Conventional and ultrashort time-to-echo magnetic resonance imaging of articular cartilage, meniscus, and intervertebral disk

Topics in Magnetic Resonance Imaging

Volumn 21, Issue 5, 2010, Pages 275-289

  Bae, Won C ^a   Du, Jiang ^a   Bydder, Graeme M ^a   Chung, Christine B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Endplate; Joint; Knee; Osteoarthritis; Spine; Ultrashort time to echo magnetic resonance imaging

Indexed keywords

ARTICLE; ARTICULAR CARTILAGE; INTERVERTEBRAL DISK; KNEE MENISCUS; NUCLEAR MAGNETIC RESONANCE IMAGING; OSTEOARTHRITIS; PRIORITY JOURNAL;

CARTILAGE, ARTICULAR; HUMANS; IMAGE ENHANCEMENT; INTERVERTEBRAL DISC; JOINT DISEASES; JOINTS; MAGNETIC RESONANCE IMAGING; MENISCI, TIBIAL;

EID: 82555172132     PISSN: 08993459     EISSN: 15361004     Source Type: Journal    
DOI: 10.1097/RMR.0b013e31823ccebc     Document Type: Article

References (165)

1. Gold GE, Thedens DR, Pauly JM, et al. MR imaging of articular cartilage of the knee: new methods using ultrashort TEs. AJR Am J Roentgenol. 1998;170:1223Y1226.
2. Gatehouse PD, Thomas RW, Robson MD, et al. Magnetic resonance imaging of the knee with ultrashort TE pulse sequences. Magn Reson Imaging. 2004;22:1061Y1067.
3. Young IR, Bydder GM. Magnetic resonance: new approaches to imaging of the musculoskeletal system. Physiol Meas. 2003;24:R1Y23.
4. Robson MD, Gatehouse PD, Bydder M, et al. Magnetic resonance: an introduction to ultrashort TE (UTE) imaging. J Comput Assist Tomogr. 2003;27:825Y846.
5. Gatehouse PD, Bydder GM. Magnetic resonance imaging of short T2 components in tissue. Clin Radiol. 2003;58:1Y19.
6. Du J, Bydder M, Takahashi AM, et al. Two-dimensional ultrashort echo time imaging using a spiral trajectory. Magn Reson Imaging. 2008;26:304Y312.
7. Qian Y, Boada FE. Acquisition-weighted stack of spirals for fast high-resolution three-dimensional ultra-short echo time MR imaging. Magn Reson Med. 2008;60:135Y145.
8. Idiyatullin D, Corum C, Park JY, et al. Fast and quiet MRI using a swept radiofrequency. J Magn Reson. 2006;181:342Y349.
9. Du J, Bydder M, Takahashi AM, et al. Short T2 contrast with three-dimensional ultrashort echo time imaging. Magn Reson Imaging. 2011;29:470Y482.
10. Rahmer J, Börnert P, Groen J, et al. Three-dimensional radial ultrashort echo-time imaging with T2 adapted sampling. Magn Reson Imaging. 2006;55:1075Y1082.
11. Lu A, Daniel BL, Pauly JM, et al. Improved slice selection for R2* mapping during cryoablation with eddy current compensation. J Magn Reson Imaging. 2008;28:190Y198.
12. Wu Y, Ackerman JL, Chesler DA, et al. Density of organic matrix of native mineralized bone measured by water- and fat-suppressed proton projection MRI. Magn Reson Imaging. 2003;50:59Y68.
13. Techawiboonwong A, Song HK, Wehrli FW. In vivo MRI of submillisecond T(2) species with two-dimensional and three-dimensional radial sequences and applications to the measurement of cortical bone water. NMR Biomed. 2008;21:59Y70.
14. Sussman MS, Pauly JM, Wright GA. Design of practical T2-selective RF excitation (TELEX) pulses. Magn Reson Imaging. 1998;40:890Y899.
15. Du J, Takahashi AM, Bae WC, et al. Dual inversion recovery, ultrashort echo time (DIR UTE) imaging: creating high contrast for short-T(2) species. Magn Reson Imaging. 2010;63:447Y455.
16. Du J, Takahashi AM, Chung CB. Ultrashort TE spectroscopic imaging (UTESI): application to the imaging of short T2 relaxation tissues in the musculoskeletal system. J Magn Reson Imaging. 2009;29:412Y421.
