Advertisement

Cells, soluble factors and matrix harmonically play the concert of allograft integration

  • Laura de Girolamo
  • Enrico Ragni
  • Magali Cucchiarini
  • Christian J. A. van Bergen
  • Ernst B. Hunziker
  • Susanna Chubinskaya
KNEE
  • 62 Downloads

Abstract

Implantation of allograft tissues has massively grown over the last years, especially in the fields related to sports medicine. Beside the fact that often no autograft option exists, autograft related disadvantages as donor-site morbidity and prolonged operative time are drastically reduced with allograft tissues. Despite the well documented clinical success for bone allograft procedures, advances in tissue engineering raised the interest in meniscus, osteochondral and ligament/tendon allografts. Notably, their overall success rates are constantly higher than 80%, making them a valuable treatment option in orthopaedics, especially in knee surgery. Complications reported for allografting procedures are a small risk of disease transmission, immunologic rejection, and decreased biologic incorporation together with nonunion at the graft-host juncture and, rarely, massive allograft resorption. Although allografting is a successful procedure, improved techniques and biological knowledge to limit these pitfalls and maximize graft incorporation are needed. A basic understanding of the biologic processes that affect the donor-host interactions and eventual incorporation and remodelling of various allograft tissues is a fundamental prerequisite for their successful clinical use. Further, the importance of the interaction of immunologic factors with the biologic processes involved in allograft incorporation has yet to be fully dissected. Finally, new tissue engineering techniques and use of adjunctive growth factors, cell based and focused gene therapies may improve the quality and uniformity of clinical outcomes. The aim of this review is to shed light on the biology of meniscus, osteochondral and ligament/tendon allograft incorporation and how collection and storage techniques may affect graft stability and embodiment.

Level of evidence V.

Keywords

Allograft Meniscus Tendon Cartilage Integration Cytokines Inflammation Irradiation Deep-freezing Scaffold 

Notes

Author contributions

LdG, ER, MC, CJAvB, EBH and SC have been involved in drafting the manuscript and revising it critically. All authors read and approved the final manuscript.

Funding

No funding has been received for this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

