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DOI: 10.1148/rg.235035113
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(Radiographics. 2003;23:1227-1242.)
© RSNA, 2003

PLENARY SESSION

Special Focus Session

What’s New in Cartilage?1

Garry E. Gold, MD, Thomas R. McCauley, MD, Martha L. Gray, PhD and David G. Disler, MD

1 From the Department of Radiology, Stanford University, Packard EE Bldg, Rm 222, Stanford, CA 94305-9510 (G.E.G.); the Department of Radiology, Yale University, New Haven, Conn (T.R.M.); the Division of Health Sciences and Technology, Harvard University–Massachusetts Institute of Technology, Cambridge, Mass (M.L.G.); and Commonwealth Radiology, Richmond, Va (D.G.D.). From the Plenary Session, Special Focus Session: What’s New in Cartilage? presented at the 2002 RSNA scientific assembly. Received April 17, 2003; revision requested April 23 and received May 21; accepted May 27. Supported by grants AR46904-02 and AR41773-04 from the National Institutes of Health, by the Whitaker Foundation, and by the Arthritis Foundation. Address correspondence to G.E.G. (e-mail: gold@stanford.edu).


   Abstract
Top
 Abstract
Introduction
 Conventional MR Imaging Methods
 New Morphologic Cartilage...
 Physiologic Imaging of Cartilage
 Discussion
 Conclusions
 References
 
Magnetic resonance (MR) imaging of articular cartilage is important in evaluation of new surgical and pharmacologic treatments for cartilage damage. Many techniques exist for MR imaging of articular cartilage. Standard techniques for morphologic imaging of cartilage include fast spin-echo and spoiled gradient-echo imaging. These methods provide high-resolution morphologic images of cartilage but are time-consuming in the clinical setting. New methods for faster or higher-resolution morphologic imaging include techniques based on steady-state free precession imaging. These fast techniques will allow detailed evaluation of cartilage in the routine clinical setting. There are also several MR imaging methods that may provide information about the structure and physiology of cartilage. Physiologic imaging may allow detailed evaluation of the glycosaminoglycan matrix or collagen network of articular cartilage and may be the most sensitive method for detection of early changes. With the development of new therapies for osteoarthritis and cartilage injury, MR imaging of articular cartilage is of increasing clinical importance. MR imaging will play an important role in evaluation of the effectiveness of these therapies.

© RSNA, 2003

Index Terms: Cartilage, MR, 4521.1214 • Joints, MR, 40.1214 • Knee, ligaments, menisci, and cartilage, 4521.4851, 4521.77 • Knee, MR, 4521.1214


   Introduction
Top
 Abstract
 Introduction
Conventional MR Imaging Methods
 New Morphologic Cartilage...
 Physiologic Imaging of Cartilage
 Discussion
 Conclusions
 References
 
Osteoarthritis is primarily a disease of articular cartilage, either from injury or degeneration (1–4). This disease is an important cause of disability in our society, affecting millions and resulting in loss of time at work and activity limitations (5–9). New pharmacologic therapies for this disease are becoming available (10–12), some of which are hypothesized to have structure-modifying effects on the progression of the disease (13,14). Evaluation of the effectiveness of these therapies requires a fast, noninvasive test for cartilage injury or degeneration, and magnetic resonance (MR) imaging is the most promising test available (15).

In a young patient, injury to the articular cartilage, if left undiagnosed or untreated, may result in premature osteoarthritis (16). Until recently, surgical treatment options for cartilage damage were limited to osteotomy to redistribute load or joint replacement surgery. Many new surgical treatment strategies for cartilage damage have been proposed, which include microfracture, osteochondral grafting, and autologous chondrocyte implantation (17–19). The effectiveness of these treatments in the setting of acute cartilage injury is unknown. MR imaging will be important in evaluation and follow-up of these procedures.

Unfortunately, conventional methods for assessment of the effectiveness of these therapies are limited to clinical evaluation and occasional opportunities for arthroscopic examination. Clinical evaluation is important to track the patient symptoms, but the results correlate poorly with radiographic or even MR imaging data (20). MR imaging offers a noninvasive means of assessing the degree of damage to cartilage and adjacent bone and the effectiveness of treatment (21).

The accepted standard for monitoring cartilage damage and repair is arthroscopy, preferably with full-thickness cartilage biopsy (22). Arthroscopy is both invasive and expensive. Although biopsy may be performed during the arthroscopic procedure, patients are understandably reluctant to undergo biopsy of an area of cartilage repair. Arthroscopy allows visual inspection of the cartilage surface for color changes or fissuring and allows probing of cartilage, which involves using a small metallic probe to apply pressure on the cartilage surface to determine if it is softer than normal (23). Arthroscopy has been used to follow the potential structure-modifying effects of hyaluronic acid injections but in general is too invasive and expensive for large studies (22).

Many imaging methods are available to assess the articular cartilage. Conventional radiography can be used to detect gross loss of cartilage, evident as narrowing of the distance between the bony components of the joint (24,25), but does not image cartilage directly. Secondary changes such as osteophyte or subchondral cyst formation can be seen. Conventional radiography alone is insensitive to early chondral damage (26). Arthrography, alone or combined with conventional radiography, computed tomography, or MR imaging, is also mildly invasive and provides information limited to the contour of the cartilage surface (27).