17. Du J, Carl M, Diaz E, et al. Ultrashort TE T1rho (UTE T1Q) imaging of the Achilles tendon and meniscus. Magn Reson Med. 2010;64:834Y842.
18. Du J, Pauli C, Diaz E, et al. Free and bound water evaluation of articular cartilage. Proc Intl Soc Magn Reson Med. 2011;19:565.
19. Mow VC, Zhu W, Ratcliffe A. Structure and function of articular cartilage and meniscus. In: Mow VC, Hayes WC, eds. Basic Orthopaedic Biomechanics. New York, NY: Raven Press; 1991:143Y198.
20. Maroudas A. Physico-chemical properties of articular cartilage. In: Freeman MAR, ed. Adult Articular Cartilage. 2nd ed. TunbridgeWells, England: Pitman Medical; 1979:215Y290.
21. Buschmann MD, Grodzinsky AJ. A molecular model of proteoglycan-associated electrostatic forces in cartilage mechanics. J Biomech Eng. 1995;117:179Y192.
22. Lane LB, Bullough PG. Age-related changes in the thickness of the calcified zone and the number of tidemarks in adult human articular cartilage. J Bone Joint Surg Br. 1980;62:372Y375.
23. Green WT Jr, Martin GN, Eanes ED, et al. Microradiographic study of the calcified layer of articular cartilage. Arch Pathol. 1970;90:151Y158.
24. Lyons TJ, Stoddart RW, McClure SF, et al. The tidemark of the chondro-osseous junction of the normal human knee joint. J Mol Histol. 2005;36:207Y215.
25. Aspden RM, Hukins DWL. Collagen organization in articular cartilage, determined by x-ray diffraction, and its relationship to tissue function. Proc R Soc Lond B. 1981;212:299Y304.
26. Broom ND. The collagen framework of articular cartilage: its profound influence on normal and abnormal load-bearing function. In: Nimni ME, ed. Collagen: Chemistry, Biology, and Biotechnology. Vol II. Boca Raton, FL: CRC Press, Inc; 1988:243Y265.
27. Lane JM, Weiss C. Review of articular cartilage collagen research. Arthritis Rheum. 1975;18:553Y562.
28. Muir H, Bullough P, Maroudas A. The distribution of collagen in human articular cartilage with some of its physiological implications. J Bone Joint Surg Br. 1970;52:554Y563.
29. Erickson SJ, Prost RW, Timins ME. The "magic angle" effect: background physics and clinical relevance. Radiology. 1993;188:23Y25.
30. Du J, Pak BC, Znamirowski R, et al. Magic angle effect in magnetic resonance imaging of the Achilles tendon and enthesis. Magn Reson Imaging. 2009;27:557Y564.
31. Chen SS, Falcovitz YH, Schneiderman R, et al. Depth-dependent compressive properties of normal aged human femoral head articular cartilage: relationship to fixed charge density. Osteoarthritis Cartilage. 2001;9:561Y569.
32. Kempson GE. Age-related changes in the tensile properties of human articular cartilage: a comparative study between the femoral head of the hip joint and the talus of the ankle joint. Biochim Biophys Acta. 1991;1075:223Y230.
33. Bae WC, Wong VW, Hwang J, et al. Wear-lines and split-lines of human patellar cartilage: relation to tensile biomechanical properties. Osteoarthritis Cartilage. 2008;16:841Y845.
34. Kempson GE. Mechanical properties of articular cartilage and their relationship to matrix degradation and age. Ann Rheum Dis. 1975;34S2:111Y114.
35. Temple MM, Xue Y, Chen MQ, et al. Interleukin-1a induction of tensile weakening associated with collagen degradation in bovine articular cartilage. Arthritis Rheum. 2006;54:3267Y3276.
36. Boyde A, Riggs CM, Bushby AJ, et al. Cartilage damage involving extrusion of mineralisable matrix from the articular calcified cartilage and subchondral bone. Eur Cell Mater. 2011;21:470Y478.
37. Hwang J, Bae WC, Shieu W, et al. Increased hydraulic conductance of human articular cartilage and subchondral bone plate with progression of osteoarthritis. Arthritis Rheum. 2008;58:3831Y3842.
