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DOI: 10.1148/radiol.2291021041
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(Radiology 2003;229:269-274.)
© RSNA, 2003

Technical Developments

In Vivo Proton MR Three-dimensional T1{rho} Mapping of Human Articular Cartilage: Initial Experience1

Ravinder Reddy Regatte, PhD, Sarma V. S. Akella, PhD, Arijitt Borthakur, PhD, J. Bruce Kneeland, MD and Ravinder Reddy, PhD

1 From the MMRRCC, Department of Radiology, B1, Stellar-Chance Laboratories, University of Pennsylvania Medical Center, 422 Curie Blvd, Philadelphia, PA 19104-6100. Received August 26, 2002; revision requested October 18; revision received December 2; accepted February 3, 2003. Supported by NIH research resource grant RR02305, grants R0145242 and R0145404 from National Institutes of Arthritis and Musculoskeletal and Skin Diseases, and the Arthritis Foundation. Address correspondence to R.R.R. (e-mail: regatte@mail.mmrrcc.upenn.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
The purpose of this study was to demonstrate the feasibility of computing three-dimensional relaxation maps of spin-lattice relaxation time in the rotating frame (T1{rho}) from in vivo magnetic resonance (MR) images of the human patellofemoral joint. T1{rho} was measured by applying a three-dimensional gradient-echo pulse sequence in six healthy subjects and one symptomatic subject by using a 1.5-T MR imager and a 15-cm–diameter transmit-receive quadrature birdcage radiofrequency coil. Average T1{rho} measured in healthy patellar cartilage was 49.7 msec ± 3.2 (mean ± SD). Two-dimensional T1{rho}-weighted images were obtained with a fast spin-echo pulse sequence for comparison. There was good correlation between two-dimensional and three-dimensional T1{rho} values for the six healthy subjects (R2 = 0.88, slope = 1.16).

© RSNA, 2003

Index terms: Arthritis, 45.77 • Cartilage, MR, 45.12141 • Magnetic resonance (MR), three-dimensional


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
Results
 Discussion
 REFERENCES
 
Articular cartilage is a connective tissue consisting of relatively few cells and a highly charged and hydrated extracellular matrix. The constituents of the extracellular matrix are proteoglycans, collagen, noncollagenous proteins, and water (1–3). Early osteoarthritic changes are associated predominantly with loss of proteoglycan. Although collagen content does not change in the early stage, structural changes in collagen have been observed (4,5). Recent developments in chondroprotective therapies, cartilage grafting, gene therapy, and tissue engineering have increased the demand for accurate and noninvasive techniques for detecting in vivo biochemical changes characteristic of the initial stages of cartilage degeneration. Conventional proton magnetic resonance (MR) imaging techniques are capable of depicting the late stages of degeneration, in which visible structural defects are present (6,7). Delayed gadolinium-enhanced proton MR imaging of cartilage, or dGEMRIC (8–10), positively charged nitroxide–based techniques (11), and sodium MR imaging (12–14) have been employed to assess proteoglycan changes in cartilage both in vivo and in vitro. However, these techniques have practical limitations. In delayed gadolinium-enhanced proton MR imaging of cartilage, the long waiting period between contrast agent injection and imaging, as well as variations in relaxivity between tissues, may lead to errors in proteoglycan quantitation. Although sodium MR imaging has high specificity for proteoglycan, it has an inherently low sensitivity, and special radiofrequency (RF) hardware modifications must be made before it can be performed with a routine clinical MR imaging unit.

Spin-lattice relaxation in the rotating frame (T1{rho}) provides another alternative to conventional MR imaging methods. Since this technique was described by Redfield (15), it has been used extensively to investigate low-frequency interactions between macromolecules and bulk water. Exploiting the sensitivity of T1{rho} MR imaging, several authors have investigated the dispersion characteristics of tissues including brain (16,17), tumors (16,18), and articular cartilage (10,19–21). These investigators have demonstrated the potential value of T1{rho} weighting for evaluating various physiologic and pathologic states. The results of several studies have demonstrated that two-dimensional (2D) T1{rho} MR imaging is sensitive to changes in the proteoglycan content of cartilage (19–21). Although these studies demonstrated the potential of T1{rho} MR imaging for assessing cartilage degeneration, they were restricted to single-section imaging and are hence impractical as guides for T1{rho} imaging of a typical anatomic region. The use of single-section techniques in these studies resulted from the need to make the spin-locking pulse section selective. The purpose of this study, therefore, was to investigate the feasibility of computing 3D T1{rho} relaxation maps of the human patellofemoral joint from proton MR imaging data acquired in vivo at 1.5 T.


