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(Radiology. 1999;213:715-722.)
© RSNA, 1999

Musculoskeletal Imaging

Bone Marrow Edema and Associated Pain in Early Stage Osteonecrosis of the Femoral Head: Prospective Study with Serial MR Images1

Kyung-Hoi Koo, MD, In-Oak Ahn, MD, Rokho Kim, MD, Hae-Ryong Song, MD, Soon-Taek Jeong, MD, Jae-Boem Na, MD, Yong-Sik Kim, MD and Se-Hyun Cho, MD

1 From the Departments of Orthopedic Surgery (K.H.K., H.R.S., S.T.J., S.H.C.) and Radiology (I.O.A., J.B.N.), Gyeong-Sang National University School of Medicine, 90 Chilam-dong, Chinju 660-702, South Korea; the Department of Environmental Health, School of Public Health, Seoul National University, South Korea (R.K.); and the Department of Orthopedic Surgery, Saint Mary's Hospital, the Catholic University of Korea, Seoul, South Korea (Y.S.K.). Received December 16, 1998; revision requested March 6, 1999; final revision received April 13; accepted June 9. Address reprint requests to K.H.K. (e-mail: khkoo@nongae.gsnu.ac.kr).


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To determine whether the marrow edema around focal osteonecrosis on magnetic resonance (MR) images is associated with clinical symptoms.

MATERIALS AND METHODS: Thirty-three patients with 37 hips showing early stage osteonecrosis of the femoral head were followed up at 3-month intervals with clinical evaluation, conventional radiography, and serial MR imaging.

RESULTS: Seven (50%) of 14 symptomatic hips showed marrow edema around focal osteonecrosis on initial MR images, whereas only one (4%) of 23 asymptomatic hips showed edema (P < .01). Six (86%) of seven hips that were moderately to severely painful were associated with surrounding marrow edema. All eight hips showing osteonecrosis with marrow edema at the initial MR examination had joint effusion and exhibited intense radionuclide uptake in the proximal femur, which corresponded to the extent of edema on MR images. In all eight hips, the marrow edema resolved on follow-up MR images, and the pain subsided with the resolution of edema.

CONCLUSION: The results of this study suggest that the combination of marrow edema of the proximal femur and focal osteonecrosis of the femoral head are strongly associated with hip pain in early stage osteonecrosis, even prior to collapse. Pain improvement usually parallels the resolution of edema.

Index terms: Bone marrow, edema, 443.833 • Bone marrow, MR, 443.121411 • Bone marrow, radionuclide studies, 443.12172 • Femur, MR, 443.121411 • Femur, necrosis, 443.44 • Femur, radionuclide studies, 443.12172 • Hip, MR, 44.121411 • Hip, necrosis, 44.44 • Hip, radionuclide studies, 44.12172


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In osteonecrosis of the femoral head, disabling pain may appear before collapse and joint incongruity are evident radiographically (1–5). The cause of pain in this early stage of osteonecrosis is not well understood. Accurate knowledge of the cause of pain in early stage osteonecrosis is essential to select an appropriate treatment plan and to avoid unnecessary joint replacement.

Transient osteoporosis of the hip differs from osteonecrosis in that there is no focal subchondral abnormality as is seen in osteonecrosis of the femoral head. Bone marrow edema seen on magnetic resonance (MR) images of the proximal femur has been a characteristic finding of transient osteoporosis of the hip (6–11). Marrow edema appears as low signal intensity on T1-weighted MR images and high signal intensity on T2-weighted images of the proximal femur. Several authors (12,13) observed similar findings around the focal lesion of osteonecrosis of the femoral head on MR images. In these early studies, these findings were described as a diffuse or homogeneous pattern of osteonecrosis. Rao et al (14) showed a strong correlation between marrow edema and the pain in acute bone infarct in their MR imaging study of patients with sickle cell anemia.

In this prospective study with serial MR images, we investigated the course of marrow edema of the proximal femur and its relationship with the pain in early stage osteonecrosis prior to collapse.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
The subjects for this study were the patients who participated in a clinical trial for the effectiveness of core decompression, which was previously reported (15,16). To detect early stage osteonecrosis of the femoral head and to evaluate the marrow of the proximal femur around focal osteonecrosis, MR imaging was performed in the following three categories of hips: (a) the contralateral hips of patients who had findings of osteonecrosis in one hip at conventional radiography, (b) the hips of patients who had hip symptoms without evidence of osteonecrosis at conventional radiography, and (c) osteonecrotic hips that had been diagnosed at conventional radiography and that were also without evidence of collapse. From this base population, hips that met predefined diagnostic criteria for osteonecrosis of the femoral head were investigated.

The diagnosis was established by evidence of osteonecrosis on conventional radiographs, MR images, or both. MR images considered positive for osteonecrosis showed crescentic areas of low signal intensity in the weight-bearing portion of the femoral head, small or large ringlike lesions with homogeneous or inhomogeneous central areas, diffuse decreased signal intensity with a dark band, and collapse of the femoral head (17).

The hips were staged according to the international classification system of the Association Research Circulation Osseous (ARCO) (18): stage 0, bone biopsy results consistent with osteonecrosis, normal findings on all other tests; stage I, positive scintigram, MR image, or both; stage II, radiographic abnormalities, no sign of collapse of the femoral head; stage III, crescent sign; stage IV, flattened articular surface, narrow joint space, and changes in acetabulum. Those with early osteonecrosis without radiologic evidence of collapse (ARCO stages I, II, and III) were selected.

