Skip to main content
SpringerLink
Log in

Peri-tunnel bone loss: does it affect early tendon graft to bone tunnel healing after ACL reconstruction?

  • Knee
  • Published:
Knee Surgery, Sports Traumatology, Arthroscopy Aims and scope

Abstract

Purpose

The clinical relevance and mechanisms of local bone loss early post-anterior cruciate ligament (ACL) reconstruction remain unclear. The early spatial and temporal changes of peri-tunnel bone, its molecular mechanisms and its relationships with graft–bone tunnel healing were investigated in a 12-week-old rat model.

Methods

At various times, the reconstructed ACL complex was harvested for vivaCT imaging, biomechanical test, histology and immunohistochemical staining of CD68+ cells (a monocyte–macrophage lineage marker), MMP1 and MMP13.

Results

The peri-tunnel bone resorbed simultaneously with improvement of graft–bone tunnel healing. There were 30.1 ± 17.4, 46.8 ± 10.5 and 81.5 ± 12.3 % loss of peri-tunnel BMD as well as 43.2 ± 21.7, 78.7 ± 8.5 and 92.4 ± 17.7 % loss of peri-tunnel bone volume/total volume (BV/TV) at week 6 at the distal femur, epiphysis and metaphysis of tibia, respectively. MMP1, MMP13 and CD68+ cells were expressed at the graft–bone tunnel interface and peri-tunnel bone and increased with time post-reconstruction at the tibia. The ultimate load and stiffness of the healing complex positively correlated with tibial tunnel bone formation and negatively correlated with tibial peri-tunnel bone. Tunnel BV/TV at the tibial metaphysis and epiphysis showed the highest correlation with ultimate load (ρ = 0.591; p = 0.001) and stiffness (ρ = 0.427; p = 0.026) of the complex, respectively.

Conclusion

There was time-dependent loss of peri-tunnel bone early post-reconstruction, with the greatest loss occurring at the tibial metaphysis. This was consistent with high expression of MMP1, MMP13 and CD68+ cells at the graft–bone tunnel interface and the peri-tunnel region. The significant loss of peri-tunnel bone, though not critically affecting early tunnel healing, suggested the need to protect the knee joint early post-reconstruction.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  1. 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(6):689–698

    CAS  PubMed  Google Scholar 

  2. Bedi A, Fox AJ, Kovacevic D et al (2010) Doxycycline-mediated inhibition of matrix metalloproteinases improves healing after rotator cuff repair. Am J Sports Med 38(2):308–317

    Article  PubMed  Google Scholar 

  3. Bedi A, Kovacevic D, Hettrich C et al (2010) The effect of matrix metalloproteinase inhibition on tendon-to-bone healing in a rotator cuff repair model. J Should Elbow Surg 19(3):384–391

    Article  Google Scholar 

  4. 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(11):2401–2410

    Article  PubMed  Google Scholar 

  5. Ditsios K, Boyer MI, Kusano N et al (2003) Bone loss following tendon laceration, repair and passive mobilization. J Orthop Res 21(6):990–996

    Article  PubMed  Google Scholar 

  6. Dong Y, Zhang Q, Li Y et al (2012) Enhancement of tendon-bone healing for anterior cruciate ligament (ACL) reconstruction using bone marrow-derived mesenchymal stem cells infected with BMP-2. Int J Mol Sci 13(10):13605–13620

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Ejerhed L, Kartus J, Nilsen R et al (2004) The effect of anterior cruciate ligament surgery on bone mineral in the calcaneus: a prospective study with a 2-year follow-up evaluation. Arthroscopy 20(4):352–359

    Article  PubMed  Google Scholar 

  8. Fleming BC, Spindler KP, Palmer MP et al (2009) Collagen-platelet composites improve the biomechanical properties of healing anterior cruciate ligament grafts in a porcine model. Am J Sports Med 37(8):1554–1563

    Article  PubMed Central  PubMed  Google Scholar 

  9. Galatz LM, Rothermich SY, Zaegel M et al (2005) Delayed repair of tendon to bone injuries leads to decreased biomechanical properties and bone loss. J Orthop Res 23(6):1441–1447

    Article  CAS  PubMed  Google Scholar 

  10. Jager A, Radlanski RJ, Gotz W (1993) Demonstration of cells of the mononuclear phagocyte lineage in the periodontium following experimental tooth movement in the rat. An immunohistochemical study using monoclonal antibodies ED1 and ED2 on paraffin-embedded tissues. Histochemistry 100:161–166

