Migration of Mesenchymal Stem Cells of Bursal Tissue after Rotator Cuff Repair in RatsFunding All the authors report grants from Munich Working Group for sponsorship of orthopaedic and trauma surgery research, during the conduct of the study. This study was funded by the Munich Working Group for sponsorship of orthopaedic and trauma surgery research at the Ludwig-Maximilian-University e.V (Münchner Arbeitsgemeinschaft zur Förderung der Orthopädischen und Unfallchirurgischen Forschung an der LMU e.V [MAOUF], a nonprofit organization) 2014.
22 October 2017
04 February 2018
13 March 2018 (eFirst)
Purpose The purpose of this study is to verify migration of mesenchymal stem cells of bursal tissue into the healing site after rotator cuff repair in rats.
Methods Fischer rats and green fluorescent protein (GFP)-transgenic rats were used. Bursal tissue from GFP rats was isolated and transplanted into tendon repair sites in Fischer rats. We examined the histology of the rotator cuff and the proportion of GFP-positive cells in the repaired rotator cuff 1, 3, and 6 weeks after surgery.
Results Cell migration was observed during the third and sixth week after surgery. We also found mesenchymal stem cells and formed bursal cluster patterns in the repaired rotator cuff tendons.
Conclusion Mesenchymal stem cells migrated from bursal tissue and infiltrated the repaired rotator cuff tendons.
Clinical Relevance Mesenchymal stem cells from bursal tissue can contribute to the healing progress of the repaired rotator cuff.
* Both the authors contributed equally to this article.
- 1 Denaro V, Ruzzini L, Longo UG. , et al. Effect of dihydrotestosterone on cultured human tenocytes from intact supraspinatus tendon. Knee Surg Sports Traumatol Arthrosc 2010; 18 (07) 971-976
- 2 Ficklscherer A, Loitsch T, Serr M. , et al. Does footprint preparation influence tendon-to-bone healing after rotator cuff repair in an animal model?. Arthroscopy 2014; 30 (02) 188-194
- 3 Ficklscherer A, Scharf M, Hartl TK. , et al. Tissue characteristics in tendon-to-bone healing change after rotator cuff repair using botulinumneurotoxin A for temporary paralysis of the supraspinatus muscle in rats. Connect Tissue Res 2014; 55 (02) 140-146
- 4 Franceschi F, Longo UG, Ruzzini L. , et al. Circulating substance P levels and shoulder joint contracture after arthroscopic repair of the rotator cuff. Br J Sports Med 2008; 42 (09) 742-745
- 5 Galatz LM, Ball CM, Teefey SA, Middleton WD, Yamaguchi K. The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears. J Bone Joint Surg Am 2004; 86-A (02) 219-224
- 6 Bishop J, Klepps S, Lo IK, Bird J, Gladstone JN, Flatow EL. Cuff integrity after arthroscopic versus open rotator cuff repair: a prospective study. J Shoulder Elbow Surg 2006; 15 (03) 290-299
- 7 Ficklscherer A, Hartl TK, Scharf M. , et al. Effects of selective paralysis of the supraspinatus muscle using botulinum neurotoxin a in rotator cuff healing in rats. J Orthop Res 2013; 31 (05) 716-723
- 8 Fuchs B, Gilbart MK, Hodler J, Gerber C. Clinical and structural results of open repair of an isolated one-tendon tear of the rotator cuff. J Bone Joint Surg Am 2006; 88 (02) 309-316
- 9 Jost B, Zumstein M, Pfirrmann CW, Gerber C. Long-term outcome after structural failure of rotator cuff repairs. J Bone Joint Surg Am 2006; 88 (03) 472-479
- 10 Meyer M, Klouche S, Rousselin B, Boru B, Bauer T, Hardy P. Does arthroscopic rotator cuff repair actually heal? Anatomic evaluation with magnetic resonance arthrography at minimum 2 years follow-up. J Shoulder Elbow Surg 2012; 21 (04) 531-536
