Advanced MR imaging of the shoulder: dedicated cartilage techniques

Magn Reson Imaging Clin N Am 12 (2004) 143–159

Advanced MR imaging of the shoulder: dedicated cartilage techniques Garry E. Gold, MD*, Scott B. Reeder, MD, PhD, Christopher F. Beaulieu, MD, PhD Department of Radiology, Stanford University, 300 Pasteur Drive SO-68B, Stanford, CA 94305-5105, USA

Osteoarthritis is an important cause of disability in our society, affecting millions and resulting in loss of time at work and activity limitations [1– 5]. Osteoarthritis is primarily a disease of articular cartilage from injury or degeneration [6–8]. Many treatment strategies for cartilage damage have been proposed [9–11], but methods for assessment of the effectiveness of these therapies are limited to clinical evaluation and occasional opportunities for arthroscopic examination. MR imaging offers a noninvasive means of assessing the degree of damage to cartilage and adjacent bone, and effectiveness of treatment. The accepted gold standard for monitoring cartilage damage in the shoulder is arthroscopy, with high resolution and the ability to probe the cartilage surface. Arthroscopy is invasive and expensive, and allows only visual inspection of the cartilage surface for such abnormalities as color changes and fissuring. Arthroscopy also allows probing of cartilage, which involves using a small metallic probe to apply pressure on the cartilage surface to assess softening (chondromalacia). Many imaging methods are available to assess articular cartilage in the shoulder. Conventional radiography can be used to detect gross loss of cartilage, evident as narrowing of the glenohumeral distance [12], but it does not image cartilage directly. Secondary changes, such as osteophyte formation or subchondral cysts, can be seen, but conventional radiography is insensitive to early chondral damage. Arthrography, alone or com-

* Corresponding author. E-mail address: [email protected] (G.E. Gold).

bined with conventional radiography, CT scanning, or MR imaging, also is invasive and provides information limited to the contour of the cartilage surface [13]. MR imaging, with its excellent soft tissue contrast, is the best technique available for assessment of articular cartilage [14–18]. Imaging of glenohumeral cartilage damage has the potential to provide morphologic information, such as fissuring, and presence of partial- or full-thickness cartilage defects. An ideal MR imaging technique for cartilage should provide accurate assessment of cartilage thickness, demonstrate morphologic changes of the cartilage surface, demonstrate internal cartilage signal changes, and allow evaluation of the subchondral bone for signal abnormalities. Unfortunately, conventional MR imaging sequences are limited in providing a detailed assessment of cartilage, lacking either spatial resolution [19] or information about cartilage physiology. Research in MR imaging of articular cartilage has focused mostly on knee imaging. There are several reasons for this: knee cartilage is the thickest in the body; it can be placed at isocenter of the scanner; and it is near the joint surface. The glenohumeral joint, by contrast, cannot be placed at isocenter of most systems. Glenohumeral cartilage also is thin compared with knee cartilage, meaning less tissue is present to provide signal, and higher resolution is needed to see changes. The shoulder joint is deep compared with the patellofemoral joint, requiring a larger surface coil with lower signal to noise. Imaging of the glenohumeral joint cartilage is challenging, but many of the techniques outlined below are available to use in the shoulder.

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Fig. 1. Axial images of glenohumeral cartilage at 1.5T after injection of a dilute mixture of gadolinium in saline. (A, B) Axial proton density 512  192 images without fat saturation, 3 mm slice thickness, scan time 3 minutes, 30 seconds. (C, D) Axial 256  192 T1-weighted images with fat saturation, 3 mm slice thickness, scan time 3 minute, 30 seconds. Note the labral tear (arrow) and excellent depiction of cartilage with joint distended.

Conventional MR imaging methods MR image contrast One of the major advantages of MR imaging is the ability to manipulate contrast to highlight tissue types. The common contrast mechanisms used in MR imaging are T1-weighted, protondensity, and T2-weighted imaging. Clinical use of these mechanisms has evolved over time with the introduction of fast or turbo spin-echo imaging and the use of fat saturation.

Tissue relaxation times and imaging parameters are the major determinants of contrast between cartilage and fluid. Lipid suppression, however, increases contrast between nonlipid and lipid-containing tissues and affects how the MR scanner sets the overall dynamic range of the image. The most common type of lipid suppression is fat saturation, in which fat spins are excited then diphase before imaging. Another option is spectral-spatial excitation, in which only water spins in a slice are excited [20].

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Fig. 2. Dixon fast spin-echo (FSE) images of the shoulder joint at 1.5T. (A) Axial water image. (B) Axial fat image. (C) Axial source image. Dixon FSE provides robust fat suppression and excellent signal to noise. Images were acquired with TR/TE 4000/15 milliseconds, 256  256 matrix, 20 cm field of view, 3 mm slice thickness, and a scan time of 5 minutes.

