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Published in: Knee Surgery, Sports Traumatology, Arthroscopy 1/2018

Open Access 01-01-2018 | Shoulder

More histologic and ultrastructural degenerative signs in the subscapularis tendon and the joint capsule in male patients with shoulder impingement

Authors: Stefanos Farfaras, Lars Erik Ejerhed, Erling K. Hallström, Kjell Hultenby, Khaled Meknas, Tomas Movin, Nikos Papadogiannakis, Jüri-Toomas Kartus

Published in: Knee Surgery, Sports Traumatology, Arthroscopy | Issue 1/2018

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Abstract

Purpose

The purpose of the present study was to analyze biopsy samples from the subscapularis tendon and from the joint capsule from male patients with shoulder impingement syndrome (SAIS) and compare them with samples from male patients with post-traumatic recurrent shoulder instability. The hypothesis of the study was that patients with SAIS would have more histologic and ultrastructural degenerative changes in their subscapularis tendon and joint capsule than patients with post-traumatic recurrent shoulder instability.

Methods

Male patients scheduled for surgery, with either subacromial decompression or Bankart reconstruction, were included. Four biopsies from each patient were obtained from the capsule and four from the subscapularis tendon during arthroscopic surgery. The histologic characteristics and the presence of glycosaminoglycans were assessed using the light microscope, and the ultrastructure was assessed using a transmission electron microscope.

Results

Eight patients, median age 53 (45–74) years (p < 0.0001), were included in the impingement group, and 12 patients, median age 27 (22–48) years, were included in the instability group. The histologic assessment revealed significantly higher cellularity and total degeneration score in the capsule (p = 0.016 and p = 0.014 respectively) in patients with subacromial impingement compared with the instability patients. The corresponding finding was not made for the subscapularis tendon. The ultrastructural evaluation revealed that the instability patients had more fibrils with a large diameter (indicating less degeneration) in both the subscapularis tendon and the capsule compared with the impingement patients (p < 0.0001).

Conclusion

Male patients with subacromial impingement have more histologic and ultrastructural degenerative changes in their shoulder compared with patients with post-traumatic recurrent shoulder instability.

Clinical relevance

It appears that in patients with subacromial impingement, the whole shoulder joint is affected and not only the subacromial space. It is the opinion of the authors that intra-articular therapeutic injections could be tried more often in these patients.

