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Nuclear Medicine |
1 From the Departments of Internal Medicine, Division of Nuclear Medicine (B.L.S., B.S., J.C.S.), Surgery (N.W.T.), and Radiology (I.R.F.), University of Michigan Medical Center, 1500 E Medical Center Dr, Ann Arbor, MI 48109. Received July 9, 1998; revision requested August 18; revision received September 16; accepted December 16. Supported in part by grant CA54216 from the National Cancer Institute and grant MO1 RR 00042 from the University of Michigan Clinical Research Center. Address reprint requests to B.L.S. (e-mail: bshulkin@umich.edu).
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Abstract |
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MATERIALS AND METHODS: Twenty-nine patients with one or more known or subsequently proved pheochromocytomas underwent FDG PET (35 scans) and MIBG scintigraphy (35 scans). Tumor uptake of FDG was quantified on positive PET scans.
RESULTS: Tumor uptake of FDG was detected in 22 of 29 patients. Most benign (seven of 12 patients) and most malignant (15 of 17 patients) pheochromocytomas and their metastases avidly concentrated FDG. In four patients whose pheochromocytomas failed to accumulate MIBG, uptake of FDG in the tumors was intense. For the majority of the 16 patients whose tumors concentrated both agents, however, ratings for MIBG images compared to FDG PET images for delineation of the tumor in comparison to background and normal organ accumulation were superior for nine patients (56%) and as good or better for 14 (88%).
CONCLUSION: Most pheochromocytomas accumulate FDG. Uptake is found in a greater percentage of malignant than benign pheochromocytomas. FDG PET is especially useful in defining the distribution of those pheochromocytomas that fail to concentrate MIBG.
Index terms: Adrenal gland, emission CT (ECT), 86.12161, 86.12162, 86.12163 • Fluorine, radioactive metaiodobenzylguanidine (MIBG) • Pheochromocytoma, 67.3163, 86.328
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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A variety of imaging techniques have been used to locate pheochromocytoma, each of which exhibits important drawbacks. Since approximately 90% of pheochromocytomas occur within the adrenal glands, computed tomography (CT) of the adrenal glands has been found efficacious (5,6). However, CT depicts only anatomic abnormalities. Occasional false-positive studies can lead to unnecessary surgery (7). Although CT in the past has been less accurate than other approaches for the detection of extraadrenal lesions, to our knowledge, there are no recent studies comparing the accuracy of CT with that of other imaging techniques. Magnetic resonance (MR) imaging, like CT, provides excellent anatomic detail and has the advantages of lack of ionizing radiation, the potential for better tissue characterization, and the capacity for imaging in multiple planes without the need for intravenous iodinated contrast material (8,9). The effect of new, shorter imaging sequences has yet to be determined.
The procedure of choice for the localization of pheochromocytoma is currently scintigraphy with metaiodobenzylguanidine (MIBG) (9–13). Not all pheochromocytomas concentrate MIBG, however, and MIBG uptake can be adversely affected by a variety of medications. Thus, there is a need for another procedure that has either a higher sensitivity or will at least supplement currently available techniques (14). Our preliminary experience suggests that positron emission tomography (PET) with 2-[fluorine-18]fluoro-2-deoxy-D-glucose (FDG) has promise, and we previously reported the depiction with FDG PET of two pheochromocytomas that did not accumulate MIBG (15). The purpose of this study was to estimate the sensitivity of FDG PET for pheochromocytomas and to compare findings with MIBG scintigraphy to demonstrate the complementary role of FDG PET.
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MATERIALS AND METHODS |
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Images of the tumor were acquired dynamically for 50–60 minutes (patients 1–7, 13, 15, 18, and 29). Data obtained with the dynamic sequence were reconstructed into transverse cross-sectional images by means of filtered back projection and a Hann filter with a cutoff frequency of 0.35 cycles per projection ray. From the transverse images, attenuation-corrected images were constructed in the coronal and sagittal planes. In addition, in most studies, limited "whole-body" views of the chest and abdomen were obtained to screen for metastatic disease. These views consisted of sequential acquisitions covering 40–60 cm in the z axis. The data from the whole-body acquisition were stacked in a three-dimensional volume and forward projected into images every 10° to allow viewing as a rotating cine display of 32 images.
