The peripheral neuronal phenotype is important in the pathogenesis of painful human tendinopathy: A systematic review

Clinical Orthopaedics and Related Research

Volumn 471, Issue 9, 2013, Pages 3036-3046

  Dean, Benjamin John Floyd ^a   Franklin, Sarah L ^a   Carr, Andrew Jonathan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; CALCITONIN GENE RELATED PEPTIDE; CANNABINOID 1 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NEUROPEPTIDE Y; SUBSTANCE P; TYROSINE 3 MONOOXYGENASE;

CELL DENSITY; CELL TYPE; DISEASE ASSOCIATION; GLUTAMINERGIC SYSTEM; HISTOPATHOLOGY; HUMAN; MOLECULAR PATHOLOGY; MONOAMINERGIC SYSTEM; NERVE GROWTH; NERVOUS SYSTEM; NEUROPATHOLOGY; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; ROTATOR CUFF INJURY; SHOULDER PAIN; SYMPTOMATOLOGY; SYSTEMATIC REVIEW; TENDINITIS; TENOCYTE; UPREGULATION;

EID: 84881664371     PISSN: 0009921X     EISSN: 15281132     Source Type: Journal    
DOI: 10.1007/s11999-013-3010-y     Document Type: Review

References (68)

1. Ackermann PW, Li J, Lundeberg T, Kreicbergs A. Neuronal plasticity in relation to nociception and healing of rat achilles tendon. J Orthop Res. 2003;21:432-441.
2. Ackermann PW, Salo PT, Hart DA. Neuronal pathways in tendon healing. Front Biosci. 2009;14:5165-5187.
3. Alfredson H, Forsgren S, Thorsen K, Fahlstrom M, Johansson H, Lorentzon R. Glutamate NMDAR1 receptors localised to nerves in human Achilles tendons. Implications for treatment? Knee Surg Sports Traumatol Arthrosc. 2001;9:123-126.
4. Alfredson H, Forsgren S, Thorsen K, Lorentzon R. In vivo microdialysis and immunohistochemical analyses of tendon tissue demonstrated high amounts of free glutamate and glutamate NMDAR1 receptors, but no signs of inflammation, in Jumper's knee. J Orthop Res. 2001;19:881-886.
5. Alfredson H, Ljung BO, Thorsen K, Lorentzon R. In vivo investigation of ECRB tendons with microdialysis technique - no signs of inflammation but high amounts of glutamate in tennis elbow. Acta Orthop Scand. 2000;71:475-479.
6. Alfredson H, Ohberg L, Forsgren S. Is vasculo-neural ingrowth the cause of pain in chronic Achilles tendinosis? An investigation using ultrasonography and colour Doppler, immunohistochemistry, and diagnostic injections. Knee Surg Sports Traumatol Arthrosc. 2003;11:334-338.
7. Alfredson H, Thorsen K, Lorentzon R. In situ microdialysis in tendon tissue: high levels of glutamate, but not prostaglandin E2 in chronic Achilles tendon pain. Knee Surg Sports Traumatol Arthrosc. 1999;7:378-381.
8. Andersson G, Backman LJ, Scott A, Lorentzon R, Forsgren S, Danielson P. Substance P accelerates hypercellularity and angiogenesis in tendon tissue and enhances paratendinitis in response to Achilles tendon overuse in a tendinopathy model. Br J Sports Med. 2011;45:1017-1022.
9. Andersson G, Danielson P, Alfredson H, Forsgren S. Presence of substance P and the neurokinin-1 receptor in tenocytes of the human Achilles tendon. Regul Pept. 2008;150:81-87.
10. Backman LJ, Andersson G, Wennstig G, Forsgren S, Danielson P. Endogenous substance P production in the Achilles tendon increases with loading in an in vivo model of tendinopathy-peptidergic elevation preceding tendinosis-like tissue changes. J Musculoskelet Neuronal Interact. 2011;11:133-140.
11. Backman LJ, Fong G, Andersson G, Scott A, Danielson P. Substance P is a mechanoresponsive, autocrine regulator of human tenocyte proliferation. PloS One. 2011;6:e27209.
