Abstract
Objective
To evaluate repair tissue (RT) after microfracture treatment for full-thickness cartilage defect models using quantitative MRI and investigate the correlations between MRI and histological findings.
Materials and methods
The animal experiment was approved by the Animal Care and Use Committee of our college. Thirty-six full-thickness cartilage defect models in rabbit knee joints were assigned to the microfracture or joint debridement group (as control). Each group consisted of 3-week, 5-week, and 7-week subgroups. MR imaging, including a three-dimensional double-echo steady-state sequence (3D-DESS), and T2 mapping were performed at 3, 5, and 7 weeks postoperatively. The thickness and T2 indices of RT were calculated. After MRI scans at each time point, operation sites were removed to make hematoxylin-eosin (H&E)-stained sections. Histological results were evaluated using the modified O’Driscoll score system. Comparisons were made between the two groups with respect to the MRI and histological findings, and correlation analysis was performed within each group.
Results
The thickness index and histological O’Driscoll score of RT in the two groups increased over time, while the T2 index decreased. The thickness index and histological O’Driscoll score of the microfracture group were higher than in the joint debridement group at each time point. The T2 index of the microfracture group was lower than in the joint debridement group at 3 weeks (P = 0.006), while it was higher than in the joint debridement group at 5 and 7 weeks (P = 0.025 and 0.025). The thickness index was positively correlated with the histological O’Driscoll score in both groups (microfracture: r s = 0.745, P < 0.001; joint debridement: r s = 0.680, P = 0.002). The T2 index was negatively correlated with the histological O’Driscoll score in both groups (microfracture: r s = −0.715, P = 0.002; joint debridement: r s = −0.826, P < 0.001).
Conclusion
Significant improvement over time after microfracture can be expected on the basis of the quantitative MRI finding and histological O’Driscoll score. MRI was correlated with the histological O’Driscoll score, which indicated that quantitative MRI 3D-DESS and T2 mapping could evaluate cartilage repair after microfracture as an effective noninvasive tool.
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References
Eshed I, Trattnig S, Sharon M, et al. Assessment of cartilage repair after chondrocyte transplantation with a fibrin-hyaluronan matrix—correlation of morphological MRI, biochemical T2 mapping and clinical outcome. Eur J Radiol. 2012;81(6):1216–23.
Marder RA, Hopkins G, Timmerman LA. Arthroscopic microfracture of chondral defects of the knee: a comparison of two postoperative treatments. Arthrosc. 2005;21(2):152–8.
Von Keudella A, Atzwanger J, Forstner R, et al. Radiological evaluation of cartilage after microfracture treatment: a long-term follow-up study. Eur J Radiol. 2012;81(7):1618–24.
Lim HC, Bae JH, Song SH, et al. Current treatments of isolated articular cartilage lesions of the knee achieve similar outcomes. Clin Orthop Relat Res. 2012;470(8):2261–7.
Kreuz PC, Steinwachs MR, Erggelet C, et al. Results after microfracture of full-thickness chondral defects in different compartments in the knee. Osteoarthritis Cartilage. 2006;14(11):1119–25.
Mithoefer K, Williams RJ, Warren RF, et al. The microfracture technique for the treatment of articular cartilage lesions in the knee—a prospective cohort study. J Bone Joint Surg Am. 2005;87A(9):1911–20.
Mithoefer K, McAdams T, Williams RJ, et al. Clinical efficacy of the microfracture technique for articular cartilage repair in the knee an evidence-based systematic analysis. Am J Sports Med. 2009;37(10):2053–63.
Steadman JR, Rodkey WG, Briggs KK, et al. The microfracture technique to treat full thickness articular cartilage defects of the knee. Orthopade. 1999;28(1):26–32.
Henderson I, Lavigne P, Valenzuela H, et al. Autologous chondrocyte implantation: superior biologic properties of hyaline cartilage repairs. Clin Orthop Relat Res 2007;455.
Peterson L, Minas T, Brittberg M, et al. Two- to 9-year outcome after autologous chondrocyte transplantation of the knee. Clin Orthop Relat Res. 2000;374:212–34.
Apprich S, Trattnig S, Welsch GH, et al. Assessment of articular cartilage repair tissue after matrix-associated autologous chondrocyte transplantation or the microfracture technique in the ankle joint using diffusion-weighted imaging at 3 Tesla (vol 20, pg 703, 2012). Osteoarthr Cartil. 2012;20(9):1056.