In the glenohumeral joint, lipid suppression and spectral-spatial excitation can fail because the shoulder is far off isocenter of the scanner. At the edges of the scanner, field inhomogeneity is more severe and shimming is more difficult. For these reasons, techniques based on Dixon separation of fat and water may work better than conventional fat suppression in the shoulder. MR coils Choice of a good coil for shoulder imaging is crucial to the ability to examine articular carti-

lage. A coil with a high intrinsic signal-to-noise ratio (SNR) that images the entire joint will enable higher resolution imaging. Most hardware manufacturers have developed dedicated phasedarray surface coils for the shoulder, which will maximize the available SNR and hence the resolution that can be achieved. T1- and T2-weighted spin echo imaging T1- and T2-weighted spin-echo MR imaging allows depiction of articular cartilage, and can demonstrate defects and gross morphologic

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Fig. 3. Three-dimensional Dixon steady-state free precession images of the glenohumeral cartilage done at 1.5T. (A) Water image. (B) Fat image. (C) Source image. Note the excellent uniform fat saturation. Images were acquired with TR/TE 6.4/1.5 milliseconds, 256  256 matrix, 20 cm field of view, 3 mm slice thickness, and a scan time of 2 minutes and 40 seconds.

changes. T1-weighted images are characterized by excellent signal from hyaline cartilage [21,22]. However, T1-weighted imaging does not show significant contrast between joint effusion and the cartilage surface, making surface irregularities and intrasubstance defects difficult to detect. Fat suppression adds dynamic range and reduces the effects of chemical shift artifacts [23]. T2-weighted imaging demonstrates joint effusions and thus surface abnormalities cartilage, but because some components of cartilage have short T2 relaxation times [24,25], these components are not well

depicted. Because of the long scan times of conventional T1- and T2-weighted spin-echo imaging, these sequences have been mostly replaced by fast or turbo spin-echo imaging in the shoulder. Gradient-recalled echo imaging Gradient-recalled echo imaging has been employed primarily in the knee because of its 3D capability and ability to provide high-resolution images with shorter scan times than spin-echo imaging. Fat-suppressed 3D spoiled gradient echo

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Fig. 4. Axial images of the glenohumeral cartilage of a healthy volunteer done at 3.0 Tesla. (A) Fat-suppressed proton density image. Imaging parameters were TR/TE 5000/15 milliseconds, 512  192 matrix, 2.5 mm slice thickness, 14 cm field of view. (B) Two-dimensional gradient echo image. Imaging parameters were TR/TE 600/20 milliseconds, 25-degree flip angle, 256  192 matrix, 2.5 mm slice thickness, 14 cm field of view. Note the relative blurring of the glenohumeral cartilage on the proton density image. These images were acquired with higher resolution compared with typical images done at 1.5T.

(FS-3D-SPGR) imaging has been shown to be more sensitive than standard MR imaging for the detection of hyaline cartilage defects in the knee [26,27]. Though increased sensitivity and spatial resolution are advantages of 3D gradient-recalled echo imaging, imaging times can be long, and contrast between cartilage and adjacent joint fluid is not always optimal. In addition, metal fragments, too small to demonstrate on conventional radiographs, are often present in the joint after surgical therapy. These fragments may cause artifacts on gradient-recalled echo imaging, limiting the evaluation of cartilage in the postoperative shoulder. Fast spin-echo imaging Fast spin-echo imaging (FSE) or turbo spinecho imaging uses multiple echoes per repetition time (TR) to acquire data faster than conventional spin echo imaging. Proton density FSE has been shown to be useful in cartilage imaging [28]. One disadvantage of proton density FSE is blurring of short-T2 species due to acquisition of high spatial frequencies late in the echo train [29]. T2-weighted FSE has been shown to be accurate for detection of cartilage surface lesions [30] in the knee. Because the cartilage-to-fluid contrast in T2weighted FSE is generated at the expense of

cartilage signal, this method is less useful for detection of intrasubstance abnormalities. MR arthrography Direct MR arthrography, in which a dilute solution containing gadolinium is injected directly into the joint, improves contrast between cartilage and the injected fluid (Fig. 1) [31]. Though not yet clinically available, liposome-entrapped contrast agents show reduced diffusion into the cartilage itself, aiding in the visualization of the articular cartilage surface [32]. MR arthrography allows improved visualization of the surface of cartilage in joints such as the shoulder where cartilage is normally quite thin. Advanced morphologic MR imaging methods High-resolution imaging MR imaging of the morphology of glenohumeral cartilage requires close attention to the spatial resolution used. To see degenerative cartilage, imaging with resolution on the order of 0.2 mm to 0.4 mm is required [19]. The actual resolution achievable is governed by the SNR possible within a given imaging time and for a given coil. Ultimately, a high-resolution imaging technique

