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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
Osteoarthritis Cartilage. Author manuscript; available in PMC Mar 1, 2011.
Published in final edited form as:
PMCID: PMC2826588
NIHMSID: NIHMS161839

FUNCTIONAL CARTILAGE MRI T2 MAPPING: EVALUATING THE EFFECT OF AGE AND TRAINING ON KNEE CARTILAGE RESPONSE TO RUNNING

Timothy J. Mosher, MS, MD,1 Yi Liu, MD,2 and Collin M. Torok, MD3

Abstract

Objective

To characterize effects of age and physical activity level on cartilage thickness and T2 response immediately after running.

Design

Institutional review board approval was obtained and all subjects provided informed consent prior to study participation. Cartilage thickness and MRI T2 values of 22 marathon runners and 15 sedentary controls were compared before and after 30 minutes of running. Runner and control groups were stratified by age ≤ 45 and ≥ 46 years. Multi-echo (TR/TE 1500 ms/9 –109 ms) MR images obtained using a 3.0 T scanner were used to calculate thickness and T2 values from the central femoral and tibial cartilage. Baseline cartilage T2 values, and change in cartilage thickness and T2 values after running were compared between the four groups using 1-way ANOVA.

Results

After running MRI T2 values decreased in superficial femoral (2 ms to 4 ms) and tibial (1 ms to 3 ms) cartilage along with a decrease in cartilage thickness: (femoral: 4% to 8%, tibial: 0% to 12%). Smaller decrease in cartilage t2 values were observed in the middle zone of cartilage, and no change was observed in the deepest layer. There was no difference cartilage deformation or T2 response to running as a function of age or level of physical activity.

Conclusions

Running results in a measurable decrease in cartilage thickness and MRI T2 values of superficial cartilage consistent with greater compressibility of the superficial cartilage layer. Age and level of physical activity did not alter the T2 response to running.

Keywords: Cartilage, Osteoarthritis, Magnetic Resonance Imaging, Exercise, Knee

INTRODUCTION

A primary function of articular cartilage is absorption and redistribution of biomechanical forces applied to the joint through activities of daily living. While controlled laboratory experiments provide quantitative information on biomechanical forces in cartilage, ultimately it is necessary to extrapolate this information to the intact human joint. For future research applications it would be valuable to have quantitative non-invasive techniques to evaluate long-term and short-term effects of exercise on cartilage.

The capability of magnetic resonance imaging (MRI) to directly visualize articular cartilage provides a means to evaluate function in the intact human joint. High-resolution 3- dimensional (3D) gradient echo techniques provide reproducible measures of cartilage volume and mean thickness that can be used to assess tissue deformation in response to compressive loading (1). These techniques have been used to measure cartilage deformation in excised samples (2) and cadaver joints (3, 4) under static load, and human joints following exercise (58). Using techniques such as T2 mapping it is possible to detect changes in MRI relaxation properties that occur when cartilage is compressed (9, 10). Cartilage compression decreases water content and alters collagen fiber orientation of the extracellular matrix, which influences the transverse relaxation time (T2) (11). Initial feasibility studies have detected bulk changes in patellar cartilage T2 during recovery from deep knee bends (12), and depth-dependent changes in cartilage T2 after running (13)..

Previous studies have shown that elevation in cartilage T2 results from a loss of structural anisotropy of the type II collagen matrix as well as a concomitant increase in cartilage water and decrease in collagen content (11). A recent study by Stahl et al demonstrated longer cartilage T2 values in asymptomatic physically active individuals (14) compatible with degenerative changes in the collagen matrix. Similarly we previously demonstrated an age dependent elevation of cartilage T2 in asymptomatic individuals over age 45 years (15, 16). It remains to be determined if structural changes in the collagen matrix observed with higher levels of physical activity and age alter the cartilage T2 response to exercise.. Thus the purpose of this study is to characterize the effect of age and physical activity level on cartilage thickness and regional T2 changes immediately after running.

