Advanced Morphological and Biochemical Magnetic Resonance Imaging of Cartilage Repair Procedures in the Knee Joint at 3 Tesla

ABSTRACT

Morphological and biochemical magnetic resonance imaging (MRI) is due to high field MR systems, advanced coil technology, and sophisticated sequence protocols capable of visualizing articular cartilage in vivo with high resolution in clinical applicable scan time. Several conventional two-dimensional (2D) and three-dimensional (3D) approaches show changes in cartilage structure. Furthermore newer isotropic 3D sequences show great promise in improving cartilage imaging and additionally in diagnosing surrounding pathologies within the knee joint. Functional MR approaches are additionally able to provide a specific measure of the composition of cartilage. Cartilage physiology and ultra-structure can be determined, changes in cartilage macromolecules can be detected, and cartilage repair tissue can thus be assessed and potentially differentiated. In cartilage defects and following nonsurgical and surgical cartilage repair, morphological MRI provides the basis for diagnosis and follow-up evaluation, whereas biochemical MRI provides a deeper insight into the composition of cartilage and cartilage repair tissue. A combination of both, together with clinical evaluation, may represent a desirable multimodal approach in the future, also available in routine clinical use.

KEYWORDS

MRI - cartilage repair - dGEMRIC - T2 - 3 Tesla

REFERENCES

• 1 Widuchowski W, Widuchowski J, Trzaska T. Articular cartilage defects: study of 25,124 knee arthroscopies.  Knee. 2007;  14(3) 177-182
• 2 Ding C, Garnero P, Cicuttini F et al.. Knee cartilage defects: association with early radiographic osteoarthritis, decreased cartilage volume, increased joint surface area and type II collagen breakdown.  Osteoarthritis Cartilage. 2005;  13(3) 198-205
• 3 Peyron J G. Epidemiological aspects of osteoarthritis.  Scand J Rheumatol Suppl. 1988;  77 29-33
• 4 Reginster J Y. The prevalence and burden of arthritis.  Rheumatology (Oxford). 2002;  41(Supp 1) 3-6
• 5 Zhang W, Doherty M. EULAR recommendations for knee and hip osteoarthritis: a critique of the methodology.  Br J Sports Med. 2006;  40(8) 664-669
• 6 Bartlett W, Skinner J A, Gooding C R et al.. Autologous chondrocyte implantation versus matrix-induced autologous chondrocyte implantation for osteochondral defects of the knee: a prospective, randomised study.  J Bone Joint Surg Br. 2005;  87(5) 640-645
• 7 Behrens P, Bitter T, Kurz B, Russlies M. Matrix-associated autologous chondrocyte transplantation/implantation (MACT/MACI)—5-year follow-up.  Knee. 2006;  13(3) 194-202
• 8 Gudas R, Kalesinskas R J, Kimtys V et al.. A prospective randomized clinical study of mosaic osteochondral autologous transplantation versus microfracture for the treatment of osteochondral defects in the knee joint in young athletes.  Arthroscopy. 2005;  21(9) 1066-1075
• 9 Gudas R, Stankevicius E, Monastyreckiene E, Pranys D, Kalesinskas R J. Osteochondral autologous transplantation versus microfracture for the treatment of articular cartilage defects in the knee joint in athletes.  Knee Surg Sports Traumatol Arthrosc. 2006;  14(9) 834-842
• 10 Knutsen G, Drogset J O, Engebretsen L et al.. A randomized trial comparing autologous chondrocyte implantation with microfracture. Findings at five years.  J Bone Joint Surg Am. 2007;  89(10) 2105-2112
• 11 Knutsen G, Engebretsen L, Ludvigsen T C et al.. Autologous chondrocyte implantation compared with microfracture in the knee. A randomized trial.  J Bone Joint Surg Am. 2004;  86-A(3) 455-464
• 12 Eckstein F, Ateshian G, Burgkart R et al.. Proposal for a nomenclature for magnetic resonance imaging based measures of articular cartilage in osteoarthritis.  Osteoarthritis Cartilage. 2006;  14(10) 974-983
