High resolution MRI imaging at 9.4 Tesla of the osteochondral unit in a translational model of articular cartilage repair

BMC Musculoskeletal Disorders

Henning Madry²  Arno Bücker¹  Andreas Müller¹  Lars Goebel² 

[1]Department of Diagnostic and Interventional Radiology, Saarland University Medical Center, Kirrberger Straße, Building 57, Homburg/Saar D-66421, Germany

[2]Cartilage Net of the Greater Region, University of the Greater Region, Homburg/Saar D-66421, Germany

关键词: SGE 3D;    Marrow stimulation;    Cartilage defect;    Sheep;    High-field MRI;   

Others  :  1174845
DOI  :  10.1186/s12891-015-0543-0

 received in 2014-10-29, accepted in 2015-03-27,  发布年份 2015

【 摘 要 】

Background

Non-destructive structural evaluation of the osteochondral unit is challenging. Here, the capability of high-field magnetic resonance imaging (μMRI) at 9.4 Tesla (T) was explored to examine osteochondral repair ex vivo in a preclinical large animal model. A specific aim of this study was to detect recently described alterations of the subchondral bone associated with cartilage repair.

Methods

Osteochondral samples of medial femoral condyles from adult ewes containing full-thickness articular cartilage defects treated with marrow stimulation were obtained after 6 month in vivo and scanned in a 9.4 T μMRI. Ex vivo imaging of small osteochondral samples (typical volume: 1–2 cm³) at μMRI was optimised by variation of repetition time (TR), time echo (TE), flip angle (FA), spatial resolution and number of excitations (NEX) from standard MultiSliceMultiEcho (MSME) and three-dimensional (3D) spoiled GradientEcho (SGE) sequences.

Results

A 3D SGE sequence with the parameters: TR = 10 ms, TE = 3 ms, FA = 10 °, voxel size = 120 × 120 × 120 μm³ and NEX = 10 resulted in the best fitting for sample size, image quality, scanning time and artifacts. An isovolumetric voxel shape allowed for multiplanar reconstructions. Within the osteochondral unit articular cartilage, cartilaginous repair tissue and bone marrow could clearly be distinguished from the subchondral bone plate and subarticular spongiosa. Specific alterations of the osteochondral unit associated with cartilage repair such as persistent drill holes, subchondral bone cysts, sclerosis of the subchondral bone plate and of the subarticular spongiosa and intralesional osteophytes were precisely detected.

Conclusions

High resolution, non-destructive ex vivo analysis of the entire osteochondral unit in a preclinical large animal model that is sufficient for further analyses is possible using μMRI at 9.4 T. In particular, 9.4 T is capable of accurately depicting alterations of the subchondral bone that are associated with osteochondral repair.

