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Stem Cells International
Volume 2017, Article ID 1609685, 13 pages
https://doi.org/10.1155/2017/1609685
Review Article

Bone Marrow Aspirate Concentrate-Enhanced Marrow Stimulation of Chondral Defects

1Institute of Experimental Orthopaedics and Osteoarthritis Research, Saarland University, Kirrberger Strasse, Building 37, Homburg, 66421 Saar, Germany
2Department of Orthopaedic Surgery, Saarland University Medical Center, Kirrberger Strasse, Building 37, Homburg, 66421 Saar, Germany
3Institute for Clinical Haemostaseology and Transfusion Medicine, Saarland University, Kirrberger Strasse, Building 1/Building 57, Homburg, 66421 Saar, Germany

Correspondence should be addressed to Henning Madry; ue.sku@yrdam.gninneh

Received 29 January 2017; Revised 15 March 2017; Accepted 12 April 2017; Published 18 May 2017

Academic Editor: Mitsuo Ochi

Copyright © 2017 Henning Madry et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. A. Kocher, M. D. Schuster, M. J. Szabolcs et al., “Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function,” Nature Medicine, vol. 7, no. 4, pp. 430–436, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. L. L. Johnson, “Arthroscopic abrasion arthroplasty historical and pathologic perspective: present status,” Arthroscopy, vol. 2, no. 1, pp. 54–69, 1986. View at Publisher · View at Google Scholar
  3. J. F. Stoltz, N. de Isla, Y. P. Li et al., “Stem cells and regenerative medicine: myth or reality of the 21th century,” Stem Cells International, vol. 2015, Article ID 734731, p. 19, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. A. I. Caplan, “Adult Mesenchymal stem cells: When, where, and how,” Stem Cells International, vol. 2015, Article ID 628767, p. 6, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. B. H. Min, W. H. Choi, Y. S. Lee et al., “Effect of different bone marrow stimulation techniques (BSTs) on MSCs mobilization,” Journal of Orthopaedic Research, vol. 31, no. 11, pp. 1814–1819, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Tateishi-Yuyama, H. Matsubara, T. Murohara et al., “Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial,” Lancet, vol. 360, no. 9331, pp. 427–435, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Ivkovic, A. Pascher, D. Hudetz et al., “Articular cartilage repair by genetically modified bone marrow aspirate in sheep,” Gene Therapy, vol. 17, no. 6, pp. 779–789, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Holton, M. Imam, J. Ward, and M. Snow, “The basic science of bone marrow aspirate concentrate in chondral injuries,” Orthopedic Reviews, vol. 8, no. 3, p. 6659, 2016. View at Publisher · View at Google Scholar
  9. J. Chahla, M. E. Cinque, J. M. Shon et al., “Bone marrow aspirate concentrate for the treatment of osteochondral lesions of the talus: a systematic review of outcomes,” Journal Experimental Orthopaedics, vol. 3, no. 1, p. 33, 2016. View at Publisher · View at Google Scholar
  10. J. Holton, M. A. Imam, and M. Snow, “Bone marrow aspirate in the treatment of chondral injuries,” Frontiers in Surgery, vol. 3, p. 33, 2016. View at Publisher · View at Google Scholar
  11. G. Smith, G. Knutsen, and J. Richardson, “A clinical review of cartilage repair techniques,” Journal of Bone and Joint Surgery (British Volume), vol. 87, no. 4, pp. 445–449, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. J. R. Steadman, W. G. Rodkey, and J. J. Rodrigo, “Microfracture: surgical technique and rehabilitation to treat chondral defects,” Clinical Orthopaedics and Related Research, Supplement 391, pp. S362–S369, 2001. View at Google Scholar
  13. I. Smillie, “Treatment of osteochondritis dissecans,” Journal of Bone and Joint Surgery (British Volume), vol. 39, no. 2, pp. 248–260, 1957. View at Google Scholar
