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Value of FDG PET in the Assessment of Patients with Multiple Myeloma

¹ Department of Radiology, Massachusetts General Hospital, 15 Parkman St., WACC 515, Boston, MA 02114.
² Department of Radiology, University of California San Francisco, San Francisco, CA 94143-0628.
³ Department of Nuclear Medicine, VA Palo Alto Health Care System, Palo Alto, CA 94304.

Received April 8, 2004; accepted after revision July 14, 2004.

 
Address correspondence to M. A. Bredella (mbredella{at}yahoo.com).

Abstract

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OBJECTIVE. Our objective was to evaluate if whole-body PET with FDG is able to detect bone marrow involvement in patients with multiple myeloma and to assess its appearance and distribution pattern.

MATERIALS AND METHODS. Seventeen whole-body FDG PET scans were performed in 13 patients with multiple myeloma. Four patients were referred for evaluation of extent of disease pretherapy and nine patients were referred for assessment of therapy response (chemotherapy, radiation therapy, bone marrow transplant). FDG PET images were evaluated for distribution and uptake pattern. Standardized uptake values were obtained to quantify FDG uptake. Results of other imaging examinations (MRI, CT, radiography), laboratory data, biopsies, and the clinical course were used for verification of detected lesions.

RESULTS. FDG PET was able to detect medullary involvement of multiple myeloma. There were two false-negative results. In one patient, the radiographic skeletal survey showed subcentimeter lytic lesions within the ribs that were not detected on FDG PET and in the other patient, a lytic lesion detected on radiographs showed only mildly increased FDG uptake that was not identified prospectively. There was one false-positive FDG PET result in a patient who had undergone radiation therapy 3 weeks before PET. FDG PET was helpful in differentiating between posttherapeutic changes and residual/recurrent tumor and in assessing response to therapy. FDG PET resulted in upstaging of disease in four patients, which influenced subsequent management and prognosis. Sensitivity of FDG PET in detecting myelomatous involvement was 85% and specificity was 92%.

CONCLUSION. FDG PET is able to detect bone marrow involvement in patients with multiple myeloma. FDG PET is useful in assessing extent of disease at time of initial diagnosis, contributing to staging that is more accurate. FDG PET is also useful for evaluating therapy response.

Introduction

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Multiple myeloma is a malignant hematologic disorder characterized by bone marrow infiltration with neoplastic plasma cells [1, 2]. Multiple myeloma accounts for 10% of all hematologic cancers with an incidence of approximately 4/100,000 per year [3]. The diagnosis of multiple myeloma is based on specific criteria that include paraproteinemia, plasma cell infiltration of bone marrow, and osteolytic bone destruction. Approximately 5-10% of patients have a solitary plasmacytoma and two thirds of these patients progress to multiple myeloma, presumably because occult disease is present at initial diagnosis [4, 5]. According to the staging system introduced by Durie and Salomon [6], the extent of bone lesions in multiple myeloma significantly influences therapy. Patients with stage I multiple myeloma, with only limited alteration in blood parameters and not more than one skeletal lesion, are followed clinically without therapy, whereas patients with stage II or III multiple myeloma require chemotherapy [2, 4, 6, 7]. With the development of new therapeutic options for treating multiple myeloma [1, 4], it becomes increasingly important to accurately and noninvasively diagnose myelomatous lesions and follow them after treatment.

It has been shown that bone scintigraphy is inadequate for the detection of myeloma-associated bone lesions due to minimal osteoblastic activity and hypovascularity of the lesion [8, 9]. Radiographs are usually obtained for staging, but are limited for evaluating early disease (stages I and II), and several studies have shown that multifocal disease may be present despite normal radiographs [10-12]. MRI is more sensitive than radiographs in detecting bone marrow lesions, and studies have shown that MRI of the vertebral column can detect additional lesions in one third of patients considered to have solitary plasmacytoma based on radiographic findings; however, the sensitivity of detecting early disease is limited [13, 14]. MRI and radiographs often cannot differentiate between treated bone marrow lesions and viable neoplastic tissue.

FDG is an analog of glucose that is radiolabeled with the positron-emitting radionuclide ¹⁸F. Metabolically active cells take up and phosphorylate FDG, which then is not further metabolized and remains trapped within the cell. The resulting intracellular accumulation of FDG is imaged with PET. High uptake is seen in tumor cells, which have increased rates of metabolism compared with normal tissue [15]. FDG PET has been extensively used to detect occult malignant and metastatic lesions in patients with carcinoma or lymphoma and has been become a standard tool for staging patients with bronchogenic carcinoma [16-19].