References

  1. 1.
    Abe S, Kurosaka M, Iguchi T, Yoshiya S, Hirohata K (1993) Light and electron microscopic study of remodeling and maturation process in autogenous graft for anterior cruciate ligament reconstruction. Arthroscopy 9:394–405CrossRefGoogle Scholar
  2. 2.
    Ahsan T, Sah RL (1999) Biomechanics of integrative cartilage repair. Osteoarthr Cartil 7(1):29–40 (review) CrossRefGoogle Scholar
  3. 3.
    Arnoczky SP (2006) The biology of allograft incorporation. J Knee Surg 19(3):207–214CrossRefGoogle Scholar
  4. 4.
    Arnoczky SP, DiCarlo EF, O’Brien SJ, Warren RF (1992) Cellular repopulation of deep-frozen meniscal autografts: an experimental study in the dog. Arthroscopy 8(4):428–436CrossRefGoogle Scholar
  5. 5.
    Arnoczky SP, Warren RF, Ashlock MA (1986) Replacement of the anterior cruciate ligament using a patellar tendon allograft. An experimental study. J Bone Jt Surg Am 68(3):376–385CrossRefGoogle Scholar
  6. 6.
    Baker BE, Peckham AC, Pupparo F, Sanborn JC (1985) Review of meniscal injury and associated sports. Am J Sports Med 13(1):1–4CrossRefGoogle Scholar
  7. 7.
    Barber FA, Cowden CH 3rd, Sanders EJ (2014) Revision rates after anterior cruciate ligament reconstruction using bone-patellar tendon-bone allograft or autograft in a population 25 years old and younger. Arthroscopy 30(4):483–491CrossRefGoogle Scholar
  8. 8.
    Bastiaansen-Jenniskens YM, Koevoet W, Feijt C, Bos PK, Verhaar JA, Van Osch GJ, DeGroot J (2009) Proteoglycan production is required in initial stages of new cartilage matrix formation but inhibits integrative cartilage repair. J Tissue Eng Regen Med 3(2):117–123CrossRefGoogle Scholar
  9. 9.
    Bhatia S, Bell R, Frank RM, Rodeo SA, Bach BR Jr, Cole BJ, Chubinskaya S, Wang VM, Verma NN (2012) Bony incorporation of soft tissue anterior cruciate ligament grafts in an animal model: autograft versus allograft with low-dose gamma irradiation. Am J Sports Med 40(8):1789–1798CrossRefGoogle Scholar
  10. 10.
    Binnet MS, Akan B, Kaya A (2012) Lyophilised medial meniscus transplantations in ACL-deficient knees: a 19-year follow-up. Knee Surg Sports Traumatol Arthrosc 20:109–113CrossRefGoogle Scholar
  11. 11.
    Bitar AC, Santos LA, Croci AT, Pereira JA, França Bisneto EN, Giovani AM, Oliveira CR (2010) Histological study of fresh versus frozen semitendinous muscle tendon allografts. Clinics (Sao Paulo) 65(3):297–303CrossRefGoogle Scholar
  12. 12.
    Buckwalter JA, Mankin HJ (1998) Articular cartilage: degeneration and osteoarthritis, repair, regeneration, and transplantation. Instr Course Lect 47:487–504PubMedGoogle Scholar
  13. 13.
    Bugbee WD, Pallante-Kichura AL, Görtz S, Amiel D, Sah R (2016) Osteochondral allograft transplantation in cartilage repair: graft storage paradigm, translational models, and clinical applications. J Orthop Res 34(1):31–38CrossRefGoogle Scholar
  14. 14.
    Caplan AI, Elyaderani M, Mochizuki Y, Wakitani S, Goldberg VM (1997) Principles of cartilage repair and regeneration. Clin Orthop Relat Res 342:254–269CrossRefGoogle Scholar
  15. 15.
    Cerulli G, Placella G, Sebastiani E, Tei MM, Speziali A, Manfreda F (2013) ACL reconstruction: choosing the graft. Joints 1(1):18–24PubMedPubMedCentralGoogle Scholar
  16. 16.
    Chahal J, Gross AE, Gross C, Mall N, Dwyer T, Chahal A, Whelan DB, Cole BJ (2013) Outcomes of osteochondral allograft transplantation in the knee. Arthroscopy 29(3):575–588CrossRefGoogle Scholar
  17. 17.
    Chandler S, Cossins J, Lury J, Wells G (1996) Macrophage metalloelastase degrades matrix and myelin proteins and processes a tumour necrosis factor-alpha fusion protein. Biochem Biophys Res Commun 228:421–429CrossRefGoogle Scholar
  18. 18.