  14. K. Pridie and G. Gordon, “A method of resurfacing osteoarthritic knee joints,” Journal of Bone and Joint Surgery (British Volume), vol. 41, no. 3, pp. 618-619, 1959. View at Google Scholar
  15. L. L. Johnson, “Arthroscopic abrasion arthroplasty historical and pathologic perspective: present status,” Arthroscopy: The Journal of Arthroscopic & Related Surgery, vol. 2, no. 1, pp. 54–69, 1986. View at Google Scholar
  16. M. Eldracher, P. Orth, M. Cucchiarini, D. Pape, and H. Madry, “Small subchondral drill holes improve marrow stimulation of articular cartilage defects,” American Journal of Sports Medicine, vol. 42, no. 11, pp. 2741–2750, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Orth, J. Duffner, D. Zurakowski, M. Cucchiarini, and H. Madry, “Small-diameter awls improve articular cartilage repair after microfracture treatment in a translational animal model,” American Journal of Sports Medicine, vol. 44, no. 1, pp. 209–219, 2016. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Cucchiarini, J. K. Venkatesan, M. Ekici, G. Schmitt, and H. Madry, “Human mesenchymal stem cells overexpressing therapeutic genes: from basic science to clinical applications for articular cartilage repair,” Bio-Medical Materials and Engineering, vol. 22, no. 4, pp. 197–208, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. D. J. Prockop, “Marrow stromal cells as stem cells for nonhematopoietic tissues,” Science, vol. 276, no. 5309, pp. 71–74, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. A. I. Caplan, “Mesenchymal stem cells,” Journal of Orthopaedic Research, vol. 9, no. 5, pp. 641–650, 1991. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Dominici, K. Le Blanc, I. Mueller et al., “Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement,” Cytotherapy, vol. 8, no. 4, pp. 315–317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. C. M. Kolf, E. Cho, and R. S. Tuan, “Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation,” Arthritis Research & Therapy, vol. 9, no. 1, p. 204, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. A. I. Caplan and J. E. Dennis, “Mesenchymal stem cells as trophic mediators,” Journal of Cellular Biochemistry, vol. 98, no. 5, pp. 1076–1084, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. J. M. Cassano, J. G. Kennedy, K. A. Ross, E. J. Fraser, M. B. Goodale, and L. A. Fortier, “Bone marrow concentrate and platelet-rich plasma differ in cell distribution and interleukin 1 receptor antagonist protein concentration,” Knee Surgery, Sports Traumatology, Arthroscopy, pp. 1–10, 2016. View at Publisher · View at Google Scholar
  25. A. Uccelli, V. Pistoia, and L. Moretta, “Mesenchymal stem cells: a new strategy for immunosuppression?” Trends in Immunology, vol. 28, no. 5, pp. 219–226, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Aggarwal and M. F. Pittenger, “Human mesenchymal stem cells modulate allogeneic immune cell responses,” Blood, vol. 105, no. 4, pp. 1815–1822, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. E. L. Fong, C. K. Chan, and S. B. Goodman, “Stem cell homing in musculoskeletal injury,” Biomaterials, vol. 32, no. 2, pp. 395–409, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Augello and C. De Bari, “The regulation of differentiation in mesenchymal stem cells,” Human Gene Therapy, vol. 21, no. 10, pp. 1226–1238, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. D. E. Shepherd and B. B. Seedhom, “Thickness of human articular cartilage in joints of the lower limb,” Annals of the Rheumatic Diseases, vol. 58, no. 1, pp. 27–34, 1999. View at Publisher · View at Google Scholar
  31. D. Zucker-Franklin and L. Drosenberg, “Platelet interaction with modified articular cartilage. Its possible relevance to joint repair,” Journal of Clinical Investigation, vol. 59, no. 4, pp. 641–651, 1977. View at Publisher · View at Google Scholar
