2013 Neer Award: Effect of the adipose-derived stem cell for the improvement of fatty degeneration and rotator cuff healing in rabbit model

Journal of Shoulder and Elbow Surgery

Volumn 23, Issue 4, 2014, Pages 445-455

  Oh, Joo Han ^a   Chung, Seok Won ^b   Kim, Sae Hoon ^c   Chung, Jin Young ^c   Kim, Joon Yub ^d  

^a Seoul National University Bundang Hospital   (South Korea)

^b Konkuk University School of Medicine   (South Korea)

^c Seoul National University Hospital   (South Korea)

^d Seonam University of Medicine Myongji Hospital   (South Korea)

Author keywords

Adipose derived stem cell; Compound muscle action potential; Fatty infiltration; Rotator cuff tear; Tendon to bone healing

Indexed keywords

ADIPOSE DERIVED STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; CONTROLLED STUDY; ELECTROMYOGRAPHY; FATTY LIVER; HISTOLOGY; MALE; MUSCLE ACTION POTENTIAL; MUSCLE FUNCTION; NONHUMAN; PRIORITY JOURNAL; RABBIT MODEL; ROTATOR CUFF RUPTURE; SUBSCAPULARIS MUSCLE; TENDON; WOUND HEALING;

ADIPOSE-DERIVED STEM CELL; COMPOUND MUSCLE ACTION POTENTIAL; FATTY INFILTRATION; ROTATOR CUFF TEAR; TENDON-TO-BONE HEALING;

ADIPOSE TISSUE; ANIMALS; AWARDS AND PRIZES; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; MALE; RABBITS; RANDOM ALLOCATION; ROTATOR CUFF; STEM CELL TRANSPLANTATION; TENDON INJURIES; WOUND HEALING;

EID: 84895930930     PISSN: 10582746     EISSN: 15326500     Source Type: Journal    
DOI: 10.1016/j.jse.2013.07.054     Document Type: Article

References (51)

