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Musculoskeletal Imaging |
1 From the Department of Radiology and Medical Imaging, Cliniques Universitaires St Luc, Universite catholique de Louvain, 10 Avenue Hippocrate, 1200 Brussels, Belgium (B.C.V.B., J.J.M., F.E.L., B.E.M.) and the Center for Biostatistics and Medical Documentation, Universite catholique de Louvain, Cliniques Universitaires de Mont Godinne, Yvoir, Belgium (J.J.). Received June 29, 1998; revision requested August 5; final revision received November 11; accepted February 22, 1999. Address reprint requests to B.C.V.B. (e-mail: vandeberg@rdgn.ucl.ac.be).
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: The authors reviewed MR images of 72 femoral head lesions in 42 men and 25 women (median age, 48 years) with equivocal radiographic findings and bone marrow edema seen at MR imaging (T1- and T2-weighted images in all patients and contrast material–enhanced T1-weighted images in 39 patients). Follow-up MR images showed 57 lesions to be transient and 15 to be irreversible. The presence and size of subtle subchondral features observed on initial MR images were compared for both types of lesion.
RESULTS: Lack of any additional subchondral change on T2-weighted or contrast-enhanced T1-weighted images had 100% positive predictive value for transient lesions. For irreversible lesions, presence of a subchondral area of low signal intensity at least 4 mm thick or 12.5 mm long had positive predictive values of 85% and 73%, respectively, on T2-weighted images and 87% and 86%, respectively, on contrast-enhanced T1-weighted images.
CONCLUSION: Careful assessment of subchondral changes enables confident differentiation between early irreversible lesions and transient bone marrow edema lesions.
Index terms: Alcohol, 443.869 • Bone marrow, edema, 443.499 • Hip, MR, 443.121411, 443.12143 • Hip, necrosis, 443.44 • Myeloma, 443.34 • Osteoporosis, 443.56 • Osteomalacia, 443.57 • Steroids, complications, 443.542
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Typically, femoral head osteonecrosis is characterized by a subchondral lesion of variable signal intensity that is demarcated from the surrounding tissue by a rim of low signal intensity on T1-weighted MR images and of low and high signal intensity on T2-weighted MR images (2,3,6–10). This lesion pattern differs from the bone marrow edema pattern that is characterized by an ill-defined epiphyseal marrow area of low signal intensity on T1-weighted MR images and of intermediate to high signal intensity on T2-weighted images (11–14). The bone marrow edema pattern is nonspecific and can be observed in association with several conditions, including transient osteoporosis (12,15–17), transient bone marrow edema syndrome (12,13,16), and epiphyseal stress fracture (18,19). These conditions are self-limiting disorders that necessitate no specific therapy other than palliative measures.
Femoral head osteonecrosis occasionally manifests with the bone marrow edema pattern at MR imaging, with, however, no visible reactive interface between necrotic and viable tissue (3,12,20–22). Therefore, when the bone marrow edema pattern is present in a femoral head, early differentiation between irreversible epiphyseal osteonecrosis and a spontaneously transient lesion is important to prevent overtreatment of spontaneously resolving lesions and reserve more aggressive therapy for lesions that are associated with a poor prognosis (1,13,14,23–26).
On T2-weighted and contrast material–enhanced T1-weighted MR images of bone marrow edema lesions of the femoral head, several discrete features can occasionally be observed in the subchondral area of the femoral head (12,17,19,26). In hypothetical terms, assessment of the presence of these subchondral changes and precise determination of their spatial characteristics on MR images could help differentiate irreversible from transient epiphyseal lesions. We previously demonstrated the prognostic value of MR imaging in the setting of lesions of the femoral condyle (27), and we now address lesions of the femoral head that show the bone marrow edema pattern.