The purpose of our study was to evaluate if whole body FDG PET is able to detect bone marrow involvement in patients with multiple myeloma and to assess its appearance and distribution pattern. We also evaluated the performance of FDG PET in detecting myelomatous disease compared with other standard imaging methods such as MRI, CT, or radiography and assessed the influence of the additional information obtained by FDG PET on staging and therapy

Materials and Methods

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We retrospectively studied 13 patients with multiple myeloma, who were referred for imaging (MRI, CT, radiographs) of the musculoskeletal system to evaluate for myelomatous involvement. Patients were diagnosed with multiple myeloma on the basis of the criteria defined by Durie and Salmon [6]. All patients underwent whole-body FDG PET. The patient population included 10 males and three females, aged 41-79 years, with a mean age of 54 years. Four patients were referred for evaluation of disease extent pretherapy and nine patients were referred for assessment of therapy response (chemotherapy, bone marrow transplant, radiation therapy, surgical resection). Three patients underwent serial MRI, CT, radiographs, and FDG PET scans to assess response to therapy.

All patients underwent whole-body FDG PET using an ECAT EXACT HR (CTI, Siemens Medical Solutions) camera, allowing simultaneous acquisition of 47 contiguous slices with a slice thickness of 3.375 mm (one bed position, 15.86-cm axial field of view). The patients fasted at least for 4 hr before the study, with plasma glucose levels obtained at the time of FDG administration. Blood glucose levels at the time of injection were less than 6.5 mmol/L in all patients. FDG (3.7 MBq [0.1 mCi]/kg body weight) was injected IV. Whole-body emission scanning (8 to 12 bed positions; acquisition time, 5 min/bed position) was performed 45 min after FDG administration. The PET scans were reconstructed by filtered-back projection using a Hanning filter. FDG PET images were evaluated visually by two experienced radiologists. The radiologists had results of other imaging studies available to them at the time of PET.

Regions of interest (ROIs) were drawn manually around areas of increased uptake. The average and peak activity within each tumor was then corrected for radioactive decay and normalized for patient weight. The standardized uptake values were calculated based on the following equation: Standardized uptake value (SUV) = tissue concentration (MBq/g)/[injected dose (MBq)/body weight(g)]. While the optimal method for drawing ROIs would be using CT or MRI as an anatomic template that projects ROIs onto PET data with coregistered PET/CT or PET/MRI data sets, this was not possible in this study because coregistered data sets were not available. We felt the best approach was to use direct visualization of the radiographic and PET results to guide manual definition of ROIs on PET images. In addition, because lesions often had somewhat irregular borders, iscontouring or other semiautomatic ROI definition methods would likely not change the results and could, with relatively low-intensity margins of lesions, actually introduce more error and noise into the analysis.

Ten patients underwent MRI using a 1.5-T magnet (Signa; GE Healthcare) with the following imaging sequences: T1-weighted spin-echo (TR/TE, 600/20), STIR (3,000/150), fat-suppressed T2-weighted fast spinecho (3,000/90), and fat-suppressed T1-weighted spin-echo (600/20) before and after the administration of gadopentetate dimeglumine. Section thickness was 4 mm, intersection gap was 1 mm, field of view was 14 cm, and the matrix was 256 x 256 pixels.

MR images were evaluated for diffuse or focal bone marrow infiltration that was hypointense on T1- and hyperintense on T2-weighted and STIR images. The number, location, size, signal intensity, and enhancement pattern of each lesion were recorded.

Four patients underwent CT of the spine, and six patients underwent radiography of the spine, pelvis, ribs, skull, and proximal long bones (skeletal survey). CT images and radiographs were evaluated for lytic and permeative bone lesions, and the location and size of each lesion were recorded. FDG PET was performed within 6 weeks of MRI, CT, or radiographs. The results of the imaging studies, laboratory data, biopsies, and clinical course were used for verification of detected lesions.

Results

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We evaluated 17 FDG PET, 16 MRI, four CT studies, and six radiographic bone surveys in 13 patients over a period of 2 years.

Four patients underwent FDG PET and MRI at baseline before initiation of therapy. One of these patients showed diffuse abnormal increased FDG uptake throughout the spine, ribs, pelvis, and long bones, consistent with diffuse myelomatous involvement (Fig. 1). MRI of the spine in this patient showed abnormal infiltrative bone marrow signal that was low on T1- and high on T2-weighted images, consistent with myelomatous involvement. One patient showed no abnormal uptake on FDG PET, and radiographs and MRI were deemed normal. There were two false-negative results on FDG PET. In one patient, a skeletal survey showed subcentimeter lytic lesions within the ribs that were not detected on FDG PET. Subcentimeter radiolucencies in this patient might have been too small to characterize with FDG PET. The other patient showed a large lytic lesion on radiographs, which showed only mildly increased FDG uptake and was not identified prospectively. The lytic lesion was due to myelomatous involvement as proven by subsequent biopsy (Figs. 2A, 2B, and 2C). None of these patients received immunosuppressive therapy before imaging, which could have led to suppressed FDG uptake.

