Occurrence of tendon pathologies in metabolic disorders

Rheumatology (United Kingdom)

Volumn 52, Issue 4, 2013, Pages 599-608

  Abate, Michele ^a   Schiavone, Cosima ^a   Salini, Vincenzo ^a   Andia, Isabel ^b  

^a UNIVERSITY OF CHIETI   (Italy)

^b BIOCRUCES BIZKAIA HEALTH RESEARCH INSTITUTE   (Spain)

Author keywords

Diabetes mellitus; Hypercholesterolaemia; Hyperuricaemia; Obesity; Tendinopathy

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CHOLESTEROL; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; OXIDIZED LOW DENSITY LIPOPROTEIN; TRIACYLGLYCEROL; URATE; URIC ACID;

ALKAPTONURIA; ARTHROPATHY; CARPAL TUNNEL SYNDROME; CHOLESTEROL BLOOD LEVEL; CLINICAL ASSESSMENT; CRYSTALLIZATION; DEGENERATIVE DISEASE; DIABETES MELLITUS; DIABETIC FOOT; DIABETIC NEUROPATHY; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE DURATION; DUPUYTREN CONTRACTURE; FAMILIAL HYPERCHOLESTEROLEMIA; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; GOUT; HISTOPATHOLOGY; HUMEROSCAPULAR PERIARTHRITIS; HYPERCHOLESTEROLEMIA; HYPERURICEMIA; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RHEUMATIC DISEASE; ROTATOR CUFF RUPTURE; SOFT TISSUE; TENDON DISEASE; WEIGHT BEARING; WEIGHT GAIN; XANTHOMA;

DIABETES COMPLICATIONS; HUMANS; HYPERCHOLESTEROLEMIA; HYPERURICEMIA; METABOLIC DISEASES; TENDINOPATHY;

EID: 84875614967     PISSN: 14620324     EISSN: 14620332     Source Type: Journal    
DOI: 10.1093/rheumatology/kes395     Document Type: Review

References (88)