Between June 1990 and June 1992, 37 femoral heads in 33 consecutive patients (31 men, two women; age range, 18–68 years) were investigated. There were 22 stage I hips (20 contralateral hips of patients who had findings of osteonecrosis in one hip at conventional radiography and two hips of patients who had hip symptoms without evidence of osteonecrosis at conventional radiography), 11 stage II and four stage III hips (osteonecrotic hips that were diagnosed at conventional radiography and that were also without evidence of collapse). The conditions or factors associated with osteonecrosis included alcohol abuse in 28 patients and a history of high-dose steroids in three patients with nephrotic syndromes (n = 2) or hypophysectomy state due to craniopharyngioma (n = 1). In the remaining two patients, no risk factor could be identified.

All the femoral heads were studied by means of clinical evaluation, conventional radiography, MR imaging, and bone scintigraphy. After the initial evaluation, hips were randomized for treatment with either core decompression with cancellous bone graft or conservative management. Eighteen hips were treated with core decompression, and the remaining 19 hips were treated conservatively. Every 3 months, the patients underwent clinical, radiographic, and MR examinations. The occurrence of marrow edema around focal necrosis was estimated from the serial MR images. The association of marrow edema with joint effusion was also evaluated. Bone marrow pressure measurements and histopathologic findings of hips in patients undergoing core decompression or arthroplasty were studied. In the cases treated with core decompression, the effect of core decompression on the relief or prevention of marrow edema was evaluated.

The follow-up evaluation was continued until the conventional radiographs demonstrated the collapse of the femoral head. The collapse of the femoral head was defined as a sinking of the articular surface of 2 mm or more in comparison with the normal contour in the initial radiograph by using a template of concentric circles (15,16). In cases in which marrow edema persisted at the time of collapse, follow-up MR imaging was continued until the edema resolved. All patients provided written informed consent for participation, and the protocol was approved after institutional review at the Gyeong-Sang National University Hospital.

The clinical evaluation focused on the presence and severity of pain. Other functional evaluations had limited value because most patients had advanced osteonecrosis of the contralateral hip, which was treated with total hip arthroplasty before or after the initial evaluation. Pain was recorded by using the method of Merle d'Aubigne et al (2) as modified by Charnley (19) (Table 1).


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  		TABLE 1. Evaluation of Hip Pain
 
MR imaging was performed by using either of two 1.0-T superconducting units (SMT 100X; Shimadzu, Kyoto, Japan). T1-weighted spin-echo images (150–600/15–20 [repetition time msec/echo time msec]) and T2-weighted images (1,800–2,500/80–90) were obtained in coronal and sagittal planes. The section thickness was 5–10 mm with no gap. Images were reconstructed by using a 128 x 256 or 256 x 256 matrix. The number of signals acquired ranged from one to four. MR images were assessed by three observers (I.O.A., H.R.S., S.T.J.) who were blinded to the clinical status of the hips. The MR findings considered positive for marrow edema were signal abnormalities that were of low intensity on T1-weighted images and isointense or hyperintense on T2-weighted images and that involved the femoral head and neck beyond the necrotic zone and extended to the trochanteric area. The joint effusion was assessed and graded by using the system suggested by Mitchell et al (20). The hips with enough fluid to surround the femoral neck (grade 2) or with distended joint capsule (grade 3) on T2-weighted images were considered as having joint effusion, because a small amount of joint fluid in normal hips is a frequent finding on MR images (20).

Bone scintigraphy with technetium 99m methylene diphosphonate was performed within 5 days after the first MR imaging examination in cases that showed marrow edema surrounding a focal necrotic lesion.

Core biopsy was performed with a 9.5-mm trephine with fluoroscopic guidance. During this procedure, bone marrow pressure was measured by using the method described by Ficat et al (3) and Hungerford (4). A pressure of 30 mm Hg or greater was considered abnormal. Biopsy specimens were fixed in 10% neutral buffered formalin (Junsei Chemical, Tokyo, Japan) and were decalcified in a solution of formic acid (Amresco, Solon, Ohio) and sodium citrate (Junsei Chemical). Sections 4 µm thick were cut and stained with hematoxylin-eosin.

Postoperative care after core decompression consisted of walking with crutches with protected weight bearing for 6 weeks, followed by a gradual increase in weight bearing for another 6 weeks. Conservative treatment consisted of walking with crutches without weight bearing and intermittent use of analgesics until the pain subsided. Total hip arthroplasty was performed in cases with collapsed femoral heads and intractable pain.

The statistical significance of crude, unadjusted association between the presence of marrow edema and the occurrence of pain was tested by means of the Fisher exact test because of the possibility of small cell sizes in the contingency table. Logistic regression was applied to test the hypothesis of the association between marrow edema and pain after adjusting for potential confounders. The dependent variable for the logistic regression model was whether pain occurred at the first examination, and the independent variables were the occurrence of marrow edema at the same examination, age, and sex. Similarly, we performed multiple logistic regressions to test the hypothesis of the association between joint effusion and pain. We report two-sided P values, and a P value less than .05 was considered to indicate a statistically significant difference.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
At the first evaluation, 14 hips (38%) were symptomatic and 23 hips (62%) were asymptomatic. Seven (50%) of 14 symptomatic hips showed characteristic findings of marrow edema around focal osteonecrosis on MR images (Figs 1, 2), whereas only one (4%) of 23 asymptomatic hips showed edema (Fisher exact test, P < .01). Of seven hips that were moderately to severely painful (pain score of 1–3 [Table 1]), six (86%) were associated with surrounding edema. However, only two (7%) of 30 hips with mild or no pain were associated with edema (Fisher exact test, P < .001). Seven (88%) of eight hips that showed marrow edema around focal necrosis were associated with pain, whereas seven (24%) of 29 hips with focal osteonecrosis without marrow edema were symptomatic (Fisher exact test, P < .01) (Table 2).



