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Orthop Clin N Am 37 (2006) 331–347

Advanced Magnetic Resonance Imaging


of Articular Cartilage
Garry E. Gold, MD*, Brian A. Hargreaves, PhD,
Kathryn J. Stevens, MD, Christopher F. Beaulieu, MD, PhD
Department of Radiology, Stanford University, 300 Pasteur Drive S0-56, Stanford, CA 94305-9510, USA

Articular cartilage pathology may be the result MRI techniques have the potential to provide bio-
of degeneration or acute injury. Osteoarthritis is chemical and physiologic information about carti-
an important cause of disability in society [1–5] lage [13].
and is primarily a disease of articular cartilage An ideal MRI study for cartilage should pro-
[6–8]. Acute injury to cartilage may be character- vide accurate assessment of cartilage thickness
ized using MRI [9]. Whether the result of degener- and volume, show morphologic changes of the
ation or injury, MRI offers a noninvasive means cartilage surface, show internal cartilage signal
of assessing the degree of damage to cartilage changes, and allow evaluation of the subchondral
and adjacent bone and measuring the effectiveness bone for signal abnormalities. Also desirable
of treatment. would be an evaluation of the underlying cartilage
Many imaging methods are available to assess physiology, including the status of the proteogly-
articular cartilage. Conventional radiography can can and collagen matrices. Conventional MRI
be used to detect gross loss of cartilage, evident as sequences in current clinical use do not provide
narrowing of the distance between the bony a comprehensive assessment of cartilagedlacking
components of the joint [10], but it does not image in spatial resolution [17] or specific information
cartilage directly. Secondary changes, such as os- about cartilage physiology or requiring impracti-
teophyte formation, can be seen, but conventional cally long scan times for such assessments.
radiography is insensitive to early chondral dam-
age. Arthrography, alone or combined with con-
Conventional magnetic resonance imaging
ventional radiography or CT, is mildly invasive
methods
and provides information limited to the contour
of the cartilage surface [11]. MRI has emerged as the leading method of
MRI, with its excellent soft tissue contrast, is imaging soft tissue structures around joints [18].
the best technique currently available for assess- A major advantage of MRI is the ability to ma-
ment of articular cartilage [12–16]. Imaging of re- nipulate contrast to highlight tissue types. The
gions of cartilage damage has the potential to common contrast mechanisms used in MRI are
provide morphologic information about the re- two-dimensional or multislice T1-weighted, pro-
gion, such as fissuring, and presence of partial- ton density, and T2-weighted imaging, with or
thickness or full-thickness cartilage defects. The without fat suppression. Imaging hardware and
many tissue parameters that can be measured by software have changed considerably over time,
including improved gradients and radiofrequency
This article was supported by NIH grants
coils, fast or turbo spin echo imaging, and tech-
EB002524 and EB005790 and the Whitaker niques such as water-only excitation.
Foundation. Although the tissue relaxation times and
* Corresponding author. imaging parameters are the major determinants
E-mail address: gold@stanford.edu (G.E. Gold). of contrast between cartilage and fluid, lipid
0030-5898/06/$ - see front matter Ó 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.ocl.2006.04.006 orthopedic.theclinics.com
332 GOLD et al

Fig. 1. Axial images showing degrees of patella cartilage damage. (A) Axial intermediate-weighted FSE image shows
superficial fibrillation and signal changes in the patellar cartilage (arrow). (B) Axial T2-weighted FSE image shows mar-
row edema at the same location (arrow). (C) Axial intermediate-weighted FSE image shows fissuring involving approx-
imately 50% of the thickness of the cartilage (arrow). (D) Axial intermediate-weighted FSE image shows a full-thickness
cartilage fissure in the patella (arrow).