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Fig. 5. Axial fat-suppressed three-dimensional spoiled gradient-echo images of the glenohumeral cartilage at 3.0 Tesla. Imaging parameters were TR/TE 13.5/1.5 milliseconds, 256  256 matrix, 16 cm field of view, 2 mm slice thickness, and three signal averages. Despite the increase in signal at 2.0 Tesla, the acquisition time was 5 minutes, 30 seconds. Flip angle was 10 degrees because of the increased T1 relaxation time of cartilage at 3.0T. Excellent detail in the glenohumeral cartilage is seen.

that combines morphologic and physiologic information would be ideal in the evaluation of shoulder cartilage, including that related to various therapeutic regimens. Dixon FSE imaging The authors have recently described an iterative least-squares Dixon water-fat separation algorithm in combination with FSE that allows the calculation of water and fat images at

arbitrary and short-echo time increments [33]. This is beneficial for FSE Dixon imaging because shorter echo time increments reduce the time between refocusing pulses (echo spacing) to minimize blurring from long echo trains (Fig. 2). Dixon SSFP imaging Considerable work in cartilage has been devoted to screening patients with high-resolution three-dimensional imaging techniques. High

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Fig. 6. Axial proton density Dixon fast spin-echo images from the shoulder of a healthy volunteer done at 3.0 Tesla. (A) Water image. (B) Fat image. (C) Source image. Image parameters were TR/TE 5000/14 milliseconds, 512  192 matrix, 2.5 mm slice thickness, 14 cm field of view. Scan time was 5 minutes, 15 secconds. Note the excellent fat/water separation, even a high field strength and off isocenter.

accuracy for cartilage lesions has been show with 3D-SPGR imaging [26,27,34]. Cartilage volumes in the shoulder can be measured using this method [35]. There are two main disadvantages of this approach: lack of reliable contrast between cartilage and fluid that outlines surface defects, and long imaging times (about 8 minutes). In addition, SPGR uses gradient or radiofrequency spoiling to reduce artifacts and achieve near-T1 weighting. This reduces the overall signal compared with steady-state techniques.

Steady-state free precession (SSFP) MR imaging is an efficient, high-signal method for obtaining 3D MR images [36]. This method also has been called true-fast imaging with steady-state precession (FISP) or balanced fast field echo (FFE) imaging [37]. With recent advances in MR gradient hardware, it is now possible to use SSFP without suffering from the banding or off-resonance artifacts that have been problematic for this method. SSFP has been shown to be a promising method for cartilage imaging in the knee [38,39],

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Fig. 7. Coronal proton density Dixon fast spin-echo images from the shoulder of a healthy volunteer done at 3.0 Tesla. (A) Water image. (B) Fat image. (C) Source image. Image parameters were TR/TE 5000/14 milliseconds, 512192 matrix, 2.5 mm slice thickness, 14 cm field of view. Scan time was 5 minutes, 15 secconds. Note the excellent fat/water separation, even a high field strength and off isocenter.

where field homogeneity is better than in the shoulder. Dixon SSFP is a variant of SSFP that is useful in imaging cartilage in the knee [40]. Dixon SSFP provides robust fat saturation in areas of inhomogeneity and may be useful for detecting cartilage defects in the shoulder (Fig. 3). The contrast produced in SSFP sequences is also favorable for cartilage imaging. Dixon SSFP produces contrast based on the ratio of T2/T1 in tissues. This results in bright fluid signal while preserving cartilage signal. The largest disadvantage of SSFP techniques is

sensitivity to off-resonance artifacts. Another approach that may provide reliable fat suppression at high resolution is to use linear combination steady-state free precession [41]. Imaging at 3.0 Tesla The intrinsic SNR available in an MR imaging study is proportional to the main magnetic field strength, the voxel volume, and the sensitivity of the radiofrequency coil being used. Most conventional MR imaging of the musculoskeletal system

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Fig. 8. Axial 3D steady-state free precession Dixon images from the shoulder of a healthy volunteer done at 3.0 Tesla. (A) Water image. (B) Fat image. (C) Source image. Image parameters were TR/TE 5.4/1.5 milliseconds, 256  256 matrix, 2 mm slice thickness, 16 cm field of view. Acquisition time for this three-dimensional cartilage sequence was only 2 minutes. Note the banding artifact (arrow) in the deltoid as well as a light venetian-blind artifact across the image due to field inhomogeneity.

is done at 1.5 Tesla. Higher field systems, typically 3.0 Tesla, are now becoming more prevalent in the clinical setting. Because the available magnetization varies linearly with field strength, imaging at 3.0T should provide twice the intrinsic SNR of imaging at 1.5T for the equivalent coil and subject [42]. However, field-dependent changes in tissue relaxation times and in the chemical shift difference between fat and water may limit the SNR benefit seen at 3.0T. T2 relaxation is constant at different field strengths, decreasing slightly at higher field strength [43]. T1 relaxation,

however, increases as the field strength increases [43]. Prior measurements of relaxation times at 4.0T showed increases of T1 of 70% to 90% and decreases of T2 of 10% to 20% compared with 1.5T [44]. At 3.0 Tesla, TI increases 30% to 40% and T2 decreases 10% to 20% compared with 1.5T [45]. The changes in these parameters affect the choice of TR and echo time (TE) that are appropriate for 3.0T, and ultimately impact the contrast and SNR of the images produced. At 3.0T, the chosen TR and TE must reflect the