MATERIALS AND METHODS

Study Population

Self described marathon runners were recruited from three local community based running clubs using print advertisement. Sedentary volunteers matched for age were recruited from the community using print advertisements and screened to exclude volunteers with regular participation in a running exercise program over the past 5 years. All subjects were greater than 18 years of age. Exclusion criteria for both groups consisted of a known contraindication for MRI, history of prior trauma, orthopedic surgery, chronic disease requiring medical treatment, and joint pain or stiffness indicated by a score of 10 or greater on the Western Ontario and McMasters Universities (WOMAC) Osteoarthritis Index (visual analogue). After the nature of the procedure was explained, all participants provided informed consent to participate in the study, which was approved by the institutional review board. Subjects completed a questionnaire to determine the average number of miles of running completed per week over the past year, the number of years the individual participated in an active running program, and the number of marathons entered. Additional demographic data collected at time of the MRI study included age, height, and weight. Body mass index (BMI) was calculated by dividing weight in kilograms by the square of height in meters.

For analysis the study population was divided into four cohorts based on age ≤ 45 years and history of running exercise. This resulted in four cohorts: Young Control (YC: age ≤ 45, sedentary) Young Marathoners (YM: age ≤ 45, marathon training), Old Control (OC: age ≥ 46, sedentary), and Old Marathoners (OM: age ≥ 46, marathon training).

MRI Data Acquisition

All MRI studies were conducted in the morning to minimize potential diurnal effects on cartilage T2 measurements. Subjects were randomized for study of either the right or left leg. To minimize variation in location of the cartilage T2 measurements, the study leg was stabilized with an MRI compatible holder that attached directly to the MRI table. This device was adjusted to place the inferior pole of the patella in the center of the radiofrequency (RF) coil with the knee in less than 5 degrees of flexion. In addition to calibrated positioning of the knee within the MRI scanner in all 3 anatomic planes, the device also allows for precise internal/external rotation of the leg. Using this technique the reproducibility of femoral/tibial cartilage T2 measurements has been studied and found to be 3% CV% (17).

Quantitative MRI T2 maps were acquired with a Bruker 3.0 T MR imaging-spectrometer (Medspec S300; Bruker Instruments, Ettlingen, Germany) using a dedicated 24 cm gradient insert delivering ± 6 gauss/cm, and a 15 cm linear Litz coil (Doty Scientific, Columbia, South Carolina, USA) as previously described (18). Sagittal multi-slice multi-echo (MSME) source images of the femoral tibial joint were obtained from a 6 section, 12 echo sequence with TR/TE = 1500 ms/9–108 ms, 75.8 kHz bandwidth, 4 mm section thickness, 384 x 384 matrix and a 12.75 cm field of view (FOV) using a linear sampling of k-space. Of the 6 sections acquired, 3 sections were obtained from the medial, and 3 sections were obtained from the lateral femoral tibial compartment. This targeted the analysis to the thickest region of cartilage, and further decreased magic angle effects by excluding peripheral cartilage near the tibial eminence and margin of the tibial plateau where oblique orientation of the collagen matrix has been shown to increase T2 weighted signal (19). The resultant pixel resolution was 0.33 mm. Total image acquisition time was 9.6 minutes.

Exercise Protocol

After completing the baseline MRI examination subjects were instructed to jog for 30 minutes on an asphalt trail located adjacent to the MRI facility. The protocol did not control for distance or intensity of running. Immediately after completing the exercise, subjects were repositioned in the MRI scanner using the positioning device to place the knee in the same position as the baseline scan. To minimize set-up time, we did not adjust tuning and matching parameters of the RF coil or magnetic field homogeneity between the baseline and follow-up scan. A second set of MSME MR images were obtained using acquisition parameters and scan locations identical to the baseline study. The total time to reposition the subject in the MRI scanner and acquire the MRI T2 mapping data was less than 15 minutes after completion of exercise.

Data Analysis

MRI T2 maps

Magnitude images and T2 maps were calculated from 11 spin-echo images by means of linear least squares curve fitting, on a voxel-by-voxel basis with CCHIPS/IDL software (Cincinnati Children’s Hospital Image Processing Software/Interactive Data Language, (RSI, Inc. Boulder, CO) (18). The first of the 12 echoes was excluded from the fit to reduce error resulting from signal produced by stimulated echoes (20). Prior spectroscopic measurements have demonstrated a mono-exponential T2 decay of normal cartilage (21), thus fitting of the signal intensity (SI) for the ith, jth voxel as a function of time, t, can be expressed as follows:

SIi,j(t)=SI0i,j·exp(t/T2i,j),

Where SI0i,j is the voxel intensity at t = 0 and T2i,j is the T2 time constant of voxel i,j. A magnitude image is generated from the voxel SI0i, j data, and a T2 map is generated from the T2i,j data (22). Magnitude images were analyzed in gray scale, and quantitative T2 maps were analyzed as a color-coded image, using an ordinal rainbow scale.

