Intra‐articular remodelling of hamstring tendon grafts after anterior cruciate ligament reconstruction

Abstract

Purpose A summary is provided on the existing knowledge about the specific healing phases of the intra‐articular hamstring tendon graft used for ACL reconstruction. Differences between human and animal in vivo studies are explained, and implications for the postoperative time period are laid out. Methods A systematic review of the existing literature was performed on the topic of tendon remodelling of hamstring grafts in ACL reconstruction using Medline database. Publications between 1982 and 2012 were included. Special focus was directed on in vivo human and animal studies analysing intra‐articular free tendon graft remodelling. Results Animal and human in vitro and vivo researches have demonstrated three characteristic stages of graft healing after ACL reconstruction: an early graft healing phase with central graft necrosis and hypocellularity and no detectable revascularization of the graft tissue, followed by a phase of proliferation, the time of most intensive remodelling and revascularization and finally, a ligamentization phase with characteristic restructuring of the graft towards the properties of the intact ACL. However, a full restoration of either the biological or biomechanical properties of the intact ACL is not achieved. Conclusion Significant knowledge on human cruciate ligament remodelling has been added in the understanding of the processes during the course of graft healing. Most importantly, the remodelling process in humans is prolonged compared to animal studies. While today´s rehabilitation protocols are often extrapolated from findings of animal in vivo healing studies, current findings of human in vivo healing studies might require new post‐operative regimens following hamstring ACL reconstruction.

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References 66

1. 1.

   Abe S, Kurosaka M, Iguchi T, et al. Light and electron microscopic study of remodeling and maturation process in autogenous graft for anterior cruciate ligament reconstruction. Arthroscopy. 1993;9:394-405.

   Not in our library10.1016/s0749-8063(05)80313-5

2. 2.

   Amiel D, Frank C, Harwood F, et al. Tendons and ligaments: a morphological and biochemical comparison. J Orthop Res. 1984;1:257-265.

   Not in our library10.1002/jor.1100010305

3. 3.

   Amiel D, Kleiner JB, Akeson WH. The natural history of the anterior cruciate ligament autograft of patellar tendon origin. Am J Sports Med. 1986;14:449-462.

   Not in our library10.1177/036354658601400603

4. 4.

   Amiel D, Kleiner JB, Roux RD, et al. The phenomenon of “ligamentization”: anterior cruciate ligament reconstruction with autogenous patellar tendon. J Orthop Res. 1986;4:162-172.

   Not in our library10.1002/jor.1100040204

5. 5.

   Arnoczky SP, Tarvin GB, Marshall JL (1982) Anterior cruciate ligament replacement using patellar tendon. An evaluation of graft revascularization in the dog. J Bone Joint Surg 64-A:217–224

   Not in our library

6. 6.

   Ballock RT, Woo SL, Lyon RM, et al. Use of patellar tendon autograft for anterior cruciate ligament reconstruction in the rabbit: a long-term histologic and biomechanical study. J Orthop Res. 1989;7:474-485.

   Not in our library10.1002/jor.1100070404

7. 7.

   Beynnon BD, Uh BS, Johnson RJ, et al. Rehabilitation after anterior cruciate ligament reconstruction: a prospective, randomized, double-blind comparison of programs administered over 2 different time intervals. Am J Sports Med. 2005;33:347-359.

   Not in our library10.1177/0363546504268406

8. 8.

   Beynnon BD, Johnson RJ, Naud S, et al. Accelerated versus nonaccelerated rehabilitation after anterior cruciate ligament reconstruction: a prospective, randomized, double blind investigation evaluating knee joint laxity using stereophotogrammetric analysis. Am J Sports Med. 2011;39:2536-2548.

   Not in our library10.1177/0363546511422349

9. 9.

   Blickenstaff KR, Grana WA, Egle D. Analysis of a semitendinosus autograft in a rabbit model. Am J Sports Med. 1997;25:554-559.

