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1
Department of Orthopaedic Surgery, Chiba University School of Medicine, 1-8-1
Inohana, Chuo-ku, Chiba City, 260-8677, Japan.
2
Department of Orthopaedic Surgery, Matsudo City Hospital, 4005, Kamihongou,
Matsudo City, 271-0064, Japan.
3
Department of Radiology, Chiba University School of Medicine, Chiba City,
260-8677, Japan.
Received November 16, 1998;
accepted after revision August 25, 1999.
Address correspondence to S. Iida.
Abstract
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SUBJECTS AND METHODS. Forty-eight hips with osteonecrosis were examined consecutively with MR imaging and radiography. In a previously reported screening program, osteonecrosis was diagnosed on MR imaging when subchondral bands of abnormal signals were present. In the screening program, the MR images of 200 hips of 100 patients receiving high-dose steroid therapy were examined prospectively. Subchondral bands were detected in 48 hips at a mean of 14 weeks after the initiation of steroid therapy.
RESULTS. On follow-up MR imaging of 47 hips (one hip excluded) bone marrow edema was initially observed in 13 hips after the onset of hip pain. MR imaging of the remaining 34 hips did not reveal bone marrow edema and the patients were all asymptomatic. MR imaging of 31 of the 34 hips continued to show subchondral bands and MR imaging of the other three hips indicated that the subchondral bands had disappeared. When bone marrow edema was detectable, abnormal findings on radiography were slight but 11 (85%) of the 13 hips progressed to advanced osteonecrosis. Bone marrow edema was highly correlated with the subsequent collapse of the femoral head (p <0.0001).
CONCLUSION. Bone marrow edema was not present on initial MR imaging of osteonecrosis. Bone marrow edema should be considered a marker for potential progression to advanced osteonecrosis, and careful examinations for osteonecrosis are necessary when bone marrow edema is seen.
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Bone marrow edema is not an MR finding specific to osteonecrosis and has been reported to occur in the course of various conditions including transient osteoporosis [11,12,13,14,15], osteomyelitis [16], occult intraosseous fracture [17], and stress fracture [18]. Hofmann et al. [15], Potter et al. [14], and Dunstan et al. [19] reported histologic findings of transient osteoporosis similar to those of early osteonecrosis and mentioned that bone marrow edema with transient osteoporosis may be a reversible ischemic change; thereby, the theory of transformation of transient osteoporosis into osteonecrosis has made its way into the literature. Bone marrow edema is controversially considered to be the initial MR finding of osteonecrosis and an early ischemic change [20,21].
To clarify the initial MR finding of osteonecrosis, it is important to examine osteonecrosis in its earliest development. We think that the initiation of high-dose steroid therapy is a good method for evaluating the early development of steroid-induced osteonecrosis; therefore, we performed a prospective study using MR imaging in high-risk patients who started receiving high-dose steroids in a previous study so that we could detect osteonecrosis soon after its development [6]. In the current study, bone marrow edema was observed in 13 of 48 hips during a follow-up examination of early osteonecrosis. The purpose of this study was to evaluate the development of bone marrow edema in the early development of steroid-induced osteonecrosis and to clarify the relation of bone marrow edema to osteonecrosis.
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Screening Program
We performed a prospective study for steroid-induced osteonecrosis in
screened high-risk patients between June 1989 and December 1994. In that
earlier study, we first detected early osteonecrosis in 31 hips from a
screened population of 96 hips and reported that the appearance on MR imaging
of abnormal findings (bandlike zones), indicative of osteonecrosis, occurred
approximately 3 months after the initiation of high-dose steroid therapy
[6].
Eventually, 100 patients (200 hips) who had started receiving high-dose corticosteroids were enrolled in the screening program. The group consisted of 22 male patients and 78 female patients, with a mean age of 38 years (range, 8-76 years). The screening population consisted of 39 patients with systemic lupus erythematosus, 17 renal allograft recipients, 10 patients with pemphigus, 14 patients with polymyositis or dermatomyositis, three with mixed connective tissue disease, two with purpura, and 15 with other ailments. The initial steroid dose was at least 60 mg of prednisolone per day. This dosage was maintained for 4-8 weeks and then gradually decreased. Thirty-three patients were treated with pulse therapy (250-1000 mg/day of methylprednisolone for 3 days) during the first 3 months. After 6 months the mean dose was maintained at 15 mg/day.