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
Asymptomatic Subjects
Eight volunteers with a mean age of 34 years (range, 22–46 years), all men, were initially recruited for MR imaging. After the MR imaging protocol was explained fully, all of the participants consented to participate in the study, which was approved by our institutional review board for human studies. Immediately before MR imaging, the volunteers were questioned to determine whether they had a history of knee surgery, knee injury, or current joint pain, swelling, or morning stiffness. Volunteers were considered asymptomatic if they responded in the negative. Two of the eight subjects responded positively and were dropped from the study. The asymptomatic study population therefore consisted of only six volunteers with a mean age of 28 years (range, 22–34 years).

Symptomatic Subject
One 40-year-old symptomatic woman volunteer who had a history of chronic retropatellar pain was believed, on the basis of her clinical symptoms, to have early osteoarthritis.

MR Imaging
All imaging was performed on a 1.5-T whole-body clinical MR imager (Signa; GE Medical Systems, Milwaukee, Wis). A 15-cm–diameter transmit-receive quadrature birdcage RF coil tuned to 63.75 MHz was employed. A diagram of the 3D T1{rho} pulse sequence is shown in Figure 1. The spin-lock magnetization was prepared by using a three-pulse cluster consisting of two hard pulses and a low-power spin-locking pulse (22). The duration of each 90° hard pulse was 200 µsec. T1{rho}-weighted images were acquired with a 3D gradient-echo (GRE) pulse sequence (repetition time msec/echo time msec, 140/2.2; total number of sections, 16; flip angle, 30°; field of view, 10 x 10 cm; section thickness, 3 mm; matrix size, 256 x 128 pixels; bandwidth, 16 kHz; one signal acquired; acquisition time, 4 minutes 48 seconds). For comparison, another set of T1{rho} images was acquired with a 2D fast spin-echo sequence (SE) (22) (repetition time msec/effective echo time msec, 3,000/17; flip angle, 90°; field of view, 10 x 10 cm; number of sections, one; section thickness, 3 mm; matrix size, 256 x 128; echo train length, four; bandwidth, 16 kHz; one signal acquired; acquisition time, 1 minute 42 seconds). The amplitude of the spin-locking pulse ({omega}1 = {gamma}B1/2{pi}) was fixed at 440 Hz, while the TSL was varied systematically from 1 to 38 msec during both 2D and 3D imaging in all subjects (ie, TSL of 1, 10, 20, 30, and 38 msec). Both 2D and 3D imaging were performed in the transverse plane. At 2D imaging, a thick center section was selected to provide anatomic comparison with the 3D image data set. The frequency-encoding direction was anteroposterior across the patella. Fat suppression was achieved at both 2D and 3D imaging by choosing the fat saturation setting on the imager. The total acquisition time per patient for single-section 2D T1{rho} imaging was 8 minutes 30 seconds, and that for multisection 3D T1{rho} imaging was 24 minutes.



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  		Figure 1. Diagram of the pulse sequence used for 3D T1{rho}-weighted MR imaging. The first three pulses (two hard pulses at 90° and a long rectangular spin-locking pulse) prepared the spin-lock magnetization and stored it along the z axis. The strong crusher gradient (black rectangle) was applied before the {alpha} pulse to destroy any residual magnetization in the transverse plane and prevent the formation of unwanted coherences. The stacked lines in the gradient region indicate phase-encoding gradient pulses. TSL = duration of spin-locking pulse.

 
Data Processing
The MR images were processed offline at a Silicon Graphics computer with custom-built software written in IDL data processing language (RSI, Boulder, Colo). The 2D T1{rho} maps were constructed from images acquired with various TSL values and with the image signal intensity data fitted to the following expression (23):

where S(TSL) and S0 are the signal intensity at a particular TSL and at the shortest TSL, respectively.

