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Nuclear Medicine |
1 From the Department of Radiology, Divisions of Nuclear Medicine (S.H., E.M., E.N.) and Diagnostic Radiology (C.A., N.G.), Department of Pathology (G.K.), and Department of Internal Medicine, Division of Hemato-oncology (C.F.W.), Albert-Ludwigs University, Hugstetterstrasse 55, 79106 Freiburg, Germany; and the Department of Gastroenterology, University Hospital Benjamin Franklin, Free University Berlin, Germany (H.S.). Received August 25, 2000; revision requested October 17; revision received December 21; accepted February 12, 2001. Address correspondence to S.H.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: After evaluation of the normal distribution of 18F dopa, 17 patients with histologically confirmed tumors were examined with 18F dopa PET. Results of 2-[fluorine 18]fluoro-2-deoxy-D-glucose (FDG) PET, somatostatin-receptor scintigraphy, and morphologic imaging (computed tomography and/or magnetic resonance imaging) were available for all patients. Results of the procedures were evaluated by two radiologists and two nuclear medicine specialists, whose consensus based on all available histologic, imaging, and follow-up findings was used as the reference standard.
RESULTS: Ninety-two tumors were diagnosed: eight primary tumors, 47 lymph node metastases, and 37 organ metastases. 18F dopa PET led to 60 true-positive findings (seven primary tumors, 41 lymph node metastases, 12 organ metastases); FDG PET, 27 (two primary tumors, 14 lymph node metastases, 11 organ metastases); somatostatin-receptor scintigraphy, 52 (four primary tumors, 27 lymph node metastases, 21 organ metastases); and morphologic imaging, 67 (two primary tumors, 29 lymph node metastases, 36 organ metastases). This resulted in the following overall sensitivities: 18F dopa PET, 65% (60 of 92); FDG PET, 29% (27 of 92); somatostatin-receptor scintigraphy, 57% (52 of 92); morphologic procedures, 73% (67 of 92). Although the morphologic procedures were most sensitive for organ metastases, 18F dopa PET enabled best localization of primary tumors and lymph node staging.
CONCLUSION: 18F dopa PET is a promising procedure and useful supplement to morphologic methods in diagnostic imaging of gastrointestinal carcinoid tumors.
Index terms: Carcinoid, 70.316 • Fluorine, radioactive • Gastrointestinal tract, CT, 70.12112, 70.12115 • Gastrointestinal tract, MR, 70.121411, 70.121412 • Gastrointestinal tract, neoplasms, 70.316 • Gastrointestinal tract, PET, 70.12163 • Gastrointestinal tract, SPECT, 70.12162
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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A widespread characteristic of these tumors is the uptake and metabolization of amino acids, which resulted in the term amine precursor uptake and decarboxylation, or APUD, system being used to denote the diffuse neuroendocrine system (14). This property of taking up amino acids, transforming them into biogenic amines by means of decarboxylation, and storing them in vesicles was already used for imaging of neuroendocrine pancreatic tumors with carbon 11 (11C) dopa (3,4-dihydroxyphenylalanine) positron emission tomography (PET) (15,16). In addition, there is a single case report on the successful use of fluorine 18 (18F) dopa PET for staging a metastasizing carcinoid tumor (17). PET offers the highest resolution among the functional methods, and the use of 18F dopa, such as 2-[fluorine 18]fluoro-2-deoxy-D-glucose (FDG), enables performance of whole-body examinations in one session.
The purpose of the present study was to evaluate 18F dopa whole-body PET in comparison with established imaging procedures in gastrointestinal carcinoid tumors.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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None of the patients presented with clinical symptoms of carcinoid syndrome. Urinary 5-hydroxyindoleacetic acid was moderately elevated in two patients. In all patients, the carcinoid tumor was found unexpectedly during surgical, endoscopic, or imaging procedures. On the basis of the unexpected finding, imaging procedures were used for staging after surgical resection of the primary tumor in seven cases: three appendiceal tumors (2.2-cm diameter, 2.0-cm diameter with solitary lymph node metastasis, and 1.7-cm diameter with infiltration of the mesoappendix), two ileal tumors, one colonic tumor within an intestinal polyp, and one rectal tumor. In the remaining 10 patients, no previous surgery had been performed. After staging in all patients, surgery was performed in six; no surgery was performed in the other 11 patients.
In all patients, results of morphologic imaging (CT and/or MR imaging), somatostatin-receptor scintigraphy, and FDG PET were available as part of clinical routine staging. All of the imaging procedures were performed within a maximum of 6 weeks after the tumor was found.