suppression increases contrast between non– cartilage and synovial fluid, it does so at the
lipid-containing and lipid-containing tissues and expense of cartilage signal. The high signal from
affects how the MRI scanner sets the overall fluid is useful to highlight surface defects, such as
dynamic range of the image. The most common fibrillation or fissuring, but variation in internal
type of lipid suppression is fat saturation, in cartilage signal is poorly depicted. These scans
which fat spins are excited then dephased before also are often two-dimensional in nature, leaving
imaging. Another option is spectral-spatial exci- a small gap between slices, which may miss small
tation, in which only water spins in a slice are areas of cartilage damage.
excited [19]. Finally, in areas of magnetic field Three-dimensional spoiled gradient recalled
inhomogeneity, inversion recovery provides echo imaging with fat suppression (SPGR) pro-
a way to suppress lipids at the expense of signal- duces high cartilage signal, but low signal from
to-noise ratio (SNR) and contrast-to-noise ratio. adjacent joint fluid. Currently, this technique is the
The type of contrast material used in cartilage standard for quantitative morphologic imaging of
imaging is crucial to the visibility of lesions and cartilage [20–22]. Three-dimensional SPGR is
the SNR of the cartilage itself. Although T2- useful for cartilage volume and thickness measure-
weighted imaging creates contrast between ments, but does not highlight adequately surface
ADVANCED MRI OF ARTICULAR CARTILAGE 333

Fig. 2. FSE images of a cartilage fragment from the patella cartilage with full-thickness loss (arrows). (A) Axial inter-
mediate-weighted FSE image shows the cartilage fragment. (B) Sagittal intermediate-weighted image without fat sup-
pression. (C) Sagittal T2-weighted image with fat suppression shows edema in the patella and the fragment (arrow).

defects with fluid and does not allow thorough eval- Two-dimensional fast spin echo imaging
uation of other joint structures, such as ligaments
Currently, imaging of the musculoskeletal
or menisci.
system with MRI is often limited to two-dimen-
MRI of cartilage requires close attention to
sional multislice acquisitions acquired in multiple
imaging spatial resolution. To see degenerating
planes. This imaging is commonly done with turbo
cartilage, imaging with resolution on the order of
or fast spin echo (FSE) methods. These methods
0.2 to 0.4 mm is required [17]. The ultimate reso-
provide excellent SNR and contrast between
lution achievable is governed by the SNR possible
tissues of interest, but the inherently anisotropic
within a given imaging time and with a given ra-
voxels in these two-dimensional acquisitions re-
diofrequency coil. Ultimately, a high-resolution
quire that multiple planes of data be acquired to
imaging technique that combines morphologic
minimize partial-volume artifacts. A typical sagit-
and physiologic information would be ideal in
tal image may have 0.3 to 0.6 mm in plane
the evaluation of osteoarthritis. Given current
resolution, but a slice thickness of 3 to 5 mm.
techniques, it is likely that a combination of
FSE techniques show excellent results in detection
a high-resolution morphologic imaging sequence
of cartilage lesions (Figs. 1 and 2) [23]. These
with a sequence for matrix evaluation would be
methods provide excellent depiction of structures
the most useful.
in the imaging plane, but evaluation of oblique
334 GOLD et al