MR imaging, with its excellent soft-tissue contrast, is the best technique available for assessment of cartilage injury and repair (28–32). Imaging of regions of cartilage damage has the potential to provide morphologic information about the region, such as fissuring and the presence of partial or full-thickness cartilage defects (33). The many tissue parameters that can be measured with MR imaging techniques have the potential to provide physiologic information about cartilage. Ideally, MR imaging of cartilage should provide accurate assessment of cartilage thickness, demonstrate morphologic changes of the cartilage surface, demonstrate changes in internal cartilage signal intensity, and allow evaluation of the subchondral bone for signal intensity abnormalities. In addition, MR imaging has the potential to provide information on cartilage physiology such as glycosaminoglycan content or collagen matrix integrity. Unfortunately, conventional MR imaging sequences are limited in providing a detailed assessment of cartilage, lacking either spatial resolution (34) or information about cartilage physiology.

This article first describes the current state of the art in cartilage imaging, including fat suppression, fast spin-echo (SE), and spoiled gradient-echo (GRE) imaging. Next, advanced methods for fast, high-resolution morphologic imaging of cartilage are described, including driven equilibrium and steady-state imaging. Finally, the article describes several new exciting techniques for imaging the physiology of articular cartilage with MR, including T2 mapping, sodium imaging, diffusion-weighted imaging, and contrast material–enhanced imaging.


   Conventional MR Imaging Methods
Top
 Abstract
 Introduction
 Conventional MR Imaging Methods
New Morphologic Cartilage...
 Physiologic Imaging of Cartilage
 Discussion
 Conclusions
 References
 
Lipid Suppression
Although the tissue relaxation times and imaging parameters are the major determinants of contrast between cartilage and fluid, lipid suppression increases contrast between lipid-containing and non–lipid-containing tissues and affects how the MR imager sets the overall dynamic range of the image. The most common types of lipid suppression include fat saturation, in which fat spins are excited then dephase prior to imaging (Fig 1). Another option is spectral excitation, in which water-only spins are excited, or spectral-spatial excitation, in which only water spins in a section are excited (35,36). Finally, in areas of poor magnetic field homogeneity, inversion recovery provides a way to suppress lipids at the expense of signal-to-noise ratio (SNR).



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  		Figure 1a.  Sagittal three-dimensional (3D) spoiled GRE images of the knee obtained without (a) and with (b) fat suppression. Use of fat suppression or water-only excitation improves the dynamic range settings and allows demonstration of more detail in the cartilage.

 


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  		Figure 1b.  Sagittal three-dimensional (3D) spoiled GRE images of the knee obtained without (a) and with (b) fat suppression. Use of fat suppression or water-only excitation improves the dynamic range settings and allows demonstration of more detail in the cartilage.

 
T1- and T2-weighted SE Imaging
Two-dimensional T1- and T2-weighted SE imaging allows depiction of articular cartilage and can demonstrate defects and gross morphologic changes. T1-weighted images are characterized by excellent intrasubstance anatomic detail of hyaline cartilage (37,38). However, T1-weighted imaging does not show significant contrast between a joint effusion and the cartilage surface, making surface irregularities difficult to detect. Fat suppression adds dynamic range and reduces the effects of chemical shift artifacts (39). T2-weighted imaging demonstrates joint effusions and thus surface abnormalities of cartilage. However, because some components of cartilage have relatively short T2s (40,41), these components are not well depicted.

Fast SE Imaging
Two-dimensional fast SE or turbo SE imaging uses multiple echoes per repetition time to acquire data faster than conventional SE imaging. Proton-density fast SE imaging has been shown to be useful in cartilage imaging and detection of meniscal tears. One disadvantage of proton-density fast SE imaging is blurring of short-T2 species due to acquisition of high spatial frequencies late in the echo train (42). T2-weighted fast SE imaging has been shown to be accurate for detection of cartilage surface lesions and marrow edema (43). Since the cartilage-to-fluid contrast in T2-weighted fast SE imaging is generated at the expense of cartilage signal, this method is less useful for detection of intrasubstance abnormalities. High-resolution proton-density fast SE imaging with long echo trains has been used to image articular cartilage defects and is a promising technique in the clinical setting (44).

Spoiled GRE Imaging
MR imaging of the morphology of cartilage requires close attention to the spatial resolution used. To see subtle damage to cartilage, imaging with resolution on the order of 0.2–0.4 mm is required (34). The ultimate resolution achievable is governed by the SNR possible within a given imaging time and with a given coil. Three-dimensional imaging is ideal for this purpose to avoid partial volume artifacts and accurately measure cartilage thickness and volume (45).

GRE imaging has been used because of its 3D capability and the ability to provide high-resolution images with shorter imaging times than SE imaging. Fat-suppressed 3D spoiled GRE imaging has been shown to be more sensitive than standard MR imaging for detection of hyaline cartilage defects in the knee (Figs 2 –6) (46,47). This method is useful for detection of subchondral osteophytes (Fig 7) but is not sensitive for marrow edema (Fig 4).



