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Published in: Journal of Orthopaedic Surgery and Research 1/2015

Open Access 01-12-2015 | Research article

Efficacy of supraspinatus tendon repair using mesenchymal stem cells along with a collagen I scaffold

Authors: Pilar Tornero-Esteban, José Antonio Hoyas, Esther Villafuertes, Cruz Rodríguez-Bobada, Yamila López-Gordillo, Francisco J. Rojo, Gustavo V. Guinea, Anna Paleczny, Yaiza Lópiz-Morales, Luis Rodriguez-Rodriguez, Fernando Marco, Benjamín Fernández-Gutiérrez

Published in: Journal of Orthopaedic Surgery and Research | Issue 1/2015

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Abstract

Objectives

Our main objective was to biologically improve rotator cuff healing in an elderly rat model using mesenchymal stem cells (MSCs) in combination with a collagen membrane and compared against other current techniques.

Methods

A chronic rotator cuff tear injury model was developed by unilaterally detaching the supraspinatus (SP) tendons of Sprague-Dawley rats. At 1 month postinjury, the tears were repaired using one of the following techniques: (a) classical surgery using sutures (n = 12), (b) type I collagen membranes (n = 15), and (c) type I collagen membranes + 1 × 106 allogeneic MSCs (n = 14). Lesion restoration was evaluated at 1, 2, and 3 months postinjury based on biomechanical criteria. Continuous variables were described using mean and standard deviation (SD). To analyse the effect of the different surgical treatments in the repaired tendons’ biomechanical capabilities (maximum load, stiffness, and deformity), a two-way ANOVA model was used, introducing an interaction between such factor and time (1, 2, and 3 months postinjury).

Results

With regard to maximum load, we observed an almost significant interaction between treatment and time (F = 2.62, df = 4, p = 0.053). When we analysed how this biomechanical capability changed with time for each treatment, we observed that repair with OrthADAPT and MSCs was associated with a significant increase in maximum load (p = 0.04) between months 1 and 3. On the other hand, when we compared the different treatments among themselves at different time points, we observed that the repair with OrthADAPT and MSCs has associated with a significant higher maximum load, when compared with the use of suture, but only at 3 months (p = 0.014). With regard to stiffness and deformity, no significant interaction was observed (F = 1.68, df = 4, p = 0.18; F = 0.40, df = 4, p = 0.81; respectively).

