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Radiology. Feb 2010; 254(2): 509–520.
Published online Jan 7, 2010. doi:  10.1148/radiol.09090596
PMCID: PMC2809928

Patellar Cartilage: T2 Values and Morphologic Abnormalities at 3.0-T MR Imaging in Relation to Physical Activity in Asymptomatic Subjects from the Osteoarthritis Initiative1

Abstract

Purpose:

To study the interrelationship between patella cartilage T2 relaxation time, other knee abnormalities, and physical activity levels in asymptomatic subjects from the Osteoarthritis Initiative (OAI) incidence cohort.

Materials and Methods:

The study had institutional review board approval and was HIPAA compliant. One hundred twenty subjects from the OAI without knee pain (age, 45–55 years) and with risk factors for knee osteoarthritis (OA) were studied by using knee radiographs, 3.0-T knee magnetic resonance (MR) images (including intermediate-weighted fast spin-echo and T2 mapping sequences), and the Physical Activity Scale for the Elderly. MR images of the right knee were assessed by two musculoskeletal radiologists for the presence and grade of abnormalities. Segmentation of the patella cartilage was performed, and T2 maps were generated. Statistical significance was determined by using analysis of variance, χ2 analysis, correlation coefficient tests, the Cohen κ, and a multiple linear regression model.

Results:

Cartilage lesions were found in 95 (79.0%) of 120 knees, and meniscal lesions were found in 54 (45%) of 120 knees. A significant correlation between patella cartilage T2 values and the severity and grade of cartilage (P = .0025) and meniscus (P = .0067) lesions was demonstrated. Subjects with high activity levels had significantly higher prevalence and grade of abnormalities and higher T2 values (48.7 msec ±4.35 vs 45.8 msec ±3.93; P < .001) than did subjects with low activity levels.

Conclusion:

Middle-aged asymptomatic individuals with risk factors for knee OA had a high prevalence of cartilage and meniscus knee lesions. Physically active individuals had more knee abnormalities and higher patellar T2 values. Additional studies will be needed to determine causality.

© RSNA, 2010

Introduction

Osteoarthritis (OA) is a multifactorial degenerative joint disease and a leading cause of disability worldwide, with radiographic evidence seen in at least 70% of the population over age 65 (1). Nearly 27 million individuals have clinically symptomatic OA, with the knee being the most commonly affected joint (2). OA is characterized by the progressive loss of hyaline articular cartilage; however, cartilage loss and OA symptoms are preceded by damage to the collagen-proteoglycan matrix and elevation of cartilage water content (3,4). Therefore, a sensitive method for detecting structural and functional changes in the early stages of OA would be valuable for assessing the progression of disease and for therapeutic monitoring. Magnetic resonance (MR) imaging has an increasing role in the diagnosis and monitoring of OA (5), with typical MR characteristics including cartilage defects, meniscal and ligamentous abnormalities, bone marrow edema–like lesions, and subchondral cysts (2,6).

In addition to enabling semiquantitative assessment of cartilage morphology and quantification of its thickness and volume, MR imaging has been shown (7,8) to have potential for the characterization of changes in the biochemical composition of cartilage during early OA. Techniques include T2 quantification (9), which may be able to be used as a biomarker to noninvasively assess cartilage quality and susceptibility to injury. Characterization of the cartilage matrix integrity with T2 relaxation time measurements could potentially help in prevention of OA progression by enabling identification of individuals at risk for OA who may benefit from treatment or behavioral interventions before irreversible morphologic changes occur (10,11). Researchers in a number of studies (1216) have examined OA risk factors in relation to quantitative and qualitative cartilage loss at MR imaging. However, there is a paucity of data analyzing cartilage changes on MR images, particularly T2 cartilage matrix measurements, in relation to physical activity as biomarkers for early OA changes.

To better understand the natural evolution of OA by using MR imaging, the National Institutes of Health (Bethesda, Md) launched the Osteoarthritis Initiative (OAI). It is a multicenter longitudinal observational study of 4796 persons with, or at risk for developing, knee OA that has created a public archive of data, biologic samples, and joint images. T2 relaxation times and measures of physical activity were also obtained as part of the OAI MR imaging protocol.

The aim of our study was to assess the cartilage T2 relaxation time in relation to knee abnormalities on 3.0-T MR images and the physical activity levels in asymptomatic subjects from the incidence cohort of the OAI.

Materials and Methods

This Health Insurance Portability and Accountability Act–compliant study was performed in accordance with the rules and regulations of the University of California Committee for Human Research. This article received the approval of the OAI Publications Committee on the basis of a review of its scientific content and data interpretation. The study protocol, amendments, and informed consent documentation were reviewed and approved by the local institutional review boards.

Subjects

The right knees of 120 subjects were included in our analysis, which is a subset of the 4796 participants in the OAI. Data were obtained from the OAI database, which is publicly accessible (http://www.oai.ucsf.edu/). The specific data sets used were baseline clinical data set 0.2.2 and baseline image data set 0.E.1. Subjects analyzed were from the incidence subcohort of the OAI, who were characterized by the absence of symptomatic knee OA and presence of risk factors for OA. These risk factors included knee symptoms (ie, pain, aching, or stiffness in or around the joints) during the past 12 months, obesity, a history of knee surgery or injury, a family history of total knee replacement, Heberden nodes, and repetitive knee-bending activities. Exclusion criteria were rheumatoid arthritis, bilateral severe knee joint space narrowing, and contraindications to or inability to undergo MR imaging. Specific inclusion criteria were (a) a baseline Western Ontario and McMaster University (WOMAC) Osteoarthritis Index pain score of zero for both knees, (b) age of 45–55 years, and (c) a body mass index (BMI) of 19–27 kg/m2. These criteria were used to exclude obesity as a risk factor and to focus on younger subjects. On the basis of these criteria, 120 patients (mean age, 50.8 years ± 2.84 [standard deviation]; range, 45–55 years), including 60 women (mean age, 50.88 years ± 2.72) and 60 men (mean age, 50.72 years ± 2.97), were identified and included.