    Article  CAS  PubMed  Google Scholar 

  11. Kadonishi Y, Deie M, Takata T et al (2012) Acceleration of tendon-bone healing in anterior cruciate ligament reconstruction using an enamel matrix derivative in a rat model. J Bone Joint Surg Br 94(2):205–209

    Article  CAS  PubMed  Google Scholar 

  12. Kannus P, Sievanen H, Jarvinen M et al (1992) A cruciate ligament injury produces considerate, permanent osteoporosis in the affected knee. J Bone Miner Res 7(12):1429–1434

    Article  CAS  PubMed  Google Scholar 

  13. Kartus J, Sterner S, Nilsen R et al (1998) Bone mineral assessments in the calcaneus after anterior cruciate ligament injury. An investigation of 92 male patients before and 2 years after reconstruction or revision surgery. Scand J Med Sci Sports 8(6):449–455

    Article  CAS  PubMed  Google Scholar 

  14. Leppala J, Kannus P, Natri A et al (1999) Effect of anterior cruciate ligament injury of the knee on bone mineral density of the spine and affected lower extremity: a prospective one-year follow-up study. Calcif Tissue Int 64(4):357–363

    Article  CAS  PubMed  Google Scholar 

  15. Lovric V, Chen D, Yu Y et al (2012) Effects of demineralized bone matrix on tendon-bone healing in an intra-articular rodent model. Am J Sports Med 40(10):2365–2374

    Article  PubMed  Google Scholar 

  16. Lui PPY, Chan LS, Fu SC et al (2010) Expression of sensory neuropeptides in tendon is associated with failed healing and activity-related tendon pain in collagenase-induced tendon injury. Am J Sports Med 38(4):757–764

    Article  PubMed  Google Scholar 

  17. Lui PP, Cheng YY, Yung SH et al (2012) A randomized controlled trial comparing bone mineral density changes of three different ACL reconstruction techniques. Knee 19(6):779–785

    Article  PubMed  Google Scholar 

  18. Lui PPY, Ho G, Lee YW et al (2011) Validation of a histologic scoring system for the examination of quality of tendon graft to bone tunnel healing in ACL reconstruction: TBTH Score (Tendon-Bone Tunnel Healing) Score. Anal Quant Cyto Histol 33(1):36–49

    Google Scholar 

  19. Lui PPY, Ho G, Shum WT et al (2010) Inferior tendon graft to bone tunnel healing at the tibia compared to that at the femur after anterior cruciate ligament reconstruction. J Orthop Sci 15(3):389–401

    Article  PubMed  Google Scholar 

  20. Lui PP, Lee YW, Mok TY et al (2013) Alendronate reduced peri-tunnel bone loss and enhanced tendon graft to bone tunnel healing in anterior cruciate ligament reconstruction. Eur Cell Mater 25:78–96

    CAS  PubMed  Google Scholar 

  21. 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-A(7):1123–1131

    PubMed  Google Scholar 

  22. Mifune Y, Matsumoto T, Ota S et al (2012) Therapeutic potential of anterior cruciate ligament-derived stem cells for anterior cruciate ligament reconstruction. Cell Transplant 21(8):1651–1665

    Article  PubMed  Google Scholar 

  23. Mithofer K, Gill TJ, Vrahas MS (2004) Tibial plateau fracture following anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc 12(4):325–328

    Article  PubMed  Google Scholar 

  24. Nyland J, Fisher B, Brand E et al (2010) Osseous deficits after anterior cruciate ligament injury and reconstruction: a systematic literature review with suggestions to improve osseous homeostasis. Arthroscopy 26(9):1248–1257

    Article  PubMed  Google Scholar 

  25. Pan W, Wei Y, Zhou L et al (2011) Comparative in vivo study of injectable biomaterials combined with BMP for enhancing tendon graft osteointegration for anterior cruciate ligament reconstruction. J Orthop Res 29(7):1015–1021

    Article  CAS  PubMed  Google Scholar 

  26. Rittweger J, Maffulli N, Maganaris CN et al (2005) Reconstruction of the anterior cruciate ligament with a patella-tendon-bone graft may lead to a permanent loss of bone mineral content due to decreased patellar tendon stiffness. Med Hypotheses 64(6):1166–1169

