Skip to main content
Log in

Differences in Tendon Graft Healing Between the Intra-articular and Extra-articular Ends of a Bone Tunnel

  •  
  • Published:
HSS Journal

Abstract

The basic biology of healing between a tendon graft and bone tunnel remains incompletely understood. Distinct variability in the morphological characteristics of the healing tendon–bone attachment site has been reported. We hypothesized that spatial and temporal differences in tendon-to-bone healing exist at different regions of a surgically created bone tunnel. Twenty-four male, Sprague–Dawley rats underwent anterior cruciate ligament (ACL) reconstruction in the left knee using a flexor digitorum longus tendon graft secured using suspensory periosteal fixation. Animals were sacrificed at 4, 7, 11, 14, 21, and 28 days after surgery and prepared for routine histology and immunohistochemical analysis of the healing enthesis at the intra-articular aperture (IAA), mid-tunnel, and extra-articular aperture (EAA). Six animals were used to measure mineral apposition rate (MAR) along the healing bone tunnel by double fluorochrome labeling at 14 and 28 days after surgery. The total area of calcified bone matrix was assessed with von Kossa staining and Goldner-Masson trichrome staining, respectively. The healing tendon–bone interface tissue exhibited a wide chondroid matrix at the IAA, in contrast to a narrow, fibrous matrix at the EAA. There were significantly more osteoclasts at the IAA compared to EAA throughout the study period, except 4 days after surgery (p < 0.05). Collagen continuity between the tendon graft and bone tunnel increased over time, with a more parallel orientation and increased collagen fiber continuity between tendon and bone at the EAA compared to the IAA. MAR was also significantly greater at the EAA at 4 weeks (p < 0.001). Significant differences in healing between the tendon graft and bone exist along the length of bone tunnel secured with suspensory fixation. The etiology of these differences is likely multifactorial in nature, including variable biological and biomechanical environments at different ends of the tunnel. Understanding these differences may ultimately allow surgeons to improve the quality of graft fixation and long-term outcomes after ACL reconstruction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Ishibashi Y, Rudy TW, Livesay GA, Stone JD, Fu FH, Woo SL (1997) The effect of anterior cruciate ligament graft fixation site at the tibia on knee stability: evaluation using a robotic testing system. Arthroscopy 13:177–182

    PubMed  CAS  Google Scholar 

  2. Otsuka H, Ishibashi Y, Tsuda E, Sasaki K, Toh S (2003) Comparison of three techniques of anterior cruciate ligament reconstruction with bone–patellar tendon–bone graft: differences in anterior tibial translation and tunnel enlargement with each technique. Am J Sports Med 31:282–288

    PubMed  Google Scholar 

  3. Scheffler SU, Sudkamp NP, Gockenjan A, Hoffmann RF, Weiler A (2002) Biomechanical comparison of hamstring and patellar tendon graft anterior cruciate ligament reconstruction techniques: the impact of fixation level and fixation method under cyclic loading. Arthroscopy 18:304–315

    PubMed  Google Scholar 

  4. Tsuda E, Fukuda Y, Loh JC, Debski RE, Fu FH, Woo SL (2002) The effect of soft-tissue graft fixation in anterior cruciate ligament reconstruction on graft-tunnel motion under anterior tibial loading. Arthroscopy 18:960–967

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  6. Chiroff RT (1975) Experimental replacement of the anterior cruciate ligament: a histological and microradiographic study. J Bone Joint Surg Am 57:1124–1127

    PubMed  CAS  Google Scholar 

  7. Grana WA, Egle DM, Mahnken R, Goodhart CW (1994) An analysis of autograft fixation after anterior cruciate ligament reconstruction in a rabbit model. Am J Sports Med 22:344–351

    Article  PubMed  CAS  Google Scholar 

  8. Kjaer M (2004) Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84:649–698

    Article  PubMed  CAS  Google Scholar 

  9. Liu SH, Panossian V, Al-Shaikh R et al (1997) Morphology and matrix composition during early tendon to bone healing. Clin Orthop Relat Res 339:253–260

