Skip to main content
The Yale Journal of Biology and Medicine logoLink to The Yale Journal of Biology and Medicine
. 1997 Sep-Dec;70(5-6):509–522.

Comparative analysis of diagnostic techniques for localization of gastrointestinal neuroendocrine tumors.

F Gibril 1, R T Jensen 1
PMCID: PMC2589275  PMID: 9825478

Abstract

In vitro studies have shown that gastroenteropancreatic tumors, with the exception of insulinomas, have a high density of somatostatin receptors and can be imaged in vivo using somatostatin receptor scintigraphy (SRS) with either [123I-Tyr3]octreotide or [111In DTPA,DPhe1]octreotide. However, the sensitivity in relation to conventional imaging studies (ultrasound, CT, MRI, angiography) remains unclear. To address this question, we performed a prospective study of 80 patients with gastrinomas where SRS was compared with other conventional imaging techniques for detecting extrahepatic gastrinomas or liver metastases. Extrahepatic gastrinomas were identified by SRS in 58 percent of patients, whereas conventional imaging studies detected gastrinomas in 9 percent to 48 percent of patients. In detecting hepatic metastases in 24 patients with histologically-proven metastases, SRS was positive in 92 percent; ultrasound, CT or angiography in 42 percent to 62 percent; and MRI in 71 percent of patients. These results are compared with other studies in detecting gastrinomas as well as series including other PETs, excluding insulinomas, with insulinomas alone, and with carcinoid tumors. An analysis of the ability of SRS to identify gastrinomas found in different sites at surgery was performed. The role of endoscopic ultrasound (EUS) in detecting various PETs, in comparison to that of SRS, is yet to be established, particularly for extrapancreatic PETs. Therefore, the results of EUS in various studies containing patients with PETs are compared to those with SRS and conventional imaging studies. These data suggest that EUS is the first choice of localization methods for detecting insulinoma, which is an intrapancreatic tumor in almost all cases. In other PETs there still is not sufficient data to establish the relative roles of EUS and SRS.

