Imaging of neuroendocrine tumors of the pancreas

Review Article


Background. Neuroendocrine tumors of the pancreas are uncommon neoplasms of the pancreas that can occur sporadically or in association with various syndromes such as multiple endocrine neoplasia type 1 (MEN 1). Patients can present with a specific clinical syndrome related to biochemically functioning tumors or with nonspecific symptoms related to mass effect or metastases. The size, function, consistency, and malignant behavior of neuroendocrine tumors are integrally related. Imaging has a major role in the preoperative localization of the primary tumor and detection of metastases. Several techniques are available including ultrasound, endoscopic ultrasound, computed tomography (CT), MR, somatostatin receptor scintigraphy, angiography, and arterial stimulation with venous sampling; each with unique advantages and limitations. The reported performance for these techniques vary widely, and as a result, recommended imaging algorithms are controversial. Recent technical advances in ultrasound, CT, and MRI have occurred that may improve the sensitivity of some of the techniques. Further improvements are likely in the future. In this chapter we will review imaging techniques used to study the pancreas as it relates to the detection of neuroendocrine tumors, imaging findings of these tumors using various imaging modalities, and the advantages, limitations and results obtained with each technique.

Key Words

Pancreas neoplasms pancreas CT pancreas MR pancreas US 


  1. 1.
    Jensen RT. Endocrine tumors of the gastrointestinal tract, in Harrison’s Online. Braunwald EIA, Kasp DL, et al., eds. McGraw-Hill: New York, 2001, pp. 1–26.Google Scholar
  2. 2.
    Winter TC, Freeny PC, Nghiem HV. Extrapancreatic gastrinoma localization: value of arterial-phase helical CT with water as an oral contrast agent. AJR 1996;51–52.Google Scholar
  3. 3.
    Stabile BE, Morrow DJ, Passaro EJ. The gastrinoma triangle: operative implications. Am J Surg 1984;147.Google Scholar
  4. 4.
    Semelka RC, Custodio CM, Balci C, et al. Neuroendocrine tumors of the pancreas: spectrum of appearances on MRI. J Magnet Reson Imag 2000;141–148.Google Scholar
  5. 5.
    Rosch T, Ligtdale CJ, Botet JF, et al. Localization of pancreatic endocrine tumors by endoscopic ultrasonography. N Engl J Med 1992;1721–1726.Google Scholar
  6. 6.
    Mozell E, Stenzel P, Woltering EA, et al. Functional endocrine tumors of the pancreas: clinical presentation, diagnosis, and treatment. Curr Probl Surg 1990; 304–385.Google Scholar
  7. 7.
    Thoeni RF, Mueller-Lisse UG, Chan R, et al. Detection of small, functional islet cell tumors in the pancreas: selection of MR imaging sequences for optimal sensitivity. Radiology 2000;483–490.Google Scholar
  8. 8.
    Modlin IM, Lawton, GP. Duodenal gastrinoma: the solution to the pancreatic paradox (Editoria). J Clin Gastroenterol 1994;184–188.Google Scholar
  9. 9.
    Doppman JL, Nieman LK. Cutler GB, et al. Adrenocorticotropic hormone—secreting islet cell tumors: are they always malignant. Radiology 1994;59–64.Google Scholar
  10. 10.
    Buetow PC, Parrino TV, Buck JL, et al. Islet cell tumors of the pancreas: pathologic—imaging correlation among size, necrosis and cysts, calcification, malignant behavior, and functional status. AJR 1995;1175–1179.Google Scholar
  11. 11.
    Stafford Johnson DB, Francis IR, Eckhauser FE, et al. Dual-phase helical CT of nonfunctioning islet cell tumors. J Comput Assist Tomogr 1998;22:59–63.PubMedCrossRefGoogle Scholar
  12. 12.
    Eelkema EA, Stephens DH, Ward EM, et al. CT features of nonfunctioning islet cell carcinoma. AJR 1984;943–948.Google Scholar
  13. 13.
    Takeshita K, Furui S, Makita K, et al. Cystic islet cell tumors: radiologic findings in three cases. Abdom Imag 1994;19:225–228.CrossRefGoogle Scholar
  14. 14.
    Baba Y, Miyazono N, Nakajo M, et al. Small cystic insulinoma: value of arterial stimulation venous sampling. Cardio Vase Intervent Radiol 1997;308–310.Google Scholar
