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Knee Surgery, Sports Traumatology, Arthroscopy
Published in: Knee Surgery, Sports Traumatology, Arthroscopy 10/2011

01-10-2011 | Shoulder

Expression of matrix metalloproteinases 1, 3, and 9 in differing extents of tendon retraction in the torn rotator cuff

Authors: Stefan Lakemeier, Juliane Braun, Turgay Efe, Christian Foelsch, Eleni Archontidou-Aprin, Susanne Fuchs-Winkelmann, Juergen R. J. Paletta, Markus D. Schofer

Published in: Knee Surgery, Sports Traumatology, Arthroscopy | Issue 10/2011

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Abstract

Purpose

Differing extents of tendon retraction are found in full-thickness rotator cuff tears. The pathophysiologic context of tendon degeneration and the extent of tendon retraction are unclear. Tendon integrity depends on the extracellular matrix, which is regulated by matrix metalloproteinases (MMP). It is unknown which enzymes play a role in tendon degeneration. The hypotheses are that (1) the expression of MMPs 1, 3, and 9 is altered in the torn rotator cuff when compared with healthy tendon samples; and (2) that there is a relationship between MMP expression and the extent of tendon retraction in the torn cuff.

Methods

Rotator cuff tendon samples of 33 patients with full-thickness rotator cuff tears (Bateman grade III) were harvested during reconstructive surgery. Samples were dehydrated and paraffin-embedded. Immunohistologic determination of MMP 1, 3, and 9 expression was performed by staining sample slices with MMP antibody. The extent of tendon retraction was determined intraoperatively according to Patte’s classification and patients were assigned to 4 groups (control group, and by tendon retraction grade Patte I-III). The control group consisted of six healthy tendon samples.

Results

Expression of MMPs 1 and 9 was significantly higher in torn cuff samples than in healthy tendons whereas MMP 3 expression was significantly decreased (P < 0.05). MMP 9 expression significantly increased with rising extent of tendon retraction in the torn cuff (P < 0.05). No significant association was found between expression of MMPs 1 and 3 and the rising extent of tendon retraction by Patte’s classification.