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  		Figure 1a. Cases 1 and 9. (a-g) Images obtained in a 55-year-old man with a history of alcohol abuse. He had pain in the right hip for 6 weeks. Radiographs revealed ARCO stage III osteonecrosis of the right hip and stage II osteonecrosis of the left hip. (a) Coronal T1-weighted spin-echo image (500/15) reveals focal osteonecrosis (arrowheads) of both femoral heads. Diffuse low-signal-intensity abnormality (arrows) compatible with marrow edema is visible in the right proximal femur around focal osteonecrosis. (b) Coronal T2-weighted spin-echo image (1,900/80) shows the lesion (arrows) changed to one that is now isointense in some areas and of high signal intensity in other areas. Grade 3 joint effusion (arrowhead) is present in the right hip. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months reveals the disappearance of marrow edema. The hip pain improved even with the radiologic progression of collapse of the femoral head (arrowheads). (d) Coronal T1-weighted spin-echo image (500/20) shows diffuse marrow edema (arrows) around focal osteonecrosis (arrowheads) in the left hip. Nine months after the initial study, the patient had pain in the left hip.(e) Sagittal T2-weighted spin-echo images (1,900/80) show that the isointense (left) lesion (arrowheads) changes to one of high signal intensity (right). Grade 3 joint effusion (arrows) is present in the left hip. (f) Photomicrograph of the focal lesion in the left femoral head confirms osteonecrosis (arrowheads); the patient underwent total hip arthroplasty on the left side 1 week after the last MR imaging examination. (Hematoxylin-eosin stain; original magnification, x1.) (g) Photomicrograph of the proximal femur below the necrotic zone (hematoxylin-eosin stain; original magnification, x100). Although the trabecular bone (arrows) appears viable, the hematopoietic cells are depleted, fat cells are necrotic in the marrow (arrowheads), and the marrow space is filled with eosinophilic fibrinoid material, a finding compatible with marrow edema. Those histologic findings of the proximal femur below the necrotic zone are compatible with Ficat classification type 2 osteonecrosis (21).

 


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  		Figure 1b. Cases 1 and 9. (a-g) Images obtained in a 55-year-old man with a history of alcohol abuse. He had pain in the right hip for 6 weeks. Radiographs revealed ARCO stage III osteonecrosis of the right hip and stage II osteonecrosis of the left hip. (a) Coronal T1-weighted spin-echo image (500/15) reveals focal osteonecrosis (arrowheads) of both femoral heads. Diffuse low-signal-intensity abnormality (arrows) compatible with marrow edema is visible in the right proximal femur around focal osteonecrosis. (b) Coronal T2-weighted spin-echo image (1,900/80) shows the lesion (arrows) changed to one that is now isointense in some areas and of high signal intensity in other areas. Grade 3 joint effusion (arrowhead) is present in the right hip. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months reveals the disappearance of marrow edema. The hip pain improved even with the radiologic progression of collapse of the femoral head (arrowheads). (d) Coronal T1-weighted spin-echo image (500/20) shows diffuse marrow edema (arrows) around focal osteonecrosis (arrowheads) in the left hip. Nine months after the initial study, the patient had pain in the left hip.(e) Sagittal T2-weighted spin-echo images (1,900/80) show that the isointense (left) lesion (arrowheads) changes to one of high signal intensity (right). Grade 3 joint effusion (arrows) is present in the left hip. (f) Photomicrograph of the focal lesion in the left femoral head confirms osteonecrosis (arrowheads); the patient underwent total hip arthroplasty on the left side 1 week after the last MR imaging examination. (Hematoxylin-eosin stain; original magnification, x1.) (g) Photomicrograph of the proximal femur below the necrotic zone (hematoxylin-eosin stain; original magnification, x100). Although the trabecular bone (arrows) appears viable, the hematopoietic cells are depleted, fat cells are necrotic in the marrow (arrowheads), and the marrow space is filled with eosinophilic fibrinoid material, a finding compatible with marrow edema. Those histologic findings of the proximal femur below the necrotic zone are compatible with Ficat classification type 2 osteonecrosis (21).

 


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  		Figure 1c. Cases 1 and 9. (a-g) Images obtained in a 55-year-old man with a history of alcohol abuse. He had pain in the right hip for 6 weeks. Radiographs revealed ARCO stage III osteonecrosis of the right hip and stage II osteonecrosis of the left hip. (a) Coronal T1-weighted spin-echo image (500/15) reveals focal osteonecrosis (arrowheads) of both femoral heads. Diffuse low-signal-intensity abnormality (arrows) compatible with marrow edema is visible in the right proximal femur around focal osteonecrosis. (b) Coronal T2-weighted spin-echo image (1,900/80) shows the lesion (arrows) changed to one that is now isointense in some areas and of high signal intensity in other areas. Grade 3 joint effusion (arrowhead) is present in the right hip. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months reveals the disappearance of marrow edema. The hip pain improved even with the radiologic progression of collapse of the femoral head (arrowheads). (d) Coronal T1-weighted spin-echo image (500/20) shows diffuse marrow edema (arrows) around focal osteonecrosis (arrowheads) in the left hip. Nine months after the initial study, the patient had pain in the left hip.(e) Sagittal T2-weighted spin-echo images (1,900/80) show that the isointense (left) lesion (arrowheads) changes to one of high signal intensity (right). Grade 3 joint effusion (arrows) is present in the left hip. (f) Photomicrograph of the focal lesion in the left femoral head confirms osteonecrosis (arrowheads); the patient underwent total hip arthroplasty on the left side 1 week after the last MR imaging examination. (Hematoxylin-eosin stain; original magnification, x1.) (g) Photomicrograph of the proximal femur below the necrotic zone (hematoxylin-eosin stain; original magnification, x100). Although the trabecular bone (arrows) appears viable, the hematopoietic cells are depleted, fat cells are necrotic in the marrow (arrowheads), and the marrow space is filled with eosinophilic fibrinoid material, a finding compatible with marrow edema. Those histologic findings of the proximal femur below the necrotic zone are compatible with Ficat classification type 2 osteonecrosis (21).