38. Burr DB. Anatomy and physiology of the mineralized tissues: role in the pathogenesis of osteoarthrosis. Osteoarthritis Cartilage. 2004;12:S20YS30.
39. Boyde A, Firth EC. High resolution microscopic survey of third metacarpal articular calcified cartilage and subchondral bone in the juvenile horse: possible implications in chondro-osseous disease. Microsc Res Tech. 2008;71:477Y488.
40. Chiang ER, Ma HL, Chen TH. Chondral delamination injury over tibial plateau mimicking a torn lateral discoid meniscus. Clin J Sport Med. 2010;20:120Y121.
41. Kendell SD, Helms CA, Rampton JW, et al. MRI appearance of chondral delamination injuries of the knee. AJR Am J Roentgenol. 2005;184:1486Y1489.
42. Levy AS, Lohnes J, Sculley S, et al. Chondral delamination of the knee in soccer players. Am J Sports Med. 1996;24:634Y639.
43. Altman RD. Criteria for classification of clinical osteoarthritis. J Rheumatol Suppl. 1991;27:10Y12.
44. Reginster JY, Deroisy R, Rovati LC, et al. Long-term effects of glucosamine sulphate on osteoarthritis progression: a randomised, placebo-controlled clinical trial. Lancet. 2001;357:251Y256.
45. Pavelka K, Gatterova J, Olejarova M, et al. Glucosamine sulfate use and delay of progression of knee osteoarthritis: a 3-year, randomized, placebo-controlled, double-blind study. Arch Intern Med. 2002;162:2113Y2123.
46. Brandt KD, Mazzuca SA, Katz BP, et al. Effects of doxycycline on progression of osteoarthritis: results of a randomized, placebo-controlled, double-blind trial. Arthritis Rheum. 2005;52:2015Y2025.
47. Kellgren JH, Lawrence JS. Radiological assessment of osteo-arthrosis. Ann Rheum Dis. 1957;16:494Y502.
48. Disler DG, McCauley TR, Wirth CR, et al. Detection of knee hyaline cartilage defects using fat-suppressed three-dimensional spoiled gradient-echo MR imaging: comparison with standard MR imaging and correlation with arthroscopy. AJR Am J Roentgenol. 1995;165:377Y382.
49. Hodler J, Resnick D. Current status of imaging of articular cartilage. Skeletal Radiol. 1996;25:703Y709.
50. Recht MP, Piraino DW, Paletta GA, et al. Accuracy of fat-suppressed three-dimensional spoiled gradient-echo FLASH MR imaging in the detection of patellofemoral articular cartilage abnormalities. Radiology. 1996;198:209Y212.
51. Taylor C, Carballido-Gamio J, Majumdar S, et al. Comparison of quantitative imaging of cartilage for osteoarthritis: T2, T1rho, dGEMRIC and contrast-enhanced computed tomography. Magn Reson Imaging. 2009;27:779Y784.
52. Alparslan L, Minas T, Winalski CS. Magnetic resonance imaging of autologous chondrocyte implantation. Semin Ultrasound CT MR. 2001;22:341Y351.
53. Potter HG, Foo LF. Magnetic resonance imaging of articular cartilage: trauma, degeneration, and repair. Am J Sports Med. 2006;34:661Y677.
54. Bredella MA, Tirman PF, Peterfy CG, et al. Accuracy of T2-weighted fast spin-echo MR imaging with fat saturation in detecting cartilage defects in the knee: comparison with arthroscopy in 130 patients. AJR Am J Roentgenol. 1999;172:1073Y1080.
55. Li X, Cheng J, Lin K, et al. Quantitative MRI using T1Q and T2 in human osteoarthritic cartilage specimens: correlation with biochemical measurements and histology. Magn Reson Imaging. 2011;29:324Y334.
56. Wheaton AJ, Dodge GR, Elliott DM, et al. Quantification of cartilage biomechanical and biochemical properties via T1rho magnetic resonance imaging. Magn Reson Med. 2005;54:1087Y1093.
57. Duvvuri U, Kudchodkar S, Reddy R, et al. T(1rho) relaxation can assess longitudinal proteoglycan loss from articular cartilage in vitro. Osteoarthritis Cartilage. 2002;10:838Y844.