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  		Figure 2a.  Focal cartilage contusion after tearing of the anterior cruciate ligament. (a) Sagittal proton-density fast SE image shows a tear of the anterior cruciate ligament (arrow). (b) Image from arthroscopy shows cartilage damage in the lateral femoral condyle (arrow). (c) Sagittal 3D spoiled GRE image shows cartilage step-off in the lateral femoral condyle (arrow). (d) Sagittal fast SE image obtained at the same location shows less detail of the cartilage (arrow).

 


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  		Figure 2b.  Focal cartilage contusion after tearing of the anterior cruciate ligament. (a) Sagittal proton-density fast SE image shows a tear of the anterior cruciate ligament (arrow). (b) Image from arthroscopy shows cartilage damage in the lateral femoral condyle (arrow). (c) Sagittal 3D spoiled GRE image shows cartilage step-off in the lateral femoral condyle (arrow). (d) Sagittal fast SE image obtained at the same location shows less detail of the cartilage (arrow).

 


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  		Figure 2c.  Focal cartilage contusion after tearing of the anterior cruciate ligament. (a) Sagittal proton-density fast SE image shows a tear of the anterior cruciate ligament (arrow). (b) Image from arthroscopy shows cartilage damage in the lateral femoral condyle (arrow). (c) Sagittal 3D spoiled GRE image shows cartilage step-off in the lateral femoral condyle (arrow). (d) Sagittal fast SE image obtained at the same location shows less detail of the cartilage (arrow).

 


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  		Figure 2d.  Focal cartilage contusion after tearing of the anterior cruciate ligament. (a) Sagittal proton-density fast SE image shows a tear of the anterior cruciate ligament (arrow). (b) Image from arthroscopy shows cartilage damage in the lateral femoral condyle (arrow). (c) Sagittal 3D spoiled GRE image shows cartilage step-off in the lateral femoral condyle (arrow). (d) Sagittal fast SE image obtained at the same location shows less detail of the cartilage (arrow).

 


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  		Figure 3a.  Cartilage defect. Sagittal 3D spoiled GRE (a) and T2-weighted fast SE (b) images show a partial-thickness cartilage defect in the medial femoral condyle (solid arrow). Note that fluid (dashed arrow) is dark on the 3D spoiled GRE image (a), whereas it provides an outline of the defect on the T2-weighted fast SE image (b).

 


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  		Figure 3b.  Cartilage defect. Sagittal 3D spoiled GRE (a) and T2-weighted fast SE (b) images show a partial-thickness cartilage defect in the medial femoral condyle (solid arrow). Note that fluid (dashed arrow) is dark on the 3D spoiled GRE image (a), whereas it provides an outline of the defect on the T2-weighted fast SE image (b).

 


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  		Figure 4a.  Focal cartilage contusion in a 17-year-old patient after trauma. (a) Sagittal 3D spoiled GRE image shows a contusion of the medial femoral condyle (arrow). (b) Sagittal fast SE image obtained with fat suppression shows the contusion (solid arrow) and adjacent marrow edema (dashed arrow). Marrow edema is an excellent marker for cartilage damage but is not seen with the relatively T1-weighted spoiled GRE technique.

 


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  		Figure 4b.  Focal cartilage contusion in a 17-year-old patient after trauma. (a) Sagittal 3D spoiled GRE image shows a contusion of the medial femoral condyle (arrow). (b) Sagittal fast SE image obtained with fat suppression shows the contusion (solid arrow) and adjacent marrow edema (dashed arrow). Marrow edema is an excellent marker for cartilage damage but is not seen with the relatively T1-weighted spoiled GRE technique.

 


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  		Figure 5a.  Cartilage fissure after trauma. Sagittal fast SE image obtained without fat suppression (a) and sagittal 3D spoiled GRE image obtained with fat suppression (b) show a cartilage fissure in the lateral patella (arrow). The fissure is outlined by bright synovial fluid on the fast SE image (a), but the underlying cartilage is better seen on the spoiled GRE image (b).

 


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  		Figure 5b.  Cartilage fissure after trauma. Sagittal fast SE image obtained without fat suppression (a) and sagittal 3D spoiled GRE image obtained with fat suppression (b) show a cartilage fissure in the lateral patella (arrow). The fissure is outlined by bright synovial fluid on the fast SE image (a), but the underlying cartilage is better seen on the spoiled GRE image (b).

 


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  		Figure 6a.  Delaminating cartilage injury in a 14-year-old soccer player. (a) Sagittal 3D spoiled GRE image shows delamination of the trochlear cartilage (arrow). (b) Sagittal image obtained adjacent to a shows further delamination (solid arrow). Also seen is a piece of delaminated cartilage in the joint (dashed arrow).

 


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  		Figure 6b.  Delaminating cartilage injury in a 14-year-old soccer player. (a) Sagittal 3D spoiled GRE image shows delamination of the trochlear cartilage (arrow). (b) Sagittal image obtained adjacent to a shows further delamination (solid arrow). Also seen is a piece of delaminated cartilage in the joint (dashed arrow).

 


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  		Figure 7a.  Subchondral osteophyte as a sign of cartilage damage. (a) Anterior radiograph shows a small osteophyte of the lateral femoral condyle (arrow). (b) Sagittal 3D spoiled GRE image shows the osteophyte in an area of cartilage damage (arrow). (c) Sagittal T2-weighted fast SE image shows the osteophyte (arrow). The full thickness of the remaining cartilage is difficult to see due to cartilage signal loss. (Reprinted, with permission, from reference 76.)

