Glucocorticoids induce specific ion-channel-mediated toxicity in human rotator cuff tendon: A mechanism underpinning the ultimately deleterious effect of steroid injection in tendinopathy?

British Journal of Sports Medicine

Volumn 48, Issue 22, 2014, Pages 1620-1626

  Dean, Benjamin John Floyd ^a   Franklin, Sarah Louise ^a   Murphy, Richard J ^a   Javaid, Muhammad K ^a   Carr, Andrew Jonathan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; GLUCOCORTICOID; GLUTAMIC ACID; GRIN1 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; METHYLPREDNISOLONE; METHYLPREDNISOLONE ACETATE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE PROTEIN;

ADULT; AGED; ANALOGS AND DERIVATIVES; ATHLETIC INJURIES; CASE CONTROL STUDY; CELL PROLIFERATION; CHEMICALLY INDUCED; ENDOSCOPIC ECHOGRAPHY; FEMALE; HUMAN; IMAGE GUIDED BIOPSY; IMMUNOHISTOCHEMISTRY; INJURIES; INTRAARTICULAR DRUG ADMINISTRATION; MALE; METABOLISM; MIDDLE AGED; OBSERVER VARIATION; PATHOLOGY; PHYSIOLOGY; ROTATOR CUFF; SHOULDER PAIN; SURGERY; TENDINITIS; TENDON INJURIES; WOUND HEALING;

ADULT; AGED; ANTI-INFLAMMATORY AGENTS; ATHLETIC INJURIES; CASE-CONTROL STUDIES; CELL PROLIFERATION; FEMALE; GLUCOCORTICOIDS; GLUTAMIC ACID; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMAGE-GUIDED BIOPSY; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRA-ARTICULAR; MALE; METHYLPREDNISOLONE; MIDDLE AGED; NERVE TISSUE PROTEINS; OBSERVER VARIATION; RECEPTORS, N-METHYL-D-ASPARTATE; ROTATOR CUFF; SHOULDER PAIN; TENDINOPATHY; TENDON INJURIES; ULTRASONOGRAPHY, INTERVENTIONAL; WOUND HEALING;

EID: 84911806219     PISSN: 03063674     EISSN: 14730480     Source Type: Journal    
DOI: 10.1136/bjsports-2013-093178     Document Type: Article

References (53)