or small structures across multiple slices can be enhancement in spectroscopy [33]. The sequence
challenging. For these reasons, three-dimensional uses a 90-degree pulse to return magnetization
acquisitions with thin sections are appealing. to the z-axis, increasing signal from tissue with
long T1 relaxation times, such as synovial fluid.
Three dimensional gradient echo techniques In contrast to conventional T1-weighted or T2-
weighted MRI, the contrast in DEFT depends
Traditional three-dimensional gradient echo on the ratio of the T1 to T2 of a given tissue.
(GRE) methods have the potential to acquire For musculoskeletal imaging, DEFT produces
data with more isotropic voxel sizes, but have contrast by enhancing the signal from synovial
a lack of contrast compared with spin echo fluid, rather than attenuation of cartilage signal as
approaches. High accuracy for cartilage lesions in T2-weighted sequences. Bright synovial fluid
has been shown with three-dimensional SPGR results at short repetition times (TR). At short
imaging [24–26]. There are two main disadvan- TR, DEFT shows much greater cartilage-to-fluid
tages to this approach: (1) lack of reliable contrast contrast than SPGR, proton density FSE, or T2-
between cartilage and fluid that outlines surface weighted FSE [34].
defects, and (2) long imaging times (approxi- DEFT imaging has been combined with
mately 8 minutes). In addition, SPGR uses gradi- a three-dimensional echo-planar readout to
ent and radiofrequency spoiling to reduce artifacts make it an efficient three-dimensional cartilage
and achieve near T1 weighting; this reduces the imaging technique. In DEFT, there is no blurring
overall signal compared with steady-state tech- of high spatial frequencies such as in proton
niques. Despite these limitations, three-dimen- density FSE [35]. In contrast to T2-weighted
sional SPGR is considered the standard for FSE, cartilage signal is preserved because of the
morphologic imaging of cartilage [20,27]. short echo time (TE). A high-resolution three-
SPGR and GRE techniques produce excellent dimensional data set of the entire knee using
quality images with high resolution (0.3  0.6  512  192 matrix, 14 cm field of view (FOV), and
1.5 mm) [28]. The SPGR method suppresses signal 3-mm slices can be acquired in about 6 minutes.
from joint fluid, whereas the GRE method accen- Initial studies of cartilage morphology have been
tuates it. Compared with balanced steady-state done using DEFT imaging [36,37], but this tech-
free precession (bSSFP), which is described later nique has not been conclusively proven superior
in greater detail, these methods are less SNR effi- to two-dimensional approaches. A sequence simi-
cient, but also less sensitive to magnetic field inho- lar to DEFT that has been used in musculoskele-
mogeneity. An ideal three-dimensional cartilage tal imaging is FSE with driven equilibrium pulses,
imaging sequence that provides an optimal combi- referred to as DRIVE [38].
nation of resolution, SNR efficiency, and minimal
artifacts has yet to be established. As such, many
newer techniques have been established to im- Balanced steady-state free precession imaging
prove cartilage imaging. bSSFP MRI is an efficient, high signal method
for obtaining three-dimensional MRI images [39].
Depending on the manufacturer of the MRI scan-
New magnetic resonance imaging methods ner, this method also has been called True-FISP
(Siemens Medical Solutions, Malvern, PA),
Dual-echo steady-state imaging FIESTA (General Electric Healthcare, Waukesha,
Dual-echo steady-state imaging (DESS) has WI), or Balanced FFE imaging (Phillips Medical
proved useful for evaluation of cartilage morphol- Systems, Andover, MA) [40]. With advances in
ogy [29–32]. This technique acquires two gradient MRI gradient hardware, it is now possible to use
echoes separated by a refocusing pulse, then com- bSSFP without the banding or off-resonance arti-
bines both echoes into the image. An image results facts that were previously a problem with this
with higher T2 weighting, which has bright carti- method. Banding artifacts resulting from off-
lage signal and bright synovial fluid. resonance are still an issue, however, as repetition
time increases, or at 3 Tesla (T). TR usually is
kept at less than 10 ms with these techniques, which
Driven equilibrium Fourier transform imaging
limits overall image resolution. Multiple acquisi-
Driven equilibrium Fourier transform (DEFT) tion bSSFP can be used to achieve higher resolution
has been used in the past as a method of signal [41,42] at the cost of additional scan time.
ADVANCED MRI OF ARTICULAR CARTILAGE 335

Fig. 3. Two sagittal images from the knee of a normal volunteer. (A) FEMR, scan time 2:43 minutes. (B) SPGR, scan
time 8:56 minutes. Both scans were done at the same spatial resolution (512  256, 2-mm slice thickness) and have sim-
ilar SNR. The higher SNR efficiency of FEMR allows a similar morphologic scan to be acquired in a much shorter time.
(From Gold GE, Hargreaves BA, Vasanawala SS, et al. Articular cartilage of the knee: evaluation with fluctuating equi-
librium MR imagingdinitial experience in healthy volunteers. Radiology 2006;238:712–8; with permission.)

