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DOI: 10.1148/radiol.2203001662
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(Radiology. 2001;220:822-826.)
© RSNA, 2001

Technical Developments

Human Knee: In Vivo T1{rho}-weighted MR Imaging at 1.5 T—Preliminary Experience1

Umamaheswar Duvvuri, MS, Sridhar R. Charagundla, MD, PhD, Sagar B. Kudchodkar, MS, Jonathan H. Kaufman, PhD, J. Bruce Kneeland, MD, Rahim Rizi, PhD, John S. Leigh, PhD and Ravinder Reddy, PhD

1 From the Department of Radiology, University of Pennsylvania Medical Center, Philadelphia. Received October 16, 2000; revision requested November 26; revision received February 15, 2001; accepted March 9. Supported by grants AR45242 and AR45404 from the National Institute of Arthritis and Musculoskeletal and Skin Diseases and National Institutes of Health. Address correspondence to U.D., B-1 Stellar-Chance Laboratories, 422 Curie Blvd, Philadelphia, PA 19104-6100 (e-mail: uduvvuri@mail.med.upenn.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 
A fast spin-echo sequence weighted with a time constant that defines the magnetic relaxation of spins under the influence of a radio-frequency field (T1{rho}) was used in six subjects to measure magnetic resonance (MR) relaxation times in the knee joint with a 1.5-T MR imager. A quantitative comparison of T2- and T1{rho}-weighted MR images was also performed. Substantial T1{rho} dispersion was demonstrated in human articular cartilage, but muscle did not demonstrate much dispersion. T1{rho}-weighted images depicted a chondral lesion with 25% better signal-difference-to-noise ratios than comparable T2-weighted images. This technique may depict cartilage and muscular abnormalities.

Index terms: Cartilage, 4521.121411, 4521.121415 • Cartilage, MR, 4521.121411, 4521.121415 • Knee, arthritis, 452.77 • Knee, MR, 452.121411, 452.121415, 452.121416 • Muscles, MR, 459.121411, 459.121415


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
 Results
 Discussion
 REFERENCES
 
Spin-lattice relaxation in the rotating frame is characterized by the time constant that defines the magnetic relaxation of spins under the influence of a radio-frequency field (T1{rho}). A spin-locking (SL) experiment was described by Redfield (1), and it has been used to investigate the slow-motion interactions that cause relaxation (1,2). The increase in T1{rho} that occurs as the strength of the SL field is increased has been termed T1{rho} dispersion. The dispersion profile contains information about the spectral density functions and elucidates relaxation mechanisms.

The dispersion characteristics of biologic tissues, including rat muscle, brain, spleen, and bovine cartilage tissue, have been investigated in vitro (3–6). The usefulness of T1{rho} magnetic resonance (MR) imaging for studying cartilage degeneration has been investigated by several authors (4,6,7). Changes in T1{rho} were observed in proteoglycan-depleted bovine tissue but not in collagenase-treated tissue (6). Koskinen et al (4) and Mlynarik et al (7) found that T1{rho} was elevated in ex vivo arthritic human tissue. Findings in these studies demonstrate the potential role of T1{rho}-weighted MR imaging in the detection of osteoarthritis.

Sepponen et al (8) reported a method to perform T1{rho}-weighted MR imaging in vivo in 1985. In other studies, T1{rho}-weighted MR imaging has demonstrated intramuscular tumors in rat models (9). In vivo T1{rho}-weighted MR imaging of various human tumors at low field strength has also been reported (10–12). Findings in these studies demonstrated that T1{rho} weighting may be useful in the evaluation of a variety of pathologic states. To our knowledge, the literature about T1{rho}-weighted MR imaging performed at clinical field strengths is sparse.

The goals of this study were to evaluate the feasibility of performing SL MR imaging with a 1.5-T clinical MR imager, to measure T1{rho} and T1{rho} dispersion in the tissues of the musculoskeletal system in vivo, and to compare T1{rho}-weighted MR images with conventional T2-weighted fast spin-echo MR images.


