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1 Department of Radiology, Tri-Service General Hospital, National Defense
Medical Center, 325 Cheng-Kung Rd., Section 2, Neihu, Taipei 114, Taiwan,
Republic of China.
2 Department of Radiology, School of Medicine, Taipei Medical University, 250
Wu-Hsing St., Taipei 110, Taiwan, Republic of China.
3 Department of Radiology, Taipei Medical University-Municipal Wan Fang
Hospital, 111 Hsing-Long Rd., Section 3, Taipei 116, Taiwan, Republic of
China.
4 Department of Mathematics, Tamkang University, 151 Ying-Chuan Rd., Tamsui,
Taipei County 251, Taiwan, Republic of China.
5 Department of Radiology, Taipei Veterans General Hospital, 201 Shih-Pai Rd.,
Section 2, Taipei 112, Taiwan, Republic of China.
6 Department of Radiology, Ohio State University Medical Center, S-255 Rhodes
Hall, 450 W. 10th Ave., Columbus, OH 43210.
Received September 10, 2002;
accepted after revision February 27, 2003.
Address correspondence to W. P. Chan.
Abstract
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MATERIALS AND METHODS. There were 71 patients with osteonecrosis of the femoral head based on characteristic radiographic and MR imaging findings. All patients had surgical confirmation of the disease. Both hips were affected with osteonecrosis in 39 patients, whereas only one hip was involved in 31 patients. The last patient underwent an arthroplasty of one hip during the study and had only one hip imaged. We evaluated a total of 110 hips in this study, of which 98 were painful. We staged osteonecrosis of the femoral head, using the classification of Steinberg et al. The 31 unaffected hips served as controls. Bone marrow edema and joint fluid were evaluated on MR images. Bone marrow edema was defined as an ill-defined area of low signal intensity on T1-weighted images with corresponding high signal intensity on T2-weighted or inversion recovery images localizing to the femoral head, neck, and intertrochanteric region. The amount of joint fluid was graded from 0 to 3.
RESULTS. The peak of bone marrow edema occurred in stage III disease (72%); its odds ratio was seven times greater than that for stage I osteonecrotic hips. Effusions of a grade greater than or equal to 2 were seen most often in stage III disease (92%), compared with 10% in the control hips. With an effusion, bone marrow edema was 12.6 times greater when the hip was painful than when it was not.
CONCLUSION. Both bone marrow edema and joint effusions existed with a peak occurrence in stage III disease. Bone marrow edema seems to have a stronger association with pain than does joint effusion in osteonecrosis of the femoral head.
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We attempted to determine the occurrence of bone marrow edema and joint effusion and its relationship to pain in patients with osteonecrosis of the femoral head on the basis of MR imaging.
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No patients had a history of trauma to either hip. Potential risk factors for osteonecrosis of the femoral head included alcoholic consumption (n = 52) and steroid therapy (n = 11). The remaining eight patients denied any potential risk factors for osteonecrosis of the femoral head. Medical records revealed that 98 hips with osteonecrosis of the femoral head were painful at the time of imaging and 12 were free of pain [6]. Of the 31 control hips, only one was painful at the time of imaging. All patients had surgical confirmation of the disease. Patients with early stages received core decompression; those with advanced stages underwent hip arthroplasty.
All MR imaging examinations were performed on a 1.5-T magnet (Vista, Picker, Cleveland, OH). Imaging was performed using a body coil with the patient in a supine position. We obtained the following sequences: coronal spin-echo T1-weighted (TR range/TE range, 450–650/16–20), intermediate-weighted (1500–2200/20–40), T2-weighted (1500–2200/80–90), and inversion recovery (2500–3000/35–40; inversion time, 100–150) sequences of both hips. Subsequent intermediate-weighted and T2-weighted images also were obtained in the sagittal plane using the same parameters as those in the coronal plane. The field of view ranged from 32 to 38 cm. Slice thickness was 4–5 mm, with an interslice gap of 0.5 mm. The matrices varied from 192 x 256 to 256 x 256, depending on the size of the patient.
