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Subchondral Bone Marrow Edema in Patients with Degeneration of the Articular Cartilage of the Knee Joint¹

¹ From the Departments of Radiology (R.K., P.S., J.F., A.D.S.) and Statistics (J.F.), University of Wisconsin Hospital, Clinical Science Center-E3/311, 600 Highland Ave, Madison, WI 53792-3252. Received January 25, 2005; revision requested March 31; revision received April 6; accepted May 6; final version accepted May 24. Address correspondence to R.K. (e-mail: rkijowski{at}mail.radiology.wisc.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 
Purpose: To retrospectively determine at magnetic resonance (MR) imaging the prevalence of subchondral bone marrow edema beneath arthroscopically proved articular cartilage defects.

Materials and Methods: The study was performed in compliance with HIPAA regulations, and a waiver of informed consent was obtained from the institutional review board before the study was performed. The study consisted of 132 patients (70 men, 62 women; average age, 53 years) with articular cartilage defects of the knee joint who underwent MR imaging of the knee and subsequent arthroscopic knee surgery. At the time of arthroscopy, each articular cartilage lesion was graded by using the Noyes classification system. MR examinations were retrospectively reviewed to determine the size, depth, and location of subchondral bone marrow edema without knowledge of the arthroscopic findings. Pairwise Fisher exact tests and two-sample t tests were used to correlate MR imaging findings of subchondral bone marrow edema with the arthroscopic grade of articular cartilage degeneration.

Results: Subchondral bone marrow edema was seen beneath 105 (19%) of 554 articular cartilage defects identified at arthroscopy. It was not observed beneath any of the six grade 1 cartilage defects but was observed beneath eight (4.9%) of 163 grade 2A defects, 40 (14.4%) of 278 grade 2B defects, 54 (55.1%) of 98 grade 3A defects, and three (33.3%) of nine grade 3B defects. Subchondral bone marrow edema was also seen beneath four (1.4%) of 238 articular surfaces that appeared normal at arthroscopy. The mean depth and cross-sectional area of subchondral bone marrow edema increased with increasing grade of the articular cartilage lesion.

Conclusion: Higher grades of articular cartilage defects are associated with higher prevalence and greater depth and cross-sectional area of subchondral bone marrow edema.

© RSNA, 2006

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 
Osteoarthritis of the knee joint is extremely common. Nearly 75% of individuals aged 65 years or older in the United States have evidence of degenerative joint disease on knee radiographs. Furthermore, approximately 1.6% of the American population has symptomatic osteoarthritis of the knee joint (1,2).

Pain is the major source of disability in patients with osteoarthritis of the knee joint (3). The exact cause of pain in patients with degenerative joint disease is presently unknown. Degeneration of articular cartilage is the pathologic hallmark of osteoarthritis; however, articular cartilage has no nociceptive pain fibers and thus cannot be the source of pain in patients with degenerative joint disease (4,5).

Subchondral bone marrow is richly innervated with nociceptive pain fibers and may be a source of pain in patients with symptomatic degenerative joint disease (4,5). Abnormalities of subchondral bone marrow are common manifestations of various painful disorders of the knee, including posttraumatic contusions, transient osteoporosis, infectious and inflammatory arthropathies, insufficiency fractures, and spontaneous osteonecrosis. These painful osseous disorders are characterized by the presence of subchondral bone marrow edema on magnetic resonance (MR) images (6–9). Subchondral bone marrow edema is also commonly seen in patients with degenerative joint disease (10–14). Subchondral bone marrow edema in patients with osteoarthritis of the knee joint has been associated with knee pain and the progression of articular cartilage degeneration (12,13).

The association between subchondral bone marrow edema and degeneration of the articular cartilage of the knee joint has been well documented (10–14); however, the prevalence of subchondral bone marrow edema beneath areas of articular cartilage degeneration has not been previously reported. Thus, the purpose of our study was to retrospectively determine at MR imaging the prevalence of subchondral bone marrow edema beneath arthroscopically proved articular cartilage defects of the knee joint.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 
Study Group
The study was performed in compliance with Health Insurance Portability and Accountability Act regulations. Our institutional review board approved the study and granted a waiver of informed consent before the study was performed.

