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Diabetes mellitus tendino-myopathy: epidemiology, clinical features, diagnosis and management of an overlooked diabetic complication

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Abstract

Tendino-myopathy, an unexplored niche, is a non-vascular unstated T2DM complication, which is largely disregarded in clinical practice, thus, we aim to explore it in this review. Literature search using published data from different online resources. Epidemiologically, reported prevalence varies around 10–90%, which is marked variable and unreliable. Clinically, diabetic tendino-myopathy is typified by restriction of movement, pain/tenderness, cramps and decreased functions. Moreover, myopathy is characterized by muscle atrophy, weakness and ischemia, and tendinopathy by deformities and reduced functions/precision. In tendonapthy, the three most affected regions are: the hand (cheiroarthropathy, Dupuytren's contracture, flexor tenosynovitis and carpel tunnel syndrome), shoulder (adhesive capsulitis, rotator cuff tendinopathy and tenosynovitis) and foot (Achilles tendinopathy with the risk of tear/rupture), in addition to diffuse idiopathic skeletal hyperostosis. Pathologically, it is characterized by decreased muscle fiber mass and increased fibrosis, with marked extracellular matrix remodeling and deposition of collagens. The tendon changes include decreased collagen fibril diameter, changed morphology, increased packing and disorganization, with overall thickening, and calcification. Diagnosis is basically clinical and radiological, while diagnostic biomarkers are awaited. Management is done by diabetes control, special nutrition and physiotherapy, while analgesics, steroids and surgery are used in tendinopathy. Several antisarcopenic drugs are in the pipeline. This review aims to bridge clinical practice with research and update routine diabetic checkup by inclusion of tendino-myopathies in the list with an emphasis on management.

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References

  1. Cho NH, Shaw JE, Karuranga S et al (2018) IDF diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 138:271–281

    Article  CAS  PubMed  Google Scholar 

  2. Izzo A, Massimino E, Riccardi G, Della Pepa G (2021) A narrative review on sarcopenia in type 2 diabetes mellitus: prevalence and associated factors. Nutrients 13(1):183.12

    Article  Google Scholar 

  3. Fearon K, Evans WJ, Anker SD (2011) Myopenia—a new universal term for muscle wasting. J Cachexia Sarcopenia Muscle 2:1–3

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mesinovic J, Zengin A, De Courten B, Ebeling PR, Scott D (2019) Sarcopenia and type 2 diabetes mellitus: a bidirectional relationship. Diabetes Metab Syndr Obes 12:1057–1072

    Article  PubMed  PubMed Central  Google Scholar 

  5. Mukund K, Subramaniam S (2020) Skeletal muscle: A review of molecular structure and function, in health and disease. WIREs Syst Biol Med 12:e1462

    Google Scholar 

  6. Nedergaard A, Karsdal MA, Sun S, Henriksen K (2013) Serological muscle loss biomarkers: an overview of current concepts and future possibilities. J Cachexia Sarcopenia Muscle 4(1):1–17

    Article  PubMed  Google Scholar 

  7. Abate M, Schiavone C, Salini V (2010) Sonographic evaluation of the shoulder in asymptomatic elderly subjects with diabetes. BMC Musculoskelet Disord 11:278

    Article  PubMed  PubMed Central  Google Scholar 

  8. Nichols AEC, Oh I, Loiselle AE (2020) Effects of Type II Diabetes Mellitus on Tendon Homeostasis and Healing. J Orthop Res 38(1):13–22

    Article  PubMed  Google Scholar 

  9. Vance MC, Tucker JJ, Harness NG (2012) The association of hemoglobin A1c with the prevalence of stenosing flexor tenosynovitis. J Hand Surg Am 37:1765–1769

    Article  PubMed  Google Scholar 

  10. Leenders M, Verdijk LB, van der Hoeven L et al (2013) Patients with type 2 diabetes show a greater decline in muscle mass, muscle strength, and functional capacity with aging. J Am Med Dir Assoc 8:585–592

    Article  Google Scholar 

  11. Sarodnik C, Bours SPG, Schaper NC, van den Bergh JP, van Geel TACM (2018) The risks of sarcopenia, falls and fractures in patients with type 2 diabetes mellitus. Maturitas 109:70–77