    Chang YC, Yang SF, Lai CC, Liu JY, Hsieh YS (2002) Regulations of matrix metalloproteinase production by cytokines, pharmacological agents and periodontal pathogens in human peridontal ligament fibroblasts cultures. J Peridontal Res 37:196–203CrossRefGoogle Scholar
  19. 19.
    Chiarello E, Cadossi M, Tedesco G, Capra P, Calamelli C, Shehu A, Giannini S (2013) Autograft, allograft and bone substitutes in reconstructive orthopedic surgery. Aging Clin Exp Res 25(Suppl 1):S101–S103CrossRefGoogle Scholar
  20. 20.
    Conrad BP, Rappé M, Horodyski M, Farmer KW, Indelicato PA (2013) The effect of sterilization on mechanical properties of soft tissue allografts. Cell Tissue Bank 14:359–366CrossRefGoogle Scholar
  21. 21.
    Cooper JA, Sahota JS, Gorum WJ 2nd, Carter J, Doty SB, Laurencin CT (2007) Biomimetictissue-engineered anterior cruciate ligament replacement. Proc Natl Acad Sci USA 104:3049–3054CrossRefGoogle Scholar
  22. 22.
    De Bruycker M, Verdonk PCM, Verdonk RC (2017) Meniscal allograft transplantation: a meta-analysis. SICOT J 3:33CrossRefGoogle Scholar
  23. 23.
    Debeer P, Decorte R, Delvaux S, Bellemans J (2000) DNA analysis of a transplanted cryopreserved meniscal allograft. Arthroscopy 16:71–75CrossRefGoogle Scholar
  24. 24.
    DiBartola AC, Everhart JS, Magnussen RA, Carey JL, Brophy RH, Schmitt LC, Flanigan DC (2016) Correlation between histological outcome and surgical cartilage repair technique in the knee: a meta-analysis. Knee 23(3):344–349CrossRefGoogle Scholar
  25. 25.
    DiMicco MA, Sah RL (2001) Integrative cartilage repair: adhesive strength is correlated with collagen deposition. J Orthop Res 19(6):1105–1112CrossRefGoogle Scholar
  26. 26.
    Djouad F, Rackwitz L, Song Y, Janjanin S, Tuan RS (2009) ERK1/2 activation induced by inflammatory cytokines compromises effective host tissue integration of engineered cartilage. Tissue Eng Part A 15(10):2825–2835CrossRefGoogle Scholar
  27. 27.
    Eagan MJ, McAllister DR (2009) Biology of allograft incorporation. Clin Sports Med 28(2):203–214CrossRefGoogle Scholar
  28. 28.
    Eppley BL, Woodell JE, Higgins J (2004) Platelet quantification and growth factor analysis from platelet-rich plasma: implications for wound healing. Plast Reconstr Surg 114:1502–1508CrossRefGoogle Scholar
  29. 29.
    Farrar CA, Kupiec-Weglinski JW, Sacks SH (2013) The innate immune system and transplantation. Cold Spring Harb Perspect Med 3(10):a015479CrossRefGoogle Scholar
  30. 30.
    Fortier LA, Potter HG, Rickey EJ, Schnabel LV, Foo LF, Chong LR, Stokol T, Cheetham J, Nixon AJ (2010) Concentrated bone marrow aspirate improves full-thickness cartilage repair compared with microfracture in the equine model. J Bone Jt Surg Am 92(10):1927–1937CrossRefGoogle Scholar
  31. 31.
    Garrity JT, Stoker AM, Sims HJ, Cook JL (2012) Improved osteochondral allograft preservation using serum-free media at body temperature. Am J Sports Med 40(11):2542–2548CrossRefGoogle Scholar
  32. 32.
    Gasimov E, Sabah D, Yilmaz O, Kececi B, Oktem G (2014) Experimental remodellation of extracorporeal irradiated autogenous and allogenic patellar grafts. Eur J Orthop Surg Traumatol 24(8):1539–1547CrossRefGoogle Scholar
  33. 33.
    Gelber PE, Gonzalez G, Lloreta JL, Reina F, Caceres E, Monllau JC (2008) Freezing causes changes in the meniscus collagen net: a new ultrastructural meniscus disarray scale. Knee Surg Sports Traumatol Arthrosc 16:353–359CrossRefGoogle Scholar
  34. 34.
    Gelber PE, Gonzalez G, Torres R, Garcia Giralt N, Caceres E, Monllau JC (2009) Cryopreservation does not alter the ultrastructure of the meniscus. Knee Surg Sports Traumatol Arthrosc 17:639–644CrossRefGoogle Scholar
  35. 35.
    Gitelis SL, Bodker A, Laurent MP, Kirk SS, Filardo G, Meyer MA, Hakimiyan AA, Rappoport L, Wimmer MA, Cole BJ, Chubinskaya S (2018) The effect of surgical insertion and proinflammatory cytokines on osteochondral allograft survival and metabolism. Cartilage 9(3):284–292CrossRefGoogle Scholar
