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Effect of open wedge high tibial osteotomy on the lateral tibiofemoral compartment in sheep. Part III: analysis of the microstructure of the subchondral bone and correlations with the articular cartilage and meniscus

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

Abstract

Purpose

First, to evaluate whether medial open wedge high tibial osteotomy (HTO) induces alterations of the microstructure of the lateral tibial subchondral bone plate of sheep. Second, to test the hypothesis that specific correlations exist between topographical structural alterations of the subchondral bone, the cartilage and the lateral meniscus.

Methods

Three experimental groups received biplanar osteotomies of the right proximal tibiae: (a) closing wedge HTO (4.5° of tibial varus), (b) opening wedge HTO (4.5° tibial valgus; standard correction) and (c) opening wedge HTO (9.5° of valgus; overcorrection), each of which was compared to the non-osteotomised contralateral proximal tibiae. After 6 months, subchondral bone structure indices were measured by computed tomography. Correlations between the subchondral bone, the articular cartilage and the lateral meniscus were determined.

Results

Increased loading by valgus overcorrection led to an enlarged specific bone surface (BS/BV) in the subarticular spongiosa compared with unloading by varisation. The subchondral bone plate was 3.9-fold thicker in the central region of the lateral tibial plateau than in the submeniscal periphery. Its thickness in the central region significantly correlated with the thickness of the articular cartilage. In the submeniscal region, such correlation did not exist. In general, a higher degree of osteoarthritis (OA) correlated with alterations of the subchondral bone plate microstructure. OA of the submeniscal articular cartilage also correlated with worse matrix staining of the lateral meniscus.

Conclusion

Osteoarthritis changes are associated with alterations of the subchondral bone plate microstructure. Specific topographical relationships exist in the central region between the articular cartilage and subchondral bone plate thickness, and in the submeniscal periphery between and the articular cartilage and lateral meniscus. From a clinical perspective, the combined follow-up data from this and the previous two investigations suggest that open wedge valgus HTO is a safe procedure for the lateral compartment to manage medial osteoarthritis of the knee with varus malalignment in the short term.

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References

  1. Anetzberger H, Mayer A, Glaser C, Lorenz S, Birkenmaier C, Muller-Gerbl M (2014) Meniscectomy leads to early changes in the mineralization distribution of subchondral bone plate. Knee Surg Sports Traumatol Arthrosc 22(1):112–119

    Article  PubMed  Google Scholar 

  2. Bhattacharyya T, Gale D, Dewire P, Totterman S, Gale ME, McLaughlin S, Einhorn TA, Felson DT (2003) The clinical importance of meniscal tears demonstrated by magnetic resonance imaging in osteoarthritis of the knee. J Bone Joint Surg Am 85-A(1):4–9

    PubMed  Google Scholar 

  3. Brouwer GM, van Tol AW, Bergink AP, Belo JN, Bernsen RM, Reijman M, Pols HA, Bierma-Zeinstra SM (2007) Association between valgus and varus alignment and the development and progression of radiographic osteoarthritis of the knee. Arthritis Rheum 56(4):1204–1211

    Article  CAS  PubMed  Google Scholar 

  4. Cicuttini F, Wluka A, Hankin J, Wang Y (2004) Longitudinal study of the relationship between knee angle and tibiofemoral cartilage volume in subjects with knee osteoarthritis. Rheumatology (Oxford) 43(3):321–324

    Article  CAS  Google Scholar 

  5. Dempsey AR, Wang Y, Thorlund JB, Mills PM, Wrigley TV, Bennell KL, Metcalf BR, Hanna F, Cicuttini FM, Lloyd DG (2012) The relationship between patellofemoral and tibiofemoral morphology and gait biomechanics following arthroscopic partial medial meniscectomy. Knee Surg Sports Traumatol Arthrosc 21(5):1097–1103

    Article  PubMed  Google Scholar 

  6. Floerkemeier S, Staubli AE, Schroeter S, Goldhahn S, Lobenhoffer P (2013) Outcome after high tibial open-wedge osteotomy: a retrospective evaluation of 533 patients. Knee Surg Sports Traumatol Arthrosc 21(1):170–180

    Article  PubMed  Google Scholar 

  7. Heiligenstein S, Cucchiarini M, Laschke MW, Bohle RM, Kohn D, Menger MD, Madry H (2011) In vitro and in vivo characterization of nonbiomedical- and biomedical-grade alginates for articular chondrocyte transplantation. Tissue Eng Part C Methods 17(8):829–842

    Article  CAS  PubMed  Google Scholar 

  8. Henrotin Y, Pesesse L, Sanchez C (2012) Subchondral bone and osteoarthritis: biological and cellular aspects. Osteoporos Int 23(Suppl 8):S847–851

    Article  PubMed  Google Scholar 

  9. Hunter DJ, Zhang YQ, Niu JB, Tu X, Amin S, Clancy M, Guermazi A, Grigorian M, Gale D, Felson DT (2006) The association of meniscal pathologic changes with cartilage loss in symptomatic knee osteoarthritis. Arthritis Rheum 54(3):795–801