1. Aspenberg P., Virchenko O. Platelet concentrate injection improves Achilles tendon repair in rats. Acta Orthop Scand 2004, 75:93-99. 10.1080/00016470410001708190.
2. Awad H.A., Butler D.L., Boivin G.P., Smith F.N., Malaviya P., Huibregtse B., et al. Autologous mesenchymal stem cell-mediated repair of tendon. Tissue Eng 1999, 5:267-277.
3. Baar K., Nader G., Bodine S. Resistance exercise, muscle loading/unloading and the control of muscle mass. Essays Biochem 2006, 42:61-74. 10.1042/bse0420061.
4. Baker J.H., Hall-Craggs E.C. Changes in sarcomere length following tenotomy in the rat. Muscle Nerve 1980, 3:413-416.
5. Bjorkenheim J.M., Paavolainen P., Ahovuo J., Slatis P. Resistance of a defect of the supraspinatus tendon to intraarticular hydrodynamic pressure: an experimental study on rabbits. J Orthop Res 1990, 8:175-179.
6. Boileau P., Brassart N., Watkinson D.J., Carles M., Hatzidakis A.M., Krishnan S.G. Arthroscopic repair of full-thickness tears of the supraspinatus: does the tendon really heal?. J Bone Joint Surg Am 2005, 87:1229-1240. 10.2106/JBJS.D.02035.
7. Burkhart S.S., Lo I.K. Arthroscopic rotator cuff repair. J Am Acad Orthop Surg 2006, 14:333-346.
8. Chen C.H., Chang C.H., Wang K.C., Su C.I., Liu H.T., Yu C.M., et al. Enhancement of rotator cuff tendon-bone healing with injectable periosteum progenitor cells-BMP-2 hydrogel invivo. Knee Surg Sports Traumatol Arthrosc 2011, 19:1597-1607. 10.1007/s00167-010-1373-0.
9. Di Rocco G., Iachininoto M.G., Tritarelli A., Straino S., Zacheo A., Germani A., et al. Myogenic potential of adipose-tissue-derived cells. JCell Sci 2006, 119:2945-2952. 10.1242/jcs.03029.
10. Eriksen H.A., Pajala A., Leppilahti J., Risteli J. Increased content of type III collagen at the rupture site of human Achilles tendon. J Orthop Res 2002, 20:1352-1357. 10.1016/S0736-0266(02)00064-5.
11. Gantz B.J., Gmuer A.A., Holliday M., Fisch U. Electroneurographic evaluation of the facial nerve. Method and technical problems. Ann Otol Rhinol Laryngol 1984, 93:394-398.
12. Gazielly D.F., Gleyze P., Montagnon C. Functional and anatomical results after rotator cuff repair. Clin Orthop Relat Res 1994, 304:43-53.
13. Gerber C., Fuchs B., Hodler J. The results of repair of massive tears of the rotator cuff. J Bone Joint Surg Am 2000, 82:505-515.
14. Gimbel J.A., Van Kleunen J.P., Mehta S., Perry S.M., Williams G.R., Soslowsky L.J. Supraspinatus tendon organizational and mechanical properties in a chronic rotator cuff tear animal model. J Biomech 2004, 37:739-749. 10.1016/j.jbiomech.
15. Gimble J.M., Grayson W., Guilak F., Lopez M.J., Vunjak-Novakovic G. Adipose tissue as a stem cell source for musculoskeletal regeneration. Front Biosci (Schol Ed) 2011, 3:69-81.
16. Gimble J.M., Katz A.J., Bunnell B.A. Adipose-derived stem cells for regenerative medicine. Circ Res 2007, 100:1249-1260. 10.1161/01.RES.0000265074.83288.09.
17. Gladstone J.N., Bishop J.Y., Lo I.K., Flatow E.L. Fatty infiltration and atrophy of the rotator cuff do not improve after rotator cuff repair and correlate with poor functional outcome. Am J Sports Med 2007, 35:719-728. 10.1177/0363546506297539.
18. Goutallier D., Postel J.M., 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, 12:550-554. 10.1016/S1058274603002118.
19. Goutallier D., Postel J.M., Van Driessche S., Voisin M.C. [Histological lesions of supraspinatus tendons in full thickness tears of the rotator cuff]. Rev Chir Orthop Reparatrice Appar Mot 2005, 91:109-113. http://dx.doi.org/MDOI-RCO-04-2005-91-2-0035-1040-101019-200513185.
20. Grumet R.C., Hadley S., Diltz M.V., Lee T.Q., Gupta R. Development of a new model for rotator cuff pathology: the rabbit subscapularis muscle. Acta Orthop 2009, 80:97-103. 10.1080/17453670902807425.
21. Gulotta L.V., Kovacevic D., Ehteshami J.R., Dagher E., Packer J.D., Rodeo S.A. Application of bone marrow-derived mesenchymal stem cells in a rotator cuff repair model. Am J Sports Med 2009, 37:2126-2133. 10.1177/0363546509339582.
22. Gupta R., Lee T.Q. Contributions of the different rabbit models to our understanding of rotator cuff pathology. J Shoulder Elbow Surg 2007, 16:S149-S157. 10.1016/j.jse.2007.05.002.
23. Kawiak J., Brzoska E., Grabowska I., Hoser G., Streminska W., Wasilewska D., et al. Contribution of stem cells to skeletal muscle regeneration. Folia Histochem Cytobiol 2006, 44:75-79.
24. Kim M., Choi Y.S., Yang S.H., Hong H.N., Cho S.W., Cha S.M., et al. Muscle regeneration by adipose tissue-derived adult stem cells attached to injectable PLGA spheres. Biochem Biophys Res Commun 2006, 348:386-392. 10.1016/j.bbrc.2006.07.063.
25. Kim S.H., Chung S.W., Oh J.H. 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, [Epub ahead of print]. 10.1007/s00167-013-2560-6.
26. Kuhbier J.W., Weyand B., Sorg H., Radtke C., Vogt P.M., Reimers K. [Stem cells from fatty tissue: A new resource for regenerative medicine?]. Chirurg 2010, 81:826-832. 10.1007/s00104-010-1962-y.