  15. 15.
    Pogany AC, Kerlan RK, Karam JH, et al. Cystic insulinoma. AJR 1984;951–952.Google Scholar
  16. 16.
    Carlson BC, Johnson CD, Stephens DH, et al. MRI of pancreatic islet cell carcinoma. J Comput Assist Tomogr 1993;735–740.Google Scholar
  17. 17.
    Fugazzola C, Procacci C, Andreis IAB, et al. The contribution of ultrasonography and computed tomography in the diagnosis of nonfunctioning islet cell tumors of the pancreas. Gastrointest Radiol 1990;139–144.Google Scholar
  18. 18.
    Thompson NW, Eckhauser FE, Vinik AI, et al. Cystic neuroendocrine neoplasms of the pancrease and liver. Ann Surg 1984;199:158–164.PubMedCrossRefGoogle Scholar
  19. 19.
    Pavone P, Mitchell DG, Leonetti F, et al. Pancreatic B-cell tumors: MRI. J Comput Assist Tomogr 1993;403–407.Google Scholar
  20. 20.
    Ichikawa T, Peterson MS, Federle MP, et al. Islet cell tumor of the pancreas: biphasic CT versus MR imaging in tumor detection. Radiology 2000;163–171.Google Scholar
  21. 21.
    Koito K, Namieno T, Nagakawa T, et al. Delayed enhancement of islet cell carcinoma on dynamic computed tomography: a sign of its malignancy. Abdom Imag 1997;304–306.Google Scholar
  22. 22.
    Aspestrand F, Kolmannskog F, Jacobsen M. CT, MR imaging and angiography in pancreatic apudomas. Acta Radiologica 1993;34:468–473.PubMedCrossRefGoogle Scholar
  23. 23.
    Boukhman MP, Karam JM, Shaver JS, et al. Localization of insulinomas. Arch Surg 1999;818–823.Google Scholar
  24. 24.
    Hashimoto LA, Wash RM. Preoperative localization of insulinomas is not necessary. J Am Coll Surg 1999;189:368–373.PubMedCrossRefGoogle Scholar
  25. 25.
    Norton JA, Cromack DT, Shawker TH, et al. Intraoperative ultrasonographic localization of islet cell tumors: a prospective comparison to palpation. Ann Surg 1988;160–168.Google Scholar
  26. 26.
    Grant CS, Van Heerden J, Charboneau JW, et al. Insulinoma. The value of intraoperative ultrasonography. Arch Surg 1988;123:843–848.PubMedGoogle Scholar
  27. 27.
    Huai JC, Zhengzhou H, Zhang W, et al. Localization and surgical treatment of pancreatic insulinomas guided by intraoperative ultrasound. Am J Surg 1998;18–21.Google Scholar
  28. 28.
    Kuzin NM, Egorov AV, Kondrashin SA, et al. Preoperative and intraoperative topographic diagnosis of insulinomas. World J Surg 1998;593–598.Google Scholar
  29. 29.
    Bottger TS, Junginger T. Is preoperative radiographic localization of islet cell tumors in patients with insulinoma necessary? World J Surg 1993;17:427–432.PubMedCrossRefGoogle Scholar
  30. 30.
    King AD, Ko GTC, Yeung VTF, et al. Dual phase spiral CT in the detection of small insulinomas of the pancreas. Brit J Radiol 1998;20–23.Google Scholar
  31. 31.
    Van Hoe L, Gryspeerdt S, Marchal G, et al. Helical CT for the preoperative localization of islet cell tumors of the pancreas: value of arterial and parenchymal phase images. AJR 1995;1437–1439.Google Scholar
  32. 32.
    Keogan MT, McDermott VG, Paulson EK, et al. Pancreatic malignancy: effect of dual-phase helical CT in tumor detection and vascular opacification. Radiology 1997;513–518.Google Scholar
  33. 33.
    Kurosakij Y, Kuramoto YI. Hyperattenuating insulinoma at unenhanced CT. Abdom Imag 1996; 334–336.Google Scholar
  34. 34.
    Legmann P, Vignaux O, Dousset B, et al. Pancreatic tumors: comparison of dual phase helical CT and endoscopic sonography. AJR 1998;1315–1322.Google Scholar
  35. 35.
    Chung MJ, Choi BI, Han JK, et al. Functioning islet cell tumor of the pancreas: localization with dynamic spiral CT. Acta Radiologica 1997;135–138.Google Scholar
  36. 36.
    Schirmer WJ, Melvin WS, Rush RM, Indium-111-pentetreotide scanning versus conventional imaging techniques for the localization of gastrinoma. Surgery 1995;118:1105–1113.PubMedCrossRefGoogle Scholar
  37. 37.
