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MR Imaging and T2 Mapping of Femoral Cartilage:

In Vivo Determination of the Magic Angle Effect

OBJECTIVE

.

The purpose of this study was to perform a quantitative evaluation of the effectof static magnetic field orientation on cartilage transverse (T2) relaxation time in the intact livingjoint and to determine the magnitude of the magic angle effect on in vivo femoral cartilage.

MATERIALS AND METHODS

.

Quantitative T2 maps of the femoral–tibial joint wereobtained in eight asymptomatic male volunteers using a 3-T magnet. Cartilage T2 profiles (T2vs normalized distance from subchondral bone) were evaluated as a function of orientation ofthe radial zone of cartilage with the applied static magnetic field (B

0

).

RESULTS

.

At a normalized distance of 0.3 from bone, cartilage T2 is 8.6% longer in car-tilage oriented 55° to B

0

compared with cartilage oriented parallel with B

0

. Greater orienta-tion 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 sur-face where T2 is 29.1% longer at 55°.

CONCLUSION

.

The effect of orientation on cartilage T2 is substantially less than thatpredicted from prior ex vivo studies. The greatest variation in cartilage T2 is observed in thesuperficial 20% of cartilage. Given the small orientation effect, it is unlikely that the “magicangle effect” accounts for regional differences in cartilage signal intensity observed in clinicalimaging. We hypothesize that regional differences in the degree of cartilage compression areprimarily responsible for the observed regional differences in cartilage T2.

tudies using excised cartilage speci-mens have shown a strong orienta-tion dependence of the transverse

(T2) relaxation time of articular cartilage [1-4].This orientation effect, first described in tendons[5], is attributed to the highly structured col-lagen matrix in the radial zone of cartilage. Inthe radial zone, collagen fibers are preferentiallyoriented perpendicular to subchondral bone. Fortissues such as cartilage that have restricted wa-ter mobility, this tissue anisotropy provides anefficient T2 relaxation mechanism. However,when collagen fibers are oriented 55° relative tothe applied static magnetic field (B

0

), this relax-ation mechanism is minimized resulting in alonger T2. This has been termed the “magic an-gle effect,” derived from the technique of magicangle spinning used to shorten the T2 of crystal-line solids in nuclear MR spectroscopy.

In clinical MR imaging, the magic angleeffect has been invoked to explain the etiol-ogy of the focally increased signal observedon short TE images of cartilage with curvedarticular surfaces, such as the femoral

condyle [6] and talar dome [7]. Because in-creased T2 is associated with cartilage dam-age, artifact from the magic angle effect is apotential source of diagnostic error.

Although the magic angle effect has beenwidely discussed in the literature, no studies, toour knowledge, have documented an orientationdependence of T2 in living tissue. Previous stud-ies on the orientation dependence of cartilage T2have been limited to excised cartilage specimens[1-4], and a single in vivo study evaluating carti-lage signal intensity as a function of orientationwith B

0

[6]. Results of ex vivo preparations maynot be representative of tissue in the intact joint.For example, Rubenstein et al. [8] has shownthat compression changes the MR imaging ap-pearance of cartilage. It is likely that intrinsiccompression of cartilage in the intact restingjoint influences the T2 behavior of cartilage.

Because of its curved surface, the femoralcondyle provides a natural model to study the ef-fect of B

0

field orientation on in vivo cartilageT2. In this study, we performed quantitative T2measurements of femoral cartilage and evaluated

Timothy J. Mosher

1

Harvey Smith

1

Bernard J. Dardzinski

2,3

Vincent J. Schmithorst

2

Michael B. Smith

1,4

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.

T. J. Mosher and B. J. Dardzinski received grant support for this project from the Arthritis Foundation. H. Smith received support from a research training fellowship provided by the Howard Hughes Medical Institute.

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. Address correspondence to T. J. Mosher.

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.

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© American Roentgen Ray Society

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cartilage T2 profiles as a function of orientation.We sought, first, to determine if the magnitude ofthe in vivo magic angle effect is comparable tothat previously observed ex vivo, and, second, todetermine if signal intensity differences in articu-lar cartilage previously attributed to magic angleeffects are due to T2 anisotropy.

Materials and Methods

Population

We performed quantitative T2 mapping of the fem-oral–tibial joint in eight asymptomatic men; these vol-unteers ranged in age from 24 to 42 years (mean ± SD,31 ± 7 years). All provided informed consent to partic-ipate in the study, which was approved by the institu-tional review board. Immediately before the MRimaging examination, the volunteers completeda Western Ontario and McMaster Universities(WOMAC) osteoarthritis questionnaire for assessmentof symptoms. Volunteers were considered asymptom-atic if their normalized score was less than 10.