Questionnaires and Clinical Examination

The WOMAC Osteoarthritis Index is a multidimensional health status instrument that is used to assess pain, stiffness, and physical function in patients with OA of the knee and hip (17,18). We included only subjects with a WOMAC pain score of zero for both knees for the 7 days preceding the baseline clinic visit. OAI participants with a WOMAC pain score higher than zero (3485 of 4796) were excluded.

Physical activity level was assessed by using the Physical Activity Scale for the Elderly (PASE), an established questionnaire for measuring physical activity in older individuals (19) that has also been validated in younger subjects (2022). Washburn et al (19) found the PASE to be a reliable and valid instrument for the assessment of physical activity in epidemiologic studies.

The Knee Injury and Osteoarthritis Outcome Score (KOOS) is an extension of the WOMAC Osteoarthritis Index for evaluating short- and long-term symptoms and function in subjects with knee injury and OA. The KOOS adds three subscales to the WOMAC Osteoarthritis Index: other knee symptoms, physical function in sport and recreation, and knee-related quality of life (23).

Subjects completed a 400-m walk and isometric muscle strength tests. The time (in seconds) to complete the 400-m walk was recorded for each subject (24). The maximum isometric strength of the right knee was obtained in newtons in maximum force flexion and extension by using the Good Strength Chair (Metitur, Jyvaskyla, Finland) (25).

Imaging

Bilateral standing posteroanterior fixed-flexion knee radiographs were obtained. Knees were positioned in a Plexiglas frame (SynaFlexer; CCBR-Synarc, San Francisco, Calif) with 20°–30° flexion and 10° internal rotation of the feet bilaterally. A focus-to-film distance of 72 inches (1 inch = 2.54 cm) was used. All radiographs were evaluated by two radiologists (T.M.L. and C.S., with 20 and 4 years experience in musculoskeletal imaging, respectively) in consensus, who graded the images by using the Kellgren-Lawrence technique (6,26).

MR images were obtained with a 3.0-T MR imager (Trio; Siemens, Erlangen, Germany). Both knees were examined with standard morphologic sequences, and T2-mapping sequences were used for the right knee only. A standard knee coil was used. For the right knee, the images obtained with the following sequences were analyzed: (a) coronal intermediate-weighted two-dimensional fast spin-echo (SE), (b) sagittal three-dimensional dual-echo steady-state with selective water excitation with coronal and axial reformations, (c) sagittal two-dimensional intermediate-weighted fast SE with fat suppression, (d) sagittal T2-weighted two-dimensional multiecho SE, and (e) coronal T1-weighted three-dimensional fast low-angle shot with water excitation (27). The sequence parameters are presented in Table 1.

Table 1
MR Imaging Parameters

Image Analysis

Semiquantitative morphologic analyses.—MR images of the right knee were reviewed on picture archiving and communication system workstations (Agfa, Ridgefield Park, NJ) by two musculoskeletal radiologists (T.M.L. and C.S.). If scores were not identical, consensus readings were performed. Ambient light was reduced during the reading session, and no time constraints were used. Radiologists had access to all sequences acquired, and the sequences listed in Table 1 were used for the analysis.

The Whole-Organ Magnetic Resonance Imaging Score (WORMS) was used to evaluate the images for OA-related abnormalities of the knee (2830). The original 15 WORMS regions at the knee were condensed to six regions for our study: patella, trochlea, medial femur, lateral femur, medial tibia, and lateral tibia. By using the semiquantitative scoring system, the following joint structures were separately evaluated: (a) cartilage, (b) ligaments, (c) menisci, (d) bone marrow edema pattern, (e) osteophytes, (f) synovitis or effusion, (g) subarticular cysts, (h) flattening or depression of the articular surfaces, (i) loose bodies, and (j) popliteal cysts.

Cartilage signal intensity and morphology were scored together by using an eight-point scale: 0 = normal thickness and signal intensity; 1 = normal thickness but increased signal intensity on T2-weighted images; 2.0 = partial-thickness focal defect less than 1 cm at its greatest width; 2.5 = full-thickness focal defect less than 1 cm at its greatest width; 3 = multiple areas of partial-thickness (grade 2.0) defects intermixed with areas of normal thickness or a grade 2.0 defect wider than 1 cm but occupying less than 75% of the region; 4 = diffuse (≥75% of the region) partial-thickness loss; 5 = multiple areas of full-thickness loss (grade 2.5) or a grade 2.5 lesion wider than 1 cm but occupying less than 75% of the region; and 6 = diffuse (≥75% of the region) full-thickness loss.

Alterations in meniscal morphology were assessed separately in six regions (medial and lateral aspects of the anterior, body, and posterior portions of the meniscus) by using a four-level scale: 0 = normal, 1 = intrasubstance abnormalities, 2 = nondisplaced tear, 3 = displaced or complex tear, and 4 = complete destruction or maceration. Meniscal extrusion was graded as follows: 0 = none and 1 = meniscal extrusion more than 3 mm beyond the tibial plateau. Subarticular bone marrow abnormalities were defined as poorly marginated areas of increased signal intensity in the normal subchondral and epiphyseal bone marrow on T2-weighted fast SE fat-suppressed MR images. This feature was graded on a four-point scale on the basis of the extent of regional involvement: 0 = none, 1 = 25% of the region or less, 2 = 25%–50%, and 3 = more than 50%. Ligaments were evaluated by using a four-point scale: 0 = no lesion, 1 = grade 1 sprain (signal intensity changes around ligament), 2 = grade 2 sprain (partial tear), and 3 = complete tear. Joint effusion was evaluated by using a four-point scale: 0 = normal, 1 = less than 33% of maximum potential distention, 2 = 33%–66%, and 3 = greater than 66%.