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Fig. 9. MR images of nine cartilage-bone plugs from the humeral head placed side-by-side in their original order on the joint surface. Each specimen was imaged at four different angles in the magnetic field. Note that at 55 degrees to Bo (the magic angle), the laminar appearance of cartilage disappears and the tissue appears homogeneous. (From Xia Y, Moody JB, Alhadlaq H, et al. Characteristics of topographical heterogeneity of articular cartilage over the joint surface of a humeral head. Osteoarthritis Cartilage 2002;10:370–80; with permission.)

underlying tissues being imaged and the contrast desired. Musculoskeletal imaging protocols typically consist of several two-dimensional multisection scans, with or without fat saturation. At 3.0T, because the T1 relaxation times have increased, the TR must be longer to maximize the SNR gain. At 3.0T, TR must also be longer to achieve the similar contrast to T1-weighted images acquired at 1.5T. Similarly, the TE should be slightly shorter to account for decreases in T2 relaxation times. The number of slices and spatial resolution required may also influence the choice of TR and TE. Conventional FSE imaging (Fig. 4) shows improved SNR at 3.0 Tesla, enabling higherresolution imaging. This is also true of threedimensional fat-suppressed gradient-echo imaging (Fig. 5) at 3.0T. Advanced imaging of articular cartilage in the shoulder is also possible at 3.0 Tesla. Dixon FSE

works well at 3.0T, providing fat, water, and source images of the shoulder (Figs. 6 and 7). The advantages of this technique are similar to those at 1.5T, with the additional benefit that the incremental echo time spacing is half as long, allowing for shorter interecho spacing than at 1.5T. Dixon SSFP imaging is also possible at 3.0T, but more difficult off isocenter because of field inhomogeneity (Fig. 8). Physiologic MR imaging of shoulder cartilage Articular cartilage composition Articular cartilage is approximately 70% water by weight. The remainder of the tissue consists predominately of type II collagen fibers and proteoglycans. The proteoglycans contain negative charges, typically bound to sodium (Na +) in intact cartilage. The collagen fibers have an ordered structure, making the water associated

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Fig. 10. Coronal proton density maps (A–C) and T2 maps (D–F) done at 3.0 Tesla. Grayscale T2 images show uniform T2 relaxation of glenohumeral cartilage in this healthy volunteer (arrow). In the knee, increased T2 relaxation times have been correlated with loss of collagen matrix in cartilage. Changes in the collagen matrix may occur earlier than morphologic changes. T2 maps are on a scale of 0 to 255 milliseconds, with lighter greyscale values indicating longer relaxation times. (Courtesy of Bernard Dardzinski, PhD, Cincinnati, OH.)

with them exhibit both magnetization transfer and magic-angle effects. Advanced MR imaging of articular cartilage takes advantage of these characteristics to explore whether the collagen and proteoglycan matrices are intact. Contrast-enhanced imaging Gadolinium-enhanced imaging also has the potential to allow monitoring of glycosaminoglycan content within the cartilage, which may have important implications for longitudinal evaluations of injured cartilage [46,47]. The ability to

monitor glycosaminoglycan content in a cartilage repair site may be helpful in determining the physiologic state of the repair. This technique requires careful attention to protocol issues, but has good reproducibility and holds promise for seeing early changes of osteoarthritis [48,49]. This technique has shown promise in the knee and the hip, but has not been applied to glenohumeral cartilage. T2 mapping The T2 relaxation time of articular cartilage is a function of the water content of the tissue.

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Fig. 10 (continued )

Measurement of the spatial distribution of the T2 relaxation time may reveal areas of increased or decreased water content, correlating with cartilage damage. To measure the T2 relaxation time with a high degree of accuracy, care must be taken with the MR technique [50]. Cartilage T2 in the shoulder is a function of magic angle, among other parameters (Fig. 9) [51]. Typically, a multiecho spin-echo technique is used and signal levels are fitted to one or more decaying exponentials, depending on whether it is believed that there is more than one distribution of T2 within the sample [52]. An image of the T2 relaxation time is then generated, either with a color map or grayscale representing the relaxation time. Several investigators have measured the spatial distribution of T2 relaxation times within cartilage [53,54]. Aging appears to be associated with a symptomatic increase in T2 relaxation times in the transitional zone [55]. Relaxation time measurements have also been shown to be anisotropic with respect to orientation in the main magnetic field [56–58]. Focal increases in T2 relaxation times within cartilage have been associated with matrix damage, particularly loss of collagen matrix [54]. T2 mapping has been shown at 3.0 Tesla in the knee and the PIP joints of the hand. Mapping of shoulder cartilage in vivo at 3.0 Tesla is feasible (Fig. 10) but challenging because of the spatial resolution and signal to noise required.