  36. 36.
    Goodman RB, Pugin J, Lee JS, Matthay MA (2003) Cytokine-mediated inflammation in acute lung injury. Cytokine Growth Factor Rev 14:523–535CrossRefGoogle Scholar
  37. 37.
    Greaves L, Hecker A, Brown C (2008) The effect of donor age and low-dose gamma irradiation on the initial biomechanical properties of human tibialis tendon allografts. Am J Sport Med 36(7):1358–1366CrossRefGoogle Scholar
  38. 38.
    Greis PE, Bardana DD, Holmstrom MC, Burks RT (2002) Meniscal injury: I. Basic science and evaluation. J Am Acad Orthop Surg 10(3):168–176CrossRefGoogle Scholar
  39. 39.
    Hinsenkamp M, Muylle L, Eastlund T, Fehily D, Noel L, Strong DM (2011) Adverse reactions and events related to musculoskeletal allografts: reviewed by the World Health Organisation Project NOTIFY. Int Orthop 36(3):633–641CrossRefGoogle Scholar
  40. 40.
    Hoburg A, Keshlaf S, Schmidt T, Smith M, Gohs U, Perka C, Pruss A, Scheffler S (2011) Fractionation of high-dose electron beam irradiation of BPTB grafts provides significantly improved viscoelastic and structural properties compared to standard gamma irradiation. Knee Surg Sports Traumatol Arthrosc 19(11):1955–1961CrossRefGoogle Scholar
  41. 41.
    Hoburg A, Keshlaf S, Schmidt T, Smith M, Gohs U, Perka C, Pruss A, Scheffler S (2015) High-dose electron beam sterilization of soft-tissue grafts maintains significantly improved biomechanical properties compared to standard gamma treatment. Cell Tissue Bank 16(2):219–226CrossRefGoogle Scholar
  42. 42.
    Hunziker EB (1999) Articular cartilage repair: are the intrinsic biological constraints undermining this process insuperable? Osteoarthr Cartil 7(1):15–28 (review) CrossRefGoogle Scholar
  43. 43.
    Hunziker EB (2002) Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthr Cartil 10(6):432–463CrossRefGoogle Scholar
  44. 44.
    Hunziker EB, Quinn TM (2003) Surgical removal of articular cartilage leads to loss of chondrocytes from cartilage bordering the wound edge. J Bone Jt Surg Am 85-A(Suppl 2):85–92CrossRefGoogle Scholar
  45. 45.
    Hunziker EB, Rosenberg LC (1996) Repair of partial-thickness defects in articular cartilage: cell recruitment from the synovial membrane. J Bone Jt Surg Am 78(5):721–733CrossRefGoogle Scholar
  46. 46.
    Indelli PF, Dillingham MF, Fanton GS, Schurman DJ (2004) Anterior cruciate ligament reconstruction using cryopreserved allografts. Clin Orthop Relat Res 420:268–275CrossRefGoogle Scholar
  47. 47.
    Jackson DW, Corsetti J, Simon TM (1996) Biologic incorporation of allograft anterior cruciate ligament replacements. Clin Orthop Relat Res 324:126–133CrossRefGoogle Scholar
  48. 48.
    Jackson DW, Simon TM, Kurzweil PR, Rosen MA (1992) Survival of cells after intra-articular transplantation of fresh allografts of the patellar and anterior cruciate ligaments. DNA-probe analysis in a goat model. J Bone Jt Surg Am 74(1):112–118CrossRefGoogle Scholar
  49. 49.
    Judas F, Rosa S, Teixeira L, Lopes C, Ferreira MA (2007) Chondrocyte viability in fresh and frozen large human osteochondral allografts: effect of cryoprotective agents. Transplant Proc 39(8):2531–2534CrossRefGoogle Scholar
  50. 50.
    Kainer MA, Linden JV, Whaley DN, Holmes HT, Jarvis WR, Jernigan DB, Archibald LK (2004) Clostridium infections associated with musculoskeletal-tissue allografts. N Engl J Med 350(25):2564–2571CrossRefGoogle Scholar
  51. 51.
    Kang RW, Friel NA, Williams JM, Cole BJ, Wimmer MA (2010) Effect of impaction sequence on osteochondral graft damage: the role of repeated and varying loads. Am J Sports Med 38(1):105–113CrossRefGoogle Scholar
  52. 52.