    Alexander HR, Fraker DL, Norton JA, et al. Prospective study of somatostatin receptor scintigraphy and its effect on operative outcome in patients with Zollinger-Ellison syndrome. Ann Surg 1998;228:228–238.PubMedCrossRefGoogle Scholar
  38. 38.
    Kraus BB, Ros PR. Insulinoma: diagnosis with fatsuppressed MR imaging. AJR 1994;69–70.Google Scholar
  39. 39.
    Mitchell DG, Cruvella M, Eschelman DJ, et al. MRI of pancreatic gastrinomas. J Comput Assist Tomogr 1992;583–585.Google Scholar
  40. 40.
    Semelka RC, Ascher SM. MR imaging of the pancreas. Radiology 1993;593–602.Google Scholar
  41. 41.
    Semelka RC, Cumming MJ, Shoenut JP, et al. Islet cell tumors: comparison of dynamic contrast-enhanced CT and MR imaging with dynamic gadolinium enhancement and fat suppression. Radiology 1993;799–802.Google Scholar
  42. 42.
    Mori M, Fukuda T, Nagayoshi K, et al. Insulinoma: correlation of short-T1 inversion-recovery (STIR) imaging and histopathologic findings. Abdom Imag 1996 336–341.Google Scholar
  43. 43.
    Angeli E, Vanzulli A, Castrucci M, et al. Value of abdominal sonography and MR imaging at 0.5 T in preoperative detection of pancreatic insulinoma: a comparison with dynamic CT and angiography. Abdom Imag 1997;295–303.Google Scholar
  44. 44.
    Catalano C, Pavone P, Laghi A, et al. Localization of pancreatic insulinomas with MR imaging at 0.5 T. Acta Radiologica 1999;644–648.Google Scholar
  45. 45.
    Schumacher B, Lubke HJ, Frieling T, et al. Prospective study on the detection of insulinomas by endoscopic ultrasonography. Endoscopy 1996;28:273–276.PubMedCrossRefGoogle Scholar
  46. 46.
    Thompson NW, Czako PF, Fritts LL, et al. Role of endoscopic ultrasonography in the localization of insulinomas and gastrinomas. Surgery 1994;116:1131–1138.PubMedGoogle Scholar
  47. 47.
    DeAngelis C, Repici A, Arena V, et al. Preoperative endoscopic ultrasonography in decision making and management of pancreatic endocrine tumors: a 6-year experience. Endoscopy 1998;A182–A186.Google Scholar
  48. 48.
    Chavan A, Kirchhoff TD, Brabant G. Role of the intraarterial calcium stimulation test in the preoperative localization of insulinomas. Eur Radiol 2000;1582–1586.Google Scholar
  49. 49.
    Zimmer T, Scherubl H, Faiss S, et al. Endoscopic ultrasonography of neuroendocrine tumours. Digestion 2000;45–50.Google Scholar
  50. 50.
    Pitre J, Soubrane O, Palazzo L, et al. Endoscopic ultrasonography for the preoperative localization of insulinomas. Pancreas 1996;13:55–60.PubMedCrossRefGoogle Scholar
  51. 51.
    Brown CK, Bartlett DL, Doppman JL, et al. Intra-arterial calcium stimulation and intraoperative ultrasonography in the localization and resection of insulinomas. Surgery 1997;122:1189–1193.PubMedCrossRefGoogle Scholar
  52. 52.
    Frucht H, Doppman JL, Norton JA, et al. Gastrinomas: comparison of MR imaging with CT, angiography, and US. Radiology 1989;713–717.Google Scholar
  53. 53.
    Galiber AK, Reading CC, Charboneau JW, et al. Localization of pancreatic insulinoma: comparison of pre- and intraoperative US with CT and angiography. Abdom Gastrointest Radiol 1988;405–408.Google Scholar
  54. 54.
    Ariyama J, Suyama M, Satoh K, et al. Endoscopic ultrasound and intraductal ultrasound in the diagnosis of small pancreatic tumors, Abdom Imag 1998;380–386.Google Scholar
  55. 55.
    de Kerviler E, Cadiot G, Lebtahi R, et al. Somatostatin receptor scintigraphy in forty-eight patients with the Zollinger-Ellison Syndrome. Eur J Nucl Med 1994;1191–1197.Google Scholar
  56. 56.
    Cadiot G, Lebtahi R, Sarda L, et al. Preoperative detection of duodenal gastrinomas and peripancreatic lymph nodes by somatostatin receptor scintigraphy. Gastroenterology 1996;845–854.Google Scholar
  57. 57.
    Schillaci O, Annibale B, Scopinar F, et al. Somatostatin receptor scintigraphy of malignant somatostatinoma with indium-111-pentetreotide. J Nucl Med 1997;38:886–887.PubMedGoogle Scholar
  58. 58.
    Krausz Y, Bar-Ziv J, deJong RB, et al. Somatostatin-receptor scintigraphy in the management of gastroenteropancreatic tumors. Amer J Gastroenterol 1998;93:66–70.CrossRefGoogle Scholar