Data Acquisition

MR images of the femoral–tibial joint were ob-tained with a 3-T MR imaging spectrometer (Med-Spec S300; Bruker Instruments, Ettlingen, Germany)with a 14-cm-diameter transmit–receive linear birdcagecoil operating at 125 MHz for protons. A 33-cm-di-ameter asymmetric gradient insert capable of deliver-ing ±5 G/cm field profile was used. Volunteers werepositioned supinely in the imager, with the femoral–tibial joint placed at the gradient isocenter.

Spin-echo images used to calculate T2 mapswere obtained with the following parameters: TR/TE, 1500/10 msec; echo train length, 11; sectionthickness, 2 mm; field of view, 12.75 cm; image ma-trix, 384

×

384; bandwidth, 75.8 kHz; section-selec-tion and refocusing-pulse duration, 2 msec; signalacquisition, 2; total acquisition time, 21 min. Usinga coronal locator, a single sagittal data set was ob-tained through the lateral femoral condyle. A singlesagittal slice was used to minimize off-resonance ef-fects. Frequency encoding was head to foot acrossthe femoral–tibial joint.

Data Analysis

Magnitude images and T2 maps were calculatedfrom 10 spin-echo images, using linear least squarescurve fitting on a pixel-by-pixel basis, on CCHIPS/IDL software (Interactive Data Language, Boulder,CO; Dardzinski BJ et al. presented at the annualmeeting of the International Society for MagneticResonance in Medicine, May 1999.) Because ech-oes 2–11 contain signal from the stimulated echo,exclusion of the initial spin-echo minimizes artifactin the T2 calculation. The influence of this error inthe determination of in vivo T2 measurement hasbeen discussed [9, 10]. Fitting of the signal intensity(SI) for the

i

th

,

j

th

pixel as a function of time,

t

, canbe expressed as follows:

SI

i,j

(

t

) = SI0

i,j

· exp (– t / T2

i,j

)

where SI0

i,j

is the pixel intensity at

t

= 0 and T2

i,j

is the T2 time constant of pixel

i,j

. A magnitudeimage is generated from the pixel SI0

i,j

data, and aT2 map is generated from the T2

i,j

data. The automated volumetric segmentation subroutine

in the CCHIPS/IDL software was used to determinethe boundaries of the articular cartilage and to generatethe T2 profiles and calculate their respective angles toB

0

. The T2 profile is a plot of T2 versus distance fromthe bone–cartilage interface. The subroutine automati-cally generates the T2 profiles by defining a tangentperpendicular to the bone–cartilage boundary and cal-culating the angle between the T2 profile and the

z

-axis, which is parallel to B

0

. A total of 2130 profileswere obtained from the eight volunteers. For compari-son, each profile was normalized for cartilage thick-ness such that cartilage at the subchondral surface hada normalized distance of 0, and cartilage at the articularsurface had a normalized distance of 1 [9].

A comparison of response functions was used todetermine whether a difference in the normalized T2profiles occurred as a function of B

0

field orientation.The response function is a theoretical equation thatbest approximates T2 as a function of normalized dis-tance for the population. To minimize bias in selectionof a response function, data points from all 2130 pro-files were initially pooled and fit to 3665 candidateequations with a standard commercially availablecurve-fitting software package (Tablecurve; Jandel

Scientific Software, San Rafael, CA). The responsefunction was determined by sorting the fit of the can-didate equations by a degrees-of-freedom-adjusted

r

2

.The 2130 T2 profiles were then stratified into sevengroups by orientation of the radial zone of cartilagerelative to B

0

: 0–10° (693 profiles), 11–20° (439 pro-files), 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 thenpooled and fit to the response function. The 99.99%confidence interval (CI) for the response function ofeach group was calculated to determine statistical dif-ference in T2 profiles at different orientations. Re-gions of the response function in which no overlap ofthe 99.99% confidence interval was present were con-sidered significantly different, with a Bonferroni-cor-rected

p

value of less than 0.05.