Kurkijarvi JE, Mattila L, Ojala RO, et al. Evaluation of cartilage repair in the distal femur after autologous chondrocyte transplantation using T-2 relaxation time and dGEMRIC. Osteoarthr Cartil. 2007;15(4):372–8.
Welsch GH, Mamisch TC, Domayer SE, et al. Cartilage T2 assessment at 3-T MR imaging: in vivo differentiation of normal hyaline cartilage from reparative tissue after two cartilage repair procedures—initial experience. Radiology. 2008;247(1):154–61.
Trattnig S, Ba-Ssalamah A, Pinker K, et al. Matrix-based autologous chondrocyte implantation for cartilage repair: noninvasive monitoring by high-resolution magnetic resonance imaging. Magn Reson Imaging. 2005;23(7):779–87.
Welsch GH, Trattnig S, Scheffler K, et al. Magnetization transfer contrast and T2 mapping in the evaluation of cartilage repair tissue with 3T MRI. J Magn Reson Imaging. 2008;28(4):979–86.
Welsch GH, Trattnig S, Domayer S, et al. Multimodal approach in the use of clinical scoring, morphological MRI and biochemical T2-mapping and diffusion-weighted imaging in their ability to assess differences between cartilage repair tissue after microfracture therapy and matrix-associated autologous chondrocyte transplantation: a pilot study. Osteoarthr Cartil. 2009;17(9):1219–27.
Lee KT, Choi YS, Lee YK, et al. Comparison of MRI and arthroscopy in modified MOCART scoring system after autologous chondrocyte implantation for osteochondral lesion of the talus. Orthop 2011;34(8).
Ramappa AJ, Gill TJ, Bradford CH, et al. Magnetic resonance imaging to assess knee cartilage repair tissue after microfracture of chondral defects. J Knee Surg 2007;20(3).
Oneto JMM, Ellermann J, LaPrade RF. Longitudinal evaluation of cartilage repair tissue after microfracture using T2-mapping: a case report with arthroscopic and MRI correlation. Knee Surg Sports Traumatol. Arthrosc: Off J ESSKA 2010;18(11).
Domayer SE, Kutscha-Lissberg F, Welsch G, et al. T2 mapping in the knee after microfracture at 3.0 T: correlation of global T2 values and clinical outcome—preliminary results. Osteoarthritis Cartilage. 2008;16(8):903–8.
Glaser C. New techniques for cartilage imaging: T2 relaxation time and diffusion-weighted MR imaging. Radiol Clin N Am. 2005;43(4):641.
Watanabe A, Boesch C, Anderson SE, et al. Ability of dGEMRIC and T2 mapping to evaluate cartilage repair after microfracture: a goat study. Osteoarthr Cartil. 2009;17(10):1341–9.
Trattnig S, Mamisch TC, Welsch GH, et al. Quantitative T-2 mapping of matrix-associated autologous chondrocyte transplantcation at 3 Tesla—an in vivo cross-sectional study. Invest Radiol. 2007;42(6):442–8.
Theologis AA, Schairer WW, Carballido-Gamio J, et al. Longitudinal analysis of T-1 rho and T-2 quantitative MRI of knee cartilage laminar organization following microfracture surgery. Knee. 2012;19(5):652–7.
White LM, Sussman MS, Hurtig M, et al. Cartilage T2 assessment: differentiation of normal hyaline cartilage and reparative tissue after arthroscopic cartilage repair in equine subjects. Radiology. 2006;241(2):407–14.
Frisbie DD, Trotter GW, Powers BE, et al. Arthroscopic subchondral bone plate microfracture technique augments healing of large chondral defects in the radial carpal bone and medial femoral condyle of horses. Vet Surg. 1999;28(4):242–55.
Jackson DW, Lalor PA, Aberman HM, et al. Spontaneous repair of full-thickness defects of articular cartilage in a goat model—a preliminary study. J Bone Joint Surg Am. 2001;83A(1):53–64.
Hunziker EB. Biologic repair of articular cartilage. Defect models in experimental animals and matrix requirements. Clin Orthop Relat Res 1999(367 Suppl):S135-46.
Wei X, Gao J, Messner K. Maturation-dependent repair of untreated osteochondral defects in the rabbit knee joint. J Biomed Mater Res. 1997;34(1):63–72.
Dell’Accio F, Vanlauwe J, Bellemans J, et al. Expanded phenotypically stable chondrocytes persist in the repair tissue and contribute to cartilage matrix formation and structural integration in a goat model of autologous chondrocyte implantation. J Orthop Res. 2003;21(1):123–31.
Chu CR, Szczodry M, Bruno S. Animal models for cartilage regeneration and repair. Tissue Eng Part B Rev. 2010;16(1):105–15.