Level of evidence

III.
Literature
1.
go back to reference Ahlen M, Liden M, Movin T, Papadogiannakis N, Rostgard-Christensen L, Kartus J (2014) Histological evaluation of regenerated semitendinosus tendon a minimum of 6 years after harvest for anterior cruciate ligament reconstruction. Orthop J Sports Med 2(9):2325967114550274CrossRefPubMedPubMedCentral Ahlen M, Liden M, Movin T, Papadogiannakis N, Rostgard-Christensen L, Kartus J (2014) Histological evaluation of regenerated semitendinosus tendon a minimum of 6 years after harvest for anterior cruciate ligament reconstruction. Orthop J Sports Med 2(9):2325967114550274CrossRefPubMedPubMedCentral
2.
go back to reference Bot SD, van der Waal JM, Terwee CB, van der Windt DA, Schellevis FG, Bouter LM, Dekker J (2005) Incidence and prevalence of complaints of the neck and upper extremity in general practice. Ann Rheum Dis 64(1):118–123CrossRefPubMedPubMedCentral Bot SD, van der Waal JM, Terwee CB, van der Windt DA, Schellevis FG, Bouter LM, Dekker J (2005) Incidence and prevalence of complaints of the neck and upper extremity in general practice. Ann Rheum Dis 64(1):118–123CrossRefPubMedPubMedCentral
3.
go back to reference Castagna A, Cesari E, Gigante A, Conti M, Garofalo R (2013) Metalloproteases and their inhibitors are altered in both torn and intact rotator cuff tendons. Musculoskelet Surg 97(Suppl 1):39–47CrossRefPubMed Castagna A, Cesari E, Gigante A, Conti M, Garofalo R (2013) Metalloproteases and their inhibitors are altered in both torn and intact rotator cuff tendons. Musculoskelet Surg 97(Suppl 1):39–47CrossRefPubMed
4.
go back to reference Chillemi C, Petrozza V, Garro L, Sardella B, Diotallevi R, Ferrara A, Gigante A, Di Cristofano C, Castagna A, Della Rocca C (2011) Rotator cuff re-tear or non-healing: histopathological aspects and predictive factors. Knee Surg Sports Traumatol Arthrosc 19(9):1588–1596CrossRefPubMed Chillemi C, Petrozza V, Garro L, Sardella B, Diotallevi R, Ferrara A, Gigante A, Di Cristofano C, Castagna A, Della Rocca C (2011) Rotator cuff re-tear or non-healing: histopathological aspects and predictive factors. Knee Surg Sports Traumatol Arthrosc 19(9):1588–1596CrossRefPubMed
5.
go back to reference Cho NS, Hwang JH, Lee YT, Chae SW (2011) Tendinosis-like histologic and molecular changes of the Achilles tendon to repetitive stress: a pilot study in rats. Clin Orthop Relat Res 469(11):3172–3180CrossRefPubMedPubMedCentral Cho NS, Hwang JH, Lee YT, Chae SW (2011) Tendinosis-like histologic and molecular changes of the Achilles tendon to repetitive stress: a pilot study in rats. Clin Orthop Relat Res 469(11):3172–3180CrossRefPubMedPubMedCentral
7.
go back to reference Garofalo R, Cesari E, Vinci E, Castagna A (2011) Role of metalloproteinases in rotator cuff tear. Sports Med Arthrosc 19(3):207–212CrossRefPubMed Garofalo R, Cesari E, Vinci E, Castagna A (2011) Role of metalloproteinases in rotator cuff tear. Sports Med Arthrosc 19(3):207–212CrossRefPubMed
8.
go back to reference Goutallier D, Postel JM, Van Driessche S, Voisin MC (2005) Histological lesions of supraspinatus tendons in full thickness tears of the rotator cuff. Rev Chir Orthop Reparatrice Appar Mot 91(2):109–113CrossRefPubMed Goutallier D, Postel JM, Van Driessche S, Voisin MC (2005) Histological lesions of supraspinatus tendons in full thickness tears of the rotator cuff. Rev Chir Orthop Reparatrice Appar Mot 91(2):109–113CrossRefPubMed
9.
go back to reference Gyftopoulos S, Carpenter E, Kazam J, Babb J, Bencardino J (2012) MR imaging of subscapularis tendon injury in the setting of anterior shoulder dislocation. Skeletal radiol 41(11):1445–1452CrossRefPubMed Gyftopoulos S, Carpenter E, Kazam J, Babb J, Bencardino J (2012) MR imaging of subscapularis tendon injury in the setting of anterior shoulder dislocation. Skeletal radiol 41(11):1445–1452CrossRefPubMed