    Article  PubMed  Google Scholar 

  27. Rodeo SA, Kawamura S, Kim HJ et al (2006) Tendon healing in a bone tunnel differs at the tunnel entrance versus the tunnel exit. Am J Sports Med 34(11):1790–1800

    Article  PubMed  Google Scholar 

  28. Salem K, Rees DC, Geutjens G (2007) Low velocity bicondylar tibial fracture following ACL reconstruction. Injury Extra 38:179–181

    Article  Google Scholar 

  29. Silva MJ, Boyer MI, Ditsios K et al (2002) The insertion site of the canine flexor digitorum profundus tendon heals slowly following injury and suture repair. J Orthop Res 20(3):447–453

    Article  PubMed  Google Scholar 

  30. Siminia T, Dukstra CD (1986) The origin of osteoclasts: an immunohistochemical study on macrophages and osteoclasts in embryonic rat bone. Calcif Tissue Int 39:263–266

    Article  Google Scholar 

  31. Thangamani VB, Flanigan DC, Merk BR (2009) Intra-articular distal femur fracture extending from an expanded femoral tunnel in an anterior cruciate ligament (ACL) reconstructed knee: a case report. J Trauma 67(6):E209–E212

    Article  PubMed  Google Scholar 

  32. Thomopoulos S, Matsuzaki H, Zaegel M et al (2007) Alendronate prevents bone loss and improves tendon-to-bone repair strength in a canine model. J Orthop Res 25(4):473–479

    Article  CAS  PubMed  Google Scholar 

  33. Torabinia N, Razavi SM, Shokrolahi Z (2011) A comparative immunohistochemical evaluation of CD68 and TRAP protein expression in central and peripheral giant cell granulomas of the jaws. J Oral Pathol Med 40(4):334–337

    Article  CAS  PubMed  Google Scholar 

  34. Voos JE, Drako MC, Lorich DG et al (2008) Proximal tibia fracture after anterior cruciate ligament reconstruction using bone-patellar tendon–bone autograft: a case report. HSS J 4(1):20–24

    Article  PubMed Central  PubMed  Google Scholar 

  35. Wen CY, Qin L, Lee KM et al (2009) Influence of bone adaption on tendon-to-bone healing in bone tunnel after anterior cruciate ligament reconstruction in a rabbit model. J Orthop Res 27(11):1447–1456

    Article  PubMed  Google Scholar 

  36. Wilson TC, Rosenblum WJ, Johnson DL (2004) Fracture of the femoral tunnel after an anterior cruciate ligament reconstruction. Arthroscopy 20(5):e45–e47

    Article  PubMed  Google Scholar 

  37. Yamazaki S, Yasuda K, Tomita F et al (2005) The effect of transforming growth factor-beta 1 on intraosseous healing of flexor tendon allograft replacement of anterior cruciate ligament in dogs. Arthroscopy 21(9):1034–1041

    Article  PubMed  Google Scholar 

  38. Zerahn B, Munk AO, Helweg J et al (2006) Bone mineral density in the proximal tibia and calcaneus before and after arthroscopic reconstruction of the anterior cruciate ligament. Arthroscopy 22(3):265–269

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This project was supported by the GRF (project no. 470808, 08/001/ERG) from University Grant Council, CUHK Direct Grant (Reference No.: 2011.1.045) and the Hong Kong Jockey Club Charities Trust.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Headquarter, Hospital Authority, 9/F, Rumsey Street Multi-Storey Carpark Building, 2 Rumsey Street, Hong Kong SAR, China

    Pauline Po Yee Lui

  2. Department of Orthopaedics and Traumatology, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong SAR, China

    Yuk Wa Lee, Tsui Yu Mok & Yau Chuk Cheuk

  3. The Hong Kong Jockey Club Sports Medicine and Health Sciences Centre, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong SAR, China

    Yuk Wa Lee, Tsui Yu Mok & Yau Chuk Cheuk

Authors
  1. Pauline Po Yee Lui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuk Wa Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tsui Yu Mok
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yau Chuk Cheuk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pauline Po Yee Lui.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lui, P.P.Y., Lee, Y.W., Mok, T.Y. et al. Peri-tunnel bone loss: does it affect early tendon graft to bone tunnel healing after ACL reconstruction?. Knee Surg Sports Traumatol Arthrosc 23, 740–751 (2015). https://doi.org/10.1007/s00167-013-2697-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00167-013-2697-3

Keywords

Search

Navigation