 


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  		Figure 1d. Cases 1 and 9. (a-g) Images obtained in a 55-year-old man with a history of alcohol abuse. He had pain in the right hip for 6 weeks. Radiographs revealed ARCO stage III osteonecrosis of the right hip and stage II osteonecrosis of the left hip. (a) Coronal T1-weighted spin-echo image (500/15) reveals focal osteonecrosis (arrowheads) of both femoral heads. Diffuse low-signal-intensity abnormality (arrows) compatible with marrow edema is visible in the right proximal femur around focal osteonecrosis. (b) Coronal T2-weighted spin-echo image (1,900/80) shows the lesion (arrows) changed to one that is now isointense in some areas and of high signal intensity in other areas. Grade 3 joint effusion (arrowhead) is present in the right hip. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months reveals the disappearance of marrow edema. The hip pain improved even with the radiologic progression of collapse of the femoral head (arrowheads). (d) Coronal T1-weighted spin-echo image (500/20) shows diffuse marrow edema (arrows) around focal osteonecrosis (arrowheads) in the left hip. Nine months after the initial study, the patient had pain in the left hip.(e) Sagittal T2-weighted spin-echo images (1,900/80) show that the isointense (left) lesion (arrowheads) changes to one of high signal intensity (right). Grade 3 joint effusion (arrows) is present in the left hip. (f) Photomicrograph of the focal lesion in the left femoral head confirms osteonecrosis (arrowheads); the patient underwent total hip arthroplasty on the left side 1 week after the last MR imaging examination. (Hematoxylin-eosin stain; original magnification, x1.) (g) Photomicrograph of the proximal femur below the necrotic zone (hematoxylin-eosin stain; original magnification, x100). Although the trabecular bone (arrows) appears viable, the hematopoietic cells are depleted, fat cells are necrotic in the marrow (arrowheads), and the marrow space is filled with eosinophilic fibrinoid material, a finding compatible with marrow edema. Those histologic findings of the proximal femur below the necrotic zone are compatible with Ficat classification type 2 osteonecrosis (21).

 


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  		Figure 1e. Cases 1 and 9. (a-g) Images obtained in a 55-year-old man with a history of alcohol abuse. He had pain in the right hip for 6 weeks. Radiographs revealed ARCO stage III osteonecrosis of the right hip and stage II osteonecrosis of the left hip. (a) Coronal T1-weighted spin-echo image (500/15) reveals focal osteonecrosis (arrowheads) of both femoral heads. Diffuse low-signal-intensity abnormality (arrows) compatible with marrow edema is visible in the right proximal femur around focal osteonecrosis. (b) Coronal T2-weighted spin-echo image (1,900/80) shows the lesion (arrows) changed to one that is now isointense in some areas and of high signal intensity in other areas. Grade 3 joint effusion (arrowhead) is present in the right hip. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months reveals the disappearance of marrow edema. The hip pain improved even with the radiologic progression of collapse of the femoral head (arrowheads). (d) Coronal T1-weighted spin-echo image (500/20) shows diffuse marrow edema (arrows) around focal osteonecrosis (arrowheads) in the left hip. Nine months after the initial study, the patient had pain in the left hip.(e) Sagittal T2-weighted spin-echo images (1,900/80) show that the isointense (left) lesion (arrowheads) changes to one of high signal intensity (right). Grade 3 joint effusion (arrows) is present in the left hip. (f) Photomicrograph of the focal lesion in the left femoral head confirms osteonecrosis (arrowheads); the patient underwent total hip arthroplasty on the left side 1 week after the last MR imaging examination. (Hematoxylin-eosin stain; original magnification, x1.) (g) Photomicrograph of the proximal femur below the necrotic zone (hematoxylin-eosin stain; original magnification, x100). Although the trabecular bone (arrows) appears viable, the hematopoietic cells are depleted, fat cells are necrotic in the marrow (arrowheads), and the marrow space is filled with eosinophilic fibrinoid material, a finding compatible with marrow edema. Those histologic findings of the proximal femur below the necrotic zone are compatible with Ficat classification type 2 osteonecrosis (21).

 


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  		Figure 1f. Cases 1 and 9. (a-g) Images obtained in a 55-year-old man with a history of alcohol abuse. He had pain in the right hip for 6 weeks. Radiographs revealed ARCO stage III osteonecrosis of the right hip and stage II osteonecrosis of the left hip. (a) Coronal T1-weighted spin-echo image (500/15) reveals focal osteonecrosis (arrowheads) of both femoral heads. Diffuse low-signal-intensity abnormality (arrows) compatible with marrow edema is visible in the right proximal femur around focal osteonecrosis. (b) Coronal T2-weighted spin-echo image (1,900/80) shows the lesion (arrows) changed to one that is now isointense in some areas and of high signal intensity in other areas. Grade 3 joint effusion (arrowhead) is present in the right hip. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months reveals the disappearance of marrow edema. The hip pain improved even with the radiologic progression of collapse of the femoral head (arrowheads). (d) Coronal T1-weighted spin-echo image (500/20) shows diffuse marrow edema (arrows) around focal osteonecrosis (arrowheads) in the left hip. Nine months after the initial study, the patient had pain in the left hip.(e) Sagittal T2-weighted spin-echo images (1,900/80) show that the isointense (left) lesion (arrowheads) changes to one of high signal intensity (right). Grade 3 joint effusion (arrows) is present in the left hip. (f) Photomicrograph of the focal lesion in the left femoral head confirms osteonecrosis (arrowheads); the patient underwent total hip arthroplasty on the left side 1 week after the last MR imaging examination. (Hematoxylin-eosin stain; original magnification, x1.) (g) Photomicrograph of the proximal femur below the necrotic zone (hematoxylin-eosin stain; original magnification, x100). Although the trabecular bone (arrows) appears viable, the hematopoietic cells are depleted, fat cells are necrotic in the marrow (arrowheads), and the marrow space is filled with eosinophilic fibrinoid material, a finding compatible with marrow edema. Those histologic findings of the proximal femur below the necrotic zone are compatible with Ficat classification type 2 osteonecrosis (21).

