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Published in: Knee Surgery, Sports Traumatology, Arthroscopy 7/2017

01-07-2017 | Shoulder

Degree of tendon degeneration and stage of rotator cuff disease

Authors: Chris Hyunchul Jo, Won Hyoung Shin, Ji Wan Park, Ji Sun Shin, Ji Eun Kim

Published in: Knee Surgery, Sports Traumatology, Arthroscopy | Issue 7/2017

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Abstract

Purpose

While tendon degeneration has been known to be an important cause of rotator cuff disease, few studies have objectively proven the association of tendon degeneration and rotator cuff disease. The purpose of this study was to investigate changes of tendon degeneration with respect to the stage of rotator cuff disease.

Methods

A total of 48 patients were included in the study: 12 with tendinopathy, 12 with a partial-thickness tear (pRCT), 12 with a full-thickness tear (fRCT), and 12 as the control. A full-thickness supraspinatus tendon sample was harvested en bloc from the middle portion between the lateral edge and the musculotendinous junction of the tendon using a biopsy punch with a diameter of 3 mm. Harvested samples were evaluated using a semi-quantitative grading scale with 7 parameters after haematoxylin and eosin staining.

Results

There was no significant difference in age, gender, symptom duration, and Kellgren-Lawrence grade between the groups except for the global fatty degeneration index. All of the seven parameters were significantly different between the groups and could be categorized as follows: early responders (fibre structure and arrangement), gradual responder (rounding of the nuclei), after-tear responders (cellularity, vascularity, and stainability), and late responder (hyalinization). The total degeneration scores were not significantly different between the control (6.08 ± 1.16) and tendinopathy (6.67 ± 1.83) (n.s.). However, the score of pRCT group (10.42 ± 1.31) was greater than that of tendinopathy (P < 0.001), and so was the score of fRCT (12.33 ± 1.15) than that of pRCT (p = 0.009).

Conclusion

This study showed that the degeneration of supraspinatus tendon increases as the stage of rotator cuff disease progresses from tendinopathy to pRCT, and then to fRCT. The degree of degeneration of tendinopathy was not different from that of normal but aged tendons, and significant tendon degeneration began from the stage of pRCT. The clinical relevance of the study is that strategies and goals of the treatment for rotator cuff disease should be specific to its stage, in order to prevent disease progression for tendinopathy and pRCT, as well to restore the structural integrity for fRCT.

