetes, Metabolism and Endocrinology,

Kawasaki Medical School, Dr. Hiroshi Osaka, and Dr. Hiromi Matsumoto of Kawasaki University of Health and Welfare, and the physiotherapists of Kawasaki Medical School Hospital.

Author contribution All authors contributed to the study’s conception

and design. YK contributed to analysis and drafted the manuscript.

YM conceptualized and designed the study protocol and developed the

manuscript. SN recruited participants and participated in data analysis

and interpretation. ST, KK, and SM critically reviewed the manuscript

for intellectual content. KH contributed to data acquisition and interpretation of data and revised the manuscript. All authors read and approved the final manuscript before submission.

Funding The authors declare that they have no financial relationship

relevant to this article to disclose.

Open access funding provided by Kobe University.

4. 5. 6. 7. 8. 9. 10. 11. 12. Declarations

Ethics approval and consent to participate This study was approved

by the ethics review board of Kawasaki Medical School. All participants provided written, informed consent to participate in the study.

Competing interests The authors declare that they have no competing

interests.

Open Access This article is licensed under a Creative Commons

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use, you will need to obtain permission directly from the copyright

13

13. 14. 15. 16. 17. Magliano D, Boyko EJ. IDF diabetes atlas. 10th edition. Brussels:

International Diabetes Federation; 2021.

Pijpers E, Ferreira I, de Jongh RT, Deeg DJ, Lips P, Stehouwer

CDA, et al. Older individuals with diabetes have an increased

risk of recurrent falls: analysis of potential mediating factors:

the Longitudinal Ageing Study Amsterdam. Age Ageing. 2012

May;41(3):358–65.

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 Apr 27;11(4):e0154654.

Moreland JD, Richardson JA, Goldsmith CH, Clase CM. Muscle

weakness and falls in older adults: a systematic review and Metaanalysis: MUSCLE WEAKNESS AND FALLS IN OLDER

ADULTS. Journal of the american Geriatrics Society. 2004

Jul;52(7):1121–9.

Nomura T, Ishiguro T, Ohira M, Oka H, Ikeda Y. Isometric knee

extension force in japanese type 2 diabetic patients without apparent diabetic polyneuropathy: data from the Multicenter Survey of

the isometric lower extremity strength in type 2 diabetes study.

SAGE Open Medicine. 2019 Jan;7:1–8.

Nomura T, Ishiguro T, Ohira M, Ikeda Y. Diabetic polyneuropathy

is a risk factor for decline of lower extremity strength in patients

with type 2 diabetes. J Diabetes Investig 2018 Jan;9(1):186–92.

Andersen H. Motor dysfunction in diabetes: motor dysfunction in

diabetes. Diabetes Metab Res Rev. 2012 Feb;28:89–92.

Andersen H, Nielsen S, Mogensen CE, Jakobsen J. Muscle

strength in type 2 diabetes. Diabetes. 2004 Jun;1(6):1543–8.

Andersen H, Gjerstad MD, Jakobsen J. Atrophy of Foot muscles.

Diabetes Care. 2004 Oct;27(1):2382–5.

Endo M, Ashton-Miller JA, Alexander NB. Effects of Age and

Gender on Toe Flexor Muscle Strength. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2002

Jun 1;57(6):M392–7.

Hughes J, Clark P, Klenerman L. The importance of the toes in

walking. J Bone Joint Surg Br volume. 1990 Mar;72–B(2):245–51.

Menz HB, Morris ME, Lord SR. Foot and Ankle Risk Factors

for Falls in Older People: A Prospective Study. The Journals of

Gerontology Series A: Biological Sciences and Medical Sciences.

2006 Aug 1;61(8):866–70.

Healy A, Naemi R, Sundar L, Chatzistergos P, Ramachandran A,

Chockalingam N. Hallux plantar flexor strength in people with

diabetic neuropathy: validation of a simple clinical test. Diabetes

Res Clin Pract. 2018 Oct;144:1–9.

Kataoka H, Miyatake N, Kitayama N, Murao S, Tanaka S. Toe

pinch force in male type 2 diabetes Mellitus Patients. Acta Med

Okayama. 2017;71(2):7.

Chatzistergos PE, Healy A, Balasubramanian G, Sundar L, Ramachandran A, Chockalingam N. Reliability and validity of an

enhanced paper grip test; a simple clinical test for assessing lower

limb strength. Gait Posture. 2020 Sep;81:120–5.

Tesfaye S, Boulton AJM, 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 Oct 1;33(10):2285–93.

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 Sep;77(3):178–83.