The study group consisted of 132 patients with articular cartilage defects of the knee joint who underwent an MR examination of the knee prior to arthroscopic knee surgery. An MR database was retrospectively reviewed by one author (P.S.), who identified 1235 patients with articular cartilage defects of the knee joint on MR images obtained at our institution between January 1999 and June 2004. The medical records of these 1235 patients were reviewed by the same author, and 152 patients were identified who were seen by any one of three orthopedic sports medicine specialists at our institution and who underwent subsequent arthroscopic surgery on their symptomatic knee. The medical records and MR images of these 152 patients were retrospectively reviewed by two authors (R.K. and P.S.). Patients with clinical manifestations or MR imaging findings of metabolic bone disease, septic arthritis, inflammatory arthritis, connective tissue disease, insufficiency fracture, spontaneous osteonecrosis, or neoplastic disease were excluded from the study. In addition, patients with a history of trauma within 12 months of the MR examination or history of knee surgery were excluded from the study. Twenty of the 152 patients were excluded from the study on the basis of these criteria. The study group consisted of the remaining 132 patients (70 men and 62 women) with arthroscopically proved articular cartilage defects of the knee joint. The patients were aged between 31 and 77 years, with an average age of 53 years.

All 132 patients were evaluated by any one of three orthopedic surgeons at our institution who specialized in sports medicine and who had between 5 and 20 years of clinical experience treating patients with musculoskeletal disorders. The clinical notes of all patients were thoroughly reviewed by two authors (R.K. and P.S.) to determine the location of each patient's knee pain if it was specified. The location of knee pain was not specified in the clinical notes nor was described as being diffusely distributed throughout the knee in 22 of the 132 patients.

MR Imaging
All 132 patients had undergone MR imaging of the symptomatic knee within 2 months after their clinic visit. All MR examinations were performed with the same 1.5-T field strength magnet (GE Medical Systems, Milwaukee, Wis) by using a phased-array extremity coil. All MR examinations of the knee consisted of coronal T1-weighted spin-echo (repetition time msec/echo time msec, 400–800/15–30), coronal fat-suppressed intermediate-weighted fast spin-echo (2000–4000/30–50, echo train length of four), sagittal intermediate-weighted fast spin-echo (2000–4000/30–50, echo train length of four), sagittal fat-suppressed T2-weighted fast spin-echo (2000–4000/60–80, echo train length of eight), and transverse fat-suppressed T2-weighted fast spin-echo (2000–4000/60–80, echo train length of eight) sequences. All fat-suppressed intermediate-weighted and T2-weighted fast spin-echo sequences were performed by using a frequency-selective chemical presaturation pulse (ChemSat; GE Medical Systems) to suppress signal from adipose tissue. All MR examinations were performed with a field of view of 14–16 cm, a section thickness of 3–4 mm with an intersection gap of 1.0–1.5 mm, a 256 x 256 matrix, and two signals.

Arthroscopic Surgery
All 132 patients had undergone arthroscopic knee surgery of their symptomatic knee within 2 months after their MR examination. All arthroscopic knee surgeries were performed by one of the three experienced orthopedic sports medicine specialists described earlier. The indications for surgery were débridement or repair of a meniscal tear in 57 patients, débridement or repair of a meniscal tear and débridement of an articular cartilage defect in 45 patients, débridement of an articular cartilage defect in 24 patients, and removal of intraarticular loose bodies in six patients. The articular cartilage of the patella, femoral trochlea, medial femoral condyle, lateral femoral condyle, medial tibial plateau, and lateral tibial plateau of each patient was graded at the time of arthroscopic knee surgery by using the Noyes classification system (15), which resulted in a review of 792 cartilaginous surfaces (Table 1). The orthopedic surgeons were aware of the MR imaging findings in all patients at the time of arthroscopic knee surgery; however, the surgeons thoroughly evaluated each articular surface of the knee joint in all patients regardless of whether a cartilage defect was identified at the MR examination. The presence and location of meniscal tears were also documented at the time of arthroscopic knee surgery.

If subchondral bone marrow edema was identified on an MR image, the depth and cross-sectional diameter of the bone marrow edema were measured with a caliber by using the numeric scale present at the periphery of each MR image. The maximum depth of the subchondral bone marrow edema was measured perpendicular to the articular surface on fat-suppressed T2-weighted fast spin-echo images. The cross-sectional diameter of the subchondral bone marrow edema was measured on fat-suppressed T2-weighted fast spin-echo images and fat-suppressed intermediate-weighted fast spin-echo images at its largest dimension parallel to the articular surface. The cross-sectional area of the subchondral bone marrow edema was then calculated by multiplying the cross-sectional dimensions of the bone marrow edema measured in two planes. For subchondral bone marrow edema within the femoral condyles and tibial plateau, cross-sectional dimensions measured in the coronal and sagittal planes were used to calculate the cross-sectional area. For subchondral bone marrow edema within the patella and femoral trochlea, cross-sectional dimensions measured in transverse and sagittal planes were used to calculate the cross-sectional area.