  32. F. Shapiro, S. Koide, and M. J. Glimcher, “Cell origin and differentiation in the repair of full-thickness defects of articular cartilage,” Journal of Bone and Joint Surgery (American Volume), vol. 75, no. 4, pp. 532–553, 1993. View at Google Scholar
  33. P. Orth and H. Madry, “Advancement of the subchondral bone plate in translational models of osteochondral repair: implications for tissue engineering approaches,” Tissue Engineering Part B: Reviews, vol. 21, no. 6, pp. 504–520, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Mathieu, A. Chevrier, V. Lascau-Coman, G. E. Rivard, and C. D. Hoemann, “Stereological analysis of subchondral angiogenesis induced by chitosan and coagulation factors in microdrilled articular cartilage defects,” Osteoarthritis and Cartilage, vol. 21, no. 6, pp. 849–859, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. H. Imhof, I. Sulzbacher, S. Grampp, C. Czerny, S. Youssefzadeh, and F. Kainberger, “Subchondral bone and cartilage disease: a rediscovered functional unit,” Investigative Radiology, vol. 35, no. 10, pp. 581–588, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. H. Brem and J. Folkman, “Inhibition of tumor angiogenesis mediated by cartilage,” Journal of Experimental Medicine, vol. 141, no. 2, pp. 427–439, 1975. View at Publisher · View at Google Scholar
  37. M. Blanke, H. D. Carl, P. Klinger, B. Swoboda, F. Hennig, and K. Gelse, “Transplanted chondrocytes inhibit endochondral ossification within cartilage repair tissue,” Calcified Tissue International, vol. 85, no. 5, pp. 421–433, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Pfander, T. Cramer, D. Deuerling, G. Weseloh, and B. Swoboda, “Expression of thrombospondin-1 and its receptor CD36 in human osteoarthritic cartilage,” Annals of the Rheumatic Diseases, vol. 59, no. 6, pp. 448–454, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. D. K. Taylor, J. A. Meganck, S. Terkhorn et al., “Thrombospondin-2 influences the proportion of cartilage and bone during fracture healing,” Journal of Bone and Mineral Research, vol. 24, no. 6, pp. 1043–1054, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. M. A. Moses, D. Wiederschain, I. Wu et al., “Troponin I is present in human cartilage and inhibits angiogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 6, pp. 2645–2650, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. X. Chevalier, N. Groult, B. Larget-Piet, L. Zardi, and W. Hornebeck, “Tenascin distribution in articular cartilage from normal subjects and from patients with osteoarthritis and rheumatoid arthritis,” Arthritis and Rheumatism, vol. 37, no. 7, pp. 1013–1022, 1994. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Pesesse, C. Sanchez, and Y. Henrotin, “Osteochondral plate angiogenesis: A new treatment target in osteoarthritis,” Joint, Bone, Spine: Revue du Rhumatisme, vol. 78, no. 2, pp. 144–149, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Klinger, C. Surmann-Schmitt, M. Brem et al., “Chondromodulin 1 stabilizes the chondrocyte phenotype and inhibits endochondral ossification of porcine cartilage repair tissue,” Arthritis and Rheumatism, vol. 63, no. 9, pp. 2721–2731, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Kusafuka, Y. Hiraki, C. Shukunami, T. Kayano, and T. Takemura, “Cartilage-specific matrix protein, chondromodulin-I (ChM-I), is a strong angio-inhibitor in endochondral ossification of human neonatal vertebral tissues in vivo: relationship with angiogenic factors in the cartilage,” Acta Histochemica, vol. 104, no. 2, pp. 167–175, 2002. View at Publisher · View at Google Scholar
  45. C. Shukunami and Y. Hiraki, “Role of cartilage-derived anti-angiogenic factor, chondromodulin-I, during endochondral bone formation,” Osteoarthritis and Cartilage, vol. 9, Supplement A, pp. S91–S101, 2001. View at Google Scholar