On the basis of MR findings, a knee was defined as abnormal if a WORMS value of 1 or higher was found in any of the subregions evaluated. A summary WORMS score for each abnormality was calculated by adding the scores for all subregions in a knee.

Cartilage lesions were also graded by using the MR imaging classification described by Recht et al (31) that is based on the arthroscopic Noyes and Stabler scoring system (32): I = areas of inhomogeneous signal intensity on intermediate-weighted fast SE fat-saturated sequences, II = defects involving less than half of the articular cartilage thickness, III = defects involving more than half of the cartilage but less than full thickness, and IV = full thickness defects exposing the bone. In addition, the largest diameter of the cartilage lesion in the sagittal, coronal, or axial plane and the two largest diameters of bone marrow edema in the sagittal plane were measured.

T2 measurements.—By using the sagittal two-dimensional multiecho SE images of the right knee, T2 maps were created and provided exponential curve fits and T2 for each pixel. Images were transferred to a remote workstation (SPARC; Sun Microsystems, Mountain View, Calif). The relaxation time, T2, was estimated by fitting an exponential function to the signal intensity at different echo times as follows: SI(TE) ~ exp(–TE/T2), where SI(TE) is signal intensity as a function of echo time, TE is echo time, and T2 is the transverse relaxation time. Investigators have suggested that articular cartilage has a multiexponential T2 decay, with a short (eg, microseconds) component and a longer component. Without the use of unvalidated specialized hardware, echo times on the order of microseconds cannot be obtained; thus, we did not attempt to measure the multiexponential relaxation times. We used a simplified monoexponential decay model that has been previously described (9). The seven echoes (10, 20, 30, 40, 50, 60, and 70 milliseconds) that are available from the OAI image database provided stable T2 data.

Images were transferred to the remote workstation and analyzed by using software developed at our institution with an interactive display language (Research Systems, Boulder, Colo) environment. An interactive display language routine was used for segmentation of the patella cartilage to simplify the manual drawing of splines delineating cartilage areas. Each patella had a range of 8–15 sections, and all sections with well-visualized artifact-free cartilage were segmented. Tissue contrast was excellent, and water-fat shift artifacts occurring at the bone-cartilage interface were well visualized on the first echo time images of the multiecho sequence, whereas fluid was shown well on the sagittal T2 maps. To exclude both fluid and water-fat shift artifacts from the regions of interest, adjustment of the splines was performed simultaneously by opening both image panels and using a synchronized cursor, section number, and zoom (Fig 11).). An interactive display language routine was used to calculate the mean T2 values from the regions of interest created in the T2 maps.

Figure 1a:
Sagittal (a, c) two-dimensional T2-weighted first-echo MR images and (b, d) corresponding T2 maps show manually drawn region of interest (white outline) of patella cartilage as ...
Figure 1b:
Sagittal (a, c) two-dimensional T2-weighted first-echo MR images and (b, d) corresponding T2 maps show manually drawn region of interest (white outline) of patella cartilage as ...
Figure 1c:
Sagittal (a, c) two-dimensional T2-weighted first-echo MR images and (b, d) corresponding T2 maps show manually drawn region of interest (white outline) of patella cartilage as ...
Figure 1d:
Sagittal (a, c) two-dimensional T2-weighted first-echo MR images and (b, d) corresponding T2 maps show manually drawn region of interest (white outline) of patella cartilage as ...

Reproducibility measurements.—Reproducibility for the semiquantitative analyses of cartilage with the WORMS for each compartment was calculated in a sample of 12 OAI image data sets that were each assessed twice by the two radiologists. Each subregion was graded by using the cartilage WORMS, and grades given by each radiologists were compared (30). Cohen κ statistics were calculated for inter- and intraobserver agreement.

The coefficient of variation was calculated for patella cartilage to determine reproducibility of the quantitative T2 measurements (33). To test intraobserver reliability, 12 data sets were randomly selected and segmented three times by the same investigator.

Statistical Analysis

Statistical processing was performed by using software (JMP, version 6; SAS Institute, Cary, NC). Descriptive statistics were obtained, and differences between measurements for men and those for women were determined by using one-way analysis of variance and the Pearson χ2 test. A multiple linear regression model was used to correct correlation data for the effects of age, sex, BMI, and other risk factors (eg, history of knee injury or surgery, family history of knee replacement, and Herbeden nodes in hands). A P value of less than .05 was considered to indicate a significant difference.

Results

Subject Characteristics

Table 2 shows baseline characteristics, including risk factors, for all subjects and for subject by sex. While there were no sex-related differences in age, Kellgren-Lawrence scores, PASE scores, or the time required for the 400-m walk, women had significantly lower mean BMI (P = .002), KOOS (P = .026), and muscle strength (P < .001). On the basis of physical activity level, subjects were divided into two groups: a low-activity group (PASE score: 0–199) and a high-activity group (PASE score: 200–400). The threshold PASE score of 200 separated subjects into two equal groups of 60. The range of the PASE is from zero to 400. The mean PASE scores for the low- and high-activity groups were 95.87 ± 34.63 (range, 27–149) and 295.15 ± 39.4 (range, 244–400), respectively. The median PASE score for all subjects was 196.5. There were no significant differences in BMI, age, KOOS, 400-m walk, or muscle strength between subjects in the low- and high-activity groups.

