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1 All authors: Department of Radiology, University of California, San Francisco, 505 Parnassus Ave., San Francisco, CA 94143-0628.
Received March 15, 2002;
accepted after revision April 9, 2002.
Address correspondence to M. A. Bredella.
Abstract
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MATERIALS AND METHODS. We evaluated 12 patients (nine males, three females; age range, 9-56 years; mean age, 25 years) with a history of bone or soft-tissue sarcoma who had undergone various treatments (surgery, chemotherapy, radiation therapy, or a combination of treatments) and who presented with clinically suspected recurrent or residual tumor. All patients underwent gadopentetate dimeglumine—enhanced MR imaging and whole-body FDG PET. Imaging results were correlated with histologic findings or with clinical findings from long-term follow-up.
RESULTS. In nine patients, MR imaging findings were equivocal in differentiating between posttherapeutic changes and tumor recurrence. FDG PET images showed increased uptake, suggestive of recurrent tumor, in five patients. These findings were confirmed by biopsy. Four patients showed no increased uptake on FDG PET and were closely monitored clinically. No tumor recurrence was found in these patients. One patient showed MR imaging findings suggestive of recurrent tumor that was confirmed on FDG PET and at histology. Two patients underwent a limb salvage procedure before MR imaging, but MR images were deemed inadequate for interpretation because of extensive metallic artifacts. FDG PET was helpful in evaluating these patients for tumor recurrence.
CONCLUSION. FDG PET is a useful adjunct to MR imaging in distinguishing viable tumor from posttherapeutic changes in patients with bone and soft-tissue sarcomas.
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Positron emission tomography (PET) is an imaging technique that uses radiopharmaceuticals, typically a radionuclide-labeled analog of glucose, such as FDG, to detect abnormal metabolic activity [8]. Because malignant tumors usually have increased cellular and thus increased glucose metabolism, PET is able to provide unique information, complementary to that provided by MR imaging, about the biologic activity of musculoskeletal tumors. Recently, FDG PET has shown promising results in distinguishing benign from malignant musculoskeletal neoplasms [9,10,11].
The purpose of our study was to investigate the potential of FDG PET in conjunction with MR imaging to distinguish viable tumor from changes caused by therapy in patients with musculoskeletal sarcomas.
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The patient population included nine males and three females who ranged in ages from 9 to 56 years, with a mean age of 25 years. Primary tumors included rhabdomyosarcoma, angiosarcoma, undifferentiated high-grade soft-tissue sarcoma, hemangiopericytoma, Ewing's sarcoma, clear cell sarcoma, extraosseous myxoid chondrosarcoma, spindle cell sarcoma, and osteogenic sarcoma (Table 1).
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All patients underwent standard MR imaging using a 1.5-T magnet (Signa; General Electric Medical Systems, Milwaukee, WI). The following imaging sequences were performed: T1-weighted spin-echo (TR/TE, 600/20), fat-suppressed T2-weighted fast spin-echo (3000/90), and fat-suppressed T1-weighted spin-echo (600/20) before and after the administration of gadopentetate dimeglumine. The section thickness was 4-5 mm, the intersection gap was 1 mm, and the matrix size was 256 x 256 pixels. For all MR imaging sequences, we used the smallest field of view that encompassed the region to be imaged and allowed an adequate signal-to-noise ratio.
MR imaging criteria for possible recurrent or residual tumor were as follows: areas of low signal intensity on T1-weighted images that became high signal intensity on fat-suppressed fast spin-echo T2-weighted images, an increase in tumor size or a new mass lesion with or without infiltration of the surrounding tissues, and enhancement after the administration of gadopentetate dimeglumine. The radiologists who reviewed the MR images had access to the clinical data at the time of interpretation.
Because MR examinations were deemed equivocal or nondiagnostic, all patients underwent whole-body FDG PET using an Ecat Exact 921/47 camera (CTI; Siemens, Knoxville, TN), 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 FDG PET examinations were performed during the 3 weeks after the initial MR examination. Patients fasted for at least 4 hr before the study. Plasma glucose levels were obtained at the time of FDG administration; the blood glucose level in all patients was less than 6.5 mmol/L at the time of injection. FDG (dose in adults, 15 mCi [555 MBq]; dose in pediatric patients, adjusted based on body weight) was injected IV. Attenuated, corrected whole-body emission scanning (from eight to 12 bed positions; acquisition time, 8 min per bed position with 33% of time spent in transmission mode) was performed 45 min after FDG administration. The PET scans were reconstructed by interactive filtered back-projection using a Hanning filter.
FDG PET images were evaluated by two experienced radiologists. The radiologists had the MR examinations available to them at the time of PET imaging.
Regions of interest were drawn manually around areas of increased FDG uptake. The average activity and peak activity in each tumor were then corrected for radioactive decay and were normalized for patient weight. The standardized uptake values were calculated on the basis of the following equation: standardized uptake value = [tissue concentration (MBq/g)] / [injected dose (MBq) / body weight (g)]. The size, shape, extent, and standardized uptake value of each region with abnormal FDG uptake were recorded. Standardized uptake values greater than 2.0 were considered suggestive of residual or recurrent tumor.
Four patients underwent serial (between two and three) MR imaging and FDG
PET examinations during the 3-year period. In these patients, the previous
examinations were available to the radiologist for comparison. If imaging
findings (MR imaging or PET) were positive for recurrent or residual tumor,
histologic specimens were obtained and the findings were then correlated with
imaging findings. If imaging findings were negative, long-term clinical
follow-up (
3 years), including repeated PET and MR examinations or
biopsy, was performed.