    Khoury MA, Goldberg VM, Stevenson S (1994) Demonstration of HLA and ABH antigens in fresh and frozen human menisci by immunohistochemistry. J Orthop Res 12:751–757CrossRefGoogle Scholar
  53. 53.
    Kleiner JB, Amiel D, Harwood FL, Akeson WH (1989) Early histological, metabolic, and vascular assessment of anterior cruciate ligament autografts. J Orthop Res 7:235–242CrossRefGoogle Scholar
  54. 54.
    Kleiner JB, Amiel D, Roux RD, Akeson WH (1986) Origin of replacement cells for the anterior cruciate ligament autograft. J Orthop Res 4:466–474CrossRefGoogle Scholar
  55. 55.
    Knauper V, Will H, Lopez-Otin C, Smith B, Atkinson SJ, Stanton H, Hembry RM, Murphy G (1996) Cellular mechanisms for human procollagenase-3 (MMP-13) activation: evidence that MT1-MMP (MMP-14) and gelatinase a (MMP-2) are able to generate active enzyme. J Biol Chem 271:17124–17131CrossRefGoogle Scholar
  56. 56.
    LaPrade RF, Botker J, Herzog M, Agel J (2009) Refrigerated osteoarticular allografts to treat articular cartilage defects of the femoral condyles. A prospective outcomes study. J Bone Jt Surg Am 91(4):805–811CrossRefGoogle Scholar
  57. 57.
    Leask A, Holmes A, Abraham DJ (2002) Connective tissue growth factor: a new and important player in the pathogenesis of fibrosis. Curr Rheumatol Rep 4:136–142CrossRefGoogle Scholar
  58. 58.
    Lotz M (2001) Cytokines in cartilage injury and repair. Clin Orthop Relat Res 391:S108–S115 (review) CrossRefGoogle Scholar
  59. 59.
    Lubowitz JH, Verdonk PCM, Reid JB III, Verdonk R (2007) Meniscus allograft transplantation: a current concepts review. Knee Surg Sports Traumatol Arthrosc 15(5):476–492CrossRefGoogle Scholar
  60. 60.
    Mahirogullari M, Ferguson CM, Whitlock PW, Stabile KJ, Poehling GG (2007) Freeze-dried allografts for anterior cruciate ligament reconstruction. Clin Sports Med 26(4):625–637CrossRefGoogle Scholar
  61. 61.
    Malinin TI, Levitt RL, Bashore C, Temple HT, Mnaymneh W (2002) A study of retrieved allografts used to replace anterior cruciate ligaments. Arthroscopy 18(2):163–170CrossRefGoogle Scholar
  62. 62.
    Marui T, Niyibizi C, Georgescu HI, Cao M, Kavalkovich KW, Levine RE, Woo SL (1997) Effect of growth factors on matrix synthesis by ligament fibroblasts. J Orthop Res 15(1):18–23CrossRefGoogle Scholar
  63. 63.
    McCormick F, Harris JD, Frank RM, Hussey KE, Wilson H, Gupta AK, Abrams GD, Bach BR, Cole BJ (2014) Meniscal allograft transplantation reoperation rates, operative findings, and survival analysis: a review of 200 consecutive transplants at minimum two-year follow-up. Orthop J Sports Med 2(1 Suppl):2325967114S00003PubMedCentralGoogle Scholar
  64. 64.
    Mroz TE, Joyce MJ, Steinmetz MP, Lieberman IH, Wang JC (2008) Musculoskeletal allograft risks and recalls in the United States. J Am Acad Orthop Surg 16(10):559–565CrossRefGoogle Scholar
  65. 65.
    Ochi M, Ikuta Y, Ishida O, Akiyama M (1993) Cellular and humoral immune responses after fresh meniscal allografts in mice. A preliminary report. Arch Orthop Trauma Surg 112:163–166CrossRefGoogle Scholar
  66. 66.
    Ochi M, Ishida O, Daisaku H, Ikuta Y, Akiyama M (1995) Immune response to fresh meniscal allografts in mice. J Surg Res 58:478–484CrossRefGoogle Scholar
  67. 67.
    O’Driscoll SW (1998) The healing and regeneration of articular cartilage. J Bone Jt Surg Am 80(12):1795–1812 (review) CrossRefGoogle Scholar
  68. 68.
    Ohlendorf C, Tomford WW, Mankin HJ (1996) Chondrocyte survival in cryopreserved osteochondral articular cartilage. J Orthop Res 14(3):413–416CrossRefGoogle Scholar
  69. 69.
    Pallante AL, Bae WC, Chen AC, Görtz S, Bugbee WD, Sah RL (2009) Chondrocyte viability is higher after prolonged storage at 37 °C than at 4 °C for osteochondral grafts. Am J Sports Med 37(Suppl 1):24S–32CrossRefGoogle Scholar