Conclusion

Elevated expression of MMPs 1 and 9 as well as decreased MMP 3 expression can be detected in torn rotator cuff tendon tissue. There is a significant association between the extent of tendon retraction and MMP 9 expression. The results of this study give evidence that early surgical treatment of small and partial-thickness rotator cuff tears is required.
Literature
1.
Alfredson H (2005) The chronic painful Achilles and patellar tendon: research on basic biology and treatment. Scand J Med Sci Sports 15:252–259PubMedCrossRef
2.
Andarawis-Puri N, Ricchetti ET, Soslowsky LJ (2009) Rotator cuff tendon strain correlates with tear propagation. J Biomech 42:158–163PubMedCrossRef
3.
Asundi KR, Rempel DM (2008) Cyclic loading inhibits expression of MMP-3 but not MMP-1 in an in vitro rabbit flexor tendon model. Clin Biomech (Bristol, Avon) 23:117–121CrossRef
4.
Bateman JE (1963) The diagnosis and treatment of ruptures of the rotator cuff. Surg Clin North Am 43:1523–1530PubMed
5.
Bedi A, Fox AJ, Kovacevic D, Deng XH, Warren RF, Rodeo SA (2010) Doxycycline-mediated inhibition of matrix metalloproteinases improves healing after rotator cuff repair. Am J Sports Med 38:308–317PubMedCrossRef
6.
Budoff JE, Rodin D, Ochiai D, Nirschl RP (2005) Arthroscopic rotator cuff debridement without decompression for the treatment of tendinosis. Arthroscopy 21:1081–1089PubMedCrossRef
7.
Chong AK, Ang AD, Goh JC, Hui JH, Lim AY, Lee EH, Lim BH (2007) Bone marrow-derived mesenchymal stem cells influence early tendon-healing in a rabbit achilles tendon model. J Bone Joint Surg Am 89:74–81PubMedCrossRef
8.
Dudhia J, Scott CM, Draper ER, Heinegard D, Pitsillides AA, Smith RK (2007) Aging enhances a mechanically-induced reduction in tendon strength by an active process involving matrix metalloproteinase activity. Aging Cell 6:547–556PubMedCrossRef
9.
Fu SC, Chan BP, Wang W, Pau HM, Chan KM, Rolf CG (2002) Increased expression of matrix metalloproteinase 1 (MMP1) in 11 patients with patellar tendinosis. Acta Orthop Scand 73:658–662PubMedCrossRef
10.
Fuchs S, Skwara A, Bloch M, Dankbar B (2004) Differential induction and regulation of matrix metalloproteinases in osteoarthritic tissue and fluid synovial fibroblasts. Osteoarthr Cartil 12:409–418PubMedCrossRef
11.
Gohlke F (1993) Ultrasonographic appearance of the rotator cuff in elderly subjects. Orthopade 22:288–293PubMed
12.
Gulotta LV, Kovacevic D, Montgomery S, Ehteshami JR, Packer JD, Rodeo SA (2010) Stem cells genetically modified with the developmental gene MT1-MMP improve regeneration of the supraspinatus tendon-to-bone insertion site. Am J Sports Med 38:1429–1437PubMedCrossRef
13.
Gwilym SE, Watkins B, Cooper CD, Harvie P, Auplish S, Pollard TC, Rees JL, Carr AJ (2009) Genetic influences in the progression of tears of the rotator cuff. J Bone Joint Surg Br 91:915–917PubMedCrossRef
14.
Ireland D, Harrall R, Curry V, Holloway G, Hackney R, Hazleman B, Riley G (2001) Multiple changes in gene expression in chronic human Achilles tendinopathy. Matrix Biol 20:159–169PubMedCrossRef
15.
Irie T, Takahata M, Majima T, Abe Y, Komatsu M, Iwasaki N, Minami A (2010) Effect of selective estrogen receptor modulator/raloxifene analogue on proliferation and collagen metabolism of tendon fibroblast. Connect Tissue Res 51:179–187PubMedCrossRef
16.
Jones GC, Corps AN, Pennington CJ, Clark IM, Edwards DR, Bradley MM, Hazleman BL, Riley GP (2006) Expression profiling of metalloproteinases and tissue inhibitors of metalloproteinases in normal and degenerate human achilles tendon. Arthritis Rheum 54:832–842PubMedCrossRef
17.
Karaoglu S, Celik C, Korkusuz P (2009) The effects of bone marrow or periosteum on tendon-to-bone tunnel healing in a rabbit model. Knee Surg Sports Traumatol Arthrosc 17:170–178PubMedCrossRef
18.
Kjaer M (2004) Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84:649–698PubMedCrossRef
19.
Lehmann LJ, Schollmeyer A, Stoeve J, Scharf HP (2009) Biochemical analysis of the synovial fluid of the shoulder joint in patients with and without rotator cuff tears. Z Orthop Unfall 148:90–94PubMedCrossRef
20.
21.
Lewis JS (2009) Rotator cuff tendinopathy/subacromial impingement syndrome: is it time for a new method of assessment? Br J Sports Med 43:259–264PubMedCrossRef
22.
Lewis JS, Sandford FM (2009) Rotator cuff tendinopathy: is there a role for polyunsaturated fatty acids and antioxidants? J Hand Ther 22:49–55 quiz 56PubMedCrossRef
23.