View larger version (73K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1. —55-year-old woman with newly diagnosed multiple myeloma, evaluated pretherapy. Whole-body FDG PET shows multiple foci of increased FDG uptake in bone marrow throughout the body, consistent with myelomatous involvement. Standardized uptake values of lesions ranged from 3.8 to 6.2.

View larger version (71K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —56-year-old woman with multiple myeloma, pretherapy. Coronal FDG PET shows no abnormal FDG uptake and was interpreted as normal.

View larger version (28K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —56-year-old woman with multiple myeloma, pretherapy. Sagittal FDG PET through left upper extremity shows only mildly increased FDG uptake in left humerus (arrow) that was not detected prospectively.

View larger version (58K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —56-year-old woman with multiple myeloma, pretherapy. Radiograph of left humerus shows large lytic lesion (arrow), corresponding to area of abnormal FDG uptake. This was found to represent myelomatous involvement on subsequent biopsy.

Nine patients underwent chemotherapy, radiation therapy, bone marrow transplant, surgical resection, or a combination of these. In four patients, MRI findings were equivocal in differentiating between posttherapeutic changes and residual/recurrent tumor. Subsequent FDG PET demonstrated increased uptake, consistent with myelomatous involvement in two cases, confirmed by biopsy. No abnormal FDG uptake was noted in the remaining two cases. These two patients showed clinical improvement. One patient with initial diagnosis of solitary plasmacytoma, based on MRI and radiographic bone survey, showed multiple FDG-avid foci, suspicious for myelomatous involvement, which influenced staging and subsequent therapy. Extensive medullary and extramedullary involvement was confirmed in this patient on autopsy.

One patient with plasmacytoma of the right hemipelvis showed abnormal enhancing soft tissue, consistent with plasmacytoma. This was confirmed on subsequent FDG PET (Figs. 3A, and 3B). One patient who had undergone radiation therapy of the right clavicle three weeks before FDG PET, showed abnormal uptake in the region of the radiated clavicle and surrounding musculature. Increased uptake was likely due to postradiation changes; however, residual tumor could not be excluded. Clinical follow-up in this patient showed good response to therapy without evidence of residual tumor.

View larger version (127K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —43-year-old man with high-grade plasmacytoma of right hemipelvis, status postchemotherapy and bone marrow transplant. Coronal fat-suppressed T1-weighted MRI with gadopentetate dimeglumine shows abnormal enhancing soft tissue in right hemipelvis.

View larger version (66K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —43-year-old man with high-grade plasmacytoma of right hemipelvis, status postchemotherapy and bone marrow transplant. Coronal FDG PET shows abnormal FDG uptake in right hemipelvis with standardized uptake value ranging from 4.3 to 5.0.

Three patients underwent serial MRI, CT, radiographs, and FDG PET scans to assess response to chemotherapy and bone marrow transplant. All patients showed persistent abnormal bone marrow signal on MRI, and abnormal lytic lesions on CT and radiographs, suspicious for residual tumor. Subsequent FDG PET demonstrated decline in metabolic activity in two patients, which was concordant with clinical improvement. In one patient, a new focus of abnormal uptake was detected on follow-up scan in an area distant to the original tumor, consistent with recurrent disease (Figs. 4A, 4B, 4C, 4D, 4E, and 4F). Results of imaging studies and clinical findings are summarized in Table 1. Sensitivity of FDG PET in detecting myelomatous involvement was 85% and specificity was 92%.

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —41-year-old patient with multiple myeloma of C1/C2, status post posterior spinal fusion, chemotherapy, and bone marrow transplant 9 months ago. Sagittal fat-suppressed T1-weighted MRI with gadopentetate dimeglumine shows abnormal enhancing soft tissue (arrow) at C1/C2, suspicious for recurrent myeloma.

View larger version (47K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —41-year-old patient with multiple myeloma of C1/C2, status post posterior spinal fusion, chemotherapy, and bone marrow transplant 9 months ago. Sagittal FDG PET shows no abnormal FDG uptake in cervical spine. Patient was followed clinically and there was no evidence of recurrent tumor over 1 year. Note physiologic FDG uptake in the oropharynx (arrow).