In patients 9–13 and 15–28, images were acquired on an Exact PET scanner beginning 45 minutes after FDG injection. This device contains three rotating 68Ge rods, which allow performance of emission scanning followed by transmission scanning for attenuation correction. This method does not eliminate contamination for the emission events but does reduce its effect, and the resultant scan values do not differ by more than 5% from those corrected on the basis of standard preinjection transmission scans (17).
MIBG Scintigraphy
Iodine 131 MIBG.—In 14 patients (patients 1, 8, 13, 15, 17–21, 24, 26–29), planar scintigraphy with 131I MIBG was performed as previously described (18). In brief, overlapping anterior and posterior images from the top of the head to the knees were acquired for 100,000 counts or 20 minutes, whichever came first, at 24, 48, and 72 hours after administration of 19 MBq (0.5 mCi) or 38 MBq (1 mCi) 131I MIBG (the higher dose was administered to patients with malignant pheochromocytoma who were undergoing evaluation for possible 131I MIBG therapy). Data were acquired with a gamma camera with a large field of view and a high-energy collimator interfaced with a computer.
Iodine 123 MIBG.—In 19 patients (patients 2–7, 9–14, 16, 18, 21–23, 25, 26), 123I MIBG was used and was preferred whenever possible. After the intravenous administration of 370 MBq (10 mCi) 123I MIBG, both planar and tomographic images were obtained (19).
Planar images.—Anterior views from the head to the knees and posterior views of the chest and abdomen were obtained at 18–24 and 48 hours. Each image was acquired for 10 minutes with use of a gamma camera with a large field of view and a low-energy collimator interfaced to a computer.
Tomographic images.—Single photon emission CT (SPECT) was performed at 24 hours with use of a single or multihead rotating gamma camera with one or more low-energy collimators. The camera was rotated through 360° with 64 stops of 20 seconds each. Data were reconstructed by means of filtered back projection and a Butterworth filter with a cutoff frequency of 0.2–0.5 Nyquist.
In most patients, findings at CT (models CT/T 8800 or 9800; GE Medical Systems, Milwaukee, Wis) of the principal tumor were available for confirmation. An intravenous bolus of approximately 150 mL of ionic (Conray 60; Mallinckrodt Medical, St Louis, Mo) or nonionic (Omnipaque 300; Nycomed-Amersham, Princeton, NJ) contrast material was administered at a rate of 2 mL/sec followed by acquisition of 10-mm-thick contiguous axial sections through the thorax, abdomen, or pelvis depending on the site of the principal tumor. Both 
- and ß-adrenergic blockades were used when necessary to prevent contrast media–induced hypertensive crises.
Image Analysis
Images were reviewed by three nuclear imaging physicians (B.L.S., B.S., J.C.S.) by consensus. The images for each patient were presented in random order, with the FDG PET images of a patient analyzed immediately before the MIBG images of the same patient. Any identifying information on each image was masked. Results of other studies (eg, bone scanning, MR imaging, biochemistry) were not revealed prior to analysis of the FDG PET and MIBG images. Tumor uptake of FDG and MIBG was assessed both qualitatively and semiquantitatively.
Qualitative analysis.—Organs that normally accumulate the tracers were identified by means of visual inspection. Sites of accumulation that did not conform to the usual anatomic configurations of normal sites of radiotracer accumulation were considered abnormal. A scale was used to visually assess tumor uptake with reference to the surrounding background: 0, no uptake; 1, faint uptake less than that of the surrounding background; 2, uptake equal to that of the background; and 3, uptake greater than that of the background. FDG and MIBG images were then compared for overall quality and clarity of tumor definition, and the set of images was selected that was considered to better depict the tumors.
