Original Article
Somatostatin-Receptor Imaging in the Localization of Endocrine Tumors
N Engl J Med 1990; 323:1246-1249November 1, 1990
- Abstract
- Abstract
Background and Methods.
A number of different tumors have receptors for somatostatin. We evaluated the efficacy of scanning with 123l-labeled Tyr3octreotide, a somatostatin analogue, for tumor localization in 42 patients with carcinoid tumors, pancreatic endocrine tumors, or paragangliomas. We then evaluated the response to octreotide therapy in some of these patients.
Results.
Primary tumors or métastases, often previously unrecognized, were visualized in 12 of 13 patients with carcinoid tumors and in 7 of 9 patients with pancreatic endocrine tumors. The endocrine symptoms of these patients responded well to therapy with octreotide. Among 20 patients with paragangliomas, 8 of whom had more than one tumor, 10 temporal (tympanic or jugular), 9 carotid, and 10 vagal tumors could be visualized. One small tympanic tumor and one small carotid tumor were not seen on the scan.
Conclusions.
The 123I-labeled Tyr3-octreotide scanning technique is a rapid and safe procedure for the visualization of some tumors with somatostatin receptors. A positive scan may predict the ability of octreotide therapy to control symptoms of hormonal hypersecretion. (N Engl J Med 1990; 323:1246–9.)
Media in This Article
Figure 1
Primary Tumor and Metastases in a Patient with Metastatic Carcinoid Disease.Figure 2
Gamma-Camera Picture Four Hours after the Administration of 123I-Labeled Tyr3-Octreotide in a Patient with Multiple Paragangliomas, Showing Bilateral Carotid Paragangliomas and One Vagal Paraganglioma (Anterior View).Article Activity
- Article
LARGE numbers of high-affinity somatostatin binding sites have been found on most pancreatic endocrine tumors and carcinoid tumors.1 2 3 4 In the majority of patients with such tumors, long-term therapy with octreotide successfully controls clinical symptoms, apparently through the somatostatin receptor—mediated inhibition of hormone release.5 6 7
We recently described the visualization of such tumors in vivo after the intravenous administration of a somatostatin analogue labeled with iodine-123.8 In this study we describe the results of this scanning procedure in 42 patients with known endocrine tumors.
Methods
Patients
We studied 13 patients with metastatic carcinoid disease (9 men and 4 women; mean age, 61 years [range, 24 to 78]). All 13 patients had histologically confirmed metastatic carcinoid disease. In seven patients the primary carcinoid tumor, which was in the gut in all seven, had been removed. The results of the scanning procedure in one of these patients have been described elsewhere.8 In addition, we studied nine patients with pancreatic endocrine tumors (four men and five women; mean age, 62 years [range, 45 to 81]). In all nine patients the diagnosis was histologically confirmed after the removal of the primary tumor; in seven of them preoperative hormonal examinations suggested the presence of the tumor. In both the patients with metastatic carcinoid disease and those with pancreatic endocrine tumors, the spread of the disease had been investigated by CT scanning of the abdomen and ultrasonography. In five of the patients the results of scanning with 123I-labeled Tyr3-octreotide have been described elsewhere.8 , 9 Twenty patients with paragangliomas (10 men and 10 women; mean age, 51 years [range, 16 to 83]) were also studied. In all of them the presence of at least one paraganglioma was suspected, because of earlier arteriography. AH the patients gave informed consent to participate in the study, which was approved by the ethics committee of our hospital.
Materials
The somatostatin analogues octreotide (Sandostatin, SMS 201–995) and Tyr3-octreotide (204–090) were obtained from Sandoz (Basel, Switzerland). The Tyr3-octreotide was labeled with 123I with use of chloramine-T.10 As a final preparatory step the radiopharmaceutical agent was passed through a low protein—binding 0.22-μm Millex-GV filter (Millipore, Milford, Mass.) in order to sterilize it. Depending on the results of the labeling procedure, the interval between injection and scintigraphy, and whether single-photon-emission CT (SPECT) was also performed, the doses of 123I-labeled Tyr3-octreotide ranged from 37 to 555 MBq, given as a bolus intravenous injection.8 There were no side effects of the administration of 123I-labeled Tyr3-octreotide.
