Advertisement

Knee Surgery, Sports Traumatology, Arthroscopy

, Volume 18, Issue 8, pp 1038–1051 | Cite as

Osteointegration of soft tissue grafts within the bone tunnels in anterior cruciate ligament reconstruction can be enhanced

  • Guan-Ming KuangEmail author
  • W. P. Yau
  • William W. Lu
  • K. Y. Chiu
Knee

Abstract

Anterior cruciate ligament reconstruction with a soft tissue autograft (hamstring autograft) has grown in popularity in the last 10 years. However, the issues of a relatively long healing time and an inferior histological healing result in terms of Sharpey-like fibers connection in soft tissue grafts are still unsolved. To obtain a promising outcome in the long run, prompt osteointegration of the tendon graft within the bone tunnel is essential. In recent decades, numerous methods have been reported to enhance osteointegration of soft tissue graft in the bone tunnel. In this article, we review the current literature in this research area, mainly focusing on strategies applied to the local bone tunnel environment. Biological strategies such as stem cell and gene transfer technology, as well as the local application of specific growth factors have been reported to yield exciting results. The use of biological bone substitute and physical stimulation also obtained promising results. Artificially engineered tissue has promise as a solution to the problem of donor site morbidity. Despite these encouraging results, the current available evidence is still experimental. Further clinical studies in terms of randomized control trial in the future should be conducted to extrapolate these basic science study findings into clinical practice.