Cartilage thickness and T2 profiles

For quantitative analysis, regions of interest (ROIs) were generated by semi-automated segmentation of the central zone of femoral and tibial cartilage from all six sections using an interactive subroutine in the CCHIPS/IDL software. Femoral and tibial cartilage was analyzed separately. As illustrated in Figure 1, anterior and posterior borders of the menisci were used to define the margins of the femoral and tibial cartilage ROI. For each ROI the software automatically generated multiple perpendicular tangents to the cartilage/bone interface, terminating at the articular surface. On average (± standard deviation) 1147 ± 281 tangents were generated for each subject (range 593 to 1879 tangents). Cartilage thickness was estimated by calculating the average length in millimeters of the computer generated tangents before and after running.

FIGURE 1
Anatomic landmarks are indicated on a representative sagital 3.0 T source image (TR/TE: 1500ms/36ms) obtained from the lateral femoral/tibial compartment. The anterior and posterior margin of the meniscus (dashed lines) define the boundaries for the cartilage ...

To determine if there were regional differences in response of cartilage to exercise a subset analysis was performed in which cartilage ROIs were separately generated from the medial and lateral knee compartments. This subset analysis used regional ROIs from the central femoral and tibial cartilage, defined as the uncovered portion of cartilage between the free edge of the anterior and posterior meniscal horns; and from the posterior region of cartilage covered by the posterior meniscal horn. As illustrated in Figure 1 this produced 8 subregions: central medial femoral condyle (cMF), posterior medial femoral condyle (pMF), central medial tibia (cMT), posterior medial tibia (pMT), central lateral femoral condyle (cLF), posterior lateral femoral condyle (pLF), central lateral tibia (cLT), and posterior lateral tibia (pLT) (23).

Spatial variation in cartilage T2 was evaluated by generating T2 profiles for each cohort where T2 is determined as a function of normalized distance from bone. In the first step of this analysis the T2 of each voxel in the cartilage ROIs was evaluated as a function of distance from bone using the computer generated tangents described for analysis of cartilage thickness. On average (± standard deviation) 5819 ± 2377 voxels were evaluated for each subject (range 2167 to 13291 voxels). Second, to allow comparison between individuals with different cartilage thickness, the length of each tangent was divided by cartilage thickness to yield a normalized distance where cartilage at the subchondral surface has a normalized distance of 0.0, and cartilage at the articular surface has a normalized distance of 1.0. Third, for each subject, voxels were clustered into 3 equal zones based on normalized distance from bone. The deep zone was comprised of voxels with a normalized distance of 0.0 to 0.35, middle zone 0.36 to 0.66, and superficial zone 0.67 to 1.0. The mean T2 value was calculated for each zone. Fourth, to determine the mean T2 for each cohort, mean T2 values for each subject in the group were pooled and the mean T2 ± standard deviation was calculated for each zone.

The average baseline T2 value for each zone and femoral and tibial cartilage thickness was compared pair-wise between groups using 1-way analysis of variance (ANOVA) with Tukey error protection at a 95% confidence interval. To determine the response of cartilage T2 to exercise, baseline and post-exercise cartilage thickness and T2 values for each zone were compared using a paired samples t-test for each group. The difference between baseline and post exercise endpoints was considered statistically significant if the 2-tailed p-value was less than .05. The difference in femoral and tibial cartilage T2 and thickness was calculated for each subject, and then pooled to calculate mean change and standard deviation for each cohort. Change in cartilage T2 and thickness after exercise was compared between the four groups using 1-way ANOVA (Statistical package: Analyse-it Software, Ltd, Leeds, United Kingdom).