Statistical Analysis
All statistical analyses were performed by using statistical software (S-Plus, version 3.4; MathSoft, Seattle, Wash). The association between the mean depth and mean cross-sectional area of the subchondral bone marrow edema and the grade of the overlying articular cartilage defect was determined by using two-sample t tests. All other statistical analyses were performed by using pairwise Fisher exact tests. When determining whether the location of subchondral bone marrow edema could help predict the location of a patient's knee pain, it was assumed that bone marrow edema within the patellofemoral compartment would cause anterior knee pain, that within the medial compartment would cause medial knee pain, and that within the lateral compartment would cause lateral knee pain. When determining whether the location of a meniscal tear could help predict the location of a patient's knee pain, it was assumed that a medial meniscal tear would cause medial knee pain and a lateral meniscal tear would cause lateral knee pain. Statistical significance was defined as P < .05 for the two-sample t tests or pairwise Fisher exact tests. The data were also reviewed to determine whether clustering (ie, multiple lesions in patients) influenced the prevalence of subchondral bone marrow edema beneath areas of articular cartilage degeneration.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 
All 132 patients in the study group had arthroscopically proved articular cartilage defects of the knee joint. Subchondral bone marrow edema was observed in 79 (60%) of the 132 patients. There were 554 cartilage defects (69.9%) within 792 articular surfaces of knee joints evaluated at the time of arthroscopic knee surgery. Subchondral bone marrow edema was observed beneath 105 (19%) of the 554 articular cartilage defects.

Subchondral Bone Marrow Edema and Grades of Articular Cartilage Defects
The prevalence of subchondral bone marrow edema beneath different grades of articular cartilage defects of the knee joint is summarized in Table 2. Subchondral bone marrow edema was observed beneath 48 (10.1%) of 441 partial-thickness cartilage defects and beneath 57 (53.2%) of 107 full-thickness cartilage defects (Fig 1). Subchondral bone marrow edema was also observed beneath four (1.4%) of the 238 articular surfaces that appeared normal at arthroscopic knee surgery (Fig 2).

View larger version (121K): [in this window] [in a new window] [Download PPT slide]   Figure 1a: MR images in a 51-year-old man with grade 2B articular cartilage defects of the medial femoral condyle and medial tibial plateau at arthroscopy. (a) Coronal fat-suppressed intermediate-weighted fast spin-echo image of the knee shows subchondral bone marrow edema within the medial femoral condyle (arrow) and medial tibial plateau (arrowhead). (b) Sagittal fat-suppressed T2-weighted fast spin-echo image of the knee shows subchondral bone marrow edema within the medial femoral condyle (arrow) and medial tibial plateau (arrowhead).

View larger version (152K): [in this window] [in a new window] [Download PPT slide]   Figure 1b: MR images in a 51-year-old man with grade 2B articular cartilage defects of the medial femoral condyle and medial tibial plateau at arthroscopy. (a) Coronal fat-suppressed intermediate-weighted fast spin-echo image of the knee shows subchondral bone marrow edema within the medial femoral condyle (arrow) and medial tibial plateau (arrowhead). (b) Sagittal fat-suppressed T2-weighted fast spin-echo image of the knee shows subchondral bone marrow edema within the medial femoral condyle (arrow) and medial tibial plateau (arrowhead).

View larger version (145K): [in this window] [in a new window] [Download PPT slide]   Figure 2: MR image in a 37-year-old man with normal articular cartilage of the medial tibial plateau at arthroscopy. Sagittal fat-suppressed T2-weighted fast spin-echo image of the knee shows a small area of subchondral bone marrow edema (arrow) within the medial tibial plateau.

The degree of subchondral bone marrow edema beneath areas of articular cartilage degeneration was also strongly influenced by the grade of the cartilage defect (Figs 3, 4). There was a statistically significant increase (P < .05) in the mean depth and mean cross-sectional area of the subchondral bone marrow edema with increasing grade of cartilage defect.

View larger version (142K): [in this window] [in a new window] [Download PPT slide]   Figure 3: MR image in a 44-year-old man with a grade 2A articular cartilage defect of the medial tibial plateau at arthroscopy. Coronal fat-suppressed intermediate-weighted fast spin-echo image of the knee shows a small area of subchondral bone marrow edema (arrow) within the medial tibial plateau.

View larger version (133K): [in this window] [in a new window] [Download PPT slide]   Figure 4: MR image in a 57-year-old man with a grade 3A articular cartilage defect of the medial tibial plateau at arthroscopy. Coronal fat-suppressed intermediate-weighted fast spin-echo image of the knee shows a large area of subchondral bone marrow edema (arrow) within the medial tibial plateau.