Histologic and Immunohistochemical Findings
Carcinoid tumors were diagnosed on the basis of the histologic findings and additional immunohistochemical tests in which the expression of neuroendocrine tumor markers such as synaptophysin, neuron-specific enolase, or chromogranin was examined. According to recent classifications, all cases were malignant carcinoid tumors that were subdivided into categories of high, moderate, or low differentiation (13,18). All preparations were tested by using standard immunohistochemical procedures for serotonin expression. Histologic and immunohistochemical examinations were performed by one pathologist (G.K.) blinded to the imaging findings.
FDG and 18F Dopa PET
All patients fasted for 12 hours prior to the start of the examination to provide optimal conditions for uptake of the radiopharmaceuticals. Blood glucose levels were controlled in all patients for the FDG PET; none was greater than normal (110 mg/dL [6.1 mmol/L]). For FDG PET, 360 MBq ± 30 of FDG was injected intravenously; for 18F dopa PET, 200 MBq ± 30 of 18F dopa was injected intravenously. Both radiopharmaceuticals were produced by using standard procedures (19,20). The uptake time was 90 minutes for FDG to attain optimization of the tumor-to-background ratio. For 18F dopa, the uptake time was 60–90 minutes, which is analogous to the uptake time for brain examinations (21). Data were acquired with a two-dimensional ring scanner (Ecat Exact; Siemens/CTI, Knoxville, Tenn) with a rod source by using postinjection segmented attenuation correction. Eight to 10 bed positions with an 11-cm transverse field of view were measured (2 minutes transmission and 8 minutes emission per position). Images were reconstructed by means of an iterative procedure with ordered subsets (ordered subset-expectation maximization, or OSEM, two iterations, eight subsets) (22), no pre- or postfiltering was used, and final reconstruction resolution of the images was 6 mm.
Comparison with Control Group
The study group was compared with a control group to determine normal distribution of 18F dopa in the body. The control group consisted of five consecutive patients (three men, two women; age range, 42–73 years; mean age, 57 years) in whom an examination with 18F dopa was clinically indicated for Parkinson disease. None of the control subjects had malignant disease.
Somatostatin-Receptor Scintigraphy
After intravenous injection of 170 MBq ± 25 of indium 111 pentetreotide (OctreoScan; Mallinckrodt, Petten, the Netherlands), planar scintigrams were obtained with a large-field-of-view gamma camera (Bodyscan; Siemens, Erlangen, Germany) and a medium-energy collimator. Four hours and 24 hours after injection, ventral and dorsal whole-body images were acquired, and target images of the abdomen and thorax were also obtained. The SPECT examination of the thorax and abdomen was performed 24 hours after injection by using a triple-headed camera (Prism XP 3000; Picker Marconi, Cleveland, Ohio) with the following parameters: 128 x 128 matrix, 120 projections in 3° angle increments, and 40-second acquisition time per projection. Images were reconstructed by using filtered back-projection: no prefiltering, reconstruction with ramp filter, and postprocessing with a low-pass filter with a cutoff frequency corresponding to a 5% noise level, order of five.
Interpretation of the PET Images and Somatostatin-Receptor Scintigrams
The reconstructed images were assessed by two nuclear medicine specialists (S.H., E.N.) on a standard computer monitor (Sun Microsystems, San Diego, Calif) at all three levels (transverse, coronal, and sagittal views) by using an inverse gray scale. Somatostatin-receptor scintigrams and FDG and 18F dopa PET scans in each patient were interpreted at different times, with the readers blinded to the results of the other studies. Images were interpreted by means of consensus of the two nuclear medicine specialists; there were no discrepancies. Any focal tracer accumulation exceeding normal regional tracer uptake was rated as a pathologic finding—a tumor. These pathologic findings were classified as primary tumors (lesion within the intestine), lymph node metastases (tracer accumulations in regional and distant lymph nodes), and organ metastases (pathologic uptake in parenchymatous organs such as the liver or lungs). Intestinal uptake that was linearly and nonfocally limited was rated as a nonspecific nonpathologic finding.
Morphologic Imaging
Morphologic imaging was performed according to standard protocols. Abdominal CT and/or MR images were available for all patients; additional thoracic CT examinations were performed in all patients with proved abdominal tumors to detect potential tumors in the thorax. Since the decision whether to use CT and/or MR imaging was made within the clinical routine independent of this study, it can be considered randomized: There were nine patients with abdominal CT scans, six patients with abdominal MR images, and two with both.