In January 1989, we started a prospective study that included all patients in whom MR imaging demonstrated the bone marrow edema pattern in the femoral head and in whom radiographs were inconclusive; these patients were treated conservatively and were followed up to determine the outcome of the lesions. Our aims were to compare irreversible and transient lesions for the frequency and extent of subchondral changes observed at MR imaging and to determine the features that most reliably enable differentiation between these lesions.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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All patients underwent an initial MR study performed at our institution between January 1989 and January 1997. None of the patients had been referred for consultation. In addition, 10 other lesions (in 10 patients) that fulfilled the inclusion criteria at the onset of the disease were excluded from the current study because of the lack of definite imaging proof of lesion outcome. Of the 10 patients with no available imaging follow-up, seven, who were contacted by phone, reported no residual pain, and three were lost to follow-up.
Nine lesions occurred during or immediately after pregnancy. Other associated findings were frank, diffuse osteoporosis seen on conventional radiographs (n = 5); osteomalacia (n = 5); history of alcohol abuse (n = 5), steroid therapy (n = 4), or fluoride therapy (n = 1); renal transplantation (n = 5); chronic renal failure (n = 1); radiation therapy (n = 1); and untreated multiple myeloma (n = 2). Because all patients were not primarily evaluated for the presence of these conditions, we cannot verify the importance of the conditions in the pathogenesis of the lesions. In the other 34 patients (34 lesions), the medical history was unremarkable.
Conventional radiographs, including anteroposterior views of the pelvis and anteroposterior and lateral views of the symptomatic hips, showed either no abnormality (n = 22) or nonspecific findings, which were described as discrete subchondral sclerosis (n = 10), subchondral bone rarefaction (n = 25), or both (n = 15). Forty-seven patients had undergone technetium 99m bone scanning that consistently demonstrated increased isotope uptake in the femoral heads, which corresponded to the bone marrow edema pattern seen at MR imaging.
Initial MR Imaging
MR imaging was performed at a mean (±SD) of 9.7 weeks ± 6.4 (median interval, 8 weeks; range, 2–32 weeks) after the onset of symptoms by using a 1.5-T (56 lesions) or a 0.5-T (16 lesions) superconducting magnet (Gyroscan; Philips Medical Systems, Best, the Netherlands).
After acquisition of sets of transverse T1-weighted scout MR images and comparative coronal T1-weighted MR images of both hips, coronal T1-weighted images of the symptomatic hips were systematically obtained by using a 40 x 20-cm supple receiver-only surface coil (Philips Medical Systems) wrapped around the symptomatic hip joint. In 57 lesions, sagittal T1-weighted images were obtained in a plane with approximately 10° of internal rotation with respect to the plane perpendicular to the femoral neck.
T1-weighted spin-echo MR images were obtained with the following parameters: 350–550/20–25 (repetition time msec/echo time msec), 14–20-cm field of view, 3.5–5.0-mm section thickness, 0.5-mm intersection gap, two to four signals acquired, and a 230 x 256 matrix.
T2-weighted spin-echo MR images also were obtained by using the surface coil. Coronal or sagittal images were obtained as necessary, depending on the topography of the marrow changes on the T1-weighted images. The sagittal plane was favored when femoral head changes predominated anteriorly or posteriorly, and the coronal plane was selected when the predominant area of involvement was the upper aspect of the femoral head. Both sagittal and coronal images were obtained in 21 lesions.
Fifty-four sets of sagittal and 39 sets of coronal T2-weighted spin-echo images were obtained with the following parameters: 2,000–2,500/100–120, 16–20-cm field of view, 4–5-mm section thickness, 0.5-mm intersection gap, one to two signals acquired, and a 180 x 256 matrix.
T1-weighted spin-echo MR images were obtained after administration of 0.1 mmol/kg gadoterate dimeglumine (Dotarem; Guerbet, Roissy, France) in 39 consecutive lesions observed between 1989 and 1993. In these patients, the technique and spatial parameters were identical to those used for nonenhanced T1-weighted sagittal (n = 29) or coronal (n = 32) MR imaging. At the time of the study, fat-saturated T1-weighted MR images were not available at our MR unit. The duration of the MR examination was 25–45 minutes.