Results

Figure 1 is a representative T2-weightedsource image with the corresponding calculatedmagnitude and T2 map. The T2-weighted sourceimage shows hypointense radial striations in thedeep layers of the femoral tibial cartilage withhigher signal intensity in the superficial cartilage.The cartilage of the posterior femoral condylehas more uniform signal intensity. Radial stria-tions are not observed in this location. Although

C

BA

Fig. 1.—Sample MR images ob-tained from asymptomatic 23-year-old man. A, T2-weighted source image showsuniform signal intensity in posteriorfemoral condyle (arrow) without hy-pointense striations of radial zone ob-served in weight-bearing cartilage(arrowhead). B, Calculated magnitude map showsuniform intensity in posterior femoralcondyle (arrow).C, Calculated T2 map shows longerT2 values in superficial layers ofposterior femoral condyle (arrow)oriented 55° relative to B0.

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667

the magnitude map also has uniform signal in-tensity at the 55° orientation, the T2 map showslonger T2 values near the articular surface com-pared with the deeper radial zone.

Figure 2 is a three-dimensional plot of the fit-ted T2 profiles correlating cartilage T2 valueswith normalized distance and orientation to B

0

.As observed on the T2 maps, the T2 profilesshow a spatial variation in cartilage T2, with val-ues initially decreasing with distance from thesubchondral bone and then increasing toward thearticular surface. The least variation in cartilageT2 occurs in cartilage that is oriented 0–10° toB

0

. At this orientation, T2 increases from a mini-mum value of 45.6 msec (99.99% CI: 44.8–46.5msec) at a normalized distance of 0.4–55 msec(99.99% CI: 53.7–57.1 msec) at the articular sur-face. The greatest variation in T2 occurs whenthe radial zone is oriented 50–60° B

0

. At this ori-entation, T2 increases from a minimum of 48.2msec (99.99% CI: 46.2–50.2 msec) at a normal-ized distance of 0.2–77 msec (99.99% CI: 73.7–81.3 msec) at a distance of 1.0. Over the normalizeddistance of 0.3–1.0, the T2 profiles oriented 50–60° to B

0

are statistically significantly longerthan the T2 profiles oriented 0–10°.

Figure 3 shows the percent change in carti-lage T2 at a normalized distance of 0.3, 0.6, and0.9 as a function of radial zone orientation. Atall three distances, cartilage T2 is maximizedwhen oriented 55° to B

0

. At a normalized dis-tance of 0.3, cartilage T2 is 8.6% longer in carti-lage oriented 55° to B

0

compared with cartilageoriented parallel to B

0

. Greater T2 variationwith orientation is observed in more superficialcartilage. At a normalized distance of 0.6 carti-lage, T2 is 18.3% longer. The greatest orienta-tion effect is observed at a normalized distanceof 0.9, at which T2 is 29.1% longer at 55°.

Discussion

The organization of the collagen frameworkforms the basis of the histologic zones of carti-lage [11]. As illustrated in Figure 4, the deep40–60% of cartilage is termed the radial zone;it is characterized by a preferential orientationof collagen perpendicular to subchondral zone.The next layer is the transitional zone, whichcomprises 20–30% of the cartilage thickness.In this layer, the orientation of collagen fibersappears more random. A thin superficial zoneis characterized by alignment of collagen par-allel to the surface. The highly organized ar-chitecture of the extracellular collagen matrixresults in structural anisotropy of cartilage. Inaddition to anisotropy of collagen, there isanisotropy of cartilage proteoglycans in the ra-dial zone of cartilage [12].

Fig. 2.—Three-dimensional plot of cartilage T2 as function of normalized distance and orientation to B0. For all orientations,cartilage T2 values are long near bone–cartilage interface and decrease to minimum near normalized distance of 0.2–0.4.Cartilage T2 then increases toward articular surface. At all normalized distances, cartilage T2 is longest when oriented 55°.Greatest variation in cartilage T2 as a function of orientation is in superficial 20% of cartilage (normalized distance = 0.8–1.0).

Fig. 3.—Graph showing percent change in cartilage T2 (relative to 0°) as a function of orientation to B0. Greatestvariation in T2 is observed in superficial cartilage (dashed line, normalized distance [ND] = 0.9). Least variationin cartilage T2 occurs in the radial zone (solid line, ND = 0.3). Dotted line represents 0.6 ND.

