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.
Similar content being viewed by others
References
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
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
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
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
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
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
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
Henrotin Y, Pesesse L, Sanchez C (2012) Subchondral bone and osteoarthritis: biological and cellular aspects. Osteoporos Int 23(Suppl 8):S847–851
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
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
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
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
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
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
Lobenhoffer P, Agneskirchner JD (2003) Improvements in surgical technique of valgus high tibial osteotomy. Knee Surg Sports Traumatol Arthrosc 11(3):132–138
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
Madry H (2010) The subchondral bone: a new frontier in articular cartilage repair. Knee Surg Sports Traumatol Arthrosc 18(4):417–418
Madry H, Luyten FP, Facchini A (2012) Biological aspects of early osteoarthritis. Knee Surg Sports Traumatol Arthrosc 30(3):407–422
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
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
Mankin HJ (1971) Biochemical and metabolic aspects of osteoarthritis. Orthop Clin North Am 2(1):19–31
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
Muller-Gerbl M (1998) The subchondral bone plate. Adv Anat Embryol Cell Biol 141:III–XI, 1–134
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
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
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
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
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
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
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
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
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
Radin EL, Rose RM (1986) Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop Relat Res 213:34–40
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
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
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
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
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
Zielinska B, Donahue TL (2006) 3D finite element model of meniscectomy: changes in joint contact behavior. J Biomech Eng 128(1):115–123
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.
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00167-014-3134-y