    Article  CAS  PubMed  Google Scholar 

  10. Jung WH, Takeuchi R, Chun CW, Lee JS, Ha JH, Kim JH, Jeong JH (2014) Second-look arthroscopic assessment of cartilage regeneration after medial opening-wedge high tibial osteotomy. Arthroscopy 30(1):72–79

    Article  PubMed  Google Scholar 

  11. Kumar D, Schooler J, Zuo J, McCulloch CE, Nardo L, Link TM, Li X, Majumdar S (2013) Trabecular bone structure and spatial differences in articular cartilage MR relaxation times in individuals with posterior horn medial meniscal tears. Osteoarthr Cartil 21(1):86–93

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Lee SJ, Aadalen KJ, Malaviya P, Lorenz EP, Hayden JK, Farr J, Kang RW, Cole BJ (2006) Tibiofemoral contact mechanics after serial medial meniscectomies in the human cadaveric knee. Am J Sports Med 34(8):1334–1344

    Article  PubMed  Google Scholar 

  13. Little CB, Smith MM, Cake MA, Read RA, Murphy MJ, Barry FP (2010) The OARSI histopathology initiative—recommendations for histological assessments of osteoarthritis in sheep and goats. Osteoarthr Cartil 18(Suppl 3):S80–92

    Article  PubMed  Google Scholar 

  14. Lo GH, Niu J, McLennan CE, Kiel DP, McLean RR, Guermazi A, Genant HK, McAlindon TE, Hunter DJ (2008) Meniscal damage associated with increased local subchondral bone mineral density: a Framingham study. Osteoarthr Cartil 16(2):261–267

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Lobenhoffer P, Agneskirchner JD (2003) Improvements in surgical technique of valgus high tibial osteotomy. Knee Surg Sports Traumatol Arthrosc 11(3):132–138

    PubMed  Google Scholar 

  16. Lustig S, Scholes CJ, Costa AJ, Coolican MJ, Parker DA (2013) Different changes in slope between the medial and lateral tibial plateau after open-wedge high tibial osteotomy. Knee Surg Sports Traumatol Arthrosc 21(1):32–38

    Article  CAS  PubMed  Google Scholar 

  17. Madry H (2010) The subchondral bone: a new frontier in articular cartilage repair. Knee Surg Sports Traumatol Arthrosc 18(4):417–418

    Article  PubMed  Google Scholar 

  18. Madry H, Luyten FP, Facchini A (2012) Biological aspects of early osteoarthritis. Knee Surg Sports Traumatol Arthrosc 30(3):407–422

    Article  Google Scholar 

  19. Madry H, van Dijk CN, Mueller-Gerbl M (2010) The basic science of the subchondral bone. Knee Surg Sports Traumatol Arthrosc 18(4):419–433

    Article  PubMed  Google Scholar 

  20. Madry H, Ziegler R, Orth P, Goebel L, Ong MF, Kohn D, Cucchiarini M, Pape D (2013) Effect of open wedge high tibial osteotomy on the lateral compartment in sheep. Part I: analysis of the lateral meniscus. Knee Surg Sports Traumatol Arthrosc 21(1):39–48

    Article  PubMed  Google Scholar 

  21. Mankin HJ (1971) Biochemical and metabolic aspects of osteoarthritis. Orthop Clin North Am 2(1):19–31

    CAS  PubMed  Google Scholar 

  22. McNamara I, Birmingham TB, Fowler PJ, Giffin JR (2013) High tibial osteotomy: evolution of research and clinical applications–a Canadian experience. Knee Surg Sports Traumatol Arthrosc 21(1):23–31

    Article  CAS  PubMed  Google Scholar 

  23. Muller-Gerbl M (1998) The subchondral bone plate. Adv Anat Embryol Cell Biol 141:III–XI, 1–134

  24. Muller-Gerbl M, Putz R, Hodapp NH, Schulta E, Wimmer B (1990) Computed tomography-osteoaboorptiometry: a method of assessing the mechanical condition of the major joints in a living subject. Clin Biomech (Bristol, Avon) 5(4):193–198

    Article  CAS  Google Scholar 

  25. Neogi T, Felson D, Niu J, Lynch J, Nevitt M, Guermazi A, Roemer F, Lewis CE, Wallace B, Zhang Y (2009) Cartilage loss occurs in the same subregions as subchondral bone attrition: a within-knee subregion-matched approach from the Multicenter Osteoarthritis Study. Arthritis Rheum 61(11):1539–1544

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Odgaard A, Pedersen CM, Bentzen SM, Jorgensen J, Hvid I (1989) Density changes at the proximal tibia after medial meniscectomy. J Orthop Res 7(5):744–753