10.
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
11.
go back to reference Jozsa L, Balint BJ, Reffy A, Demel Z (1984) Fine structural alterations of collagen fibers in degenerative tendinopathy. Arch Orthop Trauma Surg 103(1):47–51CrossRefPubMed Jozsa L, Balint BJ, Reffy A, Demel Z (1984) Fine structural alterations of collagen fibers in degenerative tendinopathy. Arch Orthop Trauma Surg 103(1):47–51CrossRefPubMed
12.
go back to reference Kartus J, Movin T, Papadogiannakis N, Christensen LR, Lindahl S, Karlsson J (2000) A radiographic and histologic evaluation of the patellar tendon after harvesting its central third. Am J Sports Med 28(2):218–226CrossRefPubMed Kartus J, Movin T, Papadogiannakis N, Christensen LR, Lindahl S, Karlsson J (2000) A radiographic and histologic evaluation of the patellar tendon after harvesting its central third. Am J Sports Med 28(2):218–226CrossRefPubMed
13.
go back to reference Liden M, Movin T, Ejerhed L, Papadogiannakis N, Blomen E, Hultenby K, Kartus J (2008) A histological and ultrastructural evaluation of the patellar tendon 10 years after reharvesting its central third. Am J Sports Med 36(4):781–788CrossRefPubMed Liden M, Movin T, Ejerhed L, Papadogiannakis N, Blomen E, Hultenby K, Kartus J (2008) A histological and ultrastructural evaluation of the patellar tendon 10 years after reharvesting its central third. Am J Sports Med 36(4):781–788CrossRefPubMed
14.
go back to reference Linsell L, Dawson J, Zondervan K, Rose P, Randall T, Fitzpatrick R, Carr A (2006) Prevalence and incidence of adults consulting for shoulder conditions in UK primary care; patterns of diagnosis and referral. 45(2):215–221 Linsell L, Dawson J, Zondervan K, Rose P, Randall T, Fitzpatrick R, Carr A (2006) Prevalence and incidence of adults consulting for shoulder conditions in UK primary care; patterns of diagnosis and referral. 45(2):215–221
15.
go back to reference Longo UG, Franceschi F, Ruzzini L, Rabitti C, Morini S, Maffulli N, Denaro V (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, Denaro V (2008) Histopathology of the supraspinatus tendon in rotator cuff tears. Am J Sports Med 36(3):533–538CrossRefPubMed
16.
go back to reference Longo UG, Franceschi F, Ruzzini L, Rabitti C, Morini S, Maffulli N, Forriol F, Denaro V (2007) Light microscopic histology of supraspinatus tendon ruptures. Knee Surg Sports Traumatol Arthrosc 15(11):1390–1394CrossRefPubMed Longo UG, Franceschi F, Ruzzini L, Rabitti C, Morini S, Maffulli N, Forriol F, Denaro V (2007) Light microscopic histology of supraspinatus tendon ruptures. Knee Surg Sports Traumatol Arthrosc 15(11):1390–1394CrossRefPubMed
17.
go back to reference Lundgreen K, Lian OB, Engebretsen L, Scott A (2011) Tenocyte apoptosis in the torn rotator cuff: a primary or secondary pathological event? Br J Sports Med 45 (13):1035–1039CrossRefPubMedPubMedCentral Lundgreen K, Lian OB, Engebretsen L, Scott A (2011) Tenocyte apoptosis in the torn rotator cuff: a primary or secondary pathological event? Br J Sports Med 45 (13):1035–1039CrossRefPubMedPubMedCentral
18.
19.
go back to reference Magnusson SP, Qvortrup K, Larsen JO, Rosager S, Hanson P, Aagaard P, Krogsgaard M, Kjaer M (2002) Collagen fibril size and crimp morphology in ruptured and intact Achilles tendons. Matrix biol 21(4):369–377CrossRefPubMed Magnusson SP, Qvortrup K, Larsen JO, Rosager S, Hanson P, Aagaard P, Krogsgaard M, Kjaer M (2002) Collagen fibril size and crimp morphology in ruptured and intact Achilles tendons. Matrix biol 21(4):369–377CrossRefPubMed