 


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  		Figure 7b.  Subchondral osteophyte as a sign of cartilage damage. (a) Anterior radiograph shows a small osteophyte of the lateral femoral condyle (arrow). (b) Sagittal 3D spoiled GRE image shows the osteophyte in an area of cartilage damage (arrow). (c) Sagittal T2-weighted fast SE image shows the osteophyte (arrow). The full thickness of the remaining cartilage is difficult to see due to cartilage signal loss. (Reprinted, with permission, from reference 76.)

 


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  		Figure 7c.  Subchondral osteophyte as a sign of cartilage damage. (a) Anterior radiograph shows a small osteophyte of the lateral femoral condyle (arrow). (b) Sagittal 3D spoiled GRE image shows the osteophyte in an area of cartilage damage (arrow). (c) Sagittal T2-weighted fast SE image shows the osteophyte (arrow). The full thickness of the remaining cartilage is difficult to see due to cartilage signal loss. (Reprinted, with permission, from reference 76.)

 
Although increased sensitivity and spatial resolution are advantages of 3D GRE 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 at GRE imaging, limiting the evaluation of cartilage in some cases.

Evaluation of cartilage thickness and volume in the research setting is commonly performed with fat-suppressed 3D spoiled GRE imaging (48,49). These methods require extremely high resolution (0.3 mm in-plane) and long imaging times. Overall, clinical use of fat-suppressed 3D spoiled GRE techniques has been limited by long imaging times, from 5 minutes at low resolution to 13 minutes for detailed volume and thickness measurements (50,51).


   New Morphologic Cartilage Imaging Techniques
Top
 Abstract
 Introduction
 Conventional MR Imaging Methods
 New Morphologic Cartilage...
Physiologic Imaging of Cartilage
 Discussion
 Conclusions
 References
 
Considerable work in cartilage has been devoted to screening patients with high-resolution 3D imaging techniques. High accuracy for cartilage lesions has been shown with 3D spoiled GRE imaging (46,47). There are two main disadvantages to this approach: lack of reliable contrast between cartilage and fluid that outlines surface defects and long imaging times (about 8 minutes). In addition, fat-suppressed 3D spoiled GRE imaging uses spoiling at the end of each repetition time to reduce artifacts and achieve near T1-weighting. This reduces the overall signal compared with driven equilibrium or steady-state techniques.

Driven Equilibrium Imaging
Driven equilibrium Fourier transform (DEFT) imaging has been used in the past as a method of signal enhancement in spectroscopy (52). The sequence uses a -90° pulse to return magnetization to the z axis, resulting in enhanced signal from tissue with long T1s such as synovial fluid. Unlike in conventional T1- or T2-weighted imaging, the contrast in DEFT imaging is dependent on the ratio of the T1/T2 of a given tissue. This results in bright synovial fluid at short echo and repetition times. At short repetition time, DEFT imaging shows much greater cartilage-to-fluid contrast than spoiled GRE, proton-density fast SE, or T2-weighted fast SE imaging (53,54). The cartilage-to-fluid contrast in DEFT imaging is created by enhancing fluid signal and results in higher cartilage signal than T2-weighted fast SE imaging (Fig 8).



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  		Figure 8a.  DEFT imaging of articular cartilage. (a) Sagittal 3D DEFT image shows a fissure in the patellofemoral cartilage (arrow). (b) Sagittal two-dimensional fast SE image shows the fissure (arrow) with lower cartilage signal. (c) Sagittal 3D DEFT image shows full-thickness cartilage loss in the medial femoral condyle (arrow). (d) Sagittal two-dimensional fast SE image shows the cartilage loss (arrow). DEFT imaging produces bright synovial fluid while maintaining cartilage signal; thus, the remaining cartilage is distinguished from the subchondral bone with DEFT imaging but not with fast SE imaging. (Courtesy of Samuel Fuller, MD, Stanford University, Stanford, Calif.)

 


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  		Figure 8b.  DEFT imaging of articular cartilage. (a) Sagittal 3D DEFT image shows a fissure in the patellofemoral cartilage (arrow). (b) Sagittal two-dimensional fast SE image shows the fissure (arrow) with lower cartilage signal. (c) Sagittal 3D DEFT image shows full-thickness cartilage loss in the medial femoral condyle (arrow). (d) Sagittal two-dimensional fast SE image shows the cartilage loss (arrow). DEFT imaging produces bright synovial fluid while maintaining cartilage signal; thus, the remaining cartilage is distinguished from the subchondral bone with DEFT imaging but not with fast SE imaging. (Courtesy of Samuel Fuller, MD, Stanford University, Stanford, Calif.)

 


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  		Figure 8c.  DEFT imaging of articular cartilage. (a) Sagittal 3D DEFT image shows a fissure in the patellofemoral cartilage (arrow). (b) Sagittal two-dimensional fast SE image shows the fissure (arrow) with lower cartilage signal. (c) Sagittal 3D DEFT image shows full-thickness cartilage loss in the medial femoral condyle (arrow). (d) Sagittal two-dimensional fast SE image shows the cartilage loss (arrow). DEFT imaging produces bright synovial fluid while maintaining cartilage signal; thus, the remaining cartilage is distinguished from the subchondral bone with DEFT imaging but not with fast SE imaging. (Courtesy of Samuel Fuller, MD, Stanford University, Stanford, Calif.)