Sodium MR imaging Sodium MR imaging has recently shown some promising results in the imaging of articular cartilage. This is based on the ability of sodium imaging to depict regions of proteoglycan depletion [59]. 23Na atoms are associated with the high fixed-charge density present in proteoglycan sulfate and carboxylate groups. Some spatial variation in 23Na concentration is present within normal cartilage [60]. In cartilage samples, sodium imaging has been shown to be sensitive to small changes in proteoglycan concentration [61]. This method shows promise to be sensitive to early decreases in proteoglycan concentration in osteoarthritis. The resolution and SNR required to do 23 Na imaging in the glenohumeral joint has not yet been achieved on clinical MR imaging scanners. Short TE imaging A number of the water molecules within articular cartilage are closely associated with collagen fibers. Some of these 1H spins have extremely short T2 relaxation times and contribute to the ‘‘bound’’ pool of 1H that are used to produce the magnetization transfer effect. However, there may be species within cartilage that exhibit short T2 relaxation times that can be imaged with MR [62]. In addition, the T2 relaxation time of cartilage deceases in the radial zone near the cartilage/bone interface, making the

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Fig. 11. Ultra-short echo-time (UTE) images of the glenohumeral cartilage. (A, B) Conventional UTE sequence. (C, D) Frequency-based fat-suppression sequence. All images are 512  512, 17 cm field of view, TR/TE 500/0.08 milliseconds. These images are subtracted from an image done with a TE of 11.70 milliseconds to highlight short T2 components in the articular cartilage and the rotator cuff. Note the higher signal in the deeper layers of cartilage. (Courtesy of Graeme Bydder, ChB, San Diego, CA.)

use of a short echo time necessary to obtain signal from these protons (Fig. 11). One approach to obtaining MR images with minimum echo time is to use half-excitation pulses. A chopped, short-T2 excitation is used in which two half-pulses are added together from successive excitations to form a slice [63]. This removes the requirement for the usual refocusing pulse that follows a slice-selective excitation. In addition, rather than a Cartesian readout of k-

space, a projection-reconstruction (PR) approach is used which begins at the k-space origin. The combination of the short T2 excitation and PR readout make the echo time as short as 80 microseconds, maximizing signal from protons with short T2 relaxation times [64]. Another approach that is useful for obtaining short echo times is to use a 3D readout that begins at the origin of k-space. The readout can take the form of a 3D PR trajectory (‘‘koosh ball’’) [65] or

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Fig. 12. Imaging of the glenohumeral joint with intraarticular coils. (A) Expandable loop coil, tuned with a varactor diode. (B) Image of a cadaver glenohumeral joint using the expandable intraarticular coil. The cartilage on the humeral head (arrow) is clearly seen. This image was 0.15 mm in-plane resolution with a 1.5 mm slice thickness. (C) Same cadaver shoulder imaged with identical parameters using a 3-in surface coil. The image at the same window and level shows the signal-to-noise advantage for the intraarticular coil for examining focal cartilage defects. This coil can be inserted into the joint at the time of arthrography. G, glenoid; H, humeral hear; L, superior labrum.

follow arcs on cones for a more efficient scan [66]. This has been used to produce 3D images of cartilage with echo times as short as 0.6 milliseconds. A recent study of patellar cartilage specimens compared the sensitivity of an ultrashort TE projection-reconstruction imaging sequence with FS 3D SPGR and magnetization transfer contrast subtraction MR imaging [62]. In this study, the projection-reconstruction imaging technique was found to provide superior delineation of cartilage lesions when compared with the other two techniques. The authors believed that this superiority was due to the detection of water associated with collagen that had short T2 relaxation times. Short echo times also have been shown to be important in cartilage thickness measurements as

well as analysis of zonal anatomy at high field [24]. Another promising approach to short TE imaging is to acquire a full spectroscopic data set along with a short TE image [66]. This technique allows for high-resolution imaging without chemical shift artifact. Because the widths of spectra obtained from the water resonance are inversely proportional to the T2 relaxation times, this technique can also map water content. Intraarticular coils Optimal imaging of shoulder cartilage requires continued improvement in MR technology. The fundamental trade-off between image resolution and SNR still limits our ability to image shoulder