Fat suppression in balanced steady-state free suppression [46] uses transient suppression methods
precession imaging to provide intermittent fat saturation pulses and
suppress lipid signal. Iterative decomposition of wa-
Many methods have been proposed to provide
ter and fat with echo asymmetry and least-squares
fat suppression with bSSFP imaging. If the repeti-
estimation (IDEAL) uses multiple acquisitions to
tion time is sufficiently short and the magnetic
separate fat and water, but does not depend on the
field homogeneous, conventional fat suppression
fat-water frequency difference to constrain the rep-
or water excitation pulses can be used [43]. Linear
etition time [47]. Rapid separation of water and
combinations of bSSFP [44] and fluctuating
fat can be achieved with phase detection [48,49].
equilibrium MRI (FEMR) [45] use the frequency
Fat and water separation also has been achieved
difference between fat and water and multiple acqui-
with phase detection and a radial acquisition
sitions to separate fat and water. Intermittent fat
method using multiple echoes [50,51].

Fig. 4. bSSFP images of the knee of a normal volunteer acquired using IDEAL bSSFP. (A) Water image. (B) Fat image.
Joint fluid is bright in A using this bSSFP technique. (From Gold GE, Reeder SB, Yu H, et al. Rapid 3D cartilage MR
imaging at 3.0 T with IDEAL-SSFP: initial experience. Radiology 2006;240: in press. DOI:10.1148/radiol.2402050288;
with permission.)
336 GOLD et al

Fig. 5. Phase-sensitive bSSFP images from the knee of a normal volunteer. This is from a three-dimensional dataset ac-
quired with fat and water separation with 0.625  0.625  2 mm resolution in 90 seconds.

Fluctuating equilibrium magnetic resonance high-resolution FEMR is shown in Fig. 3 com-


imaging pared with a three-dimensional SPGR image
that took almost 9 minutes to acquire.
FEMR is a variant of bSSFP that may be
useful in imaging cartilage [45]. Similar to DEFT,
Linear combinations of balanced steady-state
FEMR and other bSSFP-based sequences pro-
free precession and fat-suppressed steady-state
duce contrast based on the ratio of T1 to T2 in tis-
free precession
sues. With appropriate choice of flip angle, bright
fluid signal results, while preserving cartilage sig- Other bSSFP approaches may provide more
nal. In scanning the entire knee, FEMR can pro- reliable fat suppression at high resolution than
duce three-dimensional images with a 2-mm slice FEMR. These methods include linear combina-
thickness, 512  256 matrix over a 16 cm FOV tion bSSFP [44], which uses multiple acquisitions
in about 2 minutes and 30 seconds [52]. The TR to create fat and water images, and fat-suppressed
was set at 6.6 ms at 1.5 T, which can be used for bSSFP, which uses intermittent fat saturation
fat-water separation with careful shimming to pulses with preparation pulses that allow transi-
minimize artifacts. An example water image using tions in and out of the steady state [53].
ADVANCED MRI OF ARTICULAR CARTILAGE 337

Fig. 6. IDEAL SPGR and GRE images at 3 T. (A) IDEAL SPGR image. (B) IDEAL GRE image, flip angle 14 . (C)
IDEAL GRE, flip angle 25 . Increasing the flip angle increases contrast between synovial fluid and articular cartilage.

Iterative decomposition of water and fat resonance frequency is periodic. The periodicity
with echo asymmetry and least-squares estimation decreases with decreasing TR, resulting in less
steady-state free precession field inhomogeneity sensitivity [48]. Voxels are as-
signed to water or fat to form two separate im-
Another approach to fat-water separation that
ages. This method is a rapid means of fat-water
is relatively insensitive to field variations combines
separation using bSSFP, not requiring additional
IDEAL with bSSFP [54]. Example knee images
acquisitions or saturation pulses [49]. One draw-
using this technique are shown in Fig. 4. Excellent
back to this approach is partial volume artifact,
separation of fat and water are seen, with little off-
as pixels are assigned as either fat or water, so
resonance artifact [55]. This method works at 1.5
high resolution is required. Example images of
T and 3 T.
this method are shown in Fig. 5. These images
show a three-dimensional, fat-suppressed data
Phase-sensitive balanced steady-state free
set of an entire knee that can be acquired with
precession imaging
0.625  0.625  2 mm resolution in about 90 sec-
Phase-sensitive bSSFP employs an bSSFP se- onds. In a limited study, phase-sensitive bSSFP
quence with the TE restricted to be half of the TR. was sensitive to marrow edema and meniscal tears
The spectral response of the signal with respect to in a similar manner to FSE imaging [49].
338 GOLD et al

