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Graft remodeling during growth following anterior cruciate ligament reconstruction in skeletally immature sheep

  • Arthroscopy and Sports Medicine
  • Published:
Archives of Orthopaedic and Trauma Surgery Aims and scope Submit manuscript

Abstract

Introduction

Ruptures of the anterior cruciate ligament are being diagnosed with increasing frequency in skeletally immature individuals. It was our aim to investigate the graft remodelling process following an autologous, transphyseal reconstruction of the anterior cruciate ligament (ACL) in skeletally immature sheep. We hypothesized that the ligamentisation process in immature sheep is quicker and more complete when compared to adult sheep.

Materials and methods

Skeletally immature sheep with an age of 4 months underwent a fully transphyseal ACL reconstruction using an autologous tendon. The animals were subsequently sacrificed at 3, 6, 12 and 24 weeks following surgery. Each group was characterised histomorphometrically, by immunostaining (VEGF, SMA), by transmission electron microscopy (TEM) and biomechanically (UFS Roboter).

Results

The histomorphometric analysis and presence of VEGF and SMA positive cells demonstrated a rapid return to a ligament like structure. The biomechanical analysis revealed an anteroposterior translation that was still increased even 6 months following surgery.

Conclusion

As in adult sheep models, the remodeling of a soft tissue graft used for ACL reconstruction results in a biomechanically inferior substitute. However, the immature tissue seems to remodel faster and more complete when compared to adults.

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References

  1. Amiel D, Kleiner JB, Akeson WH (1986) The natural history of the anterior cruciate ligament autograft of patellar tendon origin. Am J Sports Med 14:449–462. doi:10.1177/036354658601400603

    Article  PubMed  CAS  Google Scholar 

  2. Amiel D, Kleiner JB, Roux RD et al (1986) The phenomenon of ligamentization: anterior cruciate ligament reconstruction with autogenous patellar tendon. J Orthop Res 4:162–172. doi:10.1002/jor.1100040204

    Article  PubMed  CAS  Google Scholar 

  3. Arnoczky SP, Warren RF, Ashlock MA (1986) Replacement of the anterior cruciate ligament using a patellar tendon allograft. An experimental study. J Bone Joint Surg Am 68:376–385

    PubMed  CAS  Google Scholar 

  4. Aronowitz ER, Ganley TJ, Goode JR et al (2000) Anterior cruciate ligament reconstruction in adolescents with open physes. Am J Sports Med 28:168–175

    PubMed  CAS  Google Scholar 

  5. Bales CP, Guettler JH, Moorman CT 3rd (2004) Anterior cruciate ligament injuries in children with open physes: evolving strategies of treatment. Am J Sports Med 32:1978–1985. doi:10.1177/0363546504271209

    Article  PubMed  Google Scholar 

  6. Behr CT, Potter HG, Paletta GA Jr (2001) The relationship of the femoral origin of the anterior cruciate ligament and the distal femoral physeal plate in the skeletally immature knee. An anatomic study. Am J Sports Med 29:781–787

    PubMed  CAS  Google Scholar 

  7. Bosch U, Decker B, Moller HD et al (1995) Collagen fibril organization in the patellar tendon autograft after posterior cruciate ligament reconstruction. A quantitative evaluation in a sheep model. Am J Sports Med 23:196–202. doi:10.1177/036354659502300212

    Article  PubMed  CAS  Google Scholar 

  8. Clancy WG Jr, Narechania RG, Rosenberg TD et al (1981) Anterior and posterior cruciate ligament reconstruction in rhesus monkeys. J Bone Joint Surg Am 63:1270–1284

    PubMed  Google Scholar 

  9. Cummings JF, Grood ES (2002) The progression of anterior translation after anterior cruciate ligament reconstruction in a caprine model. J Orthop Res 20:1003–1008. doi:10.1016/S0736-0266(02)00033-5

