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Prognostic Significance of Magnetic Resonance Imaging of Femoral Marrow in Patients With Myelodysplastic Syndromes

From the Division of Hematology and Department of Radiology, Omiya Medical Center, Jichi Medical School, Omiya, Saitama; Division of Biostatistics, Toyama Med-Pharm University, Toyama; and Division of Hematology, Jichi Medical School, Tochigi, Japan.

Address reprint requests to Shojiro Takagi, MD, Division of Hematology, Omiya Medical Center, Jichi Medical School, 1–847 Amanuma-cho, Omiya, Saitama 330, Japan.

	ABSTRACT

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PURPOSE: To investigate whether the abnormalities observed on femoral marrow magnetic resonance images are related to the development of leukemia and survival of patients with myelodysplastic syndromes (MDS).

PATIENTS AND METHODS: The findings on magnetic resonance images of the femoral marrow were evaluated over periods of 1 to 92 months (median, 18 months) in 42 consecutive adult patients with newly diagnosed MDS. Magnetic resonance images were obtained by the T1-weighted spin echo method and the short TI inversion recovery technique.

RESULTS: Magnetic resonance images showed that the femoral marrow patterns changed from fatty, faint, or nodular to scattered or uniform as the disease progressed. Development of acute myeloid leukemia was observed in only 13 patients whose marrow exhibited a scattered or uniform pattern. The overall survival of the 29 patients with a scattered or uniform marrow pattern was significantly shorter than that of the 13 patients with a fatty, faint, or nodular marrow pattern (10.7% v 73.3% at 7 years; P < .01). The period of leukemia-free survival was also significantly shorter in the patients with a scattered or uniform marrow pattern versus a fatty, faint, or nodular pattern (37.7% v 100% at 7 years; P < .01).

CONCLUSION: Magnetic resonance images of the femoral marrow can provide valuable information for assessing the prognosis and determining the most appropriate management of patients with MDS.

	INTRODUCTION

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MYELODYSPLASTIC SYNDROMES (MDS), a heterogeneous group of bone marrow disorders, are characterized by ineffective hematopoiesis with bone marrow dysplasia.¹ The prognosis of patients with MDS is related to the French-American-British (FAB) category.² Patients with refractory anemia (RA) and refractory anemia with ring sideroblasts (RARS) generally have a good prognosis, whereas those with either refractory anemia with excess of blasts (RAEB) or RAEB in transformation (RAEB-T) have a poor prognosis. The prognosis for patients with chronic myelomonocytic leukemia (CMML) or hypoplastic MDS varies widely.^3-7 The major causes of death in MDS are the development of leukemia and hemorrhage or infection related to the cytopenia.⁴ Factors that influence the outcome of patients with MDS include age, sex, hemoglobin concentration, WBC count, neutrophil count, platelet count, percentage of blasts in the blood and bone marrow, abnormal localization of immature precursors, FAB classification, karyotype, and DNA ploidy.^4,8-12

Magnetic resonance imaging (MRI) of the marrow is a sensitive method for evaluating patients with bone marrow disorders that provides a better understanding of disease progression and remission.^13-17 Several investigators have evaluated magnetic resonance (MR) images of the vertebral or femoral marrow in patients with MDS.^18-24 Although abnormalities were observed in the vertebral marrow,^21,22 the degree of reduction in signal intensity on T1-weighted images was unrelated to the FAB classification.²¹ However, our previous study suggested that MRI findings in the femoral marrow may be related to disease progression.²⁵ In another study, we reported that patients with MDS who had a poor prognosis showed significantly higher T1 relaxation times in the femoral marrow than did patients with MDS who had a good prognosis.²⁶ In the present study, we investigated the relationship between abnormal patterns in the femoral marrow MR images, the development of leukemia, and the survival of patients with MDS.

	PATIENTS AND METHODS

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Patients
We studied retrospectively the data on 42 consecutive adult Japanese patients with newly diagnosed MDS. Diagnoses included RA (n = 15), RARS (n = 7), RAEB (n = 6), RAEB-T (n = 11), and CMML (n = 3). Patients had visited the Omiya Medical Center at the Jichi Medical School, Omiya, Japan, between December 1989 and March 1997 and included 27 men and 15 women ranging in age from 22 to 87 years (median, 64 years) (Table 1). Diagnoses were made according to FAB criteria.¹ In four of the 15 patients with RA, the bone marrow was hypoplastic, and the clinical findings in these four patients were compatible with a diagnosis of hypoplastic MDS.^6,7 MRI studies were performed within 2 weeks of the diagnosis of MDS and were repeated during a follow-up period ranging from 1 to 92 months. Patients who had other diseases, such as malignant solid tumors and hematologic disorders, that might influence the evaluation of the MR images were excluded from the study. Also excluded were patients who had previously received intensive chemotherapy and patients with secondary MDS. During the observation period, the patients received various therapies, including transfusions, prednisolone, androgens, 1,25-dihydroxy vitamin D₃, and cytotoxic agents. None of the patients received transfusions of peripheral blood stem cells or bone marrow transplants during this study. Each patient gave written informed consent.