RESULTS

Study Group

Demographic information on the study population is presented in Table 1. The study population had a bimodal age distribution with a mean age of the younger cohorts of 27.0 years (range 19 to 40) and older cohorts with a mean age of 53.1 years (range 46 to 64). Although not statistically significant, sedentary controls were slightly older than the marathoners (YC age (s.d): 28.4 years (6.3), versus YM: 25.7 (5.0), OC: 54.0 (5.2), versus OM: 52.6 (4.8) and had a higher BMI (YC): 25.4 kg/m2 (3.9), versus YM: 24.0 (2.6), OC: 25.5 (3.2), versus OM: 23.4 (3.3) All subjects had a BMI < 30. In the running groups 7 of 22 subjects had a BMI > 25 kg/m2, while in the sedentary groups 6 of 15 subjects had a BMI > 25 kg/m2. All runners averaged 10 miles or more of running per week. Twelve of the 22 runners reported more than 5 years of marathon training. Except for the two youngest runners, age 19 and 21, all subjects in the running cohorts had participated in at least one marathon. Older runners averaged more miles per week and on average had more than twice the number of years of training compared to younger marathoners. Except for two subjects in the young control cohort that reported occasionally running 5 miles per week over the past two years, none of the sedentary control subjects reported a history of running exercise.

TABLE 1
Demographic summary of study population: mean (s.d)

Cartilage Thickness

The thickness of femoral and tibial cartilage pre- and post-exercise is presented in Figure 2. For each age group the thickness of femoral cartilage was greater in marathoners compared to sedentary controls. In older groups this differences was statistically significant (difference in thickness: 0.50 mm Tukey 95% confidence interval (CI): 0.05mm to 0.94 mm). A similar pattern was observed in tibial cartilage; however, there was no statistically significant difference between groups. Although there was a trend toward thinner cartilage in the older sedentary cohort, this was not statistically different when compared to either the young marathoners or control groups.

FIGURE 2FIGURE 2
Graphs of mean thickness (± standard error of the mean) for (a) femoral and (b) tibial cartilage before (grey bar) and after (black bar) 30 minutes of running exercise for the 4 groups: YC – young control group, YM – young marathoner ...

Both femoral and tibial cartilage thickness decreased in 31 of 37 subjects (84%) after running. As indicated in Figure 2, for young control and marathoners the mean decrease in femoral and tibial cartilage thickness was statistically significant (p<.05). In older control and marathoner groups the mean decrease in femoral and tibial cartilage thickness after running was less than that observed in the younger subjects, and was not statistically significant.

Cartilage T2

Representative cartilage T2 maps are presented in Figure 3.. All subjects demonstrated similar spatial dependency of cartilage T2 as a function of normalized distance from bone. Focally high T2 values indicated by red pixels were observed near the bone cartilage interface, decreasing in the deep 20% to 30% of cartilage, and then increasing monotonically toward the articular surface. None of the subjects demonstrated evidence of focal cartilage defects, or focal T2 signal abnormalities in the limited regions of the femoral and tibial surfaces evaluated in this protocol. No additional morphologic images were obtained that could potentially identify focal cartilage lesions in other regions of the knee. Subjectively the T2 maps demonstrated greater heterogeneity in older subjects compared to younger individuals independent of their level of training.

FIGURE 3FIGURE 3
Representative quantitative sagittal cartilage T2 maps from two runners (A) 25-year-old female runner with 10 years of running experience, averaging 12 miles per week. (B) 47 year old male runner with 15 years of experience, averaging 20 miles per week. ...

The zonal dependency of cartilage T2 is observed in the baseline values presented in Figure 4. Compared to tibial cartilage, femoral cartilage has longer T2 values and demonstrates greater variation with depth from the articular surface. At all locations, the T2 values were longer in older groups compared to younger subjects, however this difference was not statistically significant. We did not observe a statistically significant effect of physical activity level on baseline cartilage T2 values. For younger subjects, T2 values were increased in marathoners compared to the young sedentary controls; however, this trend was not observed in older subjects.

FIGURE 4FIGURE 4
Baseline cartilage T2 values as a function of depth from the articular surface for (A) central femur and (B) tibia cartilage. There was no statistically significant difference in baseline cartilage T2 values as a function of age or level of physical activity. ...