Pain Prediction
The location of a meniscal tear helped predict with statistical significance (P < .05) the location of a patient's knee pain. The location of subchondral bone marrow edema did not help predict the location of a patient's knee pain with statistical significance (P = .31).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 
Subchondral bone marrow abnormalities observed on MR images in patients with articular cartilage degeneration may be secondary to a combination of mechanisms similar to those responsible for the formation of subchondral cysts. Synovial fluid may be pumped into subchondral bone marrow through defects in articular cartilage, resulting in increased water content in the marrow extracellular space (16,17). Alternatively, the increased stress placed on the subchondral bone because of loss of the overlying articular cartilage may result in subchondral microfracture and marrow edema (17,18). Both mechanisms may be responsible for the MR signal abnormalities commonly identified within the subchondral bone marrow in patients with articular cartilage degeneration (10).

Zanetti and associates (14) have questioned the concept that subchondral bone marrow abnormalities on MR images in patients with articular cartilage degeneration truly represent edema. Tibial plateau specimens collected from patients with osteoarthritis who had MR signal abnormalities within the subchondral bone marrow showed no significant edema at histologic analysis. Instead, the MR signal abnormalities corresponded to a number of nonspecific histologic findings, including bone marrow fibrosis, bone marrow necrosis, and necrotic or remodeled trabeculae. However, the histologic diagnosis of bone marrow edema is relatively crude and relies on secondary signs such as the presence of swollen fat cells and the incipient disintegration of fat cells. Furthermore, water-sensitive MR pulse sequences such as fat-suppressed T2-weighted fast spin-echo sequence and short tau inversion-recovery sequence may depict minimal changes in extracellular water content of the subchondral bone marrow, which are undetectable at histologic analysis.

Subchondral bone marrow edema was frequently seen on MR images in our patients with articular cartilage degeneration of the knee joint. Bone marrow edema was identified in 60% of the 132 patients with arthroscopically proved articular cartilage defects. Other studies (10–13) have documented a 60%–80% prevalence of subchondral bone marrow edema in patients with osteoarthritis of the knee joint.

The prevalence of subchondral bone marrow edema beneath areas of articular cartilage degeneration in our study was strongly influenced by the grade of the cartilage defect. Subchondral bone marrow edema was more commonly observed beneath deep articular cartilage defects. To our knowledge, no previous study has documented the prevalence of subchondral bone marrow edema beneath arthroscopically proved articular cartilage defects of varying severity. However, authors of previous studies have found an association between the prevalence of subchondral bone marrow edema and the degree of osteoarthritis on knee radiographs. Using the Kellgren-Lawrence scale to grade the severity of articular cartilage degeneration, Link and associates (11) identified subchondral bone marrow edema in 30% of patients with grade 1 osteoarthritis, 36% of patients with grade 2 osteoarthritis, 77% of patients with grade 3 osteoarthritis, and 81% of patients with grade 4 osteoarthritis of the knee joint. Felson and associates (13) also noted that subchondral bone marrow edema was more commonly observed in patients with higher Kellgren-Lawrence grades of osteoarthritis of the knee joint.

One interesting observation in our study was that an overlying articular cartilage defect of grade 2B or greater was present in 87.4% of patients with subchondral bone marrow edema. Grading the severity of an articular cartilage defect on MR images may be difficult. Authors of previous studies using various MR pulse sequences have shown that articular cartilage defects were graded identically at MR imaging and at arthroscopy in only 57%–77% of patients (19–22). The presence of subchondral bone marrow edema may be useful as a secondary sign to help diagnose a deep partial-thickness or full-thickness articular cartilage defect of the knee joint.

The depth and cross-sectional area of subchondral bone marrow edema beneath areas of articular cartilage degeneration in our study were also strongly influenced by the grade of the cartilage defect. Deeper and larger areas of subchondral bone marrow edema were more commonly observed beneath deeper articular cartilage defects. To our knowledge, no previous study has documented an association between the depth and cross-sectional area of subchondral bone marrow edema and the degree of degeneration of the overlying articular cartilage. However, Link and associates (11) noted that large areas of subchondral bone marrow were more commonly seen in patients with higher Kellgren-Lawrence grades of osteoarthritis of the knee joint.

The prevalence of subchondral bone marrow edema in our study was higher within the medial compartment of the knee joint than within the lateral and patellofemoral compartments; the exact cause of this increased prevalence is unknown. The greater prevalence of subchondral bone marrow edema may be related to the normal increased loading of the medial compartment during weight bearing (23).

