The Correlation Between Biomechanical Parameters of Lower Limb and Overall Risk for Diabetic Foot Ulcer
Abstract
Background/Aim: Preventing lower limb diabetic complications begins with identifying those at risk for diabetic foot ulceration (DFU). DFU development is related to abnormal pattern of plantar pressure distribution caused by alterations in foot rollover process due to loss of foot-ankle muscular strength, impaired range of motion (ROM) and nervous function, as their integrity is needed to enable proper load absorption on plantar surface. Objective of study was to determine correlation between biomechanical parameters of lower limb: ankle and foot muscle strength, ROM at ankle joint (AJ), subtalar joint (SJ) and first metatarsophalangeal joint (I MTP) and overall risk for DFU assessed by IWGDF 2019 Guidance risk stratification system.
Methods: A cross-sectional study included 100 diabetic patients, both types. Patients were classified into 4 DFU risk categories applying IWGDF Guidelines 2019 stratification risk system. Function of ten foot and ankle muscles was evaluated by manual muscle testing applying Michigan Diabetic Neuropathy Score system and was expressed by muscle score (MS) on dominant leg. ROM at AJ, SJ and I MTP was measured with a goniometer on dominant leg and was expressed by degree (°).
Results: Average MS in specified categories were as follows: Category 0: 9.2; Category 1: 13.9; Category 2: 13.3; Category 3: 15.2 and they were significantly different. Average ROM at AJ in specified categories were as follows: Category 0: 49.3º; Category 1: 48.8º; Category 2: 45.5º; Category 3: 44.6º and they were not significantly different. Average ROM at SJ in specified categories were as follows: Category 0: 37.8º; Category 1: 31.3º; Category 2: 35.0º; Category 3: 28.7º and they were significantly different. Average ROM at I MTP in specified categories were as follows: Category 0: 78.6º; Category 1: 74.4º; Category 2: 65.5º; Category 3: 57.9º and they were significantly different.
Conclusions: Risk for DFU ulcer significantly correlates with decreased ankle and foot muscle strength and ROM at SJ and I MTP but does not correlate with ROM at AJ.
References
1. International Diabetes Federation. IDF Diabetes Atlas, 9th ed. Brussels, Belgium: 2019.
2. Armstrong DG, Boulton AJM, Bus SA. Diabetic foot ulcers and their recurrence. N Engl J Med 2017;376(24):2367-75.
3. International Diabetes Federation. The Diabetic Foot. Brussels, Belgium: 2020 [Internet]. [Cited: 1-Jan-2023] Available at: https://idf.org/our-activities/care-prevention/diabetic-foot.html.>
4. American Diabetes Association. Economic costs of diabetes in the U.S. in 2017. Diabetes Care 2018 May;41(5):917-28.
5. Bus SA, van Netten JJ, Monteiro-Soares M, Lipsky BA, Schaper NC. Diabetic foot disease: "The Times They are A Changin' ". Diabetes Metab Res Rev 2020 Mar;36 Suppl 1(Suppl 1):e3249. doi: 10.1002/dmrr.3249.
6. Schaper NC, van Netten JJ, Apelqvist J, Bus SA, Hinchliffe RJ, Lipsky BA; IWGDF Editorial Board. Practical Guidelines on the prevention and management of diabetic foot disease (IWGDF 2019 update). Diabetes Metab Res Rev 2020 Mar;36 Suppl 1:e3266. doi: 10.1002/dmrr.3266.
7. Nagawa MHB, Shawky AF, Basant H. Gait analysis in patients with diabetic peripheral neuropathy. Med J Cairo Univ 2010;78(2):827-34.
8. Sawacha Z, Spolaor F, Guarneri G, Contessa P, Carraro E, Venturin A, et al. Abnormal muscle activation during gait in diabetes patients with and without neuropathy. Gait Posture 2012;35(1):101-5.
9. 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 Apr 27;15:137. doi: 10.1186/1471-2474-15-137.
10. Sartor CD, Watari R, Pássaro AC, Picon AP, Hasue RH, Sacco ICN. Effects of a combined strengthening, stretching and functional training program versus usual-care on gait biomechanics and foot function for diabetic neuropathy: a randomized controlled trial. BMC Musculoskelet Disord 2012 Mar 19;13:36. doi: 10.1186/1471-2474-13-36.
11. Sacco IC, 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 (Bristol, Avon) 2009 Oct;24(8):687-92.
12. Alam U, Riley DR, Jugdey RS, Azmi S, Rajbhandari S, D'Août K, et al. Diabetic neuropathy and gait: a review. Diabetes Ther 2017 Dec;8(6):1253-64.