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cartilage in vivo with high resolution in an efficient manner. One approach is to limit the field of view to a specific area of cartilage loss or therapy, enabling the use of a small surface coil or intraarticular coil [67]. These coils have the potential to greatly improve SNR over a small area compared with surface coils (Fig. 12). Diffusion-weighted imaging (DWI) Imaging the diffusion of water through articular cartilage is also possible with MR imaging. DWI of cartilage has been demonstrated in vitro to be sensitive to early cartilage degradation [25,68]. Water undergoing diffusion, however, accrues a random amount of phase and does not refocus, resulting in signal loss in tissue undergoing diffusion. The amount of diffusion weighting applied depends on the amplitude of the diffusion-sensitizing gradients and is termed the ‘‘b value.’’ A map of the amount of diffusion that has occurred is usually constructed from images with and without diffusion gradients applied, and this map is called the apparent diffusion coefficient (ADC) map. In vivo DWI of cartilage poses several challenges. The T2 relaxation time of cartilage varies from 10 to 50 ms, so the TE must be short to maximize cartilage signal. Diffusion-sensitizing gradients increase the TE and render the sequence sensitive to motion. Single-shot techniques have been used for DWI, but these suffer from low SNR and spatial resolution. Multiple acquisitions improve the SNR and resolution, but motion correction is required for accurate reconstruction [69]. A promising new approach to DWI of cartilage is using SSFP combined with diffusion weighting [70]. Diffusion imaging of glenohumeral cartilage has not yet been demonstrated in vivo.

Summary Imaging of articular cartilage in the shoulder is challenging for MR imaging, but improvements in morphologic and physiologic imaging continue to be made. Improvements have been made in contrast and resolution of cartilage imaging sequences used in routine clinical cases. Progress has been made in the understanding of cartilage physiology and the ability to detect proteoglycan and collagen loss. New hardware, such as higher field-strength systems and new coils, may allow further improvements in resolution. Progress in

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imaging the shoulder cartilage holds promise to improve diagnosis and therapy for glenohumeral disease.

Acknowledgments The authors acknowledge support from NIH grant 1R01-EB002524 and the generous support of the Whitaker Foundation. The authors also acknowledge the assistance of General Electric Applied Sciences Laboratory (West) and Anne Sawyer-Glover from the Lucas Center at Stanford University. The authors thank Graeme Bydder, ChB, and Bernard Darzinski, PhD, for providing images for this article. References [1] Swedberg JA, Steinbauer JR. Osteoarthritis. Am Fam Physician 1992;45:557–68. [2] Brandt KD. Osteoarthritis. Clin Geriatr Med 1988; 4:279–93. [3] Davis MA. Epidemiology of osteoarthritis. Clin Geriatr Med 1988;4:241–55. [4] Peyron JG. Epidemiological aspects of osteoarthritis. Scand J Rheumatol Suppl 1988;77:29–33. [5] Sangha O. Epidemiology of rheumatic diseases. Rheumatology (Oxford) 2000;39(Suppl 2):3–12. [6] Poole AR. An introduction to the pathophysiology of osteoarthritis. Front Biosci 1999;4:D662–70. [7] Roos H, Adalberth T, Dahlberg L, Lohmander LS. Osteoarthritis of the knee after injury to the anterior cruciate ligament or meniscus: the influence of time and age. Osteoarthritis Cartilage 1995;3: 261–7. [8] van den Berg WB. Pathophysiology of osteoarthritis. Joint Bone Spine 2000;67:555–6. [9] Bentley G, Minas T. Treating joint damage in young people. BMJ 2000;320:1585–8. [10] Chevalier X. Autologous chondrocyte implantation for cartilage defects: development and applicability to osteoarthritis. Joint Bone Spine 2000;67: 572–8. [11] Chikanza I, Fernandes L. Novel strategies for the treatment of osteoarthritis. Expert Opin Investig Drugs 2000;9:1499–510. [12] Boegard T, Jonsson K. Radiography in osteoarthritis of the knee. Skeletal Radiol 1999;28:605–15. [13] Coumas JM, Palmer WE. Knee arthrography. Evolution and current status. Radiol Clin North Am 1998;36:703–28. [14] Disler DG, Recht MP, McCauley TR. MR imaging of articular cartilage. Skeletal Radiol 2000;29: 367–77. [15] Gold GE, Bergman AG, Pauly JM, et al. Magnetic resonance imaging of knee cartilage repair. Top Magn Reson Imaging 1998;9:377–92.