Level of evidence

Diagnostic, Level I.
Literature
1.
go back to reference Arnoczky SP, Lavagnino M, Egerbacher M (2007) The mechanobiological aetiopathogenesis of tendinopathy: is it the over-stimulation or the under-stimulation of tendon cells? Int J Exp Pathol 88(4):217–226CrossRefPubMedPubMedCentral Arnoczky SP, Lavagnino M, Egerbacher M (2007) The mechanobiological aetiopathogenesis of tendinopathy: is it the over-stimulation or the under-stimulation of tendon cells? Int J Exp Pathol 88(4):217–226CrossRefPubMedPubMedCentral
2.
go back to reference Del Buono A, Battery L, Denaro V, Maccauro G, Maffulli N (2011) Tendinopathy and inflammation: some truths. Int J Immunopathol Pharmacol 24(1 Suppl 2):45–50CrossRefPubMed Del Buono A, Battery L, Denaro V, Maccauro G, Maffulli N (2011) Tendinopathy and inflammation: some truths. Int J Immunopathol Pharmacol 24(1 Suppl 2):45–50CrossRefPubMed
3.
go back to reference Ensor KL, Kwon YW, Dibeneditto MR, Zuckerman JD, Rokito AS (2013) The rising incidence of rotator cuff repairs. J Shoulder Elbow Surg 22(12):1628–1632CrossRefPubMed Ensor KL, Kwon YW, Dibeneditto MR, Zuckerman JD, Rokito AS (2013) The rising incidence of rotator cuff repairs. J Shoulder Elbow Surg 22(12):1628–1632CrossRefPubMed
4.
go back to reference Ersen A, Demirhan M, Atalar AC, Kapicioglu M, Baysal G (2014) Platelet-rich plasma for enhancing surgical rotator cuff repair: evaluation and comparison of two application methods in a rat model. Arch Orthop Trauma Surg 134(3):405–411CrossRefPubMed Ersen A, Demirhan M, Atalar AC, Kapicioglu M, Baysal G (2014) Platelet-rich plasma for enhancing surgical rotator cuff repair: evaluation and comparison of two application methods in a rat model. Arch Orthop Trauma Surg 134(3):405–411CrossRefPubMed
5.
go back to reference Harvie P, Ostlere SJ, Teh J, McNally EG, Clipsham K, Burston BJ et al (2004) Genetic influences in the aetiology of tears of the rotator cuff. J Bone Joint Surg 86(5):696–700CrossRef Harvie P, Ostlere SJ, Teh J, McNally EG, Clipsham K, Burston BJ et al (2004) Genetic influences in the aetiology of tears of the rotator cuff. J Bone Joint Surg 86(5):696–700CrossRef
6.
go back to reference Hashimoto T, Nobuhara K, Hamada T (2003) Pathologic evidence of degeneration as a primary cause of rotator cuff tear. Clin Orthop Relat Res 415:111–120CrossRef Hashimoto T, Nobuhara K, Hamada T (2003) Pathologic evidence of degeneration as a primary cause of rotator cuff tear. Clin Orthop Relat Res 415:111–120CrossRef
7.
8.
go back to reference Hermans J, Luime JJ, Meuffels DE, Reijman M, Simel DL, Bierma-Zeinstra SM (2013) Does this patient with shoulder pain have rotator cuff disease?: The Rational Clinical Examination systematic review. JAMA: J Am Med Assoc 310(8):837–847CrossRef Hermans J, Luime JJ, Meuffels DE, Reijman M, Simel DL, Bierma-Zeinstra SM (2013) Does this patient with shoulder pain have rotator cuff disease?: The Rational Clinical Examination systematic review. JAMA: J Am Med Assoc 310(8):837–847CrossRef
9.
go back to reference Jo CH, Chang MS (2015) Degeneration Exists along the Entire Length of the Supraspinatus Tendon in Patients with a Rotator Cuff Tear. Clin Shoulder Elbow 18(2):61–67CrossRef Jo CH, Chang MS (2015) Degeneration Exists along the Entire Length of the Supraspinatus Tendon in Patients with a Rotator Cuff Tear. Clin Shoulder Elbow 18(2):61–67CrossRef
10.
go back to reference Jo CH, Kim JE, Yoon KS, Lee JH, Kang SB, Lee JH et al (2011) Does platelet-rich plasma accelerate recovery after rotator cuff repair? A prospective cohort study. Am J Sports Med 39(10):2082–2090CrossRefPubMed Jo CH, Kim JE, Yoon KS, Lee JH, Kang SB, Lee JH et al (2011) Does platelet-rich plasma accelerate recovery after rotator cuff repair? A prospective cohort study. Am J Sports Med 39(10):2082–2090CrossRefPubMed
