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1
Department of Radiology—MC H066, Center for Nuclear Magnetic Resonance
Research, M108 NMR Building, M.S. Hershey Medical Center, Pennsylvania State
University College of Medicine, 500 University Dr., Hershey, PA 17033.
2
Imaging Research Center, The Children's Hospital Research Foundation,
Children's Hospital Medical Center, Cincinnati, OH 45229.
3
Departments of Radiology and Pediatrics, University of Cincinnati College of
Medicine, 3333 Burnet Ave., Cincinnati, OH 45229.
4
Department of Cellular and Molecular Physiology, Pennsylvania State University
College of Medicine, Hershey, PA 17033.
Received September 13, 2000;
accepted after revision January 17, 2001.
Presented at the annual meeting of the International Society for Magnetic
Resonance in Medicine, Denver, April 1-7, 2000.
Abstract
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MATERIALS AND METHODS. Quantitative T2 maps of the femoral—tibial joint were obtained in eight asymptomatic male volunteers using a 3-T magnet. Cartilage T2 profiles (T2 vs normalized distance from subchondral bone) were evaluated as a function of orientation of the radial zone of cartilage with the applied static magnetic field (B0).
RESULTS. At a normalized distance of 0.3 from bone, cartilage T2 is 8.6% longer in cartilage oriented 55° to B0 compared with cartilage oriented parallel with B0. Greater orientation variation is observed in more superficial cartilage. At a normalized distance of 0.6, cartilage T2 is 18.3% longer. The greatest orientation effect is observed near the articular surface where T2 is 29.1% longer at 55°.
CONCLUSION. The effect of orientation on cartilage T2 is substantially less than that predicted from prior ex vivo studies. The greatest variation in cartilage T2 is observed in the superficial 20% of cartilage. Given the small orientation effect, it is unlikely that the "magic angle effect" accounts for regional differences in cartilage signal intensity observed in clinical imaging. We hypothesize that regional differences in the degree of cartilage compression are primarily responsible for the observed regional differences in cartilage T2.
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In clinical MR imaging, the magic angle effect has been invoked to explain the etiology of the focally increased signal observed on short TE images of cartilage with curved articular surfaces, such as the femoral condyle [6] and talar dome [7]. Because increased T2 is associated with cartilage damage, artifact from the magic angle effect is a potential source of diagnostic error.
Although the magic angle effect has been widely discussed in the literature, no studies, to our knowledge, have documented an orientation dependence of T2 in living tissue. Previous studies on the orientation dependence of cartilage T2 have been limited to excised cartilage specimens [1,2,3,4], and a single in vivo study evaluating cartilage signal intensity as a function of orientation with B0 [6]. Results of ex vivo preparations may not be representative of tissue in the intact joint. For example, Rubenstein et al. [8] has shown that compression changes the MR imaging appearance of cartilage. It is likely that intrinsic compression of cartilage in the intact resting joint influences the T2 behavior of cartilage.
Because of its curved surface, the femoral condyle provides a natural model to study the effect of B0 field orientation on in vivo cartilage T2. In this study, we performed quantitative T2 measurements of femoral cartilage and evaluated cartilage T2 profiles as a function of orientation. We sought, first, to determine if the magnitude of the in vivo magic angle effect is comparable to that previously observed ex vivo, and, second, to determine if signal intensity differences in articular cartilage previously attributed to magic angle effects are due to T2 anisotropy.
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Data Acquisition
MR images of the femoral—tibial joint were obtained with a 3-T MR
imaging spectrometer (Med-Spec S300; Bruker Instruments, Ettlingen, Germany)
with a 14-cm-diameter transmit—receive linear birdcage coil operating at
125 MHz for protons. A 33-cm-diameter asymmetric gradient insert capable of
delivering ±5 G/cm field profile was used. Volunteers were positioned
supinely in the imager, with the femoral—tibial joint placed at the
gradient isocenter.
Spin-echo images used to calculate T2 maps were obtained with the following parameters: TR/TE, 1500/10 msec; echo train length, 11; section thickness, 2 mm; field of view, 12.75 cm; image matrix, 384 x 384; bandwidth, 75.8 kHz; section-selection and refocusing-pulse duration, 2 msec; signal acquisition, 2; total acquisition time, 21 min. Using a coronal locator, a single sagittal data set was obtained through the lateral femoral condyle. A single sagittal slice was used to minimize off-resonance effects. Frequency encoding was head to foot across the femoral—tibial joint.