MRI
MRI was performed using spin echo (SE) sequences with the whole-body coil in a 1.5-tesla superconducting system (MRT 200 FX/II; Toshiba, Tokyo, Japan). MR images of the femoral marrow were obtained by the T1-weighted SE method and the short TI inversion recovery (STIR) technique.²⁷ Coronal T1-weighted SE images of the femur were obtained from contiguous 10-mm slices in a 256 x 256 matrix by a repetition time of 400 milliseconds, an echo time of 20 milliseconds, and two signal acquisitions. STIR coronal images of the femur were obtained from 10-mm slices in a 256 x 256 matrix with a repetition time of 1,500 milliseconds, an echo time of 20 milliseconds, and an inversion time of 150 milliseconds. MRI results were evaluated blindly by two independent observers who had no knowledge of the patients' FAB subtype. The coefficient between the two observers was 0.84 (95% confidence interval, 0.70 to 0.97), which indicated an excellent agreement.

Categorization of Patterns
The general patterns in the femurs were categorized into one of five groups as follows: (1) fatty, showing a low-signal-intensity marrow that appeared dark on STIR images (but high-signal-intensity marrow that appeared bright on T1-weighted SE images); (2) faint, showing an abnormally faint signal intensity in the fatty-signal-density marrow (this abnormal intensity of the femoral marrow on the STIR images was equal to or lower than that of muscle); (3) nodular, showing low-signal marrow density with small nodules of a higher intensity on STIR images (but high-signal marrow density with small nodules of a lower intensity on T1-weighted SE images); (4) scattered, showing multiple scattered areas of higher signal intensity in the low-signal-intensity marrow on STIR images (but lower signal intensity in the high-signal-intensity marrow on T1-weighted SE images); or (5) uniform, a uniformly high-signal-intensity marrow as compared with the low-signal-intensity muscles on STIR images (but low-signal-intensity marrow as compared with high-signal-intensity muscles on T1-weighted SE images) (Fig 1).

View larger version (12K): [in this window] [in a new window]   Fig 1. Five categories of MRI patterns of the femoral marrow of 42 patients with MDS based on STIR images.

Statistical Analysis
Data are reported as mean ± SD. MR images of the femoral marrow were compared with the patients' clinical characteristics and analyzed by the ² test with the Yates correction. Means were compared by two-sample t tests. The duration of overall survival was measured from the time of MRI evaluation to the time of death or the last follow-up visit. The leukemia-free period was calculated from the time of MRI evaluation until the time when leukemia was diagnosed or until the last follow-up visit. Survival curves were constructed using the Kaplan-Meier method.²⁸ Statistical significance was determined by the log-rank test.²⁹ Factors that affected survival were assessed by a multivariate regression analysis according to the Cox proportional hazards regression model.³⁰ A level of P less than .05 was accepted as statistically significant.

	RESULTS

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Forty-two patients were followed for 1 to 92 months (median follow-up, 18 months). At the time of analysis, 18 of the 42 patients were alive for 4 to 92 months (median, 32 months) after the initial MRI evaluation. Twenty-four patients died at a median interval of 9 months (range, 1 to 65 months). Thirteen patients developed acute myeloid leukemia between 1 and 33 months (median, 6 months) after the initial MRI evaluation (Table 1).

MRI Patterns of the Femoral Marrow
Of the 42 patients with MDS, five (12%) had marrow that exhibited a fatty or faint pattern, eight (19%) had marrow that demonstrated a nodular pattern, 19 (45%) had marrow that showed a scattered pattern, and 10 (24%) had marrow that exhibited a uniform pattern (Table 2). All five patterns were observed in patients with RA or RARS, whereas the patients with RAEB, RAEB-T, or CMML had marrow that exhibited either a scattered or uniform pattern. A fatty, faint, or nodular pattern was observed only in the marrow of the 13 patients with RA or RARS. These results indicate that the change in the femoral marrow from a fatty, faint, or nodular pattern to a scattered or uniform pattern was correlated with disease progression, and the results suggest that the pattern of the femoral marrow on MRI may indicate differing prognoses for patients with MDS.