Subchondral bone marrow edema was identified beneath 1.4% of the articular surfaces of the knee joint that appeared normal at arthroscopy. The etiology of subchondral bone marrow edema beneath these areas of normal articular cartilage is unknown. One possibility is that the articular surfaces were incorrectly graded at the time of arthroscopic knee surgery. Articular cartilage softening or shallow cartilage defects may not always be detected at arthroscopy. In addition, diffuse loss of articular cartilage may be difficult to appreciate during arthroscopic examination of the knee joint. It is also possible that in some patients in our study, subchondral bone marrow edema could be contributed to other causes, such as altered weight bearing secondary to chronic knee pain or prior trauma that was not documented in the medical records.

The location of a meniscal tear in our study helped predict with statistical significance the location of a patient's knee pain. This finding may be partly explained by the selection bias inherent to our study. The majority of patients in the study underwent arthroscopic knee surgery for débridement or repair of meniscal tears detected at previously performed MR examinations. It is highly unlikely that the experienced orthopedic surgeons at our institution would choose to operate on these patients if their symptoms did not correlate with the location of their meniscal tears.

The location of subchondral bone marrow edema in our study did not help predict with statistical significance the location of a patient's knee pain. This finding may also be partially explained by the selection bias inherent to our study. Nevertheless, this finding suggests that factors other than subchondral bone marrow edema are responsible for knee pain in many patients with degeneration of the articular cartilage of the knee joint. Authors of other studies have come to similar conclusions. Sowers and associates (10) found that the presence of subchondral bone marrow edema could not satisfactorily explain knee pain in patients with osteoarthritis of the knee joint. Furthermore, Link and associates (11) found no correlation between subchondral bone marrow edema and the severity of knee pain in patients with degenerative joint disease. Additional studies need to be performed to better understand the precise etiology of knee pain in patients with osteoarthritis of the knee joint.

A major limitation of our study was the selection bias. In the majority of our patients with articular cartilage defects of the knee joint, meniscal tears had been identified at arthroscopy. In addition, all of the patients were symptomatic. Because of selection bias, our patient population represented only a subset of all individuals in our community with degeneration of the articular cartilage of the knee joint. Selection bias may have resulted in an overestimation or underestimation of the true prevalence of subchondral bone marrow edema in patients with articular cartilage degeneration. It is possible that asymptomatic individuals or individuals without meniscal tears have a higher or lower prevalence of subchondral bone marrow edema beneath articular cartilage defects than did patients in our study group. Selection bias must also be considered as a possible explanation of our finding that the location of a meniscal tear, but not the location of subchondral bone marrow edema, helped predict the location of a patient's knee pain with statistical significance.

There were several additional limitations. First, the interval between MR examination and arthroscopic knee surgery was as long as 2 months for some patients. It is possible that subchondral bone marrow edema developed or that articular cartilage degeneration worsened in some individuals during this period. Second, the location of knee pain was not documented in the clinical notes nor was described as being diffusely distributed throughout the knee in 22 patients in our study. These individuals had to be excluded from the statistical analysis used to determine whether the location of a meniscal tear and the location of subchondral bone marrow edema could help predict the location of a patient's knee pain. Third, the depth and cross-sectional diameter of subchondral bone marrow edema were measured with a caliber by using the numeric scale present at the periphery of each MR image. This is a somewhat crude method of measuring depth and cross-sectional diameter and provides merely a rough estimate of the degree of subchondral bone marrow edema within the osseous structures of the knee joint.

In conclusion, findings of our study have shown that subchondral bone marrow edema is commonly observed on MR images in patients with degeneration of the articular cartilage of the knee joint. Higher grades of articular cartilage defects are associated with higher prevalence and greater depth and cross-sectional area of subchondral bone marrow edema. When subchondral bone marrow edema is present, there is usually an overlying deep partial-thickness or full-thickness defect within the articular cartilage of the knee joint.

	ADVANCE IN KNOWLEDGE

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 

• The overall prevalence of subchondral bone marrow edema in patients with surgically confirmed articular cartilage degeneration of the knee joint is 19%, and the prevalence varies with the severity of the defect.
  

	FOOTNOTES

 
Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, R.K.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, R.K., P.S., A.D.S.; clinical studies, R.K., P.S., A.D.S.; statistical analysis, R.K., P.S., J.F.; and manuscript editing, all authors

	References

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2382050122v1 238/3/943    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Kijowski, R. Articles by De Smet, A. Search for Related Content PubMed PubMed Citation Articles by Kijowski, R. Articles by De Smet, A.