Table 2
Subject Characteristics

Radiographic Evaluation

Kellgren-Lawrence scores of 0, 1, 2, and 3 were found in 87, 29, two, and two right knees, respetively. Separate data for men and women are listed in Table 2.

Semiquantitative Morphologic Analyses

A high prevalence of meniscal (45.0%, 54 of 120) and overall cartilage (79.0%, 95 of 120) lesions (WORMS > 0) was found in all subjects (Table 3). Meniscal lesions were found more frequently in men, while cartilage lesions were more prevalent in women. Cartilage lesions at the patella were found in a high percentage (40.0%, 48 of 120) of subjects, with the finding more frequent in women (45%, 27 of 60) than in men (35%, 21 of 60). If cartilage lesions at the patella were found, subjects had a greater number of more severe cartilage lesions in all other regions (Table 4). Ligament lesions, bone marrow edema, joint effusion, and popliteal cysts were seen more frequently in men than in women. Ligament lesions were found most frequently at the patella tendon (all WORMS = 2; all subjects: 8.3% [10 of 120]; men: 11.7% [seven of 60]; women: 5.0% [three of 60]) and the anterior cruciate ligament (all subjects: 6.7% [eight of 120]; men: 8.3% [five of 60]; women: 5.0% [three of 60]).

Table 3
Prevalence of Focal Knee Abnormalities on MR Images
Table 4
Prevalence of Nonpatellar Cartilage Lesions in Subjects with and Those without Patellar Cartilage Lesions

The interobserver agreement was 95.3%, and the intraobserver agreements were 95.4% and 95.1%. Additionally, inter- and intraoberserver agreement were evaluated by using the Cohen κ. Values over 0.61 showed good reproducibility. The interobserver agreement κ value was 0.67, and intraobserver agreements κ values were 0.69 and 0.72.

When subjects were separated into low-activity (PASE score: 0–199) and high-acitivity (PASE score: 200–400) groups, a significantly higher prevalence of abnormalities was found in the high-activity group for the meniscus, cartilage, ligaments, bone marrow edema, and joint effusion. Cartilage lesions (WORMS > 0) were found in 56 (93.3%) of the 60 highly active subjects versus in 39 (65.0%) of the 60 less active subjects. In addition, lesions seen in the active subjects were more severe, as evidenced by the significantly higher maximum cartilage WORMS and Recht scores, than those in less active subjects (Table 5,,6).6). The same results were found by using PASE as a continuous scale.

Table 5
Prevalence of Knee Abnormalities by Activity Level
Table 6
Patient Characteristics by Activity Level

T2 Measurements

Owing to MR artifacts, one male subject in the low-activity group was excluded from T2 analysis. In comparison to T2 values of patella cartilage in subjects without abnormalities, those in subjects with cartilage abnormalities in the whole knee (44.6 msec ± 3.51 vs 47.94 msec ± 4.35; P = .0025) and at the patella (45.9 msec ± 3.62 vs 49.94 msec ± 4.75; P < .001) were significantly higher. Similar findings of higher T2 values were seen in subjects with meniscus abnormalities (46.2 msec ± 3.92 vs 48.5 msec ± 4.63; P = .0067) and those with joint effusion (46.3 msec ± 4.16 vs 49.71 msec ± 4.08; P ≤ .0018) versus patients without those abnormalities.

The T2 values of the patella cartilage were significantly higher in the high-activity group than in the low-activity group (48.7 msec ± 4.4 vs 45.8 msec ± 3.9; P < .001) (Table 6; Figs 22,,3).3). At multiple linear regression analysis, high correlation was observed between the patellar cartilage T2 values and the PASE score (P < .001), WORMS and Recht score of the patella cartilage (P < .001), WORMS and Recht cartilage summation score of the entire knee (P < .001), and joint effusion (P < .001).

Figure 2a:
Color-coded T2 maps overlaid on first-echo MR images obtained with multiecho SE sequence show (a)low patellar T2 values in a sedentary patient and (b) high patellar T2 values in an ...
Figure 2b:
Color-coded T2 maps overlaid on first-echo MR images obtained with multiecho SE sequence show (a)low patellar T2 values in a sedentary patient and (b) high patellar T2 values in an ...
Figure 3:
Mean patellar T2 values in subjects in low-activity (left, 1) and high-activity (right, 2) PASE groups (P < .001). Significance was determined by using a multivariate ...

In a multiregression model (adjusted for sex, age, BMI, and OA risk factors) for correlation of T2 values and cartilage lesions (WORMS) versus PASE scores, both parameters independently contributed (T2: P = .0035; cartilage WORMS: P = .0022) to the correlation with PASE scores.

On the basis of presence of cartilage lesions in the entire knee (any subregion with a WORMS >), we identified subgroups in the high- and low-activity groups. In the low-activity group, 27 of 59 subjects had cartilage lesions. These subjects had significantly higher T2 values than did subjects without cartilage lesions (47.0 msec ± 3.77 vs 44.7 msec ± 3.79; P = .0361). In the high-activity group, 38 of 60 subjects demonstrated cartilage lesions. These subjects also had higher T2 values than did those without lesions (49.72 msec ± 4.42 vs 47 msec ± 3.72; P = .0426). Among subjects without cartilage lesions, we also compared the high- and low-activity groups and found that the high-activity group had higher T2 values (47.0 msec ± 3.72 vs 44.7 msec ± 3.79; P = .0275). Comparing subjects with cartilage lesions between activity groups also showed significantly different T2 values (49.72 msec ± 4.42 vs 47.0 msec ± 3.77; P = .0199) (Table 7).