Semiquantitative analysis.—On images obtained 50–60 minutes after injection of FDG, regions of interest were placed over the tumor and identifiable noninvolved organs to serve as reference organs. For chest lesions, the reference organ was the lung; for abdominal lesions, the liver; and for extremity lesions, the surrounding muscle. Irregular regions of interest were constructed around the entire tumor, and a region of interest of approximately the same size was placed over the reference organs. Tumor-to–reference-organ ratios of radioactivity were calculated for those sets of images on which both the tumor and reference organ were within the attenuation-corrected field of view. Regions of interest of similar size and shape were drawn on SPECT images, and tumor-to–reference-organ ratios were calculated. Standardized uptake values (SUVs) were derived from 3 x 3-pixel regions of interest centered over areas of greatest FDG accumulation within the tumor at 50–60 minutes. Tumor-to–reference-organ ratios for planar MIBG studies were derived from the geometric mean of the tumor activity divided by the geometric mean of the reference organ uptake and for SPECT studies from regions of interest of the same size and shape as those on the PET studies.
Biochemical Characterization
At the time of FDG PET, approximately 10 mL of blood was withdrawn via an indwelling intravenous catheter after the patient lay recumbent for 20 minutes. Plasma was separated and analyzed for catecholamines by means of high-performance liquid chromatography.
The 12- or 24-hour urine was collected for analysis of catecholamines—norepinephrine and epinephrine—and catecholamine metabolites—normetanephrine and metanephrine—by means of high-performance liquid chromatography and vanillylmandelic acid by means of column extraction.
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RESULTS |
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Benign Pheochromocytomas
Qualitative analysis.—For the 12 benign tumors (Fig 1), uptake of FDG was seen in seven (58%) and of MIBG in 10 (83%). The pheochromocytomas in five of these patients accumulated both FDG and MIBG (Table 2), whereas those in the remaining seven patients accumulated either one or the other tracer but not both. The tumors that failed to accumulate MIBG avidly concentrated FDG (15). Each of the tumors that did not accumulate FDG was visualized with MIBG scintigraphy. For four of the five patients whose tumors accumulated both agents, MIBG images were ranked superior to FDG images.
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Malignant Pheochromocytomas
Findings in malignant pheochromocytomas are presented in Figures 2 –4.
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Semiquantitative analysis.—SUVs for positive FDG PET scans (n = 14 [only the initial study was used in patients examined more than once]) ranged from 1.6 to 13.3 (mean, 6.6 ± 3.4). Tumor-to–reference-organ ratios for FDG ranged from 2.0 to 17.0 (mean, 6.0 ± 3.8) and for MIBG (n = 16 [only the initial study was used in patients examined more than once]) ranged from 1.0 to 3.6 (mean, 2.2 ± 0.8).
In both benign and malignant pheochromocytomas, FDG uptake was unrelated to tumoral catecholamine production.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Semiquantitative analysis on the basis of SUVs and tumor-to–reference-organ ratios did not distinguish benign from malignant pheochromocytomas. The tumor-to–reference-organ index was calculated for FDG to allow comparison with that of MIBG, since the usually accepted quantification of FDG, the SUV, is based on very small regions of interest and may not reflect global tumor FDG uptake. Tumor-to–reference-organ SUVs for benign and malignant pheochromocytomas that accumulated FDG were in the range described for common malignant neoplasms. However, pheochromocytomas in eight (28%) of the 29 patients in this series did not show FDG uptake. SUV determinations are dependent on multiple factors, including time after injection, plasma glucose levels, recovery coefficients, and partial volume effects (20). Thus, different values might be found in different laboratories depending on the protocol and equipment used.
It is unclear why some pheochromocytomas, which appear clinically and histologically indistinct from tumors that concentrate FDG, do not concentrate the tracer. It is believed that increased glucose use by tumor cells may be due to a combination of factors—overexpression of glucose transporter proteins, elevated concentrations of hexokinase, and decreased rates of glucose-6-phosphate dephosphorylation (21–23). However, some pheochromocytomas that accumulate MIBG poorly were well visualized with FDG and all that fail to concentrate FDG were well visualized with MIBG in this study. We have yet to encounter a pheochromocytoma that cannot be localized with one tracer or the other. FDG uptake appears unrelated to the secretory status of the tumor.