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
A T1{rho}-weighted fast spin-echo sequence was implemented with a 1.5-T MR imaging system (Signa, version 5.8 software; GE Medical Systems, Milwaukee, Wis). The sequence diagram is shown in Figure 1. A spin-echo version of this sequence has been reported previously (6). The sequence generates T1{rho} weighting by preparing the magnetization with an SL pulse cluster, which consists of 90°, SL, and 90° pulses. The first 90° pulse (duration, 200 µsec) tips the magnetization into the y axis. The SL pulse is applied along this direction and spin-locks the magnetization vector in the transverse plane. The second 90° pulse brings the magnetization back into the z axis. The T1{rho}-weighted magnetization can now be imaged with a conventional two-dimensional sequence. A standard quadrature-driven birdcage coil was used for all acquisitions.



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  		Figure 1. Schematic depicts the pulse sequence for T1{rho}-weighted fast spin-echo MR imaging. The magnetization was prepared with the SL pulse cluster, which consists of 90°, SL, 90° pulses. The magnetization underwent T1{rho} relaxation during the time of spin locking, which generated T1{rho} weighting. A crusher gradient (G) was used after the SL pulse cluster to dephase any residual transverse magnetization. The magnetization was then imaged with a standard two-dimensional fast spin-echo sequence. T2 relaxation occurred during the echo time and during the collection of the echo trains. Only three echos are shown for the sake of clarity. FREQ = frequency, 1H RF = proton radio frequency, TSL = time of the SL pulse, and {pi} = 180° refocusing pulse.

 
This study was approved by our institutional review board for human studies. Five healthy adult volunteers (three men, two women) and one male volunteer with a history of anterior knee pain (age range, 25–34 years; mean age 27.6 years ± 3.65 [SD]) underwent MR imaging after informed consent was obtained.

T1{rho}-weighted MR imaging was performed with the following parameters: repetition time msec/echo time (effective) of 2,000/22; echo train length of four; matrix of 256 x 128 with one signal acquired; field of view of 16 x 16 cm; bandwidth of 16 kHz; SL times of 10, 30, 50, and 70 msec; acquisition time of 1 minute 4 seconds per image. The effective echo time of the sequence was reported but not the interecho spacing (13). The amplitude of the SL pulse was set to the following values: 14.1, 29.36, 58.73, and 88.1 mG, to allow measurement of T1{rho} dispersion in vivo. The frequency-encoding direction was along the thickness of the cartilage. Fat saturation was used to improve cartilage demarcation. By using a pixel-by-pixel least-squares fitting algorithm (IDL software; Research Systems, Boulder, Colo) to generate T1{rho} maps, the signal intensity (SI) values on the T1{rho}-weighted images were then fit to the following equation: SI = SI0 exp(-TSL/T1{rho}), where TSL is the time of the SL pulse.

T2 values were measured by acquiring single-echo spin-echo MR images with the same parameters except for the following: 2,000/10, 30, 50, 70; field of view of 16 x 16 cm; matrix of 256 x 128 with one signal acquired; acquisition time of 4 minutes 16 seconds per image. T2 maps were calculated in the same manner as were the T1{rho} maps, except the SI was fit as a function of the echo time. The goodness of fit of the relaxation time calculations was determined by computing the correlation coefficient for each pixel. Pixels that were fit with r < 0.95 were discarded from the maps and were not used in any further analysis. The relaxation times were measured by defining regions of interest in the various tissue groups.

The signal-to-noise ratio (SNR) of cartilage and muscle and the signal-difference-to-noise ratio (SDNR) between cartilage and fluid on T1{rho}-weighted MR images were compared with those on T2-weighted images acquired with parameters commonly used at our institution for the imaging of cartilage. T2-weighted images were obtained with the following parameters: 2,000/60, echo train length of four, matrix of 256 x 192, two signals acquired, bandwidth of 16 kHz, field of view of 16 x 16, 4-mm-thick sections with 0.5-mm gap, and imaging time of 3 minutes 12 seconds per image. T1{rho}-weighted MR images were acquired with the same parameters as were used to obtain the T2-weighted MR images, with the total spin-evolution SL time (SL time plus echo time) equal to 60 msec, and imaging time of 3 minutes 12 seconds per image. The T1{rho}- and T2-weighted MR images were compared. Intermediate-weighted images were acquired with the same parameters, except 2,000/22, echo train length of four, and imaging time of 3 minutes 12 seconds per image. Fat saturation was also used to improve the cartilage-to-fat contrast. The relaxation times and image characteristics of both muscle and cartilage were evaluated.

