Increased vascularization during early healing after biologic augmentation in repair of chronic rotator cuff tears using autologous leukocyte- and platelet-rich fibrin (L-PRF): A prospective randomized controlled pilot trial

Journal of Shoulder and Elbow Surgery

Volumn 23, Issue 1, 2014, Pages 3-12

  Zumstein, Matthias A ^a   Rumian, Adam ^a   Lesbats, Virginie ^a   Schaer, Michael ^a   Boileau, Pascal ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

Leukocyte and platelet rich fibrin (L PRF); Rotator cuff; Shoulder arthroscopy; Vascularization

Indexed keywords

FIBRIN; LEUKOCYTE AND PLATELET RICH FIBRIN; THROMBOCYTE CONCENTRATE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BONE; CHRONIC DISEASE; CLINICAL ARTICLE; CLINICAL EXAMINATION; CONSTANT SHOULDER TEST SCORE; CONTROLLED STUDY; DOPPLER ECHOGRAPHY; FEMALE; HUMAN; MALE; OUTCOME ASSESSMENT; PILOT STUDY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; ROTATOR CUFF RUPTURE; SCORING SYSTEM; SHOULDER ARTHROSCOPY; SHOULDER SURGERY; SIMPLE SHOULDER TEST SCORE; SUBJECTIVE SHOULDER VALUE SCORE; TENDON; TREATMENT RESPONSE; VASCULARIZATION; VISUAL ANALOG SCALE; WOUND HEALING;

LEUKOCYTE- AND PLATELET-RICH FIBRIN (L-PRF); LEVEL I; RANDOMIZED CONTROLLED TRIAL; ROTATOR CUFF; SHOULDER ARTHROSCOPY; TREATMENT STUDY; VASCULARIZATION;

AGED; ARTHROSCOPY; BLOOD PLATELETS; BLOOD TRANSFUSION, AUTOLOGOUS; CHRONIC DISEASE; FEMALE; FIBRIN; HUMANS; LEUKOCYTE TRANSFUSION; MALE; MIDDLE AGED; NEOVASCULARIZATION, PHYSIOLOGIC; PILOT PROJECTS; PROSPECTIVE STUDIES; ROTATOR CUFF; TREATMENT OUTCOME; WOUND HEALING;

EID: 84890198678     PISSN: 10582746     EISSN: 15326500     Source Type: Journal    
DOI: 10.1016/j.jse.2013.08.017     Document Type: Article

References (61)