1. Chaudhury S, Gwilym SE, Moser J, et al. Surgical options for patients with shoulder pain. Nat Rev Rheumatol 2010;6:217-26.
2. Dean BJF, Franklin SL, Carr AJ. A systematic review of the histological and molecular changes in rotator cuff disease. Bone Joint Res 2012;1:158-66.
3. Dean BJ, Franklin SL, Carr AJ. The peripheral neuronal phenotype is important in the pathogenesis of painful human tendinopathy: a systematic review. Clin Orthop Relat Res 2013;471:3036-46.
4. Authority NBS. Electronic Prescribing & Financial Information for Practices (EPFIP). http://wwwnhsbsanhsuk/PrescriptionServices/963aspx, 2009.
5. Molloy TJ, Kemp MW, Wang Y, et al. Microarray analysis of the tendinopathic rat supraspinatus tendon: glutamate signaling and its potential role in tendon degeneration. J Appl Physiol 2006;101:1702-9.
6. Stromberg BV, Wood FM, Simmons DJ. Enzymatic changes in the healing rat Achilles tendon. J Surg Rre 1977;23:132-40.
7. Greve K, Domeij-Arverud E, Labruto F, et al. Metabolic activity in early tendon repair can be enhanced by intermittent pneumatic compression. Scand J Med Sci Sports 2012;22:e55-63.
8. Post M, Silver R, Singh M. Rotator cuff tear. Diagnosis and treatment. Clin Orthop Relat Res 1983:78-91.
9. Dawson J, Fitzpatrick R, Carr A. Questionnaire on the perceptions of patients about shoulder surgery. J Bone Joint Surg Br Vol 1996;78:593-600.
10. Murphy RJ, Floyd Dean BJ, Wheway K, et al. A novel minimally invasive ultrasound-guided technique to biopsy supraspinatus tendon. Oper Tech Orthop 2013;23:56-62.
11. Ruifrok AC, Johnston DA. Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 2001;23:291-9.
12. Napolitano LA, Grant RM, Deeks SG, et al. Increased production of IL-7 accompanies HIV-1-mediated T-cell depletion: implications for T-cell homeostasis. Nat Med 2001;7:73-9.
13. Brey EM, Lalani Z, Johnston C, et al. Automated selection of DAB-labeled tissue for immunohistochemical quantification. J Histochem Cytochem 2003;51:575-84.
14. Safadi RA, Musleh AS, Al-Khateeb TH, et al. Analysis of immunohistochemical expression of k19 in oral epithelial dysplasia and oral squamous cell carcinoma using color deconvolution-image analysis method. Head Neck Pathol 2010;4:282-9.
15. Rizzardi AE, Johnson AT, Vogel RI, et al. Quantitative comparison of immunohistochemical staining measured by digital image analysis versus pathologist visual scoring. Diagn Pathol 2012;7:42.
16. van Diest PJ, van Dam P, Henzen-Logmans SC, et al. A scoring system for immunohistochemical staining: consensus report of the task force for basic research of the EORTC-GCCG. European organization for research and treatment of cancer-gynaecological cancer cooperative group. J Clin Pathol 1997;50:801-4.
17. Coombes BK, Bisset L, Brooks P, et al. Effect of corticosteroid injection, physiotherapy, or both on clinical outcomes in patients with unilateral lateral epicondylalgia: a randomized controlled trial. JAMA 2013;309:461-9.
18. Buchbinder R, Green S, Youd JM. Corticosteroid injections for shoulder pain. Cochrane Database Syst Rev 2003(1):CD004016.
19. Coombes BK, Bisset L, Vicenzino B. Efficacy and safety of corticosteroid injections and other injections for management of tendinopathy: a systematic review of randomised controlled trials. Lancet 2010;376:1751-67.
20. Barnes PJ. Corticosteroid effects on cell signalling. Eur Respir J 2006;27:413-26.
21. Lannan EA, Galliher-Beckley AJ, Scoltock AB, et al. Proinflammatory actions of glucocorticoids: glucocorticoids and TNFalpha coregulate gene expression in vitro and in vivo. Endocrinology 2012;153:3701-12.
22. Dean BJ, Lostis E, Oakley T, et al. The risks and benefits of glucocorticoid treatment for tendinopathy: a systematic review of the effects of local glucocorticoid on tendon. Semin Arthritis Rheum 2013;43:570-6.
23. Lee SK, Ling CM. The response of human tendon to hydrocortisone injection. Singapore Med J 1975;16:259-62.
24. Poulsen RC, Watts AC, Murphy RJ, et al. Glucocorticoids induce senescence in primary human tenocytes by inhibition of sirtuin 1 and activation of the p53/p21 pathway: in vivo and in vitro evidence. Ann Rheum Dis 2013.
25. Jacobs CM, Trinh MD, Rootwelt T, et al. Dexamethasone induces cell death which may be blocked by NMDA receptor antagonists but is insensitive to Mg2+ in cerebellar granule neurons. Brain Res 2006;1070:116-23.
26. Jing H, Iwasaki Y, Nishiyama M, et al. Multisignal regulation of the rat NMDA1 receptor subunit gene - a pivotal role of glucocorticoid-dependent transcription. Life Sci 2008;82:1137-41.