Relationship Between MRI and Patient Characteristics
Patients whose femoral marrow demonstrated a scattered or uniform pattern had a significantly more advanced disease (P < .0001) and a significantly higher percentage of blasts in the bone marrow (P < .0013) than patients whose femoral marrow had a fatty, faint, or nodular pattern (Table 1). Only the 13 patients whose femoral marrow demonstrated a scattered or uniform pattern developed leukemia. The positive predictive probability of the scattered or uniform pattern for the development of leukemia was .45, and the negative predictive probability was 1.00. Although the incidence of nonleukemic death from causes such as infection and hemorrhage was somewhat higher in patients with the scattered or uniform pattern, the difference was not statistically significant. At the time of the last follow-up, 11 of the 13 patients (85%) whose marrow demonstrated the fatty, faint, or nodular pattern were still alive, whereas 22 of the 29 patients (76%) whose marrow exhibited a scattered or uniform pattern had died, a highly significant difference (P < .0003). The characteristics of the patients who exhibited a fatty, faint, or nodular marrow pattern did not differ significantly with respect to sex, age, WBC count, hemoglobin concentration, platelet count, or karyotype from those of the patients who had a scattered or uniform marrow pattern.

When all 42 patients were classified according to the International Prognostic Scoring System,⁹ the patients with the fatty, faint, or nodular marrow pattern fell into either the low-risk or intermediate-1–risk group (Table 3). Patients who fell into the high-risk or intermediate-2–risk group were those with a scattered or uniform marrow pattern. These results suggest that patients with the scattered or uniform marrow pattern are more likely to develop leukemia and to have a poorer prognosis.

Development of Acute Myeloid Leukemia in Patients With the Scattered or Uniform Marrow Pattern
Among the 29 patients who had a scattered or uniform marrow pattern, eight of the 19 patients (42%) with the scattered marrow pattern and five of the 10 patients (50%) with the uniform marrow pattern developed acute myeloid leukemia. There was no significant difference between the scattered pattern and the uniform pattern in predicting the development of leukemia. The 13 patients who developed leukemia exhibited more advanced disease (P < .0408), a higher percentage of blasts in the bone marrow (16.3% v 6.3%, P < .0022), and a lower hemoglobin concentration (7.5 g/dL v 8.6 g/dL, P < .0325) as compared with the 16 patients with the scattered or uniform marrow pattern who did not develop leukemia. The 29 patients with the scattered or uniform marrow pattern showed no significant difference in sex, age, WBC count, platelet count, or karyotype, regardless of whether they developed leukemia (data not shown). All 13 patients who developed leukemia died during follow-up. Nine (56%) of the 16 patients who did not develop leukemia died from nonleukemic causes. At the time leukemia was diagnosed, MR images of the femoral marrow were brighter with the STIR technique, but darker with the T1-weighted SE method, and showed more extensive distal involvement than when the MDS was diagnosed. Patients who initially had a scattered marrow pattern showed a uniform marrow pattern when they developed leukemia (data not shown).

Prognostic Significance of Femoral Marrow MRI
The 7-year overall survival rates for all 42 patients, for the 13 patients who had a fatty, faint, or nodular marrow pattern, and for the 29 patients who had a scattered or uniform marrow pattern were 24.6%, 73.3%, and 10.7%, respectively (Fig 2). The overall survival of the patients with a scattered or uniform marrow pattern was significantly shorter than that of patients with a fatty, faint, or nodular marrow pattern (P < .01). The incidence of leukemia-free survival over 7 years was as follows: 60.4% for all 42 patients, 100% for the 13 patients who had a fatty, faint, or nodular marrow pattern, and 37.7% for the 29 patients who had a scattered or uniform marrow pattern (Fig 3). The leukemia-free survival of the patients with a scattered or uniform marrow pattern was also significantly shorter than that of patients with a fatty, faint, or nodular marrow pattern (P < .01). There was no significant difference between the scattered and the uniform patterns in overall or leukemia-free survival. By proportional hazards regression multivariate analysis, the estimated risk ratios of the marrow MRI findings (fatty, faint, or nodular pattern v scattered or uniform pattern) for overall survival and for leukemia-free survival were 0.640 and 0.001, respectively. The marrow MRI showed no significant relationship to such independent clinical variables as FAB subtype, International Prognostic Scoring System category, and karyotype (P = .36 for overall survival and P = .10 for leukemia-free survival), perhaps because of the relatively small number of patients in each subset.

View larger version (17K): [in this window] [in a new window]   Fig 2. Relationship between overall survival and MRI pattern. Overall survival was significantly shorter in the patients whose marrow exhibited a scattered or uniform pattern than in patients whose marrow exhibited a fatty, faint, or nodular pattern (P < .01).

View larger version (17K): [in this window] [in a new window]   Fig 3. Relationship between progression to leukemia and MRI pattern. The incidence of progression to acute myeloid leukemia was significantly higher in the patients whose marrow exhibited a scattered or uniform pattern than in patients whose marrow exhibited a fatty, faint, or nodular pattern (P < .01).