The 3D T1{rho} maps were constructed from images acquired with various TSL values and with the image signal intensity data fitted to the signal expression obtained by solving the following Bloch equations (16):

where TR is the time between subsequent {alpha} imaging pulses, TSL is the length of the spin-locking pulse, and T1 is the spin-lattice relaxation time constant for the tissue of interest. The image data were fitted to Equation (2) on a pixel-by-pixel basis with a least-squares algorithm based on the assumption that T1 relaxation time for articular cartilage is 1 second (24). Given that actual values of T1 measured in cartilage vary by about 10% (ie, ±100 msec) from this estimated value, we expected to find a maximum of 4% (ie, ±2 msec) error in T1{rho} relaxation times.

The region of interest (ROI) in the patellar cartilage was selected manually on each map by one of the authors (R.R.R.). Each ROI was rectangular and contained approximately 5 x 10 pixels. Average T1{rho} relaxation time was calculated for each ROI.

Validation of 3D T1{rho} Mapping
In order to validate the 3D T1{rho}-mapping technique, we first acquired the 2D and 3D data as a function of TSL at T1{rho} MR imaging of a homogeneous agarose phantom (containing 50 mmol/L saline solution with 4% agarose). We chose an agarose phantom because the MR imaging characteristics of agarose mimic those of cartilage tissue. The signal intensity values from 2D and 3D T1{rho} imaging were fitted to Equations (2) and (3), respectively, on a pixel-by-pixel basis, to generate the T1{rho} maps. ROIs were selected in the same region on both maps, and average T1{rho} relaxation times were calculated and compared.

Specific Energy Absorption Rate
In general, T1{rho}-weighted pulse sequences require more RF power than do conventional sequences that do not include long RF pulses. The Food and Drug Administration (FDA) has suggested that the specific energy absorption rate (SAR) be monitored during MR imaging of each patient to ensure that the standard for maximum SAR is not exceeded. The current limit recommended by the International Electro-technical Commission is 12 W/kg in 1 g of tissue in the extremities for 15 minutes (25). Collins et al (26) calculated the SAR and B1 field distributions in a heterogeneous human head model in a birdcage coil. Since it is impossible to measure the maximum SAR per gram of tissue at in vivo imaging and since there are no published calculations for the knee, we used the numbers calculated by Collins et al as approximations. The SAR of a single pulse with flip angle {alpha} and duration {tau} (in milliseconds) may be calculated with the equation (26)

where SAR(90°,3) is the maximum SAR calculated for a 3-msec rectangular pulse that achieves a flip angle of 90° in a quadrature head coil (equal to 1.46 W/kg in 1 g of tissue at 1.5 T), and f is a shape factor that equals 1 for a hard pulse and 2 for a sinc pulse. The minimum permissible TR for the 3D T1{rho} pulse sequence was calculated by using the SAR values suggested by Collins et al (26):

SAR({alpha}1,{tau}1) was calculated from Equation (3) for all four RF pulses (two 90° hard pulses, the low-power spin-locking pulse, and the sinc pulse) by using 3D T1{rho} imaging parameters. SARFDA is the FDA-specified maximum SAR level and equals 12 W/kg in 1 g of tissue in the extremities.

With reference to the FDA limit, the minimum permissible TR for the 3D T1{rho}-weighted pulse sequence, which was calculated according to the SAR model of Collins et al for a given {omega}1 of 440 Hz and a TSL of 38 msec, was 140 msec. The calculated {sum}SAR({alpha}1,{tau}1) · {tau}1 from all four RF pulses (two 90° hard pulses, the low-power spin-locking pulse, and the sinc pulse) was 1.68 J/kg. Similarly, we also calculated {sum}SAR({alpha}1,{tau}1) · {tau}1 from all eight RF pulses in the 2D T1{rho} pulse sequence (two 90° hard pulses, the low-power spin-locking pulse, and five sinc pulses, for an echo train length of four) to be 2.27 J/kg. There was almost 16 times less energy deposition (0.75 W/kg) in the 2D T1{rho} pulse sequence because of longer TR (3,000 msec) compared with TR in the 3D T1{rho} pulse sequence. Furthermore, we not only used the model developed by Collins et al but we also measured the output power of the RF transmitter to make sure that the FDA-suggested SAR limits were not exceeded. The 1.5-T MR imager that we used monitors the RF power deposition continuously during clinical imaging and will stop if the power exceeds the FDA safety limits.

