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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
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Knee Surgery, Sports Traumatology, Arthroscopy Aims and scope

Abstract

Purpose

To evaluate whether medial open wedge high tibial osteotomy (HTO) results in structural changes in the articular cartilage in the lateral tibiofemoral compartment of adult sheep.

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 contralateral knees that only received an arthrotomy. After 6 months, the macroscopic and microscopic characteristics of the articular cartilage of the lateral tibiofemoral compartment were assessed.

Results

The articular cartilage in the central region of the lateral tibial plateau in sheep had a higher safranin O staining intensity and was 4.6-fold thicker than in the periphery (covered by the lateral meniscus). No topographical variation in the type-II collagen immunoreactivity was seen. All lateral tibial plateaus showed osteoarthritic changes in regions not covered by the lateral meniscus. No osteoarthritis was seen in the peripheral submeniscal regions of the lateral tibial plateau and the lateral femoral condyle. Opening wedge HTO resulting in both standard and overcorrection was not associated with significant macroscopic and microscopic structural changes between groups in the articular cartilage of the lateral tibial plateau and femoral condyle after 6 months in vivo.

Conclusion

Opening wedge HTO resulting in both standard and overcorrection is a safe procedure for the articular cartilage in an intact lateral tibiofemoral compartment of adult sheep at 6 months postoperatively.

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References

  1. Agneskirchner JD, Hurschler C, Wrann CD, Lobenhoffer P (2007) The effects of valgus medial opening wedge high tibial osteotomy on articular cartilage pressure of the knee: a biomechanical study. Arthroscopy 23(8):852–861

    Article  PubMed  Google Scholar 

  2. Allen MJ, Houlton JE, Adams SB, Rushton N (1998) The surgical anatomy of the stifle joint in sheep. Vet Surg 27(6):596–605

    Article  CAS  PubMed  Google Scholar 

  3. Amis AA (2013) Biomechanics of high tibial osteotomy. Knee Surg Sports Traumatol Arthrosc 21(1):197–205

    Article  PubMed  Google Scholar 

  4. Appleyard RC, Burkhardt D, Ghosh P, Read R, Cake M, Swain MV, Murrell GA (2003) Topographical analysis of the structural, biochemical and dynamic biomechanical properties of cartilage in an ovine model of osteoarthritis. Osteoarthritis Cartilage 11(1):65–77

    Article  CAS  PubMed  Google Scholar 

  5. Bedi A, Kelly N, Baad M, Fox AJ, Ma Y, Warren RF, Maher SA (2012) Dynamic contact mechanics of radial tears of the lateral meniscus: implications for treatment. Arthroscopy 28(3):372–381

    Article  PubMed  Google Scholar 

  6. 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 

  7. Cucchiarini M, Thurn T, Weimer A, Kohn D, Terwilliger EF, Madry H (2007) Restoration of the extracellular matrix in human osteoarthritic articular cartilage by overexpression of the transcription factor SOX9. Arthritis Rheum 56(1):158–167

    Article  CAS  PubMed  Google Scholar 

  8. DeFrate LE, Sun H, Gill TJ, Rubash HE, Li G (2004) In vivo tibiofemoral contact analysis using 3D MRI-based knee models. J Biomech 37(10):1499–1504

    Article  PubMed  Google Scholar 

  9. Dye SF (1987) An evolutionary perspective of the knee. J Bone Joint Surg Am 69(7):976–983

    CAS  PubMed  Google Scholar 

  10. Elliott DM, Guilak F, Vail TP, Wang JY, Setton LA (1999) Tensile properties of articular cartilage are altered by meniscectomy in a canine model of osteoarthritis. J Orthop Res 17(4):503–508

    Article  CAS  PubMed  Google Scholar 

  11. Fairbank TJ (1948) Knee joint changes after meniscectomy. J Bone Joint Surg Br 30B(4):664–670

    CAS  PubMed  Google Scholar 

  12. Fine KM, Glasgow SG, Torg JS (1995) Tibial chondral fissures associated with the lateral meniscus. Arthroscopy 11(3):292–295

    Article  CAS  PubMed  Google Scholar 

  13. 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 

  14. Frisbie DD, Cross MW, McIlwraith CW (2006) A comparative study of articular cartilage thickness in the stifle of animal species used in human pre-clinical studies compared to articular cartilage thickness in the human knee. Vet Comp Orthop Traumatol 19(3):142–146