For the screening program, the initial MR imaging was performed within 6 months after the initiation of steroid therapy. MR imaging was repeated every 1-3 months for approximately 1 year and every 3-6 months thereafter.
Patients
In this study, we reviewed 48 hips of 26 patients considered to have early
osteonecrosis in the screening program. The three males and 23 females had a
mean age of 36 years (range, 15-76 years). The patients with osteonecrosis
consisted of 14 with systemic lupus erythematosus, two with dermatomyositis,
three with polymyositis, two renal allograft recipients, two with pemphigus,
and three with other ailments. The diagnosis of osteonecrosis on MR imaging
was based on bandlike abnormal signals, bandlike hypointense zones on
T1-weighted images (Figs.
1A,2A,
and 3A), and matching
hyperintense zones on short tau inversion recovery (STIR) images (Figs.
1B,2B,
and 3B). The abnormal findings
on MR imaging with osteonecrosis were detected at a mean of 14 weeks (6-24
weeks) after the initiation of steroid therapy in the screening program.
Furthermore, 15 of the 48 hips with osteonecrosis in this study showed no
abnormalities at the first MR imaging, but a bandlike pattern developed 1-3
months after the screening. At the initial diagnosis of osteonecrosis, with
abnormal MR findings, the radiographic findings of the hips were normal (Figs.
1C,2C,
and 3C) and the patients were
asymptomatic. The mean follow-up period after the initial MR imaging was 52
months (8-96 months). Informed consent was obtained before the patients were
enrolled in this study.
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MR Imaging Studies
Forty-eight hips with osteonecrosis were studied consecutively using MR
imaging, radiography, and clinical examination. When a patient complained of
hip pain, MR imaging was performed as early as possible. On follow-up MR
imaging, an ill-defined marrow area of decreased signal intensity on
T1-weighted MR images and of increased signal intensity on STIR images was
considered to be bone marrow edema. Joint effusion was evaluated on STIR
images. The findings of MR imaging of the femoral head were regarded as normal
if the signal intensity was isointense with fat with or without the appearance
of an epiphyseal scar.
All MR imaging was performed using a 0.5-T superconductive unit (MRT-50; Toshiba, Tokyo, Japan) or a 1.5-T superconductive unit (Signa; General Electric Medical Systems, Milwaukee, WI). T1-weighted spin-echo images were obtained at 5- to 7.5-mm thickness with 1-mm intervals (TR range/TE range, 300-400/18-40). STIR images were obtained at 10-mm thickness without intervals (1500-3000/30-45; tau range, 100-150 msec) with a 0.5-T unit. Fast multiplanar inversion recovery images were obtained at 7.5-mm thickness with 1-mm intervals (TR/TE range, 3000/30-45; tau range, 130-150 msec) with a 1.5-T unit. Most images were reconstructed using a 256 x 256 data matrix acquired as the average of two signals.
The images were obtained with a body coil and a 35-cm field of view. Continuous slices in both the coronal and sagittal planes were taken in all patients. We obtained sagittal planes of the femoral neck on T1-weighted fat-saturated contrast-enhanced images for four hips before surgery.
Radiographic Studies
Radiographically, anteroposterior and frog-leg lateral views of the hips
and pelvis were obtained. Independent of the MR images, the radiographic stage
was determined according to the classification of Steinberg et al.
[22]: stage I, normal findings
on radiography; stage II, cystic and sclerotic change; stage III, subchondral
lucency or crescent sign; stage IV, flattening of the femoral head; stage V,
joint space narrowing; and stage VI, advanced degenerative change.
The MR images and radiographs were reviewed in conference. The observers were unaware of the patients' symptoms, and interpretations were determined by consensus.
Histologic Examinations
Histologic examinations were performed when patients underwent surgery. All
specimens were fixed in Bouin's solution and were decalcified overnight in a
solution of ammonium chloride, formic acid, and hydrochloric acid in water.
The specimens were rinsed in ethanol and were processed for paraffin
embedding. The histologic sections were cut at 5 µm and were stained with H
and E.
Statistical Analysis
For evaluation of statistical significance, the Fisher's exact test and the
Mann-Whitney test were performed using StatView version 4.0 software (Abacus,
Berkeley, CA).
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MR Images, Radiographic Findings, and Symptoms
On follow-up MR imaging, the imaging of osteonecrosis in 31 (66%) of 47
hips continued to reveal a bandlike pattern. The final radiographs revealed
that the 31 hips with bandlike patterns did not show collapse of the femoral
head; 29 hips were in stage I, and two hips were in stage II.