Data Analysis
Magnitude images and T2 maps were calculated from 10 spin-echo images,
using linear least squares curve fitting on a pixel-by-pixel basis, on
CCHIPS/IDL software (Interactive Data Language, Boulder, CO; Dardzinski BJ et
al. presented at the annual meeting of the International Society for Magnetic
Resonance in Medicine, May 1999.) Because echoes 2-11 contain signal from the
stimulated echo, exclusion of the initial spin-echo minimizes artifact in the
T2 calculation. The influence of this error in the determination of in vivo T2
measurement has been discussed
[9,
10]. Fitting of the signal
intensity (SI) for the ith, jth pixel
as a function of time, t, can be expressed as follows:
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The automated volumetric segmentation subroutine in the CCHIPS/IDL software was used to determine the boundaries of the articular cartilage and to generate the T2 profiles and calculate their respective angles to B0. The T2 profile is a plot of T2 versus distance from the bone—cartilage interface. The subroutine automatically generates the T2 profiles by defining a tangent perpendicular to the bone—cartilage boundary and calculating the angle between the T2 profile and the z-axis, which is parallel to B0. A total of 2130 profiles were obtained from the eight volunteers. For comparison, each profile was normalized for cartilage thickness such that cartilage at the subchondral surface had a normalized distance of 0, and cartilage at the articular surface had a normalized distance of 1 [9].
A comparison of response functions was used to determine whether a difference in the normalized T2 profiles occurred as a function of B0 field orientation. The response function is a theoretical equation that best approximates T2 as a function of normalized distance for the population. To minimize bias in selection of a response function, data points from all 2130 profiles were initially pooled and fit to 3665 candidate equations with a standard commercially available curve-fitting software package (Tablecurve; Jandel Scientific Software, San Rafael, CA). The response function was determined by sorting the fit of the candidate equations by a degrees-of-freedom-adjusted r2. The 2130 T2 profiles were then stratified into seven groups by orientation of the radial zone of cartilage relative to B0: 0-10° (693 profiles), 11-20° (439 profiles), 21-30° (308 profiles), 31-40° (251 profiles), 41-50° (244 profiles), 51-60° (126 profiles), and 61-70° (69 profiles). Profiles from each group were then pooled and fit to the response function. The 99.99% confidence interval (CI) for the response function of each group was calculated to determine statistical difference in T2 profiles at different orientations. Regions of the response function in which no overlap of the 99.99% confidence interval was present were considered significantly different, with a Bonferroni-corrected p value of less than 0.05.
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Figure 2 is a three-dimensional plot of the fitted T2 profiles correlating cartilage T2 values with normalized distance and orientation to B0. As observed on the T2 maps, the T2 profiles show a spatial variation in cartilage T2, with values initially decreasing with distance from the subchondral bone and then increasing toward the articular surface. The least variation in cartilage T2 occurs in cartilage that is oriented 0-10° to B0. At this orientation, T2 increases from a minimum value of 45.6 msec (99.99% CI: 44.8-46.5 msec) at a normalized distance of 0.4-55 msec (99.99% CI: 53.7-57.1 msec) at the articular surface. The greatest variation in T2 occurs when the radial zone is oriented 50-60° B0. At this orientation, T2 increases from a minimum of 48.2 msec (99.99% CI: 46.2-50.2 msec) at a normalized distance of 0.2-77 msec (99.99% CI: 73.7-81.3 msec) at a distance of 1.0. Over the normalized distance of 0.3-1.0, the T2 profiles oriented 50-60° to B0 are statistically significantly longer than the T2 profiles oriented 0-10°.
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Figure 3 shows the percent change in cartilage T2 at a normalized distance of 0.3, 0.6, and 0.9 as a function of radial zone orientation. At all three distances, cartilage T2 is maximized when oriented 55° to B0. At a normalized distance of 0.3, cartilage T2 is 8.6% longer in cartilage oriented 55° to B0 compared with cartilage oriented parallel to B0. Greater T2 variation with orientation is observed in more superficial cartilage. At a normalized distance of 0.6 cartilage, T2 is 18.3% longer. The greatest orientation effect is observed at a normalized distance of 0.9, at which T2 is 29.1% longer at 55°.