 


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  		Figure 1g. Cases 1 and 9. (a-g) Images obtained in a 55-year-old man with a history of alcohol abuse. He had pain in the right hip for 6 weeks. Radiographs revealed ARCO stage III osteonecrosis of the right hip and stage II osteonecrosis of the left hip. (a) Coronal T1-weighted spin-echo image (500/15) reveals focal osteonecrosis (arrowheads) of both femoral heads. Diffuse low-signal-intensity abnormality (arrows) compatible with marrow edema is visible in the right proximal femur around focal osteonecrosis. (b) Coronal T2-weighted spin-echo image (1,900/80) shows the lesion (arrows) changed to one that is now isointense in some areas and of high signal intensity in other areas. Grade 3 joint effusion (arrowhead) is present in the right hip. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months reveals the disappearance of marrow edema. The hip pain improved even with the radiologic progression of collapse of the femoral head (arrowheads). (d) Coronal T1-weighted spin-echo image (500/20) shows diffuse marrow edema (arrows) around focal osteonecrosis (arrowheads) in the left hip. Nine months after the initial study, the patient had pain in the left hip.(e) Sagittal T2-weighted spin-echo images (1,900/80) show that the isointense (left) lesion (arrowheads) changes to one of high signal intensity (right). Grade 3 joint effusion (arrows) is present in the left hip. (f) Photomicrograph of the focal lesion in the left femoral head confirms osteonecrosis (arrowheads); the patient underwent total hip arthroplasty on the left side 1 week after the last MR imaging examination. (Hematoxylin-eosin stain; original magnification, x1.) (g) Photomicrograph of the proximal femur below the necrotic zone (hematoxylin-eosin stain; original magnification, x100). Although the trabecular bone (arrows) appears viable, the hematopoietic cells are depleted, fat cells are necrotic in the marrow (arrowheads), and the marrow space is filled with eosinophilic fibrinoid material, a finding compatible with marrow edema. Those histologic findings of the proximal femur below the necrotic zone are compatible with Ficat classification type 2 osteonecrosis (21).

 


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  		Figure 2a. Case 2. (a-c) Images obtained in a 38-year-old man who had a 1-week history of pain in the right groin. Conventional radiographs (not shown) revealed ARCO stage II osteonecrosis of the right hip. (a) Coronal T1-weighted spin-echo image (500/20) shows small osteonecrosis of the apex of the femoral head (arrowheads). Marked loss of signal intensity, which is compatible with marrow edema, in the femoral head and neck (arrows) is demonstrated beyond the necrotic lesion. (b) Scintigram obtained in the anterior view shows increased radionuclide uptake in the proximal femur. The area of osteonecrosis is small, and decreased uptake in the necrotic zone is obscured by intense radionuclide uptake (arrowheads). The uptake in the area of pubic rami appears exaggerated owing to the overlap of radionuclide activity in the urinary bladder and the rami. (c) Coronal T1-weighted spin-echo image (500/20) demonstrates complete resolution of marrow edema at follow-up examination at 3 months; the patient was asymptomatic. The patient underwent core decompression in the right hip 3 days after the first MR imaging examination. The core tract (arrowheads) is seen as an area of low signal intensity. The extent of necrosis is small, and the femoral head did not collapse until the latest follow-up.

 


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  		Figure 2b. Case 2. (a-c) Images obtained in a 38-year-old man who had a 1-week history of pain in the right groin. Conventional radiographs (not shown) revealed ARCO stage II osteonecrosis of the right hip. (a) Coronal T1-weighted spin-echo image (500/20) shows small osteonecrosis of the apex of the femoral head (arrowheads). Marked loss of signal intensity, which is compatible with marrow edema, in the femoral head and neck (arrows) is demonstrated beyond the necrotic lesion. (b) Scintigram obtained in the anterior view shows increased radionuclide uptake in the proximal femur. The area of osteonecrosis is small, and decreased uptake in the necrotic zone is obscured by intense radionuclide uptake (arrowheads). The uptake in the area of pubic rami appears exaggerated owing to the overlap of radionuclide activity in the urinary bladder and the rami. (c) Coronal T1-weighted spin-echo image (500/20) demonstrates complete resolution of marrow edema at follow-up examination at 3 months; the patient was asymptomatic. The patient underwent core decompression in the right hip 3 days after the first MR imaging examination. The core tract (arrowheads) is seen as an area of low signal intensity. The extent of necrosis is small, and the femoral head did not collapse until the latest follow-up.

 


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  		Figure 2c. Case 2. (a-c) Images obtained in a 38-year-old man who had a 1-week history of pain in the right groin. Conventional radiographs (not shown) revealed ARCO stage II osteonecrosis of the right hip. (a) Coronal T1-weighted spin-echo image (500/20) shows small osteonecrosis of the apex of the femoral head (arrowheads). Marked loss of signal intensity, which is compatible with marrow edema, in the femoral head and neck (arrows) is demonstrated beyond the necrotic lesion. (b) Scintigram obtained in the anterior view shows increased radionuclide uptake in the proximal femur. The area of osteonecrosis is small, and decreased uptake in the necrotic zone is obscured by intense radionuclide uptake (arrowheads). The uptake in the area of pubic rami appears exaggerated owing to the overlap of radionuclide activity in the urinary bladder and the rami. (c) Coronal T1-weighted spin-echo image (500/20) demonstrates complete resolution of marrow edema at follow-up examination at 3 months; the patient was asymptomatic. The patient underwent core decompression in the right hip 3 days after the first MR imaging examination. The core tract (arrowheads) is seen as an area of low signal intensity. The extent of necrosis is small, and the femoral head did not collapse until the latest follow-up.

