Skip to main content
PMC home page
Annals of Surgery logoLink to Annals of Surgery
. 1989 Dec;210(6):685–703. doi: 10.1097/00000658-198912000-00001

Current diagnosis and management of Zollinger-Ellison syndrome.

D K Andersen 1
PMCID: PMC1357859  PMID: 2686566

Abstract

The treatment of patients with Zollinger-Ellison syndrome (ZES) has undergone dramatic evolution during the past decade. Although initially regarded as an incurable tumor, resection of gastrinoma for potential cure has been reported in 30% to 40% of selected patients in recent series. Conversely, although definitive control of acid hypersecretion is achieved by total gastrectomy, histamine (H2)-receptor antagonists and the newly introduced agents omeprazole and somatostatin analogues allow effective medical therapy of gastric acid overproduction. Confirmation of the diagnosis is best achieved with the I.V. secretin stimulation test, and tumor localization techniques are mandatory to identify candidates for operative tumor resection. Intraoperative sonography and careful exploration are required for tumor removal; successful tumor resection is associated with prolonged survival. The majority of patients (60%) are still found to have malignant disease at the time of diagnosis, but 10-year overall survival commonly exceeds 40%. The presence of multiple endocrine neoplasia type I (MEN-I) is seen in 10% to 25% of patients; correction of hypercalcemia alone may have therapeutic benefit in some ZES patients, and while gastrinoma resection is rarely possible, MEN-I patients demonstrate prolonged survival. The choice of medical rather than surgical therapy for acid hypersecretion depends on the suitability of each patient for careful and repeated endoscopic and chemical studies, versus the likelihood of a successful postoperative outcome. Socioeconomic, geographic, and related medical factors in each case may dictate the form of long-term antisecretory therapy. Exploration for possible tumor resection is indicated for virtually all patients who have no documented metastatic disease.

Full text

PDF
685

Images in this article

687Fig. 1.
on p.687
691Fig. 3.
on p.691
692Figs. 4A and B.
on p.692
693Figs. 5A-C.
on p.693
694Fig. 6.
on p.694
696Figs. 7A and B.
on p.696

Selected References

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

  1. Barreras R. F., Mack E., Goodfriend T., Damm M. Resection of gastrinoma in the Zollinger-Ellison syndrome. Gastroenterology. 1982 May;82(5 Pt 1):953–956. [PubMed] [Google Scholar]
  2. Bauer W., Briner U., Doepfner W., Haller R., Huguenin R., Marbach P., Petcher T. J., Pless SMS 201-995: a very potent and selective octapeptide analogue of somatostatin with prolonged action. Life Sci. 1982 Sep 13;31(11):1133–1140. doi: 10.1016/0024-3205(82)90087-x. [DOI] [PubMed] [Google Scholar]
  3. Bloom S. R., Mortimer C. H., Thorner M. O., Besser G. M., Hall R., Gomez-Pan A., Roy V. M., Russell R. C., Coy D. H., Kastin A. J. Inhibition of gastrin and gastric-acid secretion by growth-hormone release-inhibiting hormone. Lancet. 1974 Nov 9;2(7889):1106–1109. doi: 10.1016/s0140-6736(74)90869-1. [DOI] [PubMed] [Google Scholar]
  4. Bonfils S., Landor J. H., Mignon M., Hervoir P. Results of surgical management in 92 consecutive patients with Zollinger-Ellison syndrome. Ann Surg. 1981 Dec;194(6):692–697. doi: 10.1097/00000658-198112000-00005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bonfils S., Mignon M., Gratton J. Cimetidine treatment of acute and chronic Zollinger-Ellison syndrome. World J Surg. 1979 Sep 20;3(5):597–604. doi: 10.1007/BF01654767. [DOI] [PubMed] [Google Scholar]
  6. Borch K., Renvall H., Liedberg G., Andersen B. N. Relations between circulating gastrin and endocrine cell proliferation in the atrophic gastric fundic mucosa. Scand J Gastroenterol. 1986 Apr;21(3):357–363. doi: 10.3109/00365528609003087. [DOI] [PubMed] [Google Scholar]