Fig. 7. VIPR bSSFP imaging of the knee at 1.5 T. This SSFP-based technique produces isotropic 0.7-mm resolution
across the knee, allowing reformations in any imaging plane. Scan time was only 5 minutes. (A) Coronal image with
cartilage defect (arrow). (B) Sagittal reformation with cartilage defect (arrow) and the meniscus (arrowhead). (Courtesy
of R. Kijowski and W. Block, University of Wisconsin, Madison.)

Vastly interpolated projection reconstruction and cartilage damage [56]. Contrast between the
imaging cartilage and bone is generated by separating fat
and water with linear combinations of bSSFP,
Imaging of the knee with a combination of
as shown in Fig. 6. Scan time for the isotropic
a three-dimensional radial k-space acquisition and
acquisition was only 5 minutes. An alternative
bSSFP has several advantages. Three-dimensional
single-pass method separates fat and water by
radial acquisitions are often undersampled in
exploiting the different phase progression of fat
sparse, high contrast imaging environments, such
and water spins between the two echoes acquired
as contrast-enhanced magnetic resonance angiog-
each TR [51]. At 3 T, fat and water separation is
raphy, to decrease imaging time. Vastly interpo-
achieved by using an alternative fat stopband
lated projection reconstruction (VIPR), first
with a TR of 3.6 ms. Here the multiple echo acqui-
developed for time-resolved contrast-enhanced
sition allows for the removal of the unwanted
magnetic resonance angiography [50], was later
passband between the water and fat resonance
adapted for bSSFP imaging of the musculoskele-
frequencies at the longer TR [57].
tal system. Instead of using the radial trajectory
to undersample in musculoskeletal imaging, the
radial acquisition allows for a very efficient
High field magnetic resonance imaging
k-space trajectory that collects two radial lines
each TR without wasting time on frequency de- High-field MRI may enable the acquisition of
phasing and rephasing gradients. One radial line morphologic images at spatial resolutions that
begins at the k-space origin, while the other is ac- cannot be achieved in a reasonable scan time at
quired along a different return path to the origin, 1.5 T. Currently, 3 T MRI units are available that,
allowing acquisition to occur during nearly the en- theoretically, have twice the SNR of 1.5 T
tire TR. The optimal TR needed for the most effi- scanners. In addition, the increased chemical shift
cient implementation of linear combinations of allows for shorter fat suppression or water exci-
bSSFP at 1.5 T (2.4 ms) can be met while still tation pulses, improving the speed of three-
having time for adequate spatial encoding. dimensional SPGR and three-dimensional GRE
Application of VIPR to the knee provides scans. IDEAL fat-water separation also is avail-
isotropic 0.5- to 0.7-mm three-dimensional imag- able at 3 T [58,59] with SPGR and GRE imaging,
ing that allows for reformations in arbitrary as shown in Fig. 7. Also available are fat, water,
planes. Because this method is based on bSSFP, and combined images that are corrected for chem-
joint fluid is bright, providing excellent contrast ical shift [60]. This method could be used to mea-
for diagnosis of meniscal tears, ligament injuries, sure subchondral bone thickness. Other fat
ADVANCED MRI OF ARTICULAR CARTILAGE 339

Fig. 8. Medial compartment cartilage T2 maps from a healthy volunteer. (A) Spin echo maps acquired with four echoes
and a scan time of 11:30 minutes. (B) Spiral T2 map acquired in 7 minutes. T2 relaxation time in cartilage is sensitive to
collagen matrix damage of articular cartilage.