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The T2 of connective tissue is sensitive to theanisotropic structure of the collagen matrix [13].Using isolated bovine patellae, Rubenstein et al.[1] were the first investigators to show that theMR imaging signal intensity of articular carti-lage is dependent on sample orientation. Theyattributed this orientation dependency to theanisotropic arrangement of collagen fibers inthe radial zone of articular cartilage. Subsequenthigh-field (7-T) studies on excised cartilageplugs have confirmed a strong orientation de-pendence of cartilage T2 [2, 3, 14, 15]. Using14

µ

m resolution T2 maps of excised caninecartilage plugs, Xia [14] identified three distinctzones of cartilage with different orientation de-pendence. Cartilage immediately beneath thearticular surface showed less T2 anisotropy withincreasing distance from the surface. A secondregion, corresponding in location to the transi-tional zone of cartilage, did not show an orienta-tion dependence of T2. The third zone,corresponding to the radial zone, showed uni-form orientation dependence, with T2 increas-ing by approximately 80% when the radialcollagen fibers were aligned 57° to B

0

com-pared with a 0° orientation. In studies correlat-ing cartilage T2 mapping with electronmicroscopy, Goodwin et al. [16] observed a164% increase in T2 of the radial zone whenaligned 55° to B

0

. This study also identified a28% increase in T2 of the transitional zone.Correlation with freeze fracture samples sug-gests this may be the result of a planar organiza-tion of collagen fibrils in the transitional zone.In an early study, Mlynarik et al. [3] found a50% increase in T2 of the intermediate cartilagezone when it was angled obliquely with B

0

. Us-ing a Carr-Purcell Meiboom-Gill sequence todetermine effect of orientation on bulk cartilageT2, Grunder et al. [15] found a maximum in T2when the radial zone was oriented 55° to B

0

, in-creasing by 300% compared with the T2 mea-surement at 0° orientation. Similar results have

been obtained at 1.5 T, with a more uniform ap-pearance of T2-weighted signal intensity in im-ages of cartilage oriented 55° to B

0

[17].Prior in vivo studies evaluating the effect

of orientation on the MR imaging appear-ance of articular cartilage have been limitedto assessment of signal intensity. Wacker etal. [6] evaluated MR imaging signal intensityof the femoral condyle as a function of orien-tation in asymptomatic children 8–12 yearsold. Cartilage oriented 55° to B

0

was morehomogeneous, with loss of the laminar ap-pearance observed in cartilage at other orien-tations. In the same study, cartilage oriented55° relative to B

0

showed increased signalintensity. Because the study did not measurethe T2 of cartilage, these observations cannotbe attributed directly to T2 anisotropy.

Our results on regional differences in signalintensity of articular cartilage agree well withearlier work. As shown in the T2-weighted im-age presented in Figure 1, focal increased signalintensity is observed in femoral cartilage ori-ented 55° relative to B

0

. This finding is consis-tent with previous observations made at 1.5 T[1, 6]. In weight-bearing cartilage oriented par-allel to B

0

, hypointense radial bands are ob-served in the deep layer of cartilage, with highersignal intensity near the subchondral surface. Asobserved in both in vivo and isolated cartilagesamples, images of cartilage have more uniformsignal intensity in regions where the radial zoneis oriented 55° to B

0

. Hypointense bands are notobserved in this location. These bands havebeen attributed to collagen fibers in the radialzone [16, 18]. In high resolution 1.5-T MR im-ages of cartilage samples, Waldschmidt et al.[18] have shown loss of these bands when carti-lage is oriented 55° to B

0

. Regional variation in cartilage T2 differs

from that observed with signal intensity. Asshown in Figure 2, all regions of femoral car-tilage have longer T2 values near the articu-

lar surface. The magnitude of the T2 valuesand increase of T2 toward the articular sur-face is consistent with that previously ob-served in patellar cartilage of asymptomaticvolunteers [9, 19]. However, the effect of ori-entation on cartilage T2 in the living joint isquite different from that previously reportedin excised samples. In our study, changes incartilage orientation resulted in a 9–29% in-crease in T2. This increase is substantiallyless than the magnitude of the orientation ef-fect previously reported in ex vivo studies.Our results, unlike those of T2-mappingstudies that reported a high orientation de-pendence of the radial zone and little orienta-tion dependence of more superficial cartilage[2, 3, 14], suggest that the least variationwith orientation is in the radial zone. Thegreatest change in T2 as a function of orien-tation occurs in the superficial 20% of carti-lage. This discrepancy suggests factors otherthan tissue anisotropy are responsible for theorientation dependence in T2 observed nearthe articular surface.