CT examinations were performed with two scanners (Somatom Plus 4 or Somatom Plus S; Siemens). Abdominal helical CT was performed with 70–120 mL of intravenously administered iopromide (Ultravist 300; Schering, Berlin, Germany) and included the portal venous phase. In addition, the gastrointestinal tract was imaged after oral administration of diluted diatrizoate meglumine (Gastrografin; Schering). Collimation was set to 8 or 10 mm at a table feed of 12 or 15 mm; the reconstruction interval was 8 or 10 mm. For thoracic helical CT, 70–100 mL of iopromide was administered intravenously, and the following scanning parameters were used: collimation of 8 or 10 mm, table feed of 12 or 15 mm, and reconstruction interval of 8 or 10 mm.
Static abdominal MR images were acquired with 1.5-T imagers (Magnetom Vision or Magnetom Symphony; Siemens) by using a body coil or body phased-array coil for signal reception. The upper abdomen was imaged during a single breath hold by using nonenhanced T2-weighted turbo spin-echo sequences (2,800–3,200/120–138 [repetition time msec/echo time msec]), nonenhanced T1-weighted gradient-echo sequences (fast low angle shot, 87–148/4.0–4.8, 70° flip angle), and gadolinium-enhanced T1-weighted gradient-echo sequences after spectral fat saturation (104–168/4.0–4.8). The standard dose of 0.1 mmol of gadopentetate dimeglumine (Magnevist; Schering) per kilogram of body weight was administered intravenously. Pelvic MR imaging with a phased-array coil and abdominal MR imaging with a body coil were performed without breath hold. T2-weighted turbo spin-echo sequences (4,700/120–138) and nonenhanced and gadolinium-enhanced T1-weighted spin-echo sequences (500–750/12–15) were used. The section thickness was 6–8 mm for all sequences.
Interpretation of Morphologic Images
Images were interpreted by two radiologists (C.A., N.G.) blinded to the results of the scintigraphic and PET examinations. If CT and MR imaging had been performed in the same patient, both examinations were assessed at the same time. Images were interpreted by means of consensus of the two radiologists. Every contrast medium–enhancing tumor within the walls of the hollow organs of the gastrointestinal tract was rated as a primary tumor. Lesions within parenchymatous organs were rated as organ metastases if they were not clearly identified as benign lesions (eg, cystic lesions or hemangiomas) according to standard criteria (attenuation or signal intensity and enhancement pattern after administration of contrast medium). Lymph nodes were staged morphologically according to the standard criterion of nodal diameter. Lymph nodes with a diameter as large as 1 cm were rated as tumor free, and lymph nodes with a diameter of more than 1 cm in the longest axis were rated as lymph node metastases (5,6,23). No other lymph node criteria were assessed.
Data Evaluation
Since not all lesions could be histologically proved and the different imaging modalities frequently showed discrepancies, the results of the individual imaging procedures were evaluated as follows. The results of the individual procedures were interpreted by the two radiologists and the two nuclear medicine specialists without knowledge of clinical data or other findings, as described earlier. For further data evaluation, a committee consisting of the two radiologists and the two nuclear medicine specialists achieved a consensual diagnosis regarding the presence of tumor and the number and localization of tumors in each patient.
This consensus, serving as the reference standard against which the results of the individual procedures were measured, was based on histologic findings in surgical specimens in 31 lesions or the results of all of the imaging procedures, with inclusion of serial follow-up morphologic imaging, in 61 lesions. On the basis of these data, no discrepancies between radiologists and nuclear medicine specialists were observed. All lesions detected solely by means of 18F dopa PET were accepted for the reference standard only on condition that the specific lesion was histologically verified or that a correlate in morphologic imaging was present initially or disclosed at follow-up examinations (eg, a lymph node initially not fulfilling the morphologic criterion of malignancy [<1 cm] but showing 18F dopa accumulation and increasing size at follow-up examinations). This consensus procedure resulted in a set of data for each patient with respect to primary tumor, lymph node status, and organ metastases. Sensitivity and specificity of the individual procedures were calculated from these data.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Table 3 shows the sensitivities of the individual procedures calculated on the basis of the applied reference standard, which cannot yet be considered optimal (see Discussion). Since all of the procedures led to only isolated false-positive results that were confirmed with histologic or follow-up findings, specificity was greater than 90% for all of the imaging methods.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Although morphologic imaging procedures showed the greatest sensitivity with respect to the total number of tumors, it was again confirmed that localization of primary tumor and lymph node staging are not satisfactory. The reasons for this may lie in the fact that primary tumors are often small and situated in the walls of hollow organs (1,13). The weakness of morphologic lymph node staging is the known lack of reliable criteria, since assessment can be made only on the basis of size (5,6,23). Owing to this uncertainty, the size limits vary slightly, and some examiners use the longest lymph node axis, whereas others use the shortest axis.