• 13 Gold G E, Burstein D, Dardzinski B et al.. MRI of articular cartilage in OA: novel pulse sequences and compositional/functional markers.  Osteoarthritis Cartilage. 2006;  14 Suppl A A76-86
• 14 Recht M, White L M, Winalski C S et al.. MR imaging of cartilage repair procedures.  Skeletal Radiol. 2003;  32(4) 185-200
• 15 Recht M P, Goodwin D W, Winalski C S, White L M. MRI of articular cartilage: revisiting current status and future directions.  AJR Am J Roentgenol. 2005;  185(4) 899-914
• 16 Trattnig S, Millington S A, Szomolanyi P, Marlovits S. MR imaging of osteochondral grafts and autologous chondrocyte implantation.  Eur Radiol. 2007;  17(1) 103-118
• 17 Van Breuseghem I. Ultrastructural MR imaging techniques of the knee articular cartilage: problems for routine clinical application.  Eur Radiol. 2004;  14(2) 184-192
• 18 Mamisch T C, Menzel M I, Welsch G H et al.. Steady-state diffusion imaging for MR in-vivo evaluation of reparative cartilage after matrix-associated autologous chondrocyte transplantation at 3 Tesla—preliminary results.  Eur J Radiol. 2008;  65(1) 72-79
• 19 Trattnig S, Mamisch T C, Pinker K et al.. Differentiating normal hyaline cartilage from post-surgical repair tissue using fast gradient echo imaging in delayed gadolinium-enhanced MRI (dGEMRIC) at 3 Tesla.  Eur Radiol. 2008;  18 1251-1259
• 20 Trattnig S, Mamisch T C, Welsch G H et al.. Quantitative T2 mapping of matrix-associated autologous chondrocyte transplantation at 3 Tesla: an in vivo cross-sectional study.  Invest Radiol. 2007;  42(6) 442-448
• 21 Watanabe A, Wada Y, Obata T et al.. Delayed gadolinium-enhanced MR to determine glycosaminoglycan concentration in reparative cartilage after autologous chondrocyte implantation: preliminary results.  Radiology. 2006;  239(1) 201-208
• 22 Zuo J, Li X, Banerjee S, Han E, Majumdar S. Parallel imaging of knee cartilage at 3 Tesla.  J Magn Reson Imaging. 2007;  26(4) 1001-1009
• 23 Ramnath R R. 3T MR imaging of the musculoskeletal system (Part I): considerations, coils, and challenges.  Magn Reson Imaging Clin N Am. 2006;  14(1) 27-40
• 24 Buckwalter J A, Mankin H J. Articular cartilage: degeneration and osteoarthritis, repair, regeneration, and transplantation.  Instr Course Lect. 1998;  47 487-504
• 25 Poole A R, Kojima T, Yasuda T et al.. Composition and structure of articular cartilage: a template for tissue repair.  Clin Orthop Relat Res. 2001;  (391, Suppl) S26-S33
• 26 Goodwin D W, Zhu H, Dunn J F. In vitro MR imaging of hyaline cartilage: correlation with scanning electron microscopy.  AJR Am J Roentgenol. 2000;  174(2) 405-409
• 27 Clar C, Cummins E, McIntyre L et al.. Clinical and cost-effectiveness of autologous chondrocyte implantation for cartilage defects in knee joints: systematic review and economic evaluation.  Health Technol Assess. 2005;  9(47) iii-iv ix-x 1-82
• 28 Smith G D, Knutsen G, Richardson J B. A clinical review of cartilage repair techniques.  J Bone Joint Surg Br. 2005;  87(4) 445-449
• 29 Steadman J R, Rodkey W G, Rodrigo J J. Microfracture: surgical technique and rehabilitation to treat chondral defects.  Clin Orthop Relat Res. 2001;  (391, Suppl) S362-S369
• 30 Mithoefer K, Williams III R J, Warren R F 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;  87(9) 1911-1920
• 31 Ueblacker P, Burkart A, Imhoff A B. Retrograde cartilage transplantation on the proximal and distal tibia.  Arthroscopy. 2004;  20(1) 73-78
• 32 Hangody L, Rathonyi G K, Duska Z et al.. Autologous osteochondral mosaicplasty. Surgical technique.  J Bone Joint Surg Am. 2004;  86-A(Suppl 1) 65-72
• 33 Brittberg M, Lindahl A, Nilsson A et al.. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation.  N Engl J Med. 1994;  331(14) 889-895
• 34 Minas T, Chiu R. Autologous chondrocyte implantation.  Am J Knee Surg. 2000;  13(1) 41-50