  59. 59.
    Gibril F, Reynolds JC, Chen CC, et al. Specificity of somatostatin receptor scintigraphy: a prospective study and effects of false-positive localizations on management in patients with gastrinomas. J Nucl Med 1999;40:539–553.PubMedGoogle Scholar
  60. 60.
    Benevento A, Dominioni L, Carcano G, et al. Intraoperative localization of gut endocrine tumors with radiolabeled somatostatin analogs and a gamma-detector probe. Semin Surg Oncol 1998;239–244.Google Scholar
  61. 61.
    Proye C, Malvaux P, Pattou F, et al. Noninvasive imaging of insulinomas and gastrinomas with endoscopic ultrasonography and somatostatin receptor scintigraphy. Surgery 1998;124:1134–1143.PubMedCrossRefGoogle Scholar
  62. 62.
    Krenning EP, Kwekkeboom DJ, Oei HY, et al. Somatostatin-receptor scintigraphy in gastroenteropancreatic tumors. An overview of European results. Ann NY Acad Sci 1994;416–424.Google Scholar
  63. 63.
    Gibril F, Reynolds JC, Doppman JL, et al. 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; 26–34.Google Scholar
  64. 64.
    Modlin IM, Cornelius E, Lawton GP. Use of an isotopic somatostatin receptor probe to image gut endocrine tumors. Arch Surg 1995;130:367–373.PubMedGoogle Scholar
  65. 65.
    Weinel RJ, Neuhaus C, Stapp J, et al. Preoperative localization of gastrointestinal endocrine tumors using somatostatin-receptor scintigraphy. Ann Surg 1993; 640–645.Google Scholar
  66. 66.
    Krenning EP, Kwekkeboom DJ, Bakker WH, et al. 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;716–731.Google Scholar
  67. 67.
    Scherubl H, Bader M, Fett U, et al. Somatostatin-receptor imaging of neuroendocrine gastroenteropancreatic tumors. Gastroenterology 1993;1705–1709.Google Scholar
  68. 68.
    Kisker O, Bartsch D, Winel RJ, et al. The value of somatostatin-receptor scintigraphy in newly diagnosed endocrine gastroenteropancreatic tumors. J Am Coll Surg 1997;184:487–492.PubMedGoogle Scholar
  69. 69.
    Signore A, Procaccini E, Chianelli M. SPECT imaging with 111 In-octreotide for the localization of pancreatic insulinoma. Quart J Nucl Med 1995; 39:111–112.Google Scholar
  70. 70.
    Schillaci O, Massa R, Scopinaro F. 111In-Pentetreotide scintigraphy in the detection of insulinomas: importance of SPECT imaging. J Nucl Med 2000;459–462.Google Scholar
  71. 71.
    Cohen MS, Picus D, Lairmore TC. Prospective study of provocative angiograms to localize functional islet cell tumors of the pancreas. Surgery 1997;122:1091–1100.PubMedCrossRefGoogle Scholar
  72. 72.
    Doppman JL, Miller DL, Chang R. Insulinomas: localization with selective intraarterial injection of calcium. Radiology 1991;178:237–241.PubMedGoogle Scholar
  73. 73.
    Imamura M, Takahashi K, Adachi H, et al. Usefulness of selective arterial secretin injection test for localization of gastrinoma in the Zollinger-Ellison syndrome. Ann Surg 1987;230–239.Google Scholar
  74. 74.
    Baba Y, Miyazono N, Nakajo M, et al. Localization of insulinomas: comparison of conventional arterial stimulation with venous sampling (ASVS) and superselective ASVS. Acta Radiologica 2000;172–177.Google Scholar
  75. 75.
    Defreyne L, Konig K, Lerch M, et al. Modified intraarterial calcium stimulation with venous sampling test for preoperative localization of insulinomas. Abdom Imag 1998; 322–331.Google Scholar
  76. 76.
    Jensen RT, Gibril F, Termanini B. Definition of the role of somatostatin receptor scintigraphy in gastrointestinal neuroendocrine tumor localization. Yale J Biol Med 1997;70:481–500.PubMedGoogle Scholar
  77. 77.
    Pereira PL, Roche AJ, Maier GW, et al. Insulinoma and islet cell hyperplasia: value of the calcium intraarterial stimulation test when findings of other preoperative studies are negative. Radiology 1998;703–709.Google Scholar

Copyright information

© Humana Press Inc 2001

Authors and Affiliations

  1. 1.Department of RadiologyMayo ClinicRochester

Personalised recommendations