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The T2 of connective tissue is sensitive to the anisotropic structure of the collagen matrix [13]. Using isolated bovine patellae, Rubenstein et al. [1] were the first investigators to show that the MR imaging signal intensity of articular cartilage is dependent on sample orientation. They attributed this orientation dependency to the anisotropic arrangement of collagen fibers in the radial zone of articular cartilage. Subsequent high-field (7-T) studies on excised cartilage plugs have confirmed a strong orientation dependence of cartilage T2 [2, 3, 14, 15]. Using 14 µm resolution T2 maps of excised canine cartilage plugs, Xia [14] identified three distinct zones of cartilage with different orientation dependence. Cartilage immediately beneath the articular surface showed less T2 anisotropy with increasing distance from the surface. A second region, corresponding in location to the transitional zone of cartilage, did not show an orientation dependence of T2. The third zone, corresponding to the radial zone, showed uniform orientation dependence, with T2 increasing by approximately 80% when the radial collagen fibers were aligned 57° to B0 compared with a 0° orientation. In studies correlating cartilage T2 mapping with electron microscopy, Goodwin et al. [16] observed a 164% increase in T2 of the radial zone when aligned 55° to B0. This study also identified a 28% increase in T2 of the transitional zone. Correlation with freeze fracture samples suggests this may be the result of a planar organization of collagen fibrils in the transitional zone. In an early study, Mlynarik et al. [3] found a 50% increase in T2 of the intermediate cartilage zone when it was angled obliquely with B0. Using a Carr-Purcell Meiboom-Gill sequence to determine effect of orientation on bulk cartilage T2, Grunder et al. [15] found a maximum in T2 when the radial zone was oriented 55° to B0, increasing by 300% compared with the T2 measurement at 0° orientation. Similar results have been obtained at 1.5 T, with a more uniform appearance of T2-weighted signal intensity in images of cartilage oriented 55° to B0 [17].
Prior in vivo studies evaluating the effect of orientation on the MR imaging appearance of articular cartilage have been limited to assessment of signal intensity. Wacker et al. [6] evaluated MR imaging signal intensity of the femoral condyle as a function of orientation in asymptomatic children 8-12 years old. Cartilage oriented 55° to B0 was more homogeneous, with loss of the laminar appearance observed in cartilage at other orientations. In the same study, cartilage oriented 55° relative to B0 showed increased signal intensity. Because the study did not measure the T2 of cartilage, these observations cannot be attributed directly to T2 anisotropy.
Our results on regional differences in signal intensity of articular cartilage agree well with earlier work. As shown in the T2-weighted image presented in Figure 1A,1B,1C, focal increased signal intensity is observed in femoral cartilage oriented 55° relative to B0. This finding is consistent with previous observations made at 1.5 T [1, 6]. In weight-bearing cartilage oriented parallel to B0, hypointense radial bands are observed in the deep layer of cartilage, with higher signal intensity near the subchondral surface. As observed in both in vivo and isolated cartilage samples, images of cartilage have more uniform signal intensity in regions where the radial zone is oriented 55° to B0. Hypointense bands are not observed in this location. These bands have been attributed to collagen fibers in the radial zone [16, 18]. In high resolution 1.5-T MR images of cartilage samples, Waldschmidt et al. [18] have shown loss of these bands when cartilage is oriented 55° to B0.
Regional variation in cartilage T2 differs from that observed with signal intensity. As shown in Figure 2, all regions of femoral cartilage have longer T2 values near the articular surface. The magnitude of the T2 values and increase of T2 toward the articular surface is consistent with that previously observed in patellar cartilage of asymptomatic volunteers [9, 19]. However, the effect of orientation on cartilage T2 in the living joint is quite different from that previously reported in excised samples. In our study, changes in cartilage orientation resulted in a 9-29% increase in T2. This increase is substantially less than the magnitude of the orientation effect previously reported in ex vivo studies. Our results, unlike those of T2-mapping studies that reported a high orientation dependence of the radial zone and little orientation dependence of more superficial cartilage [2, 3, 14], suggest that the least variation with orientation is in the radial zone. The greatest change in T2 as a function of orientation occurs in the superficial 20% of cartilage. This discrepancy suggests factors other than tissue anisotropy are responsible for the orientation dependence in T2 observed near the articular surface.