Scanning
Planar and SPECT images were obtained with a large-field-of-view gamma camera (Counterbalance 3700, Siemens Gammasonics, Erlangen, Germany) equipped with a 190-KeV parallel-hole collimator. Generally, the field of view when the Tyr3-octreotide was injected covered the abdomen and some of the thorax. Starting at the time of the injection, digital images were recorded with a Gamma-II computer (Nuclear Diagnostics, Uppsala, Sweden) every 3 seconds for 2 minutes, then every 60 seconds for 28 minutes. In this 30-minute period analogue images were also obtained regularly. Thirty minutes after the injection, the patients underwent anterior and posterior whole-body static scintigraphy and, if indicated, SPECT. Static images, both analogue and digital, were obtained about 30 minutes and 2, 4, 24, and sometimes 48 hours after injection. Subtraction scintigraphy with albumin microcolloid labeled with technetium-99m (56 MBq; Albu-Res, Solco, Birsfelden, Switzerland) was performed in normal liver tissue.
We used a simple yes-or-no system to define the tumors as visualized during this scanning procedure, but always at a time when the surrounding organs were virtually devoid of radioactivity. Depending on the type and location of the tumor we chose different standard times and techniques of visualization. The best time for obtaining optimal gamma-camera pictures, as well as SPECT scans, is discussed below.
Results
Patients with Carcinoid Tumors
Among the patients with metastatic carcinoid disease, 10 had undergone surgery and in 7 the primary carcinoid tumor had been removed. In the six whose primary carcinoid tumors had not been removed, the tumor was visualized; in all six the primary tumor was located in the small intestine. In 11 of the 13 patients liver metastases were detected; in 1 patient only peritoneal metastases were visualized, and in 1 no uptake of 123I-labeled Tyr3-octreotide was seen. The best gamma-camera pictures showing the metastases were obtained within 2 minutes after the injection of the isotope (when normal liver tissue had not yet been fully visualized) or after 24 to 48 hours (when the normal liver, gallbladder, and bile ducts no longer contained appreciable amounts of radioactivity). The 123I-labeled Tyr3-octreotide liver scan and the 99mTc-labeled colloid scan of one of these patients are shown in Figures 1Figure 1
Primary Tumor and Metastases in a Patient with Metastatic Carcinoid Disease.A and 1B. The tumor tissue visualized in the Tyr3-octreotide scan was localized mainly in the right lobe of the liver (Fig. 1A), whereas the 99mTc-labeled colloid was localized mainly in the left lobe (Fig. 1B). The two scans show a greatly enlarged liver. Extrahepatic metastases (Fig. 1C) were found in lymph nodes on the left side of the neck in seven patients, and in bone (ribs, vertebrae, skull, or pelvis) in eight; in five there was evidence of peritoneal or intraabdominal metastases (or both). None of the 13 patients were known on the basis of symptoms, physical examination, or other imaging studies to have such extensive disease. In particular, the lymph nodes containing tumor in the left side of the neck had been detected on physical examination in only two of the patients who had abnormal scans in this region, but they were palpated in three other patients after the results of the Tyr3-octreotide scan were known. In the first four patients studied, the presence of carcinoid-tumor tissue in the lymph nodes in the neck, liver, or both and in the peritoneum was confirmed by needle biopsy. The one patient with no abnormality on the Tyr3-octreotide scan had extensive carcinoid tumor in the liver, abdomen, and thorax.All 13 patients were subsequently treated with octreotide, given subcutaneously in divided doses varying from 150 to 600 μg per day. In 10 of the 11 patients who had episodes of flushing, the number per day decreased by 50 percent or more; in 8 of the 9 who had diarrhea, it decreased by 50 percent or more; and in all 4 with abdominal or bone pain (or both) the pain virtually disappeared. After three days of octreotide therapy, urinary excretion of 5-hydroxyindoleacetic acid decreased by 22 to 85 percent (mean, 36) in the six patients in whom it was measured. The patient whose carcinoid tumor was not visualized with 123I-labeled Tyr3-octreotide had no decrease in flushing episodes and diarrhea during two weeks of therapy with octreotide in doses of up to 1500 μg per day.