【 授权许可】

   
2015 Goebel et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Gomoll AH, Madry H, Knutsen G, van Dijk N, Seil R, Brittberg M, et al.: The subchondral bone in articular cartilage repair: current problems in the surgical management. Knee Surg Sports Traumatol Arthrosc 2010, 18:434-47.
• [2]Madry H: The subchondral bone: a new frontier in articular cartilage repair. Knee Surg Sports Traumatol Arthrosc 2010, 18:417-8.
• [3]Madry H, van Dijk CN, Mueller-Gerbl M: The basic science of the subchondral bone. Knee Surg Sports Traumatol Arthrosc 2010, 18:419-33.
• [4]Orth P, Cucchiarini M, Kohn D, Madry H: Alterations of the subchondral bone in osteochondral repair-translational data and clinical evidence. Eur Cell Mater 2013, 25:299-316.
• [5]Orth P, Madry H: A low morbidity surgical approach to the sheep femoral trochlea. BMC Musculoskelet Disord 2013, 14:5. BioMed Central Full Text
• [6]Osterhoff G, Loffler S, Steinke H, Feja C, Josten C, Hepp P: Comparative anatomical measurements of osseous structures in the ovine and human knee. Knee 2011, 18:98-103.
• [7]Pape D, Filardo G, Kon E, van Dijk CN, Madry H: Disease-specific clinical problems associated with the subchondral bone. Knee Surg Sports Traumatol Arthrosc 2010, 18:448-62.
• [8]Madry H, Grun UW, Knutsen G: Cartilage repair and joint preservation: medical and surgical treatment options. Dtsch Arztebl Int 2011, 108:669-77.
• [9]Goebel L, Orth P, Muller A, Zurakowski D, Bucker A, Cucchiarini M, et al.: Experimental scoring systems for macroscopic articular cartilage repair correlate with the MOCART score assessed by a high-field MRI at 9.4 T–comparative evaluation of five macroscopic scoring systems in a large animal cartilage defect model. Osteoarthritis Cartilage 2012, 20(9):1046-55.
• [10]Goebel L, Zurakowski D, Müller A, Pape D, Cucchiarini M, Madry H: 2D and 3D MOCART scoring systems assessed by 9.4 Tesla high-field MRI correlate with elementary and complex histological scoring systems in a translational model of osteochondral repair. Osteoarthritis Cartilage 2014, 22:1386-95.
• [11]Garnov N, Grunder W, Thormer G, Trampel R, Turner R, Kahn T, et al.: In vivo MRI analysis of depth-dependent ultrastructure in human knee cartilage at 7 T. NMR Biomed 2013, 26:1412-9.
• [12]Kijowski R, Blankenbaker DG, Munoz Del Rio A, Baer GS, Graf BK: Evaluation of the articular cartilage of the knee joint: value of adding a T2 mapping sequence to a routine MR imaging protocol. Radiology 2013, 267:503-13.
• [13]Krug R, Stehling C, Kelley DA, Majumdar S, Link TM: Imaging of the musculoskeletal system in vivo using ultra-high field magnetic resonance at 7 T. Invest Radiol 2009, 44:613-8.
• [14]Kudo H, Inaoka T, Kitamura N, Nakatsuka T, Kasuya S, Kasai R, et al.: Clinical value of routine use of thin-section 3D MRI using 3D FSE sequences with a variable flip angle technique for internal derangements of the knee joint at 3 T. Magn Reson Imaging 2013, 31:1309-17.
• [15]Roemer FW, Guermazi A, Trattnig S, Apprich S, Marlovits S, Niu J, et al.: Whole joint MRI assessment of surgical cartilage repair of the knee: cartilage repair osteoarthritis knee score (CROAKS). Osteoarthritis Cartilage 2014, 22:779-99.
• [16]Van Dyck P, Kenis C, Vanhoenacker FM, Lambrecht V, Wouters K, Gielen JL, et al.: Comparison of 1.5- and 3-T MR imaging for evaluating the articular cartilage of the knee. Knee Surg Sports Traumatol Arthrosc 2014, 22:1376-84.
• [17]Bottcher P, Bruhschwein A, Winkels P, Werner H, Ludewig E, Grevel V, et al.: Value of low-field magnetic resonance imaging in diagnosing meniscal tears in the canine stifle: a prospective study evaluating sensitivity and specificity in naturally occurring cranial cruciate ligament deficiency with arthroscopy as the gold standard. Vet Surg 2010, 39:296-305.
• [18]McErlain DD, Ulici V, Darling M, Gati JS, Pitelka V, Beier F, et al.: An in vivo investigation of the initiation and progression of subchondral cysts in a rodent model of secondary osteoarthritis. Arthritis Res Ther 2012, 14:R26. BioMed Central Full Text
• [19]Pepin SR, Griffith CJ, Wijdicks CA, Goerke U, McNulty MA, Parker JB, et al.: A comparative analysis of 7.0-Tesla magnetic resonance imaging and histology measurements of knee articular cartilage in a canine posterolateral knee injury model: a preliminary analysis. Am J Sports Med 2009, 37:119S-24.
• [20]Wang M, Radjenovic A, Stapleton TW, Venkatesh R, Williams S, Ingham E, et al.: A novel and non-destructive method to examine meniscus architecture using 9.4 Tesla MRI. Osteoarthritis Cartilage 2010, 18:1417-20.
• [21]Moser E, Stahlberg F, Ladd ME, Trattnig S: 7-T MR–from research to clinical applications? NMR Biomed 2012, 25:695-716.
• [22]Moser E: Ultra-high-field magnetic resonance: Why and when? World J Radiol 2010, 2:37-40.
• [23]Chang G, Friedrich KM, Wang L, Vieira RL, Schweitzer ME, Recht MP, et al.: MRI of the wrist at 7 tesla using an eight-channel array coil combined with parallel imaging: preliminary results. J Magn Reson Imaging 2010, 31:740-6.