1. Heinemeier KM, Kjaer M. In vivo investigation of tendon responses to mechanical loading. J Musculoskelet Neuronal Interact 2011;11:115-23.
2. Parkinson J, Samiric T, Ilic MZ et al. Involvement of proteoglycans in tendinopathy. J Musculoskelet Neuronal Interact 2011;11:86-93.
3. Abate M, Silbernagel KG, Siljeholm C et al. Pathogenesis of tendinopathies: inflammation or degeneration? Arthritis Res Ther 2009;11:235.
4. Thornton GM, Hart DA. The interface of mechanical loading and biological variables as they pertain to the development of tendinosis. J Musculoskelet Neuronal Interact 2011;11:94-105.
5. Dirks RC, Warden SJ. Models for the study of tendinopathy. J Musculoskelet Neuronal Interact 2011;11: 141-9.
6. Ramchurn N, Mashamba C, Leitch E et al. Upper limb musculoskeletal abnormalities and poor metabolic control in diabetes. Eur J Intern Med 2009;20:718-21.
7. Gaida JE, Cook JL, Bass SL. Adiposity and tendinopathy. Disabil Rehabil 2008;30:1555-62.
8. Ozgurtas T, Yildiz C, Serdar M et al. Is high concentration of serum lipids a risk factor for Achilles tendon rupture? Clin Chim Acta 2003;331:25-8.
9. Pineda C, Amezcua-Guerra LM, Solano C et al. Joint and tendon subclinical involvement suggestive of gouty arthritis in asymptomatic hyperuricemia: an ultrasound controlled study. Arthritis Res Ther 2011; 13:R4.
10. Perry MB, Suwannarat P, Furst GP et al. Musculoskeletal findings and disability in alkaptonuria. J Rheumatol 2006; 33:2280-5.
11. Rosenbloom AL, Silverstein JH. Connective tissue and joint disease in diabetes mellitus. Endocrinol Metab Clin North Am 1996;25:473-83.
12. Aydeniz A, Gursoy S, Guney E. Which musculoskeletal complications are most frequently seen in type 2 diabetes mellitus? J Int Med Res 2008;36:505-11.
13. Abate M, Schiavone C, Pelotti P et al. Limited joint mobility in diabetes and ageing: recent advances in pathogenesis and therapy. Int J Immunopathol Pharmacol 2010;23: 997-1003.
14. Viikari-Juntura E, Shiri R, Solovieva S et al. Risk factors of atherosclerosis and shoulder pain-is there an association? A systematic review. Eur J Pain 2008;12: 412-26.
15. Cole A, Gill TK, Shanahan EM et al. Is diabetes associated with shoulder pain or stiffness? Results from a population based study. J Rheumatol 2009;36:371-7.
16. Longo UG, Franceschi F, Ruzzini L et al. Higher fasting plasma glucose levels within the normoglycaemic range and rotator cuff tears. Br J Sports Med 2009;43: 284-7.
17. Abate M, Schiavone C, Salini V. Sonographic evaluation of the shoulder in asymptomatic elderly subjects with diabetes. BMC Musculoskelet Disord 2010;11:278.
18. Yamaguchi K, Tetro AM, Blam O et al. Natural history of asymptomatic rotator cuff tears: a longitudinal analysis of asymptomatic tears detected sonographically. J Shoulder Elbow Surg 2001;10:199-203.
19. Namdari S, Green A. Range of motion limitation after rotator cuff repair. J Shoulder Elbow Surg 2010;19:290-6.
20. Clement ND, Hallett A, MacDonald D et al. Does diabetes affect outcome after arthroscopic repair of the rotator cuff? J Bone Joint Surg Br 2010;92:1112-7.
21. Duffin AC, Lam A, Kidd R et al. Ultrasonography of plantar soft tissues thickness in young people with diabetes. Diabet Med 2002;19:1009-13.
22. Batista F, Nery C, Pinzur M et al. Achilles tendinopathy in diabetes mellitus. Foot Ankle Int 2008;29:498-501.
23. Akturk M, Ozdemir A, Maral I et al. Evaluation of Achilles tendon thickening in type 2 diabetes mellitus. Exp Clin Endocrinol Diabetes 2007;115:92-6.
24. Abate M, Schiavone C, Di Carlo L et al. Achilles tendon and plantar fascia in recently diagnosed type II diabetes: role of body mass index. Clin Rheumatol 2012;31:1109-13.
25. Papanas N, Courcoutsakis N, Papatheodorou K et al. Achilles tendon volume in type 2 diabetic patients with or without peripheral neuropathy: MRI study. Exp Clin Endocrinol Diabetes 2009;117:645-8.
26. Lavery LA, Armstrong DG, Wunderlich RP et al. Predictive value of foot pressure assessment as part of a population-based diabetes disease management program. Diabetes Care 2003;26:1069-73.
27. Andersen H, Mogensen PH. Disordered mobility of large joints in association with neuropathy in patients with long-standing insulin-dependent diabetes mellitus. Diabet Med 1997;14:221-7.
28. Pascual Huerta J, García JM, Matamoros EC et al. Relationship of body mass index, ankle dorsiflexion, and foot pronation on plantar fascia thickness in healthy, asymptomatic subjects. J Am Podiatr Med Assoc 2008; 98:379-85.
29. Cronin NJ, Peltonen J, Ishikawa M et al. Achilles tendon length changes during walking in long-term diabetes patients. Clin Biomech (Bristol, Avon) 2010;25: 476-82.