Other sequences included T2*-weighted gradient-echo, T2-weighted fast spin-echo, fat-saturated fast spin-echo, intermediate-weighted, and T2-weighted imaging sequences. These sequences were performed in some patients during the study period, but the images were not included in the review process.
Patient Follow-up and Determination of Lesion Outcome
All patients were advised to reduce weight bearing by using two crutches and then one crutch during 3–5 weeks. Nonsteroid analgesics were prescribed. Patients were not confined to bed rest. All patients were informed of the prospective study and consented to undergo future MR or radiographic studies to determine lesion outcome. At the time of this study, our ethical committee did not mandate its approval for noninvasive diagnostic procedures of potential clinical importance, provided that informed consent had been obtained from the patients.
Follow-up imaging was performed regardless of whether symptoms persisted and continued for at least 24 months, unless either conventional radiographs showed typical osteonecrosis with epiphyseal collapse or MR images showed complete resolution of marrow abnormalities. A total of 111 follow-up MR studies were obtained, including 64 studies obtained within 6 months after the initial study, 24 obtained 6–12 months after the initial study, and 23 obtained more than 12 months after the initial study. Seven patients did not come to the scheduled follow-up MR examination but decided to undergo follow-up MR imaging during 1997, 15–72 months (mean, 46 months) after the initial study. Follow-up MR studies included sagittal and coronal T1-weighted images obtained with the same technical parameters as for the initial studies. Follow-up T2-weighted images were obtained when persistent abnormalities were present on T1-weighted images.
A lesion was considered to be transient if normal signal intensity was observed in the femoral head on follow-up T1-weighted MR images, with resolution of the abnormalities that had been seen on initial MR studies. A lesion was considered to be irreversible if typical osteonecrosis occurred or if residual changes were demonstrated at MR imaging after at least 2 years of follow-up.
Analysis of Initial MR Images
The 283 sets of initial MR images (129 sets of T1-weighted images, 93 sets of T2-weighted images, and 61 sets of contrast-enhanced T1-weighted images) were reviewed independently by two musculoskeletal radiologists (B.C.V.B., F.E.L.) who were unaware of patient name, age, and sex and of lesion outcome. Initial radiographs, bone scans, initial large-field-of-view comparative T1-weighted coronal MR images, and all follow-up imaging studies were not available. All sets of images from each case were reviewed separately from each other. To assess intraobserver reproducibility, one radiologist (B.C.V.B.) reviewed the 283 sets of images 6 months after initial analysis.
Bone marrow edema was a common MR imaging feature of all lesions, and no lesion manifested with the demarcation rim or reactive interface typical of avascular necrosis. Because of previously reported (12,17,19,26) additional subchondral findings, we studied three parameters to determine their prognostic significance: low-signal-intensity subchondral areas, epiphyseal lines, and contour deformities (Fig 1).
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Measurements were performed on the images, which were printed on separate films with a 1.2–1.4 zoom factor, by using a 0.5-mm–graduated ruler. In addition, the extent of the ill-defined area of low signal intensity was determined on coronal T1-weighted MR images and was considered to involve either the epiphysis alone or both the epiphysis and the femoral neck. These subchondral changes are illustrated in Figures 2–5.
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2 test for independent categoric variables, the Student t test for numeric variables, and the Wilcoxon rank sum test for ordinal variables. All tests were two tailed. A P value of less than .05 was considered to indicate a significant difference. The ability of the statistically significant parameters to aid in differentiation of irreversible from transient lesions was assessed by calculating the sensitivity, specificity, and positive and negative predictive values for qualitative parameters and receiver operating characteristic (ROC) curves for quantitative measurements. ROC curves obtained for the length and the thickness of the subchondral low-signal-intensity component on T2-weighted and contrast-enhanced T1-weighted images were constructed for both observers by using maximum likelihood estimation calculated with the LABROC 1 program (C. Metz, Chicago, Ill). Values measured by the first observer were used to calculate sensitivities, specificities, and predictive values.