Table 7
Mean T2 Values by Activity Level and Presence of Cartilage Lesions

The coefficient of variation for T2 quantification measurements was 1.17.

Discussion

The results of our study show that middle-aged asymptomatic individuals with risk factors for knee OA from the OAI incidence cohort had a high prevalence of knee abnormalities, such as cartilage and meniscus lesions. A significant correlation between patellar cartilage T2 values and the presence and severity of cartilage and meniscus lesions was found. Physically active individuals showed significantly more cartilage and meniscus abnormalities than did more sedentary subjects; in addition, a significant correlation between physical activity level and patella T2 values was also observed.

T2 relaxation time mapping is sensitive to a wide range of water interactions in tissue and, in particular, depends on the content, orientation, and anisotropy of collagen (34). This parameter was therefore included in the OAI MR protocol, which will allow thorough investigation of T2 in relation to prevalence and evolution of cartilage degeneration and OA. We focused on patellar cartilage T2 measurements as segmentation of the patella can be done in a reasonable amount of time with good precision such that larger sample sizes can be analyzed. Also, it has been shown (35) that the femoropatellar joint may be particularly affected by weight-bearing physical activities. Patella cartilage differs from that of the tibiofemoral joint and exibits distinct biochemical and mechanical properties. Patella cartilage has been shown (36) to demonstrate more in vivo deformation than femoral and tibial cartilage with weight-bearing loaded activities. Varus-valgus knee alignment also appears to differ according to which knee compartment is affected by OA. Varus knee malalignment typically accompanies a loss of joint space in medial tibiofemoral joint OA. Patella malalignment within the femoral trochlea is commonly exhibited by patients with patellafemoral joint OA (37).

Multiple risk factors have been linked to OA in epidemiologic studies (3840), including age, female sex, obesity, sports activities, previous injury, proprioceptive deficits, and genetic elements. Knowledge of the relationship of physical activity and the evolution of OA is limited, as researchers (39,4143) investigating the effect of physical activity on weight-bearing joints have reported conflicting results. Investigators in a number of studies (1216) examined OA risk factors in relation to quantitative and qualitative cartilage loss determined with MR imaging. However, there is a paucity of data analyzing cartilage degeneration by using MR imaging in relation to physical activity. Therefore, the aim of out study was to assess the prevalence of cartilage, meniscal, and ligamentous damage; bone marrow edema; and cartilage T2 in relatively healthy young subjects from the incidence cohort of the OAI who had no pain and either high or low levels of physical activity. We focused on younger subjects because they could potentially best benefit from preventive intervention. Researchers in previous studies (4448) have shown similar results in smaller populations and younger subjects with higher physical activity levels. Stahl et al (29) examined 10 marathon runners and 12 physically active asymptomatic subjects. They also found a high prevalence of cartilage abnormalities in the marathon runners (60%) and active control subjects (50%). Vignon et al (49) stated in their review that the activities of daily life, as well as sports and recreational activities, are risk factors for knee OA and that risk increases with intensity and duration of activity.

A number of studies have examined the influence of age on the risk of developing knee OA in physically active individuals. Most of these investigators examined individuals in a specific stage of the lifespan. A lower prevalence of OA has been reported (50) in middle-aged (range, 48–60 years) physically active teachers as compared with control subjects. In contrast to these results, McAlindon et al (51) examined the level of physical activity and the risk of radiographic and symptomatic knee OA in an elderly population of the Framingham Study. They found that heavy physical activity is an important risk factor for the development of knee OA in elderly patients. These investigators, however, based their diagnosis on radiographs, which unfortunately show advanced disease stages, limiting possible preventive measures. Findings in several studies (52,53) have shown the age dependency of cartilage T2 maps. Mosher et al indicated in studies of asymptomatic male and female volunteers that aging is associated with an increase in T2 of articular cartilage. We only examined middle-aged individuals and did not find a correlation between age and T2 values or age and cartilage lesions in our small age range.

A small number of studies have used MR imaging to assess the relationship between physical activity and knee joint structure. Stahl et al (35) examined the relationship in a smaller cohort than we did. Physically active subjects (mean age, 33 years) had a high prevalence of focal cartilage abnormalities. In some studies (5456), the most frequent findings in physically active subjects were abnormalities in meniscal signal intensity or tears (13%–50%), bone marrow edema (up to 41%), or joint effusion (up to 35%). Two studies performed at 1.5 T also found cartilage lesions: Kaplan et al (56) examined both knees of 20 basketball players. In 47.5% of the knees, articular cartilage lesions were detected. Most of them were seen at the patella (35%) or trochlea (25%). Major and Helms (55) performed a study with 17 varsity basketball players; eight (24%) of the 34 knees had abnormal signal intensity in the patellar and trochlear cartilage, and six (18%) had focal cartilage lesions. These studies clearly show that high-level physical activity in young and middle-aged individuals is associated with cartilage lesions. In our study, lesions were found with a higher prevalence, which is most likely related to differences in age between studies.