    CAS  PubMed  Google Scholar 

  15. Fukuda Y, Takai S, Yoshino N, Murase K, Tsutsumi S, Ikeuchi K, Hirasawa Y (2000) Impact load transmission of the knee joint-influence of leg alignment and the role of meniscus and articular cartilage. Clin Biomech (Bristol, Avon) 15(7):516–521

    Article  CAS  Google Scholar 

  16. Heijink A, Gomoll AH, Madry H, Drobnic M, Filardo G, Espregueira-Mendes J, Van Dijk CN (2012) Biomechanical considerations in the pathogenesis of osteoarthritis of the knee. Knee Surg Sports Traumatol Arthrosc 20(3):423–435

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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 

  18. Hernigou P, Medevielle D, Debeyre J, Goutallier D (1987) Proximal tibial osteotomy for osteoarthritis with varus deformity. A ten to thirteen-year follow-up study. J Bone Joint Surg Am 69(3):332–354

    CAS  PubMed  Google Scholar 

  19. Ishida K, Kuroda R, Sakai H, Doita M, Kurosaka M, Yoshiya S (2006) Rapid chondrolysis after arthroscopic partial lateral meniscectomy in athletes: a case report. Knee Surg Sports Traumatol Arthrosc 14(12):1266–1269

    Article  PubMed  Google Scholar 

  20. Kaul G, Cucchiarini M, Arntzen D, Zurakowski D, Menger MD, Kohn D, Trippel SB, Madry H (2006) Local stimulation of articular cartilage repair by transplantation of encapsulated chondrocytes overexpressing human fibroblast growth factor 2 (FGF-2) in vivo. J Gene Med 8(1):100–111

    Article  CAS  PubMed  Google Scholar 

  21. Kwon SK, Moon HK, Choi CJ, Park SH, Lee JJ, Kim YC, Park YS, Koh YG (2012) Accelerated degeneration of the discoid lateral meniscus after medial opening wedge high tibial osteotomy. Knee Surg Sports Traumatol Arthrosc. doi:10.1007/s00167-012-2289-7

    Google Scholar 

  22. Lai WM, Hou JS, Mow VC (1991) A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng 113(3):245–258

    Article  CAS  PubMed  Google Scholar 

  23. Lanzer WL, Komenda G (1990) Changes in articular cartilage after meniscectomy. Clin Orthop Relat Res 252:41–48

    PubMed  Google Scholar 

  24. LeRoux MA, Arokoski J, Vail TP, Guilak F, Hyttinen MM, Kiviranta I, Setton LA (2000) Simultaneous changes in the mechanical properties, quantitative collagen organization, and proteoglycan concentration of articular cartilage following canine meniscectomy. J Orthop Res 18(3):383–392

    Article  CAS  PubMed  Google Scholar 

  25. Li G, DeFrate LE, Park SE, Gill TJ, Rubash HE (2005) In vivo articular cartilage contact kinematics of the knee: an investigation using dual-orthogonal fluoroscopy and magnetic resonance image-based computer models. Am J Sports Med 33(1):102–107

    Article  CAS  PubMed  Google Scholar 

  26. Li G, Park SE, DeFrate LE, Schutzer ME, Ji L, Gill TJ, Rubash HE (2005) The cartilage thickness distribution in the tibiofemoral joint and its correlation with cartilage-to-cartilage contact. Clin Biomech (Bristol, Avon) 20(7):736–744

    Article  Google Scholar 

  27. Little C, Smith S, Ghosh P, Bellenger C (1997) Histomorphological and immunohistochemical evaluation of joint changes in a model of osteoarthritis induced by lateral meniscectomy in sheep. J Rheumatol 24(11):2199–2209

    CAS  PubMed  Google Scholar 

  28. 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. Osteoarthritis Cartilage 18(Suppl 3):S80–S92

    Article  PubMed  Google Scholar 

  29. Madry H, Cucchiarini M, Stein U, Remberger K, Menger MD, Kohn D, Trippel SB (2003) Sustained transgene expression in cartilage defects in vivo after transplantation of articular chondrocytes modified by lipid-mediated gene transfer in a gel suspension delivery system. J Gene Med 5(6):502–509

    Article  CAS  PubMed  Google Scholar 

  30. Madry H, Kaul G, Cucchiarini M, Stein U, Zurakowski D, Remberger K, Menger MD, Kohn D, Trippel SB (2005) Enhanced repair of articular cartilage defects in vivo by transplanted chondrocytes overexpressing insulin-like growth factor I (IGF-I). Gene Ther 12(15):1171–1179