27. Li Y.G., Wei J.N., Lu J., Wu X.T., Teng G.J. Labeling and tracing of bone marrow mesenchymal stem cells for tendon-to-bone tunnel healing. Knee Surg Sports Traumatol Arthrosc 2011, 19:2153-2158. 10.1007/s00167-011-1506-0.
28. Machin D., Campbell M.J., Fayers P., Pinol A. Statistical tables for the design of clinical studies 1998, Blackwell, Oxford. 2nd edition.
29. Matsen F.A., Arntz C.T. Rotator cuff tendon failure. The shoulder 1990, 647-677. WB Saunders Company, Philadelphia, PA. 1st ed. C.A. Rockwood, F.A. Matsen (Eds.).
30. Milgrom C., Schaffler M., Gilbert S., van Holsbeeck M. Rotator-cuff changes in asymptomatic adults. The effect of age, hand dominance and gender. J Bone Joint Surg Br 1995, 77:296-298.
31. Molloy T., Wang Y., Murrell G. The roles of growth factors in tendon and ligament healing. Sports Med 2003, 33:381-394. 10.2165/00007256-200333050-00004.
32. 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. 10.1371/journal.pone.0012248.
33. Oh J.H., Kim S.H., Ji H.M., Jo K.H., Bin S.W., Gong H.S. Prognostic factors affecting anatomic outcome of rotator cuff repair and correlation with functional outcome. Arthroscopy 2009, 25:30-39. 10.1016/j.arthro.2008.08.010.
34. Oh J.H., Kim S.H., Kim J.H., Shin Y.H., Yoon J.P., Oh C.H. The level of vitamin D in the serum correlates with fatty degeneration of the muscles of the rotator cuff. J Bone Joint Surg Br 2009, 91:1587-1593. 10.1302/0301-620X.91B12.22481.
35. Park J.Y., Lhee S.H., Choi J.H., Park H.K., Yu J.W., Seo J.B. Comparison of the clinical outcomes of single- and double-row repairs in rotator cuff tears. Am J Sports Med 2008, 36:1310-1316. 10.1177/0363546508315039.
36. Romeo A.A., Hang D.W., Bach B.R., Shott S. Repair of full thickness rotator cuff tears. Gender, age, and other factors affecting outcome. Clin Orthop Relat Res 1999, 367:243-255.
37. Rubino L.J., Sprott D.C., Stills H.F., Crosby L.A. Fatty infiltration does not progress after rotator cuff repair in a rabbit model. Arthroscopy 2008, 24:936-940. 10.1016/j.arthro.2008.03.004.
38. Safran O., Derwin K.A., Powell K., Iannotti J.P. Changes in rotator cuff muscle volume, fat content, and passive mechanics after chronic detachment in a canine model. J Bone Joint Surg Am 2005, 87:2662-2670. 10.2106/JBJS.D.02421.
39. Sher J.S., Uribe J.W., Posada A., Murphy B.J., Zlatkin M.B. Abnormal findings on magnetic resonance images of asymptomatic shoulders. J Bone Joint Surg Am 1995, 77:10-15.
40. Spees J.L., Olson S.D., Whitney M.J., Prockop D.J. Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci U S A 2006, 103:1283-1288. 10.1073/pnas.0510511103.
41. Stalberg E. Skeletal muscle: structure and function. Clinical neurophysiology of disorders of muscle and neuromuscular junction, including fatigue. Handbook of clinical neurophysiology. Vol. 2 2003, Elsevier, Philadelphia, PA.
42. Trudel G., Ramachandran N., Ryan S.E., Rakhra K., Uhthoff H.K. Supraspinatus tendon repair into a bony trough in the rabbit: mechanical restoration and correlative imaging. J Orthop Res 2010, 28:710-715. 10.1002/jor.21045.
43. Uhthoff H.K., Matsumoto F., Trudel G., Himori K. Early reattachment does not reverse atrophy and fat accumulation of the supraspinatus-an experimental study in rabbits. J Orthop Res 2003, 21:386-392. 10.1016/S0736-0266(02)00208-5.
44. Uhthoff H.K., Seki M., Backman D.S., Trudel G., Himori K., Sano H. Tensile strength of the supraspinatus after reimplantation into a bony trough: an experimental study in rabbits. J Shoulder Elbow Surg 2002, 11:504-509. http://dx.doi.org/S1058274602000721.
45. Uysal A.C., Mizuno H. Tendon regeneration and repair with adipose derived stem cells. Curr Stem Cell Res Ther 2010, 5:161-167.
46. Uysal C.A., Tobita M., Hyakusoku H., Mizuno H. Adipose-derived stem cells enhance primary tendon repair: biomechanical and immunohistochemical evaluation. J Plast Reconstr Aesthet Surg 2012, 65:1712-1719. 10.1016/j.bjps.2012.06.011.
47. Wang X.J., Dong Z., Zhong X.H., Shi R.Z., Huang S.H., Lou Y., et al. Transforming growth factor-beta1 enhanced vascular endothelial growth factor synthesis in mesenchymal stem cells. Biochem Biophys Res Commun 2008, 365:548-554. 10.1016/j.bbrc.2007.11.014.
48. Yokoya S., Mochizuki Y., Natsu K., Omae H., Nagata Y., Ochi M. Rotator cuff regeneration using a bioabsorbable material with bone marrow-derived mesenchymal stem cells in a rabbit model. Am J Sports Med 2012, 40:1259-1268. 10.1177/0363546512442343.
49. Young R.G., Butler D.L., Weber W., Caplan A.I., Gordon S.L., Fink D.J. Use of mesenchymal stem cells in a collagen matrix for Achilles tendon repair. J Orthop Res 1998, 16:406-413.
50. Zhang F., Liu H., Stile F., Lei M.P., Pang Y., Oswald T.M., et al. Effect of vascular endothelial growth factor on rat Achilles tendon healing. Plast Reconstr Surg 2003, 112:1613-1619. 10.1097/01.PRS.0000086772.72535.A4.
51. Zumstein M.A., Jost B., Hempel J., Hodler J., Gerber C. The clinical and structural long-term results of open repair of massive tears of the rotator cuff. J Bone Joint Surg Am 2008, 90:2423-2431. 10.2106/JBJS.G.00677.