   Not in our library10.1177/036354659702500420

10. 10.

    Claes S, Verdonk P, Forsyth R, et al. The “ligamentization” process in anterior cruciate ligament reconstruction: what happens to the human graft? A systematic review of the literature. Am J Sports Med. 2011;39:2476-2483.

    Not in our library10.1177/0363546511402662

11. 11.

    Dustmann M, Schmidt T, Gangey I, et al. The extracellular remodeling of free-soft-tissue autografts and allografts for reconstruction of the anterior cruciate ligament: a comparison study in sheep model. Knee Surg Sports Traumatol Arthrosc. 2008;16:360-369.

    Not in our library10.1007/s00167-007-0471-0

12. 12.

    Falconiero RP, Distefano VJ, Cook TM. Revascularization and ligamentization of autogenous anterior cruciate ligament grafts in humans. Arthroscopy. 1998;14:197-205.

    Not in our library10.1016/s0749-8063(98)70041-6

13. 13.

    Figueroa D, Melena P, Calco R, et al. Magnetic resonance imaging evaluation of the integration and maturation of semitendinosus-gracilis graft in anterior cruciate ligament reconstruction using autologous platelet concentrate. Arthroscopy. 2010;26:1318-1325.

    Not in our library10.1016/j.arthro.2010.02.010

14. 14.

    Fujimoto E, Sumen Y, Urabe Y, et al. An early return to vigorous activity may destabilize anterior cruciate ligaments reconstructed with hamstring grafts. Arch Phys Med Rehabil. 2004;85:298-302.

    Not in our library10.1016/s0003-9993(03)00621-x

15. 15.

    Gohil S, Annear PO, Breidahl W (2007) Anterior cruciate ligament reconstruction using autologous double hamstrings: a comparison of standard versus minimal debridement techniques using MRI to assess revascularization. J Bone J Surg 89-B:1165–1171

    Not in our library10.1302/0301-620x.89b9.19339

16. 16.

    Goradia VK, Rochat MC, Grana WA, et al. Tendon-to-bone healing of a semitendinosus tendon autograft used for ACL reconstruction in a sheep model. Am J Knee Surg. 2000;13:143-151.

    Not in our library

17. 17.

    Grana WA, Egle DM, Mahnken R, et al. An analysis of autograft fixation after anterior cruciate ligament reconstruction in a rabbit model. Am J Sports Med. 1994;22:344-351.

    Not in our library10.1177/036354659402200309

18. 18.

    Howell SM, Knox KE, Farley TE, et al. Revascularization of a human anterior cruciate ligament graft during the first two years of implantation. Am J Sports Med. 1995;23:42-49.

    Not in our library10.1177/036354659502300107

19. 19.

    Howell SM, Taylor MA (1996) Brace–free rehabilitation, with early return to activity, for knees reconstructed with a double-looped semitendinosus and gracilis graft. J Bone Joint Surg 78-A:814–825

    Not in our library10.2106/00004623-199606000-00003

20. 20.

    Jackson DW, Grood ES, Cohn BT et al (1991) The effects of in situ freezing on the anterior cruciate ligament. An experimental study in goats. J Bone Joint Surg 73-A:201–213

    Not in our library

21. 21.

    Jackson DW, Grood ES, Goldstein JD, et al. A comparison of patellar tendon autograft and allograft used for anterior cruciate ligament reconstruction in the goat model. Am J Sports Med. 1993;21:176-185.

    Not in our library10.1177/036354659302100203

22. 22.

    Jackson JR, Minton JA, Ho ML, et al. Expression of vascular endothelial growth factor in synovial fibroblasts is induced by hypoxia and interleukin 1beta. J Rheumatol. 1997;24:1253-1259.

    Not in our library

23. 23.

    Janssen RP, Du Mée AW, Valkenburg VJ, et al. Anterior cruciate ligament reconstruction with hamstring tendons and accelerated rehabilitation: a 10-year prospective study on clinical results, knee osteoarthritis and its predictors. Knee Surg Sports Traumatol Arthrosc. 2012.