Because of the disadvantages cited, several functional imaging procedures such as metaiodobenzylguanidine scintigraphy and somatostatin-receptor scintigraphy have been developed (7,8), and somatostatin-receptor scintigraphy is currently the nuclear medical procedure of choice (10). Sensitivities of 44%–84% (cumulative sensitivity, 70%) have been reported for metaiodobenzylguanidine scintigraphy, and sensitivities of 71%–100% (cumulative sensitivity, 86%) have been reported for somatostatin-receptor scintigraphy (10). On the basis of these results alone, the procedures cannot be considered optimal.
Since small tumors (<1 cm) were frequently not imaged at somatostatin-receptor scintigraphy in the present study and even larger tumors showed no somatostatin-receptor expression in many cases, the results for somatostatin-receptor scintigraphy in this study (overall sensitivity, 57%) were even lower than those in the literature (9,10). This is probably because the sensitivity of somatostatin-receptor scintigraphy was frequently determined by means of comparison with morphologic imaging, which is limited, as discussed earlier. If only the established imaging procedures had been compared in the present study, all lesions detected solely by means of 18F dopa PET would not have been detected (n = 22). This would have resulted in a sensitivity of 74% (52 of 70) for somatostatin-receptor scintigraphy, which is within the range of previously published data (10).
The main advantage of lymph node staging with 18F dopa PET is that, particularly in serotonin-expressing carcinoid tumors (patients 1, 3, and 14 in Table 1), the benign or malignant nature of even small lymph nodes (<1 cm) can be classified. These nodes are hardly detectable at planar or SPECT imaging and are not unequivocally assessable at morphologic imaging. This sensitive detection of small tumors leads to an improvement of the reference standard, which is identical to the verified 18F dopa PET findings in some patients. Despite this advanced reference standard, criticism of several points is appropriate. The sensitivity of 100% (47 of 47) for lymph node staging in the combination of 18F dopa PET and morphologic imaging is not a realistic value, and it is only because all lymph node metastases negative at 18F dopa PET had a diameter considerably greater than 1 cm. However, it is plausible or even probable that individual lymph node metastases showed no 18F dopa accumulation and also were not enlarged. Since the other functional methods also did not show additional lymph node metastases, and surgical exploration with histologic analysis was not possible in a majority of cases, such findings would not have been detected.
Little experience has been gained thus far with respect to PET of neuroendocrine tumors. To date, FDG, 11C hydroxytryptophan, and 11C dopa have been used as radiopharmaceuticals (15,24,25).
Although 18F dopa has been used thus far almost exclusively for brain examinations (21,26), it also enables whole-body examinations for neuroendocrine tumors such as carcinoid tumors (17). However, similar to 11C dopa uptake (15), there is a considerable variability in tracer uptake. This variability can be explained with the heterogeneous nature of neuroendocrine gastrointestinal tumors, which present considerable differences in biologic, histologic, and clinical characteristics. The variation ranges from classic highly differentiated carcinoid tumors to poorly differentiated neuroendocrine carcinomas (small cell carcinomas) (13). Because of this heterogeneity, there are various classifications that differ in a number of criteria (18). Among these criteria are the silver affinity, histologic growth pattern, localization of the primary tumor, tumor diameter, metastasis, and hormone production. In the current study, the tumors were classified only according to biologic behavior (benign or malignant), degree of differentiation, and serotonin expression.
Comparison with the histologic and immunohistochemical findings shows that serotonin-expressing tumors especially take up 18F dopa. Immunohistochemically, general neuroendocrine tumor markers such as the neuron-specific enolase, synaptophysin, and chromogranin, and the cell-specific markers such as peptide hormones and biogenic amines (dopamine, serotonin), can be differentiated (1,27). Because 11C dopa is decarboxylated in pancreatic tumors (16), the uptake mechanism is attributed to the long-known fact that neuroendocrine tumors are capable of taking up amino acids, transforming them by means of decarboxylation to biogenic amines, and then storing them in vesicles (14). This gives rise to the hypothesis that only amine-producing tumors can be imaged with 18F dopa PET. However, this hypothesis has to be proved in further studies.
