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Journal of Clinical Oncology, Vol 25, No 16 (June 1), 2007: pp. 2262-2269 © 2007 American Society of Clinical Oncology. DOI: 10.1200/JCO.2006.09.6297 Superiority of Fluorodeoxyglucose Positron Emission Tomography to Other Functional Imaging Techniques in the Evaluation of Metastatic SDHB-Associated Pheochromocytoma and Paraganglioma
From the Reproductive Biology and Medicine Branch, National Institutes of Child Health and Human Development; Nuclear Medicine Department; Department of Diagnostic Radiology; Clinical Neurocardiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD; Department of Internal Medicine, Division of General Internal Medicine; and the Department of Endocrinology, Radboud University Nijmegen Medical Centre, Nijmegen, the Netherlands Address reprint requests to Henri J.L.M. Timmers, MD, PhD, Reproductive Biology and Medicine Branch, National Institute of Child Health and Human Development, 10 Center Dr, Bldg 10, CRC, RM 1-E 3140, MSC 1109, Bethesda MD 20892-1109; e-mail: h.timmers{at}endo.umcn.nl
Purpose: Germline mutations of the gene encoding subunit B of the mitochondrial enzyme succinate dehydrogenase (SDHB) predispose to malignant paraganglioma (PGL). Timely and accurate localization of these aggressive tumors is critical for guiding optimal treatment. Our aim is to evaluate the performance of functional imaging modalities in the detection of metastatic lesions of SDHB-associated PGL. Patients and Methods: Sensitivities for the detection of metastases were compared between [18F]fluorodopamine ([18F]FDA) and [18F]fluoro-2-deoxy-D-glucose (FDG) positron emission tomography (PET), iodine-123- (123I) and iodine-131 (131I) -metaiodobenzylguanidine (MIBG), 111In-pentetreotide, and Tc-99m-methylene diphosphonate bone scintigraphy in 30 patients with SDHB-associated PGL. Computed tomography (CT) and magnetic resonance imaging (MRI) served as standards of reference. Results: Twenty-nine of 30 patients had metastatic lesions. In two patients, obvious metastatic lesions on functional imaging were missed by CT and MRI. Sensitivity according to patient/body region was 80%/65% for 123I-MIBG and 88%/70% for [18F]FDA-PET. False-negative results on 123I-MIBG scintigraphy and/or [18F]FDA-PET were not predicted by genotype or biochemical phenotype. [18F]FDG-PET yielded a by patient/by body region sensitivity of 100%/97%. At least 90% of regions that were false negative on 123I-MIBG scintigraphy or [18F]FDA-PET were detected by [18F]FDG-PET. In two patients, 111In-pentetreotide scintigraphy detected liver lesions that were negative on other functional imaging modalities. Sensitivities were similar before and after chemotherapy or 131I-MIBG treatment, except for a trend toward lower post- (60%/41%) versus pretreatment (80%/65%) sensitivity of 123I-MIBG scintigraphy. Conclusion: With a sensitivity approaching 100%, [18F]FDG-PET is the preferred functional imaging modality for staging and treatment monitoring of SDHB-related metastatic PGL.
Paragangliomas (PGLs) are tumors that derive from either sympathetic tissue in adrenal and extra-adrenal abdominal, intrapelvic, or thoracic locations or from parasympathetic tissue of the head and neck.1 PGLs arising from the adrenal medulla are commonly referred to as pheochromocytomas.2,3 Recently, new genes involved in the pathogenesis of familial PGL have been described.4-7 Mutations of the genes encoding the B, C, and D subunits of the mitochondrial complex II enzyme succinate dehydrogenase (SDHB, SDHC, and SDHD) result in distinct clinical syndromes.8-10 SDHB-related PGLs predominantly occur in extra-adrenal abdominal or thoracic locations and up to 70% are malignant.11 Accurate localization of metastases, which are often already present at the initial diagnosis, is critical for directing appropriate treatment. Dedifferentiation of metastatic SDHB-related PGL may make tumors invisible on imaging studies using highly specific agents, such as metaiodobenzylguanidine (MIBG) and 6-[18F]fluorodopamine ([18F]FDA).12,13 This could favor the use of 2-[18F]-fluoro-2-deoxy-D-glucose positron emission tomography ([18F]FDG-PET) scanning, which is a marker of increased glucose metabolism. The aim of this study was to evaluate the performance of functional imaging in the detection of metastatic SDHB-related PGL. Sensitivities of [18F]FDA- and [18F]FDG-PET, iodine-123- (123I) and iodine-131 (131I) -MIBG, 111In-pentetreotide, and Tc-99m-methylene diphosphonate (MDP) bone scintigraphy were compared. In patients who received chemotherapy or 131I-MIBG therapy,14,15 pre- and post-treatment results were analyzed separately in order to examine suitability of different modalities for assessing the response to treatment.