Patients with Pancreatic Endocrine Tumors
In seven patients with pancreatic endocrine tumors, the primary tumors were visualized after the injection of 123I-labeled Tyr3-octreotide. Three patients had gastrinomas, two insulinomas, one a somatostatinoma, and one an undifferentiated endocrine pancreatic tumor. The size of the primary tumors in these patients ranged from 2 to 14 cm in diameter. Metastases were visualized in four of the seven patients. In none of these four patients had the metastases (in lymph nodes in the neck in two, bone in one, and liver in two) been detected earlier. In five patients a single subcutaneous dose of 50 μg of octreotide substantially decreased the secretion of hormone by the tumor from two to six hours after administration. In the patient with an undifferentiated endocrine pancreatic tumor in whom no hormonal hypersecretion was detected, long-term therapy with octreotide (300 μg a day for six months) resulted in a decrease in upper abdominal pain, but no change in tumor size as evaluated by CT scanning. In four of the patients with positive scans, in vitro autoradiography confirmed the presence of large numbers of high-affinity 123I-labeled Tyr3-octreotide binding sites. In two patients the tumors were not visualized after the administration of Tyr3-octreotide. Both patients had an insulinoma, and neither tumor bound any 125I-labeled Tyr3-octreotide in vitro.
Patients with Paragangliomas
In all 20 patients with paragangliomas, the tumors were visualized after the administration of 123I-labeled Tyr3-octreotide. Ten of the 11 temporal tumors (tympanic or jugular), 9 of the 10 carotid tumors, and all 10 vagal tumors were visualized (Fig. 2Figure 2
Gamma-Camera Picture Four Hours after the Administration of 123I-Labeled Tyr3-Octreotide in a Patient with Multiple Paragangliomas, Showing Bilateral Carotid Paragangliomas and One Vagal Paraganglioma (Anterior View).). Two tumors were not visualized in these 20 patients; one patient had a small (less than 5 mm) tympanic-nerve paraganglioma, and another patient had a small (3 mm) carotid tumor. Eight patients had more than one tumor deposit. The smallest tumors visualized were about 1 cm in diameter. The specificity of our findings was confirmed by pathological examination of the tumors in 15 patients and by arteriography, CT, or both in the other 5.Discussion
Octreotide is currently used to treat patients with metastatic carcinoid and pancreatic endocrine tumors.5 6 7 Its administration results in a remarkable improvement in the clinical condition of most patients, mainly through the suppression of hormonal hypersecretion. We have previously found that most such tumors, especially those in patients with a good response to octreotide therapy, contain large numbers of octreotide receptors.1 2 3 4 The relative affinity of the somatostatin receptors on most human tumors for natural somatostatin-14, its precursor somatostatin-28, and Tyr3-octreotide varies; in most instances the affinity for Tyr3-octreotide is slightly higher than that for somatostatin-14 or somatostatin-28.1 2 3
In 12 of 13 patients with metastatic carcinoid disease and in 7 of 9 patients with pancreatic endocrine tumors, the in vivo imaging procedure using 123I-labeled Tyr3-octreotide provided information concerning the localization of the primary tumors, the secondary spread of the disease, or both. Virtually all the patients had previously undetected metastases. The identification of tumor tissue in lymph nodes on the left side of the neck in seven patients with carcinoid tumors and two with endocrine pancreatic tumors underlines the value of a thorough examination in such patients. In one patient with carcinoid disease in whom the scan was negative, long-term octreotide therapy had no beneficial clinical effect, suggesting that the patient's tumor had no receptors. Similarly, no receptors could be detected on the insulinoma tissue of the two patients in whom the in vivo scan was negative.