	DISCUSSION

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The present study indicates that findings on MR images of the femoral marrow in patients with MDS may predict their prognosis, including whether they will develop leukemia. MRI showed that the pattern of the marrow changed from a fatty, faint, or nodular pattern to a scattered or uniform pattern as the disease progressed. Thus, patients with a scattered or uniform marrow pattern were suspected of having more advanced disease. Furthermore, only those patients with a scattered or uniform marrow pattern developed leukemia. The overall survival period and the leukemia-free period were both significantly shorter in patients with a scattered or uniform marrow pattern than in patients with a fatty, faint, or nodular marrow pattern. Death from nonleukemic causes was also more frequent in patients with the scattered or uniform marrow pattern. Among the patients whose marrow exhibited a scattered or uniform pattern, the development of leukemia was more frequent in patients with more advanced disease according to FAB category, a higher percentage of blasts in the bone marrow, and a lower hemoglobin concentration. These results confirm previous observations that the percentage of type 1 blast cells in the bone marrow and the hemoglobin concentration influence the development of acute myeloid leukemia.^10,31 Quantitative assessment of the femoral marrow by MRI indicates that patients who show a more prolonged T1 relaxation time when the MDS is diagnosed tend to develop leukemia.²⁶ In another study, however, no clear trend in changes in T1 value in the vertebral marrow was related to the development of leukemia.²⁴

If these abnormalities on the MR images of the femoral marrow accurately reflect changes in the bone marrow of patients with MDS, patients with a scattered or uniform pattern should show a higher percentage of blasts in the bone marrow than patients with a fatty, faint, or nodular pattern, and indeed, this is what we observed. The reason for these differing patterns is unclear. Interestingly, the incidence of deaths from complications, including leukemia, was higher in the patients with a scattered or uniform marrow pattern than in the patients with a fatty, faint, or nodular marrow pattern (33% v 15%), when only those patients with RA or RARS who showed a low frequency of bone marrow blasts were analyzed (data not shown).

More prominent and more extensive findings on the magnetic resonance images of the femoral marrow were observed in the patients with MDS who ultimately developed leukemia. These abnormalities were not specific for the disease. Obviously, MR images should always be interpreted in reference to the clinical findings.

Patients with MDS who exhibit complex chromosomal aberrations reportedly develop leukemia soon after the disease is diagnosed.^9,31 However, in the present study, we observed no significant correlation between the cytogenetic abnormalities and the MRI patterns, although all seven patients with a "poor" cytogenetic subtype exhibited a scattered or uniform marrow pattern.

Because of its marrow component and length, the femur seems to be the most suitable site for the detection of leukemic foci. The adult spine is rich in red marrow, whereas the femoral marrow is largely fatty.¹⁷ Infiltration of the marrow by leukemia cells is thought to originate in the red marrow. Because of its rich vascularity, the red marrow fills with leukemia cells relatively rapidly. Therefore, MR images of the vertebral marrow in patients with MDS show more advanced changes than images of the femur.³² Changes in the femoral marrow progress gradually from the proximal portion, which is rich in red marrow, to the distal fatty portions. This leads to MR images of the femoral marrow that have a greater variety of patterns than seen in the vertebral marrow. This presents an advantage when subtle changes are evaluated in the marrow of MDS patients. Accordingly, studies that evaluated the vertebral marrow of MDS patients have shown no significant relationship between such MRI findings and the number of marrow blasts, erythroblasts, and FAB subtypes or the severity of the peripheral cytopenia.^21,23

In the present evaluation of the femoral marrow, we did not use the T2-weighted SE method because such images do not readily distinguish the fatty marrow from the red marrow.¹³ T2 relaxation times of the femoral marrow in patients with MDS do not differ significantly from those of normal volunteers.²⁶ At the time that acute leukemia is diagnosed, T2 relaxation times of the marrow do not differ from normal values.^33-36

In the present study, we showed that patients whose marrow exhibited a scattered or uniform pattern seemed to have a poor prognosis, a tendency to develop acute myeloid leukemia, and a shorter survival period. Such patients may therefore require more intensive chemotherapy with allogeneic bone marrow transplantation to prevent the development of leukemia. On the other hand, patients whose marrow demonstrated a fatty, faint, or nodular pattern seemed to have a favorable prognosis and a low risk for the development of leukemia. Such patients may be followed without special treatment or may be given RBC transfusions or platelet products when indicated.

Several clinical scoring systems have been proposed to provide more precise prognostic information on patients with MDS.^{4,9,10,31,37,38} The use of MR images of the femoral marrow in conjunction with such scoring systems may improve the accuracy of the diagnosis and be useful in monitoring the status of patients with MDS.

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Submitted January 21, 1998; accepted August 24, 1998.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Takagi, S. Articles by Miura, Y. Search for Related Content PubMed PubMed Citation Articles by Takagi, S. Articles by Miura, Y. Social Bookmarking                            What's this?