Patients Thirty unrelated patients (16 males, 14 females) with an SDHB mutation and a history of histologically proven abdominal or thoracic PGL were included in this retrospective study of imaging data. All patients were referred to the National Institutes of Health (NIH) for an outline of an optimal treatment plan for (suspected) metastatic PGL between November 2000 and May 2006. The study protocol was approved by the institutional review board of the National Institutes of Child Health and Human Development at the NIH. All patients provided written informed consent for all genetic, biochemical, and imaging studies regarding PGL. Genetic testing was performed at the Department of Human Genetics of the Pittsburgh University Medical Center as described elsewhere.16 Mean ± standard deviation (SD) age at diagnosis was 33.3 ± 15.6 years. The interval between diagnosis and referral to the NIH was 4.9 ± 8.4 years. Of 30 patients, 23 had previously undergone resection of their primary tumor and four (patients 4, 8, 12, and 29) had one or more metastasis removed. Individual patient characteristics are summarized in Table 1.
Imaging Techniques Computed tomography (CT) scans of the neck, chest, abdomen, and pelvis were performed using a variety of equipment, including LightSpeed Ultra, LightSpeed QX/i, HiSpeed CT/i, Genesis HiSpeed (General Electric Healthcare Technologies, Waukesha, WI), and Mx8000 IDT (Philips Medical Systems, Andover, MA) scanners. Section thickness was up to 3 mm in the neck, 5 mm through the chest and abdomen, and 7.5 mm through the pelvis, except for the five earliest scans, where 10 mm thick images outside the neck were used. Most studies were performed with a rapid infusion of nonionic water-soluble contrast agent, given when feasible, as well as oral contrast material. Magnetic resonance imaging (MRI) scans of the neck, chest, abdomen, and pelvis were obtained with 1.5 or 3 Tesla scanners (General Electric Healthcare Technologies and Philips Medical Systems). Phased array coils were employed for neck imaging, and either phased array torso or quadrature body coils elsewhere. T1-weighted gradient-echo, and short-tau inversion recovery and/or fat-suppressed fast spin-echo T2-weighted imaging parameters were adjusted so as to minimize examination time, while achieving desired anatomic coverage. Image thickness was 5 mm for all but two of the earlier neck studies, where 7 and 10 mm images were obtained, and generally 5 to 8 mm, but never more than 10 mm for chest, abdomen, and pelvis scans. Preinjection mages were obtained in the axial plane. All but a few studies included injection of a gadolinium-diethylenetriamine pentaacetic acid contrast agent, using fat-suppressed T1-weighted gradient-echo imaging, generally in both axial and coronal planes. For PET scanning, the patients fasted for at least 4 hours before intravenous injection of [18F]FDA (1 mCi) or [18F]FDG (15 mCi) and refrained from caffeine, tobacco, and alcohol for 12 hours. Of 40 [18F]FDA scans, 28 were performed before March 2005, using an Advance scanner (General Electric Medical Systems) with a 15-cm axial field of view. Eight-minute emission images were obtained in two-dimensional mode from the midskull to the midthigh starting 3 minutes after tracer injection. Three-minute transmission scans were obtained for attenuation correction. Twelve more recent [18F]FDA scans and all [18F]FDG scans were done using a Discovery ST PET/CT scanner (General Electric Medical Systems) with a 15-cm axial field of view. CT studies for attenuation correction and anatomic coregistration were performed without contrast, and with the following imaging parameters: 140 kVp, 90 mA, 0.8 seconds per rotation, and a slice thickness of 3.25 mm. Emission images were also obtained in two-dimensional mode from the midskull to the midthigh with 5-minute acquisition at each level, starting 60 minutes after injection. PET images were reconstructed on either a 256 x 256 or a 128 x 128 matrix using an iterative algorithm provided by the manufacturer. For whole-body 123I-MIBG and 131I-MIBG scintigrapy, patients experienced imaging 24 and occasionally 48 hours after intravenous administration of 10 mCi 123I-MIBG (32 scans) or 48 hours and occasionally 72 hours after 0.5 mCi 131I-MIBG (six scans). To protect the thyroid from accumulation of free radioactive iodine, patients received 100 mg of saturated solution of potassium iodide by mouth twice a day for 4 or 8 days with 123I- and 131I-MIBG, respectively, starting the night before MIBG administration. Both planar and single photon emission computed tomography (SPECT) images were obtained with 123I-MIBG. 111In-pentetreotide scintigraphy, including SPECT, was performed at 4 and occasionally 24 hours after injection of 6 mCi 111In-pentetreotide (10 µg; Mallinckrodt, St Louis, MO). Bone scanning was performed with 25 mCi Tc-99m-MDP (Bracco Diagnostics, New Brunswick, NJ), with a 3-hour interval between injection and scanning.