We also found a significant correlation between patella cartilage T2 values and the severity of cartilage and meniscus lesions based on the WORMS and Recht scores. Stahl et al (34) showed, in a small sample, that T2 relaxation times were significantly higher in the tibiofemoral cartilage of patients with early knee OA compared with healthy controls, allowing differentiation of patients with disease from those without. In another study with asymptomatic physically active and sedentary subjects, Stahl et al (35) found that T1ρ and T2 relaxation times were not different between younger active subjects and sedentary controls; however, a significant difference in these parameters in active subjects with and those without cartilage defects was found. In contrast to their results, we found a significant correlation between physical activity level and T2 values. Interestingly, we also found an association between T2 and prevalent cartilage lesions, and this association was present in both activity groups. When cartilage lesions are present, T2 is elevated. On the basis of these findings, we hypothesize that T2 is a measure of cartilage quality and that subjects who develop cartilage lesions during physical activity have a higher T2. Since we included only subjects without pain in our analysis, we conclude that these findings may indicate that higher T2 values are associated with higher risk for development of morphologic cartilage lesions. It is also possible that, during the process of focal cartilage lesion development, substances are released into the synovial fluid that serve as mediators and initiate cartilage breakdown in areas that are not visually affected by OA. Further longitudinal studies are necessary to determine the role of T2 measurements in the evolution of OA.

A limitation of our study was that we only obtained T2 values of the patella. However, cartilage segmentation is a time-consuming process, which may take up to 4 hours for one knee. Our goal was establish a more feasible and faster technique that would also potentially allow clinical application of T2 quantification in the future. Future studies, however, will have to show whether patella T2 may be used as a surrogate measure for whole knee cartilage T2. Another limitation is that we only used T2 mapping for assessing biochemical composition of cartilage. Unfortunately, the OAI protocol only includes a T2 mapping sequence. Promising new techniques like T1ρ and delayed gadolinium-enhanced MR imaging of cartilage, or dGEMRIC, (10) are not available. The advantage of T1ρ and T2 measurements is that these techniques are noninvasive and do not require special preparation (eg, administration of contrast agent in dGEMRIC). Stahl et al (35) pointed out that T1ρ is well suited to differentiate healthy subjects and early OA patients and is more sensitive than T2 relaxation times.

Another limitation of our study was that, although images were scored separately, a consensus reading was performed if scores were not identical. A separate reading for both observers and a comparison of the results might be better. We also performed a reproducibility measurement for 12 subjects and calculated the inter- and intraobserver agreements only for the WORMS cartilage score. Further, the WORMS does not include the patella tendon. To include the patella in our scoring system, we defined patella tendinosis as a grade 2 sprain and added the score to the WORMS summation for ligaments. The PASE is intended for the elderly, but it has been validated for subjects with mean ages of 52 (standard deviation, 16) (20), 54 (range, 30–68 years) (21), and 56 (range, 37–73 years) (22) years.

In conclusion, our findings show that middle-aged asymptomatic individuals with knee OA risk factors have a high prevalence of knee abnormalities on MR images, particularly cartilage and meniscus lesions. Physically active individuals showed significantly more cartilage and meniscus abnormalities and higher patellar T2 values. Our results indicate that T2 relaxation time at the patella may be a marker for internal joint derangement in terms of cartilage and meniscal lesions.

Advances in Knowledge

  • Middle-aged asymptomatic individuals with risk factors for knee osteoarthritis had a high prevalence of cartilage and meniscus lesions.
  • A significant correlation between patellar cartilage T2 values and the presence and severity of cartilage and meniscus lesions was found.
  • Physically active individuals showed significantly more cartilage and meniscus abnormalities; in addition, a significant correlation between physical activity level and T2 values was also demonstrated.

Implications for Patient Care

  • T2 relaxation time measurements at the patella may be a marker for internal joint derangement in terms of cartilage and meniscal lesions.
  • Subjects with higher physical activity levels and high T2 have more cartilage and meniscal degeneration.

Received April 5, 2009; revision requested May 30; final revision received July 17; accepted July 29; final version accepted August 18.

Funding: This research was supported by the National Institutes of Health (grants N01-AR-2-2258, N01-AR-2-2259, N01-AR-2-2260, N01-AR-2-2261, and N01-AR-2-2262).

Supported in part by Merck Research Laboratories, Novartis Pharmaceuticals, GlaxoSmithKline, and Pfizer. Private-sector Osteoarthritis Initiative funding managed by Foundation for the National Institutes of Health. C.S. supported by Deutsche Forschungsgemeinschaft (grant STE 1829/1–1).

Authors stated no financial relationship to disclose.

Abbrevations:

KOOS
Knee Injury and Osteoarthritis Outcome Score
OA
osteoarthritis
OAI
Osteoarthritis Initiative
PASE
Physical Activity Scale for the Elderly
SE
spin-echo
WOMAC
Western Ontario and McMaster University
WORMS
Whole-Organ Magnetic Resonance Imaging Score