 

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  		TABLE 2. Associated Marrow Edema and Pain in 37 Hips with Osteonecrosis
 
All eight osteonecrotic hips with marrow edema around focal necrosis showed concomitant joint effusion on MR images. Three showed grade 2 joint effusion, and five showed grade 3 effusion (20) (Fig 1b). Two osteonecrotic hips that were not associated with edema also showed grade 2 joint effusion; one was symptomless, and the other had mild symptoms. Eight (80%) of 10 hips with joint effusion were symptomatic. The presence or absence of symptoms seemed to correlate well with joint effusion (Fisher exact test, P < .01) (Table 3). It should be noted, however, that eight (80%) of 10 hips with joint effusion also had edema. In such combined cases, the amount of effusion was relatively large, and the pain was moderate to severe. In the two cases of effusion without edema, the amount of fluid was relatively small, and the symptoms were mild or absent.


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  		TABLE 3. Joint Effusion, Pain, and Marrow Edema in 37 Hips with Osteonecrosis
 
At scintigraphy, all eight hips that were associated with marrow edema around focal necrosis exhibited intense radionuclide uptake in the proximal femur, which corresponded to the extent of edema visible on MR images (Fig 2b).

Of seven symptomatic femoral heads with associated edema at the first evaluation, core decompression with bone marrow pressure measurement was performed in four randomly selected femoral heads, and the remaining three were managed conservatively. The bone marrow pressure of four hips was substantially elevated (36–60 mm Hg; mean, 49 mm Hg). The symptoms persisted for months and improved gradually in cases in which surgery was not performed, whereas pain was relieved within 1 week after surgery in three of four cases in which core decompression was performed. The symptom improved even with the evidence of radiologic progression to a further stage, although six hips collapsed and became painful again at later follow-up. The second MR imaging examination demonstrated a complete resolution of marrow edema in six cases (Figs 1, 2). Two cases (case 4, core decompression; case 7, conservative management) revealed decreased but persistent edema, which disappeared completely at the third MR imaging examination. Those two hips were included among the three hips in which pain persisted for 4–5 months (Table 4).


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  		TABLE 4. Profile of Eight Cases with Early Stage Osteonecrosis with Marrow Edema at the First MR Imaging Examination
 
According to the logistic regression adjusting for age and sex, the existence of marrow edema was strongly associated with the occurrence of pain assessed at the first examination (P = .007). The odds ratio was 80 (95% CI: 3, 1,914). Age was inversely associated with the occurrence of pain (Table 5).


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  		TABLE 5. Logistic Regression of Pain on the Occurrence of Marrow Edema after Adjustment for Age and Sex
 
Because hips with edema also had effusion, we performed another logistic regression analysis and used effusion in place of edema. The odds ratio for effusion was 17 (95% CI: 2, 126) (Table 6). When both effusion and edema were considered as independent variables, effusion was not significantly associated with pain (Table 7). Because all eight hips with edema also had effusion (Table 3), it was statistically impossible to estimate separately the effect of effusion from that of edema on pain.


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  		TABLE 6. Logistic Regression of Pain on the Occurrence of Joint Effusion after Adjustment for Age and Sex
 

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  		TABLE 7. Logistic Regression of Pain on the Occurrence of Marrow Edema and Joint Effusion after Adjustment for Age and Sex
 
Four (cases 10, 11, and 12, core decompression; case 9, conservative management) of 29 osteonecrotic hips that had not been associated with edema at the first MR imaging examination showed edema with concomitant joint effusion at follow-up MR imaging. Three (75%) of these were moderately or severely painful (Table 8, Fig 3).


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  		TABLE 8. Profile of Four Cases with Marrow Edema on Follow-up MR Images
 


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  		Figure 3a. Case 10. (a-e) Images obtained in a 37-year-old man who had received high doses of prednisolone owing to nephrotic syndrome. He was referred owing to pain in the left hip. The right hip was asymptomatic. Conventional radiographs (not shown) revealed ARCO stage IV osteonecrosis of the left hip and normal findings for the right hip. (a) Coronal T1-weighted spin-echo image (500/15) shows focal osteonecrosis (arrowheads) of the right femoral head (ARCO stage I osteonecrosis). Total hip arthroplasty was performed in the left hip, and core decompression was performed in the right hip after the first evaluation. Histologic findings were compatible with osteonecrosis in both specimens. (b) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months shows the core tract (arrowheads) as an area of low signal intensity. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the third MR imaging examination; 6 months after surgery, the patient had sudden pain in the right hip. This MR image was obtained 3 days after the onset of pain and reveals low signal intensity (arrowheads) in the femoral head and neck and proximal femur, a finding compatible with marrow edema. (d) Scintigram obtained in the anterior view shows increased radionuclide uptake in the right proximal femur (arrowheads). (e) Coronal T1-weighted spin-echo image (500/20) obtained at the fourth follow-up examination shows radiologic evidence of mild femoral head collapse (arrowheads). The pain in the right hip improved, however, and the marrow edema resolved.