  70. 70.
    Pallante AL, Görtz S, Chen AC, Healey RM, Chase DC, Ball ST, Amiel D, Sah RL, Bugbee WD (2012) Treatment of articular cartilage defects in the goat with frozen versus fresh osteochondral allografts: effects on cartilage stiffness, zonal composition, and structure at six months. J Bone Jt Surg Am 94(21):1984–1995CrossRefGoogle Scholar
  71. 71.
    Pallante-Kichura AL, Cory E, Bugbee WD, Sah RL (2013) Bone cysts after osteochondral allograft repair of cartilage defects in goats suggest abnormal interaction between subchondral bone and overlying synovial joint tissues. Bone 57:259–268CrossRefGoogle Scholar
  72. 72.
    Peretti GM, Campo-Ruiz V, Gonzalez S, Randolph MA, Wei Xu J, Morse KR, Roses RE, Yaremchuk MJ (2006) Tissue engineered cartilage integration to live and devitalized cartilage: a study by reflectance mode confocal microscopy and standard histology. Connect Tissue Res 47(4):190–199CrossRefGoogle Scholar
  73. 73.
    Qu J, van Alphen NA, Thoreson AR, Chen Q, An KN, Amadio PC, Schmid TM, Zhao C (2015) Effects of trypsinization and mineralization on intrasynovial tendon allograft healing to bone. J Orthop Res 33(4):468–474CrossRefGoogle Scholar
  74. 74.
    Quinn TM, Hunziker EB (2002) Controlled enzymatic matrix degradation for integrative cartilage repair: effects on viable cell density and proteoglycan deposition. Tissue Eng 8(5):799–806CrossRefGoogle Scholar
  75. 75.
    Ranawat AS, Vidal AF, Chen CT, Zelken JA, Turner AS, Williams RJ (2008) Material properties of fresh cold-stored allografts for osteochondral defects at 1 year. Clin Orthop Relat Res 466:1826–1836CrossRefGoogle Scholar
  76. 76.
    Rodeo SA, Seneviratne A, Suzuki K, Felker K, Wickiewicz TL, Warren RF (2000) Histological analysis of human meniscal allograft. A preliminary report. J Bone Jt Surg Am 82:1071–1082CrossRefGoogle Scholar
  77. 77.
    Schaefer DB, Wendt D, Moretti M, Jakob M, Jay GD, Heberer M, Martin I (2004) Lubricin reduces cartilage–cartilage integration. Biorheology 41(3–4):503–508PubMedGoogle Scholar
  78. 78.
    Scheffler SU, Unterhauser FN, Weiler A (2008) Graft remodeling and ligamentization after cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc 16:834–842CrossRefGoogle Scholar
  79. 79.
    Schubert T, Cornu O, Delloye C (2010) Organization: type of grafts, conservation, regulation. In: Beaufils P, Verdonk R (eds) The meniscus. Springer, Berlin, pp 315–320CrossRefGoogle Scholar
  80. 80.
    Secretan C, Bagnall KM, Jomha NM (2010) Effects of introducing cultured human chondrocytes into a human articular cartilage explant model. Cell Tissue Res 339(2):421–427CrossRefGoogle Scholar
  81. 81.
    Seto AU, Culp BM, Gatt CJ Jr, Dunn M (2013) Radioprotection provides functional mechanics but delays healing of irradiated tendon allografts after ACL reconstruction in sheep. Cell Tissue Bank 14:655–665CrossRefGoogle Scholar
  82. 82.
    Shapiro F, Koide S, Glimcher MJ (1993) Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Jt Surg Am 75(4):532–553CrossRefGoogle Scholar
  83. 83.
    Sharma P, Maffulli N (2006) Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact 6(2):181–190PubMedGoogle Scholar
  84. 84.
    Singer AJ, Clark RA (1999) Cutaneous wound healing. N Engl J Med 341:738–746CrossRefGoogle Scholar
  85. 85.
    Stoker AM, Baumann CA, Stannard JP, Cook JL (2017) Bone marrow aspirate concentrate versus platelet rich plasma to enhance osseous integration potential for osteochondral allografts. J Knee Surg 31(4):314–320PubMedGoogle Scholar
  86. 86.
    Tachiiri H, Morihara T, Iwata Y, Yoshida A, Kajikawa Y, Kida Y, Matsuda K, Fujiwara H, Kurokawa M, Kawata M, Kubo T (2010) Characteristics of donor and host cells in the early remodeling process after transplant of Achilles tendon with and without live cells for the treatment of rotator cuff defect–what is the ideal graft for the treatment of massive rotator cuff defects? J Shoulder Elbow Surg 19(6):891–898CrossRefGoogle Scholar