Full text

PDF
518

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Cadiot G., Lebtahi R., Sarda L., Bonnaud G., Marmuse J. P., Vissuzaine C., Ruszniewski P., Le Guludec D., Mignon M. Preoperative detection of duodenal gastrinomas and peripancreatic lymph nodes by somatostatin receptor scintigraphy. Groupe D'etude Du Syndrome De Zollinger-Ellison. Gastroenterology. 1996 Oct;111(4):845–854. doi: 10.1016/s0016-5085(96)70052-5. [DOI] [PubMed] [Google Scholar]
  2. Ciaccia D., Gress F. G. Somatostatin receptor scintigraphy in the Zollinger-Ellison syndrome. Ann Intern Med. 1997 May 1;126(9):741–742. doi: 10.7326/0003-4819-126-9-199705010-00021. [DOI] [PubMed] [Google Scholar]
  3. Doppman J. L., Chang R., Fraker D. L., Norton J. A., Alexander H. R., Miller D. L., Collier E., Skarulis M. C., Gorden P. Localization of insulinomas to regions of the pancreas by intra-arterial stimulation with calcium. Ann Intern Med. 1995 Aug 15;123(4):269–273. doi: 10.7326/0003-4819-123-4-199508150-00004. [DOI] [PubMed] [Google Scholar]
  4. Doppman J. L. Pancreatic endocrine tumors--the search goes on. N Engl J Med. 1992 Jun 25;326(26):1770–1772. doi: 10.1056/NEJM199206253262609. [DOI] [PubMed] [Google Scholar]
  5. Doppman J. L., Shawker T. H., Miller D. L. Localization of islet cell tumors. Gastroenterol Clin North Am. 1989 Dec;18(4):793–804. [PubMed] [Google Scholar]
  6. Eriksson B., Oberg K., Skogseid B. Neuroendocrine pancreatic tumors. Clinical findings in a prospective study of 84 patients. Acta Oncol. 1989;28(3):373–377. doi: 10.3109/02841868909111209. [DOI] [PubMed] [Google Scholar]
  7. Frucht H., Howard J. M., Slaff J. I., Wank S. A., McCarthy D. M., Maton P. N., Vinayek R., Gardner J. D., Jensen R. T. Secretin and calcium provocative tests in the Zollinger-Ellison syndrome. A prospective study. Ann Intern Med. 1989 Nov 1;111(9):713–722. doi: 10.7326/0003-4819-111-9-713. [DOI] [PubMed] [Google Scholar]
  8. Gibril F., Doppman J. L., Chang R., Weber H. C., Termanini B., Jensen R. T. Metastatic gastrinomas: localization with selective arterial injection of secretin. Radiology. 1996 Jan;198(1):77–84. doi: 10.1148/radiology.198.1.8539410. [DOI] [PubMed] [Google Scholar]
  9. Gibril F., Reynolds J. C., Doppman J. L., Chen C. C., Venzon D. J., Termanini B., Weber H. C., Stewart C. A., Jensen R. T. Somatostatin receptor scintigraphy: its sensitivity compared with that of other imaging methods in detecting primary and metastatic gastrinomas. A prospective study. Ann Intern Med. 1996 Jul 1;125(1):26–34. doi: 10.7326/0003-4819-125-1-199607010-00005. [DOI] [PubMed] [Google Scholar]
  10. Glover J. R., Shorvon P. J., Lees W. R. Endoscopic ultrasound for localisation of islet cell tumours. Gut. 1992 Jan;33(1):108–110. doi: 10.1136/gut.33.1.108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hammond P. J., Arka A., Peters A. M., Bloom S. R., Gilbey S. G. Localization of metastatic gastroenteropancreatic tumours by somatostatin receptor scintigraphy with [111In-DTPA-D-Phe1]-octreotide. Q J Med. 1994 Feb;87(2):83–88. [PubMed] [Google Scholar]
  12. Heitz P. U., Kasper M., Polak J. M., Klöppel G. Pancreatic endocrine tumors. Hum Pathol. 1982 Mar;13(3):263–271. doi: 10.1016/s0046-8177(82)80183-4. [DOI] [PubMed] [Google Scholar]
  13. Howard T. J., Zinner M. J., Stabile B. E., Passaro E., Jr Gastrinoma excision for cure. A prospective analysis. Ann Surg. 1990 Jan;211(1):9–14. doi: 10.1097/00000658-199001000-00002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jensen R. T. Gastrointestinal endocrine tumours. Gastrinoma. Baillieres Clin Gastroenterol. 1996 Dec;10(4):603–643. doi: 10.1016/s0950-3528(96)90016-0. [DOI] [PubMed] [Google Scholar]
  15. Joseph K., Stapp J., Reinecke J., Skamel H. J., Höffken H., Neuhaus C., Lenze H., Trautmann M. E., Arnold R. Receptor scintigraphy with 111In-pentetreotide for endocrine gastroenteropancreatic tumors. Horm Metab Res Suppl. 1993;27:28–35. [PubMed] [Google Scholar]