There are multiple single photon and positron emitting tracers available for detecting pheochromocytoma. After the first reports of 131I MIBG scintigraphy to detect pheochromocytoma, this agent has been used widely and found effective for the localization of benign pheochromocytomas and for the localization and monitoring of malignant pheochromocytomas. This technique uses a guanethidine analogue, MIBG, and the specific catecholamine uptake transport system of tissues of the sympathetic nervous system to concentrate the radiopharmaceutical within the tumor. Whole-body screening allows the detection of both intraadrenal and extraadrenal pheochromocytomas. Although 123I MIBG is not widely available in the United States, it is commercially available in Europe and is synthesized for local use at several large academic facilities in the United States.
The principal advantage to use of 123I MIBG is in image quality (ie, images have much higher counts) and the ability to perform high-quality SPECT. Radiation dosimetry for 123I MIBG (10 mCi) is favorable, and this allows approximately 20-fold greater activity to be administered for radiation exposure similar to that with 131I MIBG (0.5 mCi) (24). In patients with disseminated neuroblastoma, more lesions may be identified with 123I MIBG than with 131I MIBG, but this does not affect staging (25). To our knowledge, comparison data are not available in patients with pheochromocytoma, but our experience suggests that only very rarely can a pheochromocytoma be visualized with 123I MIBG and not with 131I MIBG (26). Thus, we pooled the 131I MIBG and 123I MIBG data for analysis.
We previously observed approximately 12% false-negative studies with MIBG scintigraphy and reported successful localization at FDG PET of two pheochromocytomas that did not concentrate MIBG (15). These observations provided the foundation for this more extensive investigation of the uptake of FDG by pheochromocytomas regardless of their MIBG avidity. Indium 111 pentetreotide depicts most pheochromocytomas, although results with this agent are inferior to those with MIBG for localizing pheochromocytomas (27). Other positron emitting tracers of the sympathetic nervous system have been evaluated and found to be concentrated within pheochromocytomas. These are carbon 11 metahydroxyephedrine, which is a norepinephrine analogue that shows excellent and rapid localization of pheochromocytoma, and 11C epinephrine (28,29). Like MIBG, these tracers use the catecholamine uptake pathway and catecholamine storage mechanisms characteristic of neuroendocrine tumors, especially pheochromocytomas and neuroblastomas. These agents may also be subject to interference from agents that inhibit uptake of MIBG. A similar number of false-negative studies might be expected with use of these positron emitting tracers of the sympathetic nervous system, although direct comparison studies would be required for certainty.
Though most histologically benign tumors can be distinguished from malignant neoplasms at FDG PET, we found that most pheochromocytomas, whether benign or malignant, are metabolically active and thus concentrate FDG (30,31). On the other hand, a minority of either benign or malignant pheochromocytomas did not accumulate FDG, even when clinical evidence suggested growth and uptake of FDG was expected. Thus, caution is warranted against concluding that absence of uptake of FDG excludes pheochromocytoma.
FDG PET helps localize the majority of pheochromocytomas. Because its sensitivity is slightly less than that of MIBG and its specificity is considerably lower due to uptake of FDG by a variety of other neoplastic and nonneoplastic processes, FDG PET is not recommended as a first line method to localize pheochromocytomas. However, the technique is a useful adjunct to MIBG scintigraphy and is of most value in the localization of pheochromocytomas when other methods have failed.
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Acknowledgments |
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, B.L.S.; study concepts, B.L.S., J.C.S.; study design, B.L.S.; definition of intellectual content, B.L.S., J.C.S.; literature research, B.L.S., I.R.F.; clinical studies, B.L.S., J.C.S., B.S., N.W.T.; data acquisition, B.L.S., J.C.S., N.W.T.; data analysis, B.L.S., J.C.S., B.S.; statistical analysis, B.L.S.; manuscript preparation, editing, and review, all authors.
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References |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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