13. Fernando DJ, Masson EA, Veves A, Boulton AJ. Relationship of limited joint mobility to abnormal foot pressures and diabetic foot ulceration. Diabetes Care 1991;14(1):8-11.
14. Alam U, Riley DR, Jugdey RS, Azmi S, Rajbhandari S, D'Août K, et al. Diabetic neuropathy and gait: a review. Diabetes Ther 2017 Dec;8(6):1253-64.
15. Andreassen CS, Jakobsen J, Andersen H. Muscle weakness: a progressive late complication in diabetic distal symmetric polyneuropathy. Diabetes 2006 Mar;55(3):806-12.
16. Andersen H. Motor dysfunction in diabetes. Diabetes Metab Res Rev 2012 Feb;28 Suppl 1:89-92.
17. Iraj B, Khorvash F, Ebneshahidi A, Askari G. Prevention of diabetic foot ulcer. Int J Prev Med 2013;4(3):373‐6.
18. Bus SA, van Netten JJ. A shift in priority in diabetic foot care and research: 75% of foot ulcers are preventable. Diabetes Metab Res Rev 2016 Jan;32 Suppl 1:195-200.
19. Bus SA, Lavery LA, Monteiro-Soares M, Rasmussen A, Raspovic A, Sacco ICN, et al; International Working Group on the Diabetic Foot. Guidelines on the prevention of foot ulcers in persons with diabetes (IWGDF 2019 update). Diabetes Metab Res Rev 2020 Mar;36 Suppl 1:e3269. doi: 10.1002/dmrr.3269.
20. Boyko EJ, Ahroni JH, Stensel V, Forsberg RC, Davignon DR, Smith DG; A prospective study of risk factors for diabetic foot ulcer. The Seattle Diabetic Foot Study. Diabetes Care 1999;22(7):1036-42.
21. Tapp RJ, Shaw JE, de Courten MP, Dunstan DW, Welborn TA, Zimmet PZ; AusDiab Study Group. Foot complications in Type 2 diabetes: an Australian population-based study. Diabet Med 2003 Feb;20(2):105-13.
22. American Diabetes Association. Standards of medical care in diabetes-2015 abridged for primary care providers. Clin Diabetes 2015 Apr;33(2):97-111.
23. Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcers in patients with diabetes. JAMA 2005;293:217–28.
24. Boulton AJ, Armstrong DG, Albert SF, Frykberg RG, Hellman R, Kirkman MS, et al. American Diabetes Association; American Association of Clinical Endocrinologists. Comprehensive foot examination and risk assessment: a report of the task force of the foot care interest group of the American Diabetes Association, with endorsement by the American Association of Clinical Endocrinologists. Diabetes Care 2008;31(8):1679-85.
25. Abbott CA, Carrington AL, Ashe H, Bath S, Every LC, Griffiths J, et al. The North-West Diabetes Foot Care Study: incidence of and risk factors for, new diabetic foot ulceration in a community- based patient cohort. Diabet Med 2002 May;19(5):377-84.
26. Mayfield JA, Reiber GE, Sanders LJ, Janisse D, Pogach LM, American Diabetes Association. Preventive foot care in diabetes. Diabetes Care 2004;27(1):S63-4.
27. van Schie CHM, Vermigli C, Carrington AL, Boulton A. Muscle weakness and foot deformities in diabetes: relationship to neuropathy and foot ulceration in Caucasian diabetic men. Diabetes Care 2004;27:1668-73.
28. Feldman EL, Stevens MJ, Thomas PK, Brown MB, Canal N, Greene DA. A practical two-step quantitative clinical and electrophysiological assessment for the diagnosis and staging of diabetic neuropathy. Diabetes Care 1994;17(11):1281-9.
29. Bokan V. Muscle weakness and other late complications of diabetic polyneuropathy. Acta Clin Croat 2011;50(3):351-5.
30. Lacote M. Chevalier AM, Miranda A, Bleton JP, Stevenin P. Clinical evaluation of muscle function. Edinburgh, London, Melbourn and New York: Churchill Livingstone, 1987.
31. Jandrić S. Osnovi fizikalne medicine i rehabilitacije. Laktaši: Grafomarkt; 2009. Serbian.
32. Zimny S, Schatz H, Pfohl M. The role of limited joint mobility in diabetic patients with an at-risk foot. Diabetes Care 2004;27:942-6.