• 35 Marlovits S, Zeller P, Singer P, Resinger C, Vecsei V. Cartilage repair: generations of autologous chondrocyte transplantation.  Eur J Radiol. 2006;  57(1) 24-31
• 36 Bentley G, Biant L C, Carrington R W et al.. A prospective, randomised comparison of autologous chondrocyte implantation versus mosaicplasty for osteochondral defects in the knee.  J Bone Joint Surg Br. 2003;  85(2) 223-230
• 37 Horas U, Pelinkovic D, Herr G, Aigner T, Schnettler R. Autologous chondrocyte implantation and osteochondral cylinder transplantation in cartilage repair of the knee joint. A prospective, comparative trial.  J Bone Joint Surg Am. 2003;  85-A(2) 185-192
• 38 Henderson I J, Tuy B, Connell D, Oakes B, Hettwer W H. Prospective clinical study of autologous chondrocyte implantation and correlation with MRI at three and 12 months.  J Bone Joint Surg Br. 2003;  85(7) 1060-1066
• 39 Peterson L, Brittberg M, Kiviranta I, Akerlund E L, Lindahl A. Autologous chondrocyte transplantation. Biomechanics and long-term durability.  Am J Sports Med. 2002;  30(1) 2-12
• 40 Zheng M H, Willers C, Kirilak L et al.. Matrix-induced autologous chondrocyte implantation (MACI): biological and histological assessment.  Tissue Eng. 2007;  13(4) 737-746
• 41 Recht M, Bobic V, Burstein D et al.. Magnetic resonance imaging of articular cartilage.  Clin Orthop Relat Res. 2001;  (391, Suppl) S379-S396
• 42 Disler D G, McCauley T R, Kelman C G et al.. Fat-suppressed three-dimensional spoiled gradient-echo MR imaging of hyaline cartilage defects in the knee: comparison with standard MR imaging and arthroscopy.  AJR Am J Roentgenol. 1996;  167(1) 127-132
• 43 Peterfy C G, van Dijke C F, Lu Y et al.. Quantification of the volume of articular cartilage in the metacarpophalangeal joints of the hand: accuracy and precision of three-dimensional MR imaging.  AJR Am J Roentgenol. 1995;  165(2) 371-375
• 44 Potter H G, Linklater J M, Allen A A, Hannafin J A, Haas S B. Magnetic resonance imaging of articular cartilage in the knee. An evaluation with use of fast-spin-echo imaging.  J Bone Joint Surg Am. 1998;  80(9) 1276-1284
• 45 Trattnig S, Huber M, Breitenseher M J et al.. Imaging articular cartilage defects with 3D fat-suppressed echo planar imaging: comparison with conventional 3D fat-suppressed gradient echo sequence and correlation with histology.  J Comput Assist Tomogr. 1998;  22(1) 8-14
• 46 Kramer J, Recht M P, Imhof H, Stiglbauer R, Engel A. Postcontrast MR arthrography in assessment of cartilage lesions.  J Comput Assist Tomogr. 1994;  18(2) 218-224
• 47 Marlovits S, Singer P, Zeller P et al.. Magnetic resonance observation of cartilage repair tissue (MOCART) for the evaluation of autologous chondrocyte transplantation: determination of interobserver variability and correlation to clinical outcome after 2 years.  Eur J Radiol. 2006;  57(1) 16-23
• 48 Marlovits S, Striessnig G, Resinger C T et al.. Definition of pertinent parameters for the evaluation of articular cartilage repair tissue with high-resolution magnetic resonance imaging.  Eur J Radiol. 2004;  52(3) 310-319
• 49 Recht M P, Piraino D W, Paletta G A, Schils J P, Belhobek G H. Accuracy of fat-suppressed three-dimensional spoiled gradient-echo FLASH MR imaging in the detection of patellofemoral articular cartilage abnormalities.  Radiology. 1996;  198(1) 209-212
• 50 Eckstein F, Sittek H, Milz S et al.. The potential of magnetic resonance imaging (MRI) for quantifying articular cartilage thickness—a methodological study.  Clin Biomech (Bristol, Avon). 1995;  10(8) 434-440
• 51 Eckstein F, Winzheimer M, Westhoff J et al.. Quantitative relationships of normal cartilage volumes of the human knee joint—assessment by magnetic resonance imaging.  Anat Embryol (Berl). 1998;  197(5) 383-390