    Article  PubMed  CAS  Google Scholar 

  10. Edwards PH, Grana WA (2001) Anterior cruciate ligament reconstruction in the immature athlete: long-term results of intra-articular reconstruction. Am J Knee Surg 14:232–237

    PubMed  CAS  Google Scholar 

  11. Fenwick SA, Hazleman BL, Riley GP (2002) The vasculature and its role in the damaged and healing tendon. Arthritis Res 4:252–260. doi:10.1186/ar416

    Article  PubMed  Google Scholar 

  12. Hunt P, Scheffler SU, Unterhauser FN et al (2005) A model of soft-tissue graft anterior cruciate ligament reconstruction in sheep. Arch Orthop Trauma Surg 125:238–248. doi:10.1007/s00402-004-0643-z

    Article  PubMed  Google Scholar 

  13. Jackson DW, Grood ES, Goldstein JD et al (1993) A comparison of patellar tendon autograft and allograft used for anterior cruciate ligament reconstruction in the goat model. Am J Sports Med 21:176–185. doi:10.1177/036354659302100203

    Article  PubMed  CAS  Google Scholar 

  14. Koman JD, Sanders JO (1999) Valgus deformity after reconstruction of the anterior cruciate ligament in a skeletally immature patient. A case report. J Bone Joint Surg Am 81:711–715

    PubMed  CAS  Google Scholar 

  15. Lo IK, Ou Y, Rattner JP et al (2002) The cellular networks of normal ovine medial collateral and anterior cruciate ligaments are not accurately recapitulated in scar tissue. J Anat 200:283–296. doi:10.1046/j.1469-7580.2002.00024.x

    Article  PubMed  Google Scholar 

  16. McIntosh AL, Dahm DL, Stuart MJ (2006) Anterior cruciate ligament reconstruction in the skeletally immature patient. Arthroscopy 22:1325–1330. doi:10.1016/j.arthro.2006.07.014

    PubMed  Google Scholar 

  17. Melrose J, Smith S, Little CB et al (2002) Spatial and temporal localization of transforming growth factor-beta, fibroblast growth factor-2, and osteonectin, and identification of cells expressing alpha-smooth muscle actin in the injured anulus fibrosus: implications for extracellular matrix repair. Spine 27:1756–1764. doi:10.1097/00007632-200208150-00014

    Article  PubMed  Google Scholar 

  18. Murray MM, Spector M (1999) Fibroblast distribution in the anteromedial bundle of the human anterior cruciate ligament: the presence of alpha-smooth muscle actin-positive cells. J Orthop Res 17:18–27. doi:10.1002/jor.1100170105

    Article  PubMed  CAS  Google Scholar 

  19. Nottage WM, Matsuura PA (1994) Management of complete traumatic anterior cruciate ligament tears in the skeletally immature patient: current concepts and review of the literature. Arthroscopy 10:569–573. doi:10.1016/S0749-8063(05)80016-7

    PubMed  CAS  Google Scholar 

  20. Petersen W, Unterhauser F, Pufe T et al (2003) The angiogenic peptide vascular endothelial growth factor (VEGF) is expressed during the remodeling of free tendon grafts in sheep. Arch Orthop Trauma Surg 123:168–174

    PubMed  Google Scholar 

  21. Schindhelm K, Rogers GJ, Milthorpe BK et al (1991) Autograft and Leeds-Keio reconstructions of the ovine anterior cruciate ligament. Clin Orthop Relat Res 267:278–293

    Google Scholar 

  22. Scranton PE Jr, Lanzer WL, Ferguson MS et al (1998) Mechanisms of anterior cruciate ligament neovascularization and ligamentization. Arthroscopy 14:702–716. doi:10.1016/S0749-8063(98)70097-0

    PubMed  Google Scholar 

  23. Seil R, Kohn D (2000) Ruptures of the anterior cruciate ligament (ACL) during growth. Bull Soc Sci Med Grand Duche Luxemb 1:39–53

    Google Scholar 

  24. Seil R, Pape D, Kohn D (2008) The risk of growth changes during transphyseal drilling in sheep with open physes. Arthroscopy 24:824–833. doi:10.1016/j.arthro.2008.02.007