The 123I-labeled Tyr3-octreotide imaging technique was also used successfully in the localization of paragangliomas. Such tumors are often difficult to localize, and in most patients arteriography is necessary to confirm the diagnosis.11 , 12 Of considerable importance was the localization of multiple paragangliomas in eight patients.
We found that tumors in the abdomen were well visualized within 30 minutes after the administration of the isotope, before the surrounding background activity in the liver, biliary tract, and gastrointestinal tract was so considerable that it became difficult to distinguish between tumor and physiologic uptake. Additional scans were possible 24 hours later, when the organs again contained little radioactivity. SPECT proved to be of great value in localizing the site of Tyr3-octreotide uptake in tumors, especially when the tumors were located close to sites with physiologic uptake of radioactivity. Tumors positive for somatostatin receptors in the chest, neck, and skull, however, can be readily visualized at any time 30 to 240 minutes after the administration of the isotope because the background level of radioactivity is very low by that time.
We did not correlate the degree of radionuclide uptake in these tumors with the extent of the biochemical response or the clinical responsiveness to short-term or long-term octreotide. Uptake of 123I-labeled Tyr3-octreotide was found, however, in all tumors with a clinical or biochemical response to a single dose of octreotide or to long-term administration. Thus, 123I-labeled Tyr3-octreotide imaging may be useful in predicting responsiveness to octreotide therapy.
We conclude that 123I-labeled Tyr3-octreotide imaging is a quick and safe way to identify tumors that have somatostatin receptors, and tumors as small as 1 cm in diameter (e.g., paragangliomas) can be detected. We found this technique to be valuable in locating not only primary but also secondary deposits of these tumors, which may be very difficult to localize with current diagnostic techniques. Although these results are encouraging, the sensitivity and specificity of this scanning procedure in the localization of such tumors must be confirmed by studies of larger numbers of patients.
Supported by grants from the Dutch Cancer Foundation and a special grant from the University Hospital Dijkzigt, Rotterdam.
Source Information
From the Departments of Medicine (S.W.J.L, E.P.K.) and Nuclear Medicine (W.H.B, E.P.K.), Erasmus University, Rotterdam, the Netherlands; and Sandoz Research Institute, Bern, Switzerland (J.-C.R.). Address reprint requests to Dr. Lamberts at the Department of Medicine, University Hospital Dijkzigt, 40 Molewaterplein, 3015 GD Rotterdam, the Netherlands.
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Jean Claude Reubil, Steven J.W. Lamberts, Eric P. Krenning. (1995) Minireview: Receptor Imaging of Human Diseases Using Radiolabeled Peptides. Journal of Receptors and Signal Transduction 15:1-4, 379-392
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Jean Claude Reubi, Beatrice Waser, Hendrik M. Markusse, Eric P. Krenning, Martin VanHagen, Jean A. Laissue. (1994) Vascular somatostatin receptors in synovium from patients with rheumatoid arthritis. European Journal of Pharmacology 271:2-3, 371-378
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P. M. Vanhagen, H. M. Markusse, S. W. J. Lamberts, D. J. Kwekkeboom, J. C. Reubi, E. P. Krenning. (1994) Somatostatin receptor imaging. the presence of somatostatin receptors in rheumatoid arthritis. Arthritis & Rheumatism 37:10, 1521-1527
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C.H.J. van Eijck, J. Jeekel, E.P. Krenning, A. Bootsma, S.W.J. Lamberts, H.Y. Oei, J. Lindemans, R. van Pel, J.C. Reubi. (1994) Somatostatin-receptor scintigraphy in primary breast cancer. The Lancet 343:8898, 640-643
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P. M. VAN HAGEN, E. P. KRENNING, D. J. KWEKKEBOOM, J. C. REUBI, vd. P. J. ANKER-LUGTENBURG, B. LÖWENBERG, S. W. J. LAMBERTS. (1994) Somatostatin and the immune and haematopoetic system; a review. European Journal of Clinical Investigation 24:2, 91-99
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