Intrasubject Variability
A possible source of error in the measurement of 3D T1{rho} relaxation times is the difficulty of reproducing the exact same 3D T1{rho}-weighted imaging sequence over time. We repeated the 3D T1{rho}-weighted imaging protocol five times in one of the subjects (a 22-year-old man), with a 30-minute break between the acquisition of each data set. During this 30-minute period, we removed the subject from the magnet and allowed him to walk around, and then tried to reposition him in the magnet in exactly the same way to achieve the same section measurements and minimize the error in T1{rho} relaxation times.

Data Analysis
All T1{rho}-weighted images and maps (both 2D and 3D) were reviewed by consensus of all authors for the quantitative assessment of relaxation times. Statistical analysis was performed by one of the authors (R.R.R.), who used statistical software (JMP; SAS Institute, Cary, NC) to calculate means, SDs, and 95% CIs for inter- and intrasubject variability. The correlation coefficient (R2) between the experimental data and theoretical fit (for both 2D and 3D T1{rho} relaxation times) was used as a measure of the goodness of the fit.


   Results
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
Discussion
 REFERENCES
 
There was an intrasubject variability of less than 6% (mean ± SD, 47.6 msec ± 2.8) in T1{rho} relaxation times measured in one of the six subjects (see Intrasubject Variability).

The relaxation times (means ± SDs) measured in the agarose phantom at 2D and 3D T1{rho}-weighted imaging were 25.25 msec ± 1 and 25.52 msec ± 1, respectively. There was good agreement between T1{rho} relaxation times measured at 2D imaging and those measured at 3D imaging.

There was clearer demarcation between cartilage and bone marrow (fat) and between cartilage and fluid on 3D T1{rho} images of all subjects than on the corresponding 2D T1{rho} images (Fig 2). The superior fluid-cartilage demarcation and fat suppression on 3D images might be due to the shorter TR (140 msec) and GRE readout.



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  		Figure 2. In vivo transverse T1{rho}-weighted images of the patellofemoral joint in a 30-year-old healthy human volunteer. A, T1{rho}-weighted image obtained with a 2D fast SE pulse sequence (3,000/17, TSL = 10 msec) with {omega}1 of 440 Hz, field of view of 10 x 10 cm, section thickness of 3 mm, matrix of 256 x 128 pixels, bandwidth of 16 kHz, and one signal acquired. B, T1{rho}-weighted image obtained with a 3D GRE pulse sequence (140/2.2, TSL = 1 msec) with {omega}1 of 440 Hz, field of view of 10 x 10 cm, section thickness of 3 mm, matrix of 256 x 128, bandwidth of 16 kHz, and one signal acquired.

 
The average T1{rho} relaxation time measured in the patellar cartilage of the six asymptomatic subjects was 49.7 msec ± 3.2 (mean ± SD), with individual values ranging from approximately 45 to approximately 55 msec—within the 95% CIs. There was an intersubject variability of less than 10% (Table). There was a good correlation in computed T1{rho} relaxation values between 2D images and 3D images even with our small study population (R2 = 0.88, slope = 1.16). Representative transverse 2D and 3D T1{rho} relaxation maps from an image data set of 16 sections acquired in an asymptomatic 30-year-old subject at {omega}1 of 440 Hz are shown in Figure 3.


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  		Intersubject Variation in T1{rho} Relaxation Times Computed from 2D and 3D MR Image Data from Six Healthy Subjects

 


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  		Figure 3. In vivo transverse T1{rho} relaxation maps of the patellofemoral joint in a 30-year-old healthy human volunteer. A, 2D T1{rho} map. B, Representative transverse section of 3D T1{rho} map from a data set of 16 sections. The horizontal rectangular ROI (dotted arrow) and vertical rectangular ROI (solid arrow) were used to compute the average relaxation times and the profile plot, respectively. The bar scale at the right in A indicates variations in T1{rho} relaxation time (0-100 msec).

 
The 3D T1{rho}-weighted image and corresponding relaxation map of the patellofemoral joint in the 40-year-old symptomatic woman showed no macroscopic defect in the cartilage (Fig 4). The T1{rho} relaxation map, however, showed an average T1{rho} relaxation time in the lateral patellar facet of 72 msec ± 3.0—an increase of approximately 45% over the average value in the six healthy subjects.