Reproducibility of findings between observers was assessed with the 
coefficient for categoric parameters and with correlation coefficients for numeric variables. In general, a value of less than 0.4 represented a poor level of agreement; a value of 0.41–0.60, fair agreement; a value of 0.61–0.80, good agreement; and a value of 0.81–1.00, excellent agreement (28). To study intra- and interobserver reproducibility, parameters derived from all sagittal and coronal images were used. To study the prognostic significance of MR parameters, the more elevated values from either the sagittal or the coronal images were used for statistical analysis.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Fifteen lesions were irreversible. Nine lesions (in eight patients) showed epiphyseal collapse with a subchondral bone fracture on conventional radiographs after 2–18-month follow-up (mean, 6.3 months). Seven patients, each with one lesion, were treated with total hip replacement. Two lesions in the same patient were well tolerated 47 months after disease onset. Six other lesions (in six patients) showed small, residual subchondral changes at MR imaging but no definite signs of osteonecrosis on radiographs. These six lesions were well tolerated clinically, and none of these patients had undergone surgery at the time of this writing. These six lesions were followed with MR imaging (20 studies) for a mean of 41 months (range, 24–76 months) after the initial MR study.
Clinical and Radiographic Findings
There were no significant differences between the group of patients with irreversible lesions (n = 15) and the group with transient lesions (n = 57) in terms of sex, age, side of the lesion, and interval between the onset of symptoms and the time of initial MR imaging (Table 1). Sixteen (46%) of 35 transient lesions observed in men and 13 (59%) of 22 transient lesions observed in women involved the left femoral head. The frequencies of the different patterns of changes determined on radiographs (osteopenia, subchondral sclerosis, mixed osteopenia and sclerosis, and normal appearance) were not significantly different between the groups.
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Frequency of Subchondral Changes in Irreversible and Transient Lesions
On T1-weighted images, there was no difference in the frequency of subchondral changes between irreversible and transient lesions, and the usefulness of T1-weighted images for help in predicting the outcome was not further studied. Lack of additional subchondral changes was significantly more frequent in transient lesions than in irreversible lesions on T2-weighted images (24 [42%] of 57 transient and none [0%] of 15 irreversible lesions; P < .001) and contrast-enhanced T1-weighted images (seven [23%] of 30 transient and none [0%] of nine irreversible lesions; P < .001).
Low-signal-intensity subchondral areas (Figs 3–5) were significantly more frequent in irreversible than in transient lesions on T2-weighted images (15 [100%] of 15 irreversible and 17 [30%] of 57 transient lesions; P < .001) and on contrast-enhanced T1-weighted images (nine [100%] of nine irreversible and nine [29%] of 30 transient lesions; P < .001).
Epiphyseal deformities (Fig 4) were significantly more frequent in irreversible than in transient lesions on T2-weighted images (10 [66%] of 15 irreversible and 11 [19%] of 57 transient lesions; P = .002) and on contrast-enhanced T1-weighted images (nine [100%] of nine irreversible and eight [25%] of 30 transient lesions; P < .001).
Frequency of epiphyseal lines (Figs 2, 4) was not significantly different between irreversible and transient lesions on either T2-weighted (10 [66%] of 15 irreversible and 28 [49%] of 57 transient lesions) or contrast-enhanced T1-weighted (six [66%] of nine irreversible and 15 [50%] of 30 transient lesions) images.
Prognostic Value of the Subchondral Changes on MR Images
Lack of subchondral changes.—Lack of additional subchondral changes on both T2-weighted and contrast-enhanced T1-weighted images had excellent positive predictive value for the recognition of transient lesions (Table 2).
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coefficients for intra- and interobserver reproducibility of the degree of epiphyseal deformity were moderate (Table 6). Epiphyseal lines.—Presence of epiphyseal lines had poor positive predictive value as an indicator of an irreversible lesion (Table 3). Length and distance of epiphyseal lines from the epiphyseal contour were not significantly different between transient and irreversible lesions.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In the current prospective study, the spontaneous outcome in 72 femoral head lesions that were not treated surgically and that showed the bone marrow edema pattern was determined by using serial imaging. The features observed at initial MR imaging in 57 transient lesions and 15 irreversible lesions were reviewed to determine whether initial MR studies enabled early differentiation of irreversible lesions from transient lesions.