View larger version (125K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —41-year-old patient with multiple myeloma of C1/C2, status post posterior spinal fusion, chemotherapy, and bone marrow transplant 9 months ago. Axial CT image through upper cervical spine obtained for neck pain 8 months later shows lytic lesions at C1/C2 at site of original tumor (arrow). These findings were thought to represent recurrent tumor. Note posterior spinal fusion hardware.

View larger version (44K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4D. —41-year-old patient with multiple myeloma of C1/C2, status post posterior spinal fusion, chemotherapy, and bone marrow transplant 9 months ago. Sagittal FDG PET shows no abnormal FDG uptake and patient improved clinically without evidence of recurrent tumor.

View larger version (180K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4E. —41-year-old patient with multiple myeloma of C1/C2, status post posterior spinal fusion, chemotherapy, and bone marrow transplant 9 months ago. Sagittal fat-suppressed T1-weighted MRI with gadopentetate dimeglumine, obtained 7 months later for alteration in blood parameters that was suspicious for recurrent tumor. There is abnormal enhancing soft tissue at C1/C2 (arrow) that was thought to represent recurrent tumor.

View larger version (43K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4F. —41-year-old patient with multiple myeloma of C1/C2, status post posterior spinal fusion, chemotherapy, and bone marrow transplant 9 months ago. Sagittal FDG PET obtained same day shows no abnormal FDG uptake in cervical spine; however, new focus of intense FDG uptake (standardized uptake value: 4.3) is noted in left sacroiliac region (arrow) that was found to represent myeloma on subsequent biopsy.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The presence and extent of bone marrow and extramedullary involvement in patients with multiple myeloma are important factors influencing prognosis and clinical management [4, 7]. Radiographs are usually obtained for staging of multiple myeloma, but are limited for evaluating early disease [8]. MRI is more sensitive than radiographs in detecting bone marrow involvement; however, substitution of radiograph surveys by MRI limited to the spine and pelvis would cause understaging in 10% of patients [14]. In addition, MRI has limitations in diagnosing stage I disease, and up to 20% of MRI examinations can be normal despite diffuse bone marrow involvement [14]. A small number of patients also present with extramedullary manifestations of multiple myeloma, and these lesions are often difficult to detect but have major impact on the prognosis [7, 20]. In a recent study by Mahnken et al. [21], MDCT of the spine, in combination with MRI, was sensitive in detecting myelomatous involvement in patients with stage III disease. However, there are no studies to evaluate the performance of CT in evaluating stage I or II disease.

A recent study has shown the ability of FDG PET in differentiating posttherapeutic changes from tumor recurrence in patients with musculoskeletal sarcomas [22]. Case reports and two larger studies have shown the potential of FDG PET in detecting bone marrow involvement in patients with multiple myeloma [7, 23-26].

Our study showed that FDG PET is able to detect bone marrow involvement in patients with multiple myeloma. The ability of PET to evaluate the whole body in a single procedure and the potential to detect medullary and extramedullary lesions in a single examination are important advantages over standard imaging techniques such as MRI, CT, or radiographs. FDG PET also is helpful in monitoring response to therapy. In the group of patients who underwent serial FDG PET examinations, changes in metabolic activity of myelomatous lesions predicted clinical outcome. In four patients, FDG PET resulted in upstaging of disease and, therefore, more aggressive therapy. One of these patients presented with plasmacytoma and the detection of additional lesions influenced management and outcome. It must be noted that very small lesions may not be detected on FDG PET due to volume averaging in relation to the limited spatial resolution of the PET scanner. In our study, there was a false-negative result on FDG PET due to subcentimeter size of the lesion. In one case, myelomatous involvement of the humerus showed only mildly increased metabolic activity and was not detected prospectively. False-positive results can occur due to inflammatory changes from radiation therapy or post surgery, as in our case, where FDG PET was performed within 3 weeks of radiation therapy. Therefore, FDG PET should not be performed within 2 months following therapy.

Our study had several limitations. First, there is the small number of patients and retrospective fashion of our study. Second, the radiologists had the results of other imaging studies available at time of interpretation. Another limitation is the lack of pathologic correlation in certain patients. We used biopsy in some cases and had to rely on additional imaging studies or clinical course in the other cases. All but one patient was evaluated more than 6 months posttherapy. Previous studies have shown that diffuse bone marrow uptake can be seen during or within months after chemotherapy, which can lead to false-positive results.

Our study showed that FDG PET is useful in assessing the extent of multiple myeloma at time of initial diagnosis, contributing to more accurate staging. FDG PET is also useful for evaluating therapy response, especially when other imaging techniques (MRI, CT, radiography) remain abnormal. FDG PET also contributes to improve clinical management in patients with solitary plasmacytoma, when a higher sensitivity to detect medullary involvement is essential.

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