20.
go back to reference Meknas K, Johansen O, Steigen SE, Olsen R, Jorgensen L, Kartus J (2012) Could tendinosis be involved in osteoarthritis? Scand J Med Sci Sports 22(5):627–634CrossRefPubMed Meknas K, Johansen O, Steigen SE, Olsen R, Jorgensen L, Kartus J (2012) Could tendinosis be involved in osteoarthritis? Scand J Med Sci Sports 22(5):627–634CrossRefPubMed
21.
go back to reference Millett PJ, Gobezie R, Boykin RE (2008) Shoulder osteoarthritis: diagnosis and management. Am Fam Physician 78(5):605–611PubMed Millett PJ, Gobezie R, Boykin RE (2008) Shoulder osteoarthritis: diagnosis and management. Am Fam Physician 78(5):605–611PubMed
22.
go back to reference Movin T, Gad A, Reinholt FP, Rolf C (1997) Tendon pathology in long-standing achillodynia. Biopsy findings in 40 patients. Acta Orthop Scand 68(2):170–175CrossRefPubMed Movin T, Gad A, Reinholt FP, Rolf C (1997) Tendon pathology in long-standing achillodynia. Biopsy findings in 40 patients. Acta Orthop Scand 68(2):170–175CrossRefPubMed
23.
go back to reference Pauly S, Stahnke K, Klatte-Schulz F, Wildemann B, Scheibel M, Greiner S (2015) Do patient age and sex influence tendon cell biology and clinical/radiographic outcomes after rotator cuff repair? Am J Sports Med 43(3):549–556CrossRefPubMed Pauly S, Stahnke K, Klatte-Schulz F, Wildemann B, Scheibel M, Greiner S (2015) Do patient age and sex influence tendon cell biology and clinical/radiographic outcomes after rotator cuff repair? Am J Sports Med 43(3):549–556CrossRefPubMed
24.
go back to reference Pingel J, Fredberg U, Qvortrup K, Larsen JO, Schjerling P, Heinemeier K, Kjær M, Langberg H (2012) Local biochemical and morphological differences in human Achilles tendinopathy: a case control study. BMC musculoskelet Disord 13(1):1CrossRef Pingel J, Fredberg U, Qvortrup K, Larsen JO, Schjerling P, Heinemeier K, Kjær M, Langberg H (2012) Local biochemical and morphological differences in human Achilles tendinopathy: a case control study. BMC musculoskelet Disord 13(1):1CrossRef
25.
go back to reference Proctor CS, Jackson DW, Simon TM (1997) Characterization of the repair tissue after removal of the central one-third of the patellar ligament. An experimental study in a goat model. J Bone Jt Surg Am 79(7):997–1006CrossRef Proctor CS, Jackson DW, Simon TM (1997) Characterization of the repair tissue after removal of the central one-third of the patellar ligament. An experimental study in a goat model. J Bone Jt Surg Am 79(7):997–1006CrossRef
26.
go back to reference Rolf C, Movin T (1997) Etiology, histopathology, and outcome of surgery in achillodynia. Foot Ankle Int 18(9):565–569CrossRefPubMed Rolf C, Movin T (1997) Etiology, histopathology, and outcome of surgery in achillodynia. Foot Ankle Int 18(9):565–569CrossRefPubMed
27.
go back to reference Svensson M, Kartus J, Christensen LR, Movin T, Papadogiannakis N, Karlsson J (2005) A long-term serial histological evaluation of the patellar tendon in humans after harvesting its central third. Knee Surg Sports Traumatol Arthrosc 13(5):398–404CrossRefPubMed Svensson M, Kartus J, Christensen LR, Movin T, Papadogiannakis N, Karlsson J (2005) A long-term serial histological evaluation of the patellar tendon in humans after harvesting its central third. Knee Surg Sports Traumatol Arthrosc 13(5):398–404CrossRefPubMed
28.
go back to reference Svensson M, Movin T, Rostgard-Christensen L, Blomen E, Hultenby K, Kartus J (2007) Ultrastructural collagen fibril alterations in the patellar tendon 6 years after harvesting its central third. Am J Sports Med 35(2):301–306CrossRefPubMed Svensson M, Movin T, Rostgard-Christensen L, Blomen E, Hultenby K, Kartus J (2007) Ultrastructural collagen fibril alterations in the patellar tendon 6 years after harvesting its central third. Am J Sports Med 35(2):301–306CrossRefPubMed