    Not in our library10.1007/s00167-012-2234-9

24. 24.

    Janssen RP, van der Wijk J, Fiedler A, et al. Remodelling of human hamstring autografts after anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc. 2011;19:1299-1306.

    Not in our library10.1007/s00167-011-1419-y

25. 25.

    Johnson LL. The outcome of a free autogenous semitendinosus tendon graft in human anterior cruciate reconstructive surgery: a histological study. Arthroscopy. 1993;9:131-142.

    Not in our library10.1016/s0749-8063(05)80362-7

26. 26.

    Kawamura S, Ying L, Kim HJ, et al. Macrophages accumulate in the early phase of tendon-bone healing. J Orthop Res. 2005;23:1425-1432.

    Not in our library10.1016/j.orthres.2005.01.014

27. 27.

    Kleiner JB, Amiel D, Harwood FL, et al. Early histological, metabolic, and vascular assessment of anterior cruciate ligament autografts. J Orthop Res. 1989;7:235-242.

    Not in our library10.1002/jor.1100070211

28. 28.

    Kleiner JB, Amiel D, Roux RD, et al. Origin of replacement cells for the anterior cruciate ligament autograft. J Orthop Res. 1986;4:466-474.

    Not in our library10.1002/jor.1100040410

29. 29.

    Kuroda R, Kurosaka M, Yoshiya S, et al. Localization of growth factors in the reconstructed anterior cruciate ligament: immunohistological study in dogs. Knee Surg Sports Traumatol Arthrosc. 2000;8:120-126.

    Not in our library10.1007/s001670050198

30. 30.

    Lane JG, McFadden P, Bowden K, et al. The ligamentization process: a 4 year case study following ACL reconstruction with a semitendinosis graft. Arthroscopy. 1993;9:149-153.

    Not in our library10.1016/s0749-8063(05)80364-0

31. 31.

    Liu SH, Yang RS, Al-Shaikh R, et al. Collagen in tendon, ligament, and bone healing. A current review. Clin Orthop Relat Res. 1995;318:265-278.

    Not in our library

32. 32.

    McFarland EG. The biology of anterior cruciate ligament reconstructions. Orthopedics. 1993;16:403-410.

    Not in our library10.3928/0147-7447-19930401-04

33. 33.

    Marumo K, Saito M, Yamagishi T, et al. The “ligamentization” process in human anterior cruciate ligament reconstruction with autogenous patellar and hamstring tendons. Am J Sports Med. 2005;33:1166-1173.

    Not in our library10.1177/0363546504271973

34. 34.

    Mayr HO, Stoehr A, Dietrich M, et al. Graft-dependent differences in the ligamentization process of anterior cruciate ligament grafts in a sheep trial. Knee Surg Sports Traumatol Arthrosc. 2012;20:947-956.

    Not in our library10.1007/s00167-011-1678-7

35. 35.

    Ménétrey J, Duthon VB, Laumonier T, et al. “Biological failure” of the anterior cruciate ligament graft. Knee Surg Sports Traumatol Arthrosc. 2008;16:224-231.

    Not in our library10.1007/s00167-007-0474-x

36. 36.

    Murray MM, Martin SD, Martin TL et al (2000) Histological changes in the human anterior cruciate ligament after rupture. J Bone Joint Surg 82-A:1387–1397

    Not in our library10.2106/00004623-200010000-00004

37. 37.

    Ng GY, Oakes BW, Deacon OW, et al. Biomechanics of patellar tendon autograft for reconstruction of the anterior cruciate ligament in the goat: three-year study. J Orthop Res. 1995;13:602-608.

    Not in our library10.1002/jor.1100130416

38. 38.

    Ng GY, Oakes BW, Deacon OW, et al. Long-term study of the biochemistry and biomechanics of anterior cruciate ligament-patellar tendon autografts in goats. J Orthop Res. 1996;14:851-856.