  46. R. Sakata, T. Kokubu, I. Nagura et al., “Localization of vascular endothelial growth factor during the early stages of osteochondral regeneration using a bioabsorbable synthetic polymer scaffold,” Journal of Orthopaedic Research, vol. 30, no. 2, pp. 252–259, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. D. A. Walsh, “Angiogenesis in osteoarthritis and spondylosis: successful repair with undesirable outcomes,” Current Opinion in Rheumatology, vol. 16, no. 5, pp. 609–615, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Henrotin, L. Pesesse, and C. Sanchez, “Subchondral bone in osteoarthritis physiopathology: state-of-the art and perspectives,” Bio-Medical Materials and Engineering, vol. 19, no. 4-5, pp. 311–316, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Matsumoto, G. M. Cooper, B. Gharaibeh et al., “Cartilage repair in a rat model of osteoarthritis through intraarticular transplantation of muscle-derived stem cells expressing bone morphogenetic protein 4 and soluble Flt-1,” Arthritis and Rheumatism, vol. 60, no. 5, pp. 1390–1405, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Walsh, “Angiogenesis and arthritis,” Rheumatology, vol. 38, no. 2, pp. 103–112, 1999. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Walsh and L. Haywood, “Angiogenesis: a therapeutic target in arthritis,” Current Opinion in Investigational Drugs (London, England: 2000), vol. 2, no. 8, pp. 1054–1063, 2001. View at Google Scholar
  52. S. C. Ballara, J. M. Miotla, and E. M. Paleolog, “New vessels, new approaches: angiogenesis as a therapeutic target in musculoskeletal disorders,” International Journal of Experimental Pathology, vol. 80, no. 5, pp. 235–250, 1999. View at Google Scholar
  53. T. Saber, D. J. Veale, E. Balogh et al., “Toll-like receptor 2 induced angiogenesis and invasion is mediated through the Tie2 signalling pathway in rheumatoid arthritis,” PLoS One, vol. 6, no. 8, article e23540, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. H.-P. Gerber, T. H. Vu, A. M. Ryan, J. Kowalski, Z. Werb, and N. Ferrara, “VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation,” Nature Medicine, vol. 5, no. 6, pp. 623–628, 1999. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Murata, K. Yudoh, and K. Masuko, “The potential role of vascular endothelial growth factor (VEGF) in cartilage: how the angiogenic factor could be involved in the pathogenesis of osteoarthritis?” Osteoarthritis and Cartilage, vol. 16, no. 3, pp. 279–286, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Enomoto, I. Inoki, K. Komiya et al., “Vascular endothelial growth factor isoforms and their receptors are expressed in human osteoarthritic cartilage,” The American Journal of Pathology, vol. 162, no. 1, pp. 171–181, 2003. View at Publisher · View at Google Scholar
  57. T. Shimo, T. Nakanishi, Y. Kimura et al., “Inhibition of endogenous expression of connective tissue growth factor by its antisense oligonucleotide and antisense RNA suppresses proliferation and migration of vascular endothelial cells,” The Journal of Biochemistry, vol. 124, no. 1, pp. 130–140, 1998. View at Publisher · View at Google Scholar
  58. D. A. Walsh and C. I. Pearson, “Angiogenesis in the pathogenesis of inflammatory joint and lung diseases,” Arthritis Research & Therapy, vol. 3, no. 3, pp. 147–153, 2001. View at Publisher · View at Google Scholar · View at Scopus
  59. G. Hashimoto, I. Inoki, Y. Fujii, T. Aoki, E. Ikeda, and Y. Okada, “Matrix metalloproteinases cleave connective tissue growth factor and reactivate angiogenic activity of vascular endothelial growth factor 165,” Journal of Biological Chemistry, vol. 277, no. 39, pp. 36288–36295, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. J. T. K. Melton, N. M. Clarke, and H. I. Roach, “Matrix metalloproteinase-9 induces the formation of cartilage canals in the chondroepiphysis of the neonatal rabbit,” The Journal of Bone & Joint Surgery, vol. 88, Supplement 3, pp. 155–161, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Kubo, G. M. Cooper, T. Matsumoto