Cited by 225Knee injuries and reconstruction techniquesTendon Structure and TreatmentPeriodontal Regeneration and Treatments

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

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Janssen, Rob P. A., Scheffler, Sven U.·2014·Knee Surgery, Sports Traumatology, Arthroscopy

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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  1. [1]Abe S Kurosaka M Iguchi T Light and electron microscopic study of remodeling and maturation process in autogenous graft for anterior cruciate ligament reconstruction Arthroscopy 1993 9 394 405 10.1016/S0749-8063(05)80313-5 8216570 · DOI
  2. [2]Amiel D Frank C Harwood F Tendons and ligaments: a morphological and biochemical comparison J Orthop Res 1984 1 257 265 10.1002/jor.1100010305 6481509 · DOI
  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 10.1177/036354658601400603 3799871 · DOI
  4. [4]Amiel D Kleiner JB Roux RD The phenomenon of “ligamentization”: anterior cruciate ligament reconstruction with autogenous patellar tendon J Orthop Res 1986 4 162 172 10.1002/jor.1100040204 3712125 · DOI
  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 7056776
  6. [6]Ballock RT Woo SL Lyon RM 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 10.1002/jor.1100070404 2738766 · DOI · Paper page
  7. [7]Beynnon BD Uh BS Johnson RJ 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 10.1177/0363546504268406 15716250 · DOI
  8. [8]Beynnon BD Johnson RJ Naud S 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 10.1177/0363546511422349 21952714 · DOI
  9. [10]Claes S Verdonk P Forsyth R 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 10.1177/0363546511402662 21515806 · DOI · Paper page
  10. [11]Dustmann M Schmidt T Gangey I 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 10.1007/s00167-007-0471-0 18183370 · DOI
  11. [12]Falconiero RP Distefano VJ Cook TM Revascularization and ligamentization of autogenous anterior cruciate ligament grafts in humans Arthroscopy 1998 14 197 205 10.1016/S0749-8063(98)70041-6 9531133 · DOI · Paper page
  12. [13]Figueroa D Melena P Calco R 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 10.1016/j.arthro.2010.02.010 20800986 · DOI
  13. [14]Fujimoto E Sumen Y Urabe Y An early return to vigorous activity may destabilize anterior cruciate ligaments reconstructed with hamstring grafts Arch Phys Med Rehabil 2004 85 298 302 10.1016/S0003-9993(03)00621-X 14966717 · DOI
  14. [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 17905952
  15. [16]Goradia VK Rochat MC Grana WA 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 11277242
  16. [17]Grana WA Egle DM Mahnken R An analysis of autograft fixation after anterior cruciate ligament reconstruction in a rabbit model Am J Sports Med 1994 22 344 351 10.1177/036354659402200309 8037275 · DOI
  17. [18]Howell SM Knox KE Farley TE Revascularization of a human anterior cruciate ligament graft during the first two years of implantation Am J Sports Med 1995 23 42 49 10.1177/036354659502300107 7726349 · DOI
  18. [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 8666598
  19. [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 1993715
  20. [21]Jackson DW Grood ES Goldstein JD 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 10.1177/036354659302100203 8465909 · DOI
  21. [22]Jackson JR Minton JA Ho ML Expression of vascular endothelial growth factor in synovial fibroblasts is induced by hypoxia and interleukin 1beta J Rheumatol 1997 24 1253 1259 9228120
  22. [23]Janssen RP Du Mée AW Valkenburg VJ 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 23081710
  23. [24]Janssen RP van der Wijk J Fiedler A Remodelling of human hamstring autografts after anterior cruciate ligament reconstruction Knee Surg Sports Traumatol Arthrosc 2011 19 1299 1306 10.1007/s00167-011-1419-y 21293848 PMC3136699 · DOI · Paper page
  24. [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 10.1016/S0749-8063(05)80362-7 8461069 · DOI · Paper page
  25. [26]Kawamura S Ying L Kim HJ Macrophages accumulate in the early phase of tendon-bone healing J Orthop Res 2005 23 1425 1432 10.1016/j.orthres.2005.01.014 16111854 · DOI · Paper page
  26. [27]Kleiner JB Amiel D Harwood FL Early histological, metabolic, and vascular assessment of anterior cruciate ligament autografts J Orthop Res 1989 7 235 242 10.1002/jor.1100070211 2918422 · DOI
  27. [28]Kleiner JB Amiel D Roux RD Origin of replacement cells for the anterior cruciate ligament autograft J Orthop Res 1986 4 466 474 10.1002/jor.1100040410 2946835 · DOI
  28. [29]Kuroda R Kurosaka M Yoshiya S Localization of growth factors in the reconstructed anterior cruciate ligament: immunohistological study in dogs Knee Surg Sports Traumatol Arthrosc 2000 8 120 126 10.1007/s001670050198 10795676 · DOI
  29. [30]Lane JG McFadden P Bowden K The ligamentization process: a 4 year case study following ACL reconstruction with a semitendinosis graft Arthroscopy 1993 9 149 153 10.1016/S0749-8063(05)80364-0 8461071 · DOI
  30. [31]Liu SH Yang RS Al-Shaikh R Collagen in tendon, ligament, and bone healing. A current review Clin Orthop Relat Res 1995 318 265 278 7671527