30. Giacomozzi C, D'Ambrogi E, Uccioli L et al. Does the thickening of Achilles tendon and plantar fascia contribute to the alteration of diabetic foot loading? Clin Biomech (Bristol, Avon) 2005;20:532-9.
31. Grant WP, Sullivan R, Sonenshine DE et al. Electron microscopic investigation of the effects of diabetes mellitus on the Achilles tendon. J Foot Ankle Surg 1997;36: 272-8.
32. Fujii K, Yamagishi T, Nagafuchi T et al. Biochemical properties of collagen from ligaments and periarticular tendons of the human knee. Knee Surg Sports Traumatol Arthrosc 1994;2:229-33.
33. Eyre DR, Paz MA, Gallop PM. Cross-linking in collagen and elastin. Annu Rev Biochem 1984;53:717-48.
34. Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 2010;21:195-214.
35. DeGroot J. The AGE of the matrix: chemistry, consequence and cure. Curr Opin Pharmacol 2004;4:301-5.
36. Vazzana N, Santilli F, Cuccurullo C et al. Soluble forms of RAGE in internal medicine. Intern Emerg Med 2009;4: 389-401.
37. Franke S, Sommer M, Rüster C et al. Advanced glycation end products induce cell cycle arrest and proinflammatory changes in osteoarthritic fibroblast-like synovial cells. Arthritis Res Ther 2009;11:R136.
38. Goldin A, Beckman JA, Schmidt AM et al. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 2006;114:597-605.
39. Steenvoorden MM, Toes RE, Ronday HK et al. RAGE activation induces invasiveness of RA fibroblast-like synoviocytes in vitro. Clin Exp Rheumatol 2007; 25:740-2.
40. Huijberts MS, Schaper NC, Schalkwijk CG. Advanced glycation end products and diabetic foot disease. Diabetes Metab Res Rev 2008;24(SUPPL 1):S19-S24.
41. Alikhani Z, Alikhani M, Boyd CM et al. Advanced glycation end products enhance expression of pro-apoptotic genes and stimulate fibroblast apoptosis through cytoplasmic and mitochondrial pathways. J Biol Chem 2005;280: 12087-95.
42. Moraes do Carmo CC, Fonseca de Almeida Melão LI, Valle de Lemos Weber MF et al. Anatomical features of plantar aponeurosis: cadaveric study using ultrasonography and magnetic resonance imaging. Skeletal Radiol 2008;37:929-35.
43. Jeswani T, Morlese J, McNally EG. Getting to the heel of the problem: plantar fascia lesions. Clin Radiol 2009;64: 931-9.
44. Banse X, Sims TJ, Bailey AJ. Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res 2002;17: 1621-8.
45. Reddy GK. Cross-linking in collagen by nonenzymatic glycation increases the matrix stiffness in rabbit achilles tendon. Exp Diabesity Res 2004;5:143-53.
46. Franco R, Sánchez-Olea R, Reyes-Reyes EM et al. Environmental toxicity, oxidative stress and apoptosis: ménage à trois. Mutat Res 2009;674:3-22.
47. Abate M, Schiavone C, Salini V. Neoangiogenesis is reduced in chronic tendinopathies of type 2 diabetic patients. Int J Immunopathol Pharmacol 2012;25:757-31.
48. Abaci A, Oǧuzhan A, Kahraman S et al. Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation 1999;99:2239-4.
49. Waltenberger J. Impaired collateral vessel development in diabetes: potential cellular mechanisms and therapeutic implications. Cardiovasc Res 2001;49:554-60.
50. Shoji T, Koyama H, Morioka T et al. Receptor for advanced glycation end products is involved in impairedangiogenic response in diabetes. Diabetes 2006;55: 2245-55.
51. Wang SH, Sun ZL, Guo YJ et al. PPARgamma-mediated advanced glycation end products regulation of neural stem cells. Mol Cell Endocrinol 2009;307:176-84.
52. Beeharry D, Coupe B, Benbow EW et al. Familial hypercholesterolaemia commonly presents with Achilles tenosynovitis. Ann Rheum Dis 2006;65:312-5.
53. Tsouli SG, Xydis V, Argyropoulou MI et al. Regression of Achilles tendon thickness after statin treatment in patients with familial hypercholesterolemia: an ultrasonographic study. Atherosclerosis 2009;205:151-5.
54. Choi HK, Mount DB, Reginato AM, Pathogenesis of gout. Ann Intern Med 2005;143:499-516.
55. von Bahr S, Movin T, Papadogiannakis N et al. Mechanism of accumulation of cholesterol and cholestanol in tendons and the role of sterol 27-hydroxylase (CYP27A1). Arterioscler Thromb Vasc Biol 2002;22: 1129-35.
56. Junyent M, Gilabert R, Zambón D et al. The use of Achilles tendon sonography to distinguish familial hypercholesterolemia from other genetic dyslipidemias. Arterioscler Thromb Vasc Biol 2005;25:2203-8.
57. Abboud JA, Kim JS. The effect of hypercholesterolemia on rotator cuff disease. Clin Orthop Relat Res 2010;468: 1493-7.
58. Longo UG, Franceschi F, Spiezia F et al. Triglycerides and total serum cholesterol in rotator cuff tears: do they matter? Br J Sports Med 2010;44:948-51.
59. Siess W. Platelet interaction with bioactive lipids formed by mild oxidation of low-density lipoprotein. Pathophysiol Haemost Thromb 2006;35:292-304.