suppression methods for bSSFP imaging, such as negative charges; mobile ions such as sodium
FEMR and linear combination bSSFP, are less (Naþ) or charged gadolinium MRI contrast
applicable to high field because the shortest TR agents such as Gd-DTPA2 distribute in cartilage
during which the relative phase of fat and water in relation to the proteoglycan concentration. The
changes by p is only 1.1 ms. This TR is too short collagen fibers have an ordered structure, making
to create any meaningful spatial encoding, and the the water associated with them exhibit magnetiza-
radiofrequency power deposition would be high. tion transfer and magic-angle effects. Physiologic
MRI of articular cartilage takes advantage of
these characteristics to explore the collagen and
proteoglycan matrices for pathology. Although
Physiologic magnetic resonance imaging
the methods described here can be performed at
of cartilage
1.5 T, all of them benefit from the additional
Articular cartilage composition SNR available on 3 T systems.

Articular cartilage is approximately 70% water


T2 relaxation time mapping
by weight. The remainder of the tissue consists
predominately of type II collagen fibers and MRI is characterized by excitation of water
proteoglycans. The proteoglycans contain molecules and relaxation of the molecules back to
340 GOLD et al

Fig. 9. Inversion recovery bSSFP imaging to determine T1 and T2 relaxation times in knee cartilage, after arthroscopic
surgery. This method can be applied to monitor cartilage physiology. (A) bSSFP (T2/T1 weighting). (B) T1. (C) T2. (D)
Proton density maps of the articular cartilage are produced in the same 7-minute scan time.

an equilibrium state. The exponential time con- to one or more decaying exponentials, depending
stants describing this relaxation are referred to as on whether it is thought that there is more than
T1 and T2 relaxation times and are constant for one distribution of T2 within the sample [62].
a given tissue at a given MRI field strength. For echo times used in conventional MRI, how-
Changes in these relaxation times can be due to ever, a single exponential fit is adequate. An image
tissue pathology or introduction of a contrast of the T2 relaxation time is generated with either
agent. a color or a gray-scale map representing the relax-
The T2 relaxation time of articular cartilage is ation time as shown in Fig. 8.
a function of the water content and collagen Several investigators have measured the spatial
ultrastructure of the tissue. Measurement of the distribution of T2 relaxation times within articular
spatial distribution of the T2 relaxation time may cartilage [63,64]. Aging seems to be associated with
reveal areas of increased or decreased water an increase in T2 relaxation times in the transitional
content, correlating with cartilage damage. To zone [65]. Relaxation time measurements also have
measure the T2 relaxation time with a high degree been shown to be anisotropic with respect to orien-
of accuracy, attention must be taken with the tation in the main magnetic field [66–68]. Focal in-
MRI technique [61]. Typically, a multiecho spin creases in T2 relaxation times within cartilage have
echo technique is used, and signal levels are fitted been associated with matrix damage, particularly
ADVANCED MRI OF ARTICULAR CARTILAGE 341

loss of collagen integrity. Studies on T2 relaxation


times documenting the effects of age [69], gender
[70], and activity [71] have been published.

Contrast-enhanced imaging
The proteoglycan component of cartilage has
glycosaminoglycan (GAG) side chains with abun-
dant negatively charged carboxyl and sulfate
groups. If mobile ions are allowed time to
distribute in cartilage, they distribute in relation
to the negative fixed charge density of the carti-
lage, or effectively in relation to the GAG
concentration. One of the most common MRI
contrast agents, or Gd-DTPA2 (Magnevist; Ber-
lex, Richmond, CA) has a negative charge. After
intravenous injection of Gd-DTPA2, it pene-
trates into cartilage, and it distributes in higher
concentration in areas of cartilage in which the
GAG content is relatively low. Subsequent T1
imaging (which is reflective of Gd-DTPA2 con-
centration) yields an image depicting GAG
distribution. This technique is referred to as de-
layed gadolinium-enhanced MRI of cartilage
(dGEMRIC) (the ‘‘delay’’ referring to the time re-
quired to allow the Gd-DTPA2 to penetrate the
cartilage tissue) [72,73]. A T1 map of the cartilage
allows assessment of GAG content, with lower
Fig. 10. Color maps of T1p measurements as a function
values corresponding to areas of GAG depletion.
of spin lock frequency (Hz) in a healthy volunteer. T1p In terms of clinical studies, numerous cross-
imaging may be sensitive to proteoglycan depletion in sectional studies on specified populations have
articular cartilage. These maps were acquired with a spi- provided interesting observations. A study re-
ral T1p technique. ported that individuals who exercise on a regular
basis have higher dGEMRIC indices (denoting