Keywords

Anterior cruciate ligament Graft Healing Tendon Tunnel 

References

  1. 1.
    Adachi N, Ochi M, Uchio Y et al (2003) Harvesting hamstring tendons for ACL reconstruction influences postoperative hamstring muscle performance. Arch Orthop Trauma Surg 123:460–465CrossRefPubMedGoogle Scholar
  2. 2.
    Anderson K, Seneviratne AM, Izawa K et al (2001) Augmentation of tendon healing in an intraarticular bone tunnel with use of a bone growth factor. Am J Sports Med 29:689–698PubMedGoogle Scholar
  3. 3.
    Aune AK, Holm I, Risberg MA et al (2001) Four-strand hamstring tendon autograft compared with patellar tendon-bone autograft for anterior cruciate ligament reconstruction. A randomized study with 2-year follow-up. Am J Sports Med 29:722–728PubMedGoogle Scholar
  4. 4.
    Bartlett RJ, Clatworthy MG, Nguyen TN (2001) Graft selection in reconstruction of the anterior cruciate ligament. J Bone Joint Surg Br 83:625–634CrossRefPubMedGoogle Scholar
  5. 5.
    Beard DJ, Anderson JL, Davies S et al (2001) Hamstrings vs. patella tendon for anterior cruciate ligament reconstruction: a randomised controlled trial. Knee 8:45–50CrossRefPubMedGoogle Scholar
  6. 6.
    Beynnon BD, Johnson RJ, Fleming BC et al (2002) Anterior cruciate ligament replacement: comparison of bone-patellar tendon-bone grafts with two-strand hamstring grafts. A prospective, randomized study. J Bone Joint Surg Am 84:1503–1513PubMedGoogle Scholar
  7. 7.
    Biau DJ, Katsahian S, Nizard R (2007) Hamstring tendon autograft better than bone-patellar tendon-bone autograft in ACL reconstruction—a cumulative meta-analysis and clinically relevant sensitivity analysis applied to a previously published analysis. Acta Orthop 78:705–707CrossRefPubMedGoogle Scholar
  8. 8.
    Chen CH, Chen WJ, Shih CH et al (2003) Enveloping the tendon graft with periosteum to enhance tendon-bone healing in a bone tunnel: a biomechanical and histologic study in rabbits. Arthroscopy 19:290–296CrossRefPubMedGoogle Scholar
  9. 9.
    Chen CH, Liu HW, Tsai CL et al (2008) Photoencapsulation of bone morphogenetic protein-2 and periosteal progenitor cells improve tendon graft healing in a bone tunnel. Am J Sports Med 36:461–473CrossRefPubMedGoogle Scholar
  10. 10.
    Christen B, Jakob RP (1992) Fractures associated with patellar ligament grafts in cruciate ligament surgery. J Bone Joint Surg Br 74:617–619PubMedGoogle Scholar
  11. 11.
    Demirag B, Sarisozen B, Ozer O et al (2005) Enhancement of tendon-bone healing of anterior cruciate ligament grafts by blockage of matrix metalloproteinases. J Bone Joint Surg Am 87:2401–2410CrossRefPubMedGoogle Scholar
  12. 12.
    Denti M, Lo Vetere D, Bait C et al (2008) Revision anterior cruciate ligament reconstruction: causes of failure, surgical technique, and clinical results. Am J Sports Med 36:1896–1902CrossRefPubMedGoogle Scholar
  13. 13.
    Ejerhed L, Kartus J, Sernert N et al (2003) Patellar tendon or semitendinosus tendon autografts for anterior cruciate ligament reconstruction? A prospective randomized study with a 2-year follow-up. Am J Sports Med 31:19–25PubMedGoogle Scholar
  14. 14.
    Ferretti A, Conteduca F, Monaco E et al (2006) Revision anterior cruciate ligament reconstruction with doubled semitendinosus and gracilis tendons and lateral extra-articular reconstruction. J Bone Joint Surg Am 88:2373–2379CrossRefPubMedGoogle Scholar
  15. 15.
    Goradia VK (2003) Tendon healing in a bone tunnel. Parts I and II. Arthroscopy 19:111CrossRefPubMedGoogle Scholar
  16. 16.
    Goradia VK, Rochat MC, Grana WA et al (2000) Tendon-to-bone healing of a semitendinosus tendon autograft used for ACL reconstruction in a sheep model. Am J Knee Surg 13:143–151PubMedGoogle Scholar
  17. 17.
    Goradia VK, Rochat MC, Kida M et al (2000) Natural history of a hamstring tendon autograft used for anterior cruciate ligament reconstruction in a sheep model. Am J Sports Med 28:40–46PubMedGoogle Scholar
  18. 18.
    Gorden M, Stein M (2004) Anterior cruciate ligament injuries. In: Garrick J (ed) Orthopaedic knowledge update: sports medicine. American Academy of Orthopaedic Surgeons, Rosemont, pp 169–181Google Scholar
  19. 19.
    Gulotta LV, Kovacevic D, Ying L et al (2008) Augmentation of tendon-to-bone healing with a magnesium-based bone adhesive. Am J Sports Med 36:1290–1297CrossRefPubMedGoogle Scholar
  20. 20.
    Hays PL, Kawamura S, Deng XH et al (2008) The role of macrophages in early healing of a tendon graft in a bone tunnel. J Bone Joint Surg Am 90:565–579CrossRefPubMedGoogle Scholar
  21. 21.