In three hips (6%), the abnormal findings of the bandlike pattern on imaging returned to normal within 1 year after the development of the bandlike hypointense zones. The findings on radiography of the three hips were normal and the patients were asymptomatic.
The other 13 hips (28%) were found to have diffuse signal abnormalities in the marrow of the femoral head and neck. The abnormal regions were ill defined and decreased in signal intensity (relative to normal fat) on T1-weighted images (Figs. 1D,2D,3D) and were diffusely hyperintense on STIR images, indicating bone marrow edema. Specifically, STIR images showed a focal hypointense lesion in the subchondral area of the femoral head surrounded by a diffuse hyperintense area (Figs. 1E,2E,3E). T2-weighted images, however, could not clearly reveal the subchondral focal lesions with osteonecrosis (Fig. 1F). Bone marrow edema was found in the living bone outside the bandlike hypointense zone on the initial MR imaging of osteonecrosis. On sagittal plane imaging of the femoral neck in four hips, the area with bone marrow edema was brightly enhanced on T1-weighted fat-saturated contrast-enhanced images (Figs. 2F and 2G).
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In the 13 hips, bone marrow edema was initially observed after the onset of hip pain. The average interval from the initial diagnosis of osteonecrosis to the onset of hip pain was 24 months (range, 2-75 months). The interval from the onset of hip pain to the MR imaging that indicated bone marrow edema was 1-4 weeks in five hips, 1-3 months in six hips, and 5-6 months in two hips. At the time bone marrow edema was detectable on MR imaging, all 13 hips were symptomatic. The 34 asymptomatic hips did not develop bone marrow edema. Bone marrow edema was highly correlated with the onset of hip pain (Fisher's exact test; p <0.0001).
The presence of a joint effusion was also observed in 12 (92%) of the 13 hips at the time bone marrow edema was observed (Figs. 1E,2E, and 3E). Soon after the onset of pain, bone marrow edema was detectable on MR imaging. However, radiography revealed slight abnormalities including subchondral cyst, sclerosis, and articular incongruity (Figs. 1G,2H, and 3F).
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At the final examination, 11 (85%) of the 13 hips with bone marrow edema had progressed to advanced osteonecrosis (Figs. 1H,2I,2J, and 3G); two hips were in stage II of Steinberg's classification [22], two hips in stage III, eight hips in stage IV, and one hip in stage V. Surgery was performed on five hips. In these five hips the final radiographic stage was determined immediately before the surgery. The average interval from the onset of hip pain to articular collapse in these 11 hips was 4 months (range, 1-7 months). Bone marrow edema was highly correlated with the subsequent collapse of the femoral head (Mann-Whitney test; p <0.0001) (Table 1). Surgical procedures performed were a transtrochanteric anterior rotational osteotomy in one hip, intertrochanteric varus osteotomy in three hips, and a vascularized iliac bone graft (conversion to total hip arthroplasty) in one hip.
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Histologic Findings
Two core biopsies were performed under radiographic guidance during surgery
on two right hips. All histologic sections in the subchondral areas showed
that the osteocyte lacunae were empty and the intertrabecular spaces were
filled with nonviable cells (Fig.
1I). The spaces bordering the necrotic areas were filled with
fibrous tissue and thickened trabeculae, which was the result of viable
appositional new bone that formed around centrally located areas of necrotic
bone. The areas adjacent to the necrotic bone showed exudates and fibroblastic
proliferation in the medullary spaces but no evidence of necrosis of the bone
itself, consistent with bone marrow edema
(Fig. 1J).
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Osteonecrosis is likely to be diagnosed after the onset of hip pain, and bone marrow edema is often observed at the first MR imaging; therefore, bone marrow edema could be considered the initial MR finding of osteonecrosis and an early ischemic change [9,10,14,15]; however, this theory has at least two problems.
The first problem is that by the time patients present with complaints of hip pain, they are already past the early stage of osteonecrosis. Before the onset of pain, it is expected that MR imaging would show bandlike patterns. To clarify the initial MR findings of osteonecrosis, it is important to evaluate asymptomatic osteonecrosis as early as possible. In our screening program, the initial MR imaging was performed within 6 months of the initiation of steroid therapy. The abnormal findings of osteonecrosis on MR imaging were detected at a mean of 14 weeks after the steroid therapy. The MR images enabled us to evaluate the early development of osteonecrosis. Furthermore, 15 hips with osteonecrosis showed no abnormalities at the first MR imaging, but bandlike patterns developed 1-3 months after the screening. Before the development of bandlike patterns, bone marrow edema was not observed in our study.