Interpretation of Images
Characteristic MR imaging findings established the diagnosis of
osteonecrosis of the femoral head
[7–10].
The inclusion criteria were crescentic areas
(Fig. 1) of low signal
intensity in the weight-bearing portion of the femoral head, a bandlike
pattern (Fig. 2), a ringlike
lesion (Fig. 3A,
3B,
3C) with homogeneous or
heterogeneous signal intensity of the central area, a homogeneous area of
decreased signal intensity with a dark band
(Fig. 4), and collapse of the
femoral head (Fig. 3A,
3B,
3C). Bone marrow edema was
defined as an ill-defined area of low signal intensity on T1-weighted images,
with corresponding high signal intensity on T2-weighted or inversion recovery
images localizing to the femoral head, neck, and intertrochanteric region
[1,
3,
4,
11–14]
(Figs. 3A,
3B,
3C and
4). A well-demarcated arcuate
zone of high signal intensity on T2-weighted images surrounding the necrotic
area of the femoral head was considered granulation tissue
[11,
14,
15]. The joint fluid was
graded on the basis of the coronal images as follows: 0, no fluid; 1, minimal
fluid; 2, enough fluid to surround the femoral neck
(Fig. 4); and 3, distention of
capsule recesses [2]
(Fig. 1).
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All patients had undergone conventional hip anteroposterior and frogleg lateral radiographs preceding the MR imaging examination. No more than 1 week separated the radiographic examination from the MR study in any of the patients. We noted on MR images obtained previously that bone marrow edema might obscure early subchondral crescent. Recently, Stevens et al. [16] have reported a similar observation. The necrotic bone marrow, cellular debris, granulation tissue, and bone sclerosis can all result in low signal intensity on T1- and T2-weighted images, potentially obscuring subchondral fractures [16]. Alternatively, we staged each affected hip according to classification by Steinberg et al. [17] as follows: stage I, normal findings on radiographs; stage II, cystic or 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.
All images were interpreted together by consensus by two radiologists experienced in skeletal MR imaging. The reviewers knew the aforementioned diagnostic parameters for evaluation of osteonecrosis of the femoral head. All sets of radiographs were interpreted without awareness of the MR imaging and clinical findings of each patient. The names of patients left on the films were covered during interpretation. One week later, the same reviewers interpreted each MR imaging examination unaware of the radiographic and clinical findings of each patient.
Statistical Analysis
We used logistic regression to assess the association between the
occurrence of bone marrow edema and the presence of pain. Because the results
acquired from the hips of patients with bilateral disease were likely not to
be independent, we used a statistical method of generalized estimating
equations to fit the logistic regression and account for the subject-dependent
data [18]. The same
generalized estimating equations method was used to determine the association
between the occurrence of bone marrow edema and various stages of
osteonecrosis of the femoral head and bone marrow edema and joint effusion.
This entire model-fitting work was performed on a PC using the PROC GENMOD
procedure in the SAS/STAT V8.1 system (SAS Institute, Cary, NC). We used
StatXact 4.0 (Cytel Software, Cambridge, MA) for the Pearson's correlation
coefficient and chi-square tests. A p value of less than 0.05
indicated a statistically significant difference.
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With respect to the risk (odds) of the occurrence of bone marrow edema in various stages, there was an increasing trend from stage I to stage III, with the peak occurring in stage III disease. The risk decreased from stage III to stage V disease. The odds ratio of the occurrence of bone marrow edema for stage III disease was seven times greater than that for stage I disease.