Liu X, Han Q, Sun R, Li Z (2008) Dexamethasone regulation of matrix metalloproteinase expression in experimental pneumococcal meningitis. Brain Res 1207:237–243PubMedCrossRef
24.
Lo IK, Marchuk LL, Hollinshead R, Hart DA, Frank CB (2004) Matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase mRNA levels are specifically altered in torn rotator cuff tendons. Am J Sports Med 32:1223–1229PubMedCrossRef
25.
Lohr JF, Uhthoff HK (1990) The microvascular pattern of the supraspinatus tendon. Clin Orthop Relat Res 254:35–38PubMed
26.
Matsui Y, Maeda M, Nakagami W, Iwata H (1998) The involvement of matrix metalloproteinases and inflammation in lumbar disc herniation. Spine (Phila Pa 1976) 23:863–868 discussion 868-869CrossRef
27.
Neer CS II (1972) Anterior acromioplasty for the chronic impingement syndrome in the shoulder: a preliminary report. J Bone Joint Surg Am 54:41–50PubMed
28.
Nho SJ, Yadav H, Shindle MK, Macgillivray JD (2008) Rotator cuff degeneration: etiology and pathogenesis. Am J Sports Med 36:987–993PubMedCrossRef
29.
Pasternak B, Aspenberg P (2009) Metalloproteinases and their inhibitors-diagnostic and therapeutic opportunities in orthopedics. Acta Orthop 80:693–703PubMedCrossRef
30.
Patte D (1990) Classification of rotator cuff lesions. Clin Orthop Relat Res 254:81–86PubMed
31.
Pauly S, Klatte F, Strobel C, Schmidmaier G, Greiner S, Scheibel M, Wildemann B (2010) Characterization of tendon cell cultures of the human rotator cuff. Eur Cell Mater 20:84–97PubMed
32.
Perry SM, Getz CL, Soslowsky LJ (2009) After rotator cuff tears, the remaining (intact) tendons are mechanically altered. J Shoulder Elbow Surg 18:52–57PubMedCrossRef
33.
Raleigh SM, van der Merwe L, Ribbans WJ, Smith RK, Schwellnus MP, Collins M (2009) Variants within the MMP3 gene are associated with Achilles tendinopathy: possible interaction with the COL5A1 gene. Br J Sports Med 43:514–520PubMedCrossRef
34.
Riley G (2004) The pathogenesis of tendinopathy. A molecular perspective. Rheumatology (Oxford) 43:131–142CrossRef
35.
36.
Riley GP (2005) Gene expression and matrix turnover in overused and damaged tendons. Scand J Med Sci Sports 15:241–251PubMedCrossRef
37.
Schofer MD, Quante M, Peterlein CD, Timmesfeld N, Phan K, Fuchs-Winkelmann S (2009) Operative and follow-up treatment of rotator cuff tears–the current situation. Z Orthop Unfall 147:321–326PubMedCrossRef
38.
Tajana MS, Murena L, Valli F, Passi A, Grassi FA (2009) Correlations between biochemical markers in the synovial fluid and severity of rotator cuff disease. Chir Organi Mov 93(Suppl 1):S41–S48PubMed
39.
Tondreau T, Meuleman N, Stamatopoulos B, De Bruyn C, Delforge A, Dejeneffe M, Martiat P, Bron D, Lagneaux L (2009) In vitro study of matrix metalloproteinase/tissue inhibitor of metalloproteinase production by mesenchymal stromal cells in response to inflammatory cytokines: the role of their migration in injured tissues. Cytotherapy 11:559–569PubMedCrossRef
40.
Tsai WC, Hsu CC, Chang HN, Lin YC, Lin MS, Pang JH (2010) Ibuprofen upregulates expressions of matrix metalloproteinase-1, -8, -9, and -13 without affecting expressions of types I and III collagen in tendon cells. J Orthop Res 28:487–491PubMed
41.
Voloshin I, Gelinas J, Maloney MD, O’Keefe RJ, Bigliani LU, Blaine TA (2005) Proinflammatory cytokines and metalloproteases are expressed in the subacromial bursa in patients with rotator cuff disease. Arthroscopy 21:1076PubMed
42.
Yamaguchi K, Ditsios K, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA (2006) The demographic and morphological features of rotator cuff disease. A comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am 88:1699–1704PubMedCrossRef
43.
Yoshihara Y, Hamada K, Nakajima T, Fujikawa K, Fukuda H (2001) Biochemical markers in the synovial fluid of glenohumeral joints from patients with rotator cuff tear. J Orthop Res 19:573–579PubMedCrossRef
Metadata
Title
Expression of matrix metalloproteinases 1, 3, and 9 in differing extents of tendon retraction in the torn rotator cuff
Authors
Stefan Lakemeier
Juliane Braun
Turgay Efe
Christian Foelsch
Eleni Archontidou-Aprin
Susanne Fuchs-Winkelmann
Juergen R. J. Paletta
Markus D. Schofer
Publication date
01-10-2011
Publisher
Springer-Verlag
Published in
Knee Surgery, Sports Traumatology, Arthroscopy / Issue 10/2011
Print ISSN: 0942-2056
Electronic ISSN: 1433-7347
DOI
https://doi.org/10.1007/s00167-010-1367-y

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