Journal of Diabetes & Metabolic Disorders (2023) 22:1391–1397

18. Dyck PJ, Overland CJ, Low PA, Litchy WJ, Davies JL, Dyck

PJB, et al. Signs and symptoms versus nerve conduction studies

to diagnose diabetic sensorimotor polyneuropathy: cl vs. NPhys

trial: cl vs. NPhys trial. Muscle Nerve. 2010 Aug;42(2):157–64.

19. Kamiya H, Shibata Y, Himeno T, Tani H, Nakayama T, Murotani

K, et al. Point-of‐care nerve conduction device predicts the severity of diabetic polyneuropathy: a quantitative, but easy‐to‐use,

prediction model. J Diabetes Investig. 2021 Apr;12(4):583–91.

20. Uritani D, Fukumoto T, Matsumoto D. Intrarater and Interrater Reliabilitiesfor a toe grip Dynamometer. J Phys Ther Sci.

2012;24(8):639–43.

21. Uritani D, Fukumoto T, Matsumoto D, Shima M. Reference values

for toe grip strength among japanese adults aged 20 to 79 years: a

cross-sectional study. J Foot Ankle Res. 2014 Dec;7(1):28.

22. Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah

KS, et al. Sarcopenia in Asia: Consensus Report of the asian

Working Group for Sarcopenia. J Am Med Dir Assoc. 2014

Feb;15(2):95–101.

23. Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima

K, et al. Asian Working Group for Sarcopenia: 2019 Consensus

Update on Sarcopenia diagnosis and treatment. J Am Med Dir

Assoc. 2020 Mar;21(3):300–307e2.

24. Schaper NC, Netten JJ, Apelqvist J, Bus SA, Hinchliffe RJ, Lipsky BA, et al. Practical guidelines on the prevention and management of diabetic foot disease (IWGDF 2019 update). Diabetes

Metab Res Rev. 2020 Mar;36:1.

25. Himeno T, Kamiya H, Nakamura J. Lumos for the long trail:

strategies for clinical diagnosis and severity staging for diabetic

polyneuropathy and future directions. J Diabetes Investig. 2020

Jan;11(1):5–16.

26. 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. Diabetes. 2006

Jun;55(1):1813–8.

27. Mickle KJ, Angin S, Crofts G, Nester CJ. Effects of Age on

Strength and morphology of toe flexor muscles. J Orthop Sports

Phys Ther. 2016 Dec;46(12):1065–70.

28. Menz HB, Zammit GV, Munteanu SE, Scott G. Plantarflexion

strength of the toes: age and gender differences and evaluation of

a clinical screening test. Foot Ankle Int. 2006 Dec;27(12):1103–8.

29. Ryall JG, Schertzer JD, Lynch GS. Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontology 2008 Aug;9(4):213–28.

1397

30. Wilkinson DJ, Piasecki M, Atherton PJ. The age-related loss of

skeletal muscle mass and function: measurement and physiology

of muscle fibre atrophy and muscle fibre loss in humans. Ageing

Res Rev. 2018 Nov;47:123–32.

31. Nomura T, Kawae T, Kataoka H, Ikeda Y. Assessment of lower

extremity muscle mass, muscle strength, and exercise therapy in

elderly patients with diabetes mellitus. Environ Health Prev Med.

2018 Dec;23(1):20.

32. Stouge A, Khan KS, Kristensen AG, Tankisi H, Schlaffke L, Froeling M, et al. MRI of skeletal muscles in participants with type

2 diabetes with or without Diabetic Polyneuropathy. Radiology.

2020 Dec;297(3):608–19.

33. Almurdhi MM, Reeves ND, Bowling FL, Boulton AJM, 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 Mar 1;39(3):441–7.

34. ElSayed NA, Aleppo G, Aroda VR, Bannuru RR, Brown FM,

Bruemmer D, et al. 5. Facilitating positive Health Behaviors and

Well-being to Improve Health Outcomes: Standards of Care in

Diabetes-2023. Diabetes Care. 2023 Jan;146:68–96.

35. Kimura T, Thorhauer ED, Kindig MW, Shofer JB, Sangeorzan

BJ, Ledoux WR. Neuropathy, claw toes, intrinsic muscle volume,

and plantar aponeurosis thickness in diabetic feet. BMC Musculoskelet Disord. 2020 Dec;21(1):485.

36. Khunkaew S, Fernandez R, Sim J. Health-related quality of life

among adults living with diabetic foot ulcers: a meta-analysis.

Qual Life Res. 2019 Jun;28(6):1413–27.

37. Willemse L, Wouters EJM, Bronts HM, Pisters MF, Vanwanseele B. The effect of interventions anticipated to improve plantar

intrinsic foot muscle strength on fall-related dynamic function in

adults: a systematic review. J Foot Ankle Res. 2022 Dec;15(1):3.

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