  7. Brennan M. F., Jensen R. T., Wesley R. A., Doppman J. L., McCarthy D. M. The role of surgery in patients with Zollinger-Ellison syndrome (ZES) managed medically. Ann Surg. 1982 Sep;196(3):239–245. doi: 10.1097/00000658-198209000-00002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Broder L. E., Carter S. K. Pancreatic islet cell carcinoma. II. Results of therapy with streptozotocin in 52 patients. Ann Intern Med. 1973 Jul;79(1):108–118. doi: 10.7326/0003-4819-79-1-108. [DOI] [PubMed] [Google Scholar]
  9. Buchanan K. D., Johnston C. F., O'Hare M. M., Ardill J. E., Shaw C., Collins J. S., Watson R. G., Atkinson A. B., Hadden D. R., Kennedy T. L. Neuroendocrine tumors. A European view. Am J Med. 1986 Dec 22;81(6B):14–22. doi: 10.1016/0002-9343(86)90581-4. [DOI] [PubMed] [Google Scholar]
  10. Bukowski R. M., McCracken J. D., Balcerzak S. P., Fabian C. J. Phase II study of chlorozotocin in islet cell carcinoma. A southwest Oncology Group study. Cancer Chemother Pharmacol. 1983;11(1):48–50. doi: 10.1007/BF00257417. [DOI] [PubMed] [Google Scholar]
  11. Carrasco C. H., Chuang V. P., Wallace S. Apudomas metastatic to the liver: treatment by hepatic artery embolization. Radiology. 1983 Oct;149(1):79–83. doi: 10.1148/radiology.149.1.6611956. [DOI] [PubMed] [Google Scholar]
  12. Cherner J. A., Doppman J. L., Norton J. A., Miller D. L., Krudy A. G., Raufman J. P., Collen M. J., Maton P. N., Gardner J. D., Jensen R. T. Selective venous sampling for gastrin to localize gastrinomas. A prospective assessment. Ann Intern Med. 1986 Dec;105(6):841–847. doi: 10.7326/0003-4819-105-6-841. [DOI] [PubMed] [Google Scholar]
  13. Collen M. J., Howard J. M., McArthur K. E., Raufman J. P., Cornelius M. J., Ciarleglio C. A., Gardner J. D., Jensen R. T. Comparison of ranitidine and cimetidine in the treatment of gastric hypersecretion. Ann Intern Med. 1984 Jan;100(1):52–58. doi: 10.7326/0003-4819-100-1-52. [DOI] [PubMed] [Google Scholar]
  14. Delchier J. C., Soule J. C., Mignon M., Goldfain D., Cortot A., Travers B., Isal J. P., Bader J. P. Effectiveness of omeprazole in seven patients with Zollinger-Ellison syndrome resistant to histamine H2-receptor antagonists. Dig Dis Sci. 1986 Jul;31(7):693–699. doi: 10.1007/BF01296445. [DOI] [PubMed] [Google Scholar]
  15. Delcore R., Jr, Cheung L. Y., Friesen S. R. Outcome of lymph node involvement in patients with the Zollinger-Ellison syndrome. Ann Surg. 1988 Sep;208(3):291–298. doi: 10.1097/00000658-198809000-00006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Deveney C. W., Deveney K. E., Stark D., Moss A., Stein S., Way L. W. Resection of gastrinomas. Ann Surg. 1983 Oct;198(4):546–553. doi: 10.1097/00000658-198310000-00015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Deveney C. W., Deveney K. S., Jaffe B. M., Jones R. S., Way L. W. Use of calcium and secretin in the diagnosis of gastrinoma (Zollinger-Ellison syndrome). Ann Intern Med. 1977 Dec;87(6):680–686. doi: 10.7326/0003-4819-87-6-680. [DOI] [PubMed] [Google Scholar]
  18. Deveney C. W., Deveney K. S., Way L. W. The Zollinger-Ellison syndrome--23 years later. Ann Surg. 1978 Sep;188(3):384–393. doi: 10.1097/00000658-197809000-00014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Deveney C. W., Stein S., Way L. W. Cimetidine in the treatment of Zollinger-Ellison syndrome. Am J Surg. 1983 Jul;146(1):116–123. doi: 10.1016/0002-9610(83)90271-4. [DOI] [PubMed] [Google Scholar]
  20. ELLISON E. H., WILSON S. D. THE ZOLLINGER-ELLISON SYNDROME: RE-APPRAISAL AND EVALUATION OF 260 REGISTERED CASES. Ann Surg. 1964 Sep;160:512–530. doi: 10.1097/00000658-196409000-00013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Edkins J. S. The chemical mechanism of gastric secretion. J Physiol. 1906 Mar 13;34(1-2):133–144. doi: 10.1113/jphysiol.1906.sp001146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ekman L., Hansson E., Havu N., Carlsson E., Lundberg C. Toxicological studies on omeprazole. Scand J Gastroenterol Suppl. 1985;108:53–69. [PubMed] [Google Scholar]