1. Adler R.S., Johnson K.M., Fealy S., Maderazo A., Gallo R.A., Gamradt S.C., et al. Contrast-enhanced sonographic characterization of the vascularity of the repaired rotator cuff: utility of maximum intensity projection imaging. J Ultrasound Med 2011, 30:1103-1109. 10.1016/j.jse.2011.04.001.
2. Alfredson H., Ohberg L., Forsgren S. Is vasculo-neural ingrowth the cause of pain in chronic Achilles tendinosis? An investigation using ultrasonography and colour Doppler, immunohistochemistry, and diagnostic injections. Knee Surg Sports Traumatol Arthrosc 2003, 11:334-338. 10.1007/s00167-003-0391-6.
3. Biberthaler P., Wiedemann E., Nerlich A., Kettler M., Mussack T., Deckelmann S., et al. Microcirculation associated with degenerative rotator cuff lesions. Invivo assessment with orthogonal polarization spectral imaging during arthroscopy of the shoulder. J Bone Joint Surg Am 2003, 85:475-480.
4. 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. http://dx.doi.org/10.2106/JBJS.D.02035.
5. Boileau P., Brassart N., Youssanne Y., Scobercea R. The mattress-tension-band technique: a knotless double-row arthroscopic rotator cuff repair. Tech Shoulder Elbow Surg 2009, 10:22-25. http://dx.doi.org/10.1097/BTE.0b013e318195a69c.
6. Boyer M.I., Watson J.T., Lou J., Manske P.R., Gelberman R.H., Cai S.R. Quantitative variation in vascular endothelial growth factor mRNA expression during early flexor tendon healing: an investigation in a canine model. J Orthop Res 2001, 19:869-872. http://dx.doi.org/1010.1016/S0736-0266(01)00017-1.
7. Brasseur J., Nicolaon L., Saillant G. Echographie des tendons opérés [Ultrasonography of operated tendons]. Tendons and etheses 2003, 236ff. Sauramps, Montpellier. H. Bard (Ed.).
8. Brasseur J.-L., Lucidarme O., Tardieu M., Tordeur M., Montalvan B., Parier J., et al. Ultrasonographic rotator-cuff changes in veteran tennis players: the effect of hand dominance and comparison with clinical findings. Eur Radiol 2004, 14:857-864. 10.1007/s00330-003-2116-0.
9. Brooks C.H., Revell W.J., Heatley F.W. A quantitative histological study of the vascularity of the rotator cuff tendon. J Bone Joint Surg Br 1992, 74:151-153.
10. Cadet E.R., Adler R.S., Gallo R.A., Gamradt S.C., Warren R.F., Cordasco F.A., et al. Contrast-enhanced ultrasound characterization of the vascularity of the repaired rotator cuff tendon: short-term and intermediate-term follow-up. J Shoulder Elbow Surg 2012, 21:597-603. 10.1016/j.jse.2011.04.001.
11. Choukroun J., Diss A., Simonpieri A., Girard M.O., Schoeffler C., Dohan S.L., et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part IV: clinical effects on tissue healing. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006, 101:e56-e60. http://dx.doi.org/1010.1016/j.tripleo.2005.07.011.
12. Constant C.R. Age related recovery of shoulder function after injury 1986, University College, Cork, Ireland.
13. Constant C.R., Murley A.H. A clinical method of functional assessment of the shoulder. Clin Orthop Relat Res 1987, (214):160-164.
14. Divani K., Chan O., Padhiar N., Twycross-Lewis R., Maffulli N., Crisp T., et al. Site of maximum neovascularisation correlates with the site of pain in recalcitrant mid-tendon Achilles tendinopathy. Man Ther 2010, 15:463-468. http://dx.doi.org/1010.1016/j.math.2010.03.011.
15. Dohan D.M., Choukroun J., Diss A., Dohan S.L., Dohan A.J., Mouhyi J., et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part I: technological concepts and evolution. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006, 101:e37-e44. http://dx.doi.org/1010.1016/j.tripleo.2005.07.008.
16. Dohan D.M., Choukroun J., Diss A., Dohan S.L., Dohan A.J., Mouhyi J., et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part II: platelet-related biologic features. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006, 101:e45-e50. http://dx.doi.org/1010.1016/j.tripleo.2005.07.009.
17. Dohan D.M., Choukroun J., Diss A., Dohan S.L., Dohan A.J., Mouhyi J., et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part III: leucocyte activation: a new feature for platelet concentrates?. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006, 101:e51-e55. 10.1016/j.tripleo.2005.07.010.