• 52 Gray M L, Eckstein F, Peterfy C et al.. Toward imaging biomarkers for osteoarthritis.  Clin Orthop Relat Res. 2004;  (427, Suppl) S175-S181
• 53 Eckstein F, Kunz M, Schutzer M et al.. Two year longitudinal change and test-retest-precision of knee cartilage morphology in a pilot study for the osteoarthritis initiative.  Osteoarthritis Cartilage. 2007;  15(11) 1326-1332
• 54 Eckstein F, Hudelmaier M, Wirth W et al.. Double echo steady state magnetic resonance imaging of knee articular cartilage at 3 Tesla: a pilot study for the Osteoarthritis Initiative.  Ann Rheum Dis. 2006;  65(4) 433-441
• 55 Weckbach S, Mendlik T, Horger W et al.. Quantitative assessment of patellar cartilage volume and thickness at 3.0 Tesla comparing a 3D-fast low angle shot versus a 3D-true fast imaging with steady-state precession sequence for reproducibility.  Invest Radiol. 2006;  41(2) 189-197
• 56 Kornaat P R, Reeder S B, Koo S et al.. MR imaging of articular cartilage at 1.5T and 3.0T: comparison of SPGR and SSFP sequences.  Osteoarthritis Cartilage. 2005;  13(4) 338-344
• 57 Duc S R, Koch P, Schmid M R et al.. Diagnosis of articular cartilage abnormalities of the knee: prospective clinical evaluation of a 3D water-excitation true FISP sequence.  Radiology. 2007;  243(2) 475-482
• 58 Duc S R, Pfirrmann C W, Koch P P, Zanetti M, Hodler J. Internal knee derangement assessed with 3-minute three-dimensional isovoxel true FISP MR sequence: preliminary study.  Radiology. 2008;  246(2) 526-535
• 59 Duc S R, Pfirrmann C W, Schmid M R et al.. Articular cartilage defects detected with 3D water-excitation true FISP: prospective comparison with sequences commonly used for knee imaging.  Radiology. 2007;  245(1) 216-223
• 60 Gold G E, Busse R F, Beehler C et al.. Isotropic MRI of the knee with 3D fast spin-echo extended echo-train acquisition (XETA): initial experience.  AJR Am J Roentgenol. 2007;  188(5) 1287-1293
• 61 Burstein D, Bashir A, Gray M L. MRI techniques in early stages of cartilage disease.  Invest Radiol. 2000;  35(10) 622-638
• 62 Bashir A, Gray M L, Boutin R D, Burstein D. Glycosaminoglycan in articular cartilage: in vivo assessment with delayed Gd(DTPA)(2-)-enhanced MR imaging.  Radiology. 1997;  205(2) 551-558
• 63 Tiderius C J, Olsson L E, Leander P, Ekberg O, Dahlberg L. Delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) in early knee osteoarthritis.  Magn Reson Med. 2003;  49(3) 488-492
• 64 Williams A, Gillis A, McKenzie C et al.. Glycosaminoglycan distribution in cartilage as determined by delayed gadolinium-enhanced MRI of cartilage (dGEMRIC): potential clinical applications.  AJR Am J Roentgenol. 2004;  182(1) 167-172
• 65 Trattnig S, Marlovits S, Gebetsroither S et al.. Three-dimensional delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) for in vivo evaluation of reparative cartilage after matrix-associated autologous chondrocyte transplantation at 3.0T: preliminary results.  J Magn Reson Imaging. 2007;  26(4) 974-982
• 66 Kim Y J, Jaramillo D, Millis M B, Gray M L, Burstein D. Assessment of early osteoarthritis in hip dysplasia with delayed gadolinium-enhanced magnetic resonance imaging of cartilage.  J Bone Joint Surg Am. 2003;  85-A(10) 1987-1992
• 67 Vaga S, Raimondi M T, Caiani E G et al.. Quantitative assessment of intervertebral disc glycosaminoglycan distribution by gadolinium-enhanced MRI in orthopedic patients.  Magn Reson Med. 2008;  59(1) 85-95
• 68 Williams A, Shetty S K, Burstein D, Day C S, McKenzie C. Delayed gadolinium enhanced MRI of cartilage (dGEMRIC) of the first carpometacarpal (1CMC) joint: a feasibility study.  Osteoarthritis Cartilage. 2008;  16(4) 530-532
• 69 Ling W, Regatte R R, Navon G, Jerschow A. Assessment of glycosaminoglycan concentration in vivo by chemical exchange-dependent saturation transfer (gagCEST).  Proc Natl Acad Sci USA. 2008;  105(7) 2266-2270