 


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  		Figure 3b. Case 10. (a-e) Images obtained in a 37-year-old man who had received high doses of prednisolone owing to nephrotic syndrome. He was referred owing to pain in the left hip. The right hip was asymptomatic. Conventional radiographs (not shown) revealed ARCO stage IV osteonecrosis of the left hip and normal findings for the right hip. (a) Coronal T1-weighted spin-echo image (500/15) shows focal osteonecrosis (arrowheads) of the right femoral head (ARCO stage I osteonecrosis). Total hip arthroplasty was performed in the left hip, and core decompression was performed in the right hip after the first evaluation. Histologic findings were compatible with osteonecrosis in both specimens. (b) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months shows the core tract (arrowheads) as an area of low signal intensity. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the third MR imaging examination; 6 months after surgery, the patient had sudden pain in the right hip. This MR image was obtained 3 days after the onset of pain and reveals low signal intensity (arrowheads) in the femoral head and neck and proximal femur, a finding compatible with marrow edema. (d) Scintigram obtained in the anterior view shows increased radionuclide uptake in the right proximal femur (arrowheads). (e) Coronal T1-weighted spin-echo image (500/20) obtained at the fourth follow-up examination shows radiologic evidence of mild femoral head collapse (arrowheads). The pain in the right hip improved, however, and the marrow edema resolved.

 


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  		Figure 3c. Case 10. (a-e) Images obtained in a 37-year-old man who had received high doses of prednisolone owing to nephrotic syndrome. He was referred owing to pain in the left hip. The right hip was asymptomatic. Conventional radiographs (not shown) revealed ARCO stage IV osteonecrosis of the left hip and normal findings for the right hip. (a) Coronal T1-weighted spin-echo image (500/15) shows focal osteonecrosis (arrowheads) of the right femoral head (ARCO stage I osteonecrosis). Total hip arthroplasty was performed in the left hip, and core decompression was performed in the right hip after the first evaluation. Histologic findings were compatible with osteonecrosis in both specimens. (b) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months shows the core tract (arrowheads) as an area of low signal intensity. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the third MR imaging examination; 6 months after surgery, the patient had sudden pain in the right hip. This MR image was obtained 3 days after the onset of pain and reveals low signal intensity (arrowheads) in the femoral head and neck and proximal femur, a finding compatible with marrow edema. (d) Scintigram obtained in the anterior view shows increased radionuclide uptake in the right proximal femur (arrowheads). (e) Coronal T1-weighted spin-echo image (500/20) obtained at the fourth follow-up examination shows radiologic evidence of mild femoral head collapse (arrowheads). The pain in the right hip improved, however, and the marrow edema resolved.

 


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  		Figure 3d. Case 10. (a-e) Images obtained in a 37-year-old man who had received high doses of prednisolone owing to nephrotic syndrome. He was referred owing to pain in the left hip. The right hip was asymptomatic. Conventional radiographs (not shown) revealed ARCO stage IV osteonecrosis of the left hip and normal findings for the right hip. (a) Coronal T1-weighted spin-echo image (500/15) shows focal osteonecrosis (arrowheads) of the right femoral head (ARCO stage I osteonecrosis). Total hip arthroplasty was performed in the left hip, and core decompression was performed in the right hip after the first evaluation. Histologic findings were compatible with osteonecrosis in both specimens. (b) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months shows the core tract (arrowheads) as an area of low signal intensity. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the third MR imaging examination; 6 months after surgery, the patient had sudden pain in the right hip. This MR image was obtained 3 days after the onset of pain and reveals low signal intensity (arrowheads) in the femoral head and neck and proximal femur, a finding compatible with marrow edema. (d) Scintigram obtained in the anterior view shows increased radionuclide uptake in the right proximal femur (arrowheads). (e) Coronal T1-weighted spin-echo image (500/20) obtained at the fourth follow-up examination shows radiologic evidence of mild femoral head collapse (arrowheads). The pain in the right hip improved, however, and the marrow edema resolved.

 


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  		Figure 3e. Case 10. (a-e) Images obtained in a 37-year-old man who had received high doses of prednisolone owing to nephrotic syndrome. He was referred owing to pain in the left hip. The right hip was asymptomatic. Conventional radiographs (not shown) revealed ARCO stage IV osteonecrosis of the left hip and normal findings for the right hip. (a) Coronal T1-weighted spin-echo image (500/15) shows focal osteonecrosis (arrowheads) of the right femoral head (ARCO stage I osteonecrosis). Total hip arthroplasty was performed in the left hip, and core decompression was performed in the right hip after the first evaluation. Histologic findings were compatible with osteonecrosis in both specimens. (b) Coronal T1-weighted spin-echo image (500/20) obtained at the second MR imaging examination at 3 months shows the core tract (arrowheads) as an area of low signal intensity. (c) Coronal T1-weighted spin-echo image (500/20) obtained at the third MR imaging examination; 6 months after surgery, the patient had sudden pain in the right hip. This MR image was obtained 3 days after the onset of pain and reveals low signal intensity (arrowheads) in the femoral head and neck and proximal femur, a finding compatible with marrow edema. (d) Scintigram obtained in the anterior view shows increased radionuclide uptake in the right proximal femur (arrowheads). (e) Coronal T1-weighted spin-echo image (500/20) obtained at the fourth follow-up examination shows radiologic evidence of mild femoral head collapse (arrowheads). The pain in the right hip improved, however, and the marrow edema resolved.

 
In six cases, the biopsy specimens (four core biopsy specimens, cases 2, 3, 4, and 6; two resected femoral heads, cases 9 and 11) were obtained within 7 days of the MR imaging examination that had depicted the presence of edema. Histopathologic examination showed definite findings of focal osteonecrosis in the subchondral necrotic zone in all six cases. In the marrow space of the proximal femur surrounding focal osteonecrosis, there was a collection of eosinophilic plasmalike fluid, a finding compatible with marrow edema. Although hematopoietic marrow is macroscopically identifiable in the proximal femoral metaphysis during adult life (22), it was depleted, and fat cells were necrotic in that area. In some areas, fibrosis and dilated vessels were observed between necrotic fat cells. Although some lacunae were empty, the trabecular bone appeared viable (Fig 1g). Those histologic findings of the proximal femur around focal osteonecrosis were compatible with Ficat classification type 2 osteonecrosis (21).


   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
The results of this study show that marrow edema of the proximal femur is frequently associated with focal osteonecrosis of the femoral head and is strongly associated with pain even in the absence of collapse.