• [24]Rooney WD, Johnson G, Li X, Cohen ER, Kim SG, Ugurbil K, et al.: Magnetic field and tissue dependencies of human brain longitudinal 1H2O relaxation in vivo. Magn Reson Med 2007, 57:308-18.
• [25]van den Bergen B, van den Berg CA, Klomp DW, Lagendijk JJ: SAR and power implications of different RF shimming strategies in the pelvis for 7 T MRI. J Magn Reson Imaging 2009, 30:194-202.
• [26]Weber H, Baxan N, Paul D, Maclaren J, Schmidig D, Mohammadzadeh M, et al.: Microcoil-based MRI: feasibility study and cell culture applications using a conventional animal system. MAGMA 2011, 24:137-45.
• [27]Eldracher M, Orth P, Cucchiarini M, Pape D, Madry H: Small subchondral drill holes improve marrow stimulation of articular cartilage defects. Am J Sports Med 2014, 42:2741-50.
• [28]Orth P, Cucchiarini M, Kaul G, Ong MF, Graber S, Kohn DM, et al.: Temporal and spatial migration pattern of the subchondral bone plate in a rabbit osteochondral defect model. Osteoarthritis Cartilage 2012, 20:1161-9.
• [29]Orth P, Goebel L, Wolfram U, Ong MF, Graber S, Kohn D, et al.: Effect of subchondral drilling on the microarchitecture of subchondral bone: analysis in a large animal model at 6 months. Am J Sports Med 2012, 40:828-36.
• [30]Frisbie DD, Morisset S, Ho CP, Rodkey WG, Steadman JR, McIlwraith CW: Effects of calcified cartilage on healing of chondral defects treated with microfracture in horses. Am J Sports Med 2006, 34:1824-31.
• [31]Frisbie DD, Oxford JT, Southwood L, Trotter GW, Rodkey WG, Steadman JR, et al. McIlwraith CW. Early events in cartilage repair after subchondral bone microfracture. Clin Orthop Relat Res 2003:215–27.
• [32]Abramoff MD, Magalhaes PJ, Ram SJ: Image processing with ImageJ. Biophotonics 2004, 11:36-42.
• [33]Hermann KG, Landewe RB, Braun J, van der Heijde DM: Magnetic resonance imaging of inflammatory lesions in the spine in ankylosing spondylitis clinical trials: is paramagnetic contrast medium necessary? J Rheumatol 2005, 32:2056-60.
• [34]van der Made AD, Maas M, Beenen LF, Oostra RJ, Kerkhoffs GM: Postmortem imaging exposed: an aid in MR imaging of musculoskeletal structures. Skeletal Radiol 2012, 42:467-72.
• [35]While PT, Forbes LK, Crozier S: Designing gradient coils with reduced hot spot temperatures. J Magn Reson 2010, 203:91-9.
• [36]Deistung A, Rauscher A, Sedlacik J, Stadler J, Witoszynskyj S, Reichenbach JR: Susceptibility weighted imaging at ultra high magnetic field strengths: theoretical considerations and experimental results. Magn Reson Med 2008, 60:1155-68.
• [37]Lammentausta E, Kiviranta P, Nissi MJ, Laasanen MS, Kiviranta I, Nieminen MT, et al.: T2 relaxation time and delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) of human patellar cartilage at 1.5 T and 9.4 T: Relationships with tissue mechanical properties. J Orthop Res 2006, 24:366-74.
• [38]Maramraju SH, Smith SD, Junnarkar SS, Schulz D, Stoll S, Ravindranath B, et al.: Small animal simultaneous PET/MRI: initial experiences in a 9.4 T microMRI. Phys Med Biol 2011, 56:2459-80.
• [39]Zbyn S, Stelzeneder D, Welsch GH, Negrin LL, Juras V, Mayerhoefer ME, et al.: Evaluation of native hyaline cartilage and repair tissue after two cartilage repair surgery techniques with 23Na MR imaging at 7 T: initial experience. Osteoarthritis Cartilage 2012, 20:837-45.
• [40]Fenty MC, Dodge GR, Kassey VB, Witschey WR, Borthakur A, Reddy R: Quantitative cartilage degeneration associated with spontaneous osteoarthritis in a guinea pig model. J Magn Reson Imaging 2012, 35:891-8.
• [41]Kangarlu A, Gahunia HK: Magnetic resonance imaging characterization of osteochondral defect repair in a goat model at 8 T. Osteoarthritis Cartilage 2006, 14:52-62.
• [42]Kraff O, Theysohn JM, Maderwald S, Saylor C, Ladd SC, Ladd ME, et al.: MRI of the knee at 7.0 Tesla. Rofo 2007, 179:1231-5.
• [43]Ramaswamy S, Gurkan I, Sharma B, Cascio B, Fishbein KW, Spencer RG: Assessment of tissue repair in full thickness chondral defects in the rabbit using magnetic resonance imaging transverse relaxation measurements. J Biomed Mater Res B Appl Biomater 2008, 86:375-80.
• [44]Orth P, Zurakowski D, Wincheringer D, Madry H: Reliability, reproducibility, and validation of five major histological scoring systems for experimental articular cartilage repair in the rabbit model. Tissue Eng Part C Methods 2012, 18:329-39.
• [45]Roemer FW, Frobell R, Hunter DJ, Crema MD, Fischer W, Bohndorf K, et al.: MRI-detected subchondral bone marrow signal alterations of the knee joint: terminology, imaging appearance, relevance and radiological differential diagnosis. Osteoarthritis Cartilage 2009, 17:1115-31.
• [46]Xu L1, Hayashi D, Roemer FW, Felson DT, Guermazi A: Magnetic resonance imaging of subchondral bone marrow lesions in association with osteoarthritis. Semin Arthritis Rheum 2012, 42:105-18.
• [47]Anagnostakos K, Orth P: Role of serum lipoprotein at the site of iloprost therapy in the treatment of painful bone marrow edema. Orthopedics 2013, 36:e1283-9.
• [48]Zscharnack M, Hepp P, Richter R, Aigner T, Schulz R, Somerson J, et al.: Repair of chronic osteochondral defects using predifferentiated mesenchymal stem cells in an ovine model. Am J Sports Med 2010, 38:1857-69.