    Hopper RA, Zhang JR, Fourasier VL et al (2001) Effect of isolation of periosteum and dura on the healing of rabbit calvarial inlay bone grafts. Plast Reconstr Surg 107:454–462CrossRefPubMedGoogle Scholar
  22. 22.
    Huangfu X, Zhao J (2007) Tendon-bone healing enhancement using injectable tricalcium phosphate in a dog anterior cruciate ligament reconstruction model. Arthroscopy 23:455–462CrossRefPubMedGoogle Scholar
  23. 23.
    Jansson KA, Linko E, Sandelin J et al (2003) A prospective randomized study of patellar versus hamstring tendon autografts for anterior cruciate ligament reconstruction. Am J Sports Med 31:12–18PubMedGoogle Scholar
  24. 24.
    Kanazawa T, Soejima T, Murakami H et al (2006) An immunohistological study of the integration at the bone-tendon interface after reconstruction of the anterior cruciate ligament in rabbits. J Bone Joint Surg Br 88:682–687CrossRefPubMedGoogle Scholar
  25. 25.
    Kawaguchi H, Kurokawa T, Hoshino Y et al (1992) Immunohistochemical demonstration of bone morphogenetic protein-2 and transforming growth factor-beta in the ossification of the posterior longitudinal ligament of the cervical spine. Spine 17:S33–S36CrossRefPubMedGoogle Scholar
  26. 26.
    Kawamura S, Ying L, Kim HJ et al (2005) Macrophages accumulate in the early phase of tendon-bone healing. J Orthop Res 23:1425–1432PubMedGoogle Scholar
  27. 27.
    Kobayashi M, Watanabe N, Oshima Y et al (2005) The fate of host and graft cells in early healing of bone tunnel after tendon graft. Am J Sports Med 33:1892–1897CrossRefPubMedGoogle Scholar
  28. 28.
    Kohno T, Ishibashi Y, Tsuda E et al (2007) Immunohistochemical demonstration of growth factors at the tendon-bone interface in anterior cruciate ligament reconstruction using a rabbit model. J Orthop Sci 12:67–73CrossRefPubMedGoogle Scholar
  29. 29.
    Krych AJ, Jackson JD, Hoskin TL et al (2008) A meta-analysis of patellar tendon autograft versus patellar tendon allograft in anterior cruciate ligament reconstruction. Arthroscopy 24:292–298CrossRefPubMedGoogle Scholar
  30. 30.
    Kyung HS, Kim SY, Oh CW et al (2003) Tendon-to-bone tunnel healing in a rabbit model: the effect of periosteum augmentation at the tendon-to-bone interface. Knee Surg Sports Traumatol Arthrosc 11:9–15PubMedGoogle Scholar
  31. 31.
    Lattermann C, Zelle BA, Whalen JD et al (2004) Gene transfer to the tendon-bone insertion site. Knee Surg Sports Traumatol Arthrosc 12:510–515CrossRefPubMedGoogle Scholar
  32. 32.
    Lawhorn KW, Howell SM (2007) Principles for using hamstring tendons for anterior cruciate ligament reconstruction. Clin Sports Med 26:567–585CrossRefPubMedGoogle Scholar
  33. 33.
    Lee GH, McCulloch P, Cole BJ et al (2008) The incidence of acute patellar tendon harvest complications for anterior cruciate ligament reconstruction. Arthroscopy 24:162–166CrossRefPubMedGoogle Scholar
  34. 34.
    Lim JK, Hui J, Li L et al (2004) Enhancement of tendon graft osteointegration using mesenchymal stem cells in a rabbit model of anterior cruciate ligament reconstruction. Arthroscopy 20:899–910PubMedGoogle Scholar
  35. 35.
    Liu SH, Panossian V, al-Shaikh R et al (1997) Morphology and matrix composition during early tendon to bone healing. Clin Orthop Relat Res 339:253–260CrossRefPubMedGoogle Scholar
  36. 36.
    Ma CB, Kawamura S, Deng XH et al (2007) Bone morphogenetic proteins-signaling plays a role in tendon-to-bone healing: a study of rhBMP-2 and noggin. Am J Sports Med 35:597–604CrossRefPubMedGoogle Scholar
  37. 37.
    Martinek V, Latterman C, Usas A et al (2002) Enhancement of tendon-bone integration of anterior cruciate ligament grafts with bone morphogenetic protein-2 gene transfer: a histological and biomechanical study. J Bone Joint Surg Am 84:1123–1131PubMedGoogle Scholar
  38. 38.
    Marumoto JM, Mitsunaga MM, Richardson AB et al (1996) Late patellar tendon ruptures after removal of the central third for anterior cruciate ligament reconstruction. A report of two cases. Am J Sports Med 24:698–701CrossRefPubMedGoogle Scholar
  39. 39.
    Mihelic R, Pecina M, Jelic M et al (2004) Bone morphogenetic protein-7 (osteogenic protein-1) promotes tendon graft integration in anterior cruciate ligament reconstruction in sheep. Am J Sports Med 32:1619–1625CrossRefPubMedGoogle Scholar
  40. 40.
    Miyamoto S, Takaoka K, Yonenobu K et al (1992) Ossification of the ligamentum flavum induced by bone morphogenetic protein. An experimental study in mice. J Bone Joint Surg Br 74:279–283PubMedGoogle Scholar
  41. 41.