  23. Ellison E. C., Carey L. C., Sparks J., O'Dorisio T. M., Mekhjian H. S., Fromkes J. J., Caldwell J. H., Thomas F. B. Early surgical treatment of gastrinoma. Am J Med. 1987 May 29;82(5B):17–24. doi: 10.1016/0002-9343(87)90423-2. [DOI] [PubMed] [Google Scholar]
  24. Ellison E. C., Gower W. R., Elkhammas E., Woltering E. A., Sparks J., O'Dorisio T. M., Fabri P. J. Characterization of the in vivo and in vitro inhibition of gastrin secretion from gastrinoma by a somatostatin analogue (SMS 201-995). Am J Med. 1986 Dec 22;81(6B):56–64. doi: 10.1016/0002-9343(86)90585-1. [DOI] [PubMed] [Google Scholar]
  25. Fabri P. J., Gower W. R., Jr, Weber C., Tuttle S. Hyperparathyroid glands contain G-17 and G-34 gastrin. J Surg Res. 1986 Sep;41(3):333–337. doi: 10.1016/0022-4804(86)90045-4. [DOI] [PubMed] [Google Scholar]
  26. Fox P. S., Hofmann J. W., Decosse J. J., Wilson S. D. The influence of total gastrectomy on survival in malignant Zollinger-Ellison tumors. Ann Surg. 1974 Oct;180(4):558–566. doi: 10.1097/00000658-197410000-00020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Fox P. S., Hofmann J. W., Wilson S. D., DeCosse J. J. Surgical management of the Zollinger-Ellison syndrome. Surg Clin North Am. 1974 Apr;54(2):395–407. doi: 10.1016/s0039-6109(16)40287-2. [DOI] [PubMed] [Google Scholar]
  28. Friesen S. R., Tomita T. Pseudo-Zollinger-Ellison syndrome: hypergastrinemia, hyperchlorhydria without tumor. Ann Surg. 1981 Oct;194(4):481–493. doi: 10.1097/00000658-198110000-00011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Friesen S. R. Treatment of the Zollinger-Ellison syndrome. A 25 year assessment. Am J Surg. 1982 Mar;143(3):331–338. doi: 10.1016/0002-9610(82)90102-7. [DOI] [PubMed] [Google Scholar]
  30. GREGORY R. A., TRACY H. J., FRENCH J. M., SIRCUS W. Extraction of a gastrin-like substance from a pancreatic tumour in a case of Zollinger-Ellison syndrome. Lancet. 1960 May 14;1(7133):1045–1048. doi: 10.1016/s0140-6736(60)90932-6. [DOI] [PubMed] [Google Scholar]
  31. Gafter U., Komlos L., Weinstein T., Zevin D., Levi J. Thrombocytopenia, eosinophilia, and ranitidine. Ann Intern Med. 1987 Mar;106(3):477–477. doi: 10.7326/0003-4819-106-3-477_1. [DOI] [PubMed] [Google Scholar]
  32. Gregory R. A., Grossman M. I., Tracy H. J., Bentley P. H. Nature of the gastric secretagogue in Zollinger-Ellison tumours. Lancet. 1967 Sep 9;2(7515):543–544. doi: 10.1016/s0140-6736(67)90501-6. [DOI] [PubMed] [Google Scholar]
  33. Harris A. I., Greenberg H. Pernicious anemia and the development of carcinoid tumors of the stomach. JAMA. 1978 Mar 20;239(12):1160–1161. [PubMed] [Google Scholar]
  34. Howard J. M., Chremos A. N., Collen M. J., McArthur K. E., Cherner J. A., Maton P. N., Ciarleglio C. A., Cornelius M. J., Gardner J. D., Jensen R. T. Famotidine, a new, potent, long-acting histamine H2-receptor antagonist: comparison with cimetidine and ranitidine in the treatment of Zollinger-Ellison syndrome. Gastroenterology. 1985 Apr;88(4):1026–1033. doi: 10.1016/s0016-5085(85)80024-x. [DOI] [PubMed] [Google Scholar]
  35. Howden C. W., Forrest J. A., Reid J. L. Effects of single and repeated doses of omeprazole on gastric acid and pepsin secretion in man. Gut. 1984 Jul;25(7):707–710. doi: 10.1136/gut.25.7.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ingemansson S., Larsson L. I., Lunderquist A., Stadil F. Pancreatic vein catheterization with gastrin assay in normal patients and in patients with the Zollinger-Ellison syndrome. Am J Surg. 1977 Nov;134(5):558–563. doi: 10.1016/0002-9610(77)90433-0. [DOI] [PubMed] [Google Scholar]
  37. Isenberg J. I., Walsh J. H., Passaro E., Jr, Moore E. W., Grossman M. I. Unusual effect of secretin on serum gastrin, serum calcium, and gastric acid secretion in a patient with suspected Zollinger-Ellison syndrome. Gastroenterology. 1972 Apr;62(4):626–631. [PubMed] [Google Scholar]
  38. Jackson I. M., Barnard L. B., Lamberton P. Role of a long-acting somatostatin analogue (SMS 201-995) in the treatment of acromegaly. Am J Med. 1986 Dec 22;81(6B):94–101. doi: 10.1016/0002-9343(86)90590-5. [DOI] [PubMed] [Google Scholar]