A possible explanation for the observed difference in both the magnitude and location of the orientation dependence of cartilage T2 between our study and prior ex vivo studies is the effect of cartilage compression. In a recent study evaluating diurnal variation in cartilage thickness, Waterton et al. [20] has shown a 0.65-mm decrease in cartilage thickness of the weight-bearing region of the lateral femoral—tibial compartment. This study indicates that increased hydrostatic pressure resulting from normal daily activity can produce significant compression of articular cartilage. Rubenstein et al. [8] previously showed that the MR imaging appearance of cartilage is altered by compression; decreasing signal intensity of the superficial lamina occurs with increasing levels of compression. In their study, this layer slowly recovered signal intensity over several hours, after release of the compressive force. They attributed this observation to a combination of net water loss and alteration in collagen orientation. The results of our experiment are consistent with their hypothesis.
With compression, water is exuded from the cartilage surface. The redistribution of water in cartilage after removal of the compressive force occurs very slowly [11]. In addition, there is evidence that cartilage does not compress uniformly. The superficial 20% of articular cartilage has been shown to be more compressible than deeper cartilage [21, 22]. These results suggest that compression produces preferential loss of water from superficial cartilage. Because cartilage T2 varies proportionally with water content (Lusse et al., presented at the annual meeting of the International Society for Magnetic Resonance in Medicine, May 1999), loss of water will result in lower T2 values.
It is our hypothesis that regional differences in cartilage compression are responsible for the variation in T2 and signal intensity observed in cartilage at different orientations. Cartilage oriented parallel to B0 is located in the weight-bearing portion of the femoral—tibial joint, and is subject to compressive force that may lower the water content of the superficial cartilage. Cartilage oriented 55° to B0 is located in the non—weight-bearing portion of the femoral condyle; it is therefore less compressed and will have greater water content in the superficial zone. This hypothesis remains tentative. Additional studies are needed to evaluate the effect of regional biomechanics on the MR imaging appearance of cartilage and cartilage T2.
In the radial zone, the magnitude of the orientation effect on cartilage T2 was much less than observed in ex vivo studies. Our explanation of this observation, initially proposed by Rubenstein et al. [8], is that changes in collagen fiber orientation with compression may attenuate the magic angle effect in the intact joint. The smaller degree of orientation effect on cartilage T2 in the radial zone suggests collagen anisotropy is less in vivo than that predicted from ex vivo studies.
Several factors limit our study, because it is an in vivo determination of T2. First, the small-diameter quadrature knee coil and gradient insert needed to perform the T2 measurements did not allow the orientation of the femur to be varied. Because different cartilage regions were being compared, this study design assumed orientation to be the only factor that alters cartilage T2. As we have discussed, it is likely that cartilage T2 is influenced by regional differences in joint biomechanics. In addition, several studies have shown regional differences in the composition of proteoglycans and collagen content of the femoral condyle that influence regional cartilage biomechanics and could influence cartilage T2 [23]. Second, although T2 maps in this study were obtained with relatively high voxel resolution (2.00 x 0.33 x 0.33 mm), the resolution is generally lower than that used in prior ex vivo studies. The resultant volume averaging may diminish the magnitude of the orientation effect. This reduction is especially apparent at the bone—cartilage interface, at which there is contamination of the cartilage signal through volume averaging with bone marrow. However, it is important to note that the resolution used in this study is similar to that used in high-resolution clinical imaging of the knee, and therefore our observations should be representative of the magnitude of the magic angle effect that may be observed in routine clinical imaging. Finally, we did not determine if the cartilage used in this study was normal. It is possible that preclinical cartilage damage may decrease the degree of tissue anisotropy and contribute to the smaller-than-predicted magic angle effect observed in this study.
In conclusion, results of this study indicate that the effect of orientation on cartilage T2 is substantially less than that predicted on the basis of prior ex vivo studies. Given the small orientation effect, it is unlikely that the magic angle effect accounts for regional differences in cartilage signal intensity observed in clinical imaging. We hypothesize that regional differences in the degree of cartilage compression are primarily responsible for the observed regional differences in cartilage T2.
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