58. Gillis A, Bashir A, McKeon B, et al. Magnetic resonance imaging of relative glycosaminoglycan distribution in patients with autologous chondrocyte transplants. Invest Radiol. 2001;36:743Y748.
59. Gray ML, Burstein D, Xia Y. Biochemical (and functional) imaging of articular cartilage. Semin Musculoskelet Radiol. 2001;5:329Y343.
60. Bae WC, Statum S, Biswas R, et al. Sensitivity of quantitative UTE MRI to degradation of human TMJ discs. Proc Intl Soc Magn Reson Med. 2011;19:569.
61. Samosky JT, Burstein D, Eric Grimson W, et al. Spatially-localized correlation of dGEMRIC-measured GAG distribution and mechanical stiffness in the human tibial plateau. J Orthop Res. 2005;23:93Y101.
62. Maroudas A. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature. 1976;260:808Y809.
63. Li X, Benjamin Ma C, Link TM, et al. In vivo T(1rho) and T(2) mapping of articular cartilage in osteoarthritis of the knee using 3 T MRI. Osteoarthritis Cartilage. 2007;15:789Y797.
64. Zarins ZA, Bolbos RI, Pialat JB, et al. Cartilage and meniscus assessment using T1rho and T2 measurements in healthy subjects and patients with osteoarthritis. Osteoarthritis Cartilage. 2010;18:1408Y1416.
65. Williams A, Sharma L, McKenzie CA, et al. Delayed gadolinium-enhanced magnetic resonance imaging of cartilage in knee osteoarthritis: findings at different radiographic stages of disease and relationship to malalignment. Arthritis Rheum. 2005;52:3528Y3535.
66. 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. 2010;18:1545Y1550.
67. Domayer SE, Welsch GH, Nehrer S, et al. T2 mapping and dGEMRIC after autologous chondrocyte implantation with a fibrin-based scaffold in the knee: preliminary results. Eur J Radiol. 2010;73:636Y642.
68. 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 proceduresVinitial experience. Radiology. 2008;247:154Y161.
69. Mamisch TC, Trattnig S, Quirbach S, et al. Quantitative T2 mapping of knee cartilage: differentiation of healthy control cartilage and cartilage repair tissue in the knee with unloadingVinitial results. Radiology. 2010;254:818Y826.
70. Kim M, Foo LF, Uggen C, et al. Evaluation of early osteochondral defect repair in a rabbit model utilizing Fourier transform-infrared imaging spectroscopy, magnetic resonance imaging, and quantitative T2 mapping. Tissue Eng Part C Methods. 2010;16:355Y364.
71. Miese FR, Zilkens C, Holstein A, et al. Assessment of early cartilage degeneration after slipped capital femoral epiphysis using T2 and T2* mapping. Acta Radiol. 2011;52:106Y110.
72. Kim Y-J, Jaramillo D, Millis MB, et al. Assessment of early osteoarthritis in hip dysplasia with delayed gadolinium-enhanced magnetic resonance imaging of cartilage. J Bone Joint Surg Am. 2003;85-A:1987Y1992.
73. Mamisch TC, Kain MSH, Bittersohl B, et al. Delayed gadolinium-enhanced magnetic resonance imaging of cartilage (dGEMRIC) in femoacetabular impingement. J Orthop Res. 2011;29:1305Y1311.
74. Sur S, Mamisch TC, Hughes T, et al. High resolution fast T1 mapping technique for dGEMRIC. J Magn Reson Imaging. 2009;30:896Y900.
75. Gatehouse PD, He T, Puri BK, et al. Contrast-enhanced MRI of the menisci of the knee using ultrashort echo time (UTE) pulse sequences: imaging of the red and white zones. Br J Radiol. 2004;77:641Y647.
76. Bae WC, Dwek JR, Znamirowski R, et al. Ultrashort echo time MR imaging of osteochondral junction of the knee at 3 T: identification of anatomic structures contributing to signal intensity. Radiology. 2010;254:837Y845.
77. Nyman JS, Ni Q, Nicolella DP, et al. Measurements of mobile and bound water by nuclear magnetic resonance correlate with mechanical properties of bone. Bone. 2008;42:193Y199.
78. Horch RA, Nyman JS, Gochberg DF, et al. Characterization of 1H NMR signal in human cortical bone for magnetic resonance imaging. Magn Reson Med. 2010;64:680Y687.