Ninety-eight (89%) of 110 hips with osteonecrosis of the femoral head were painful, compared with one (3%) of 31 control hips. Pain occurred more in later stages of the disease. Also, we noted that 52 (98%) of 53 osteonecrotic hips with bone marrow edema were painful, compared with 46 (81%) of 57 osteonecrotic hips without bone marrow edema. The presence of bone marrow edema reflected a strong association with the clinical presentation of pain (p < 0.0001), particularly for patients with an earlier stage of osteonecrosis of the femoral head. Patients with bone marrow edema were 25.2 times more likely to experience pain than patients without bone marrow edema.
Similarly, the odds ratio with respect to pain for osteonecrosis of the femoral head with a joint effusion of a grade greater than or equal to 2 was 19.2 times greater than that in hips with a joint fluid grade of less than 2 (p < 0.0001). By using multiple logistic regressions adjusting for the effect of a joint effusion, we noted that the presence of bone marrow edema was still significantly associated with the presence of pain (p = 0.0068) and that the odds ratio for a painful hip was 12.6 times greater with bone marrow edema than without.
Forty-eight osteonecrotic hips with bone marrow edema had either a grade 2
(16/53, 30%) or grade 3 (32/53, 60%) effusion. There was a strong association
between the presence of bone marrow edema and a joint effusion (grade, 
2), independent of osteonecrosis of the femoral head (p < 0.0001).
The odds ratio with respect to a joint effusion was 15.9 times greater with
bone marrow edema than without bone marrow edema. When we compared joint
effusion to the disease stage, ignoring the presence of bone marrow edema, the
later stages of osteonecrosis of the femoral head were strongly associated
with a significant joint effusion (grade, 2) (p < 0.003).
When we adjusted for the effects of bone marrow edema, we observed that the
presence of osteonecrosis of the femoral head alone was still significantly
associated with a joint effusion.
The strongest association of bone marrow edema with osteonecrosis of the femoral head occurred in stage III disease with joint effusion, with an odds ratio of 15.5 times when compared with that in earlier stages of the disease. A grade 2 or grade 3 effusion was also seen most often in stage III disease (23/25, 92%), compared with stages I (9/17, 53%), II (17/26, 65%), IV (23/33, 70%), and V (7/9, 78%). The control hips had a grade 2 joint effusion in three (10%) of 31 hips.
Twelve patients with bilateral hips having osteonecrosis of the femoral head were asymptomatic in one hip. The MR images in the asymptomatic hips revealed a subchondral bandlike pattern in 10 hips and a ringlike lesion in two hips. Ten hips had a grade 1 joint effusion and two hips had a grade 2 effusion.
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Some investigators have shown that hips that present with diffuse bone marrow edema in the femoral neck and intertrochanteric region may subsequently develop focal lesions in the femoral head consistent with osteonecrosis [12]. We did not observe this phenomenon in our study. All hips exhibited focal subchondral lesions characteristic of osteonecrosis of the femoral head independent of whether it was associated with bone marrow edema.
In our study, the occurrence of bone marrow edema was 48% in hips with osteonecrosis of the femoral head. Our figure is similar to those previously reported by other investigators, which have ranged from 30% to 50% [1, 3, 4]. Kim et al. [3] reported that bone marrow edema was most often found in hips with stage III disease (88%) and that a diffuse bone edema pattern characteristic of transient osteoporosis was not seen in earlier stages of osteonecrosis of the femoral head. Iida et al. [4] observed that bone marrow edema correlated highly with hips that progressed to collapse of the femoral head. Our results corroborate that the peak occurrence of bone marrow edema is in stage III disease (72%), which was seven times (in odds ratio) more common than that in hips with stage I disease. Also, the odds ratio for pain in hips having osteonecrosis of the femoral head was 13 times greater when there was bone marrow edema than when there was no edema.