- 11 Hettrich CM, Rodeo SA, Hannafin JA, Ehteshami J, Shubin Stein BE. The effect of muscle paralysis using Botox on the healing of tendon to bone in a rat model. J Shoulder Elbow Surg 2011; 20 (05) 688-697
- 12 Longo UG, Berton A, Papapietro N, Maffulli N, Denaro V. Biomechanics of the rotator cuff: European perspective. Med Sport Sci 2012; 57: 10-17
- 13 Cheung EV, Silverio L, Sperling JW. Strategies in biologic augmentation of rotator cuff repair: a review. Clin Orthop Relat Res 2010; 468 (06) 1476-1484
- 14 Nourissat G, Diop A, Maurel N. , et al. Mesenchymal stem cell therapy regenerates the native bone-tendon junction after surgical repair in a degenerative rat model. PLoS One 2010; 5 (08) e12248
- 15 Rodeo SA, Potter HG, Kawamura S, Turner AS, Kim HJ, Atkinson BL. Biologic augmentation of rotator cuff tendon-healing with use of a mixture of osteoinductive growth factors. J Bone Joint Surg Am 2007; 89 (11) 2485-2497
- 16 Uhthoff HK, Sarkar K. Surgical repair of rotator cuff ruptures. The importance of the subacromial bursa. J Bone Joint Surg Br 1991; 73 (03) 399-401
- 17 Utsunomiya H, Uchida S, Sekiya I, Sakai A, Moridera K, Nakamura T. Isolation and characterization of human mesenchymal stem cells derived from shoulder tissues involved in rotator cuff tears. Am J Sports Med 2013; 41 (03) 657-668
- 18 Soslowsky LJ, Carpenter JE, DeBano CM, Banerji I, Moalli MR. Development and use of an animal model for investigations on rotator cuff disease. J Shoulder Elbow Surg 1996; 5 (05) 383-392
- 19 Derwin KA, Baker AR, Iannotti JP, McCarron JA. Preclinical models for translating regenerative medicine therapies for rotator cuff repair. Tissue Eng Part B Rev 2010; 16 (01) 21-30
- 20 Ackermann PW, Spetea M, Nylander I, Ploj K, Ahmed M, Kreicbergs A. An opioid system in connective tissue: a study of Achilles tendon in the rat. J Histochem Cytochem 2001; 49 (11) 1387-1395
- 21 Franchi M, Fini M, Quaranta M. , et al. Crimp morphology in relaxed and stretched rat Achilles tendon. J Anat 2007; 210 (01) 1-7
- 22 Rufai A, Ralphs JR, Benjamin M. Ultrastructure of fibrocartilages at the insertion of the rat Achilles tendon. J Anat 1996; 189 (Pt 1): 185-191
- 23 Kida Y, Morihara T, Matsuda K. , et al. Bone marrow-derived cells from the footprint infiltrate into the repaired rotator cuff. J Shoulder Elbow Surg 2013; 22 (02) 197-205
- 24 Koike Y, Trudel G, Uhthoff HK. Formation of a new enthesis after attachment of the supraspinatus tendon: a quantitative histologic study in rabbits. J Orthop Res 2005; 23 (06) 1433-1440
- 25 Iwata Y, Morihara T, Tachiiri H. , et al. Behavior of host and graft cells in the early remodeling process of rotator cuff defects in a transgenic animal model. J Shoulder Elbow Surg 2008; 17 (1, Suppl): 101S-107S
- 26 Kobayashi M, Watanabe N, Oshima Y, Kajikawa Y, Kawata M, Kubo T. The fate of host and graft cells in early healing of bone tunnel after tendon graft. Am J Sports Med 2005; 33 (12) 1892-1897
- 27 Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. ‘Green mice’ as a source of ubiquitous green cells. FEBS Lett 1997; 407 (03) 313-319
- 28 Daher RJ, Chahine NO, Razzano P, Patwa SA, Sgaglione NJ, Grande DA. Tendon repair augmented with a novel circulating stem cell population. Int J Clin Exp Med 2011; 4 (03) 214-219
- 29 Gulotta LV, Kovacevic D, Ehteshami JR, Dagher E, Packer JD, Rodeo SA. Application of bone marrow-derived mesenchymal stem cells in a rotator cuff repair model. Am J Sports Med 2009; 37 (11) 2126-2133
- 30 Randelli PS, Arrigoni P, Cabitza P, Volpi P, Maffulli N. Autologous platelet rich plasma for arthroscopic rotator cuff repair. A pilot study. Disabil Rehabil 2008; 30 (20-22): 1584-1589