    Article  CAS  PubMed  Google Scholar 

  12. Takahashi F, Hashimoto Y, Kaji A, Sakai R, Kawate Y, Okamura T, Kondo Y, Fukuda T, Kitagawa N, Okada H, Nakanishi N, Majima S, Senmaru T, Ushigome E, Hamaguchi M, Asano M, Yamazaki M, Fukui M (2021) Vitamin intake and loss of muscle mass in older people with Type 2 Diabetes: A Prospective Study of the KAMOGAWA-DM Cohort. Nutrients 13(7):2335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Moayeri A, Mohamadpour M, Mousavi SF, Shirzadpour E, Mohamadpour S, Amraei M (2017) Fracture risk in patients with type 2 diabetes mellitus and possible risk factors: a systematic review and meta-analysis. Ther Clin Risk Manag 11(13):455–468

    Article  Google Scholar 

  14. Wyatt LH, Ferrance RJ (2006) The musculoskeletal effects of diabetes mellitus. J Can Chiropr Assoc 50:43–50

    PubMed  PubMed Central  Google Scholar 

  15. Huang BK, Monu JU, Doumanian J (2010) Diabetic myopathy: MRI patterns and current trends. AJR Am J Roentgenol 195(1):198–204

    Article  PubMed  Google Scholar 

  16. Baker JC, Demertzis JL, Rhodes NG, Wessell DE, Rubin DA (2012) Diabetic Musculoskeletal Complications and Their Imaging Mimics. Radiographics 32:1959–1974

    Article  PubMed  Google Scholar 

  17. Knipe H, Weerakkody Y. Tendinopathy. (2021) Reference article, Radiopaedia.org. Article created in 2019, revised 15 times till accessed on 07 Dec 2021. https://doi.org/10.53347/rID-65577.

  18. Balci N, Balci MK, Tuzuner S (1999) Shoulder adhesive capsulitis and shoulder range of motion in type II diabetes mellitus: association with diabetic complications. J Diabetes Complications 13:135–140

    Article  CAS  PubMed  Google Scholar 

  19. Ceravolo ML, Gaida JE, Keegan RJ (2020) Quality-of-life in achilles tendinopathy: an exploratory study. Clin J Sport Med 30(5):495–502

    PubMed  Google Scholar 

  20. Cho NS, Moon SC, Jeon JW et al (2015) The influence of diabetes mellitus on clinical and structural outcomes after arthroscopic rotator cuff repair. Am J Sports Med 43:991–997

    Article  PubMed  Google Scholar 

  21. Gaida JE, Ashe MC, Bass SL et al (2009) Is adiposity an under-recognized risk factor for tendinopathy? a systematic review. Arthritis Rheum 61:840–849

    Article  PubMed  Google Scholar 

  22. Lu YC, Wang PW, Liu RT et al (1993) Limited joint mobility of the hand: prevalence and relation to chronic complications in non-insulin-dependent diabetes mellitus patients. J Formos Med Assoc 92:139–143

    CAS  PubMed  Google Scholar 

  23. Papanas N, Maltezos E (2010) The diabetic hand: a forgotten complication? J Diabetes Complications 24:154–162

    Article  PubMed  Google Scholar 

  24. Chammas M, Bousquet P, Renard E et al (1995) Dupuytren’s disease, carpal tunnel syndrome, trigger finger, and diabetes mellitus. J Hand Surg Am 20:109–114

    Article  CAS  PubMed  Google Scholar 

  25. Ravindran Rajendran S, Bhansali A, Walia R, Dutta P, Bansal V, Shanmugasundar G (2011) Prevalence and pattern of hand soft-tissue changes in type 2 diabetes mellitus. Diabetes Metab 37(4):312–317

    Article  CAS  PubMed  Google Scholar 

  26. Thomas SJ, McDougall C, Brown ID et al (2007) Prevalence of symptoms and signs of shoulder problems in people with diabetes mellitus. J Shoulder Elbow Surg 16:748–751

    Article  PubMed  Google Scholar 

  27. Huang SW, Wang WT, Chou LC, Liou TH, Chen YW, Lin HW (2016) Diabetes mellitus increases the risk of rotator cuff tear repair surgery: a population-based cohort study. J Diabetes Complications 30(8):1473–1477