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Four of the nine patients with equivocal MR imaging findings showed mild increased FDG uptake (range of standardized uptake values, 1.3-1.6; mean, 1.35) on PET, but these findings were thought to represent posttherapeutic changes. These patients were closely monitored clinically and underwent repeated PET and MR examinations over a period of 3 years. No evidence of tumor recurrence was found in these patients. In one patient, a biopsy sample was obtained. Results of the biopsy showed nonviable tumor. MR imaging findings in these four patients consisted of patchy foci of T2 hyperintensity in and surrounding the tumor bed (n = 2) (Fig. 1A,1B) and a heterogeneous soft-tissue mass with areas of enhancement (n = 2) (Fig. 2A,2B and Table 1).
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Follow-up PET and MR examinations, performed annually, in these four patients showed no change (n = 1) or further decrease in FDG uptake (n = 3), and MR examinations showed no interval change. In the patient with a history of rhabdomyosarcoma of the hypothenar eminence, FDG PET revealed no increased uptake in the region of the original tumor but detected metastatic foci in the elbow and breast. These imaging findings were confirmed at biopsy (Fig. 3A,3B,3C,3D,3E).
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In one patient, MR imaging findings showed a large heterogeneous soft-tissue mass in the region of the spinoglenoid notch with infiltration of adjacent fatty and fascial planes; these findings were consistent with recurrent tumor. Subsequent FDG PET depicted increased uptake (standardized uptake value, 4.6) suggestive of active tumor. Surgical resection of the mass confirmed recurrent extraosseous myxoid chondrosarcoma (Fig. 4A,4B).
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Two patients underwent a limb salvage procedure for osteogenic sarcoma of the femur and angiosarcoma of the pelvis before undergoing MR imaging. The MR images were deemed inadequate for interpretation because of extensive artifacts from the metallic prosthesis. In these patients FDG PET adequately depicted the area of interest (Fig. 5). No increased uptake was identified in these two patients, and clinical follow-up over a period of 3 years showed no recurrent tumor.
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In our study, FDG PET was helpful in distinguishing posttherapeutic changes from tumor recurrence in patients with equivocal MR imaging findings. We used a standardized uptake value of 2.0 as the cutoff for distinguishing active from nonactive tumor. However, no consensus exists about the accurate standardized uptake value in musculoskeletal neoplasms for differentiating tumor recurrence from posttherapeutic changes. Several studies have been performed to evaluate standardized uptake values of benign and malignant musculoskeletal neoplasms and have reported values ranging from less than 1.9 to 2.9 for benign neoplasms and from greater than 2.0 to 3.0 for malignant neoplasms [10, 11]. Aoki et al. [16] showed that the overlap of standardized uptake values for benign and malignant bone neoplasms is considerable, with standardized uptake values of greater than 2.0 in giant cell tumors and chondroblastomas.
Only a few studies have addressed the potential of FDG PET in the evaluation of tumor recurrence [17, 18]. In our study, FDG PET enabled us to correctly identify tumor recurrence and posttherapeutic changes in all 12 patients. We observed standardized uptake values between 2.6 and 4.6 in regions of viable tumor and mildly increased FDG uptake with standardized uptake values ranging from 1.3 to 1.6 in the region of treated tumor, which we attribute to changes caused by inflammation. However, limitations of our study were the small sample size and heterogeneity of our patient population.
Previous examiners have questioned the diagnostic accuracy of FDG PET in the evaluation of posttherapeutic changes because the range of standardized uptake values from the accumulation of FDG in inflammatory tissue overlaps that of residual tumor [19]. Additional data from larger, more homogeneous patient populations with treated musculoskeletal sarcomas are needed to determine an accurate cutoff standardized uptake value for benign versus malignant neoplasms. Another limitation of our study was the lack of dynamically contrast-enhanced MR imaging studies; these studies have been found to help differentiate recurrent tumor from posttherapeutic changes [5].
After chemo- or radiation therapy, areas of necrosis are frequently found in the tumor and can, if biopsied, prevent correct diagnosis of tumor recurrence. We selected the areas of peak activity shown on FDG PET images and MR images to obtain the most metabolically active tissue for biopsy.
In our study, all FDG PET scans were obtained using a whole-body technique. This technique allowed detection of metastatic disease in one patient.
In three of our four patients who underwent serial PET and MR examinations, FDG PET showed metabolic changes (interval decrease in FDG uptake), whereas MR imaging showed no changes. This discrepancy suggests that FDG PET could be used to monitor the progression or regression of tumor before morphologic changes become apparent. However, additional studies are needed to determine whether this concept remains valid in a larger patient population.
A disadvantage of FDG PET is its limited availability, high cost, and limited spatial resolution that requires complementary CT or MR imaging be performed to localize an area of increased contrast uptake [8, 20]. In our study, FDG PET in conjunction with MR imaging was helpful in monitoring patients without performing invasive biopsy. Also, FDG PET images are not affected by metallic artifacts from limb salvage prostheses.
Our preliminary results show that FDG PET can provide unique information about tumor function and metabolism in patients with equivocal MR imaging findings. In addition to its ability to distinguish recurrent tumor from posttherapeutic changes, FDG PET has the ability to examine the entire body for both primary malignancies and metastatic disease during a single procedure. It can further be used to guide biopsy to the most active tissue and to evaluate patients who have undergone limb salvage procedures.
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