27. Moghaddam B, Bolinao ML, Stein-Behrens B, et al. Glucocorticoids mediate the stress-induced extracellular accumulation of glutamate. Brain Res 1994;655:251-4.
28. Bose R, Moors M, Tofighi R, et al. Glucocorticoids induce long-lasting effects in neural stem cells resulting in senescence-related alterations. Cell Death Dis 2010;1:e92.
29. Sakhi S, Bruce A, Sun N, et al. Induction of tumor suppressor p53 and DNA fragmentation in organotypic hippocampal cultures following excitotoxin treatment. Exp Neurol 1997;145:81-8.
30. Marsolais D, Cote CH, Frenette J. Pifithrin-alpha, an inhibitor of p53 transactivation, alters the inflammatory process and delays tendon healing following acute injury. Am J Physiol Regul Integr Comp Physiol 2007;292:R321-7.
31. Zaman K, Ryu H, Hall D, et al. Protection from oxidative stress-induced apoptosis in cortical neuronal cultures by iron chelators is associated with enhanced DNA binding of hypoxia-inducible factor-1 and ATF-1/CREB and increased expression of glycolytic enzymes, p21(waf1/cip1), and erythropoietin. J Neurosci 1999;19:9821-30.
32. Newsholme P, Procopio J, Lima MM, et al. Glutamine and glutamate-their central role in cell metabolism and function. Cell Biochem Funct 2003;21:1-9.
33. Choi DW. Excitotoxic cell death. J Neurobiol 1992;23:1261-76.
34. Sattler R, Tymianski M. Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Molr Neurobiol 2001;24:107-29.
35. Alfredson H, Lorentzon R. Intratendinous glutamate levels and eccentric training in chronic Achilles tendinosis: a prospective study using microdialysis technique. Knee Surg Sports Traumatol Arthrosc 2003;11:196-9.
36. Rosendal L, Larsson B, Kristiansen J, et al. Increase in muscle nociceptive substances and anaerobic metabolism in patients with trapezius myalgia: microdialysis in rest and during exercise. Pain 2004;112:324-34.
37. Flodgren GM, Crenshaw AG, Alfredson H, et al. Glutamate and prostaglandin E2 in the trapezius muscle of female subjects with chronic muscle pain and controls determined by microdialysis. Eur J Pain 2005;9:511-15.
38. Bleakman D, Alt A, Nisenbaum ES. Glutamate receptors and pain. Sem Cell Dev Biol 2006;17:592-604.
39. Rechardt M, Shiri R, Karppinen J, et al. Lifestyle and metabolic factors in relation to shoulder pain and rotator cuff tendinitis: a population-based study. BMC Musculoskelet Disord 2010;11:165.
40. Tashjian RZ. Epidemiology, natural history, and indications for treatment of rotator cuff tears. Clin Sports Med 2012;31:589-604.
41. Salminen A, Kaarniranta K, Kauppinen A. Crosstalk between oxidative stress and SIRT1: impact on the aging process. Int J Mol Sci 2013;14:3834-59.
42. Massudi H, Grant R, Braidy N, et al. Age-associated changes in oxidative stress and NAD+ metabolism in human tissue. PLoS ONE 2012;7:e42357.
43. Kluger R, Bock P, Mittlbock M, et al. Long-term survivorship of rotator cuff repairs using ultrasound and magnetic resonance imaging analysis. Am J Sports Med 2011;39:2071-81.
44. Bartl C, Kouloumentas P, Holzapfel K, et al. Long-term outcome and structural integrity following open repair of massive rotator cuff tears. Int J Shoulder Surg 2012;6:1-8.
45. Vastamaki M, Lohman M, Borgmastars N. Rotator cuff integrity correlates with clinical and functional results at a minimum 16 years after open repair. Clin Orthop Relat Res 2013;471:554-61.
46. Sharma P, Maffulli N. Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact 2006;6:181-90.
47. Ackermann PW, Li J, Lundeberg T, et al. Neuronal plasticity in relation to nociception and healing of rat Achilles tendon. J Orthop Res 2003;21:432-41.
48. Iwanaga T, Shikichi M, Kitamura H, et al. Morphology and functional roles of synoviocytes in the joint. Arch Histol Cytol 2000;63:17-31.
49. Akishima-Fukasawa Y, Ino Y, Nakanishi Y, et al. Significance of PGP9.5 expression in cancer-associated fibroblasts for prognosis of colorectal carcinoma. Am J Clin Pathol 2010;134:71-9.
50. Asanome A, Kawabe JI, Matsuki M, et al. Nerve growth factor stimulates regeneration of perivascular nerve, and induces the maturation of microvessels around the injured artery. Biochem Biophys Res Commun 2014;443:150-5.
51. Bagge J, Lorentzon R, Alfredson H, et al. Unexpected presence of the neurotrophins NGF and BDNF and the neurotrophin receptor p75 in the tendon cells of the human Achilles tendon. Histol Histopathol 2009;24:839-48.
52. Im MJ, Freshwater MF, Hoopes JE. Enzyme activities in granulation tissue: energy for collagen synthesis. J Surg Res 1976;20:121-5.
53. Hunt TK, Conolly WB, Aronson SB, et al. Anaerobic metabolism and wound healing: an hypothesis for the initiation and cessation of collagen synthesis in wounds. Am J Surg 1978;135:328-32.