18. Dohan Ehrenfest D.M., de Peppo G.M., Doglioli P., Sammartino G. Slow release of growth factors and thrombospondin-1 in Choukroun's platelet-rich fibrin (PRF): a gold standard to achieve for all surgical platelet concentrates technologies. Growth Factors 2009, 27:63-69. http://dx.doi.org/1010.1080/08977190802636713.
19. Dohan Ehrenfest D.M., Rasmusson L., Albrektsson T. Classification of platelet concentrates: from pure platelet-rich plasma (P-PRP) to leucocyte- and platelet-rich fibrin (L-PRF). Trends Biotechnol 2009, 27:158-167. http://dx.doi.org/1010.1016/j.tibtech.2008.11.009.
20. Fealy S., Adler R.S., Drakos M.C., Kelly A.M., Allen A.A., Cordasco F.A., et al. Patterns of vascular and anatomical response after rotator cuff repair. Am J Sports Med 2006, 34:120-127. http://dx.doi.org/1010.1177/0363546505280212.
21. Franceschi F., Ruzzini L., Longo U.G., Martina F.M., Zobel B.B., Maffulli N., et al. Equivalent clinical results of arthroscopic single-row and double-row suture anchor repair for rotator cuff tears: a randomized controlled trial. Am J Sports Med 2007, 35:1254-1260. http://dx.doi.org/1010.1177/0363546507302218.
22. Fuchs B., Gilbart M.K., 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, 88:309-316. http://dx.doi.org/1010.2106/jbjs.e.00117.
23. Fuchs B., Weishaupt D., Zanetti M., Hodler J., Gerber C. Fatty degeneration of the muscles of the rotator cuff: assessment by computed tomography versus magnetic resonance imaging. J Shoulder Elbow Surg 1999, 8:599-605.
24. Fukui N., Katsuragawa Y., Sakai H., Oda H., Nakamura K. Effect of local application of basic fibroblast growth factor on ligament healing in rabbits. Rev Rhum Engl Ed 1998, 65:406-414.
25. Galatz L.M., Ball C.M., Teefey S.A., Middleton W.D., Yamaguchi K. The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears. J Bone Joint Surg Am 2004, 86:219-224.
26. 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.
27. Gilbart M.K., Gerber C. Comparison of the subjective shoulder value and the Constant score. J Shoulder Elbow Surg 2007, 16:717. http://dx.doi.org/1010.1016/j.jse.2007.02.123.
28. Goutallier D., Postel J.M., Bernageau J., Lavau L., Voisin M.C. Fatty muscle degeneration in cuff ruptures. Pre- and postoperative evaluation by CT scan. Clin Orthop 1994, 78-83.
29. Grasso A., Milano G., Salvatore M., Falcone G., Deriu L., Fabbriciani C. Single-row versus double-row arthroscopic rotator cuff repair: a prospective randomized clinical study. Arthroscopy 2009, 25:4-12. http://dx.doi.org/1010.1016/j.arthro.2008.09.018.
30. Gusmer P.B., Potter H.G., Donovan W.D., O'Brien S.J. MR imaging of the shoulder after rotator cuff repair. AJR Am J Roentgenol 1997, 168:559-563.
31. Harry L.E., Paleolog E.M. From the cradle to the clinic: VEGF in developmental, physiological, and pathological angiogenesis. Birth Defects Res C Embryo Today 2003, 69:363-374. http://dx.doi.org/1010.1002/bdrc.10024.
32. Hsu C., Chang J. Clinical implications of growth factors in flexor tendon wound healing. J Hand Surg Am 2004, 29:551-563. http://dx.doi.org/1010.1016/j.jhsa.2004.04.020.
33. Jost B. Long-term outcome after structural failure of rotator cuff repairs. J Bone Joint Surg 2006, 88:472-479. http://dx.doi.org/1010.2106/JBJS.E.00003.
34. Jost B., Pfirrmann C.W., Gerber C. Clinical outcome after structural failure of rotator cuff repairs. J Bone Joint Surg Am 2000, 82:304-314.
35. Kang H.J., Park B.M., Hahn S.B., Kang E.S. An experimental study of healing of the partially severed flexor tendon in chickens. Yonsei Med J 1990, 31:264-273.
36. Lewis J.S., Raza S.A., Pilcher J., Heron C., Poloniecki J.D. The prevalence of neovascularity in patients clinically diagnosed with rotator cuff tendinopathy. BMC Musculoskelet Disord 2009, 10:163. http://dx.doi.org/1010.1186/1471-2474-10-163.
37. Lippitt S., Harryman D.T., Matsen F.A. A pratical tool for evaluating shoulder fucntion: the Simple Shoulder Test. The shoulder: a balance of mobility and stability 1992, 501-518. Amercian Academy of Orthopaedic Surgeons, Rosemont, Ill. F. Matsen, F. Fu, R. Hawkins (Eds.).
38. Lohr J.F., Uhthoff H.K. The microvascular pattern of the supraspinatus tendon. Clin Orthop Relat Res 1990, 35-38.
39. Magee T.H., Gaenslen E.S., Seitz R., Hinson G.A., Wetzel L.H. MR imaging of the shoulder after surgery. AJR Am J Roentgenol 1997, 168:925-928.
40. Moher D., Schulz K.F., Altman D. The CONSORT statement: revised recommendations for improving the quality of reports of parallel-group randomized trials. JAMA 2001, 285:1987-1991.