  16. Kisker O., Weinel R. J., Geks J., Zacara F., Joseph K., Rothmund M. Value of somatostatin receptor scintigraphy for preoperative localization of carcinoids. World J Surg. 1996 Feb;20(2):162–167. doi: 10.1007/s002689900025. [DOI] [PubMed] [Google Scholar]
  17. Krenning E. P., Kooij P. P., Pauwels S., Breeman W. A., Postema P. T., De Herder W. W., Valkema R., Kwekkeboom D. J. Somatostatin receptor: scintigraphy and radionuclide therapy. Digestion. 1996;57 (Suppl 1):57–61. doi: 10.1159/000201398. [DOI] [PubMed] [Google Scholar]
  18. Krenning E. P., Kwekkeboom D. J., Bakker W. H., Breeman W. A., Kooij P. P., Oei H. Y., van Hagen M., Postema P. T., de Jong M., Reubi J. C. Somatostatin receptor scintigraphy with [111In-DTPA-D-Phe1]- and [123I-Tyr3]-octreotide: the Rotterdam experience with more than 1000 patients. Eur J Nucl Med. 1993 Aug;20(8):716–731. doi: 10.1007/BF00181765. [DOI] [PubMed] [Google Scholar]
  19. Krenning E. P., Kwekkeboom D. J., Oei H. Y., de Jong R. J., Dop F. J., Reubi J. C., Lamberts S. W. Somatostatin-receptor scintigraphy in gastroenteropancreatic tumors. An overview of European results. Ann N Y Acad Sci. 1994 Sep 15;733:416–424. doi: 10.1111/j.1749-6632.1994.tb17291.x. [DOI] [PubMed] [Google Scholar]
  20. Kvols L. K. Somatostatin-receptor imaging of human malignancies: a new era in the localization, staging, and treatment of tumors. Gastroenterology. 1993 Dec;105(6):1909–1911. doi: 10.1016/0016-5085(93)91091-u. [DOI] [PubMed] [Google Scholar]
  21. Lightdale C. J., Botet J. F., Woodruff J. M., Brennan M. F. Localization of endocrine tumors of the pancreas with endoscopic ultrasonography. Cancer. 1991 Oct 15;68(8):1815–1820. doi: 10.1002/1097-0142(19911015)68:8<1815::aid-cncr2820680828>3.0.co;2-b. [DOI] [PubMed] [Google Scholar]
  22. London J. F., Shawker T. H., Doppman J. L., Frucht H. H., Vinayek R., Stark H. A., Miller L. S., Miller D. L., Norton J. A., Jensen R. T. Zollinger-Ellison syndrome: prospective assessment of abdominal US in the localization of gastrinomas. Radiology. 1991 Mar;178(3):763–767. doi: 10.1148/radiology.178.3.1994415. [DOI] [PubMed] [Google Scholar]
  23. Maton P. N., Miller D. L., Doppman J. L., Collen M. J., Norton J. A., Vinayek R., Slaff J. I., Wank S. A., Gardner J. D., Jensen R. T. Role of selective angiography in the management of patients with Zollinger-Ellison syndrome. Gastroenterology. 1987 Apr;92(4):913–918. doi: 10.1016/0016-5085(87)90964-4. [DOI] [PubMed] [Google Scholar]
  24. Norton J. A., Doppman J. L., Jensen R. T. Curative resection in Zollinger-Ellison syndrome. Results of a 10-year prospective study. Ann Surg. 1992 Jan;215(1):8–18. doi: 10.1097/00000658-199201000-00012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Palazzo L., Roseau G., Salmeron M. Endoscopic ultrasonography in the preoperative localization of pancreatic endocrine tumors. Endoscopy. 1992 May;24 (Suppl 1):350–353. doi: 10.1055/s-2007-1010498. [DOI] [PubMed] [Google Scholar]
  26. Pauwels S., Leners N., Fiasse R., Jamar F. Localization of gastroenteropancreatic neuroendocrine tumors with 111indium-pentetreotide scintigraphy. Semin Oncol. 1994 Oct;21(5 Suppl 13):15–20. [PubMed] [Google Scholar]
  27. Pisegna J. R., Doppman J. L., Norton J. A., Metz D. C., Jensen R. T. Prospective comparative study of ability of MR imaging and other imaging modalities to localize tumors in patients with Zollinger-Ellison syndrome. Dig Dis Sci. 1993 Jul;38(7):1318–1328. doi: 10.1007/BF01296084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Reubi J. C., Laissue J., Waser B., Horisberger U., Schaer J. C. Expression of somatostatin receptors in normal, inflamed, and neoplastic human gastrointestinal tissues. Ann N Y Acad Sci. 1994 Sep 15;733:122–137. doi: 10.1111/j.1749-6632.1994.tb17262.x. [DOI] [PubMed] [Google Scholar]