79. Reiter DA, Lin P-C, Fishbein KW, et al. Multicomponent T2 relaxation analysis in cartilage. Magn Reson Med. 2009;61:803Y809.
80. Qian Y, Williams AA, Chu CR, et al. Multicomponent T2* mapping of knee cartilage: technical feasibility ex vivo. Magn Reson Med. 2010;64:1426Y1431.
81. Williams A, Qian Y, Bear D, et al. Assessing degeneration of human articular cartilage with ultra-short echo time (UTE) T2* mapping. Osteoarthritis Cartilage. 2010;18:539Y546.
82. Reiter DA, Roque RA, Lin P-C, et al. Mapping proteoglycan-bound water in cartilage: Improved specificity of matrix assessment using multiexponential transverse relaxation analysis. Magn Reson Med. 2011;65:377Y384.
83. Aspden RM, Yarker YE, Hukins DW. Collagen orientations in the meniscus of the knee joint. J Anat. 1985;140:371Y380.
84. Bullough PG, Munuera L, Murphy J, et al. The strength of the menisci of the knee as it relates to their fine structure. J Bone Joint Surg Br. 1970;52:564Y567.
85. Skaggs DL, Warden WH, Mow VC. Radial tie fibers influence the tensile properties of the bovine medial meniscus. J Orthop Res. 1994;12:176Y185.
86. Petersen W, Tillmann B. Collagenous fibril texture of the human knee joint menisci. Anat Embryol (Berl). 1998;197:317Y324.
87. Kambic HE, McDevitt CA. Spatial organization of types I and II collagen in the canine meniscus. J Orthop Res. 2005;23:142Y149.
88. McDevitt CA, Webber RJ. The ultrastructure and biochemistry of meniscal cartilage. Clin Orthop Relat Res. 1990:8Y18.
89. Arnoczky SP, Warren RF. Microvasculature of the human meniscus. Am J Sports Med. 1982;10:90Y95.
90. Kean DM, Worthington BS, Preston BJ, et al. Nuclear magnetic resonance imaging of the knee: examples of normal anatomy and pathology. Br J Radiol. 1983;56:355Y364.
91. Berquist TH. Magnetic resonance imaging: preliminary experience in orthopedic radiology. Magn Reson Imaging. 1984;2:41Y52.
92. Li KC, Henkelman RM, Poon PY, et al. MR imaging of the normal knee. J Comput Assist Tomogr. 1984;8:1147Y1154.
93. Crues JV 3rd, Mink J, Levy TL, et al. Meniscal tears of the knee: accuracy of MR imaging. Radiology. 1987;164:445Y448.
94. Stoller DW, Martin C, Crues JV 3rd, et al. Meniscal tears: pathologic correlation with MR imaging. Radiology. 1987;163:731Y735.
95. Hajek PC, Gylys-Morin VM, Baker LL, et al. The high signal intensity meniscus of the knee. Magnetic resonance evaluation and in vivo correlation. Invest Radiol. 1987;22:883Y890.
96. Hodler J, Haghighi P, Pathria MN, et al. Meniscal changes in the elderly: correlation of MR imaging and histologic findings. Radiology. 1992;184:221Y225.
97. Blackmon GB, Major NM, Helms CA. Comparison of fast spin-echo versus conventional spin-echo MRI for evaluating meniscal tears. AJR Am J Roentgenol. 2005;184:1740Y1743.
98. Tarhan NC, Chung CB, Mohana-Borges AV, et al. Meniscal tears: role of axial MRI alone and in combination with other imaging planes. AJR Am J Roentgenol. 2004;183:9Y15.
99. Kijowski R, Davis KW, Woods MA, et al. Knee joint: comprehensive assessment with 3D isotropic resolution fast spin-echo MR imagingVdiagnostic performance compared with that of conventional MR imaging at 3.0 T. Radiology. 2009;252:486Y495.
100. Eckstein F, Cicuttini F, Raynauld JP, et al. Magnetic resonance imaging (MRI) of articular cartilage in knee osteoarthritis (OA): morphological assessment. Osteoarthritis Cartilage. 2006;14:A46YA75.