The MR imaging protocol was also used to examine a volunteer with a history of knee pain secondary to a sports-related injury. Mild arthritis was diagnosed on the basis of the clinical symptoms. Radiographs demonstrated no changes in the thickness of the cartilage in the knee. An experienced musculoskeletal radiologist (J.B.K.) reviewed the T1{rho}- and T2-weighted MR images and concluded, on the basis of the criteria of McCauley et al (14), that the abnormally hyperintense area was indicative of degenerative joint disease. The symptomatic volunteer underwent MR imaging on three occasions with identical results. Relaxation times were measured at one of the MR imaging sessions.

The SNR and SDNR were measured by determining the SI values from regions of interest in the patellar cartilage and gastrocnemius muscle. Noise (N) values were measured as SDs from regions of interest outside anatomic structures in the frequency-encoding direction with the following equations: SNR = SI/N and SDNR = (SIA - SIB)/N, where SIA and SIB are the mean SI values in tissues A and B.

The statistical significance of the changes in the signal-difference-to-noise and SNRs was determined with a Student t test. Analysis of variance was used to test for differences between T1{rho} measurements obtained at different SL strengths. A post hoc Tukey test was used to determine where statistically significant changes occurred. All analyses were. performed with software (SIGMASTAT; SPSS, Chicago, Ill). A P value of .05 was considered significant.


   Results
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 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
Discussion
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The Table lists the relaxation times of cartilage and muscle in the healthy volunteers. The T1{rho} values were uniformly larger than the T2 values. Articular cartilage demonstrated T1{rho} dispersion in the 0-375-Hz frequency range (P < .001, analysis of variance). This finding demonstrated the T1{rho} dispersion of human cartilage in vivo. At the lowest amplitude of the SL pulse field of 60 Hz, T1{rho} was approximately equal to T2. However, an SL field strength of 375 Hz caused T1{rho} to increase by approximately 45% relative to T2. Statistically significant T1{rho} dispersion was not observed in the 0–60-Hz frequency range (P = .998, Tukey test) or in the 125–250-Hz frequency range (P = .81, Tukey test). However, significant dispersion was noted in the 60–125-Hz frequency range (P = .001) and in the 250–375-Hz frequency range (P = .002). Dispersion of muscle T1{rho} was also observed (P = .004, analysis of variance). Muscle T1{rho} increased by 8.5% over the 60–375-Hz frequency range. In contrast, T1{rho} of cartilage increased by 44% over the same frequency range.


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  		Relaxation Times of Cartilage and Muscle Tissue in Healthy Adult Volunteers

 
Figure 2 shows transverse T2- and T1{rho}-weighted MR images acquired at the level of the patellofemoral joint in a volunteer. The T1{rho}-weighted MR image in Figure 2, A, was acquired with 2,000/22, an amplitude of the SL pulse of 375 Hz, and an SL time of 38 msec. The T2-weighted image of the same section in Figure 2, B, was acquired with 2,000/60. The total spin-evolution time was the same for both images (ie, the total time during which the magnetization was allowed to relax in the transverse plane was the same for both images). The improvement in SNR on the T1{rho}-weighted MR image compared with the T2-weighted image led to a clear demarcation of the cartilage tissue at the bone-cartilage interface.



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  		Figure 2. Transverse MR images depict the same section of cartilage in a 28-year-old male volunteer with no history of knee pain. A, T2-weighted fast spin-echo MR image (2,000/60). B, T1{rho}-weighted MR image (2,000/22; SL time, 38 msec; amplitude of the SL pulse, 375 Hz). Both images were obtained with the following parameters: 256 x 192 matrix, two signals acquired, 16-kHz bandwidth, 4-mm section thickness, mean in-plane resolution of 469 µm ± 625. In B, the cartilage (white arrows) is depicted more clearly presumably owing to the higher SNR.