  39. Jaspan J., Polonsky K., Lewis M., Moossa A. R. Reduction in portal vein blood flow by somatostatin. Diabetes. 1979 Oct;28(10):888–892. doi: 10.2337/diab.28.10.888. [DOI] [PubMed] [Google Scholar]
  40. Jensen R. T. Basis for failure of cimetidine in patients with Zollinger-Ellison syndrome. Dig Dis Sci. 1984 Apr;29(4):363–366. doi: 10.1007/BF01318525. [DOI] [PubMed] [Google Scholar]
  41. Jensen R. T., Collen M. J., McArthur K. E., Howard J. M., Maton P. N., Cherner J. A., Gardner J. D. Comparison of the effectiveness of ranitidine and cimetidine in inhibiting acid secretion in patients with gastric hypersecretory states. Am J Med. 1984 Nov 19;77(5B):90–105. [PubMed] [Google Scholar]
  42. Jensen R. T., Collen M. J., Pandol S. J., Allende H. D., Raufman J. P., Bissonnette B. M., Duncan W. C., Durgin P. L., Gillin J. C., Gardner J. D. Cimetidine-induced impotence and breast changes in patients with gastric hypersecretory states. N Engl J Med. 1983 Apr 14;308(15):883–887. doi: 10.1056/NEJM198304143081508. [DOI] [PubMed] [Google Scholar]
  43. Jensen R. T., Gardner J. D., Raufman J. P., Pandol S. J., Doppman J. L., Collen M. J. Zollinger-Ellison syndrome: current concepts and management. Ann Intern Med. 1983 Jan;98(1):59–75. doi: 10.7326/0003-4819-98-1-59. [DOI] [PubMed] [Google Scholar]
  44. Kothary P. C., Fabri P. J., Gower W., O'Dorisio T. M., Ellis J., Vinik A. I. Evaluation of NH2-terminus gastrins in gastrinoma syndrome. J Clin Endocrinol Metab. 1986 May;62(5):970–974. doi: 10.1210/jcem-62-5-970. [DOI] [PubMed] [Google Scholar]
  45. Kraenzlin M. E., Ch'ng J. L., Wood S. M., Carr D. H., Bloom S. R. Long-term treatment of a VIPoma with somatostatin analogue resulting in remission of symptoms and possible shrinkage of metastases. Gastroenterology. 1985 Jan;88(1 Pt 1):185–187. doi: 10.1016/s0016-5085(85)80153-0. [DOI] [PubMed] [Google Scholar]
  46. Krudy A. G., Doppman J. L., Jensen R. T., Norton J. A., Collen M. J., Shawker T. H., Gardner J. D., McArthur K., Gorden P. Localization of islet cell tumors by dynamic CT: comparison with plain CT, arteriography, sonography, and venous sampling. AJR Am J Roentgenol. 1984 Sep;143(3):585–589. doi: 10.2214/ajr.143.3.585. [DOI] [PubMed] [Google Scholar]
  47. Kvols L. K., Buck M. Chemotherapy of metastatic carcinoid and islet cell tumors. A review. Am J Med. 1987 May 29;82(5B):77–83. doi: 10.1016/0002-9343(87)90430-x. [DOI] [PubMed] [Google Scholar]
  48. Kvols L. K., Moertel C. G., O'Connell M. J., Schutt A. J., Rubin J., Hahn R. G. Treatment of the malignant carcinoid syndrome. Evaluation of a long-acting somatostatin analogue. N Engl J Med. 1986 Sep 11;315(11):663–666. doi: 10.1056/NEJM198609113151102. [DOI] [PubMed] [Google Scholar]
  49. Lambers C. B., Lind T., Moberg S., Jansen J. B., Olbe L. Omeprazole in Zollinger-Ellison syndrome. Effects of a single dose and of long-term treatment in patients resistant to histamine H2-receptor antagonists. N Engl J Med. 1984 Mar 22;310(12):758–761. doi: 10.1056/NEJM198403223101205. [DOI] [PubMed] [Google Scholar]
  50. Landor J. H. Control of the Zollinger-Ellison syndrome by excision of primary and metastatic tumor. Am J Surg. 1984 Mar;147(3):406–409. doi: 10.1016/0002-9610(84)90178-8. [DOI] [PubMed] [Google Scholar]
  51. Lind S. E., Weitzman S. A. The insidious development of symptomatic secondary hormone syndromes in patients with malignant endocrine tumors. Am J Med Sci. 1985 Sep;290(3):107–110. doi: 10.1097/00000441-198509000-00005. [DOI] [PubMed] [Google Scholar]
  52. Lips C. J., van der Sluys V., van der Donk J. A., van Dam R. H. Common precursor molecule as origin for the ectopic-hormone-producing-tumour syndrome. Lancet. 1978 Jan 7;1(8054):16–18. doi: 10.1016/s0140-6736(78)90361-6. [DOI] [PubMed] [Google Scholar]
  53. Macleod A. F., Ayers B., Young A. E., Medd W. E., Sönksen P. H. Resolution of hypergastrinaemia after parathyroidectomy in multiple endocrine neoplasia syndrome type I (MEN type I). Clin Endocrinol (Oxf) 1987 Jun;26(6):693–698. doi: 10.1111/j.1365-2265.1987.tb00827.x. [DOI] [PubMed] [Google Scholar]