The results of our study allowed us to draw the following conclusions. First, absence of additional subchondral changes other than the bone marrow edema pattern on T2-weighted or contrast-enhanced T1-weighted images had excellent specificity and positive predictive value for transient lesions. Actually, all 24 (33%) lesions that showed no subchondral marrow changes other than the bone marrow edema pattern on T2-weighted images were found to be transient on follow-up MR studies. The transformation of a lesion that initially showed only the bone marrow edema pattern into an irreversible lesion was not observed in the current study.
Second, in about two-thirds of 72 bone marrow edema lesions, additional focal changes were depicted in the area adjacent to the subchondral bone plate on T2-weighted and contrast-enhanced T1-weighted MR images obtained with a small field of view. Actually, subchondral areas of low signal intensity, subtle deformity of the epiphyseal contours, and epiphyseal lines of low signal intensity were seen on T2-weighted images in 44%, 29%, and 52% of lesions, respectively. These three additional changes in signal intensity were observed in both transient and irreversible lesions. Subchondral low-signal-intensity areas and contour deformity, but not epiphyseal lines, were significantly more frequent in irreversible lesions than in transient lesions.
Finally, determination of the length and thickness of low-signal-intensity subchondral areas and of the importance of contour deformity on either T2-weighted or contrast-enhanced T1-weighted images helped differentiate irreversible from transient lesions. The presence and extent of epiphyseal lines of low signal intensity, however, had poor prognostic value.
Subchondral areas of low signal intensity had the greatest prognostic importance. In our study, a low-signal-intensity subchondral area with a thickness of at least 4 mm on T2-weighted or contrast-enhanced T1-weighted images had a positive predictive value of greater than 85% for prediction of lesion irreversibility. Similarly, a low-signal-intensity subchondral area with a length of at least 12.5 mm had a positive predictive value of greater than 73%. The values were indicative of excellent reproducibility of the size measurements obtained with both types of images but were greater with contrast-enhanced T1-weighted images than with T2-weighted images, probably because of better signal intensity contrast between epiphyseal marrow, subchondral changes, and articular cartilage on the contrast-enhanced T1-weighted images.
The magnitude of epiphyseal contour deformity also helped with recognition of irreversible lesions, with frank deformity more frequently associated with irreversible lesions than with transient lesions. However, because reproducibility of the determination of the degree of deformity was fair, the value of this criterion warrants further assessment. Computed tomography is superior to MR imaging for demonstrating changes in the sphericity of the femoral head (32,33) and could be used to assess epiphyseal contours when findings of bone marrow edema lesions are equivocal.
MR imaging techniques, patient selection criteria, and outcome definitions used in the current study must be emphasized to avoid misinterpretation of our results. First, all images were obtained by using a surface coil and a small field of view. The higher spatial resolution achieved on these images than on large-field-of-view images could account for the high detection rate and good reproducibility of measurement of subchondral changes. It is possible that previously described (20) irreversible bone marrow edema lesions also had additional subchondral changes that were underestimated on the relatively low-resolution images obtained in the early era of MR imaging.
Second, we deliberately focused our investigation on ambiguous clinical and imaging conditions. Femoral head osteonecrosis lesions with obvious epiphyseal collapse seen on radiographs or with well-delimited marrow changes seen on MR images were not included in this study. Bone marrow edema lesions observed in association with joint-space narrowing on conventional radiographs or with cartilage lesions on MR images also were excluded. However, we did include 20 bone marrow edema lesions with radiographic features characteristic of transient osteoporosis of the hip. These lesions were included because focal osteopenia was rarely recognized by referring physicians and radiologists.