33. Fernando DJ, Masson EA, Veves A, Boulton AJ. Relationship of limited joint mobility to abnormal foot pressures and diabetic foot ulceration. Diabetes Care 1991;14(1):8-11.
34. Boulton AJM. The diabetic foot: from art to science. The 18th Camillo Golgi lecture. Diabetologia 2004;47:1343–53.
35. Tapp RJ, Shaw JE, de Courten MP, Dunstan DW, Welborn TA, Zimmet PZ; AusDiab Study Group. Foot complications in Type 2 diabetes: an Australian population-based study. Diabet Med 2003 Feb;20(2):105-13.
36. Young MJ, Boulton AJ, MacLeod AF, Williams DR, Sonksen PH. A multicentre study of the prevalence of diabetic peripheral neuropathy in the United Kingdom hospital clinic population. Diabetologia 1993 Feb;36(2):150-4.
37. Valensi P, Giroux C, Seeboth-Ghalayini B, Attali JR. Diabetic peripheral neuropathy: effects of age, duration of diabetes, glycemic control and vascular factors. J Diabetes Complications 1997 Jan-Feb;11(1):27-34.
38. Soyoye DO, Abiodun OO, Ikem RT, Kolawole BA, Akintomide AO. Diabetes and peripheral artery disease: A review. World J Diabetes 2021 Jun 15;12(6):827-38.
39. Falzon B, Formosa C, Camilleri L, Gatt A. Duration of type 2 diabetes is a predictor of elevated plantar foot pressure. Rev Diabet Stud 2018 Winter;14(4):372-80.
40. Nisar MU, Asad A, Waqas A, Ali N, Nisar A, Qayyum MA, et al. Association of diabetic neuropathy with duration of type 2 diabetes and glycemic control. Cureus 2015 Aug 12;7(8):e302. doi: 10.7759/cureus.302.
41. 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 Syndr 2019 Oct 30;11:89. doi: 10.1186/s13098-019-0487-x.
42. Andersen H, Gjerstad MD, Jakobsen J. Atrophy of foot muscles: a measure of diabetic neuropathy. Diabetes Care 2004;27(10):2382-5.
43. Andersen H, Nielsen S, Mogensen CE, Jakobsen J. Muscle strength in type 2 diabetes. Diabetes 2004;53(6):1543-8.
44. Andreassen CS, Jakobsen J andersen H. Muscle weakness: a progressive late complication in diabetic distal symmetric polyneuropathy. Diabetes 2006;55(3):806-12.
45. 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 Jun;52(6):1182-91.
46. Regensteiner JG, Wolfel EE, Brass EP, Carry MR, Ringel SP, Hargarten ME, et al. Chronic changes in skeletal muscle histology and function in peripheral arterial disease. Circulation 1993 Feb;87(2):413-21.
47. McDermott MM, Tian L, Ferrucci L, Liu K, Guralnik JM, Liao Y, et al. Associations between lower extremity ischemia, upper and lower extremity strength and functional impairment with peripheral arterial disease. J Am Geriatr Soc 2008 Apr;56(4):724-9.
48. Soysa A, Hiller C, Refshauge K, Burns J. Importance and challenges of measuring intrinsic foot muscle strength. J Foot Ankle Res 2012 Nov 26;5(1):29. doi: 10.1186/1757-1146-5-29.
49. 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 Aug;25(8):1444-50.
50. Bakker K, Apelqvist J, Schaper NC; International Working Group on Diabetic Foot Editorial Board. Practical guidelines on the management and prevention of the diabetic foot 2011. Diabetes Metab Res Rev 2012;28(1):225-31.
51. Jeffcoate WJ, Chipchase SY, Ince P, Game FL Assesing the outcome of the management of diabetic foot ulcers using ulcer-related and person-related measures. Diabetes Care 2006;29(8):1784-7.
52. Schaper NC, Apelqvist J, Bakker K. The international consensus and practical guidelines on the management and prevention of the diabetic foot. Curr Diab Rep 2003 Dec;3(6):475-9.
53. Frykberg RG, Zgonis T, Armstrong DG, Driver VR, Giurini JM, Kravitz SR, et al. Diabetic foot disorders. A clinical practice guideline (2006 revision). J Foot Ankle Srg 2006;45(5):1-66.
54. 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(3):295-301.
55. Formosa C, Gatt A, Chockalingam N. The importance of clinical biomechanical assessment of foot deformity and joint mobility in people living with type-2 diabetes within a primary care setting. Prim Care Diabetes 2013;7(1):45-50.
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).