 
The T2- and T1{rho}-weighted MR images were quantitatively compared on the basis of the SDNRs for various tissue pairs. The SDNR between synovial fluid and cartilage decreased by approximately 13% (P = .6, t test) on the T1{rho}-weighted MR images (22.33 ± 5.50) compared with the T2-weighted MR images (25.98 ± 8.09). However, the SNR of cartilage was 20% larger on the T1{rho}-weighted images (17.76 ± 2.12) when compared with the T2-weighted MR images (21.14 ± 1.69, P = .04, t test). Similarly, the SNR of muscle was 28% larger on the T1{rho}-weighted MR images (13.21 ± 2.20) when compared with the T2-weighted images (10.34 ± 2.95, P = .008, t test).

Figure 3 shows the T2- and T1{rho}-weighted MR images obtained in the volunteer with early degenerative joint disease. A bright area was seen in the cartilage on both the T1{rho}- and T2-weighted MR images. However, the lesion was more clearly demarcated on the T1{rho}-weighted MR images, on the basis of SDNRs (25%). The T2 of the normal-appearing cartilage was 34.2 msec. The T1{rho} of the normal-appearing cartilage at an SL field strength of 0.088 G was 46.8 msec. The bright area had a T2 of 66 msec. The T1{rho} of this area was 107 msec. The T2 of synovial fluid was about 180 msec at 1.5 T (15).



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  		Figure 3. Transverse fat-saturated MR images depict the same section of cartilage in a 25-year-old male volunteer with knee pain. A, T2-weighted fast spin-echo MR image (2,000/60). B, T1{rho}-weighted MR image (2,000/38, 22; amplitude of the SL pulse of 88 mG). Both images were obtained with the following imaging parameters: mean in-plane resolution of 625 µm ± 833, section thickness of 4 mm, bandwidth of 16 kHz, two signals acquired per phase encode. In B, the arrow points to an area of hyperintensity, which is consistent with degenerative disease. A similar area is also seen in A. The contrast between the hyperintense area and normal-appearing cartilage was approximately 25% greater in B than in A.

 

   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
REFERENCES
 
T1{rho} provides a convenient method to probe the slow-motion components of the spectral-density functions that cause relaxation (16). T1{rho} measurements are sensitive to relaxation mechanisms that satisfy the condition {omega}SL{tau} ~ 1, where {omega}SL is the SL power (measured in rad [1 Gy = 100 rad] per second) and {tau} is the correlation time. When adiabatic half-passage or off-resonance SL methods are used (8,17), the relaxation analysis becomes much more complex. To understand these relaxation mechanisms, any off-resonance effects must be explicitly accounted for (18). The current technique avoids these problems and can be easily implemented with any clinical MR imaging system.

We found that muscle showed very little dispersion in the 0–375-Hz frequency range. This result was consistent with the report of Rommel et al (9), which showed that T1{rho} increased from approximately 30 to 40 msec in the 100–500-Hz frequency range. Relaxation measurements in our study showed that the T1{rho} dispersion in human muscle in vivo was small but statistically significant.

In contrast, the T1{rho} of articular cartilage exhibited a large overall increase with SL strength in the 0–375-Hz frequency range. The dispersion characteristics indicated that processes with correlation times in the submillisecond range contributed to T1{rho} in articular cartilage and skeletal muscle. The more pronounced T1{rho} dispersion of cartilage, when compared with that of muscle, indicated that these slow-motion processes played a larger role in cartilage T1{rho}. Several physical mechanisms might be responsible for this type of dispersion behavior. Further experimentation is required to separate these mechanisms. However, we postulate that (a) diffusion (19) and (b) chemical exchange modulated by spin coupling (20) are mechanisms that may be responsible for the dispersion behavior.

The T1{rho} dispersion characteristics of bovine articular cartilage in vitro have been reported previously (6). Statistically significant dispersion was reported in the 0–500-Hz frequency range for both native and enzymatically treated tissue. For this reason, we used only low SL frequencies for the human studies. The use of low SL field strength also reduced any tissue heating that may be caused by the SL pulse. T1{rho}-weighted fast spin-echo sequences can be used at 1.5 T without exceeding limits in specific absorption rate (21). In this study, we obtained high-quality images with low SL pulse powers.