    Article  PubMed  Google Scholar 

  28. Ranger TA, Wong AM, Cook JL et al (2016) Is there an association between tendinopathy and diabetes mellitus? a systematic review with meta-analysis. Br J Sports Med 50:982–989

    Article  PubMed  Google Scholar 

  29. Mavrikakis ME, Drimis S, Kontoyannis DA et al (1989) Calcific shoulder periarthritis (tendinitis) in adult onset diabetes mellitus: a controlled study. Ann Rheum Dis 48:211–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. D’Ambrogi E, Giacomozzi C, Macellari V et al (2005) Abnormal foot function in diabetic patients: the altered onset of Windlass mechanism. Diabet Med 22:1713–1719

    Article  CAS  PubMed  Google Scholar 

  31. Batista F, Nery C, Pinzur M et al (2008) Achilles tendinopathy in diabetes mellitus. Foot Ankle Int 29:498–501

    Article  PubMed  Google Scholar 

  32. Gariani K, Waibel FWA, Viehöfer AF, Uçkay I (2020) Plantar fasciitis in diabetic foot patients: risk factors, pathophysiology, diagnosis, and management. Diabetes Metab Syndr Obes 22(13):1271–1279

    Article  Google Scholar 

  33. Tanganelli F, Meinke P, Hofmeister F et al (2021) Type-2 muscle fiber atrophy is associated with sarcopenia in elderly men with hip fracture. Exp Gerontol. 144:111171

    Article  CAS  PubMed  Google Scholar 

  34. Pillai SS (2017) Prevalence of Myopathy in Type 2 Diabetes Mellitus. J Med Sci clin Res 05:21022–21027

    Article  Google Scholar 

  35. Horton WB, Taylor JS, Ragland TJ, Subauste AR (2015) Diabetic muscle infarction: a systematic review. BMJ Open Diabetes Res Care 3(1):e000082

    Article  PubMed  PubMed Central  Google Scholar 

  36. Baskerville R, McCartney DE, McCartney SM, Dawes H, Tan GD (2018) Tendinopathy in type 2 diabetes: a condition between specialties? Br J Gen Pract 68(677):593–594

    Article  PubMed  PubMed Central  Google Scholar 

  37. Ai Y, Xu R, Liu L (2021) The prevalence and risk factors of sarcopenia in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Diabetol Metab Syndr 13:93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Pandey A, Usman K, Reddy H, Gutch M, Jain N, Qidwai S (2013) Prevalence of hand disorders in type 2 diabetes mellitus and its correlation with microvascular complications. Ann Med Health Sci Res 3(3):349–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mustafa KN, Khader YS, Bsoul AK, Ajlouni K (2016) Musculoskeletal disorders of the hand in type 2 diabetes mellitus: prevalence and its associated factors. Int J Rheum Dis 19(7):730–735

    Article  CAS  PubMed  Google Scholar 

  40. Alsubheen SA, MacDermid JC, Overend TJ, Faber KJ (2019) The diabetic shoulder – a literature review. J Diabetes Clin Res 1(2):59–70

    Google Scholar 

  41. Kudsi M, Labban L (2020) The prevalence of musculoskeletal complications in type 2 diabetes mellitus. Open Access Library J 7:1–10

    Google Scholar 

  42. Beckmann NM, Tran MQ, Cai C (2019) Incidence of rotator cuff tears in the setting of calcific tendinopathy on MRI: a case controlled comparison. Skeletal Radiol 48(2):245–250

    Article  PubMed  Google Scholar 

  43. Su YC, Chung CH, Ke MJ, Chen LC, Chien WC, Wu YT (2021) Increased risk of shoulder calcific tendinopathy in diabetes mellitus: a nationwide, population-based, matched cohort study. Int J Clin Pract. 75(10):e14549

    PubMed  Google Scholar 

  44. Afolabi BI, Idowu BM, Onigbinde SO (2021) Achilles tendon degeneration on ultrasound in type 2 diabetic patients. J Ultrason 20(83):e291–e299. https://doi.org/10.15557/JoU.2020.0051

    Article  PubMed  Google Scholar 

  45. Ursini F, Arturi F, D’Angelo S et al (2017) High prevalence of achilles tendon enthesopathic changes in patients with type 2 diabetes without peripheral neuropathy. J Am Podiatr Med Assoc 107(2):99–105