  31. [32]McFarland EG The biology of anterior cruciate ligament reconstructions Orthopedics 1993 16 403 410 8493146
  32. [33]Marumo K Saito M Yamagishi T The “ligamentization” process in human anterior cruciate ligament reconstruction with autogenous patellar and hamstring tendons Am J Sports Med 2005 33 1166 1173 10.1177/0363546504271973 16000668 · DOI
  33. [34]Mayr HO Stoehr A Dietrich M 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 10.1007/s00167-011-1678-7 21953379 · DOI
  34. [35]Ménétrey J Duthon VB Laumonier T “Biological failure” of the anterior cruciate ligament graft Knee Surg Sports Traumatol Arthrosc 2008 16 224 231 10.1007/s00167-007-0474-x 18183368 · DOI · Paper page
  35. [37]Ng GY Oakes BW Deacon OW 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 10.1002/jor.1100130416 7674076 · DOI
  36. [38]Ng GY Oakes BW Deacon OW Long-term study of the biochemistry and biomechanics of anterior cruciate ligament-patellar tendon autografts in goats J Orthop Res 1996 14 851 856 10.1002/jor.1100140602 8982125 · DOI
  37. [39]Ohno K Yasuda K Yamamoto N Effects of complete stress-shielding on the mechanical properties and histology of in situ frozen patellar tendon J Orthop Res 1993 11 592 602 10.1002/jor.1100110414 8340831 · DOI
  38. [40]Papageorgiou CD Ma CB Abramowitch SD 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 11573921
  39. [41]Papalia R Franceschi F Vasta S Sparing the anterior cruciate ligament remnant: is it worth the hassle? Br Med Bull 2012 104 91 111 10.1093/bmb/ldr053 22257853 · DOI
  40. [42]Petersen W Wildemann B Pufe T 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 10.1007/s00402-003-0582-0 14586627 · DOI
  41. [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 10.1007/s001670050113 10024956 · DOI · Paper page
  42. [44]Sanchez M Anitua E Azofra J Ligamentization of tendon grafts treated with an endogenous preparation rich in growth factors: gross morphology and histology Arthroscopy 2010 26 470 480 10.1016/j.arthro.2009.08.019 20362825 · DOI · Paper page
  43. [45]Scheffler SU Scherler J Pruss A Biomechanical comparison of human bone-patellar tendon-bone grafts after sterilization with peracetic acid ethanol Cell Tissue Bank 2005 6 109 115 10.1007/s10561-004-6403-z 15909098 · DOI
  44. [46]Scheffler SU Unterhauser FN Weiler A Graft remodeling and ligamentization after cruciate ligament reconstruction Knee Surg Sports Traumatol Arthrosc 2008 16 834 842 10.1007/s00167-008-0560-8 18516592 · DOI · Paper page
  45. [47]Scranton PE Jr Lanzer WL Ferguson MS Mechanisms of anterior cruciate ligament neovascularization and ligamentization Arthroscopy 1998 14 702 716 10.1016/S0749-8063(98)70097-0 9788366 · DOI
  46. [48]Seitz H Menth-Chiari WA Lang S 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 10.1007/s00167-008-0599-6 18712354 · DOI
  47. [49]Shelbourne KD Nitz P Accelerated rehabilitation after anterior cruciate ligament reconstruction Am J Sports Med 1990 18 292 299 10.1177/036354659001800313 2372081 · DOI
  48. [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 1792884
  49. [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 6501359
  50. [52]Spindler KP Andrish JT Miller RR Distribution of cellular repopulation and collagen synthesis in a canine anterior cruciate ligament autograft J Orthop Res 1996 14 384 389 10.1002/jor.1100140307 8676250 · DOI · Paper page
  51. [53]Stener S Ejerhed L Movin T 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 10.1007/s00167-012-1908-7 22310901 · DOI
  52. [54]Tohyama H, Yasuda K (2002) The effect of increased stress on the patellar tendon. J Bone Joint Surg 84-B:440–446 12002508
  53. [55]Unterhauser FN Bail HJ Höher J Endoligamentous revascularization of an anterior cruciate ligament graft Clin Orthop Relat Res 2003 414 276 288 10.1097/01.blo.0000079442.64912.51 12966303 · DOI · Paper page
  54. [56]Unterhauser FN Bosch U Zeichen J 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 10.1007/s00402-004-0742-x 15378321 · DOI
  55. [57]Vogrin M Rupreht M Dinevski D 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 10.1159/000318597 20814217 · DOI
  56. [58]Weiler A Förster C Hunt P 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 10.1177/0363546503261711 15150033 · DOI · Paper page
  57. [59]Weiler A Hoffmann RF Bail HJ 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 10.1053/jars.2002.30657 11830805 · DOI
  58. [60]Weiler A Peine R Pahminez-Azar A 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 10.1053/jars.2002.30656 11830804 · DOI
  59. [61]Weiler A Peters G Mäurer J 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 11734489
  60. [62]Weiler A Unterhauser FN Bail HJ 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 10.1016/S0736-0266(01)00109-7 11918311 · DOI
  61. [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 10.1007/s00167-009-0764-6 19305977 · DOI
  62. [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 10.1177/0363546506294469 17092923 · DOI
  63. [65]Zaffagnini S De Pasquale V Marchesini Reggiani L Neoligamentization process of BTPB used for ACL graft: histological evaluation from 6 months to 10 years Knee 2007 14 87 93 10.1016/j.knee.2006.11.006 17188877 · DOI
  64. [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 19787336