12. Bagge J, Danielson P, Forsgren S. In situ hybridization studies favouring the occurrence of a local production of BDNF in the human Achilles tendon. Histol Histopathol. 2012;27:1239-1246.
13. Bagge J, Lorentzon R, Alfredson H, Forsgren S. 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;24:839-848.
14. Bjorklund E, Forsgren S, Alfredson H, Fowler CJ. Increased expression of cannabinoid CB(1) receptors in Achilles tendinosis. PloS One. 2011;6:e24731.
15. Bjur D, Alfredson H, Forsgren S. Presence of the neuropeptide Y1 receptor in tenocytes and blood vessel walls in the human Achilles tendon. Br J Sports Med. 2009;43:1136-1142.
16. Bjur D, Danielson P, Alfredson H, Forsgren S. Immunohistochemical and in situ hybridization observations favor a local catecholamine production in the human Achilles tendon. Histol Histopathol. 2008;23:197-208.
17. Bjur D, Danielson P, Alfredson H, Forsgren S. Presence of a non-neuronal cholinergic system and occurrence of up- and down-regulation in expression of M2 muscarinic acetylcholine receptors: new aspects of importance regarding Achilles tendon tendinosis (tendinopathy). Cell Tissue Res. 2008;331:385-400.
18. Bleakman D, Alt A, Nisenbaum ES. Glutamate receptors and pain. Semin Cell Dev Biol. 2006;17:592-604.
19. Carlsson O, Schizas N, Li J, Ackermann PW. Substance P injections enhance tissue proliferation and regulate sensory nerve ingrowth in rat tendon repair. Scand J Med Sci Sports. 2011;21:562-569.
20. Chaudhury S, Gwilym SE, Moser J, Carr AJ. Surgical options for patients with shoulder pain. Nat Rev Rheumatol. 2010;6:217-226.
21. Cochrane. Cochrane Handbook for Systematic Reviews of Interventions. Available at: http://www.cochrane.org/training/cochrane-handbook. Accessed March 2013.
22. Cook JL, Feller JA, Bonar SF, Khan KM. Abnormal tenocyte morphology is more prevalent than collagen disruption in asymptomatic athletes' patellar tendons. J Orthop Res. 2004;22:334-338.
23. Danielson P, Alfredson H, Forsgren S. Immunohistochemical and histochemical findings favoring the occurrence of autocrine/paracrine as well as nerve-related cholinergic effects in chronic painful patellar tendon tendinosis. Microsc Res Tech. 2006;69:808-819.
24. Danielson P, Alfredson H, Forsgren S. In situ hybridization studies confirming recent findings of the existence of a local nonneuronal catecholamine production in human patellar tendinosis. Microsc Res Tech. 2007;70:908-911.
25. Danielson P, Andersson G, Alfredson H, Forsgren S. Extensive expression of markers for acetylcholine synthesis and of M2 receptors in tenocytes in therapy-resistant chronic painful patellar tendon tendinosis - a pilot study. Life Sci. 2007;80:2235-2238.
26. de Jonge S, van den Berg C, de Vos RJ, van der Heide HJ, Weir A, Verhaar JA, Bierma-Zeinstra SM, Tol JL. Incidence of midportion Achilles tendinopathy in the general population. Br J Sports Med. 2011;45:1026-1028.
27. Dean BJ, Gwilym SE, Carr AJ. Why does my shoulder hurt? A review of the neuroanatomical and biochemical basis of shoulder pain. Br J Sports Med. 2013 Feb 21 [Epub ahead of print].
28. Dean BJF, Franklin SL, Carr AJ. A systematic review of the histological and molecular changes in rotator cuff disease. Bone Joint Res. 2012;1:158-166.
29. Forsgren S, Danielson P, Alfredson H. Vascular NK-1 receptor occurrence in normal and chronic painful Achilles and patellar tendons: studies on chemically unfixed as well as fixed specimens. Regulat Pept. 2005;126:173-181.
30. Fredberg U, Stengaard-Pedersen K. Chronic tendinopathy tissue pathology, pain mechanisms, and etiology with a special focus on inflammation. Scand J Med Sci Sports. 2008;18:3-15.