A possible explanation for the observed dif-ference in both the magnitude and location ofthe orientation dependence of cartilage T2 be-tween our study and prior ex vivo studies is theeffect of cartilage compression. In a recentstudy evaluating diurnal variation in cartilagethickness, Waterton et al. [20] has shown a0.65-mm decrease in cartilage thickness of theweight-bearing region of the lateral femoral–tibial compartment. This study indicates thatincreased hydrostatic pressure resulting fromnormal daily activity can produce significantcompression of articular cartilage. Rubensteinet al. [8] previously showed that the MR imag-ing appearance of cartilage is altered by com-pression; decreasing signal intensity of thesuperficial lamina occurs with increasing lev-els of compression. In their study, this layerslowly recovered signal intensity over several

Fig. 4.—Drawing of cross-sectionalstructure of articular cartilage illus-trating orientation of collagen fibers.In radial zone of cartilage collagen fi-bers are preferentially arranged per-pendicular to the subchondral bonesurface. Anisotropic arrangement ofcollagen fibers in radial zone formstheoretical basis for the magic angleeffect in articular cartilage.

MR Imaging and T2 Mapping of Femoral Cartilage

AJR:177, September 2001

669

hours, after release of the compressive force.They attributed this observation to a combina-tion of net water loss and alteration in collagenorientation. The results of our experiment areconsistent with their hypothesis.

With compression, water is exuded from thecartilage surface. The redistribution of water incartilage after removal of the compressive forceoccurs very slowly [11]. In addition, there is ev-idence that cartilage does not compress uni-formly. The superficial 20% of articularcartilage has been shown to be more compress-ible than deeper cartilage [21, 22]. These resultssuggest that compression produces preferentialloss of water from superficial cartilage. Becausecartilage T2 varies proportionally with watercontent (Lusse et al., presented at the annualmeeting of the International Society for Mag-netic Resonance in Medicine, May 1999), lossof water will result in lower T2 values.

It is our hypothesis that regional differencesin cartilage compression are responsible for thevariation in T2 and signal intensity observed incartilage at different orientations. Cartilage ori-ented parallel to B

0

is located in the weight-bearing portion of the femoral–tibial joint, andis subject to compressive force that may lowerthe water content of the superficial cartilage.Cartilage oriented 55° to B

0

is located in thenon–weight-bearing portion of the femoralcondyle; it is therefore less compressed and willhave greater water content in the superficialzone. This hypothesis remains tentative. Addi-tional studies are needed to evaluate the effect ofregional biomechanics on the MR imaging ap-pearance of cartilage and cartilage T2.

In the radial zone, the magnitude of the ori-entation effect on cartilage T2 was much lessthan observed in ex vivo studies. Our explana-tion of this observation, initially proposed byRubenstein et al. [8], is that changes in col-lagen fiber orientation with compression mayattenuate the magic angle effect in the intactjoint. The smaller degree of orientation effecton cartilage T2 in the radial zone suggests col-lagen anisotropy is less in vivo than that pre-dicted from ex vivo studies.

Several factors limit our study, because it is anin vivo determination of T2. First, the small-di-ameter quadrature knee coil and gradient insertneeded to perform the T2 measurements did notallow the orientation of the femur to be varied.Because different cartilage regions were beingcompared, this study design assumed orientationto be the only factor that alters cartilage T2. Aswe have discussed, it is likely that cartilage T2 isinfluenced by regional differences in joint bio-mechanics. In addition, several studies have

shown regional differences in the composition ofproteoglycans and collagen content of the femo-ral condyle that influence regional cartilage bio-mechanics and could influence cartilage T2 [23].Second, although T2 maps in this study were ob-tained with relatively high voxel resolution (2.00

×

0.33

×

0.33 mm), the resolution is generallylower than that used in prior ex vivo studies. Theresultant volume averaging may diminish themagnitude of the orientation effect. This reduc-tion is especially apparent at the bone–cartilageinterface, at which there is contamination of thecartilage signal through volume averaging withbone marrow. However, it is important to notethat the resolution used in this study is similar tothat used in high-resolution clinical imaging ofthe knee, and therefore our observations shouldbe representative of the magnitude of the magicangle effect that may be observed in routine clin-ical imaging. Finally, we did not determine if thecartilage used in this study was normal. It is pos-sible that preclinical cartilage damage may de-crease the degree of tissue anisotropy andcontribute to the smaller-than-predicted magicangle effect observed in this study.

In conclusion, results of this study indi-cate that the effect of orientation on cartilageT2 is substantially less than that predictedon the basis of prior ex vivo studies. Giventhe small orientation effect, it is unlikelythat the magic angle effect accounts for re-gional differences in cartilage signal inten-sity observed in clinical imaging. Wehypothesize that regional differences in thedegree of cartilage compression are prima-rily responsible for the observed regionaldifferences in cartilage T2.

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The reader’s attention is directed to the commentary on this article, which appears on the following pages.