Conclusions

The implantation of MSCs along with a collagen I scaffold into surgically created tendon defects is safe and effective. MSCs improved the tendon’s maximum load over time, indicating that MSCs could help facilitate the dynamic process of tendon repair.
Literature
1.
go back to reference 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;15:290–9.CrossRefPubMed 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;15:290–9.CrossRefPubMed
2.
go back to reference Galatz LM, Griggs S, Cameron BD, Iannotti JP. Prospective longitudinal analysis of postoperative shoulder function: a ten-year follow-up study of full-thickness rotator cuff tears. J Bone Joint Surg Am. 2001;83:1052–6.PubMed Galatz LM, Griggs S, Cameron BD, Iannotti JP. Prospective longitudinal analysis of postoperative shoulder function: a ten-year follow-up study of full-thickness rotator cuff tears. J Bone Joint Surg Am. 2001;83:1052–6.PubMed
3.
go back to reference Bjornsson HC, Norlin R, Johansson K, Adolfsson LE. The influence of age, delay of repair, and tendon involvement in acute rotator cuff tears: structural and clinical outcomes after repair of 42 shoulders. Acta Orthop. 2011;82:187–92.PubMedCentralCrossRefPubMed Bjornsson HC, Norlin R, Johansson K, Adolfsson LE. The influence of age, delay of repair, and tendon involvement in acute rotator cuff tears: structural and clinical outcomes after repair of 42 shoulders. Acta Orthop. 2011;82:187–92.PubMedCentralCrossRefPubMed
4.
go back to reference Saupe N, Pfirrmann CW, Schmid MR, Jost B, Werner CM, Zanetti M. Association between rotator cuff abnormalities and reduced acromiohumeral distance. AJR Am J Roentgenol. 2006;187:376–82.CrossRefPubMed Saupe N, Pfirrmann CW, Schmid MR, Jost B, Werner CM, Zanetti M. Association between rotator cuff abnormalities and reduced acromiohumeral distance. AJR Am J Roentgenol. 2006;187:376–82.CrossRefPubMed
5.
go back to reference Goutallier D, Postel JM, Gleyze P, Leguilloux P, Van Driessche S. Influence of cuff muscle fatty degeneration on anatomic and functional outcomes after simple suture of full-thickness tears. J Shoulder Elbow Surg. 2003;12:550–4.CrossRefPubMed Goutallier D, Postel JM, Gleyze P, Leguilloux P, Van Driessche S. Influence of cuff muscle fatty degeneration on anatomic and functional outcomes after simple suture of full-thickness tears. J Shoulder Elbow Surg. 2003;12:550–4.CrossRefPubMed
6.
go back to reference Cofield RH, Parvizi J, Hoffmeyer PJ, Lanzer WL, Ilstrup DM, Rowland CM. Surgical repair of chronic rotator cuff tears. A prospective long-term study. J Bone Joint Surg Am. 2001;83-A:71–7.PubMed Cofield RH, Parvizi J, Hoffmeyer PJ, Lanzer WL, Ilstrup DM, Rowland CM. Surgical repair of chronic rotator cuff tears. A prospective long-term study. J Bone Joint Surg Am. 2001;83-A:71–7.PubMed
7.
go back to reference Bartolozzi A, Andreychik D, Ahmad S. Determinants of outcome in the treatment of rotator cuff disease. Clin Orthop Relat Res. 1994;308:90–7.PubMed Bartolozzi A, Andreychik D, Ahmad S. Determinants of outcome in the treatment of rotator cuff disease. Clin Orthop Relat Res. 1994;308:90–7.PubMed
8.
go back to reference Hersche O, Gerber C. Passive tension in the supraspinatus musculotendinous unit after long-standing rupture of its tendon: a preliminary report. J Shoulder Elbow Surg. 1998;7:393–6.CrossRefPubMed Hersche O, Gerber C. Passive tension in the supraspinatus musculotendinous unit after long-standing rupture of its tendon: a preliminary report. J Shoulder Elbow Surg. 1998;7:393–6.CrossRefPubMed
9.
go back to reference Gimbel JA, Van Kleunen JP, Lake SP, Williams GR, Soslowsky LJ. The role of repair tension on tendon to bone healing in an animal model of chronic rotator cuff tears. J Biomech. 2007;40:561–8.CrossRefPubMed Gimbel JA, Van Kleunen JP, Lake SP, Williams GR, Soslowsky LJ. The role of repair tension on tendon to bone healing in an animal model of chronic rotator cuff tears. J Biomech. 2007;40:561–8.CrossRefPubMed
10.
go back to reference Nourissat G, Diop A, Maurel N, Salvat C, Dumont S, Pigenet A, et al. Mesenchymal stem cell therapy regenerates the native bone-tendon junction after surgical repair in a degenerative rat model. PLoS One. 2010;5, e12248.PubMedCentralCrossRefPubMed Nourissat G, Diop A, Maurel N, Salvat C, Dumont S, Pigenet A, et al. Mesenchymal stem cell therapy regenerates the native bone-tendon junction after surgical repair in a degenerative rat model. PLoS One. 2010;5, e12248.PubMedCentralCrossRefPubMed
11.