 


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  		Figure 8d.  DEFT imaging of articular cartilage. (a) Sagittal 3D DEFT image shows a fissure in the patellofemoral cartilage (arrow). (b) Sagittal two-dimensional fast SE image shows the fissure (arrow) with lower cartilage signal. (c) Sagittal 3D DEFT image shows full-thickness cartilage loss in the medial femoral condyle (arrow). (d) Sagittal two-dimensional fast SE image shows the cartilage loss (arrow). DEFT imaging produces bright synovial fluid while maintaining cartilage signal; thus, the remaining cartilage is distinguished from the subchondral bone with DEFT imaging but not with fast SE imaging. (Courtesy of Samuel Fuller, MD, Stanford University, Stanford, Calif.)

 
Steady-State Free Precession Imaging
Steady-state free precession (SSFP) imaging is an efficient, high-signal method for obtaining 3D MR images (55). This method has also been called true FISP imaging (56). With recent advances in MR gradient hardware, it is now possible to use SSFP imaging without the limitations of banding or off-resonance artifacts. The best immunity to off-resonance artifacts when using SSFP is a short repetition time (<5 msec). Longer repetition times, such as 6.6 msec at 1.5 T, can be used with careful shimming of the main magnetic field. Many different methods of SSFP-based imaging are available for imaging cartilage, and all have higher cartilage signal compared with conventional techniques (57).

Fluctuating equilibrium MR (FEMR) imaging is a variant of SSFP imaging that may be useful in imaging cartilage in the knee (58). In FEMR imaging, each phase-encoding step is repeated twice, once with a 90x and once with a 90y. The k-space data are then parsed to form two complete data sets, which are reconstructed into fat and water images. With a repetition time of 6.6 msec, high-resolution 3D imaging of cartilage is possible in about 2 minutes. In imaging the entire knee, FEMR imaging can produce 3D images with a 2-mm section thickness, 512 x 256 matrix, and 16-cm field of view (Fig 9) in a much shorter imaging time than T2-weighted fast SE or fat-suppressed 3D spoiled GRE.



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  		Figure 9a.  High-resolution FEMR imaging of cartilage in the knee. Parameters for all images were 512 x 256, 16-cm field of view, and 2-mm-thick sections. (a) Sagittal T2-weighted fast SE image obtained with interleaving (imaging time, 5:30 [minutes:seconds]). (b) Sagittal 3D spoiled GRE image obtained with fat suppression (imaging time, 8:56). (c) Sagittal FEMR water image (imaging time, 2:43). (d) Sagittal FEMR lipid image. The cartilage signal on the spoiled GRE image (b) and FEMR images (c, d) is nearly identical despite the much longer imaging time for spoiled GRE imaging (8:56 vs 2:43). The cartilage signal with fast SE imaging is much lower than with FEMR or spoiled GRE imaging.

 


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  		Figure 9b.  High-resolution FEMR imaging of cartilage in the knee. Parameters for all images were 512 x 256, 16-cm field of view, and 2-mm-thick sections. (a) Sagittal T2-weighted fast SE image obtained with interleaving (imaging time, 5:30 [minutes:seconds]). (b) Sagittal 3D spoiled GRE image obtained with fat suppression (imaging time, 8:56). (c) Sagittal FEMR water image (imaging time, 2:43). (d) Sagittal FEMR lipid image. The cartilage signal on the spoiled GRE image (b) and FEMR images (c, d) is nearly identical despite the much longer imaging time for spoiled GRE imaging (8:56 vs 2:43). The cartilage signal with fast SE imaging is much lower than with FEMR or spoiled GRE imaging.

 


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  		Figure 9c.  High-resolution FEMR imaging of cartilage in the knee. Parameters for all images were 512 x 256, 16-cm field of view, and 2-mm-thick sections. (a) Sagittal T2-weighted fast SE image obtained with interleaving (imaging time, 5:30 [minutes:seconds]). (b) Sagittal 3D spoiled GRE image obtained with fat suppression (imaging time, 8:56). (c) Sagittal FEMR water image (imaging time, 2:43). (d) Sagittal FEMR lipid image. The cartilage signal on the spoiled GRE image (b) and FEMR images (c, d) is nearly identical despite the much longer imaging time for spoiled GRE imaging (8:56 vs 2:43). The cartilage signal with fast SE imaging is much lower than with FEMR or spoiled GRE imaging.

 


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  		Figure 9d.  High-resolution FEMR imaging of cartilage in the knee. Parameters for all images were 512 x 256, 16-cm field of view, and 2-mm-thick sections. (a) Sagittal T2-weighted fast SE image obtained with interleaving (imaging time, 5:30 [minutes:seconds]). (b) Sagittal 3D spoiled GRE image obtained with fat suppression (imaging time, 8:56). (c) Sagittal FEMR water image (imaging time, 2:43). (d) Sagittal FEMR lipid image. The cartilage signal on the spoiled GRE image (b) and FEMR images (c, d) is nearly identical despite the much longer imaging time for spoiled GRE imaging (8:56 vs 2:43). The cartilage signal with fast SE imaging is much lower than with FEMR or spoiled GRE imaging.