References

1. Lane NE, Thompson JM. Management of osteoarthritis in the primary-care setting: an evidence-based approach to treatment. Am J Med 1997;103:25S–30S [PubMed]
2. Lawrence RC, Felson DT, Helmick CG, et al. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. II. Arthritis Rheum 2008;58:26–35 [PMC free article] [PubMed]
3. Mankin HJ, Brandt KD. Pathogenesis of arthritis In: Kelley WN, Harris ED Jr, Ruddy S, Clement B, editors. Textbook of rheumatology 4th ed Philadelphia, Pa: Saunders, 1993
4. Liess C, Lusse S, Karger N, Heller M, Gluer CC. Detection of changes in cartilage water content using MRI T2-mapping in vivo. Osteoarthritis Cartilage 2002;10:907–913 [PubMed]
5. Burstein D, Gray M. New MRI techniques for imaging cartilage. J Bone Joint Surg Am 2003;85-A(suppl 2):70–77 [PubMed]
6. Link TM, Steinbach LS, Ghosh S, et al. Osteoarthritis: MR imaging findings in different stages of disease and correlation with clinical findings. Radiology 2003;226:373–381 [PubMed]
7. Eckstein F, Heudorfer L, Faber SC, Burgkart R, Englmeier KH, Reiser M. Long-term and resegmentation precision of quantitative cartilage MR imaging (qMRI). Osteoarthritis Cartilage 2002;10:922–928 [PubMed]
8. Eckstein F, Tieschky M, Faber SC, et al. Effect of physical exercise on cartilage volume and thickness in vivo: MR imaging study. Radiology 1998;207:243–248 [PubMed]
9. Dunn TC, Lu Y, Jin H, Ries MD, Majumdar S. T2 relaxation time of cartilage at MR imaging: comparison with severity of knee osteoarthritis. Radiology 2004;232:592–598 [PubMed]
10. Link TM, Stahl R, Woertler K. Cartilage imaging: motivation, techniques, current and future significance. Eur Radiol 2007;17:1135–1146 [PubMed]
11. Mosher TJ, Dardzinski BJ. Cartilage MRI T2 relaxation time mapping: overview and applications. Semin Musculoskelet Radiol 2004;8:355–368 [PubMed]
12. Sharma L, Eckstein F, Song J, et al. Relationship of meniscal damage, meniscal extrusion, malalignment, and joint laxity to subsequent cartilage loss in osteoarthritic knees. Arthritis Rheum 2008;58:1716–1726 [PubMed]
13. Ding C, Martel-Pelletier J, Pelletier JP, et al. Meniscal tear as an osteoarthritis risk factor in a largely non-osteoarthritic cohort: a cross-sectional study. J Rheumatol 2007;34:776–784 [PubMed]
14. Felson DT. Relation of obesity and of vocational and avocational risk factors to osteoarthritis. J Rheumatol 2005;32:1133–1135 [PubMed]
15. Eckstein F, Burstein D, Link TM. Quantitative MRI of cartilage and bone: degenerative changes in osteoarthritis. NMR Biomed 2006;19:822–854 [PubMed]
16. Felson DT, Zhang Y, Hannan MT, et al. The incidence and natural history of knee osteoarthritis in the elderly: the Framingham Osteoarthritis Study. Arthritis Rheum 1995;38:1500–1505 [PubMed]
17. Bellamy N, Buchanan WW, Goldsmith CH, Campbell J, Stitt LW. Validation study of WOMAC: a health status instrument for measuring clinically important patient relevant outcomes to antirheumatic drug therapy in patients with osteoarthritis of the hip or knee. J Rheumatol 1988;15:1833–1840 [PubMed]
18. Bellamy N. The WOMAC Knee and Hip Osteoarthritis Indices: development, validation, globalization and influence on the development of the AUSCAN Hand Osteoarthritis Indices. Clin Exp Rheumatol 2005;23:S148–S153 [PubMed]
19. Washburn RA, Smith KW, Jette AM, Janney CA. The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 1993;46:153–162 [PubMed]
20. Johansen KL, Painter P, Kent-Braun JA, et al. Validation of questionnaires to estimate physical activity and functioning in end-stage renal disease. Kidney Int 2001;59:1121–1127 [PubMed]
21. Stibrant Sunnerhagen K. Circuit training in community-living “younger” men after stroke. J Stroke Cerebrovasc Dis 2007;16:122–129 [PubMed]
22. Willen C, Grimby G. Pain, physical activity, and disability in individuals with late effects of polio. Arch Phys Med Rehabil 1998;79:915–919 [PubMed]
23. Roos EM, Lohmander LS. The Knee injury and Osteoarthritis Outcome Score (KOOS): from joint injury to osteoarthritis. Health Qual Life Outcomes 2003;1:64. [PMC free article] [PubMed]
24. Simonsick EM, Montgomery PS, Newman AB, Bauer DC, Harris T. Measuring fitness in healthy older adults: the Health ABC Long Distance Corridor Walk. J Am Geriatr Soc 2001;49:1544–1548 [PubMed]
25. Rantanen T, Era P, Heikkinen E. Physical activity and the changes in maximal isometric strength in men and women from the age of 75 to 80 years. J Am Geriatr Soc 1997;45:1439–1445 [PubMed]
26. Kellgren JH, Lawrence JS. Radiological assessment of osteoarthritis. Ann Rheum Dis 1957;16:494–501 [PMC free article] [PubMed]
27. Peterfy CG, Schneider E, Nevitt M. The osteoarthritis initiative: report on the design rationale for the magnetic resonance imaging protocol for the knee. Osteoarthritis Cartilage 2008;16:1433–1441 [PMC free article] [PubMed]
28. Peterfy CG, Gold G, Eckstein F, Cicuttini F, Dardzinski B, Stevens R. MRI protocols for whole-organ assessment of the knee in osteoarthritis. Osteoarthritis Cartilage 2006;14(suppl A):A95–A111 [PubMed]
29. Stahl R, Luke A, Ma CB, et al. Prevalence of pathologic findings in asymptomatic knees of marathon runners before and after a competition in comparison with physically active subjects: a 3.0 T magnetic resonance imaging study. Skeletal Radiol 2008;37:627–638 [PubMed]
30. Peterfy CG, Guermazi A, Zaim S, et al. Whole-Organ Magnetic Resonance Imaging Score (WORMS) of the knee in osteoarthritis. Osteoarthritis Cartilage 2004;12:177–190 [PubMed]