    Mutsuzaki H, Sakane M, Nakajima H et al (2004) Calcium-phosphate-hybridized tendon directly promotes regeneration of tendon-bone insertion. J Biomed Mater Res A 70:319–327CrossRefPubMedGoogle Scholar
  42. 42.
    O’Driscoll SW, Recklies AD, Poole AR (1994) Chondrogenesis in periosteal explants. An organ culture model for in vitro study. J Bone Joint Surg Am 76:1042–1051PubMedGoogle Scholar
  43. 43.
    Ohtera K, Yamada Y, Aoki M et al (2000) Effects of periosteum wrapped around tendon in a bone tunnel: A biomechanical and histological study in rabbits. Crit Rev Biomed Eng 28:115–118PubMedGoogle Scholar
  44. 44.
    Ouyang HW, Goh JC, Lee EH (2004) Use of bone marrow stromal cells for tendon graft-to-bone healing: histological and immunohistochemical studies in a rabbit model. Am J Sports Med 32:321–327CrossRefPubMedGoogle Scholar
  45. 45.
    Panni AS, Milano G, Lucania L et al (1997) Graft healing after anterior cruciate ligament reconstruction in rabbits. Clin Orthop Relat Res 343:203–212CrossRefPubMedGoogle Scholar
  46. 46.
    Park MJ, Lee MC, Seong SC (2001) A comparative study of the healing of tendon autograft and tendon-bone autograft using patellar tendon in rabbits. Int Orthop 25:35–39CrossRefPubMedGoogle Scholar
  47. 47.
    Petersen W, Laprell H (2000) Insertion of autologous tendon grafts to the bone: a histological and immunohistochemical study of hamstring and patellar tendon grafts. Knee Surg Sports Traumatol Arthrosc 8:26–31CrossRefPubMedGoogle Scholar
  48. 48.
    Petrigliano FA, McAllister DR, Wu BM (2006) Tissue engineering for anterior cruciate ligament reconstruction: a review of current strategies. Arthroscopy 22:441–451CrossRefPubMedGoogle Scholar
  49. 49.
    Pinczewski LA, Clingeleffer AJ, Otto DD et al (1997) Integration of hamstring tendon graft with bone in reconstruction of the anterior cruciate ligament. Arthroscopy 13:641–643CrossRefPubMedGoogle Scholar
  50. 50.
    Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147CrossRefPubMedGoogle Scholar
  51. 51.
    Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74CrossRefPubMedGoogle Scholar
  52. 52.
    Ritsila VA, Santavirta S, Alhopuro S et al (1994) Periosteal and perichondral grafting in reconstructive surgery. Clin Orthop Relat Res 302:259–265PubMedGoogle Scholar
  53. 53.
    Robert H, Es-Sayeh J (2004) The role of periosteal flap in the prevention of femoral widening in anterior cruciate ligament reconstruction using hamstring tendons. Knee Surg Sports Traumatol Arthrosc 12:30–35CrossRefPubMedGoogle Scholar
  54. 54.
    Robertson WJ, Hatch JD, Rodeo SA (2007) Evaluation of tendon graft fixation using alpha-BSM calcium phosphate cement. Arthroscopy 23:1087–1092CrossRefPubMedGoogle Scholar
  55. 55.
    Rodeo SA (1999) Knee pain in competitive swimming. Clin Sports Med 18:379–387CrossRefPubMedGoogle Scholar
  56. 56.
    Rodeo SA, Arnoczky SP, Torzilli PA et al (1993) Tendon-healing in a bone tunnel. A biomechanical and histological study in the dog. J Bone Joint Surg Am 75:1795–1803PubMedGoogle Scholar
  57. 57.
    Rodeo SA, Kawamura S, Kim HJ et al (2006) Tendon healing in a bone tunnel differs at the tunnel entrance versus the tunnel exit: an effect of graft-tunnel motion? Am J Sports Med 34:1790–1800CrossRefPubMedGoogle Scholar
  58. 58.
    Rodeo SA, Suzuki K, Deng XH et al (1999) Use of recombinant human bone morphogenetic protein-2 to enhance tendon healing in a bone tunnel. Am J Sports Med 27:476–488PubMedGoogle Scholar
  59. 59.
    Rubin C, Bolander M, Ryaby JP et al (2001) The use of low-intensity ultrasound to accelerate the healing of fractures. J Bone Joint Surg Am 83:259–270CrossRefPubMedGoogle Scholar
  60. 60.
    Sakai H, Fukui N, Kawakami A et al (2000) Biological fixation of the graft within bone after anterior cruciate ligament reconstruction in rabbits: effects of the duration of postoperative immobilization. J Orthop Sci 5:43–51CrossRefPubMedGoogle Scholar
  61. 61.
    Sasaki K, Kuroda R, Ishida K et al (2008) Enhancement of tendon-bone osteointegration of anterior cruciate ligament graft using granulocyte colony-stimulating factor. Am J Sports Med 36:1519–1527CrossRefPubMedGoogle Scholar
  62. 62.
    Sharma P, Maffulli N (2005) Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg Am 87:187–202CrossRefPubMedGoogle Scholar
  63. 63.
    Shelbourne KD, Carr DR (2003) Meniscal repair compared with meniscectomy for bucket-handle medial meniscal tears in anterior cruciate ligament-reconstructed knees. Am J Sports Med 31:718–723PubMedGoogle Scholar
  64. 64.