et al., “Blocking vascular endothelial growth factor with soluble Flt-1 improves the chondrogenic potential of mouse skeletal muscle–derived stem cells,” Arthritis and Rheumatism, vol. 60, no. 1, pp. 155–165, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Nagai, M. Sato, T. Kutsuna et al., “Intravenous administration of anti-vascular endothelial growth factor humanized monoclonal antibody bevacizumab improves articular cartilage repair,” Arthritis Research & Therapy, vol. 12, no. 5, p. R178, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. P. Kasten, I. Beyen, M. Egermann et al., “Instant stem cell therapy: characterization and concentration of human mesenchymal stem cells in vitro,” European Cells & Materials, vol. 16, pp. 47–55, 2008. View at Publisher · View at Google Scholar
  64. K. Y. Saw, P. Hussin, S. C. Loke et al., “Articular cartilage regeneration with autologous marrow aspirate and hyaluronic acid: an experimental study in a goat model,” Arthroscopy, vol. 25, no. 12, pp. 1391–1400, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. L. A. Fortier, H. G. Potter, E. J. Rickey et al., “Concentrated bone marrow aspirate improves full-thickness cartilage repair compared with microfracture in the equine model,” Journal of Bone and Joint Surgery (American Volume), vol. 92, no. 10, pp. 1927–1937, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Pascher, G. Palmer, A. Steinert et al., “Gene delivery to cartilage defects using coagulated bone marrow aspirate,” Gene Therapy, vol. 11, no. 2, pp. 133–141, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Iwasa, L. Engebretsen, Y. Shima, and M. Ochi, “Clinical application of scaffolds for cartilage tissue engineering,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 17, no. 6, pp. 561–577, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Betsch, J. Schneppendahl, S. Thuns et al., “Bone marrow aspiration concentrate and platelet rich plasma for osteochondral repair in a porcine osteochondral defect model,” PLoS One, vol. 8, no. 8, article e71602, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Betsch, S. Thelen, L. Santak et al., “The role of erythropoietin and bone marrow concentrate in the treatment of osteochondral defects in mini-pigs,” PLoS One, vol. 9, no. 3, article e92766, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Getgood, F. Henson, C. Skelton et al., “The augmentation of a collagen/glycosaminoglycan biphasic osteochondral scaffold with platelet-rich plasma and concentrated bone marrow aspirate for osteochondral defect repair in sheep: a pilot study,” Cartilage, vol. 3, no. 4, pp. 351–363, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. L. de Girolamo, G. Bertolini, M. Cervellin, G. Sozzi, and P. Volpi, “Treatment of chondral defects of the knee with one step matrix-assisted technique enhanced by autologous concentrated bone marrow: in vitro characterisation of mesenchymal stem cells from iliac crest and subchondral bone,” Injury, vol. 41, no. 11, pp. 1172–1177, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Gobbi and G. P. Whyte, “One-stage cartilage repair using a hyaluronic acid-based scaffold with activated bone marrow-derived mesenchymal stem cells compared with microfracture: five-year follow-up,” American Journal of Sports Medicine, vol. 44, no. 11, pp. 2846–2854, 2016. View at Publisher · View at Google Scholar · View at Scopus
  73. C. P. Hannon, K. A. Ross, C. D. Murawski et al., “Arthroscopic bone marrow stimulation and concentrated bone marrow aspirate for osteochondral lesions of the talus: a case-control study of functional and magnetic resonance observation of cartilage repair tissue outcomes,” Arthroscopy, vol. 32, no. 2, pp. 339–347, 2016. View at Publisher · View at Google Scholar · View at Scopus