  54. Malagelada J. R., Edis A. J., Adson M. A., van Heerden J. A., Go V. L. Medical and surgical options in the management of patients with gastrinoma. Gastroenterology. 1983 Jun;84(6):1524–1532. [PubMed] [Google Scholar]
  55. Maton P. N., Gardner J. D., Jensen R. T. Cushing's syndrome in patients with the Zollinger-Ellison syndrome. N Engl J Med. 1986 Jul 3;315(1):1–5. doi: 10.1056/NEJM198607033150101. [DOI] [PubMed] [Google Scholar]
  56. 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]
  57. Maton P. N., Vinayek R., Frucht H., McArthur K. A., Miller L. S., Saeed Z. A., Gardner J. D., Jensen R. T. Long-term efficacy and safety of omeprazole in patients with Zollinger-Ellison syndrome: a prospective study. Gastroenterology. 1989 Oct;97(4):827–836. doi: 10.1016/0016-5085(89)91485-6. [DOI] [PubMed] [Google Scholar]
  58. McCarthy D. M. Report on the United States experience with cimetidine in Zollinger-Ellision syndrome and other hypersecretory states. Gastroenterology. 1978 Feb;74(2 Pt 2):453–458. [PubMed] [Google Scholar]
  59. McGuigan J. E., Trudeau W. L. Immunochemical measurement of elevated levels of gastrin in the serum of patients with pancreatic tumors of the Zollinger-Ellison variety. N Engl J Med. 1968 Jun 13;278(24):1308–1313. doi: 10.1056/NEJM196806132782402. [DOI] [PubMed] [Google Scholar]
  60. McGuigan J. E., Wolfe M. M. Secretin injection test in the diagnosis of gastrinoma. Gastroenterology. 1980 Dec;79(6):1324–1331. [PubMed] [Google Scholar]
  61. McIntosh C., Arnold R., Bothe E., Becker H., Köbberling J., Creutzfeldt W. Gastrointestinal somatostatin: extraction and radioimmunoassay in different species. Gut. 1978 Jul;19(7):655–663. doi: 10.1136/gut.19.7.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Meyers C. A., Coy D. H., Huang W. Y., Schally A. V., Redding T. W. Highly active position eight analogues of somatostatin and separation of peptide diastereomers by partition chromatography. Biochemistry. 1978 Jun 13;17(12):2326–2331. doi: 10.1021/bi00605a011. [DOI] [PubMed] [Google Scholar]
  63. Mignon M., Ruszniewski P., Haffar S., Rigaud D., Rene E., Bonfils S. Current approach to the management of tumoral process in patients with gastrinoma. World J Surg. 1986 Aug;10(4):703–710. doi: 10.1007/BF01655562. [DOI] [PubMed] [Google Scholar]
  64. Mills S. R., Doppman J. L., Dunnick N. R., McCarthy D. M. Evaluation of angiography in Zollinger-Ellison syndrome. Radiology. 1979 May;131(2):317–320. doi: 10.1148/131.2.317. [DOI] [PubMed] [Google Scholar]
  65. Miyata M., Nakao K., Sakamoto T., Tsumori T., Hamaji M., Himeno S., Kawashima Y. Removal of mesenteric gastrinoma: a case report. Surgery. 1986 Feb;99(2):245–248. [PubMed] [Google Scholar]
  66. Modlin I. M., Jaffe B. M., Sank A., Albert D. The early diagnosis of gastrinoma. Ann Surg. 1982 Nov;196(5):512–517. doi: 10.1097/00000658-198211000-00002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Moertel C. G., Hanley J. A., Johnson L. A. Streptozocin alone compared with streptozocin plus fluorouracil in the treatment of advanced islet-cell carcinoma. N Engl J Med. 1980 Nov 20;303(21):1189–1194. doi: 10.1056/NEJM198011203032101. [DOI] [PubMed] [Google Scholar]
  68. Moertel C. G., Lavin P. T., Hahn R. G. Phase II trial of doxorubicin therapy for advanced islet cell carcinoma. Cancer Treat Rep. 1982 Jul;66(7):1567–1569. [PubMed] [Google Scholar]
  69. Moertel C. G., Reitemeier R. J., Schutt A. J., Hahn R. G. Phase II study of strepozotocin (NSC-85998) in the treatment of advanced gastrointestinal cancer. Cancer Chemother Rep. 1971 Jun;55(3):303–307. [PubMed] [Google Scholar]
  70. Morgan J. E., Kaiser C. W., Johnson W., Doos W. G., Dayal Y., Berman L., Nabseth D. Gastric carcinoid (gastrinoma) associated with achlorhydria (pernicious anemia). Cancer. 1983 Jun 15;51(12):2332–2340. doi: 10.1002/1097-0142(19830615)51:12<2332::aid-cncr2820511228>3.0.co;2-i. [DOI] [PubMed] [Google Scholar]