    Article  CAS  PubMed  Google Scholar 

  31. Madry H, Luyten FP, Facchini A (2012) Biological aspects of early osteoarthritis. Knee Surg Sports Traumatol Arthrosc 20(3):407–422

    Article  PubMed  Google Scholar 

  32. 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 

  33. Mankin HJ, Dorfman H, Lippiello L, Zarins A (1971) Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 53(3):523–537

    CAS  PubMed  Google Scholar 

  34. McDermott ID, Amis AA (2006) The consequences of meniscectomy. J Bone Joint Surg Br 88(12):1549–1556

    Article  CAS  PubMed  Google Scholar 

  35. McLeod WD, Moschi A, Andrews JR, Hughston JC (1977) Tibial plateau topography. Am J Sports Med 5(1):13–18

    Article  CAS  PubMed  Google Scholar 

  36. Meachim G (1972) Light microscopy of Indian ink preparations of fibrillated cartilage. Ann Rheum Dis 31(6):457–464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Moen TC, Laskin W, Puri L (2011) The lateral compartment in knees with isolated medial and patellofemoral osteoarthritis: a histologic analysis of articular cartilage. J Arthroplasty 26(5):783–787

    Article  PubMed  Google Scholar 

  38. Mow VC, Holmes MH, Lai WM (1984) Fluid transport and mechanical properties of articular cartilage: a review. J Biomech 17(5):377–394

    Article  CAS  PubMed  Google Scholar 

  39. Muller-Gerbl M, Putz R, Kenn R (1992) Demonstration of subchondral bone density patterns by three-dimensional CT osteoabsorptiometry as a noninvasive method for in vivo assessment of individual long-term stresses in joints. J Bone Miner Res 7(Suppl 2):S411–S418

    Article  PubMed  Google Scholar 

  40. Muller-Gerbl M, Schulte E, Putz R (1987) The thickness of the calcified layer of articular cartilage: a function of the load supported? J Anat 154:103–111

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Nepple JJ, Wright RW, Matava MJ, Brophy RH (2012) Full-thickness knee articular cartilage defects in national football league combine athletes undergoing magnetic resonance imaging: prevalence, location, and association with previous surgery. Arthroscopy 28(6):798–806

    Article  PubMed  Google Scholar 

  42. Niemeyer P, Schmal H, Hauschild O, von Heyden J, Sudkamp NP, Kostler W (2010) Open-wedge osteotomy using an internal plate fixator in patients with medial-compartment gonarthritis and varus malalignment: 3-year results with regard to preoperative arthroscopic and radiographic findings. Arthroscopy 26(12):1607–1616

    Article  PubMed  Google Scholar 

  43. Oakley SP, Lassere MN, Portek I, Szomor Z, Ghosh P, Kirkham BW, Murrell GA, Wulf S, Appleyard RC (2004) Biomechanical, histologic and macroscopic assessment of articular cartilage in a sheep model of osteoarthritis. Osteoarthritis Cartilage 12(8):667–679

    Article  CAS  PubMed  Google Scholar 

  44. Orth P, Zurakowski D, Wincheringer D, Madry H (2012) Reliability, reproducibility, and validation of five major histological scoring systems for experimental articular cartilage repair in the rabbit model. Tissue Eng Part C Methods 18(5):329–339

    Article  CAS  PubMed  Google Scholar 

  45. Otsuki S, Nakajima M, Lotz M, Kinoshita M (2008) Hyaluronic acid and chondroitin sulfate content of osteoarthritic human knee cartilage: site-specific correlation with weight-bearing force based on femorotibial angle measurement. J Orthop Res 26(9):1194–1198

    Article  PubMed  Google Scholar 

  46. Outerbridge RE (1961) The etiology of chondromalacia patellae. J Bone Joint Surg Br 43-B:752–757

    CAS  PubMed  Google Scholar 

  47. 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 

  48. Parker DA, Beatty KT, Giuffre B, Scholes CJ, Coolican MR (2011) Articular cartilage changes in patients with osteoarthritis after osteotomy. Am J Sports Med 39(5):1039–1045

    Article  PubMed  Google Scholar 

  49. Pelletier JP, Raynauld JP, Berthiaume MJ, Abram F, Choquette D, Haraoui B, Beary JF, Cline GA, Meyer JM, Martel-Pelletier J (2007) Risk factors associated with the loss of cartilage volume on weight-bearing areas in knee osteoarthritis patients assessed by quantitative magnetic resonance imaging: a longitudinal study. Arthritis Res Ther 9(4):R74