31. Recht MP, Piraino DW, Paletta GA, Schils JP, Belhobek GH. Accuracy of fat-suppressed three-dimensional spoiled gradient-echo FLASH MR imaging in the detection of patellofemoral articular cartilage abnormalities. Radiology 1996;198:209–212 [PubMed]
32. Noyes FR, Stabler CL. A system for grading articular cartilage lesions at arthroscopy. Am J Sports Med 1989;17:505–513 [PubMed]
33. Gluer CC, Blake G, Lu Y, Blunt BA, Jergas M, Genant HK. Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques. Osteoporos Int 1995;5:262–270 [PubMed]
34. Stahl R, Blumenkrantz G, Carballido-Gamio J, et al. MRI-derived T2 relaxation times and cartilage morphometry of the tibio-femoral joint in subjects with and without osteoarthritis during a 1-year follow-up. Osteoarthritis Cartilage 2007;15:1225–1234 [PubMed]
35. Stahl R, Luke A, Li X, et al. T1rho, T(2) and focal knee cartilage abnormalities in physically active and sedentary healthy subjects versus early OA patients: a 3.0-Tesla MRI study. Eur Radiol 2009;19(1):132–143 [PubMed]
36. Eckstein F, Lemberger B, Gratzke C, et al. In vivo cartilage deformation after different types of activity and its dependence on physical training status. Ann Rheum Dis 2005;64:291–295 [PMC free article] [PubMed]
37. Hinman RS, Crossley KM. Patellofemoral joint osteoarthritis: an important subgroup of knee osteoarthritis. Rheumatology (Oxford) 2007;46:1057–1062 [PubMed]
38. Felson DT. An update on the pathogenesis and epidemiology of osteoarthritis. Radiol Clin North Am 2004;42:1–9 [PubMed]
39. Urquhart DM, Soufan C, Teichtahl AJ, Wluka AE, Hanna F, Cicuttini FM. Factors that may mediate the relationship between physical activity and the risk for developing knee osteoarthritis. Arthritis Res Ther 2008;10:203. [PMC free article] [PubMed]
40. Dekker J, van Dijk GM, Veenhof C. Risk factors for functional decline in osteoarthritis of the hip or knee Curr Opin Rheumatol, 2009;21(5):520–524 [PubMed]
41. Szoeke C, Dennerstein L, Guthrie J, Clark M, Cicuttini F. The relationship between prospectively assessed body weight and physical activity and prevalence of radiological knee osteoarthritis in postmenopausal women. J Rheumatol 2006;33:1835–1840 [PubMed]
42. Chakravarty EF, Hubert HB, Lingala VB, Zatarain E, Fries JF. Long distance running and knee osteoarthritis: a prospective study. Am J Prev Med 2008;35:133–138 [PMC free article] [PubMed]
43. Racunica TL, Teichtahl AJ, Wang Y, et al. Effect of physical activity on articular knee joint structures in community-based adults. Arthritis Rheum 2007;57:1261–1268 [PubMed]
44. Beattie KA, Boulos P, Pui M, et al. Abnormalities identified in the knees of asymptomatic volunteers using peripheral magnetic resonance imaging. Osteoarthritis Cartilage 2005;13:181–186 [PubMed]
45. Boks SS, Vroegindeweij D, Koes BW, Hunink MM, Bierma-Zeinstra SM. Magnetic resonance imaging abnormalities in symptomatic and contralateral knees: prevalence and associations with traumatic history in general practice. Am J Sports Med 2006;34:1984–1991 [PubMed]
46. Zanetti M, Pfirrmann CW, Schmid MR, Romero J, Seifert B, Hodler J. Patients with suspected meniscal tears: prevalence of abnormalities seen on MRI of 100 symptomatic and 100 contralateral asymptomatic knees. AJR Am J Roentgenol 2003;181:635–641 [PubMed]
47. Hill CL, Gale DR, Chaisson CE, et al. Periarticular lesions detected on magnetic resonance imaging: prevalence in knees with and without symptoms. Arthritis Rheum 2003;48:2836–2844 [PubMed]
48. Tschirch FT, Schmid MR, Pfirrmann CW, Romero J, Hodler J, Zanetti M. Prevalence and size of meniscal cysts, ganglionic cysts, synovial cysts of the popliteal space, fluid-filled bursae, and other fluid collections in asymptomatic knees on MR imaging. AJR Am J Roentgenol 2003;180:1431–1436 [PubMed]
49. Vignon E, Valat JP, Rossignol M, et al. Osteoarthritis of the knee and hip and activity: a systematic international review and synthesis (OASIS). Joint Bone Spine 2006;73:442–455 [PubMed]
50. White JA, Wright V, Hudson AM. Relationships between habitual physical activity and osteoarthrosis in ageing women. Public Health 1993;107:459–470 [PubMed]
51. McAlindon TE, Wilson PW, Aliabadi P, Weissman B, Felson DT. Level of physical activity and the risk of radiographic and symptomatic knee osteoarthritis in the elderly: the Framingham study. Am J Med 1999;106:151–157 [PubMed]
52. Mosher TJ, Dardzinski BJ, Smith MB. Human articular cartilage: influence of aging and early symptomatic degeneration on the spatial variation of T2–preliminary findings at 3 T. Radiology 2000;214:259–266 [PubMed]
53. Mosher TJ, Liu Y, Yang QX, et al. Age dependency of cartilage magnetic resonance imaging T2 relaxation times in asymptomatic women. Arthritis Rheum 2004;50:2820–2828 [PubMed]
54. Ludman CN, Hough DO, Cooper TG, Gottschalk A. Silent meniscal abnormalities in athletes: magnetic resonance imaging of asymptomatic competitive gymnasts. Br J Sports Med 1999;33:414–416 [PMC free article] [PubMed]
55. Major NM, Helms CA. MR imaging of the knee: findings in asymptomatic collegiate basketball players. AJR Am J Roentgenol 2002;179:641–644 [PubMed]
56. Kaplan LD, Schurhoff MR, Selesnick H, Thorpe M, Uribe JW. Magnetic resonance imaging of the knee in asymptomatic professional basketball players. Arthroscopy 2005;21:557–561 [PubMed]

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