31. Freemont AJ, Peacock TE, Goupille P, Hoyland JA, O'Brien J, Jayson MI. Nerve ingrowth into diseased intervertebral disc in chronic back pain. Lancet. 1997;350:178-181.
32. Gangadharan V, Wang R, Ulzhofer B, Luo C, Bardoni R, Bali KK, Agarwal N, Tegeder I, Hildebrandt U, Nagy GG, Todd AJ, Ghirri A, Haussler A, Sprengel R, Seeburg PH, MacDermott AB, Lewin GR, Kuner R. Peripheral calcium-permeable AMPA receptors regulate chronic inflammatory pain in mice. J Clin Invest. 2011;121:1608-1623.
33. Ghilardi JR, Freeman KT, Jimenez-Andrade JM, Coughlin KA, Kaczmarska MJ, Castaneda-Corral G, Bloom AP, Kuskowski MA, Mantyh PW. Neuroplasticity of sensory and sympathetic nerve fibers in a mouse model of a painful arthritic joint. Arthritis Rheum. 2012;64:2223-2232.
34. Gotoh M, Hamada K, Yamakawa H, Inoue A, Fukuda H. Increased substance P in subacromial bursa and shoulder pain in rotator cuff diseases. J Orthop Res. 1998;16:618-621.
35. Gwilym SE, Oag HC, Tracey I, Carr AJ. Evidence that central sensitisation is present in patients with shoulder impingement syndrome and influences the outcome after surgery. J Bone Joint Surg Br. 2011;93:498-502.
36. Hegedus EJ, Cook C, Brennan M, Wyland D, Garrison JC, Driesner D. Vascularity and tendon pathology in the rotator cuff: a review of literature and implications for rehabilitation and surgery. Br J Sports Med. 2010;44:838-847.
37. Ivie TJ, Bray RC, Salo PT. Denervation impairs healing of the rabbit medial collateral ligament. J Orthop Res. 2002;20:990-995.
38. Kemp KA, Sheps DM, Luciak-Corea C, Styles-Tripp F, Buckingham J, Beaupre LA. Systematic review of rotator cuff tears in workers' compensation patients. Occup Med (Lond). 2011;61:556-562.
39. Kreiner F, Galbo H. Elevated muscle interstitial levels of pain-inducing substances in symptomatic muscles in patients with polymyalgia rheumatica. Pain. 2011;152:1127-1132.
40. Lewis JS. Rotator cuff tendinopathy. Br J Sports Med. 2009;43:236-241.
41. Li J, Kreicbergs A, Bergstrom J, Stark A, Ahmed M. Site-specific CGRP innervation coincides with bone formation during fracture healing and modeling: a study in rat angulated tibia. J Orthop Res. 2007;25:1204-1212.
42. Lian O, Dahl J, Ackermann PW, Frihagen F, Engebretsen L, Bahr R. Pronociceptive and antinociceptive neuromediators in patellar tendinopathy. Am J Sports Med. 2006;34:1801-1808.
43. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700.
44. Longo UG, Ronga M, Maffulli N. Achilles tendinopathy. Sports Med Arthrosc Rev. 2009;17:112-126.
45. Lui PP, Chan LS, Fu SC, Chan KM. Expression of sensory neuropeptides in tendon is associated with failed healing and activity-related tendon pain in collagenase-induced tendon injury. Am J Sports Med. 2010;38:757-764.
46. Maffulli N, Longo UG, Franceschi F, Rabitti C, Denaro V. Movin and Bonar scores assess the same characteristics of tendon histology. Clin Orthop Relat Res. 2008;466:1605-1611.
47. Neer CS 2nd. Impingement lesions. Clin Orthop Relat Res. 1983;173:70-77.
48. Neviaser A, Andarawis-Puri N, Flatow E. Basic mechanisms of tendon fatigue damage. J Shoulder Elbow Surg. 2012;21:158-163.
49. Newsholme P, Procopio J, Lima MM, Pithon-Curi TC, Curi R. Glutamine and glutamate - their central role in cell metabolism and function. Cell Biochem Funct. 2003;21:1-9.