  74. N. S. Lanham, J. J. Carroll, M. T. Cooper, V. Perumal, and J. S. Park, “A comparison of outcomes of particulated juvenile articular cartilage and bone marrow aspirate concentrate for articular cartilage lesions of the talus,” Foot & Ankle Specialist, 2016. View at Publisher · View at Google Scholar
  75. R. E. Outerbridge, “The etiology of chondromalacia patellae,” Journal of Bone and Joint Surgery (British Volume), vol. 43-B, no. 4, pp. 752–757, 1961. View at Google Scholar
  76. K. E. Webster and J. A. Feller, “Comparison of the short form-12 (SF-12) health status questionnaire with the SF-36 in patients with knee osteoarthritis who have replacement surgery,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 24, no. 8, pp. 2620–2626, 2016. View at Publisher · View at Google Scholar · View at Scopus
  77. P. Orth, M. Cucchiarini, D. Kohn, and H. Madry, “Alterations of the subchondral bone in osteochondral repair—translational data and clinical evidence,” European Cells & Materials, vol. 25, pp. 299–316, 2013. View at Google Scholar
  78. G. Kaul, M. Cucchiarini, K. Remberger, D. Kohn, and H. Madry, “Failed cartilage repair for early osteoarthritis defects: A biochemical, histological and immunohistochemical analysis of the repair tissue after treatment with marrow-stimulation techniques,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 20, no. 11, pp. 2315–2324, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. A. Gobbi, G. Karnatzikos, and A. Kumar, “Long-term results after microfracture treatment for full-thickness knee chondral lesions in athletes,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 22, no. 9, pp. 1986–1996, 2014. View at Publisher · View at Google Scholar · View at Scopus
  80. W. Foster, Y. Li, A. Usas, G. Somogyi, and J. Huard, “Gamma interferon as an antifibrosis agent in skeletal muscle,” Journal of Orthopaedic Research, vol. 21, no. 5, pp. 798–804, 2003. View at Publisher · View at Google Scholar · View at Scopus
  81. T. Laumonier and J. Menetrey, “Muscle injuries and strategies for improving their repair,” Journal Experimental Orthopaedics, vol. 3, no. 1, p. 15, 2016. View at Publisher · View at Google Scholar
  82. J. Zhu, Y. Li, A. Lu et al., “Follistatin improves skeletal muscle healing after injury and disease through an interaction with muscle regeneration, angiogenesis, and fibrosis,” American Journal of Pathology, vol. 179, no. 2, pp. 915–930, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. Y. Zhang, W. Lei, W. Yan et al., “microRNA-206 is involved in survival of hypoxia preconditioned mesenchymal stem cells through targeting Pim-1 kinase,” Stem Cell Research & Therapy, vol. 7, no. 1, p. 61, 2016. View at Publisher · View at Google Scholar · View at Scopus
  84. J. Frisch, A. Rey-Rico, J. K. Venkatesan, G. Schmitt, H. Madry, and M. Cucchiarini, “rAAV-mediated overexpression of sox9, TGF-beta and IGF-I in minipig bone marrow aspirates to enhance the chondrogenic processes for cartilage repair,” Gene Therapy, vol. 23, no. 3, pp. 247–255, 2016. View at Publisher · View at Google Scholar · View at Scopus
  85. K. Tao, A. Rey-Rico, J. Frisch et al., “Effects of combined rAAV-mediated TGF-beta and sox9 gene transfer and overexpression on the metabolic and chondrogenic activities in human bone marrow aspirates,” Journal Experimental Orthopaedics, vol. 4, no. 1, p. 4, 2017. View at Publisher · View at Google Scholar
  86. L. Li, X. Chen, W. E. Wang, and C. Zeng, “How to improve the survival of transplanted mesenchymal stem cell in ischemic heart?” Stem Cells International, vol. 2016, Article ID 9682757, p. 14, 2016. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Lee, E. Choi, M. J. Cha, and K. C. Hwang, “Cell adhesion and long-term survival of transplanted mesenchymal stem cells: a prerequisite for cell therapy,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 632902, p. 9, 2015. View at Publisher · View at Google Scholar · View at Scopus