    Article  PubMed  Google Scholar 

  46. Oberbach A, Bossenz Y, Lehmann S et al (2006) Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 29(4):895–900

    Article  CAS  PubMed  Google Scholar 

  47. Rosenberg IH (2011) Sarcopenia: origins and clinical relevance. Clin Geriat Med 27(3):337–339

    Article  Google Scholar 

  48. Mann CJ, Perdiguero E, Kharraz Y et al (2011) Aberrant repair and fibrosis development in skeletal muscle. Skelet Muscle 1:21–21

    Article  PubMed  PubMed Central  Google Scholar 

  49. Serrano AL, Muñoz-Cánoves P (2010) Regulation and dysregulation of fibrosis in skeletal muscle. Exp Cell Res 316(18):3050–3058

    Article  CAS  PubMed  Google Scholar 

  50. Carmignac V, Durbeej M (2012) Cell–matrix interactions in muscle disease. J Path 226(2):200–218

    Article  CAS  PubMed  Google Scholar 

  51. Stearns-Reider KM, D’Amore A, Beezhold K et al (2017) Aging of the skeletal muscle extracellular matrix drives a stem cell fibrogenic conversion. Aging Cell 16(3):518–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Williams AS, Kang L, Wasserman DH (2015) The extracellular matrix and insulin resistance. Trends Endocrinol Metabol 26(7):357–366

    Article  CAS  Google Scholar 

  53. Chapman MA, Mukund K, Subramaniam S, Brenner D, Lieber RL (2017) Three distinct cell populations express extracellular matrix proteins and increase in number during skeletal muscle fibrosis. Am J Physiol: Cell Physiol 312(2):C131–C143

    Article  Google Scholar 

  54. Van PR, Fontelonga TM, Barraza-Flores P, Sarathy A, Nunes AM, Burkin DJ (2017) ECM-related myopathies and muscular dystrophies: Pros and cons of protein therapies. Comprehensive Physiol 7(4):1519–1536

    Article  Google Scholar 

  55. Grant WP, Sullivan R, Sonenshine DE et al (1997) Electron microscopic investigation of the effects of diabetes mellitus on the Achilles tendon. J Foot Ankle Surg 36:272–278

    Article  CAS  PubMed  Google Scholar 

  56. Singh VP, Bali A, Singh N et al (2014) Advanced glycation end products and diabetic complications. Korean J Physiol Pharmacol 18:1–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Cruz-Jentoft AJ, Bahat G, Bauer J et al (2018) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48(1):16–31

    Article  PubMed Central  Google Scholar 

  58. Sjöström LA (1991) A computer-tomography based multicompartment body composition technique and anthropometric predictions of lean body mass, total and subcutaneous adipose tissue. Int J Obesity 15:19–30

    Google Scholar 

  59. Heymsfield SB, Ross R, Wang Z, Frager D (1997) Imaging techniques of body composition: advantages of measurement and new uses. Pp. 127-150 In: Emerging technologies for nutrition research, S.J. Carlson-Newberry, editor; and R.B. Costello, editor. , eds. Institute of Medicine. Washington, DC: National Academy Press

  60. Lukasksi HC, Mendez J, Buskirk ER, Cohn SH (1981) Relationship between endogenous 3-methylhistidine excretion and body composition. Am J Physiol 240:E302–E307

    Google Scholar 

  61. Kochlik B, Stuetz W, Pérès K et al (2019) Associations of plasma 3-methylhistidine with frailty status in French Cohorts of the FRAILOMIC initiative. J Clin Med 8:1010

    Article  CAS  PubMed Central  Google Scholar 

  62. Cetrone M, Mele A, Tricarico D (2014) Effects of the antidiabetic drugs on the age-related atrophy and sarcopenia associated with diabetes type II. Curr Diabetes Rev 10(4):231–237

    Article  CAS  PubMed  Google Scholar 

  63. Perna S, Guido D, Bologna C et al (2016) Liraglutide and obesity in elderly: efficacy in fat loss and safety in order to prevent sarcopenia. A perspective case series study. Aging Clin Exp Res. 28(6):1251–1257