Fig. 11. Twisted-projection imaging sodium images of the knee of a healthy volunteer done at 3 T. (A) Single-quantum
images. (B) Triple-quantum images. Sodium content in the patellofemoral cartilage is well seen in both cases. (Courtesy
of F. Boada, University of Pittsburgh.)
342 GOLD et al

Fig. 12. Three-dimensional SSFP DWI. (A) Proton density images. (B) Heat scale maps of the diffusion coefficient. The
b-values correspond to the degree of diffusion weighting. DWI gives a sense of translational water mobility within the
articular cartilage. The diffusion coefficients measured in normal cartilage are about 0.00145 mm2/s, which correspond to
similar values in the literature. (From Miller KL, Hargreaves BA, Gold GE, et al. Steady-state diffusion-weighted imag-
ing of in vivo knee cartilage. Magn Reson Med 2004;51:394–8; with permission.)

higher GAG) than individuals who are sedentary Example images of this method are shown in
[74]. In a relatively large cross-sectional study of Fig. 9. Aside from generating quantitative T1,
patients with hip dysplasia, measures of the sever- T2, and proton density maps, bSSFP images
ity of dysplasia (the radiographically determined also are available for radiologic review. Quantita-
lateral center edge angle) and of pain correlated tive techniques such as this may elucidate physio-
with the dGEMRIC index, but not with the stan- logic changes better in musculoskeletal imaging.
dard radiologic parameter of joint space narrow-
ing [75]. In another study, lesions in patients T1p imaging
with osteoarthritis were more apparent with the
A promising technique for evaluating cartilage
dGEMRIC technique relative to standard MRI
is T1p imaging, or relaxation of spins under the in-
scans [76]. There also have been studies looking
fluence of a radiofrequency field [83,84]. This tech-
at the effects of gadolinium on measurement of
nique may be sensitive to early proteoglycan
T2 relaxation times [77,78]. A study relevant to os-
depletion [85–87]. In typical T1p imaging, magne-
teoarthritis showed that dGEMRIC correlated
tization is tipped into the transverse plane and
with Kellgren/Lawrence radiographic grading of
‘‘spin-locked’’ by a constant radiofrequency field.
osteoarthritis [79].
An example of a T1p map from the patella of
Physiologic methods such as dGEMRIC and
a healthy volunteer is shown in Fig. 10.
T2 mapping can be time-consuming and difficult
to perform on a routine basis. bSSFP methods
Sodium magnetic resonance imaging
show promise in improving the speed and SNR of
T1 and T2 relaxation time measurements [80,81]. Atoms with an odd number of protons or
Newbould and colleagues [82] developed an inver- neutrons possess a nuclear spin momentum and
sion recovery method of acquiring proton density, exhibit the MRI phenomenon. 23Na is an example
T1, and T2 maps using bSSFP in articular carti- of a nucleus other than 1H that is useful in carti-
lage. This technique employs an inversion recov- lage imaging. The Larmor frequency of 23Na is
ery–prepared three-dimensional bSSFP sequence, 11.262 MHz/T compared with 1H at 42.575
where an adiabatic nonslice selective inversion MHz/T. At 1.5 T, the resonant frequency of
23
was used. Total scan time to acquire a 256  Na is 16.9 MHz, whereas it is 63 MHz for 1H.
256  64 three-dimensional volume (FOV ¼ 16 The concentration of 23Na in normal human car-
cm, 1 signal average, 2 mm slice thickness) with tilage is about 320 mM, with T2 relaxation times
in-plane resolution of 0.83 mm was 7:18 minutes. of 2 to 10 ms [88]. The combination of lower
ADVANCED MRI OF ARTICULAR CARTILAGE 343