158

G.E. Gold et al / Magn Reson Imaging Clin N Am 12 (2004) 143–159

[16] Hodler J, Resnick D. Current status of imaging of articular cartilage. Skeletal Radiol 1996;25:703–9. [17] McCauley TR, Disler DG. Magnetic resonance imaging of articular cartilage of the knee. J Am Acad Orthop Surg 2001;9:2–8. [18] Recht MP, Resnick D. Magnetic resonance imaging of articular cartilage: an overview. Top Magn Reson Imaging 1998;9:328–36. [19] Rubenstein JD, Li JG, Majumdar S, Henkelman RM. Image resolution and signal-to-noise ratio requirements for MR imaging of degenerative cartilage. AJR Am J Roentgenol 1997;169:1089–96. [20] Meyer CH, Pauly JM, Macovski A, Nishimura DG. Simultaneous spatial and spectral selective excitation. Magn Reson Med 1990;15:287–304. [21] Snaps FR, Saunders JH, Park RD, et al. Comparison of spin echo, gradient echo and fat saturation magnetic resonance imaging sequences for imaging the canine elbow. Vet Radiol Ultrasound 1998;39: 518–23. [22] Vallotton JA, Meuli RA, Leyvraz PF, Landry M. Comparison between magnetic resonance imaging and arthroscopy in the diagnosis of patellar cartilage lesions: a prospective study. Knee Surg Sports Traumatol Arthrosc 1995;3:157–62. [23] van Leersum M, Schweitzer ME, Gannon F, et al. Chondromalacia patellae: an in vitro study. Comparison of MR criteria with histologic and macroscopic findings. Skeletal Radiol 1996;25: 727–32. [24] Freeman DM, Bergman G, Glover G. Short TE MR microscopy: accurate measurement and zonal differentiation of normal hyaline cartilage. Magn Reson Med 1997;38:72–81. [25] Xia Y, Farquhar T, Burton-Wurster N, Lust G. Origin of cartilage laminae in MRI. J Magn Reson Imaging 1997;7:887–94. [26] Disler DG. Fat-suppressed three-dimensional spoiled gradient-recalled MR imaging: assessment of articular and physeal hyaline cartilage. AJR Am J Roentgenol 1997;169:1117–23. [27] 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;198:209–12. [28] Potter HG, Linklater JM, Allen AA, et al. Magnetic resonance imaging of articular cartilage in the knee. An evaluation with use of fast-spin-echo imaging. J Bone Joint Surg Am 1998;80:1276–84. [29] Escobedo EM, Hunter JC, Zink-Brody GC, et al. Usefulness of turbo spin-echo MR imaging in the evaluation of meniscal tears: comparison with a conventional spin-echo sequence. AJR Am J Roentgenol 1996;167:1223–7. [30] 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

[31]

[32]

[33]

[34]

[35]

[36]

[37]

[38]

[39]

[40]

[41]

[42]

[43]

130 patients. AJR Am J Roentgenol 1999;172: 1073–80. Rand T, Brossmann J, Pedowitz R, et al. Analysis of patellar cartilage. Comparison of conventional MR imaging and MR and CT arthrography in cadavers. Acta Radiol 2000;41:492–7. Grunder W, Biesold M, Wagner M, Werner A. Improved nuclear magnetic resonance microscopic visualization of joint cartilage using liposome entrapped contrast agents. Invest Radiol 1998;33: 193–202. Reeder SB, Wen Z, Yu H, et al. Multicoil Dixon chemical species seperation with an iterative leastsquares estimation method. Magn Reson Med, in press. Wang SF, Cheng HC, Chang CY. Fat-suppressed three-dimensional fast spoiled gradient-recalled echo imaging: a modified FS 3D SPGR technique for assessment of patellofemoral joint chondromalacia. Clin Imaging 1999;23:177–80. Graichen H, Jakob J, von Eisenhart-Rothe R, et al. Validation of cartilage volume and thickness measurements in the human shoulder with quantitative magnetic resonance imaging. Osteoarthritis Cartilage 2003;11:475–82. Menick BJ, Bobman SA, Listerud J, Atlas SW. Thin-section, three-dimensional Fourier transform, steady-state free precession MR imaging of the brain. Radiology 1992;183:369–77. Duerk JL, Lewin JS, Wendt M, Petersilge C. Remember true FISP? A high SNR, near 1-second imaging method for T2- like contrast in interventional MRI at .2T. J Magn Reson Imaging 1998;8: 203–8. Vasnawala SS, Pauly JM, Nishimura DG, Gold GE. MR imaging of knee cartilage with FEMR. Skeletal Radiol 2002;31:574–80. Hargreaves BA, Gold GE, Beaulieu CF, et al. Comparison of new sequences for high-resolution cartilage imaging. Magn Reson Med 2003;49: 700–9. Reeder SB, Pelc NJ, Alley MT, Gold GE. Rapid MR imaging of articular cartilage with steady-state free precession and multipoint fat-water separation. AJR Am J Roentgenol 2003;180:357–62. Vasanawala SS, Pauly JM, Nishimura DG. Linear combination steady-state free precession MRI. Magn Reson Med 2000;43:82–90. Collins CM, Smith MB. Signal-to-noise ratio and absorbed power as functions of main magnetic field strength, and definition of ‘‘90 degrees’’ RF pulse for the head in the birdcage coil. Magn Reson Med 2001;45:684–91. Bottomley PA, Foster TH, Argersinger RE, Pfeifer LM. A review of normal tissue hydrogen NMR relaxation times and relaxation mechanisms from 1–100 MHz: dependence on tissue type, NMR frequency, temperature, species, excision, and age. Med Phys 1984;11:425–48.