    Article  PubMed  Google Scholar 

  64. Kwak JY, Kwon KS (2019) Pharmacological interventions for treatment of sarcopenia: current status of drug development for Sarcopenia. Ann Geriatr Med Res 23(3):98–104

    Article  PubMed  PubMed Central  Google Scholar 

  65. Bryner RW, Woodworth-Hobbs ME, Williamson DL, Alway SE (2012) Docosahexaenoic Acid protects muscle cells from palmitate-induced atrophy. ISRN Obes. 2012:647348

    PubMed  PubMed Central  Google Scholar 

  66. Beveridge LA, Ramage L, McMurdo ME, George J, Witham MD (2013) Allopurinol use is associated with greater functional gains in older rehabilitation patients. Age Ageing 42(3):400–404

    Article  PubMed  Google Scholar 

  67. Richter EA, Hargreaves M (2013) Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev 93(3):993–1017

    Article  CAS  PubMed  Google Scholar 

  68. Calvani R, Miccheli A, Landi F, et al. (2013) Current nutritional recommendations and novel dietary strategies to manage sarcopenia. J Frailty Aging doi: https://doi.org/10.14283/jfa.2013.7

  69. Milne AC, Potter J, Vivanti A, Avenell A (2009) Protein and energy supplementation in elderly people at risk from malnutrition. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD003288.pub3

    Article  PubMed  PubMed Central  Google Scholar 

  70. Wilkinson DJ, Hossain T, Hill DS et al (2013) Effects of leucine and its metabolite betahydroxy-beta-methylbutyrate on human skeletal muscle protein metabolism. J Physiol 591:2911e2923

    Article  CAS  Google Scholar 

  71. Girón MD, Vílchez JD, Salto R et al (2016) Conversion of leucine to β-hydroxy-β-methylbutyrate by α-keto isocaproate dioxygenase is required for a potent stimulation of protein synthesis in L6 rat myotubes: HMB is a potent stimulator of protein synthesis. J Cachexia, Sarcopenia and Muscle 7(1):68–78. https://doi.org/10.1002/jcsm.12032

    Article  Google Scholar 

  72. Clegg A, Young J, Iliffe S et al (2013) Frailty in elderly people. Lancet. https://doi.org/10.1016/S0140-6736(12)62167-9

    Article  PubMed  Google Scholar 

  73. Shimizu M. and Sakuma K. (2020) Nutritional Approaches for Attenuating Muscle Atrophy, Background and Management of Muscular Atrophy, Julianna Cseri, IntechOpen, DOI: https://doi.org/10.5772/intechopen.94009. https://www.intechopen.com/chapters/73448.

  74. Takahashi F, Hashimoto Y, Kaji A, Sakai R, Kawate Y, Okamura T, Kitagawa N, Okada H, Nakanishi N, Majima S, Senmaru T, Ushigome E, Hamaguchi M, Asano M, Yamazaki M, Fukui M (2020) Habitual miso (fermented soybean paste) consumption is associated with a low prevalence of sarcopenia in patients with type 2 diabetes: a cross-sectional study. Nutrients 13(1):72

    Article  PubMed Central  CAS  Google Scholar 

  75. Shils ME, Olson JA, Shike M, Ross AC (1999) Eds.: Modern Nutrition in Health and Disease. 9th edition. Philadelphia Pa., Lea & Febiger

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Authors and Affiliations

  1. Medical Biochemistry and Molecular Biology, Khartoum, Sudan

    Hayder A. Giha

  2. Department of Biochemistry, College of Medicine and Medical Sciences (CMMS), Arabian Gulf University (AGU), Manama, Kingdom of Bahrain

    Mai S. Sater

  3. Department of Internal Medicine, Faculty of Medicine and Health Sciences, Alneelain University, Khartoum, Sudan

    Osman A. O. Alamin

  4. Interventional Cardiology, Ahmad Gasim Cardiac Centre, Ahmad Gasim Hospital, Khartoum North, Sudan

    Osman A. O. Alamin

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Giha, H.A., Sater, M.S. & Alamin, O.A.O. Diabetes mellitus tendino-myopathy: epidemiology, clinical features, diagnosis and management of an overlooked diabetic complication. Acta Diabetol 59, 871–883 (2022). https://doi.org/10.1007/s00592-022-01860-9

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