go back to reference Kim SH, Chung SW, Oh JH. Expression of insulin-like growth factor type 1 receptor and myosin heavy chain in rabbit’s rotator cuff muscle after injection of adipose-derived stem cell. Knee Surg Sports Traumatol Arthrosc 2013 Jun 5. [Epub ahead of print] Kim SH, Chung SW, Oh JH. Expression of insulin-like growth factor type 1 receptor and myosin heavy chain in rabbit’s rotator cuff muscle after injection of adipose-derived stem cell. Knee Surg Sports Traumatol Arthrosc 2013 Jun 5. [Epub ahead of print]
12.
go back to reference Oliva F, Osti L, Padulo J, Maffulli N. Epidemiology of the rotator cuff tears: a new incidence related to thyroid disease. Muscles Ligaments Tendons J. 2014;4(3):309–14. eCollection 2014.PubMedCentralPubMed Oliva F, Osti L, Padulo J, Maffulli N. Epidemiology of the rotator cuff tears: a new incidence related to thyroid disease. Muscles Ligaments Tendons J. 2014;4(3):309–14. eCollection 2014.PubMedCentralPubMed
13.
go back to reference Manning CN, Kim HM, Sakiyama-Elbert S, Galatz LM, Havlioglu N, Thomopoulos S. Sustained delivery of transforming growth factor beta three enhances tendon-to-bone healing in a rat model. J Orthop Res. 2011;29:1099–105.CrossRefPubMed Manning CN, Kim HM, Sakiyama-Elbert S, Galatz LM, Havlioglu N, Thomopoulos S. Sustained delivery of transforming growth factor beta three enhances tendon-to-bone healing in a rat model. J Orthop Res. 2011;29:1099–105.CrossRefPubMed
14.
go back to reference Gulotta LV, Kovacevic D, Packer JD, Deng XH, Rodeo SA. Bone marrow-derived mesenchymal stem cells transduced with scleraxis improve rotator cuff healing in a rat model. Am J Sports Med. 2011;39:1282–9.CrossRefPubMed Gulotta LV, Kovacevic D, Packer JD, Deng XH, Rodeo SA. Bone marrow-derived mesenchymal stem cells transduced with scleraxis improve rotator cuff healing in a rat model. Am J Sports Med. 2011;39:1282–9.CrossRefPubMed
15.
go back to reference Longo UG, Lamberti A, Petrillo S, Maffulli N, Denaro V. Scaffolds in tendon tissue engineering. Stem Cells Int. 2012;2012:517165.PubMedCentralPubMed Longo UG, Lamberti A, Petrillo S, Maffulli N, Denaro V. Scaffolds in tendon tissue engineering. Stem Cells Int. 2012;2012:517165.PubMedCentralPubMed
16.
go back to reference Santoni BG, McGilvray KC, Lyons AS, Bansal M, Turner AS, Macgillivray JD, et al. Biomechanical analysis of an ovine rotator cuff repair via porous patch augmentation in a chronic rupture model. Am J Sports Med. 2010;38:679–86.CrossRefPubMed Santoni BG, McGilvray KC, Lyons AS, Bansal M, Turner AS, Macgillivray JD, et al. Biomechanical analysis of an ovine rotator cuff repair via porous patch augmentation in a chronic rupture model. Am J Sports Med. 2010;38:679–86.CrossRefPubMed
17.
go back to reference Plate JF, Brown PJ, Walters J, Clark JA, Smith TL, Freehill MT, et al. Advanced age diminishes tendon-to-bone healing in a rat model of rotator cuff repair. Am J Sports Med. 2014;42:859–68.CrossRefPubMed Plate JF, Brown PJ, Walters J, Clark JA, Smith TL, Freehill MT, et al. Advanced age diminishes tendon-to-bone healing in a rat model of rotator cuff repair. Am J Sports Med. 2014;42:859–68.CrossRefPubMed
18.
go back to reference Awad HA, Boivin GP, Dressler MR, Smith FN, Young RG, Butler DL. Repair of patellar tendon injuries using a cell-collagen composite. J Orthop Res. 2003;21:420–31.CrossRefPubMed Awad HA, Boivin GP, Dressler MR, Smith FN, Young RG, Butler DL. Repair of patellar tendon injuries using a cell-collagen composite. J Orthop Res. 2003;21:420–31.CrossRefPubMed
19.
go back to reference Barry FP, Murphy JM, English K, Mahon BP. Immunogenicity of adult mesenchymal stem cells: lessons from the fetal allograft. Stem Cells Dev. 2005;14:252–65.CrossRefPubMed Barry FP, Murphy JM, English K, Mahon BP. Immunogenicity of adult mesenchymal stem cells: lessons from the fetal allograft. Stem Cells Dev. 2005;14:252–65.CrossRefPubMed
20.
go back to reference 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;37:2126–33.CrossRefPubMed 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;37:2126–33.CrossRefPubMed
Metadata
Title
Efficacy of supraspinatus tendon repair using mesenchymal stem cells along with a collagen I scaffold
Authors
Pilar Tornero-Esteban
José Antonio Hoyas
Esther Villafuertes
Cruz Rodríguez-Bobada
Yamila López-Gordillo
Francisco J. Rojo
Gustavo V. Guinea
Anna Paleczny
Yaiza Lópiz-Morales
Luis Rodriguez-Rodriguez
Fernando Marco
Benjamín Fernández-Gutiérrez
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Journal of Orthopaedic Surgery and Research / Issue 1/2015
Electronic ISSN: 1749-799X
DOI
https://doi.org/10.1186/s13018-015-0269-6

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