    Article  PubMed  Google Scholar 

  10. Nebelung W, Becker R, Urbach D, Ropke M, Roessner A (2003) Histological findings of tendon–bone healing following anterior cruciate ligament reconstruction with hamstring grafts. Arch Orthop Trauma Surg 123:158–163

    PubMed  CAS  Google Scholar 

  11. Panni AS, Milano G, Lucania L, Fabbriciani C (1997) Graft healing after anterior cruciate ligament reconstruction in rabbits. Clin Orthop Relat Res 343:203–212

    Article  PubMed  Google Scholar 

  12. Peterson W, Laprell H (2000) Insertion of autologous tendon grafts to the bone: histological and immunohistochemical study of hamstring and patellar tendon graft. Knee Surg Sports Traumatol Arthrosc 8:26–31

    Article  Google Scholar 

  13. Pinczewski LA, Clingeleffer AJ, Otto DD, Bonar SF, Corry IS (1997) Integration of hamstring tendon graft with bone in reconstruction of the anterior cruciate 997 ligament. Arthroscopy 13:641–643

    PubMed  CAS  Google Scholar 

  14. Rodeo SA, Arnoczky SP, Torzilli PA, Hidaka C, Warren RF (1993) Tendon-healing in a bone tunnel. J Bone Joint Surg Am 75:1795–1803

    PubMed  CAS  Google Scholar 

  15. Rodeo SA, Suzuki K, Deng XH, Wozney J, Warren R (1999) Use of recombinant human bone morphogenetic protein-2 to enhance tendon healing in a bone tunnel. Am J Sports Med 27:476–488

    PubMed  CAS  Google Scholar 

  16. Rodeo SA, Kawamura S, Kim HJ, Dynybil C, Ying L (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 34:1790–800

    Article  PubMed  Google Scholar 

  17. Sakai H, Fukui N, Kawakami A, Kurosawa H (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 5:43–51

    Article  PubMed  CAS  Google Scholar 

  18. St Pierre P, Olson EJ, Elliott JJ, O’Hair KC, McKinney LA, Ryan J (1995) Tendon healing to cortical bone compared with healing to a cancellous tough: a biomechanical and histological evaluation in goats. J Bone Joint Surg Am 77:1858–1866

    PubMed  CAS  Google Scholar 

  19. Thomopoulos S, Williams GR, Soslowsky LJ (2003) Tendon to bone healing: differences in biomechanical, structural, and compositional properties due to a range of activity levels. J Biomech Eng 125:106–113

    Article  PubMed  CAS  Google Scholar 

  20. Weiler A, Hoffmann RF, Bail HJ, Rehm O, Sudkamp NP (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 18:124–135

    PubMed  Google Scholar 

  21. Weiler A, Unterhauser FN, Faensen B, Hunt P, Bail HJ, Haas NP (2002) Comparison of tendon-to-bone healing using extracortical and anatomic interference fit fixation of soft tissue grafts In a sheep model of ACL reconstruction. Trans Orthop Res Soc 27:173

    Google Scholar 

  22. Yoshiya S, Nagano M, Kurosaka M, Muratsu H, Mizuno K (2000) Graft healing in the bone tunnel in anterior cruciate ligament reconstruction. Clin Orthop Relat Res 376:278–286

    Article  PubMed  Google Scholar 

  23. Burg M, Pasqualini R, Arap W, Ruoslahti E, Stallcup W (2000) NG2 proteoglycan-binding peptides target tumor neovasculature. Cancer Res 59:2869–2874

    Google Scholar 

  24. Grako KA, Ochiya T, Barritt D, Nishiyama A, Stallcup W (1999) PDGF a-receptor is unresponsive to PDGF-AA in aortic smooth muscle cells from the NG2 knockout mouse. J Cell Sci 112:905–915