G.E. Gold et al / Magn Reson Imaging Clin N Am 12 (2004) 143–159 [44] Duewell SH, Ceckler TL, Ong K, et al. Musculoskeletal MR imaging at 4 T and at 1.5 T: comparison of relaxation times and image contrast. Radiology 1995;196:551–5. [45] Gold GE, Han EH, Stanisby JA, et al. Relaxation times and contrast in musculoskeletal MR imaging at 3.0 Tesla. Paper presented at the annual meeting of the Radiologic Society of North America. Chicago, December 1–5, 2003. [46] Bashir A, Gray ML, Boutin RD, Burstein D. Glycosaminoglycan in articular cartilage: in vivo assessment with delayed Gd(DTPA)(2-)-enhanced MR imaging. Radiology 1997;205:551–8. [47] Bashir A, Gray ML, Hartke J, Burstein D. Nondestructive imaging of human cartilage glycosaminoglycan concentration by MRI. Magn Reson Med 1999;41:857–65. [48] Burstein D, Velyvis J, Scott KT, et al. Protocol issues for delayed Gd(DTPA)(2-)-enhanced MRI (dGEMRIC) for clinical evaluation of articular cartilage. Magn Reson Med 2001;45:36–41. [49] Burstein D, Bashir A, Gray ML. MRI techniques in early stages of cartilage disease. Invest Radiol 2000; 35:622–38. [50] Poon CS, Henkelman RM. Practical T2 quantitation for clinical applications. J Magn Reson Imaging 1992;2:541–53. [51] Xia Y, Moody JB, Alhadlaq H, et al. Characteristics of topographical heterogeneity of articular cartilage over the joint surface of a humeral head. Osteoarthritis Cartilage 2002;10:370–80. [52] Smith HE, Mosher TJ, Dardzinski BJ, et al. Spatial variation in cartilage T2 of the knee. J Magn Reson Imaging 2001;14:50–5. [53] Dardzinski BJ, Mosher TJ, Li S, et al. Spatial variation of T2 in human articular cartilage. Radiology 1997;205:546–50. [54] Goodwin DW, Wadghiri YZ, Dunn JF. Microimaging of articular cartilage: T2, proton density, and the magic angle effect. Acad Radiol 1998;5: 790–8. [55] Mosher TJ, Dardzinski BJ, Smith MB. Human articular cartilage: influence of aging and early symptomatic degeneration on the spatial variation of T2—preliminary findings at 3 T. Radiology 2000; 214:259–66. [56] Grunder W, Wagner M, Werner A. MR-microscopic visualization of anisotropic internal cartilage structures using the magic angle technique. Magn Reson Med 1998;39:376–82.

159

[57] Henkelman RM, Stanisz GJ, Kim JK, Bronskill MJ. Anisotropy of NMR properties of tissues. Magn Reson Med 1994;32:592–601. [58] Xia Y. Magic-angle effect in magnetic resonance imaging of articular cartilage: a review. Invest Radiol 2000;35:602–21. [59] Reddy R, Insko EK, Noyszewski EA, et al. Sodium MRI of human articular cartilage in vivo. Magn Reson Med 1998;39:697–701. [60] Shapiro EM, Borthakur A, Dandora R, et al. Sodium visibility and quantitation in intact bovine articular cartilage using high field (23)Na MRI and MRS. J Magn Reson 2000;142:24–31. [61] Borthakur A, Shapiro EM, Beers J, et al. Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI. Osteoarthritis Cartilage 2000;8:288–93. [62] Brossmann J, Frank LR, Pauly JM, et al. Short echo time projection reconstruction MR imaging of cartilage: comparison with fat-suppressed spoiled GRASS and magnetization transfer contrast MR imaging. Radiology 1997;203:501–7. [63] Gold GE, Pauly JM, Macovski A, Herfkens RJ. MR spectroscopic imaging of collagen: tendons and knee menisci. Magn Reson Med 1995;34:647–54. [64] Bydder GM. New approaches to magnetic resonance imaging of intervertebral discs, tendons, ligaments, and menisci. Spine 2002;27:1264–8. [65] Peters DC, Korosec FR, Grist TM, et al. Undersampled projection reconstruction applied to MR angiography. Magn Reson Med 2000;43: 91–101. [66] 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; 170:1223–6. [67] Gold GE, Scott G, Butts K, et al. Interventional MR imaging of joints using intra-articular coils. Paper presented at the annual meeting of the International Society for Magnetic Resonance in Medicine. Glasgow, April 21–27, 2001. [68] Kneeland JB. MRI probes biophysical structure of cartilage. Diagn Imaging 1996;18:36–40. [69] Butts K, Pauly J, de Crespigny A, Moseley M. Isotropic diffusion-weighted and spiral-navigated interleaved EPI for routine imaging of acute stroke. Magn Reson Med 1997;38:741–9. [70] Miller KL, Hargreaves BA, Gold GE, Pauly JM. Steady state diffusion imaging of knee cartilage. Magn Reson Med 2004;51:394–8.