• 70 Mosher T J, Dardzinski B J. Cartilage MRI T2 relaxation time mapping: overview and applications.  Semin Musculoskelet Radiol. 2004;  8(4) 355-368
• 71 Goodwin D W, Wadghiri Y Z, Dunn J F. Micro-imaging of articular cartilage: T2, proton density, and the magic angle effect.  Acad Radiol. 1998;  5(11) 790-798
• 72 Smith H E, Mosher T J, Dardzinski B J et al.. Spatial variation in cartilage T2 of the knee.  J Magn Reson Imaging. 2001;  14(1) 50-55
• 73 Watrin-Pinzano A, Ruaud J P, Cheli Y et al.. Evaluation of cartilage repair tissue after biomaterial implantation in rat patella by using T2 mapping.  MAGMA. 2004;  17(3–6) 219-228
• 74 White L M, Sussman M S, 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) 407-414
• 75 Welsch G H, Mamisch T C, Domayer S E 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) 154-161
• 76 David-Vaudey E, Ghosh S, Ries M, Majumdar S. T2 relaxation time measurements in osteoarthritis.  Magn Reson Imaging. 2004;  22(5) 673-682
• 77 Dunn T C, Lu Y, Jin H, Ries M D, Majumdar S. T2 relaxation time of cartilage at MR imaging: comparison with severity of knee osteoarthritis.  Radiology. 2004;  232(2) 592-598
• 78 Burstein D, Gray M L. Is MRI fulfilling its promise for molecular imaging of cartilage in arthritis?.  Osteoarthritis Cartilage. 2006;  14(11) 1087-1090
• 79 Murphy B J. Evaluation of grades 3 and 4 chondromalacia of the knee using T2*-weighted 3D gradient-echo articular cartilage imaging.  Skeletal Radiol. 2001;  30(6) 305-311
• 80 Hughes T, Welsch G H, Trattnig S et al.. T2-star relaxation as a means to differentiate cartilage repair tissue after microfracturing therapy.  Intern Soc Magn Reson Med. 2007;  15 183
• 81 Wietek B, Martirosian P, Machann J et al.. T2 and T2* mapping of the human femoral-tibial cartilage at 1.5 and 3 Tesla.  Intern Soc Magn Reson Med. 2007;  15 516
• 82 Bauer J S, Banerjee S, Henning T D et al.. Fast high-spatial-resolution MRI of the ankle with parallel imaging using GRAPPA at 3 T.  AJR Am J Roentgenol. 2007;  189(1) 240-245
• 83 Mosher T J. Musculoskeletal imaging at 3T: current techniques and future applications.  Magn Reson Imaging Clin N Am. 2006;  14(1) 63-76
• 84 Rayan F, Bhonsle S, Shukla D D. Clinical, MRI, and arthroscopic correlation in meniscal and anterior cruciate ligament injuries.  Int Orthop. 2008;  , E-pub ahead of print
• 85 Thomas S, Pullagura M, Robinson E, Cohen A, Banaszkiewicz P. The value of magnetic resonance imaging in our current management of ACL and meniscal injuries.  Knee Surg Sports Traumatol Arthrosc. 2007;  15(5) 533-536
• 86 Gold G E, Han E, Stainsby J et al.. Musculoskeletal MRI at 3.0 T: relaxation times and image contrast.  AJR Am J Roentgenol. 2004;  183(2) 343-351
• 87 Pakin S K, Cavalcanti C, La Rocca R, Schweitzer M E, Regatte R R. Ultra-high-field MRI of knee joint at 7.0T: preliminary experience.  Acad Radiol. 2006;  13(9) 1135-1142
• 88 Stanisz G J, Odrobina E E, Pun J et al.. T1, T2 relaxation and magnetization transfer in tissue at 3T.  Magn Reson Med. 2005;  54(3) 507-512
• 89 Williams A, Mikulis B, Krishnan N et al.. Suitability of T(1Gd) as the dGEMRIC index at 1.5T and 3.0T.  Magn Reson Med. 2007;  58(4) 830-834
• 90 Dietrich O, Raya J G, Reeder S B, Reiser M F, Schoenberg S O. Measurement of signal-to-noise ratios in MR Images: influence of multichannel coils, parallel imaging, and reconstruction filters.  J Magn Reson Imaging. 2007;  26 375-385
• 91 Liess C, Lusse S, Karger N, Heller M, Gluer C C. Detection of changes in cartilage water content using MRI T2-mapping in vivo.  Osteoarthritis Cartilage. 2002;  10(12) 907-913
• 92 Domayer S E, Kutscha-Lissberg F, Welsch G et al.. T2 mapping in the knee after microfracture at 3.0T: correlation of global T2 values and clinical outcome—preliminary results.  Osteoarthritis Cartilage. 2008;  , E-pub ahead of publication