    Not in our library10.1002/jor.1100140602

39. 39.

    Ohno K, Yasuda K, Yamamoto N, et al. Effects of complete stress-shielding on the mechanical properties and histology of in situ frozen patellar tendon. J Orthop Res. 1993;11:592-602.

    Not in our library10.1002/jor.1100110414

40. 40.

    Papageorgiou CD, Ma CB, Abramowitch SD, et al. A multidisciplinary study of the healing of an intra-articular anterior cruciate ligament graft in a goat model. Am J Sports Med. 2001;29:620-626.

    Not in our library10.1177/03635465010290051501

41. 41.

    Papalia R, Franceschi F, Vasta S, et al. Sparing the anterior cruciate ligament remnant: is it worth the hassle? Br Med Bull. 2012;104:91-111.

    Not in our library10.1093/bmb/ldr053

42. 42.

    Petersen W, Wildemann B, Pufe T, et al. The angiogenic peptide pleiotrophin (PTN/HB-GAM) is expressed in fracture healing: an immunohistochemical study in rats. Arch Orthop Trauma Surg. 2003;124:603-607.

    Not in our library10.1007/s00402-003-0582-0

43. 43.

    Rougraff BT, Shelbourne KD. Early histologic appearance of human patellar tendon autografts used for anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc. 1999;7:9-14.

    Not in our library10.1007/s001670050113

44. 44.

    Sanchez M, Anitua E, Azofra J, et al. Ligamentization of tendon grafts treated with an endogenous preparation rich in growth factors: gross morphology and histology. Arthroscopy. 2010;26:470-480.

    Not in our library10.1016/j.arthro.2009.08.019

45. 45.

    Scheffler SU, Scherler J, Pruss A, et al. Biomechanical comparison of human bone-patellar tendon-bone grafts after sterilization with peracetic acid ethanol. Cell Tissue Bank. 2005;6:109-115.

    Not in our library10.1007/s10561-004-6403-z

46. 46.

    Scheffler SU, Unterhauser FN, Weiler A. Graft remodeling and ligamentization after cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc. 2008;16:834-842.

    Not in our library10.1007/s00167-008-0560-8

47. 47.

    Scranton PE, Lanzer WL, Ferguson MS, et al. Mechanisms of anterior cruciate ligament neovascularization and ligamentization. Arthroscopy. 1998;14:702-716.

    Not in our library10.1016/s0749-8063(98)70097-0

48. 48.

    Seitz H, Menth-Chiari WA, Lang S, et al. Histological evaluation of the healing potential of the anterior cruciate ligament by means of augmented and non-augmented repair: an in vivo animal study. Knee Surg Sports Traumatol Arthrosc. 2008;16:1087-1093.

    Not in our library10.1007/s00167-008-0599-6

49. 49.

    Shelbourne KD, Nitz P. Accelerated rehabilitation after anterior cruciate ligament reconstruction. Am J Sports Med. 1990;18:292-299.

    Not in our library10.1177/036354659001800313

50. 50.

    Shino K, Horibe S. Experimental ligament reconstruction by allogeneic tendon graft in a canine model. Acta Orthop Belg. 1991;57(Suppl 2):44-53.

    Not in our library

51. 51.

    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 66-B:672–681

    Not in our library10.1302/0301-620x.66b5.6501359

52. 52.

    Spindler KP, Andrish JT, Miller RR, et al. Distribution of cellular repopulation and collagen synthesis in a canine anterior cruciate ligament autograft. J Orthop Res. 1996;14:384-389.

    Not in our library10.1002/jor.1100140307

53. 53.

    Stener S, Ejerhed L, Movin T, et al. The reharvested patellar tendon has the potential for ligamentization when used for anterior cruciate ligament revision surgery. Knee Surg Sports Traumatol Arthrosc. 2012;20:1168-1174.