 
The contrast produced with SSFP sequences is favorable for cartilage imaging. As with DEFT, FEMR produces contrast based on the ratio of T1/T2 in tissues. This results in bright fluid signal while preserving cartilage signal. The largest disadvantage of FEMR and SSFP techniques is sensitivity to off-resonance artifacts.

Another similar approach that may provide more reliable fat suppression at high resolution is Dixon SSFP imaging (59). This technique is faster and can provide more reliable fat suppression than fat-suppressed 3D spoiled GRE imaging. Dixon SSFP imaging may be especially useful at high field strength (Fig 10), where field homogeneity can be challenging.



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  		Figure 10a.  Sagittal Dixon SSFP imaging of the ankle joint at 3.0 T. Parameters for all images were 256 x 256, 18-cm field of view, and 2-mm-thick sections. (a) Dixon SSFP water image (imaging time, 2:18). (b) Dixon SSFP lipid image. (c) Three-dimensional spoiled GRE image obtained with fat suppression (imaging time, 7:40). Note that the fat suppression is much more homogeneous on the Dixon SSFP image (a) than on the spoiled GRE image obtained with conventional fat suppression (c). (Courtesy of Scott Reeder, MD, PhD, Stanford University, Stanford, Calif.)

 


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  		Figure 10b.  Sagittal Dixon SSFP imaging of the ankle joint at 3.0 T. Parameters for all images were 256 x 256, 18-cm field of view, and 2-mm-thick sections. (a) Dixon SSFP water image (imaging time, 2:18). (b) Dixon SSFP lipid image. (c) Three-dimensional spoiled GRE image obtained with fat suppression (imaging time, 7:40). Note that the fat suppression is much more homogeneous on the Dixon SSFP image (a) than on the spoiled GRE image obtained with conventional fat suppression (c). (Courtesy of Scott Reeder, MD, PhD, Stanford University, Stanford, Calif.)

 


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  		Figure 10c.  Sagittal Dixon SSFP imaging of the ankle joint at 3.0 T. Parameters for all images were 256 x 256, 18-cm field of view, and 2-mm-thick sections. (a) Dixon SSFP water image (imaging time, 2:18). (b) Dixon SSFP lipid image. (c) Three-dimensional spoiled GRE image obtained with fat suppression (imaging time, 7:40). Note that the fat suppression is much more homogeneous on the Dixon SSFP image (a) than on the spoiled GRE image obtained with conventional fat suppression (c). (Courtesy of Scott Reeder, MD, PhD, Stanford University, Stanford, Calif.)

 
A final steady-state method of cartilage imaging that is useful at 3.0 T is SSFP imaging with intermittent fat saturation. This technique preserves the SNR advantage of SSFP imaging but provides uniform fat saturation, even at high field strength (Fig 11). One problem with fat-saturated SSFP imaging is possible artifacts from coming in and out of the steady state to apply the fat saturation pulses. The overall SNR efficiency and speed of the SSFP-based techniques make them very attractive for routine morphologic cartilage imaging.



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  		Figure 11a.  Sagittal fat-saturated SSFP imaging of the knee at 3.0 T. Parameters for both images were 512 x 384, 16-cm field of view, and 1-mm-thick sections. (a) Fat-saturated SSFP image shows a cartilage SNR of 21 (imaging time, 5:44). (b) Three-dimensional fat-suppressed GRE image shows a cartilage SNR of 7 (imaging time, 5:45). The higher SNR efficiency of steady-state techniques makes them appealing for high-resolution cartilage imaging.

 


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  		Figure 11b.  Sagittal fat-saturated SSFP imaging of the knee at 3.0 T. Parameters for both images were 512 x 384, 16-cm field of view, and 1-mm-thick sections. (a) Fat-saturated SSFP image shows a cartilage SNR of 21 (imaging time, 5:44). (b) Three-dimensional fat-suppressed GRE image shows a cartilage SNR of 7 (imaging time, 5:45). The higher SNR efficiency of steady-state techniques makes them appealing for high-resolution cartilage imaging.

 

   Physiologic Imaging of Cartilage
Top
 Abstract
 Introduction
 Conventional MR Imaging Methods
 New Morphologic Cartilage...
 Physiologic Imaging of Cartilage
Discussion
 Conclusions
 References
 
Composition of Articular Cartilage
Articular cartilage is approximately 70% water by weight. The remainder of the tissue consists predominately of type II collagen fibers and glycosaminoglycans. The glycosaminoglycans contain negative charges that attract sodium ions (Na+) in intact cartilage. The collagen fibers have an ordered structure, making the water associated 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 glycosaminoglycan matrices are intact. These physiologic imaging approaches complement the morphologic imaging approaches outlined earlier.