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  		Figure 4. In vivo transverse T1{rho}-weighted image and corresponding map of the patellofemoral joint in a 40-year-old woman with knee pain. A, 3D T1{rho}-weighted image obtained by using a 3D GRE pulse sequence (140/2.2, TSL = 1 msec) with {omega}1 of 440 Hz, field of view of 10 x 10 cm, section thickness of 3 mm, matrix of 256 x 128, bandwidth of 16 kHz, one signal acquired. B, Representative transverse section of 3D T1{rho} map from a data set of 16 sections. The high signal intensity in the lateral patellar facet (arrow) of cartilage reflects an increase of approximately 45% in T1{rho} relaxation time compared with baseline values. The bar scale at the right in B indicates variations in T1{rho} relaxation time (0-100 msec).

 
The variation in T1{rho} relaxation times across the patellar cartilage depicted on a representative 3D section is shown in Figure 5. The vertical rectangular ROI (solid arrow) shown in Figure 3 indicates the region of profile plotting. The T1{rho} relaxation times varied from 22 to 62 msec; the highest values were measured in the superficial cartilage and the lowest values were measured in the subchondral bone in all subjects.



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  		Figure 5. Profile plot of T1{rho} relaxation times measured in the same healthy subject as in Figure 3; the vertical rectangular ROI (Fig 3, solid arrow) was used for profile plotting. Only 7 pixels were obtained within the patellar cartilage. Each point on the profile plot is an average measurement for an area of 4 x 4 pixels. The T1{rho} relaxation times in superficial regions, at or near the articular surface, are higher than those in medial and subchondral regions.

 

   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
REFERENCES
 
Several investigators have developed and evaluated various MR imaging techniques for studying the early biochemical changes in cartilage that are associated with osteoarthritis (14,19,24,27). The results of a previous study of 2D T1{rho}-weighted MR imaging showed that the relaxation rate (1/T1{rho}) in bovine patellar cartilage decreased linearly with the percentage of proteoglycan loss (19). Compared with this 2D T1{rho}-weighted imaging technique, the 3D T1{rho}-weighted imaging method has two advantages. First, 3D imaging, in contrast to single-section 2D imaging, allows rapid acquisition of images of the entire anatomic region. Second, by suppressing the fluid and fat signals, 3D T1{rho}-weighted MR imaging generates better demarcation than does 2D T1{rho}-weighted imaging between cartilage on the one hand and bone marrow (fat) and fluid on the other. The effect of fat suppression is produced by the pre-encoded GRE pulse sequence included in the 3D pulse cluster instead of the pre-encoded fast SE pulse in the 2D sequence. In the 2D T1{rho}-weighted sequence (with fast SE readout) the four 180° refocusing pulses in the echo train have a decoupling effect (ie, eliminate J-coupling modulation), which results in higher fat signal intensity than that obtained with the 3D T1{rho}-weighted pulse sequence (with GRE readout). Henkelman et al (28) have shown in vivo and in vitro that fat has higher signal intensity on fast SE images than on conventional SE images because of this train of refocusing 180° pulses.

Given the limited number and overall youth of our study subjects, no attempt was made to adjust for intrinsic variables such as age, weight, or level of daily physical activity. Sex had no apparent effect on relaxation times in the medial and lateral facets of the joint. Additional studies in a larger population are needed to evaluate the effects of age (for young adults vs older adults, especially those older than 60 years) and sex on T1{rho} relaxation times.

In summary, the results of our study show that 3D T1{rho} spatial mapping performed with a 1.5-T clinical MR imager can achieve a good signal-to-noise ratio, with a reasonable acquisition time and without exceeding FDA guidelines for specific RF energy absorption rate.


   FOOTNOTES
 
Abbreviations: GRE = gradient-echo, RF = radiofrequency, ROI = region of interest, SE = spin-echo, 3D = three-dimensional, T1{rho} = spin-lattice relaxation time in the rotating frame, TR = repetition time, TSL = duration of the spin-locking pulse, 2D = two-dimensional

Author contributions: Guarantor of integrity of entire study, R.R.R.; study concepts, R.R.R., A.B., R.R.; study design, R.R.R., S.V.S.A., R.R.; literature research, R.R.R., S.V.S.A.; experimental studies, R.R.R., S.V.S.A., A.B.; data acquisition, R.R.R., S.V.S.A.; data analysis/interpretation, R.R.R., S.V.S.A., A.B.; statistical analysis, A.B.; manuscript preparation, R.R.R.; manuscript definition of intellectual content, R.R.R., S.V.S.A., A.B., R.R.; manuscript editing and revision/review, all authors; manuscript final version approval, R.R.R., A.B., R.R.


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 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
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