  71. Murray-Lyon I. M., Eddleston A. L., Williams R., Brown M., Hogbin B. M., Bennett A., Edwards J. C., Taylor K. W. Treatment of multiple-hormone-producing malignant islet-cell tumour with streptozotocin. Lancet. 1968 Oct 26;2(7574):895–898. doi: 10.1016/s0140-6736(68)91058-1. [DOI] [PubMed] [Google Scholar]
  72. Norton J. A., Cornelius M. J., Doppman J. L., Maton P. N., Gardner J. D., Jensen R. T. Effect of parathyroidectomy in patients with hyperparathyroidism, Zollinger-Ellison syndrome, and multiple endocrine neoplasia type I: a prospective study. Surgery. 1987 Dec;102(6):958–966. [PubMed] [Google Scholar]
  73. Norton J. A., Cromack D. T., Shawker T. H., Doppman J. L., Comi R., Gorden P., Maton P. N., Gardner J. D., Jensen R. T. Intraoperative ultrasonographic localization of islet cell tumors. A prospective comparison to palpation. Ann Surg. 1988 Feb;207(2):160–168. doi: 10.1097/00000658-198802000-00008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Norton J. A., Doppman J. L., Collen M. J., Harmon J. W., Maton P. N., Gardner J. D., Jensen R. T. Prospective study of gastrinoma localization and resection in patients with Zollinger-Ellison syndrome. Ann Surg. 1986 Oct;204(4):468–479. doi: 10.1097/00000658-198610000-00015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Norton J. A., Sugarbaker P. H., Doppman J. L., Wesley R. A., Maton P. N., Gardner J. D., Jensen R. T. Aggressive resection of metastatic disease in selected patients with malignant gastrinoma. Ann Surg. 1986 Apr;203(4):352–359. doi: 10.1097/00000658-198604000-00003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. O'Neal L. W., Kipnis D. M., Luse S. A., Lacy P. E., Jarett L. Secretion of various endocrine substances by ACTH-secreting tumors--gastrin, melanotropin, norepinephrine, serotonin, parathormone, vasopressin, glucagon. Cancer. 1968 Jun;21(6):1219–1232. doi: 10.1002/1097-0142(196806)21:6<1219::aid-cncr2820210625>3.0.co;2-m. [DOI] [PubMed] [Google Scholar]
  78. Parrish J. A., Rawlins D. C. Intestinal mucosa in the Zollinger-Ellison syndrome. Gut. 1965 Jun;6(3):286–289. doi: 10.1136/gut.6.3.286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Pauwels S., Desmond H., Dimaline R., Dockray G. J. Identification of progastrin in gastrinomas, antrum, and duodenum by a novel radioimmunoassay. J Clin Invest. 1986 Feb;77(2):376–381. doi: 10.1172/JCI112315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Price B. A., Jaffe B. M., Zinner M. J. The effect of somatostatin on central hemodynamics, renal blood flow, and renal function in dogs. Surgery. 1985 Mar;97(3):285–289. [PubMed] [Google Scholar]
  81. RAWSON A. B., ENGLAND M. T., GILLAM G. G., FRENCH J. M., STAMMERS F. A. Zollinger-Ellison syndrome with diarrhoea and malabsorption. Observations on a patient before and after pancreatic islet-cell tumour removal with-out resort. Lancet. 1960 Jul 16;2(7142):131–134. doi: 10.1016/s0140-6736(60)91271-x. [DOI] [PubMed] [Google Scholar]
  82. Raptis S., Dollinger H. C., von Berger L., Schlegel W., Schröder K. E., Pfeiffer E. F. Effects of somatostatin on gastric secretion and gastrin release in man. Digestion. 1975;13(1-2):15–26. doi: 10.1159/000197691. [DOI] [PubMed] [Google Scholar]
  83. Raufman J. P., Collins S. M., Pandol S. J., Korman L. Y., Collen M. J., Cornelius M. J., Feld M. K., McCarthy D. M., Gardner J. D., Jensen R. T. Reliability of symptoms in assessing control of gastric acid secretion in patients with Zollinger-Ellison syndrome. Gastroenterology. 1983 Jan;84(1):108–113. [PubMed] [Google Scholar]
  84. Richardson C. T., Feldman M., McClelland R. N., Dickerman R. M., Kumpuris D., Fordtran J. S. Effect of vagotomy in Zollinger-Ellison syndrome. Gastroenterology. 1979 Oct;77(4 Pt 1):682–686. [PubMed] [Google Scholar]
  85. Richter J. E., Pandol S. J., Castell D. O., McCarthy D. M. Gastroesophageal reflux disease in the Zollinger-Ellison syndrome. Ann Intern Med. 1981 Jul;95(1):37–43. doi: 10.7326/0003-4819-95-1-37. [DOI] [PubMed] [Google Scholar]