The change in cartilage T2 immediately after running is presented in Figure 5.. In both femoral and tibial cartilage there are differences in the T2 response with respect to distance from the articular surface. After exercise the greatest decrease in cartilage T2 occurs in the superficial zone. Smaller decreases in T2 are observed in the middle zone. No statistically significant change is observed in the deep zone near the bone cartilage interface. In comparing the four groups, there was no statistically significant difference in change of cartilage T2 as a function of age or level of physical activity.

FIGURE 5FIGURE 5
Change in cartilage T2 values after 30 minutes of running for (A) central femur and (B) tibia cartilage. (*) indicates the changes in cartilage T2 was statistically significant (p <.05). For all groups there was a statistically significant decrease ...

Regional response of cartilage to exercise

With the regional subset analysis, the decrease in T2 after running was greatest in the superficial zone, however, unlike the analysis that combined regions of the medial and lateral compartments, a statistically significant shortening of T2 was also observed in the middle zone for all locations. Results of the regional change in superficial cartilage T2 following exercise are presented in Figure 6. There was no statistically significant difference in T2 change of superficial cartilage after running based on location within the knee. Although results are not shown, there was also no difference in T2 change after running for the middle or deep cartilage layers based on location in the knee.

FIGURE 6
Change in superficial cartilage T2 based on location in the femoral/tibial joint (pooled values for all subjects): central medial femoral condyle (cMF), central lateral femoral condyle (cLF), posterior medial femoral condyle (pMF), posterior lateral femoral ...

DISCUSSION

The purpose of this study is to characterize the effect of age and training on cartilage thickness and T2 response immediately after running. Results from this study support the following conclusions. First, the results on cartilage thickness measurements after running support the conclusion that older subjects have stiffer cartilage independent of their level of physical activity. Second, these results confirm that with cyclical compressive loading, such as that which occurs during running, a decrease in T2 occurs preferentially near the articular surface. This is consistent with previous in vitro studies that demonstrate lower compressive stiffness of the superficial zone of cartilage (24). Third, the results do not demonstrate differences in cartilage T2 response between the medial and lateral compartments nor between central uncovered and posterior covered regions of cartilage. This suggests that in the normal joint, rather uniform tissue strains are generated within femoral tibial cartilage during running exercise

The role of MRI in evaluation of cartilage deformation for controlled biomechanical studies of osteochondral tissue samples and for several small exercise studies has been recently reviewed (1). Most in vivo exercise studies have focused on change in patellar cartilage thickness after performing deep knee bend exercise. In this study 30 minutes of running produced consistent tissue deformation, with 84% of subjects demonstrating a measurable decrease in mean thickness of femoral and tibial cartilage. Despite using relatively low-spatial resolution imaging, the measured change in thickness after running was statistically significant for younger subjects.

Of interest was the statistically significant smaller deformation of femoral and tibial cartilage observed in the older cohorts, suggesting stiffer cartilage in older individuals that is independent of training. Hudelmaier et al has also reported less deformation in elderly subjects age 50 to 75 years in a study of patellar cartilage deformation after performing deep knee bends (25). A potential cause of the increased cartilage stiffness is accumulation of advanced glycation end products and cross-linking of the collagen fibrils that occur with age which increase the stiffness of the collagen matrix and make the fibrils more prone to fatigue failure (26, 27). When comparing groups of similar age we did not observe a difference in cartilage deformation as a function of level of physical activity. This agrees with prior studies that have not found a difference in patellar cartilage compressibility after deep knee bends in young elite athletes compared to young inactive controls (5) suggesting functional adaptation of cartilage to compressive loading is limited.

Results of cartilage T2 mapping can help localize the tissue response to loading as a function of depth from the articular surface and regionally within the joint. The greatest change in cartilage T2 occurs near the articular surface with substantially less change in T2 in deeper layers of cartilage. This result supports the hypothesis that greater tissue consolidation occurs in the superficial layer of cartilage during exercise. Our findings confirm the initial observations of Mosher et al that T2 values of superficial femoral cartilage decrease after running. In contrast to this study, which did not observe a measurable change in T2 of tibial cartilage, we observed a statistically significant decrease in tibial cartilage T2 for all but the young sedentary cohorts. The T2 response to exercise as a function of depth from the articular surface was similar in all regions of the joint and not influenced by age or level of physical activity.