The second problem is that the subchondral focal lesions are likely to be overlooked on MR imaging because bone marrow edema develops at the area of the surrounding living bone, and surrounding bone marrow edema may obscure the subchondral focal abnormalities on MR images. Vande Berg et al. [23] called that which is seen on MR imaging of the surrounding bone marrow edema a "pseudo-homogeneous edema pattern."
At the stage when bone marrow edema is detectable on MR images, distinguishing osteonecrosis from transient osteoporosis is difficult but important [13,21,24,25]. Transient osteoporosis is a self-limited disease and can spontaneously resolve after protected weight-bearing and treatment of the symptoms. Osteonecrosis is likely to progress to destructive arthrosis, and, thus, early operative treatment may be needed. Vande Berg et al. [23] recommended the use of high-spatial-resolution T2-weighted images and contrast-enhanced images to see the subchondral focal lesions in relation to osteonecrosis.
To effectively evaluate the details of bone marrow abnormalities, we obtained MR images, STIR images, and T1-weighted spin-echo images. We are still lacking consensus regarding which MR sequences are best for detecting bone marrow lesions. Mirowitz et al. [26] reported that the conspicuity of bone marrow lesions is similar on fat-saturated T2-weighted and STIR images. On STIR images, the high signal intensity of normal fat is decreased; therefore, small focal lesions of osteonecrosis associated with bone marrow edema can be easily detected. On T2-weighted images it is often difficult to detect focal abnormalities with bone marrow edema. Therefore, STIR images are more useful for evaluating bone marrow edema with osteonecrosis. Furthermore, to detect focal abnormalities and to decide on the appropriate surgical procedure, MR imaging in other planes is recommended. A sagittal view of the femoral neck is sometimes useful for evaluating the necrotic area. Such precise evaluations of MR images showing osteonecrosis should lead to the recognition that bone marrow edema is likely to be observed in the surrounding living bone in the neck and intertrochanteric area of the proximal femur.
On T1-weighted fat-saturated contrast-enhanced images, the areas with bone marrow edema were brightly enhanced (Figs. 2F and 2G); the increase in enhancement could have been a result of a hyperemia and an increase in capillary permeability.
The mechanisms responsible for bone marrow edema with osteonecrosis are still unknown; however, we suspect that an abnormal mechanical stress may have an important role in the development of bone marrow edema. At the onset of hip pain, the trabecular fracture in the necrotic area leads to abnormal distribution of weight-bearing forces, and altered weight-bearing may cause abnormal mechanical stress on surrounding living bone in the neck of the femur and intertrochanteric area. As a consequence, surrounding patterns of bone marrow edema may develop. Shimizu et al. [27] reported a case in which a bandlike pattern changed to surrounding bone marrow edema, with the focal lesion appearing immediately after the femoral head was beginning to collapse. Recently, Schweitzer and White [28] reported that altered biomechanics should be added to the list of causes of bone marrow edema. We think that bone marrow edema does not represent the ischemic change of early osteonecrosis; rather, it represents a secondary phenomenon from the mechanical stress and collapse of the femoral head.
When bone marrow edema was detectable in 13 hips, abnormal findings on radiography were slight but 11 hips (85%) with bone marrow edema subsequently progressed to advanced osteonecrosis. Bone marrow edema should be considered a marker for potential progression to advanced osteonecrosis. Therefore, appropriate treatment should be instituted for a hip in which the radiographic change is slight but bone marrow edema is detectable.
Segmental collapse is mainly a matter of time and the size of the necrotic lesion. Osteonecrotic lesions in early stages have a risk of developing a segmental collapse; therefore, further follow-up is recommended.
In conclusion, the initial abnormal findings on MR imaging showed a bandlike pattern. Diffuse abnormalities indicating bone marrow edema developed after the onset of hip pain. Bone marrow edema was not revealed on initial MR imaging of osteonecrosis but developed in conjunction with the collapse of the femoral head.
Acknowledgments
We thank Yasushi Nawata and Katsuhiko Takabayasi of Chiba University and
Kaoru Sakamoto of Sakura National Hospital for contributing data regarding the
group of patients studied.
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