11.
go back to reference Jo CH, Yoon KS, Lee JH, Kang SB, Lee JH, Han HS et al (2011) The effect of multiple channeling on the structural integrity of repaired rotator cuff. Knee Surg Sports Traumatol Arthrosc 19(12):2098–2107CrossRefPubMed Jo CH, Yoon KS, Lee JH, Kang SB, Lee JH, Han HS et al (2011) The effect of multiple channeling on the structural integrity of repaired rotator cuff. Knee Surg Sports Traumatol Arthrosc 19(12):2098–2107CrossRefPubMed
12.
go back to reference Jobe FW, Moynes DR (1982) Delineation of diagnostic criteria and a rehabilitation program for rotator cuff injuries. Am J Sports Med 10(6):336–339CrossRefPubMed Jobe FW, Moynes DR (1982) Delineation of diagnostic criteria and a rehabilitation program for rotator cuff injuries. Am J Sports Med 10(6):336–339CrossRefPubMed
13.
go back to reference Kessel L, Watson M (1977) The painful arc syndrome. Clinical classification as a guide to management. J Bone Joint Surg 59(2):166–172 Kessel L, Watson M (1977) The painful arc syndrome. Clinical classification as a guide to management. J Bone Joint Surg 59(2):166–172
14.
go back to reference Khan KM, Bonar F, Desmond PM, Cook JL, Young DA, Visentini PJ et al (1996) Patellar tendinosis (jumper’s knee): findings at histopathologic examination, US, and MR imaging. Victorian Institute of Sport Tendon Study Group. Radiology 200(3):821–827CrossRefPubMed Khan KM, Bonar F, Desmond PM, Cook JL, Young DA, Visentini PJ et al (1996) Patellar tendinosis (jumper’s knee): findings at histopathologic examination, US, and MR imaging. Victorian Institute of Sport Tendon Study Group. Radiology 200(3):821–827CrossRefPubMed
15.
go back to reference Lazarides AL, Alentorn-Geli E, Choi JH, Stuart JJ, Lo IK, Garrigues GE et al (2015) Rotator cuff tears in young patients: a different disease than rotator cuff tears in elderly patients. J Shoulder Elbow Surg 24(11):1834–1843CrossRefPubMed Lazarides AL, Alentorn-Geli E, Choi JH, Stuart JJ, Lo IK, Garrigues GE et al (2015) Rotator cuff tears in young patients: a different disease than rotator cuff tears in elderly patients. J Shoulder Elbow Surg 24(11):1834–1843CrossRefPubMed
16.
go back to reference Lohr JF, Uhthoff HK (1990) The microvascular pattern of the supraspinatus tendon. Clin Orthop Relat Res 254(254):35–38 Lohr JF, Uhthoff HK (1990) The microvascular pattern of the supraspinatus tendon. Clin Orthop Relat Res 254(254):35–38
17.
go back to reference Longo UG, Franceschi F, Ruzzini L, Rabitti C, Morini S, Maffulli N et al (2008) Histopathology of the supraspinatus tendon in rotator cuff tears. Am J Sports Med 36(3):533–538CrossRefPubMed Longo UG, Franceschi F, Ruzzini L, Rabitti C, Morini S, Maffulli N et al (2008) Histopathology of the supraspinatus tendon in rotator cuff tears. Am J Sports Med 36(3):533–538CrossRefPubMed
18.
go back to reference Longo UG, Franceschi F, Ruzzini L, Rabitti C, Morini S, Maffulli N et al (2009) Characteristics at haematoxylin and eosin staining of ruptures of the long head of the biceps tendon. Br J Sports Med 43(8):603–607CrossRefPubMed Longo UG, Franceschi F, Ruzzini L, Rabitti C, Morini S, Maffulli N et al (2009) Characteristics at haematoxylin and eosin staining of ruptures of the long head of the biceps tendon. Br J Sports Med 43(8):603–607CrossRefPubMed
19.
go back to reference Matthews TJ, Hand GC, Rees JL, Athanasou NA, Carr AJ (2006) Pathology of the torn rotator cuff tendon. Reduction in potential for repair as tear size increases. J Bone Joint Surg 88(4):489–495CrossRef Matthews TJ, Hand GC, Rees JL, Athanasou NA, Carr AJ (2006) Pathology of the torn rotator cuff tendon. Reduction in potential for repair as tear size increases. J Bone Joint Surg 88(4):489–495CrossRef