    Article  PubMed  PubMed Central  Google Scholar 

  50. Pritzker KP, Gay S, Jimenez SA, Ostergaard K, Pelletier JP, Revell PA, Salter D, van den Berg WB (2006) Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage 14(1):13–29

    Article  CAS  PubMed  Google Scholar 

  51. 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

    PubMed  Google Scholar 

  52. Rutgers M, Bartels LW, Tsuchida AI, Castelein RM, Dhert WJ, Vincken KL, van Heerwaarden RJ, Saris DB (2012) dGEMRIC as a tool for measuring changes in cartilage quality following high tibial osteotomy: a feasibility study. Osteoarthritis Cartilage 20(10):1134–1141

    Article  CAS  PubMed  Google Scholar 

  53. Schallberger A, Jacobi M, Wahl P, Maestretti G, Jakob RP (2011) High tibial valgus osteotomy in unicompartmental medial osteoarthritis of the knee: a retrospective follow-up study over 13–21 years. Knee Surg Sports Traumatol Arthrosc 19(1):122–127

    Article  PubMed  Google Scholar 

  54. Schmitz N, Laverty S, Kraus VB, Aigner T (2010) Basic methods in histopathology of joint tissues. Osteoarthritis Cartilage 18(Suppl 3):S113–S116

    Article  PubMed  Google Scholar 

  55. Servien E, Acquitter Y, Hulet C, Seil R (2009) Lateral meniscus lesions on stable knee: a prospective multicenter study. Orthop Traumatol Surg Res 95(8 Suppl 1):S60–S64

    Article  CAS  PubMed  Google Scholar 

  56. Shepherd DE, Seedhom BB (1999) Thickness of human articular cartilage in joints of the lower limb. Ann Rheum Dis 58(1):27–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Spahn G, Klinger HM, Harth P, Hofmann GO (2012) Cartilage regeneration after high tibial osteotomy. Results of an arthroscopic study. Z Orthop Unfall 150(3):272–279

    CAS  PubMed  Google Scholar 

  58. Staubli AE, Jacob HA (2010) Evolution of open-wedge high-tibial osteotomy: experience with a special angular stable device for internal fixation without interposition material. Int Orthop 34(2):167–172

    Article  PubMed  PubMed Central  Google Scholar 

  59. Tetsworth K, Paley D (1994) Malalignment and degenerative arthropathy. Orthop Clin North Am 25(3):367–377

    CAS  PubMed  Google Scholar 

  60. Thambyah A, Nather A, Goh J (2006) Mechanical properties of articular cartilage covered by the meniscus. Osteoarthritis Cartilage 14(6):580–588

    Article  CAS  PubMed  Google Scholar 

  61. Wei L, Hjerpe A, Brismar BH, Svensson O (2001) Effect of load on articular cartilage matrix and the development of guinea-pig osteoarthritis. Osteoarthritis Cartilage 9(5):447–453

    Article  CAS  PubMed  Google Scholar 

  62. Yao JQ, Seedhom BB (1993) Mechanical conditioning of articular cartilage to prevalent stresses. Br J Rheumatol 32(11):956–965

    Article  CAS  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 Grant (Forschungsförderung 29/2008) to HM and DP and by a grant of the Department of Orthopaedic Surgery, 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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Authors and Affiliations

  1. Center of Experimental Orthopaedics, Saarland University, Kirrbergerstr. 1, Bldg 37, 66421, Homburg, Saar, Germany

    Raphaela Ziegler, Lars Goebel, Magali Cucchiarini & Henning Madry

  2. Department of Orthopaedic Surgery, Saarland University, 66421, Homburg, Germany

    Henning Madry

  3. Department of Orthopaedic Surgery, Centre Hospitalier de Luxembourg, 1460, Luxembourg, Luxembourg

    Dietrich Pape

  4. Sports Medicine Research Laboratory, Centre Médical de la Fondation Norbert Metz, Public Research Centre for Health, Luxembourg, 76 rue d’Eich, 1460, Luxembourg, Luxembourg

    Dietrich Pape

  5. Cartilage Net of the Greater Region, Homburg, Germany

    Magali Cucchiarini, Dietrich Pape & Henning Madry

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  1. Raphaela Ziegler
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  2. Lars Goebel
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  3. Magali Cucchiarini
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  4. Dietrich Pape
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  5. Henning Madry
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Correspondence to Henning Madry.

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Ziegler, R., Goebel, L., Cucchiarini, M. et al. 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 22, 1666–1677 (2014). https://doi.org/10.1007/s00167-013-2410-6

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