    PubMed  Google Scholar 

  25. Shrive N, Chimich D, Marchuk L et al (1995) Soft-tissue flaws are associated with the material properties of the healing rabbit medial collateral ligament. J Orthop Res 13:923–929. doi:10.1002/jor.1100130617

    Article  PubMed  CAS  Google Scholar 

  26. Simonian PT, Metcalf MH, Larson RV (1999) Anterior cruciate ligament injuries in the skeletally immature patient. Am J Orthop 28:624–628

    PubMed  CAS  Google Scholar 

  27. Weibel ER (1981) Stereological methods in cell biology: where are we—where are we going? J Histochem Cytochem 29:1043–1052

    PubMed  CAS  Google Scholar 

  28. Weiler A, Forster C, Hunt P et al (2004) The influence of locally applied platelet-derived growth factor-BB on free tendon graft remodeling after anterior cruciate ligament reconstruction. Am J Sports Med 32:881–891. doi:10.1177/0363546503261711

    Article  PubMed  Google Scholar 

  29. Weiler A, Peine R, Pashmineh-Azar A et al (2002) 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 18:113–123. doi:10.1053/jars.2002.30656

    Article  PubMed  Google Scholar 

  30. Weiler A, Unterhauser FN, Bail HJ et al (2002) 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 20:310–317. doi:10.1016/S0736-0266(01)00109-7

    Article  PubMed  CAS  Google Scholar 

  31. Woo SL, Abramowitch SD, Kilger R et al (2006) Biomechanics of knee ligaments: injury, healing, and repair. J Biomech 39:1–20. doi:10.1016/j.jbiomech.2004.10.025

    Article  PubMed  Google Scholar 

  32. Woo SL, Ohland KJ, Weiss JA (1990) Aging and sex-related changes in the biomechanical properties of the rabbit medial collateral ligament. Mech Ageing Dev 56:129–142. doi:10.1016/0047-6374(90)90004-Y

    Article  PubMed  CAS  Google Scholar 

  33. Yoshikawa T, Tohyama H, Katsura T et al (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 34:1918–1925. doi:10.1177/0363546506294469

    Article  PubMed  Google Scholar 

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Acknowledgments

The funding source of the present study was a research grant of the Research Commission of Hannover Medical School, Hannover, Germany. We gratefully acknowledge the help of Sabine Thoben and Alexandra Neddermann. The authors would like to thank Prof. Klaus Otto and Karl Napierski for their excellent animal care.

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Authors and Affiliations

  1. Trauma Department, Hannover Medical School (MHH), Carl-Neuberg-Strasse 1, 30625, Hannover, Germany

    Rupert Meller, F. Fritz, F. Schiborra, S. Hankemeier & C. Krettek

  2. Institute of Cell Biology, Center of Anatomy, Hannover Medical School, Hannover, Germany

    G. Brandes

  3. Institutes for Animal Breeding and Genetics, University of Veterinary Medicine Hannover, Hannover, Germany

    C. Drögemüller

  4. Small Animal Clinic, University of Veterinary Medicine Hannover, Hannover, Germany

    M. Fehr

  5. Orthopaedic Department, Hannover Medical School, Hannover, Germany

    C. Hurschler

Authors
  1. Rupert Meller
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  2. G. Brandes
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  3. C. Drögemüller
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  4. F. Fritz
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  5. F. Schiborra
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  9. C. Hurschler
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Corresponding author

Correspondence to Rupert Meller.

Additional information

R. Meller and G. Brandes contributed equally to this work.

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Meller, R., Brandes, G., Drögemüller, C. et al. Graft remodeling during growth following anterior cruciate ligament reconstruction in skeletally immature sheep. Arch Orthop Trauma Surg 129, 1037–1046 (2009). https://doi.org/10.1007/s00402-008-0784-6

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  • DOI: https://doi.org/10.1007/s00402-008-0784-6

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