  29. Ruszniewski P., Amouyal P., Amouyal G., Grangé J. D., Mignon M., Bouché O., Bernades P. Localization of gastrinomas by endoscopic ultrasonography in patients with Zollinger-Ellison syndrome. Surgery. 1995 Jun;117(6):629–635. doi: 10.1016/s0039-6060(95)80005-0. [DOI] [PubMed] [Google Scholar]
  30. Rösch T., Lightdale C. J., Botet J. F., Boyce G. A., Sivak M. V., Jr, Yasuda K., Heyder N., Palazzo L., Dancygier H., Schusdziarra V. Localization of pancreatic endocrine tumors by endoscopic ultrasonography. N Engl J Med. 1992 Jun 25;326(26):1721–1726. doi: 10.1056/NEJM199206253262601. [DOI] [PubMed] [Google Scholar]
  31. Scherübl H., Bäder M., Fett U., Hamm B., Schmidt-Gayk H., Koppenhagen K., Dop F. J., Riecken E. O., Wiedenmann B. Somatostatin-receptor imaging of neuroendocrine gastroenteropancreatic tumors. Gastroenterology. 1993 Dec;105(6):1705–1709. doi: 10.1016/0016-5085(93)91066-q. [DOI] [PubMed] [Google Scholar]
  32. Termanini B., Gibril F., Reynolds J. C., Doppman J. L., Chen C. C., Stewart C. A., Sutliff V. E., Jensen R. T. Value of somatostatin receptor scintigraphy: a prospective study in gastrinoma of its effect on clinical management. Gastroenterology. 1997 Feb;112(2):335–347. doi: 10.1053/gast.1997.v112.pm9024287. [DOI] [PubMed] [Google Scholar]
  33. Thom A. K., Norton J. A., Doppman J. L., Miller D. L., Chang R., Jensen R. T. Prospective study of the use of intraarterial secretin injection and portal venous sampling to localize duodenal gastrinomas. Surgery. 1992 Dec;112(6):1002–1009. [PubMed] [Google Scholar]
  34. Thompson N. W., Czako P. F., Fritts L. L., Bude R., Bansal R., Nostrant T. T., Scheiman J. M. Role of endoscopic ultrasonography in the localization of insulinomas and gastrinomas. Surgery. 1994 Dec;116(6):1131–1138. [PubMed] [Google Scholar]
  35. Wank S. A., Doppman J. L., Miller D. L., Collen M. J., Maton P. N., Vinayek R., Slaff J. I., Norton J. A., Gardner J. D., Jensen R. T. Prospective study of the ability of computed axial tomography to localize gastrinomas in patients with Zollinger-Ellison syndrome. Gastroenterology. 1987 Apr;92(4):905–912. doi: 10.1016/0016-5085(87)90963-2. [DOI] [PubMed] [Google Scholar]
  36. Weber H. C., Venzon D. J., Lin J. T., Fishbein V. A., Orbuch M., Strader D. B., Gibril F., Metz D. C., Fraker D. L., Norton J. A. Determinants of metastatic rate and survival in patients with Zollinger-Ellison syndrome: a prospective long-term study. Gastroenterology. 1995 Jun;108(6):1637–1649. doi: 10.1016/0016-5085(95)90124-8. [DOI] [PubMed] [Google Scholar]
  37. Weinel R. J., Neuhaus C., Stapp J., Klotter H. J., Trautmann M. E., Joseph K., Arnold R., Rothmund M. Preoperative localization of gastrointestinal endocrine tumors using somatostatin-receptor scintigraphy. Ann Surg. 1993 Nov;218(5):640–645. doi: 10.1097/00000658-199321850-00009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zimmer T., Stölzel U., Bäder M., Koppenhagen K., Hamm B., Buhr H., Riecken E. O., Wiedenmann B. Endoscopic ultrasonography and somatostatin receptor scintigraphy in the preoperative localisation of insulinomas and gastrinomas. Gut. 1996 Oct;39(4):562–568. doi: 10.1136/gut.39.4.562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zimmer T., Ziegler K., Bäder M., Fett U., Hamm B., Riecken E. O., Wiedenmann B. Localisation of neuroendocrine tumours of the upper gastrointestinal tract. Gut. 1994 Apr;35(4):471–475. doi: 10.1136/gut.35.4.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. de Kerviler E., Cadiot G., Lebtahi R., Faraggi M., Le Guludec D., Mignon M. Somatostatin receptor scintigraphy in forty-eight patients with the Zollinger-Ellison syndrome. GRESZE: Groupe d'Etude du Syndrome de Zollinger-Ellison. Eur J Nucl Med. 1994 Nov;21(11):1191–1197. doi: 10.1007/BF00182352. [DOI] [PubMed] [Google Scholar]

Articles from The Yale Journal of Biology and Medicine are provided here courtesy of Yale Journal of Biology and Medicine

RESOURCES