    Not in our library10.1007/s00167-012-1908-7

54. 54.

    Tohyama H, Yasuda K (2002) The effect of increased stress on the patellar tendon. J Bone Joint Surg 84-B:440–446

    Not in our library10.1302/0301-620x.84b3.11107

55. 55.

    Unterhauser FN, Bail HJ, Höher J, et al. Endoligamentous revascularization of an anterior cruciate ligament graft. Clin Orthop Relat Res. 2003;414:276-288.

    Not in our library10.1097/01.blo.0000079442.64912.51

56. 56.

    Unterhauser FN, Bosch U, Zeichen J, et al. Alpha-smooth muscle actin containing contractile fibroblastic cells in human knee arthrofibrosis tissue. Winner of the AGA-DonJoy Award 2003. Arch Orthop Trauma Surg. 2004;124:585-591.

    Not in our library10.1007/s00402-004-0742-x

57. 57.

    Vogrin M, Rupreht M, Dinevski D, et al. Effects of a platelet gel on early graft revascularization after anterior cruciate ligament reconstruction: a prospective randomized, double-blind, clinical trial. Eur Surg Res. 2010;45:77-85.

    Not in our library10.1159/000318597

58. 58.

    Weiler A, Förster C, Hunt P, et al. The influence of locally applied platelet-derived growth factor-BB on free tendon graft remodeling after anterior cruciate ligament reconstruction. Am J Sports Med. 2004;32:881-891.

    Not in our library10.1177/0363546503261711

59. 59.

    Weiler A, Hoffmann RF, Bail HJ, et al. Tendon healing in a bone tunnel. Part II: histological analysis after biodegradable interference fit fixation in a model of anterior cruciate ligament reconstruction in sheep. Arthroscopy. 2002;18:124-135.

    Not in our library10.1053/jars.2002.30657

60. 60.

    Weiler A, Peine R, Pahminez-Azar A, et al. Tendon healing in a bone tunnel. Part I: biomechanical results after biodegradable interference fit fixation in a model of anterior cruciate ligament reconstruction in sheep. Arthroscopy. 2002;18:113-123.

    Not in our library10.1053/jars.2002.30656

61. 61.

    Weiler A, Peters G, Mäurer J, et al. Biomechanical properties and vascularity of an anterior cruciate ligament graft can be predicted by contrast-enhanced magnetic resonance imaging. A two-year study in sheep. Am J Sports Med. 2001;29:751-761.

    Not in our library10.1177/03635465010290061401

62. 62.

    Weiler A, Unterhauser FN, Bail HJ, et al. Alpha-smooth muscle actin is expressed by fibroblastic cells of the ovine anterior cruciate ligament and its free tendon graft during remodeling. J Orthop Res. 2002;20:310-317.

    Not in our library10.1016/s0736-0266(01)00109-7

63. 63.

    Xu Y, Ao Y. Histological and biomechanical studies of inter-strand healing in four-strand autograft anterior cruciate ligament reconstruction in a rabbit model. Knee Surg Sports Traumatol Arthrosc. 2009;17:770-777.

    Not in our library10.1007/s00167-009-0764-6

64. 64.

    Yoshikawa T, Tohyama H, Katsura T. 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. 2006;34:1918-1925.

    Not in our library10.1177/0363546506294469

65. 65.

    Zaffagnini S, De Pasquale V, Marchesini Reggiani L, et al. Neoligamentization process of BTPB used for ACL graft: histological evaluation from 6 months to 10 years. Knee. 2007;14:87-93.

    Not in our library10.1016/j.knee.2006.11.006

66. 66.

    Zaffagnini S, De Pasquale V, Marchesini Reggiani L. Electron microscopy of the remodelling process in hamstring tendon used as ACL graft. Knee Surg Sports Traumatol Arthrosc. 2010;18:1052105-1052108.

    Not in our library10.1007/s00167-009-0925-7

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