29.
go back to reference Takase K, Yamamoto K (2005) Histological and ultrastructural changes in the undersurface of the acromion with subacromial impingement. Acta Orthop 76(3):386–391PubMed Takase K, Yamamoto K (2005) Histological and ultrastructural changes in the undersurface of the acromion with subacromial impingement. Acta Orthop 76(3):386–391PubMed
30.
go back to reference Tallon C, Maffulli N, Ewen SW (2001) Ruptured Achilles tendons are significantly more degenerated than tendinopathic tendons. Med Sci Sports Exerc 33(12):1983–1990CrossRefPubMed Tallon C, Maffulli N, Ewen SW (2001) Ruptured Achilles tendons are significantly more degenerated than tendinopathic tendons. Med Sci Sports Exerc 33(12):1983–1990CrossRefPubMed
31.
go back to reference Taylor W (2005) Musculoskeletal pain in the adult New Zealand population: prevalence and impact. N ZMed J 118(1221):U1629 Taylor W (2005) Musculoskeletal pain in the adult New Zealand population: prevalence and impact. N ZMed J 118(1221):U1629
32.
go back to reference Tillander B, Franzen L, Norlin R (2002) Fibronectin, MMP-1 and histologic changes in rotator cuff disease. J Orthop Res 20(6):1358–1364CrossRefPubMed Tillander B, Franzen L, Norlin R (2002) Fibronectin, MMP-1 and histologic changes in rotator cuff disease. J Orthop Res 20(6):1358–1364CrossRefPubMed
33.
go back to reference Tuoheti Y, Itoi E, Pradhan RL, Wakabayashi I, Takahashi S, Minagawa H, Kobayashi M, Okada K, Shimada Y (2005) Apoptosis in the supraspinatus tendon with stage II subacromial impingement. J Shoulder Elbow Surg 14(5):535–541CrossRefPubMed Tuoheti Y, Itoi E, Pradhan RL, Wakabayashi I, Takahashi S, Minagawa H, Kobayashi M, Okada K, Shimada Y (2005) Apoptosis in the supraspinatus tendon with stage II subacromial impingement. J Shoulder Elbow Surg 14(5):535–541CrossRefPubMed
34.
go back to reference White JJ, Titchener AG, Fakis A, Tambe AA, Hubbard RB, Clark DI (2014) An epidemiological study of rotator cuff pathology using The Health Improvement Network database. Bone Jt 96-b(3):350–353CrossRef White JJ, Titchener AG, Fakis A, Tambe AA, Hubbard RB, Clark DI (2014) An epidemiological study of rotator cuff pathology using The Health Improvement Network database. Bone Jt 96-b(3):350–353CrossRef
35.
go back to reference Yamakado K (2012) Histopathology of residual tendon in high-grade articular-sided partial-thickness rotator cuff tears (PASTA lesions). Arthroscopy 28(4):474–480CrossRefPubMed Yamakado K (2012) Histopathology of residual tendon in high-grade articular-sided partial-thickness rotator cuff tears (PASTA lesions). Arthroscopy 28(4):474–480CrossRefPubMed
36.
go back to reference Yuan J, Murrell GA, Wei AQ, Wang MX (2002) Apoptosis in rotator cuff tendonopathy. J Orthop Res 20(6):1372–1379CrossRefPubMed Yuan J, Murrell GA, Wei AQ, Wang MX (2002) Apoptosis in rotator cuff tendonopathy. J Orthop Res 20(6):1372–1379CrossRefPubMed
Metadata
Title
More histologic and ultrastructural degenerative signs in the subscapularis tendon and the joint capsule in male patients with shoulder impingement
Authors
Stefanos Farfaras
Lars Erik Ejerhed
Erling K. Hallström
Kjell Hultenby
Khaled Meknas
Tomas Movin
Nikos Papadogiannakis
Jüri-Toomas Kartus
Publication date
01-01-2018
Publisher
Springer Berlin Heidelberg
Published in
Knee Surgery, Sports Traumatology, Arthroscopy / Issue 1/2018
Print ISSN: 0942-2056
Electronic ISSN: 1433-7347
DOI
https://doi.org/10.1007/s00167-017-4442-9

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