Chen H, Sun J, Hoemann CD, et al. Drilling and microfracture lead to different bone structure and necrosis during bone-marrow stimulation for cartilage repair. J Orthop Res. 2009;27(11):1432–8.
Yang HS, La WG, Bhang SH, et al. Hyaline cartilage regeneration by combined therapy of microfracture and long-term bone morphogenetic protein-2 delivery. Tissue Eng Part A. 2011;17(13–14):1809–18.
Grunder W, Wagner M, Werner A. MR-microscopic visualization of anisotropic internal cartilage structures using the magic angle technique. Magn Reson Med. 1998;39(3):376–82.
Rubenstein JD, KIM JK, Moravaprotzner I, et al. Effects of collagen orientation on mr-imaging characteristics of bovine articular-cartilage. Radiology. 1993;188(1):219–26.
Ahn JH, Lee SH, Choi SH, et al. Magnetic resonance imaging evaluation of anterior cruciate ligament reconstruction using quadrupled hamstring tendon autografts: comparison of remnant bundle preservation and standard technique. Am J Sports Med. 2010;38(9):1768–77.
Strauss E, Schachter A, Frenkel S, et al. The efficacy of intra-articular hyaluronan injection after the microfracture technique for the treatment of articular cartilage lesions. Am J Sports Med. 2009;37(4):720–6.
Domayer SE, Welsch GH, Dorotka R, et al. MRI monitoring of cartilage repair in the knee: a review. Semin Musculoskelet Radiol. 2008;12(4):302–17.
Shim IK, Yook YJ, Lee SY, et al. Healing of articular cartilage defects treated with a novel drug-releasing rod-type implant after microfracture surgery. J Control Release. 2008;129(3):187–91.
Watrin-Pinzano A, Ruaud JP, Cheli Y, et al. Evaluation of cartilage repair tissue after biomaterial implantation in rat patella by using T2 mapping. MAGMA. 2004;17(3–6):219–28.
Nissi MJ, Rieppo J, Toyras J, et al. T-2 relaxation time mapping reveals age- and species-related diversity of collagen network architecture in articular cartilage. Osteoarthr Cartil. 2006;14(12):1265–71.
Mamisch TC, Hughes T, Mosher TJ, et al. T2 star relaxation times for assessment of articular cartilage at 3 T: a feasibility study. Skeletal Radiol. 2012;41(3):287–92.
Brittberg M, Nilsson A, Lindahl A, et al. Rabbit articular cartilage defects treated with autologous cultured chondrocytes. Clin Orthop Relat Res. 1996;326:270–83.
Nieminen MT, Rieppo J, Silvennoinen J, et al. Spatial assessment of articular cartilage proteoglycans with Gd-DTPA-enhanced T1 imaging. Magn Reson Med. 2002;48(4):640–8.
Raya JG, Horng A, Dietrich O, et al. Articular cartilage: in vivo diffusion-tensor imaging. Radiology. 2012;262(2):550–9.
Li X, Benjamin C, Link TM, et al. In vivo T-1 rho arid T-2 mapping of articular cartilage in osteoarthritis of the knee using 3T MRI. Osteoarthr Cartil. 2007;15(7):789–97.
Holtzman DJ, Theologis AA, Carballido-Gamio J, et al. T-1 rho and T-2 quantitative magnetic resonance imaging analysis of cartilage regeneration following microfracture and mosaicplasty cartilage resurfacing procedures. J Magn Reson Imaging. 2010;32(4):914–23.
Regatte RR, Akella S, Lonner JH, et al. T-1p relaxation mapping in human osteoarthritis (OA) cartilage: comparison of T-1p with T-2. J Magn Reson Imaging. 2006;23(4):547–53.
Borthakur A, Mellon E, Niyogi S, et al. Sodium and T-1 rho MRI for molecular and diagnostic imaging of articular cartilage. NMR Biomed. 2006;19(7):781–821.
Acknowledgments
The authors would like to thank Ye Yang for his comments on the manuscript and Dongling Yang for her advice on statistics.
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All the authors have no conflicts of interest.
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Tao, H., Li, H., Hua, Y. et al. Quantitative magnetic resonance imaging (MRI) evaluation of cartilage repair after microfracture treatment for full-thickness cartilage defect models in rabbit knee joints: correlations with histological findings. Skeletal Radiol 44, 393–402 (2015). https://doi.org/10.1007/s00256-014-2062-8
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DOI: https://doi.org/10.1007/s00256-014-2062-8