101. Potter HG, Black BR, Chong le R. New techniques in articular cartilage imaging. Clin Sports Med. 2009;28:77Y94.
102. Bolbos RI, Link TM, Ma CB, et al. T1rho relaxation time of the meniscus and its relationship with T1rho of adjacent cartilage in knees with acute ACL injuries at 3 T. Osteoarthritis Cartilage. 2009;17:12Y18.
103. Englund M, Guermazi A, Gale D, et al. Incidental meniscal findings on knee MRI in middle-aged and elderly persons. N Engl J Med. 2008;359:1108Y1115.
104. Liess C, Lusse S, Karger N, et al. Detection of changes in cartilage water content using MRI T2-mapping in vivo. Osteoarthritis Cartilage. 2002;10:907Y913.
105. Duvvuri U, Reddy R, Patel SD, et al. T1rho-relaxation in articular cartilage: effects of enzymatic degradation. Magn Reson Med. 1997;38:863Y867.
106. Regatte RR, Akella SV, Wheaton AJ, et al. T1rho-relaxation mapping of human femoral-tibial cartilage in vivo. J Magn Reson Imaging. 2003;18:336Y341.
107. Abreu M, Johnson K, Chung CB, et al. Calcification in calcium pyrophosphate dihydrate (CPPD) crystalline deposits in the knee: anatomic, radiographic, MR imaging, and histologic study in cadavers. Skeletal Radiol. 2004;33:392Y398.
108. Beltran J, Marty-Delfaut E, Bencardino J, et al. Chondrocalcinosis of the hyaline cartilage of the knee: MRI manifestations. Skeletal Radiol. 1998;27:369Y374.
109. Li X, Han ET, Busse RF, et al. In vivo T(1rho) mapping in cartilage using 3D magnetization-prepared angle-modulated partitioned k-space spoiled gradient echo snapshots (3D MAPSS). Magn Reson Med. 2008;59:298Y307.
110. Bogduk N, Endres SM. Clinical Anatomy of the Lumbar Spine and Sacrum. New York, NY: Elsevier/Churchill Livingstone; 2005.
111. Marchand F, Ahmed AM. Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine (Phila Pa 1976). 1990;15:402Y410.
112. Cassidy JJ, Hiltner A, Baer E. Hierarchical structure of the intervertebral disc. Connect Tissue Res. 1989;23:75Y88.
113. Veres SP, Robertson PA, Broom ND. The morphology of acute disc herniation: a clinically relevant model defining the role of flexion. Spine (Phila Pa 1976). 2009;34:2288Y2296.
114. Buckwalter JA. Aging and degeneration of the human intervertebral disc. Spine. 1995;20:1307Y1314.
115. Oegema TR Jr. Biochemistry of the intervertebral disc. Clin Sports Med. 1993;12:419Y439.
116. Roughley PJ. Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix. Spine. 2004;29:2691Y2699.
117. Setton LA, Zhu W, Weidenbaum M, et al. Compressive properties of the cartilaginous end-plate of the baboon lumbar spine. J Orthop Res. 1993;11:228Y239.
118. Roberts S, Menage J, Urban JP. Biochemical and structural properties of the cartilage end-plate and its relation to the intervertebral disc. Spine. 1989;14:166Y174.
119. Accadbled F, Laffosse JM, Ambard D, et al. Influence of location, fluid flow direction, and tissue maturity on the macroscopic permeability of vertebral end plates. Spine (Phila Pa 1976). 2008;33:612Y619.
120. Crock HV, Goldwasser M. Anatomic studies of the circulation in the region of the vertebral end-plate in adult greyhound dogs. Spine. 1984;9:702Y706.
121. Brodin H. Paths of nutrition in articular cartilage and intervertebral discs. Acta Orthop Scand. 1955;24:177Y183.
122. Urban JP, Holm S, Maroudas A. Diffusion of small solutes into the intervertebral disc: as in vivo study. Biorheology. 1978;15:203Y221.
123. Urban JP, Holm S, Maroudas A, et al. Nutrition of the intervertebral disc: effect of fluid flow on solute transport. Clin Orthop Rel Res. 1982;170:296Y306.
124. Maroudas A, Stockwell RA, Nachemson A, et al. Factors involved in the nutrition of the human lumbar intervertebral disc: cellularity and diffusion of glucose in vitro. J Anat. 1975;120:113Y130.