Analysis of Data
Statistics
Anatomic Imaging of Untreated Metastatic PGL Malignant PGL, defined as the presence of metastatic lesions at sites where chromaffin tissue is normally absent,17 was found in all patients except one (patient 16). Individual locations of metastases are summarized in Table 1. In two of 29 patients with evidence of metastatic disease, CT and MRI yielded false-negative results: in patient 21, multiple metastatic lesions in the abdominal para-aortic region and bone were detected by 123I-MIBG, [18F]FDA, [18F]FDG, and Tc-99m-MDP, but not by CT and MRI. In patient 3, lung, liver, and bone lesions were detected by [18F]FDA-PET but not by CT, whereas abdominal lesions were positive on CT, [18F]FDA-PET and 131I-MIBG. Because CT and MRI served as standards of reference, the regions that were negative on anatomic imaging in these two patients were excluded from the analysis. Sensitivity by patient and by region of CT (96% and 96%) was similar to that of MRI (95% and 95%). Lesions negative on CT and positive on MRI included bone metastases in two patients. Two regions (one bony and one abdominal) were negative on MRI and positive on CT.
Functional Imaging of Metastatic PGL Before Treatment
In three of 36 [18F]FDA-PET scans, a discrepancy between double readers regarding the identity or localization of a single lesion was settled by consensus. Sensitivity by patient and by region of [18F]FDA-PET was 88% and 70%, respectively (Table 2). No obvious differences in region-specific sensitivity were observed (Table 3). Maximum tumor size did not differ between [18F]FDA-PET–negative and –positive regions (3.6 ± 2.6 v 4.0 ± 2.5 cm). Of 15 [18F]FDA-PET–negative regions, one (8%) of 13 were positive on 123I-MIBG and nine (90%) of 10 were positive on [18F]FDG-PET. The highest sensitivity of functional imaging was found for [18F]FDG-PET: 100% by patient and 97% by region. Only one region (in patient 4) was found to be false negative on [18F]FDG-PET. In this patient with widespread metastatic disease, multiple hepatic lesions observed on CT, MRI, and 111In-pentetreotide [18F]FDA-PET. In contrast, additional lesions in the same patient in bone, mediastinum, and abdomen were positive on [18F]FDG-PET, but negative on [18F]FDA-PET and 123I-MIBG. 111In-pentetreotide scintigraphy yielded a sensitivity by patient and by region of 81% and 59%, respectively. Of 13 false-negative regions, six (67%) of nine were detected by 123I-MIBG, seven (58%) of 12 by [18F]FDA-PET and seven (100%) of seven by [18F]FDG-PET. In two patients (4 and 12), liver lesions were detected by 111In-pentetreotide scintigraphy that were negative on other functional imaging modalities (Fig 1). The sensitivity for detection of bone lesions by Tc-99m-MDP scintigraphy was 83%. Of nine patients in whom bony metastases were demonstrated by Tc-99m-MDP, one (17%) of six were negative for bone disease by 123I-MIBG and in two (29%) of seven by [18F]FDA, whereas [18F]FDG-PET detected bone metastases in all nine (Fig 1).