  86. Roche A., Raisonnier A., Gillon-Savouret M. C. Pancreatic venous sampling and arteriography in localizing insulinomas and gastrinomas: procedure and results in 55 cases. Radiology. 1982 Dec;145(3):621–627. doi: 10.1148/radiology.145.3.6292994. [DOI] [PubMed] [Google Scholar]
  87. Romanus M. E., Neal J. A., Dilley W. G., Leight G. S., Linehan W. M., Santen R. J., Farndon J. R., Jones R. S., Wells S. A., Jr Comparison of four provocative tests for the diagnosis of gastrinoma. Ann Surg. 1983 May;197(5):608–617. doi: 10.1097/00000658-198305000-00015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Schally A. V. Oncological applications of somatostatin analogues. Cancer Res. 1988 Dec 15;48(24 Pt 1):6977–6985. [PubMed] [Google Scholar]
  89. Seal A., Yamada T., Debas H., Hollinshead J., Osadchey B., Aponte G., Walsh J. Somatostatin-14 and -28: clearance and potency on gastric function in dogs. Am J Physiol. 1982 Aug;243(2):G97–102. doi: 10.1152/ajpgi.1982.243.2.G97. [DOI] [PubMed] [Google Scholar]
  90. Shepherd J. J., Senator G. B. Regression of liver metastases in patient with gastrin-secreting tumour treated with SMS 201-995. Lancet. 1986 Sep 6;2(8506):574–574. doi: 10.1016/s0140-6736(86)90139-x. [DOI] [PubMed] [Google Scholar]
  91. Sheppard M., Shapiro B., Pimstone B., Kronheim S., Berelowitz M., Gregory M. Metabolic clearance and plasma half-disappearance time of exogenous somatostatin in man. J Clin Endocrinol Metab. 1979 Jan;48(1):50–53. doi: 10.1210/jcem-48-1-50. [DOI] [PubMed] [Google Scholar]
  92. Sigel B., Machi J., Ramos J. R., Duarte B., Donahue P. E. The role of imaging ultrasound during pancreatic surgery. Ann Surg. 1984 Oct;200(4):486–493. doi: 10.1097/00000658-198410000-00010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Stabile B. E., Ippoliti A. F., Walsh J. H., Passaro E., Jr Failure of histamine H2-receptor antagonist therapy in Zollinger-Ellison syndrome. Am J Surg. 1983 Jan;145(1):17–23. doi: 10.1016/0002-9610(83)90160-5. [DOI] [PubMed] [Google Scholar]
  94. Stabile B. E., Morrow D. J., Passaro E., Jr The gastrinoma triangle: operative implications. Am J Surg. 1984 Jan;147(1):25–31. doi: 10.1016/0002-9610(84)90029-1. [DOI] [PubMed] [Google Scholar]
  95. Stabile B. E., Passaro E., Jr Benign and malignant gastrinoma. Am J Surg. 1985 Jan;149(1):144–150. doi: 10.1016/s0002-9610(85)80024-6. [DOI] [PubMed] [Google Scholar]
  96. Stadil F., Stage G., Rehfeld J. F., Efsen F., Fischerman K. Treatment of Zollinger-Ellison syndrome with streptozotocin. N Engl J Med. 1976 Jun 24;294(26):1440–1442. doi: 10.1056/NEJM197606242942608. [DOI] [PubMed] [Google Scholar]
  97. Stage J. G., Stadil F. The clinical diagnosis of the Zollinger-Ellison syndrome. Scand J Gastroenterol Suppl. 1979;53:79–91. [PubMed] [Google Scholar]
  98. Stark D. D., Moss A. A., Goldberg H. I., Davis P. L., Federle M. P. Magnetic resonance and CT of the normal and diseased pancreas: a comparative study. Radiology. 1984 Jan;150(1):153–162. doi: 10.1148/radiology.150.1.6689755. [DOI] [PubMed] [Google Scholar]
  99. Stark D. D., Moss A. A., Goldberg H. I., Deveney C. W. CT of pancreatic islet cell tumors. Radiology. 1984 Feb;150(2):491–494. doi: 10.1148/radiology.150.2.6318260. [DOI] [PubMed] [Google Scholar]
  100. Thompson J. C., Lewis B. G., Wiener I., Townsend C. M., Jr The role of surgery in the Zollinger-Ellison syndrome. Ann Surg. 1983 May;197(5):594–607. doi: 10.1097/00000658-198305000-00014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Thompson J. C., Reeder D. D., Villar H. V., Fender H. R. Natural history and experience with diagnosis and treatment of the Zollinger-Ellison syndrome. Surg Gynecol Obstet. 1975 May;140(5):721–739. [PubMed] [Google Scholar]
  102. Thompson N. W., Lloyd R. V., Nishiyama R. H., Vinik A. I., Strodel W. E., Allo M. D., Eckhauser F. E., Talpos G., Mervak T. MEN I pancreas: a histological and immunohistochemical study. World J Surg. 1984 Aug;8(4):561–574. doi: 10.1007/BF01654938. [DOI] [PubMed] [Google Scholar]