resonant frequency, lower concentration, and obtained on cartilage/bone plug specimens [95].
shorter T2 relaxation times than 1H make in Fig. 12 shows in vivo DWI results in a normal vol-
vivo imaging of 23Na challenging. Sodium imag- unteer using a navigated DWI technique based on
ing requires the use of special transmit and receive SSFP [98]. This technique produces diffusion-
coils and relatively long imaging times to achieve weighted images of cartilage with a resolution of
adequate SNR. 0.5  0.7  3 mm resolution, taking approxi-
Sodium MRI has shown some promising re- mately 4:40 minutes per b-value. Navigation with
sults in the imaging of articular cartilage; this is DWI techniques is essential in this application to
based on the ability of sodium imaging to depict prevent motion artifacts and allow for multiple ac-
regions of proteoglycan depletion [89]. 23Na atoms quisitions, which improves resolution and SNR.
are associated with the high fixed-charge density
present in proteoglycan sulfate and carboxylate
Discussion
groups. Some spatial variation in 23Na concentra-
tion is present within normal cartilage [88]. Fig. 11 MRI provides a powerful tool for the imaging
shows an example of a sodium image through the and understanding of cartilage. Improvements
patellar cartilage of a healthy volunteer done with have been made in morphologic imaging of carti-
a twisted-projection technique at 3 T [90]. High so- lage, in terms of contrast, resolution, and acquisi-
dium concentration is seen throughout the normal tion time. This improved imaging allows detailed
cartilage. In cartilage samples, sodium imaging has maps of the cartilage surface to be developed,
been shown to be sensitive to small changes in pro- quantifying thickness and volume. Much progress
teoglycan concentration [91,92]. This method has been made in the understanding of cartilage
shows promise to be sensitive to early decreases physiology and the ability to detect changes in
in proteoglycan concentration in osteoarthritis. It proteoglycan content and collagen ultrastructure.
also is possible to do triple-quantum–filtered imag- The choice of a particular protocol for imaging
ing of sodium in cartilage, which may be even articular cartilage depends greatly on patient
more sensitive to early changes [93]. factors. For many patients with internal derange-
ment, imaging with standard FSE or three-
dimensional SPGR sequences may suffice. For
Diffusion-weighted imaging
patients being considered for surgical or pharma-
Imaging the diffusion of water through artic- cologic therapy, a more detailed evaluation may
ular cartilage also is possible with MRI. Diffu- be required. Fast morphologic imaging along with
sion-weighted imaging (DWI) of cartilage has evaluation of cartilage physiology may allow for
been shown in vitro to be sensitive to early noninvasive evaluation of cartilage implants at
cartilage degradation [94,95]. The apparent diffu- different time points.
sion coefficient decreases at long diffusion times, The fundamental tradeoff between image res-
indicative of the water molecules being restricted olution and SNR still limits the ability to image
by cartilage components. At the diffusion times cartilage in vivo with high resolution in an
typically used, this restriction is related to the col- efficient manner. Patient motion ultimately may
lagen network in cartilage [96]. limit the resolution achievable at 1.5 Tesla; so
In vivo DWI of cartilage poses several chal- higher field systems may be required. New tech-
lenges. The T2 relaxation time of cartilage varies niques based on bSSFP may shorten imaging
from 10 to 50 ms, so the TE must be short to time, allowing the application of other sequences
maximize cartilage signal. Diffusion-sensitizing to explore important questions about cartilage
gradients increase the TE and render the sequence physiology and biochemistry. Ideally, the combi-
sensitive to motion. Single-shot techniques have nation of these techniques would lead to an MRI
been used for DWI, but these have relatively low examination for cartilage that is brief and well
SNR and spatial resolution. Multiple acquisitions tolerated, but contains important morphologic
improve the SNR and resolution, but motion and physiologic data.
correction is required for accurate reconstruction
[97].
Summary
Articular cartilage measurements done in vivo
in healthy volunteers show that apparent diffusion MRI, with its unique ability to image and
coefficient ranges from 1.5 to 2  103 mm2/s. characterize soft tissue noninvasively, has emerged
These values compare well with reported results as one of the most accurate imaging methods
344 GOLD et al

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