    Article  CAS  PubMed  Google Scholar 

  27. Orth P, Cucchiarini M, Kaul G, Ong MF, Graber S, Kohn DM, Madry H (2012) Temporal and spatial migration pattern of the subchondral bone plate in a rabbit osteochondral defect model. Osteoarthr Cartil 20(10):1161–1169

    Article  CAS  PubMed  Google Scholar 

  28. Orth P, Cucchiarini M, Wagenpfeil S, Menger MD, Madry H (2014) PTH [1-34]-induced alterations of the subchondral bone provoke early osteoarthritis. Osteoarthr Cartil. doi:10.1016/j.joca.2014.03.010

    PubMed  Google Scholar 

  29. Orth P, Goebel L, Wolfram U, Ong MF, Graber S, Kohn D, Cucchiarini M, Ignatius A, Pape D, Madry H (2012) Effect of subchondral drilling on the microarchitecture of subchondral bone: analysis in a large animal model at 6 months. Am J Sports Med 40(4):828–836

    Article  PubMed  Google Scholar 

  30. Orth P, Zurakowski D, Alini M, Cucchiarini M, Madry H (2013) Reduction of sample size requirements by bilateral versus unilateral research designs in animal models for cartilage tissue engineering. Tissue Eng Part C Methods 19(11):885–891

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Pape D, Dueck K, Haag M, Lorbach O, Seil R, Madry H (2013) Wedge volume and osteotomy surface depend on surgical technique for high tibial osteotomy. Knee Surg Sports Traumatol Arthrosc 21(1):206–212

    Article  PubMed  Google Scholar 

  32. Pape D, Madry H (2013) The preclinical sheep model of high tibial osteotomy relating basic science to the clinics: standards, techniques and pitfalls. Knee Surg Sports Traumatol Arthrosc 21(1):228–236

    Article  PubMed  Google Scholar 

  33. Radin EL, Rose RM (1986) Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop Relat Res 213:34–40

    PubMed  Google Scholar 

  34. Raynauld JP, Martel-Pelletier J, Berthiaume MJ, Abram F, Choquette D, Haraoui B, Beary JF, Cline GA, Meyer JM, Pelletier JP (2008) Correlation between bone lesion changes and cartilage volume loss in patients with osteoarthritis of the knee as assessed by quantitative magnetic resonance imaging over a 24-month period. Ann Rheum Dis 67(5):683–688

    Article  PubMed  Google Scholar 

  35. Spahn G, Hofmann GO, von Engelhardt LV, Li M, Neubauer H, Klinger HM (2013) The impact of a high tibial valgus osteotomy and unicondylar medial arthroplasty on the treatment for knee osteoarthritis: a meta-analysis. Knee Surg Sports Traumatol Arthrosc 21(1):96–112

    Article  PubMed  Google Scholar 

  36. Tanamas S, Hanna FS, Cicuttini FM, Wluka AE, Berry P, Urquhart DM (2009) Does knee malalignment increase the risk of development and progression of knee osteoarthritis? A systematic review. Arthritis Rheum 61(4):459–467

    Article  PubMed  Google Scholar 

  37. Wang Y, Dempsey AR, Lloyd DG, Mills PM, Wrigley T, Bennell KL, Metcalf B, Hanna F, Cicuttini FM (2011) Patellofemoral and tibiofemoral articular cartilage and subchondral bone health following arthroscopic partial medial meniscectomy. Knee Surg Sports Traumatol Arthrosc 20(5):970–978

    Article  CAS  PubMed  Google Scholar 

  38. Ziegler R, Goebel L, Cucchiarini M, Pape D, Madry H (2013) Effect of open wedge high tibial osteotomy on the lateral tibiofemoral compartment in sheep. Part II: standard and overcorrection do not cause articular cartilage degeneration. Knee Surg Sports Traumatol Arthrosc. doi:10.1007/s00167-013-2410-6

    Google Scholar 

  39. Zielinska B, Donahue TL (2006) 3D finite element model of meniscectomy: changes in joint contact behavior. J Biomech Eng 128(1):115–123

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. vet. Altmann and her team, Bad Langensalza, Thuringia, for their excellent support in the animal care. Supported in part by an AGA Research Grants to HM and DP, by a Grant of the Department of Orthopaedic Surgery, Saarland University, Homburg/Saar and by a grant of the Center of Experimental Orthopaedics, Saarland University, Homburg/Saar. HM, MC and DP are partners in the “Cartilage Net”, supported by the INTERREG IV Programme of the European Union.

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Correspondence to Henning Madry.

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Ziegler, R., Goebel, L., Seidel, R. et al. Effect of open wedge high tibial osteotomy on the lateral tibiofemoral compartment in sheep. Part III: analysis of the microstructure of the subchondral bone and correlations with the articular cartilage and meniscus. Knee Surg Sports Traumatol Arthrosc 23, 2704–2714 (2015). https://doi.org/10.1007/s00167-014-3134-y

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  • DOI: https://doi.org/10.1007/s00167-014-3134-y

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