60. Chen R, Chen X, Salomon RG et al. Platelet activation by low concentrations of intact oxidized LDL particles involves the PAF receptor. Arterioscler Thromb Vasc Biol 2009;29:363-71.
61. Artieda M, Cenarro A, Junquera C et al. Tendon xanthomas in familial hypercholesterolemia are associated with a differential inflammatory response of macrophages to oxidized LDL. FEBS Lett 2005;579: 4503-12.
62. Matsuura F, Hirano K, Koseki M et al. Familial massive tendon xanthomatosis with decreased high-density lipoprotein-mediated cholesterol efflux. Metabolism 2005; 54:1095-101.
63. Oosterveer DM, Versmissen J, Yazdanpanah M et al. The risk of tendon xanthomas in familial hypercholesterolaemia is influenced by variation in genes of the reverse cholesterol transport pathway and the low-density lipoprotein oxidation pathway. Eur Heart J 2010;31: 1007-12.
64. Beason DP, Abboud JA, Kuntz AF et al. Cumulative effects of hypercholesterolemia on tendon biomechanics in a mouse model. J Orthop Res 2011;29: 380-3.
65. Thiele RG, Schlesinger N. Diagnosis of gout by ultrasound. Rheumatology 2007;46:1116-21.
66. Puig JG, de Miguel E, Castillo MC et al. Asymptomatic hyperuricemia: impact of ultrasonography. Nucleosides Nucleotides Nucleic Acids 2008;27:592-5.
67. Schlesinger N, Thiele RG. The pathogenesis of bone erosions in gouty arthritis. Ann Rheum Dis 2010;69: 1907-12.
68. Pinzur M, Freeland R, Juknelis D. The association between body mass index and foot disorders in diabetic patients. Foot Ankle Int 2005;26:375-7.
69. Holmes GB, Lin J. Etiologic factors associated with symptomatic achilles tendinopathy. Foot Ankle Int 2006; 27:952-9.
70. Frey C, Zamora J. The effects of obesity on orthopaedic foot and ankle pathology. Foot Ankle Int 2007;28: 996-9.
71. Wendelboe AM, Hegmann KT, Gren LH et al. Associations between body-mass index and surgery for rotator cuff tendinitis. J Bone Joint Surg Am 2004;86-A:743-7.
72. Warrender WJ, Brown OL, Abboud JA. Outcomes of arthroscopic rotator cuff repairs in obese patients. J Shoulder Elbow Surg 2011;20:961-7.
73. Gaida JE, Alfredson H, Kiss ZS et al. Asymptomatic Achilles tendon pathology is associated with a central fat distribution in men and a peripheral fat distribution in women: a cross sectional study of 298 individuals. BMC Musculoskelet Disord 2010;11:41.
74. Gaida JE, Alfredson L, Kiss ZS et al. Dyslipidemia in Achilles tendinopathy is characteristic of insulin resistance. Med Sci Sports Exerc 2009;41:1194-7.
75. Conde J, Gomez R, Bianco G et al. Expanding the adipokine network in cartilage: identification and regulation of novel factors in human and murine chondrocytes. Ann Rheum Dis 2011;70:551-9.
76. Lago R, Gomez R, Otero M et al. A new player in cartilage homeostasis: adiponectin induces nitric oxide synthase type II and pro-inflammatory cytokines in chondrocytes. Osteoarthritis Cartilage 2008;16:1101-9.
77. Berry PA, Jones SW, Cicuttini FM et al. Temporal relationship between serum adipokines, biomarkers of bone and cartilage turnover, and cartilage volume loss in a population with clinical knee osteoarthritis. Arthritis Rheum 2011;63:700-7.
78. Cilli F, Khan M, Fu F et al. Prostaglandin E2 affects proliferation and collagen synthesis by human patellar tendon fibroblasts. Clin J Sport Med 2004;14: 232-6.
79. Cook JL, Purdam CR. Is tendon pathology a continuum? A pathology model to explain the clinical presentation of load-induced tendinopathy. Br J Sports Med 2009;43: 409-16.
80. Maffulli N, Longo UG, Loppini M et al. Current treatment options for tendinopathy. Expert Opin Pharmacother 2010;11:2177-86.
81. Battery L, Maffulli N. Inflammation in overuse tendon injuries. Sports Med Arthrosc 2011;19:213-7.
82. Scott A, Lian R, Bahr R et al. Increased mast cell numbers in human patellar tendinosis: correlation with symptom duration and vascular hyperplasia. Br J Sports Med 2008; 42:753-7.
83. Biancalana A, Veloso LA, Gomes L. Obesity affects collagen fibril diameter and mechanical properties of tendons in Zucker rats. Connect Tissue Res 2010;51: 171-8.
84. Grosicka A, Kucharz EJ. Alkaptonuria. Wiad Lek 2009;62: 197-203.
85. Manoj Kumar RV, Rajasekaran S. Spontaneous tendon ruptures in alkaptonuria. J Bone Joint Surg Br 2003;85: 883-6.
86. Chua SY, Chang HC. Bilateral spontaneous rupture of the quadriceps tendon as an initial presentation of alkaptonuria-a case report. Knee 2006;13:408-10.
87. Carvès C, Duquenoy A, Toutain F et al. Gouty tendinitis revealing glycogen storage disease Type Ia in two adolescents. Joint Bone Spine 2003;70:149-53.
88. Richard S, Tamas C, Sell DR et al. Tissue-specific effects of aldose reductase inhibition on fluorescence and cross-linking of extracellular matrix in chronic galactosemia. Relationship to pentosidine cross-links. Diabetes 1991;40:1049-56.