  103. Tielemans Y., Håkanson R., Sundler F., Willems G. Proliferation of enterochromaffinlike cells in omeprazole-treated hypergastrinemic rats. Gastroenterology. 1989 Mar;96(3):723–729. [PubMed] [Google Scholar]
  104. Upp J. R., Jr, Olson D., Poston G. J., Alexander R. W., Townsend C. M., Jr, Thompson J. C. Inhibition of growth of two human pancreatic adenocarcinomas in vivo by somatostatin analog SMS 201-995. Am J Surg. 1988 Jan;155(1):29–35. doi: 10.1016/s0002-9610(88)80254-x. [DOI] [PubMed] [Google Scholar]
  105. Vinayek R., Howard J. M., Maton P. N., Wank S. A., Slaff J. I., Gardner J. D., Jensen R. T. Famotidine in the therapy of gastric hypersecretory states. Am J Med. 1986 Oct 24;81(4B):49–59. doi: 10.1016/0002-9343(86)90600-5. [DOI] [PubMed] [Google Scholar]
  106. Vinik A. I., Tsai S. T., Moattari A. R., Cheung P., Eckhauser F. E., Cho K. Somatostatin analogue (SMS 201-995) in the management of gastroenteropancreatic tumors and diarrhea syndromes. Am J Med. 1986 Dec 22;81(6B):23–40. doi: 10.1016/0002-9343(86)90582-6. [DOI] [PubMed] [Google Scholar]
  107. Walan A., Bader J. P., Classen M., Lamers C. B., Piper D. W., Rutgersson K., Eriksson S. Effect of omeprazole and ranitidine on ulcer healing and relapse rates in patients with benign gastric ulcer. N Engl J Med. 1989 Jan 12;320(2):69–75. doi: 10.1056/NEJM198901123200201. [DOI] [PubMed] [Google Scholar]
  108. 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]
  109. Weber C., Merriam L., Koschitzky T., Karp F., Benson M., Forde K., LoGerfo P. Inhibition of growth of human breast carcinomas in vivo by somatostatin analog SMS 201-995: treatment of nude mouse xenografts. Surgery. 1989 Aug;106(2):416–422. [PubMed] [Google Scholar]
  110. Wilson S. D. The role of surgery in children with the Zollinger-Ellison syndrome. Surgery. 1982 Oct;92(4):682–692. [PubMed] [Google Scholar]
  111. Wolfe M. M., Alexander R. W., McGuigan J. E. Extrapancreatic, extraintestinal gastrinoma: effective treatment by surgery. N Engl J Med. 1982 Jun 24;306(25):1533–1536. doi: 10.1056/NEJM198206243062506. [DOI] [PubMed] [Google Scholar]
  112. Wolfe M. M., Jensen R. T. Zollinger-Ellison syndrome. Current concepts in diagnosis and management. N Engl J Med. 1987 Nov 5;317(19):1200–1209. doi: 10.1056/NEJM198711053171907. [DOI] [PubMed] [Google Scholar]
  113. Wynick D., Williams S. J., Bloom S. R. Symptomatic secondary hormone syndromes in patients with established malignant pancreatic endocrine tumors. N Engl J Med. 1988 Sep 8;319(10):605–607. doi: 10.1056/NEJM198809083191003. [DOI] [PubMed] [Google Scholar]
  114. ZOLLINGER R. M., ELLISON E. H. Primary peptic ulcerations of the jejunum associated with islet cell tumors of the pancreas. Ann Surg. 1955 Oct;142(4):709-23; discussion, 724-8. [PMC free article] [PubMed] [Google Scholar]
  115. Zollinger R. M., Ellison E. C., Fabri P. J., Johnson J., Sparks J., Carey L. C. Primary peptic ulcerations of the jejunum associated with islet cell tumors. Twenty-five-year appraisal. Ann Surg. 1980 Sep;192(3):422–430. doi: 10.1097/00000658-198009000-00018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Zollinger R. M., Ellison E. C., O'Dorisio T. M., Sparks J. Thirty years' experience with gastrinoma. World J Surg. 1984 Aug;8(4):427–435. doi: 10.1007/BF01654904. [DOI] [PubMed] [Google Scholar]
  117. Zollinger R. M. Gastrinoma: factors influencing prognosis. Surgery. 1985 Jan;97(1):49–54. [PubMed] [Google Scholar]
  118. Zollinger R. M., Martin E. W., Jr, Carey L. C., Sparks J., Minton J. P. Observations on the postoperative tumor growth behavior of certain islet cell tumors. Ann Surg. 1976 Oct;184(4):525–530. doi: 10.1097/00000658-197610000-00016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Zollinger R. M., Moore F. T. Zollinger-Ellison syndrome comes of age. Recognition of the complete clinical spectrum and its management. JAMA. 1968 Apr 29;204(5):361–365. [PubMed] [Google Scholar]

Articles from Annals of Surgery are provided here courtesy of Lippincott, Williams, and Wilkins

RESOURCES