  87. 87.
    Tew SR, Kwan AP, Hann A, Thomson BM, Archer CW (2000) The reactions of articular cartilage to experimental wounding: role of apoptosis. Arthritis Rheum 43(1):215–225CrossRefGoogle Scholar
  88. 88.
    Tsuzaki M, Guyton G, Garrett W, Haas NP, Weiler A (2003) IL-1 beta induces COX2, MMP-1, -3 and -13, ADAMTS-4, IL-1 beta and IL-6 in human tendon cells. J Orthop Res 21:256–264CrossRefGoogle Scholar
  89. 89.
    Unterhauser FN, Bail HJ, Höher J, Haas NP, Weiler A (2003) Endoligamentous revascularization of an anterior cruciate ligament graft. Clin Orthop Relat Res 414:276–288CrossRefGoogle Scholar
  90. 90.
    van der Wal RJ, Thomassen BJ, van Arkel ER (2009) Long-term clinical outcome of open meniscal allograft transplantation. Am J Sports Med 37(11):2134–2139CrossRefGoogle Scholar
  91. 91.
    Verdonk PC, Demurie A, Almqvist KF, Veys EM, Verbruggen G, Verdonk R (2005) Transplantation of viable meniscal allograft. J Bone Jt Surg 87(4):715–724CrossRefGoogle Scholar
  92. 92.
    Verdonk PC, Verstraete KL, Almqvist KF, De Cuyper K, Veys EM, Verbruggen G, Verdonk R (2006) Meniscal allograft transplantation: long-term clinical results with radiological and magnetic resonance imaging correlations. Knee Surg Sports Traumatol Arthrosc 14(8):694–706CrossRefGoogle Scholar
  93. 93.
    Vinagre G, Kennedy NI, Chahla J, Cinque ME, Hussain ZB, Olesen ML, LaPrade RF (2017) Hamstring graft preparation techniques for anterior cruciate ligament reconstruction. Arthrosc Tech 6(6):e2079–e2084CrossRefGoogle Scholar
  94. 94.
    von Lewinski G, Wirth CJ (2010) Meniscal reconstruction: allograft. 10.1. Basic science. In: Beaufils P, Verdonk R (eds) The meniscus. Springer, Berlin, pp 303–315CrossRefGoogle Scholar
  95. 95.
    Wada Y (1993) Meniscal transplantation using fresh and cryopreserved allografts. An experimental study in the genetically defined rat. J Jpn Orthop Assoc 67:677–683Google Scholar
  96. 96.
    Wada Y, Amiel M, Harwood F, Moriya H, Amiel D (1998) Architectural remodeling in deep frozen meniscal allografts after total meniscectomy. Arthroscopy 14(3):250–257CrossRefGoogle Scholar
  97. 97.
    Wei W, Liu Y, Yang X, Tian S, Liu C, Zhang Y, Xu Z, Hu B, Tian Z, Sun K (2013) Fractionation of 50 kGy electron beam irradiation: effects on biomechanics of human flexor digitorum superficialis tendons treated with ascorbate. J Biomech 46:658–661CrossRefGoogle Scholar
  98. 98.
    Williams RJ 3rd, Dreese JC, Chen CT (2004) Chondrocyte survival and material properties of hypothermically stored cartilage: an evaluation of tissue used for osteochondral allograft transplantation. Am J Sports Med 32(1):132–139CrossRefGoogle Scholar
  99. 99.
    Yoshikawa T, Tohyama H, Katsura T (2006) Effects of local administration of vascular endothelial growth factor on mechanical characteristics of the semitendinosus tendon graft after anterior cruciate ligament reconstruction in sheep. Am J Sports Med 34:1918–1925CrossRefGoogle Scholar

Copyright information

© European Society of Sports Traumatology, Knee Surgery, Arthroscopy (ESSKA) 2018

Authors and Affiliations

  1. 1.IRCCS Istituto Ortopedico Galeazzi, Laboratorio di Biotecnologie applicate all’OrtopediaMilanoItaly
  2. 2.Center of Experimental OrthopaedicsSaarland University Medical CenterHomburg/SaarGermany
  3. 3.Department of Orthopedic SurgeryAmphia HospitalBredaThe Netherlands
  4. 4.Departments of Osteoporosis and Orthopaedic SurgeryInselspital (University Hospital)BernSwitzerland
  5. 5.Department of PediatricsRush University Medical CenterChicagoUSA

Personalised recommendations