The increased T1{rho} of cartilage (compared with the T2) led to an increase inthe SNR of cartilage on the T1{rho}-weighted MR images. This allowed a clearer demarcation of the cartilage, with a total spin-evolution time equivalent to T2 weighting. The lack of T1{rho} dispersion of synovial fluid caused the fluid SI to remain fairly constant between the T1{rho}- and T2-weighted MR images. The cartilage SI was higher on the T1{rho}-weighted MR images while the fluid SI remained fairly constant; therefore, the SDNR between fluid and cartilage was somewhat reduced on the T1{rho}-weighted compared with the T2-weighted MR images.

Mlynarik et al (7) found T1{rho} changes in ex vivo diseased human tissue. The data in our study indicate that T1{rho} is more effective than T2 at highlighting chondral abnormalities. More important, hyperintense regions on T1{rho}-weighted MR images might indicate subtle changes in the biophysical properties of the tissue. Several authors have shown changes in water content and proteoglycan content in arthritic tissues (22,23). These changes in the macromolecular composition of the tissue could cause an elevation in T1{rho}. Further studies that prospectively compare MR imaging with arthroscopy and clinical symptoms are needed to establish the clinical usefulness of T1{rho}-weighted MR imaging.

The T1{rho} relaxation and dispersion data presented herein are important for optimizing the T1{rho}-weighted MR imaging of the musculoskeletal system. T1{rho}-weighted MR imaging is promising in the study of muscular dystrophies and myositis (24,25). Dystrophic muscle exhibited less T1{rho} dispersion than did normal muscle tissue. This was attributed to the increased fatty content of dystrophic muscle. Inflamed muscle had a longer T1{rho} than normal muscle, although the dispersion characteristics of the diseased muscle were not measured. The low spatial resolution of approximately 20 mm3 and the long acquisition times limit the clinical applicability of adiabatic half-passage methods; the T1{rho}-weighted fast spin-echo technique used in this study could help in these types of studies in the future.

The strength of the SL pulse is often difficult to calibrate. The simplest calibration method is to compare the amplitude of the SL pulse with that of another known pulse. This is difficult in most MR imaging schemes, since the other MR imaging pulses, such as adiabatic pulses, are generally soft pulses. In the pulse sequence used in this study, the SL power is easily calibrated by calculating the area under the rectangular 90° pulses and comparing it with the area under the SL pulse. The drawback to this type of ex-periment is the requirement for accurate 90° flip angles, which necessitates the use of homogeneous volume coils.

In conclusion, we have shown that SL MR imaging can be performed with a clinical imager to generate high-quality T1{rho}-weighted MR images with SNRs superior to those for comparable T2-weighted MR images. Furthermore, a potential cartilage lesion was depicted 25% more clearly on T1{rho}-weighted MR images than on T2-weighted MR images. T1{rho}-weighted MR imaging generates novel contrast and might be useful for the diagnosis of articular cartilage disease.


   FOOTNOTES
 
Abbreviations: SDNR = signal-difference-to-noise ratio, SI = signal intensity, SL = spin locking, SNR = signal-to-noise ratio, T1{rho} = time constant that defines the magnetic relaxation of spins under the influence of a radio-frequency field

Author contributions: Guarantor of integrity of entire study, U.D.; study concepts, U.D., J.S.L., R. Reddy; study design, U.D., S.R.C., J.H.K., S.B.K.; literature research, S.R.C., S.B.K., U.D.; experimental studies, U.D., S.R.C., J.H.K., S.B.K.; data acquisition, U.D., R. Rizi, S.R.C., J.H.K., S.B.K.; data analysis, U.D., S.R.C., J.H.K.; statistical analysis, U.D.; manuscript preparation, all authors; definition of intellectual content, U.D., R. Reddy, J.S.L.; manuscript editing and review, all authors; manuscript final version approval, U.D., J.B.K., R. Reddy, J.S.L.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 

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