20.
go back to reference McCarrel TM, Minas T, Fortier LA (2012) Optimization of leukocyte concentration in platelet-rich plasma for the treatment of tendinopathy. J Bone Joint Surg Am 94(19):e143CrossRefPubMed McCarrel TM, Minas T, Fortier LA (2012) Optimization of leukocyte concentration in platelet-rich plasma for the treatment of tendinopathy. J Bone Joint Surg Am 94(19):e143CrossRefPubMed
21.
go back to reference McElvany MD, McGoldrick E, Gee AO, Neradilek MB, Matsen FA 3rd (2015) Rotator cuff repair: published evidence on factors associated with repair integrity and clinical outcome. Am J Sports Med 43(2):491–500CrossRefPubMed McElvany MD, McGoldrick E, Gee AO, Neradilek MB, Matsen FA 3rd (2015) Rotator cuff repair: published evidence on factors associated with repair integrity and clinical outcome. Am J Sports Med 43(2):491–500CrossRefPubMed
22.
go back to reference McMaster WC, Troup J (1993) A survey of interfering shoulder pain in United States competitive swimmers. Am J Sports Med 21(1):67–70CrossRefPubMed McMaster WC, Troup J (1993) A survey of interfering shoulder pain in United States competitive swimmers. Am J Sports Med 21(1):67–70CrossRefPubMed
23.
go back to reference Movin T, Guntner P, Gad A, Rolf C (1997) Ultrasonography-guided percutaneous core biopsy in Achilles tendon disorder. Scand J Med Sci Sports 7(4):244–248CrossRefPubMed Movin T, Guntner P, Gad A, Rolf C (1997) Ultrasonography-guided percutaneous core biopsy in Achilles tendon disorder. Scand J Med Sci Sports 7(4):244–248CrossRefPubMed
24.
go back to reference Neer CS 2nd (1972) Anterior acromioplasty for the chronic impingement syndrome in the shoulder: a preliminary report. J Bone Joint Surg Am 54(1):41–50CrossRefPubMed Neer CS 2nd (1972) Anterior acromioplasty for the chronic impingement syndrome in the shoulder: a preliminary report. J Bone Joint Surg Am 54(1):41–50CrossRefPubMed
25.
go back to reference Neer CS 2nd (1983) Impingement lesions. Clin Orthop Relat Res 173(173):70–77 Neer CS 2nd (1983) Impingement lesions. Clin Orthop Relat Res 173(173):70–77
26.
go back to reference Oh LS, Wolf BR, Hall MP, Levy BA, Marx RG (2007) Indications for rotator cuff repair: a systematic review. Clin Orthop Relat Res 455:52–63CrossRefPubMed Oh LS, Wolf BR, Hall MP, Levy BA, Marx RG (2007) Indications for rotator cuff repair: a systematic review. Clin Orthop Relat Res 455:52–63CrossRefPubMed
27.
go back to reference Papadonikolakis A, McKenna M, Warme W, Martin BI, Matsen FA 3rd (2011) Published evidence relevant to the diagnosis of impingement syndrome of the shoulder. J Bone Joint Surg Am 93(19):1827–1832CrossRefPubMed Papadonikolakis A, McKenna M, Warme W, Martin BI, Matsen FA 3rd (2011) Published evidence relevant to the diagnosis of impingement syndrome of the shoulder. J Bone Joint Surg Am 93(19):1827–1832CrossRefPubMed
28.
go back to reference Rees JD, Wilson AM, Wolman RL (2006) Current concepts in the management of tendon disorders. Rheumatology 45(5):508–521CrossRefPubMed Rees JD, Wilson AM, Wolman RL (2006) Current concepts in the management of tendon disorders. Rheumatology 45(5):508–521CrossRefPubMed
29.
go back to reference Riley G (2008) Tendinopathy–from basic science to treatment. Nat Clin Pract Rheumatol 4(2):82–89CrossRefPubMed Riley G (2008) Tendinopathy–from basic science to treatment. Nat Clin Pract Rheumatol 4(2):82–89CrossRefPubMed
30.