The mechanism that produces bone marrow edema remains unknown. Some investigators have speculated that bone marrow edema could be a secondary reaction to subchondral fractures arising from mechanical stress [1, 3, 4]. Histologic analysis by some investigators of the medullary space in involved hips has shown eosinophilic plasma-like fluid surrounding the necrotic fat cells, and this could contribute to bone marrow edema [1]. In other cases, bone marrow edema correlated with areas of fibrosis, with dilated vessels and interstitial edema between the adipocytes [1, 14]. Ficat and Arlet [6] postulated that blockage of venous drainage of the femoral veins resulted in intramedullary stasis in the intertrochanteric areas. In their experiment, specimens obtained from the proximal femur revealed most marrow changes characterized by intrasinusoidal plasmostasis, interstitial edema, hemorrhage, and fibrosis in osteonecrotic hips.
Koo et al. [1] reported that the pain in all eight hips of their patients subsided with ameliorating of bone marrow edema and intramedullary hypertension after core decompression. Our data with a larger patient group further suggested that bone marrow edema might be a phenomenon indicating the latest timing for core decompression in patients with early-stage osteonecrosis of the femoral head, and this procedure might delay hip arthroplasty, especially for young patients.
A grade 2 or grade 3 effusion occurred in 72% of hips with osteonecrosis of the femoral head, compared with 10% of control hips. Our data indicate that the largest prevalence of joint effusion occurred in hips with stage III disease (92%). This finding is similar to that of a prior study by Mitchell et al. [2], which reported that 58% of hips with osteonecrosis of the femoral head had grade 2 or grade 3 effusions, in contrast to 5% of normal hips.
Koo et al. [1] reported that a joint effusion was not significantly associated with pain when both bone marrow edema and effusion were considered as independent variables in painful hips with osteonecrosis of the femoral head. Our results indicated that the occurrence of bone marrow edema was 16 times in odds ratio more likely to occur when there was a joint effusion in the hip affected by osteonecrosis of the femoral head.
Osteonecrosis of the femoral head does not always produce pain. We evaluated 12 asymptomatic hips with stage I and II disease. The MR images revealed either a bandlike or ringlike pattern in the subchondral marrow of the femoral head. Other investigators have proposed that a bandlike pattern, not bone marrow edema or joint effusion, is the initial MR imaging finding of osteonecrosis of the femoral head [3–5, 20, 21]. Our data are consistent with this proposal. In patients who have been undergoing therapy with corticosteroid medication, a bandlike pattern has been observed beginning at a mean of 14 weeks after the onset of steroid therapy [4]. In another study, the incidence of clinically occult osteonecrosis of the femoral head was 6% in patients who had undergone a renal transplantation and were treated with corticosteroids [5].
Rafii et al. [22] reported three patients with severe hip pain having insufficiency fractures of the femoral head and the presence of bone marrow edema. Two of the fractures coexisted with insufficiency fractures in the acetabular dome. The patients were osteoporotic and elderly with no predisposing factors for osteonecrosis of the femoral head. Recognition of these combined factors can avoid an erroneous diagnosis of osteonecrosis of the femoral head.
There were several limitations to our study. The clinical evaluation focused only on the presence of pain and risk factors for osteonecrosis of the femoral head. We could not adequately determine a pain-scoring system that could quantify each patient's symptoms, because many medical records did not report a score. A prospective study of patients with a logged pain scale and a series of MR images would be helpful to determine the relationship of bone marrow edema and effusions to hip pain in patients with osteonecrosis of the femoral head. Patients having contralateral hips with a normal MR appearance and osteonecrosis of the femoral head were a suboptimal control group. In fact, it would be difficult to obtain patients with bone marrow edema and joint effusions but without osteonecrosis of the femoral head as alternative control subjects.
In summary, bone marrow edema is strongly correlated with pain in hips affected by osteonecrosis of the femoral head. The effect of bone marrow edema was enhanced in the presence of a joint effusion. These findings were most pronounced in stage III disease and most likely to occur when the patient presented with pain.
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  H. Ito, T. Matsuno, and A. Minami Relationship between bone marrow edema and development of symptoms in patients with osteonecrosis of the femoral head. Am. J. Roentgenol., June 1, 2006; 186(6): 1761 - 1770. [Abstract] [Full Text] [PDF]
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