In validations studies on excised cartilage samples, anisotropy of the type II collagen matrix in cartilage is a primary mechanism responsible for regional variation in T2 (28) and appears to be altered with tissue deformation. In static compression studies, a pressure dependent decrease in cartilage T2 is observed throughout the entire thickness of cartilage and is correlated with change in collagen fiber anisotropy as measured using diffusion tensor imaging. (29). With compression the greatest change in orientation of collagen fibers is observed in the transitional zone. Using polarized light microscopy, increasing anisotropy of collagen fibers of the transitional zone during compression has also been correlated with a decrease in T2-weighted signal intensity (30). With cyclical loading of cartilage, as occurs with running, tissue deformation likely produces an increase in collagen fiber anisotropy within the more superficial layers of the transitional zone and a concomitant decrease in cartilage water which lead to lower T2 values on the post-exercise studies.

Study limitations

The lack of objective monitoring regarding the level of exercise, and effective joint loading performed by the subjects during the 30 minute protocol is a limitation of the study. It is likely that there are large discrepancies in the intensity and actual duration of running that occurred between subjects. It would seem most likely that lower levels of exercise were reached in the older sedentary cohort compared to the older marathoners. A lower level of compressive loading in the sedentary group could contribute to the failure to observe difference in cartilage T2 or thickness change after running between the older cohorts. Also the older sedentary individuals that participated in this study were self-selected and were of sufficient health and athletic training to participate in moderate intensity exercise. As such these results may not be representative of a comparison with a deconditioned older control group. In future studies it would be beneficial to perform objective measurements of loading forces applied by placing pressure sensing insoles in the shoes that can record the applied forces, or by performing the exercise in a controlled laboratory environment that would provide objective measures of joint biomechanics during the exercise protocol.

All of our measurements were completed within 15 minutes of running, with the center of k-space typically sampled between 8 to 9 minutes after running. In controlled conditions in which cartilage was compressed under unconfined static loading conditions for 210 minutes (resulting in ~ 50 % joint space narrowing), recovery of normal cartilage signal was not reached 252 minutes after release of pressure (9). Using the estimated biphasic exponential decompression function proposed by Rubenstien et al (9) approximately 8% recovery would occur 8.5 minutes after stopping the exercise and 12% recovery would occur 15 minutes after running. Because tissue consolidation occurring during cyclical loading occurs primarily near the articular surface, it is likely that recovery in our study is greater than that predicted from static loading conditions. As such our measurements regarding the change in cartilage thickness and T2 may be substantially less than that which occurs when running.

Despite the relatively large voxel dimensions, there was a statistically significant decrease in cartilage thickness after running for the younger cohorts. The larger voxel dimensions required to obtain cartilage T2 maps limits the spatial resolution needed to differentiate small differences in mean cartilage thickness. With 3D sequences optimized for determination of cartilage morphometry it may be possible to identify regional differences in cartilage deformation between cohorts that were not identified in this study. The limitations of large voxel dimensions will also increase volume averaging artifact that will be greatest for the superficial layer where tissue deformation is likely to increase signal contamination from synovial fluid on post exercise scans. In theory, because synovial fluid has a longer T2 than cartilage, volume averaging artifact should increase the T2 of the superficial zone and potentially attenuate the decrease in T2 values of superficial cartilage that are observed.

In summary, results of this study indicate cartilage T2 mapping is capable of providing unique information, regarding the response of femoral tibial cartilage to physiological loading. This provides objective information to guide understanding of the role of exercise as it relates to cartilage health and functional biomechanics. Future application of this technique may allow for quantitative assessment of cartilage response to exercise in the setting of altered biomechanics resulting from joint injury and in response to treatment.

Acknowledgments

Source of Funding: (TJM) Clinical Science Grant from the Arthritis Foundation and NIH/NIAMS RO1 AR47179, (TJM) Penn State College of Medicine MD Facilitation Award

This project is funded, in part, under a grant with the Pennsylvania Department of Health using Tobacco Settlement Funds. The Department specifically disclaims responsibility for any analyses, interpretations or conclusions.

Footnotes

Conflict of interest statement

None to declare.

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