Cited by

Sorted by citations

Authors
Janssen, R. P. A., & Scheffler, S. U.
Affiliations
  • Máxima Medisch Centrum (NL)
  • Chirurgisch Orthopädischer PraxisVerbund (COPV) Breitenbachplatz 8 14195 Berlin Germany
Corresponding author
Janssen, Rob P. A.
Venue
Knee Surgery, Sports Traumatology, Arthroscopy
Publisher
Wiley
Published
2013-08-27
Volume
22
Issue
9
Pages
2102-2108
ISSN
  • 0942-2056 (ISSN-L)
  • 1433-7347
OpenAlex
W2023416936
Cited by
225
References
2
Citations by year
2026: 14 · 2025: 20 · 2024: 18 · 2023: 23 · 2022: 23 · 2021: 26 · 2020: 22 · 2019: 19 · 2018: 13 · 2017: 14 · 2016: 19 · 2015: 8 · 2014: 6
FWCI
1.95
Type
journal article
Language
en
Open access
Locations
  • Knee Surgery Sports Traumatology Arthroscopy (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Surgery › Knee injuries and reconstruction techniques
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Tendon Structure and Treatment
  • Health Sciences › Medicine › Urology › Periodontal Regeneration and Treatments
Keywords
anterior cruciate ligament reconstruction, hamstring tendon graft, graft necrosis, graft revascularization, ligamentization, postoperative rehabilitation, graft mechanical properties
MeSH terms
Anterior Cruciate Ligament Injuries, Animals, Humans, Knee Joint, Tendons, Wound Healing, Anterior Cruciate Ligament, Transplants, Anterior Cruciate Ligament Reconstruction

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