    Shino K, Kawasaki T, Hirose H et al (1984) Replacement of the anterior cruciate ligament by an allogeneic tendon graft. An experimental study in the dog. J Bone Joint Surg Br 66:672–681PubMedGoogle Scholar
  65. 65.
    Soon MY, Hassan A, Hui JH et al (2007) An analysis of soft tissue allograft anterior cruciate ligament reconstruction in a rabbit model: a short-term study of the use of mesenchymal stem cells to enhance tendon osteointegration. Am J Sports Med 35:962–971CrossRefPubMedGoogle Scholar
  66. 66.
    Spalazzi JP, Dagher E, Doty SB et al (2008) In vivo evaluation of a multiphased scaffold designed for orthopaedic interface tissue engineering and soft tissue-to-bone integration. J Biomed Mater Res A 86:1–12PubMedGoogle Scholar
  67. 67.
    Sun JS, Hong RC, Chang WH et al (2001) In vitro effects of low-intensity ultrasound stimulation on the bone cells. J Biomed Mater Res 57:449–456CrossRefPubMedGoogle Scholar
  68. 68.
    Takakura Y, Matsui N, Yoshiya S et al (2002) Low-intensity pulsed ultrasound enhances early healing of medial collateral ligament injuries in rats. J Ultrasound Med 21:283–288PubMedGoogle Scholar
  69. 69.
    Tien YC, Chih TT, Lin JH et al (2004) Augmentation of tendon-bone healing by the use of calcium-phosphate cement. J Bone Joint Surg Br 86:1072–1076CrossRefPubMedGoogle Scholar
  70. 70.
    Tom JA, Rodeo SA (2002) Soft tissue allografts for knee reconstruction in sports medicine. Clin Orthop Relat Res 402:135–156CrossRefPubMedGoogle Scholar
  71. 71.
    Tomita F, Yasuda K, Mikami S et al (2001) Comparisons of intraosseous graft healing between the doubled flexor tendon graft and the bone-patellar tendon-bone graft in anterior cruciate ligament reconstruction. Arthroscopy 17:461–476CrossRefPubMedGoogle Scholar
  72. 72.
    Walsh WR, Stephens P, Vizesi F et al (2007) Effects of low-intensity pulsed ultrasound on tendon-bone healing in an intra-articular sheep knee model. Arthroscopy 23:197–204CrossRefPubMedGoogle Scholar
  73. 73.
    Wang CJ, Huang HY, Chen HH et al (2001) Effect of shock wave therapy on acute fractures of the tibia: a study in a dog model. Clin Orthop Relat Res: 11:2–118Google Scholar
  74. 74.
    Wang CJ, Huang HY, Pai CH (2002) Shock wave-enhanced neovascularization at the tendon-bone junction: an experiment in dogs. J Foot Ankle Surg 41:16–22CrossRefPubMedGoogle Scholar
  75. 75.
    Wang CJ, Wang FS, Yang KD et al (2003) Shock wave therapy induces neovascularization at the tendon-bone junction. A study in rabbits. J Orthop Res 21:984–989CrossRefPubMedGoogle Scholar
  76. 76.
    Wang CJ, Wang FS, Yang KD et al (2005) The effect of shock wave treatment at the tendon-bone interface-an histomorphological and biomechanical study in rabbits. J Orthop Res 23:274–280CrossRefPubMedGoogle Scholar
  77. 77.
    Wang CJ, Yang KD, Wang FS et al (2004) Shock wave treatment shows dose-dependent enhancement of bone mass and bone strength after fracture of the femur. Bone 34:225–230CrossRefPubMedGoogle Scholar
  78. 78.
    Waselau M, Samii VF, Weisbrode SE et al (2007) Effects of a magnesium adhesive cement on bone stability and healing following a metatarsal osteotomy in horses. Am J Vet Res 68:370–378CrossRefPubMedGoogle Scholar
  79. 79.
    Weiler A, Hoffmann RF, Bail HJ et al (2002) Tendon healing in a bone tunnel. Part II: Histologic analysis after biodegradable interference fit fixation in a model of anterior cruciate ligament reconstruction in sheep. Arthroscopy 18:124–135CrossRefPubMedGoogle Scholar
  80. 80.
    Xiao YT, Xiang LX, Shao JZ (2007) Bone morphogenetic protein. Biochem Biophys Res Commun 362:550–553CrossRefPubMedGoogle Scholar
  81. 81.
    Yamazaki S, Yasuda K, Tomita F et al (2005) The effect of transforming growth factor-beta1 on intraosseous healing of flexor tendon autograft replacement of anterior cruciate ligament in dogs. Arthroscopy 21:1034–1041CrossRefPubMedGoogle Scholar
  82. 82.
    Youn I, Jones DG, Andrews PJ et al (2004) Periosteal augmentation of a tendon graft improves tendon healing in the bone tunnel. Clin Orthop Relat Res 419:223–231CrossRefPubMedGoogle Scholar
  83. 83.
    Young RG, Butler DL, Weber W et al (1998) Use of mesenchymal stem cells in a collagen matrix for Achilles tendon repair. J Orthop Res 16:406–413CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Guan-Ming Kuang
    • 1
    Email author
  • W. P. Yau
    • 1
  • William W. Lu
    • 1
  • K. Y. Chiu
    • 1
  1. 1.Department of Orthopaedics and Traumatology, LKS Faculty of MedicineThe University of Hong KongPokfulamHong Kong

Personalised recommendations