Finally, irreversible lesions did not systematically correspond to typical osteonecrosis, which was observed in nine of 15 irreversible lesions. The other six such lesions showed small residual subchondral signal intensity heterogeneities at MR imaging after a follow-up of 24–72 months. These small subchondral bone lesions were well tolerated clinically. A further study with a larger series of patients is needed to determine whether initial MR studies enable differentiation of lesions that will progress to typical osteonecrosis from relatively more benign lesions that will show only small residual changes at follow-up.
The fact that contrast-enhanced T1-weighted images helped differentiate irreversible from transient lesions does not imply that contrast material is necessary: Prognostic features depicted on T2-weighted images were similar to those observed on contrast-enhanced T1-weighted images. Our initial experience with contrast-enhanced T1-weighted images definitely helped by increasing confidence for detection of low-signal-intensity areas and focal deformities on T2-weighted images, because changes were often more conspicuous on contrast-enhanced T1-weighted images. In our current routine clinical practice, we reserve the performance of contrast-enhanced MR imaging for rare cases of equivocal findings on T2-weighted images. Furthermore, in our more recent experience, subchondral changes observed on standard T2-weighted spin-echo MR images also were well depicted on fast spin-echo T2-weighted and fat-saturated fast intermediate-weighted and T2-weighted images. These observations must be addressed in future studies.
The current study has several limitations inherent to the study design. First, implicit in the determination of a spontaneous lesion course is that no surgical intervention was performed. No correlation with histologic results can thus be provided. Results from previous studies (6,34,35) have demonstrated that subchondral areas of low signal intensity on either T2-weighted or contrast-enhanced T1-weighted images correspond to bone and marrow necrosis. Our observation that the size of these subchondral low-signal-intensity areas was directly related to outcome supports those previous results. The bone marrow edema pattern in itself is nonspecific, and histologic findings (36,37) from biopsy specimens of bone marrow edema lesions have demonstrated a range of features, including immature fibrovascular tissue, interstitial edema, bone and marrow necrosis, and variable changes in the trabecular network. The prognostic importance of the finding of bone and marrow necrosis at microscopic examination remains to be assessed, because bone and marrow cell death is a sign observed not only in epiphyseal osteonecrosis (38) but also in fractures (39), degenerative disease (40,41), and transient osteoporosis (20, 37,42).
Second, the effect on lesion outcome of a decrease in physical activity, which was recommended to all patients, remains unknown. Early recognition of a lesion and a subsequent decrease in physical activity could have influenced lesion outcome.
Finally, we addressed intra- and interobserver reproducibility of the identification of features that were helpful for determination of the prognosis. As in any single-center study, reproducibility is biased due to the experience that is progressively acquired by the reviewers. A multicenter study is mandatory to validate our observations.
Results from the current study of idiopathic femoral head lesions that show the bone marrow edema pattern at MR imaging demonstrate that precise analysis of the subchondral marrow changes depicted on T2-weighted or contrast-enhanced T1-weighted images helps differentiate irreversible lesions from transient lesions. Absence of subchondral low-signal-intensity areas on T2-weighted or contrast-enhanced T1-weighted images is invariably indicative of a spontaneous favorable outcome with resolution of the lesions. Thickness and length of the subchondral areas of low signal intensity on T2-weighted or contrast-enhanced T1-weighted images are the most important reproducible features for differentiation of irreversible lesions from transient lesions.
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Acknowledgments |
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, B.C.V.B.; study concepts, B.E.M., J.J.M.; study design, B.C.V.B.; definition of intellectual content, B.C.V.B., J.J.M.; literature research, B.C.V.B.; clinical studies, B.C.V.B., J.J.M., F.E.L.; data acquisition, B.C.V.B., J.J.M., F.E.L.; data analysis, B.C.V.B., F.E.L.; statistical analysis, J.J.; manuscript preparation, B.C.V.B.; manuscript editing, B.C.V.B., J.J.M., B.E.M., F.E.L.; manuscript review, all authors.
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References |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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