In a majority of cases, the tumors are of high and moderate differentiation, so they are difficult to image with FDG PET because of slow growth and largely normal glucose metabolism (24). This phenomenon was demonstrated especially in lymphomas and in differentiated thyroid carcinomas, which lose their capacity to store radioiodine with increasing malignancy and undifferentiation, whereas glycolysis and thus FDG storage increase at the same time (28,29). The poor results of FDG PET in the present study can be explained with this hypothesis.
Potential limitations of 18F dopa PET are the substantial physiologic uptake in the duodenum and pancreas, which might mask tumors in these sites, and the unspecific accumulations within the intestine, which might lead to false-positive results.
Despite the promising results of 18F dopa PET, no basic recommendations to replace the established somatostatin-receptor scintigraphy with 18F dopa PET can be made. Rather, somatostatin-receptor scintigraphy will retain its validity, since apparently some carcinoid tumors manifest with somatostatin-receptor expression but do not take up 18F dopa. Moreover, somatostatin-receptor expression is frequently tested if somatostatin analogues, for which both nonradioactive substances and substances emitting ß radiation are available, are used palliatively (30,31).
Since both 18F dopa PET and somatostatin-receptor scintigraphy are expensive procedures and cost is increasingly important, routine use of both procedures in combination with morphologic imaging procedures cannot be realized in all cases. However, additional use of 18F dopa PET appears reasonable as part of staging when there is an immunohistochemical finding from a tumor with serotonin expression. In the current study, the results of 18F dopa PET had an important influence on further therapy in nearly one-third of the patients. A savings potential arises thanks to improved coordination of therapeutic measures with the individual tumor spread. On the one hand, unnecessary surgery, which is stressful for the patient, is avoided; on the other hand, the localization of the primary tumor can support potentially curative surgical therapy when there is little or no metastasis. This is especially important in the case of carcinoid tumors, since complete resection is the only potentially curative therapeutic approach (1,32) and should thus lead to a reduction in cost later.
Basic limitations of this study were that the number of patients was small and that the diagnostic imaging procedures were performed only after the initial surgery in some patients. This situation was unavoidable because of unexpected intraoperative findings. Moreover, only one-third of the lesions could be verified histologically, which would have been the only real reference standard. This limitation results in a certain unreliability of all statistical values calculated in this study. However, this weakness was unavoidable because in a majority of patients, postoperative staging either brought no evidence of additional tumors or surprisingly numerous tumors were diagnosed, which made surgical therapy with histologic assessment impossible.
In conclusion, 18F dopa PET is a promising imaging procedure and useful supplement to morphologic imaging methods, since it improves localization of primary tumors and lymph node staging of gastrointestinal carcinoid tumors.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, S.H., E.N.; study concepts, S.H., E.N., E.M.; study design, S.H., E.N., C.F.W.; literature research, S.H., H.S., C.F.W.; clinical studies, S.H., E.N., C.A., N.G., G.K., C.F.W.; data acquisition, S.H., E.N., C.A., N.G., G.K.; data analysis/interpretation, S.H., E.N., C.A., N.G., C.F.W.; manuscript preparation, S.H., E.N.; manuscript definition of intellectual content, all authors; manuscript editing, S.H., E.N.; manuscript revision/review and final version approval, all authors.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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 K. Pacak, G. Eisenhofer, and D. S. Goldstein Functional Imaging of Endocrine Tumors: Role of Positron Emission Tomography Endocr. Rev., August 1, 2004; 25(4): 568 - 580. [Abstract] [Full Text] [PDF]
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A. Becherer, M. Szabo, G. Karanikas, P. Wunderbaldinger, P. Angelberger, M. Raderer, A. Kurtaran, R. Dudczak, and K. Kletter Imaging of Advanced Neuroendocrine Tumors with 18F-FDOPA PET J. Nucl. Med., July 1, 2004; 45(7): 1161 - 1167. [Abstract] [Full Text] [PDF]
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 K. M. Horton, I. Kamel, L. Hofmann, and E. K. Fishman Carcinoid Tumors of the Small Bowel: A Multitechnique Imaging Approach Am. J. Roentgenol., March 1, 2004; 182(3): 559 - 567. [Full Text] [PDF]
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S. Hoegerle, E. Nitzsche, C. Altehoefer, N. Ghanem, T. Manz, I. Brink, M. Reincke, E. Moser, and H. P. H. Neumann Pheochromocytomas: Detection with 18F DOPA Whole-Body PET3Initial Results Radiology, February 1, 2002; 222(2): 507 - 512. [Abstract] [Full Text] [PDF]
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