In a previous MR imaging study of marrow infarct in 11 patients with sickle cell anemia, Rao et al (14) showed a strong correlation between marrow edema and pain. In 12 (86%) of 14 painful joints, areas of decreased signal intensity were seen on T1-weighted images. These lesions were of high signal intensity on T2-weighted images, which suggests concomitant marrow edema around the infarcted area.

The results of the present study suggest that the presence of edema signal intensity in the proximal femoral metaphysis in association with focal subchondral signal intensity abnormality is correlated with symptomatic osteonecrosis. This may have certain treatment implications. Although the associated pain is severe, it is often a transient symptom that improves spontaneously within months and that corresponds to the resolution of edema, even in cases with radiologic evidence of collapse (Fig 1). Thus, it is advisable to treat disease in these patients with measures other than total hip arthroplasty. Most patients with osteonecrosis of the femoral head are young and active (23). For such patients, it is important to delay total hip arthroplasty as long as possible (24,25). When the extent of necrosis is small, moreover, the femoral head does not collapse, and the joint can be preserved (Fig 2) (5,16,26–33).

Joint effusion of the hip also has been associated with pain (20,34,35). In this study, all the cases of surrounding edema were associated with joint effusion. In two cases, mild joint effusion was present without evidence of edema. Joint effusion concomitant with edema is usually moderate to large and is associated with moderate to severe pain, whereas effusion without edema is associated with mild or no symptoms. Joint effusion seems to play a relatively minor role in pain compared with marrow edema in the early stage. An intraosseous fracture, which might not be evident at conventional radiography, might play a role in pain (36). In that case, the collapse should progress after the onset of pain, and the pain should be aggravated with the progression of collapse. In this study, however, several cases did not show collapse after edema for a considerable period, and pain was alleviated with resolution of bone marrow edema even with radiologic evidence of collapse. Joint effusion and intraosseous fracture, which are prevalent findings in more advanced stages, would act as major factors, with subsequent collapse, joint incongruity, and degenerative arthritis at a later stage.

This study showed an age-related decrease in pain in the patients with osteonecrosis with combined edema. The finding is compatible with previous findings that the pain threshold is higher among older patients (37,38).

The pathophysiology of transient marrow edema around focal necrosis and its role in the pathogenesis of osteonecrosis is still not well understood. One possible cause of edema is occult fracture in the necrotic zone, which progresses to collapse later (39). In such a case, the collapse should occur in due time after the edema. In this study, there was no significant difference between the collapse rate in the hips associated with edema (10 of 12) and that of the remaining hips, which were not associated with edema (19 of 25). There was a mean 9.4-month lag between the appearance of edema and the time of collapse, and two cases did not collapse after edema until the end of the study. The surrounding edema in intraosseous microfracture is caused by marrow vessel injury (36,40,41). However, the fracture in an osteonecrotic femoral head occurs through the necrotic zone in which there is no marrow vessel.

Another possibility, which we favor, is that the edema is a secondary reaction to tissue ischemia (42). Ischemic infarcts of visceral organs and brain have been associated with a surrounding edema in the acute or subacute stage of the disease process (43–45). For instance, during an acute cerebral infarct, surrounding edema with increased intracranial pressure is observed for several days after the ischemic attack and is resolved later (46). Scintigraphy in eight cases in this study, which was performed during the presence of surrounding edema, exhibited increased radionuclide uptake in the proximal femur, which indicates increased blood flow, increased capillary permeability, or both rather than devascularization. Although bone marrow pressure was elevated substantially, blood flow was not decreased but rather increased as shown at scintigraphy. We think the edema itself is not the cause of ischemia, and we prefer the explanation that localized edema is a secondary phenomenon that follows ischemic attack and surrounds the necrotic region (42).

Histologic examination of the edematous region of the proximal femur showed hematopoietic and fat cell necrosis in the marrow (Fig 1g). According to the histologic criteria of Ficat (21), this finding is compatible with that of osteonecrosis, but these histologic criteria are open to question (47–50). If marrow necrosis had been true osteonecrosis or a precursor of osteonecrosis including osteocytic death, the observed area of necrotic zone should have expanded to include the edematous zone with the progression of the disease. However, the extent of the necrotic zone remained constant on follow-up MR images. Even though the earliest histologic changes of osteonecrosis might involve the marrow first (21,42,51,52), the marrow necrosis seen in the edematous region does not progress to osteonecrosis.

The results of this study suggest that core decompression relieved pain promptly, possibly through the mechanism of ameliorating marrow edema and intraosseous hypertension (4,10). The average duration of clinical symptoms was reduced by that procedure. However, pain also lessened spontaneously in cases that were managed conservatively; and in two cases in which core decompression was performed, marrow edema appeared later. Authors of recent studies (15,28,53–56) have questioned the effectiveness of the procedure because of the high rate of failure. We thus think core decompression should be used cautiously in cases resistive to conservative management.


   Acknowledgments
 
The authors thank John Paul Jones, Jr, MD, for his invaluable suggestions and critical review of the manuscript and Ho Kim, PhD, for his statistical advice. We also thank Dianne Ashman, BA, for her editorial and secretarial help in the preparation of the manuscript.


   Footnotes
 
Abbreviation: ARCO = Association Research Circulation Osseous

Author contributions: Guarantor of integrity of entire study, K.H.K.; study concepts and design, K.H.K., I.O.A., R.K., Y.S.K.; definition of intellectual content, S.H.C.; literature research, I.O.A.; clinical studies, I.O.A.; experimental studies, S.T.J.; data acquisition, J.B.N.; data analysis, K.H.K., I.O.A., S.T.J., H.R.S.; statistical analysis, R.K.; manuscript preparation and editing, K.H.K.; manuscript review, H.R.S., S.H.C.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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