T2 Mapping
The T2 of articular cartilage is a function of the water content of the tissue. Measurement of the spatial distribution of the T2 may reveal areas of increased or decreased water content, which correlate with cartilage damage (60). To measure the T2 with a high degree of accuracy, care must be take with the MR imaging technique (61). Recent studies have shown that a multiecho, multisection SE sequence should be used with care, since substantial inaccuracy can occur due to cross talk among sections (62). Typically, a multiecho SE technique is used and signal levels are fitted to one or more decaying exponentials, depending on whether it is thought that there is more than one distribution of T2 within the sample (63). An image of the T2 is then generated, with a color map or gray scale representing the relaxation time.

Several investigators have measured the spatial distribution of T2s within cartilage, both at 1.5 T and 3.0 T (64). Aging appears to be associated with a symptomatic increase in T2s in the transitional zone (65). Relaxation time measurements have also been shown to be anisotropic with respect to orientation in the main magnetic field (66,67). Focal increases in T2 within cartilage have been associated with matrix damage, particularly loss of the collagen matrix. However, in view of the intrinsic heterogeneity of T2, further work is needed to determine whether T2 mapping can be sufficiently specific to monitor disease or treatment-related changes in the cartilage matrix over time.

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 glycosaminoglycan depletion (68,69). The concentration of Na-23 in normal human cartilage is about 320 µM, with T2s between 2 and 10 msec (70). The combination of lower resonant frequency, lower concentration, and shorter T2s than H-1 make in vivo imaging of Na-23 challenging. Sodium imaging requires the use of special transmit and receive coils as well as relatively long imaging times to achieve adequate SNR.

Na-23 atoms are associated with the high fixed-charge density present in glycosaminoglycan sulfate and carboxylate groups. Some spatial variation in Na-23 concentration is present in normal cartilage (70). In cartilage samples, sodium imaging has been shown to be sensitive to small changes in glycosaminoglycan concentration. This method shows promise to be sensitive to early decreases in glycosaminoglycan concentration in osteoarthritis.

Diffusion-weighted Imaging
Imaging the diffusion of water through articular cartilage is also possible with MR imaging. Diffusion-weighted imaging of cartilage has been demonstrated in vitro to be sensitive to early cartilage degradation (71). Diffusion measurements are accomplished by application of diffusion-sensitizing gradients. These gradients cause phase accrual in the spins of the tissue, which is then reversed and reduced to zero if the spins are stationary. However, water undergoing diffusion 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.

In vivo diffusion-weighted imaging of cartilage poses several challenges. The T2 of cartilage varies from 10 to 50 msec, so the echo time must be short to maximize cartilage signal. Diffusion-sensitizing gradients increase the echo time and render the sequence sensitive to motion. Single-shot techniques have been used for diffusion-weighted imaging, but these are limited by relatively low SNR and spatial resolution. Multiple acquisitions improve the SNR and resolution, but motion correction is required for accurate reconstruction. A promising new technique for diffusion imaging of cartilage in vivo is based on steady-state imaging (Fig 12), which produces excellent diffusion-weighted images of cartilage in reasonable imaging times. Further testing of diffusion-weighted imaging in vivo will be needed to determine its sensitivity to changes in the cartilage matrix.



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  		Figure 12a.  Axial steady-state diffusion-weighted images of the patellofemoral cartilage in a healthy volunteer, obtained with effective b values (beff) of 115 (a), 350 (b), and 630 (c) sec/mm2. Imaging is performed with three levels of diffusion weighting (effective b value), and navigation is performed to minimize the effects of motion. Note the decreasing signal for cartilage as free water is suppressed at higher b values. Diffusion-weighted imaging may allow early demonstration of breakdown of the collagen matrix. (Courtesy of Karla Miller, Stanford University, Stanford, Calif.)

 


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  		Figure 12b.  Axial steady-state diffusion-weighted images of the patellofemoral cartilage in a healthy volunteer, obtained with effective b values (beff) of 115 (a), 350 (b), and 630 (c) sec/mm2. Imaging is performed with three levels of diffusion weighting (effective b value), and navigation is performed to minimize the effects of motion. Note the decreasing signal for cartilage as free water is suppressed at higher b values. Diffusion-weighted imaging may allow early demonstration of breakdown of the collagen matrix. (Courtesy of Karla Miller, Stanford University, Stanford, Calif.)

 


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  		Figure 12c.  Axial steady-state diffusion-weighted images of the patellofemoral cartilage in a healthy volunteer, obtained with effective b values (beff) of 115 (a), 350 (b), and 630 (c) sec/mm2. Imaging is performed with three levels of diffusion weighting (effective b value), and navigation is performed to minimize the effects of motion. Note the decreasing signal for cartilage as free water is suppressed at higher b values. Diffusion-weighted imaging may allow early demonstration of breakdown of the collagen matrix. (Courtesy of Karla Miller, Stanford University, Stanford, Calif.)

 
Contrast-enhanced Imaging
Delayed contrast-enhanced MR imaging of cartilage shows great promise for evaluating the cartilage matrix (72). Delayed gadolinium-enhanced imaging shows promise in mapping the distribution of glycosaminoglycans in cartilage, which may have important implications for longitudinal evaluations of cartilage (73). This technique works by allowing negatively charged gadolinium–diethylenetriamine pentaacetic acid (DTPA)2- to distribute in cartilage in inverse proportion to the negatively charged glycosaminoglycans. Double-dose Gd-DTPA2- is injected intravenously, and a delay of 90 minutes is used to allow the contrast material to diffuse into the cartilage.