125. Roberts S, Menage J, Eisenstein SM. The cartilage end-plate and intervertebral disc in scoliosis: calcification and other sequelae. J Orthop Res. 1993;11:747Y757.
126. Urban MR, Fairbank JC, Etherington PJ, et al. Electrochemical measurement of transport into scoliotic intervertebral discs in vivo using nitrous oxide as a tracer. Spine. 2001;26:984Y990.
127. Andersson GB. Epidemiological features of chronic low-back pain. Lancet. 1999;354:581Y585.
128. An HS, Anderson PA, Haughton VM, et al. Introduction: disc degeneration: summary. Spine. 2004;29:2677Y2678.
129. Kawakami M, Tamaki T, Hayashi N, et al. Possible mechanism of painful radiculopathy in lumbar disc herniation. Clin Orthop Relat Res. 1998:241Y251.
130. Moneta GB, Videman T, Kaivanto K, et al. Reported pain during lumbar discography as a function of anular ruptures and disc degeneration. A re-analysis of 833 discograms. Spine (Phila Pa 1976). 1994;19:1968Y1974.
131. Vanharanta H, Sachs BL, Spivey MA, et al. The relationship of pain provocation to lumbar disc deterioration as seen by CT/discography. Spine (Phila Pa 1976). 1987;12:295Y298.
132. Powell MC, Wilson M, Szypryt P, et al. Prevalence of lumbar disc degeneration observed by magnetic resonance in symptomless women. Lancet. 1986;2:1366Y1367.
133. Boden SD, Davis DO, Dina TS, et al. Abnormal magnetic-resonance scans of the lumbar spine in asymptomatic subjects. A prospective investigation. J Bone Joint Surg Am. 1990;72:403Y408.
134. Bernick S, Cailliet R. Vertebral end-plate changes with aging of human vertebrae. Spine (Phila Pa 1976). 1982;7:97Y102.
135. Nachemson A, Lewin T, Maroudas A, et al. In vitro diffusion of dye through the end-plates and the annulus fibrosus of human lumbar inter-vertebral discs. Acta Orthop Scand. 1970;41:589Y607.
136. Aigner T, Gresk-otter KR, Fairbank JC, et al. Variation with age in the pattern of type X collagen expression in normal and scoliotic human intervertebral discs. Calcif Tissue Int. 1998;63:263Y268.
137. van der Werf M, Lezuo P, Maissen O, et al. Inhibition of vertebral endplate perfusion results in decreased intervertebral disc intranuclear diffusive transport. J Anat. 2007;211:769Y774.
138. Forristall RM, Marsh HO, Pay NT. Magnetic resonance imaging and contrast CTof the lumbar spine. Comparison of diagnostic methods and correlation with surgical findings. Spine (Phila Pa 1976). 1988;13:1049Y1054.
139. Hashimoto K, Akahori O, Kitano K, et al. Magnetic resonance imaging of lumbar disc herniation. Comparison with myelography. Spine (Phila Pa 1976). 1990;15:1166Y1169.
140. Pearce RH, Thompson JP, Bebault GM, et al. Magnetic resonance imaging reflects the chemical changes of aging degeneration in the human intervertebral disk. J Rheumatol Suppl. 1991;27:42Y43.
141. Pfirrmann CW, Metzdorf A, Zanetti M, et al. Magnetic resonance classification of lumbar intervertebral disc degeneration. Spine. 2001;26:1873Y1878.
142. Masuda K, Imai Y, Okuma M, et al. Osteogenic protein-1 injection into a degenerated disc induces the restoration of disc height and structural changes in the rabbit anular puncture model. Spine. 2006;31:742Y754.
143. Lee S, Moon CS, Sul D, et al. Comparison of growth factor and cytokine expression in patients with degenerated disc disease and herniated nucleus pulposus. Clin Biochem. 2009;42:1504Y1511.
144. Pfirrmann CW, Metzdorf A, Elfering A, et al. Effect of aging and degeneration on disc volume and shape: a quantitative study in asymptomatic volunteers. J Orthop Res. 2006;24:1086Y1094.
145. Rajasekaran S, Babu JN, Arun R, et al. ISSLS prize winner: a study of diffusion in human lumbar discs: a serial magnetic resonance imaging study documenting the influence of the endplate on diffusion in normal and degenerate discs. Spine (Phila Pa 1976). 2004;29:2654Y2667.