41. Molloy T., Wang Y., Murrell G. The roles of growth factors in tendon and ligament healing. Sports Med 2003, 33:381-394.
42. Müller-Rath R.B., Ingenhoven E. How high is the statistical risk of infection after outpatient arthroscopy? Evaluation of over 50,000 cases from statistics of the Professional Society for Outpatient Arthroscopy. Arthroskopie 2008, 21:87-91. http://dx.doi.org/1010.1007/s00142-008-0445-3.
43. Nyffeler R. Association of a large lateral extension of the acromion with rotator cuff tears. J Bone Joint Surg 2006, 88:800-805. 10.2106/JBJS.D.03042.
44. Ohberg L., Lorentzon R., Alfredson H. Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc 2001, 9:233-238.
45. Owen R.S., Iannotti J.P., Kneeland J.B., Dalinka M.K., Deren J.A., Oleaga L. Shoulder after surgery: MR imaging with surgical validation. Radiology 1993, 186:443-447.
46. Patte D. Classification of rotator cuff lesions. Clin Orthop 1990, 81-86.
47. Perry S.M., McIlhenny S.E., Hoffman M.C., Soslowsky L.J. Inflammatory and angiogenic mRNA levels are altered in a supraspinatus tendon overuse animal model. J Shoulder Elbow Surg 2005, 14:79S-83S. http://dx.doi.org/10.1016/j.jse.2004.09.020.
48. Pufe T., Kurz B., Petersen W., Varoga D., Mentlein R., Kulow S., et al. The influence of biomechanical parameters on the expression of VEGF and endostatin in the bone and joint system. Ann Anat 2005, 187:461-472. http://dx.doi.org/10.1016/j.aanat.2005.06.008.
49. Rathbun J.B., Macnab I. The microvascular pattern of the rotator cuff. J Bone Joint Surg Br 1970, 52:540-553.
50. Rodeo S.A., Delos D., Williams R.J., Adler R.S., Pearle A., Warren R.F. The effect of platelet-rich fibrin matrix on rotator cuff tendon healing: a prospective, randomized clinical study. Am J Sports Med 2012, 40:1234-1241. http://dx.doi.org/1010.1177/0363546512442924.
51. Rothman R.H., Parke W.W. The vascular anatomy of the rotator cuff. Clin Orthop Relat Res 1965, 41:176-186.
52. Rudzki J.R., Adler R.S., Warren R.F., Kadrmas W.R., Verma N., Pearle A.D., et al. Contrast-enhanced ultrasound characterization of the vascularity of the rotator cuff tendon: age- and activity-related changes in the intact asymptomatic rotator cuff. J Shoulder Elbow Surg 2008, 17:96S-100S. http://dx.doi.org/1010.1016/j.jse.2007.07.004.
53. Ruhrberg C. Growing and shaping the vascular tree: multiple roles for VEGF. Bioessays 2003, 25:1052-1060. http://dx.doi.org/1010.1002/bies.10351.
54. Sugaya H., Maeda K., Matsuki K., Moriishi J. Functional and structural outcome after arthroscopic full-thickness rotator cuff repair: single-row versus dual-row fixation. Arthroscopy 2005, 21:1307-1316. http://dx.doi.org/1010.1016/j.arthro.2005.08.011.
55. Thomazeau H., Boukobza E., Morcet N., Chaperon J., Langlais F. Prediction of rotator cuff repair results by magnetic resonance imaging. Clin Orthop Relat Res 1997, 275-283.
56. Werther K., Christensen I.J., Nielsen H.J. Determination of vascular endothelial growth factor (VEGF) in circulating blood: significance of VEGF in various leucocytes and platelets. Scand J Clin Lab Invest 2002, 62:343-350. http://dx.doi.org/1010.1080/00365510260296492.
57. Yepes H., Tang M., Morris S.F., Stanish W.D. Relationship between hypovascular zones and patterns of ruptures of the quadriceps tendon. J Bone Joint Surg Am 2008, 90:2135-2141. http://dx.doi.org/1010.2106/JBJS.G.01200.
58. Zachary I. VEGF signalling: integration and multi-tasking in endothelial cell biology. Biochem Soc Trans 2003, 31:1171-1177. doi:1010.1042/.
59. Zumstein M., Berger S., Schober M., Boileau P., Nyffeler R.W., Horn M., et al. Leukocyte- and platelet-rich fibrin (L-PRF) for long-term delivery of growth factor in rotator cuff repair: review, preliminary results and future directions. Curr Pharm Biotechnol 2012, 13:1196-1206. http://dx.doi.org/1010.2174/138920112800624337.
60. Zumstein M., Bielecki T., Dohan Ehrenfest D.M. The future of platelet concentrates in sports medicine: platelet-rich plasma, platelet-rich fibrin, and the impact of scaffolds and cells on the long-term delivery of growth factors. Oper Tech Sports Med 2011, 19:190-197. http://dx.doi.org/1010.1053/j.otsm.2011.01.001.
61. 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. http://dx.doi.org/1010.2106/jbjs.g.00677.