Multiple inversion-recovery acquisitions are performed to calculate a map of the T1s in the cartilage, which reflects the underlying glycosaminoglycan content. Areas of glycosaminoglycan depletion can be seen (Fig 13), which correlate with the histologic appearance. The ability to monitor glycosaminoglycan content in a cartilage repair site may be helpful in determining the physiologic state of the repair (Fig 14) (74). This technique requires careful attention to protocol issues but has good reproducibility and holds promise for demonstrating early changes of osteoarthritis (75).



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  		Figure 13.  Quantitative evaluation of glycosaminoglycan content in cartilage with delayed gadolinium-enhanced imaging. Top: Delayed gadolinium-enhanced image maps T1 to glycosaminoglycan (GAG) content and shows a focal area of low glycosaminoglycan concentration (arrow). Bottom: Photograph of the specimen after staining with toluidine blue shows a focal area of cartilage damage (arrow). (Reprinted, with permission, from reference 73.)

 


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  		Figure 14a.  Delayed gadolinium-enhanced imaging after autologous chondrocyte implantation. GAG = glycosaminoglycan. (a) Coronal image obtained 2 months after implantation shows decreased glycosaminoglycan content (arrow) in part of the implant. (b) Sagittal image obtained 15 months after implantation shows almost normal levels of glycosaminoglycan (arrow) in part of the implant. This example shows the potential of MR imaging for monitoring the glycosaminoglycan content in a cartilage repair site over time. (Reprinted, with permission, from reference 74.)

 


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  		Figure 14b.  Delayed gadolinium-enhanced imaging after autologous chondrocyte implantation. GAG = glycosaminoglycan. (a) Coronal image obtained 2 months after implantation shows decreased glycosaminoglycan content (arrow) in part of the implant. (b) Sagittal image obtained 15 months after implantation shows almost normal levels of glycosaminoglycan (arrow) in part of the implant. This example shows the potential of MR imaging for monitoring the glycosaminoglycan content in a cartilage repair site over time. (Reprinted, with permission, from reference 74.)

 

   Discussion
Top
 Abstract
 Introduction
 Conventional MR Imaging Methods
 New Morphologic Cartilage...
 Physiologic Imaging of Cartilage
 Discussion
Conclusions
 References
 
MR imaging provides a powerful tool for the imaging and understanding of articular cartilage. Improvements have been made in imaging of cartilage in routine clinical cases, in terms of both contrast and resolution. New MR imaging sequences promise to improve the speed and resolution of clinical imaging even further and make specialized cartilage examination a part of routine knee imaging.

Much progress has been made in the understanding of cartilage physiology and the ability to detect glycosaminoglycan and collagen loss. Integration of biomechanical models with cartilage imaging shows promise to improve our understanding of the forces and stresses involved in everyday use of articular cartilage. The unique contrast mechanisms provided by MR imaging are poised to allow in-depth investigation into cartilage physiology. At present, techniques such as delayed gadolinium-enhanced imaging and T2 mapping are limited in application due to long acquisition times. Continued work to validate the underlying basis for contrast and to provide robust protocols for routine clinical implementation is ongoing.

The fundamental trade-off between image resolution and SNR still limits our ability to image cartilage in vivo with high resolution in an efficient manner. Patient motion may ultimately limit the resolution achievable at 1.5 T, so higher-field-strength systems such as 3.0-T systems may be required. The speed of acquisition of morphologic images needs to be improved, along with the speed of acquisition of T2 maps, delayed gadolinium-enhanced images, and images of other biochemical markers for cartilage. In the future, a 30-minute examination of cartilage in a patient with osteoarthritis may well consist of a fast morphologic imaging technique such as FEMR imaging followed by a fast T2 mapping sequence and a rapid version of delayed gadolinium-enhanced imaging. This kind of examination could provide a wealth of information about the health of the articular cartilage in a reasonable imaging time.


   Conclusions
Top
 Abstract
 Introduction
 Conventional MR Imaging Methods
 New Morphologic Cartilage...
 Physiologic Imaging of Cartilage
 Discussion
 Conclusions
References
 
MR imaging is a powerful tool for evaluation of articular cartilage. New methods under development promise to further refine and enhance our ability to characterize both the morphology and biochemical content of cartilage. Application of these methods in a clinical environment is challenging but holds promise to evaluate cartilage function as well. These new methods will be important in the evaluation of new treatments for acute cartilage damage in the younger population and for structure-modifying therapies in osteoarthritis in the older population. Overall, the future of MR imaging of articular cartilage is promising, with much work to be done and improvements to be made in the existing techniques.


   Acknowledgments
 
We acknowledge the help of General Electric Applied Sciences West Laboratory and the Lucas Center for MRI in acquisition of the 3-T images.


   Footnotes
 
Abbreviations: DEFT = driven equilibrium Fourier transform, FEMR = fluctuating equilibrium MR, GRE = gradient echo, SE = spin echo, SNR = signal-to-noise ratio, SSFP = steady-state free precession, 3D = three-dimensional


   References
Top
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 Introduction
 Conventional MR Imaging Methods
 New Morphologic Cartilage...
 Physiologic Imaging of Cartilage
 Discussion
 Conclusions
 References
 

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