go back to reference Sano H, Ishii H, Trudel G, Uhthoff HK (1999) Histologic evidence of degeneration at the insertion of 3 rotator cuff tendons: a comparative study with human cadaveric shoulders. J Shoulder Elbow Surg 8(6):574–579CrossRefPubMed Sano H, Ishii H, Trudel G, Uhthoff HK (1999) Histologic evidence of degeneration at the insertion of 3 rotator cuff tendons: a comparative study with human cadaveric shoulders. J Shoulder Elbow Surg 8(6):574–579CrossRefPubMed
31.
go back to reference Sundman EA, Cole BJ, Fortier LA (2011) Growth factor and catabolic cytokine concentrations are influenced by the cellular composition of platelet-rich plasma. Am J Sports Med 39(10):2135–2140CrossRefPubMed Sundman EA, Cole BJ, Fortier LA (2011) Growth factor and catabolic cytokine concentrations are influenced by the cellular composition of platelet-rich plasma. Am J Sports Med 39(10):2135–2140CrossRefPubMed
32.
go back to reference Tilley JM, Murphy RJ, Chaudhury S, Czernuszka JT, Carr AJ (2014) Effect of tear size, corticosteroids and subacromial decompression surgery on the hierarchical structural properties of torn supraspinatus tendons. Bone Joint Res 3(8):252–261CrossRefPubMedPubMedCentral Tilley JM, Murphy RJ, Chaudhury S, Czernuszka JT, Carr AJ (2014) Effect of tear size, corticosteroids and subacromial decompression surgery on the hierarchical structural properties of torn supraspinatus tendons. Bone Joint Res 3(8):252–261CrossRefPubMedPubMedCentral
33.
go back to reference van der Windt DA, Koes BW, Boeke AJ, Deville W, De Jong BA, Bouter LM (1996) Shoulder disorders in general practice: prognostic indicators of outcome. Br J Gen Pract: J R Coll Gen Pract 46(410):519–523 van der Windt DA, Koes BW, Boeke AJ, Deville W, De Jong BA, Bouter LM (1996) Shoulder disorders in general practice: prognostic indicators of outcome. Br J Gen Pract: J R Coll Gen Pract 46(410):519–523
34.
go back to reference Via AG, De Cupis M, Spoliti M, Oliva F (2013) Clinical and biological aspects of rotator cuff tears. Muscles Ligaments Tendons J 3(2):70–79PubMed Via AG, De Cupis M, Spoliti M, Oliva F (2013) Clinical and biological aspects of rotator cuff tears. Muscles Ligaments Tendons J 3(2):70–79PubMed
35.
go back to reference Watson EM, Sonnabend DH (2002) Outcome of rotator cuff repair. J Shoulder Elbow Surg 11(3):201–211CrossRefPubMed Watson EM, Sonnabend DH (2002) Outcome of rotator cuff repair. J Shoulder Elbow Surg 11(3):201–211CrossRefPubMed
36.
go back to reference Yadav H, Nho S, Romeo A, MacGillivray JD (2009) Rotator cuff tears: pathology and repair. Knee Surg Sports Traumatol Arthrosc 17(4):409–421CrossRefPubMed Yadav H, Nho S, Romeo A, MacGillivray JD (2009) Rotator cuff tears: pathology and repair. Knee Surg Sports Traumatol Arthrosc 17(4):409–421CrossRefPubMed
37.
go back to reference 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(8):1699–1704PubMed 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(8):1699–1704PubMed
38.
go back to reference Yamamoto A, Takagishi K, Osawa T, Yanagawa T, Nakajima D, Shitara H et al (2010) Prevalence and risk factors of a rotator cuff tear in the general population. J Shoulder Elbow Surg 19(1):116–120CrossRefPubMed Yamamoto A, Takagishi K, Osawa T, Yanagawa T, Nakajima D, Shitara H et al (2010) Prevalence and risk factors of a rotator cuff tear in the general population. J Shoulder Elbow Surg 19(1):116–120CrossRefPubMed
Metadata
Title
Degree of tendon degeneration and stage of rotator cuff disease
Authors
Chris Hyunchul Jo
Won Hyoung Shin
Ji Wan Park
Ji Sun Shin
Ji Eun Kim
Publication date
01-07-2017
Publisher
Springer Berlin Heidelberg
Published in
Knee Surgery, Sports Traumatology, Arthroscopy / Issue 7/2017
Print ISSN: 0942-2056
Electronic ISSN: 1433-7347
DOI
https://doi.org/10.1007/s00167-016-4376-7

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