50. Orita S, Koshi T, Mitsuka T, Miyagi M, Inoue G, Arai G, Ishikawa T, Hanaoka E, Yamashita K, Yamashita M, Eguchi Y, Toyone T, Takahashi K, Ohtori S. Associations between proinflammatory cytokines in the synovial fluid and radiographic grading and pain-related scores in 47 consecutive patients with osteoarthritis of the knee. BMC Musculoskelet Disord. 2011;12:144.
51. Riley G. The pathogenesis of tendinopathy. A molecular perspective. Rheumatol ogy (Oxford). 2004;43:131-142.
52. Rosendal L, Larsson B, Kristiansen J, Peolsson M, Sogaard K, Kjaer M, Sorensen J, Gerdle B. Increase in muscle nociceptive substances and anaerobic metabolism in patients with trapezius myalgia: microdialysis in rest and during exercise. Pain. 2004;112:324-334.
53. Schizas N, Lian O, Frihagen F, Engebretsen L, Bahr R, Ackermann PW. Coexistence of up-regulated NMDA receptor 1 and glutamate on nerves, vessels and transformed tenocytes in tendinopathy. Scand J Med Sci Sports. 2010;20:208-215.
54. Schizas N, Weiss R, Lian O, Frihagen F, Bahr R, Ackermann PW. Glutamate receptors in tendinopathic patients. J Orthop Res. 2012;30:1447-1452.
55. Schubert TE, Weidler C, Lerch K, Hofstadter F, Straub RH. Achilles tendinosis is associated with sprouting of substance P positive nerve fibres. Ann Rheum Dis. 2005;64:1083-1086.
56. Scott A, Alfredson H, Forsgren S. VGIuT2 expression in painful achilles and patellar tendinosis: evidence of local glutamate release by tenocytes. J Orthop Res. 2008;26:685-692.
57. Seitz AL, McClure PW, Finucane S, Boardman ND III, Michener LA. Mechanisms of rotator cuff tendinopathy: intrinsic, extrinsic, or both? Clin Biomech. 2011;26:1-12.
58. Singaraju VM, Kang RW, Yanke AB, McNickle AG, Lewis PB, Wang VM, Williams JM, Chubinskaya S, Romeo AA, Cole BJ. Biceps tendinitis in chronic rotator cuff tears: a histologic perspective. J Shoulder Elbow Surg. 2008;17:898-904.
59. Tamai M, Okajima S, Fushiki S, Hirasawa Y. Quantitative analysis of neural distribution in human coracoacromial ligaments. Clin Orthop Relat Res. 2000;373:125-134.
60. Tashjian RZ. Epidemiology, natural history, and indications for treatment of rotator cuff tears. Clin Sports Med. 2012;31:589-604.
61. Tomita Y, Ozaki J, Sakurai G, Kondo T, Nakagaki K, Tamai S. Neurohistology of the subacromial bursa in rotator cuff tear. J Orthop Sci. 1997;2:295-300.
62. Wilson JJ, Best TM. Common overuse tendon problems: a review and recommendations for treatment. Am Fam Physician. 2005;72:811-818.
63. Woolf CJ, Costigan M. Transcriptional and posttranslational plasticity and the generation of inflammatory pain. Proc Natl Acad Sci U S A. 1999;96:7723-7730.
64. Xu Y, Bonar F, Murrell GA. Neoinnervation in rotator cuff tendinopathy. Sports Med Arthrosc Rev. 2011;19:354-359.
65. Xu Y, Murrell GA. The basic science of tendinopathy. Clin Orthop Relat Res. 2008;466:1528-1538.
66. Yamaguchi K DK, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA. The demographic and morphological features of rotator cuff disease. A comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am. 2006;88:1699-1704.
67. Yilmaz Z, Renton T, Yiangou Y, Zakrzewska J, Chessell IP, Bountra C, Anand P. Burning mouth syndrome as a trigeminal small fibre neuropathy: increased heat and capsaicin receptor TRPV1 in nerve fibres correlates with pain score. J Clin Neurosci. 2007;14:864-871.
68. Zeisig E, Ljung BO, Alfredson H, Danielson P. Immunohistochemical evidence of local production of catecholamines in cells of the muscle origins at the lateral and medial humeral epicondyles: of importance for the development of tennis and golfer's elbow? Br J Sports Med. 2009;43:269-275.