    PubMed  CAS  Google Scholar 

  25. Grako KA, Stallcup W (1995) Participation of NG2 proteoglycan in rat aortic smooth muscle cell responses to platelet-derived growth factor. Exp Cell Res 221:231–240

    Article  PubMed  CAS  Google Scholar 

  26. Nishiyama A, Dahlin K, Stallcup W (1991) The expression of NG2 proteoglycan in the developing rat limb. Development 111:933–944

    PubMed  CAS  Google Scholar 

  27. Schlingemann R, Rietveld F, de Waal R, Ferrone S, Ruiter D (1990) Expression of the high molecular weight melanoma-associated antigen by pericytes during angiogenesis in tumors and in healing wounds. Am J Pathol 136:1393–1405

    PubMed  CAS  Google Scholar 

  28. Schlingemann R, Oosterwijk E, Wesseling P, Rietveld F, Ruiter D (1996) Aminopeptidase A is a constituent of activated pericytes in angiogenesis. J Pathol 179:436–442

    Article  PubMed  CAS  Google Scholar 

  29. Barber FA, Spruill B, Sheluga M (2003) The effect of outlet fixation on tunnel widening. Arthroscopy 19:485–492

    PubMed  Google Scholar 

  30. Clatworthy MG, Annear P, Bulow JU, Bartlett RJ (1999) Tunnel widening in anterior cruciate ligament reconstruction: a prospective evaluation of hamstring and patella tendon grafts. Knee Surg Sports Traumatol Arthrosc 7:138–145

    Article  PubMed  CAS  Google Scholar 

  31. Hantes ME, Mastrokalos DS, Yu J, Paessler HH (2004) The effect of early motion on tibial tunnel widening after anterior cruciate ligament replacement using hamstring tendon grafts. Arthroscopy 20:572–580

    PubMed  Google Scholar 

  32. Hoher J, Livesay GA, Ma CB, Withrow JD, Fu FH, Woo SL (1999) Hamstring graft motion in the femoral bone tunnel when using titanium button/polyester tape fixation. Knee Surg Sports Traumatol Arthrosc 7:215–219

    Article  PubMed  CAS  Google Scholar 

  33. Hoher J, Moller HD, Fu FH (1998) Bone tunnel enlargement after anterior cruciate ligament reconstruction: fact or fiction. Knee Surg Sports Traumatol Arthro 6:231–240

    Article  CAS  Google Scholar 

  34. Sidles JA, Clark JM, Garbini JL (1991) A geometric theory of the equilibrium mechanics of fibers in ligaments and tendons. J Biomech 24:943–949

    Article  PubMed  CAS  Google Scholar 

  35. Simonian PT, Erickson MS, Larson RV, O’kane JW (2000) Tunnel expansion after hamstring anterior cruciate ligament reconstruction with 1-incision EndoButton femoral fixation. Arthroscopy 16:707–714

    PubMed  CAS  Google Scholar 

  36. L’Insalata JC, Klatt B, Fu FH, Harner CD (1997) Tunnel expansion following anterior cruciate ligament reconstruction: a comparison of hamstring and patellar tendon autografts. Knee Surg Sports Traumatol Arthrosc 5:234–238

    Article  PubMed  CAS  Google Scholar 

  37. Berg EE, Pollard ME, Kang Q (2001) Interarticular bone tunnel healing. Arthroscopy 17:189–195

    Article  PubMed  CAS  Google Scholar 

  38. Noorlander ML, Melis P, Jonker A, Van Noorden CJF (2002) A quantitative method to determine the orientation of collagen fibers in the dermis. J Histolochem Cytochem 50(11):1469–1474

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Scott A. Rodeo MD.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bedi, A., Kawamura, S., Ying, L. et al. Differences in Tendon Graft Healing Between the Intra-articular and Extra-articular Ends of a Bone Tunnel. HSS Jrnl 5, 51–57 (2009). https://doi.org/10.1007/s11420-008-9096-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11420-008-9096-1

Keywords

Navigation