146. Antoniou J, Goudsouzian NM, Heathfield TF, et al. The human lumbar endplate. Evidence of changes in biosynthesis and denaturation of the extracellular matrix with growth, maturation, aging, and degeneration. Spine (Phila Pa 1976). 1996;21:1153Y1161.
147. Marinelli NL, Haughton VM, Munoz A, et al. T2 relaxation times of intervertebral disc tissue correlated with water content and proteoglycan content. Spine (Phila Pa 1976). 2009;34:520Y524.
148. Panagiotacopulos ND, Pope MH, Krag MH, et al. Water content in human intervertebral discs. Part I. Measurement by magnetic resonance imaging. Spine (Phila Pa 1976). 1987;12:912Y917.
149. Chatani K, Kusaka Y, Mifune T, et al. Topographic differences of 1H-NMR relaxation times (T1, T2) in the normal intervertebral disc and its relationship to water content. Spine (Phila Pa 1976). 1993;18:2271Y2275.
150. Kerttula L, Kurunlahti M, Jauhiainen J, et al. Apparent diffusion coefficients and T2 relaxation time measurements to evaluate disc degeneration. A quantitative MR study of young patients with previous vertebral fracture. Acta Radiol. 2001;42:585Y591.
151. Karakida O, Ueda H, Ueda M, et al. Diurnal T2 value changes in the lumbar intervertebral discs. Clin Radiol. 2003;58: 389Y392.
152. Ludescher B, Effelsberg J, Martirosian P, et al. T2- and diffusion-maps reveal diurnal changes of intervertebral disc composition: an in vivo MRI study at 1.5 tesla. J Magn Reson Imaging. 2008;28:252Y257.
153. Benneker LM, Heini PF, Anderson SE, et al. Correlation of radiographic and MRI parameters to morphological and biochemical assessment of intervertebral disc degeneration. Eur Spine J. 2005;14:27Y35.
154. Buck FM, Bae WC, Diaz E, et al. Comparison of T1rho measurements in agarose phantoms and human patellar cartilage using 2D multislice spiral and 3D magnetization prepared partitioned k-space spoiled gradient-echo snapshot techniques at 3 T. AJR Am J Roentgenol. 2011;196:W174Y179.
155. Drew SC, Silva P, Crozier S, et al. A diffusion and T2 relaxation MRI study of the ovine lumbar intervertebral disc under compression in vitro. Phys Med Biol. 2004;49:3585Y3592.
156. Majumdar S. Magnetic resonance imaging and spectroscopy of the intervertebral disc. NMR Biomed. 2006;19:894Y903.
157. Zuo J, Saadat E, Romero A, et al. Assessment of intervertebral disc degeneration with magnetic resonance single-voxel spectroscopy. Magn Reson Med. 2009;62:1140Y1146.
158. Keshari KR, Lotz JC, Link TM, et al. Lactic acid and proteoglycans as metabolic markers for discogenic back pain. Spine (Phila Pa 1976). 2008;33:312Y317.
159. Xia Y. Magic-angle effect in magnetic resonance imaging of articular cartilage: a review. Invest Radiol. 2000;35:602Y621.
160. Szeverenyi NM, Bydder GM. Dipolar anisotropy fiber imaging in a goat knee meniscus. Magn Reson Med. 2011;65:463Y470.
161. Bae WC, Statum S, Znamirowski R, et al. Dipolar anisotropy fiber imaging of human anulus fibrosus. Proc Intl Soc Magn Reson Med. 2011;19:2569.
162. Bae WC, Xu K, Inoue N, et al. Ultrashort time-to-echo MRI of human intervertebral disc endplate: association with endplate calcification. Proc Intl Soc Magn Reson Med. 2010;18:3218.
163. Bae WC, Yoshikawa T, Hemmad AR, et al. Ultrashort time-to-echo MRI of human intervertebral disc endplate: association with disc degeneration. Proc Intl Soc Magn Reson Med. 2010;18:534.
164. Gatehouse PD, He T, Hughes SP, et al. MR imaging of degenerative disc disease in the lumbar spine with ultrashort TE pulse sequences. Magma. 2004;16:160Y166.
165. Masuda K, Oegema TR Jr, An HS. Growth factors and treatment of intervertebral disc degeneration. Spine. 2004;29:2757Y2769.