Functional Imaging of Metastatic PGL After Treatment
The detection of lesions by different functional imaging modalities was studied in 30 patients with SDHB-associated PGL, 29 of whom had metastatic disease. CT and MRI served as standards of reference. [18F]FDG-PET yielded the highest diagnostic sensitivity for the detection of metastatic lesions, approaching 100%. At least 90% of regions that were false negative on 123I-MIBG scintigraphy and [18F]FDA-PET were detected by [18F]FDG-PET. Sensitivity of functional imaging was similar before and after treatment for metastatic disease, except for lower post- versus pretreatment sensitivity of 123I-MIBG scintigraphy. Agents that specifically target the catecholamine synthesis, storage, and secretion pathway include 123I/131I-MIBG, [18F]FDA, 18F-fluorodihydroxyphenylalanine, 11C-epinephrine, and 11C-hydroxyephedrine.18 These catecholamine analogs are actively transported into neurosecretory granules of catecholamine-producing cells via the vesicular monoamine transporters after uptake into cells by the norepinephrine transporter.19 The ligands are of variable utility in the diagnosis of PGLs in various locations and other tumors like neuroblastoma and ganglioneuroma.18 123I-MIBG is preferred over 131I-MIBG because of higher sensitivity, lower radiation exposure, and improved imaging quality with SPECT.20 123I-MIBG was reported to have a sensitivity of 92% to 96%21 in patients with predominantly nonmetastatic PGL versus 57% in patients with metastatic lesions.22 [18F]FDA-PET is a promising tool for the detection of PGL.12,23 In an initial report on 16 patients with malignant PGL, [18F]FDA-PET detected lesions in all patients and showed a large number of foci that were not imaged with 131I-MIBG.24 Subsequently, however, we have observed several patients with metastatic PGL in whom [18F]FDA shows lack of accumulation, especially in cases of aggressive PGL.25 Theoretically, a loss of sensitivity of MIBG and [18F]FDA in malignant PGL may result from dedifferentiation of the tumor and concomitant loss of specific cellular characteristics, including the expression of noradrenergic transporters. Indeed, in this study, 123I-MIBG scintigraphy and [18F]FDA-PET were falsely negative in 35% and 30% of body regions with metastases, respectively. These specific functional imaging studies appear to be of limited additional value to CT and MRI in these patients. The detection of lesions by 123I-MIBG and [18F]FDA appeared to be independent of genotype and biochemical phenotype. Whether these results in SDHB-mutation carriers are applicable to metastatic PGL in general is questionable, since the expression of noradrenergic transporters may vary among different familial syndromes associated with PGL.26 In the light of limited sensitivity of specific agents, other agents that do not specifically target the catecholamine pathway like [18F]FDG may be useful in the localization of metastatic PGL. [18F]FDG accumulation in tumors is an index of increased glucose metabolism and, as a marker of tumor viability, the degree of [18F]FDG uptake usually reflects tumor aggressiveness.27 The uptake of [18F]FDG by PGL does not depend on catecholamine uptake or storage in neurosecretory granules.28 Although [18F]FDG-PET identifies only 70% of primary PGLs,13,29 this technique can be useful in localizing the primary tumor in patients with biochemical evidence of PGL but negative findings in CT, MRI, and MIBG.30 However, [18F]FDG-PET appears to be particularly useful in the localization of metastatic PGL.13,25,31 Uptake of [18F]FDG was found in a higher percentage of malignant (88%) than benign PGL (58%) lesions,13 which may be explained by a higher metabolic activity of metastatic tumors. In a recent report, we described five patients, in whom the extent of metastatic PGL was grossly underestimated by 123I-MIBG and [18F]FDA.25 In these patients [18F]FDG-PET showed lesions that other functional imaging had missed. Similarly, in this study, more than 90% of regions that were false negative on 123I-MIBG scintigraphy or [18F]FDA-PET were detected by [18F]FDG-PET. In general, lesions detected with nonspecific agents like [18F]FDG should be interpreted with care. In this study, however, all regions positive with [18F]FDG corresponded to findings that were suspicious for metastases on anatomic imaging and/or other specific functional imaging. Although tissue confirmation was largely unavailable, our findings suggest, that in this subset of patients, [18F]FDG-PET is not only highly sensitive, but also has good specificity. Somatostatin receptor imaging has a sensitivity of higher than 90% for head and neck PGL32 and may be useful for screening carriers of SDH gene mutations.8,9 In this study, all head and neck PGL were positive on 111In-pentetreotide scintigraphy, whereas regional sensitivity for metastatic thoracic or abdominal PGL was only 59%. [18F]FDG-PET is increasingly incorporated in the treatment of oncology patients.27 Changes in glucose metabolism in response to therapy detected by [18F]FDG may add relevant information to clinical and biochemical parameters and tumor size. [18F]FDG-PET is also used as a marker of high-grade and/or poorly-differentiated tumors, directing more aggressive treatment.33 Our findings of an excellent sensitivity of [18F]FDG-PET after chemotherapy, and MIBG treatment indicates that this agent is a promising tool for treatment monitoring of malignant PGL. Similarly, in the follow-up of high-risk neuroblastoma, [18F]FDG-PET was considered to be a good alternative to 123I-MIBG scintigraphy.34 Post-treatment sensitivity of 123I-MIBG appeared to be lower than before treatment, although the difference was not significant. A lower sensitivity may relate to 131I-MIBG treatment, which specifically targets tumors that express noradrenergic transporters responsible for the uptake of both diagnostic and therapeutic doses of MIBG. Ideally, histologic proof of metastatic lesions detected by imaging would serve as standard of reference. For obvious reasons, surgery or biopsy of all suspicious regions is not feasible. Not all types of functional imaging were consistently available for comparison. However, no attempt was made to select imaging studies on the basis of patient characteristics or previous imaging. A suspected positive correlation between the expression of norepinephrine transporters in paraganglioma tissue and the uptake of specific imaging agents awaits histological proof. In conclusion, widely available [18F]FDG-PET is the preferred functional imaging modality for the localization of SDHB-associated metastatic PGL, and by extension, possibly of metastatic PGL in general. For these tumors, the sensitivity of specific agents like 123I-MIBG and [18F]FDA is limited.
The authors indicated no potential conflicts of interest.
Conception and design: Henri J.L.M. Timmers, Karel Pacak Administrative support: Karen T. Adams, Daniel Solis Provision of study materials or patients: Karel Pacak Collection and assembly of data: Henri J.L.M. Timmers, Anna Kozupa, Clara C. Chen, Jorge A. Carrasquillo, Alexander Ling, Karen T. Adams, Daniel Solis, Karel Pacak Data analysis and interpretation: Henri J.L.M. Timmers, Clara C. Chen, Jorge A. Carrasquillo, Alexander Ling, Graeme Eisenhofer, Jacques W.M. Lenders, Karel Pacak Manuscript writing: Henri J.L.M. Timmers, Anna Kozupa, Clara C. Chen, Jorge A. Carrasquillo, Alexander Ling, Graeme Eisenhofer, Jacques W.M. Lenders, Karel Pacak Final approval of manuscript: Henri J.L.M. Timmers, Anna Kozupa, Clara C. Chen, Jorge A. Carrasquillo, Alexander Ling, Graeme Eisenhofer, Karen T. Adams, Daniel Solis, Jacques W.M. Lenders, Karel Pacak
Robert Wesley, PhD, is acknowledged for his advice on the statistical analysis. This research was supported by the Intramural Research Program of the National Institute of Child Health and Human Development/National Institutes of Health.
Supported by the Intramural Research Program of the National Institute of Child Health and Human Development/National Institutes of Health. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Pacak K, Goldstein DS, Doppman JL, et al: A "pheo" lurks: Novel approaches for locating occult pheochromocytoma. J Clin Endocrinol Metab 86:3641-3646, 2001 24. Ilias I, Yu J, Carrasquillo JA, et al: Superiority of 6-[18F]-fluorodopamine positron emission tomography versus [131I]-metaiodobenzylguanidine scintigraphy in the localization of metastatic pheochromocytoma. J Clin Endocrinol Metab 88:4083-4087, 2003 25. Mamede M, Carrasquillo JA, Chen CC, et al: Discordant localization of 2-[18F]-fluoro-2-deoxy-D-glucose in 6-[18F]-fluorodopamine- and [(123)I]-metaiodobenzylguanidine-negative metastatic pheochromocytoma sites. Nucl Med Commun 27:31-36, 2006[CrossRef][Medline] 26. Huynh TT, Pacak K, Brouwers FM, et al: Different expression of catecholamine transporters in phaeochromocytomas from patients with von Hippel-Lindau syndrome and multiple endocrine neoplasia type 2. Eur J Endocrinol 153:551-563, 2005 27. 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Taniguchi K, Ishizu K, Torizuka T, et al: Metastases of predominantly dopamine-secreting phaeochromocytoma that did not accumulate meta-iodobenzylguanidine: Imaging with whole body positron emission tomography using 18F-labelled deoxyglucose. Eur J Surg 167:866-870, 2001[CrossRef][Medline] 32. Kwekkeboom DJ, van Urk H, Pauw BK, et al: Octreotide scintigraphy for the detection of paragangliomas. J Nucl Med 34:873-878, 1993 33. Cachin F, Prince HM, Hogg A, et al: Powerful prognostic stratification by [18F]fluorodeoxyglucose positron emission tomography in patients with metastatic breast cancer treated with high-dose chemotherapy. J Clin Oncol 24:3026-3031, 2006 34. Kushner BH, Yeung HW, Larson SM, et al: Extending positron emission tomography scan utility to high-risk neuroblastoma: Fluorine-18 fluorodeoxyglucose positron emission tomography as sole imaging modality in follow-up of patients. J Clin Oncol 19:3397-3405, 2001 Submitted October 20, 2006; accepted March 14, 2007. 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Copyright © 2007 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
