Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Endocrine
Published in: Endocrine 1/2018

01-04-2018 | Review

The Zollinger-Ellison syndrome: is there a role for somatostatin analogues in the treatment of the gastrinoma?

Authors: Valentina Guarnotta, Chiara Martini, Maria Vittoria Davì, Genoveffa Pizza, Annamaria Colao, Antongiulio Faggiano, on behalf of NIKE group

Published in: Endocrine | Issue 1/2018

Login to get access

Abstract

Purpose

Analyze the role of somatostatin analogues (SSAs) in the treatment of sporadic and MEN1-related gastrinomas, trying to define whether recent trials have changed the landscape of gastrinoma therapy.

Methods

We evaluate the rationale of SSA use in the treatment of gastrinomas, summarize the current literature concerning the effect of SSAs on the control of Zollinger-Ellison syndrome (ZES) and gastrinomas tumor progression and discuss their role in the most recent guidelines.

Results

The medical treatment of gastrinoma and related ZES is aimed at controlling acid hypersecretion and tumor progression, in inoperable patients. The use of proton pump inhibitors (PPIs) to control the syndrome is a cornerstone in the ZES therapy. SSAs are not usually indicated for antisecretory purpose, because PPIs are considered the treatment of choice, due to their long lasting high efficacy and oral availability. The antiproliferative effect of SSAs has been established by two placebo-controlled trials that have clearly demonstrated a significant increase in progression free survival in patients affected by non-functioning well-differentiated advanced neuroendocrine tumors (NETs). The recent ENETS guidelines recommend the use of SSAs in advanced well differentiated NETs as antiproliferative agents.

Conclusions

The high sstr-expression in gastrinomas make them highly responsive to SSAs and support the use of such drugs to counteract the tumour growth in patients not amenable to surgical cure. Unfortunately, limited data, mainly case reports or small series, support the use of SSAs in advanced gastrinomas, therefore, it is difficult to quantify their ability to control tumour growth and disease progression.
Literature
1.
R.M. Zollinger, E.H. Ellison, Primary peptic ulcerations of the jejunum associated with islet cell tumors of the pancreas. Ann. Surg. 142, 709–728 (1955)PubMedPubMedCentralCrossRef
2.
J.E. McGuigan, M.M. Wolfe, Secretin injection test in the diagnosis of gastrinoma. Gastroenterology 79, 1324–1331 (1980)PubMed
3.
E.C. Ellison, J.A. Johnson, The Zollinger-Ellison syndrome: a comprehensive review of historical, scientific, and clinical considerations. Curr. Probl. Surg. 46, 13–106 (2009)PubMedCrossRef
4.
G.A. Kaltsas, G.M. Besser, A.B. Grossman, The diagnosis and medical management of advanced neuroendocrine tumors. Endocr. Rev. 25, 458–511 (2004)PubMedCrossRef
5.
M.J. Berna, K.M. Hoffmann, J. Serrano, F. Gibril, R.T. Jensen, Serum gastrin in Zollinger-Ellison syndrome: i. Prospective study of fasting serum gastrin in 309 patients from the National Institutes of Health and comparison with 2229 cases from the literature. Medicine 85, 295–330 (2006)PubMedCrossRef
6.
J.A. Norton, Neuroendocrine tumors of the pancreas and duodenum. Curr. Probl. Surg. 31, 77–156 (1994)PubMedCrossRef
7.
8.
R.V. Thakker, P.J. Newey, G.V. Walls, J. Bilezikian, H. Dralle, P.R. Ebeling, S. Melmed, A. Sakurai, F. Tonelli, M.L. Brandi, Clinical practice guidelines for multiple endocrine neoplasia type 1 (MEN1). J. Clin. Endocrinol. Metabol. 97, 2990–3011 (2012)CrossRef
9.
F. Gibril, R.T. Jensen, Zollinger-Ellison syndrome revisited: diagnosis, biologic markers, associated inherited disorders, and acid hypersecretion. Curr. Gastroenterol. Rep. 6, 454–463 (2004)PubMedCrossRef
10.
M.V. Davì, L. Boninsegna, L. Dalle Carbonare, M. Toaiari, P. Capelli, A. Scarpa, G. Francia, M. Falconi, Presentation and outcome of pancreaticoduodenal endocrine tumors in multiple endocrine neoplasia type 1 syndrome. Neuroendocrinology 94, 58–65 (2011)PubMedCrossRef
11.
J.A. Norton, D.J. Venzon, M.J. Berna, H.R. Alexander, D.L. Fraker, S.K. Libutti, S.J. Marx, F. Gibril, R.T. Jensen, Prospective study of surgery for primary hyperparathyroidism (HPT) in multiple endocrine neoplasia-type 1 and Zollinger-Ellison syndrome: long-term outcome of a more virulent form of HPT. Ann. Surg. 247, 501–510 (2008)PubMedPubMedCentralCrossRef
12.
C. Donow, M. Pipeleers-Marichal, S. Schroder, B. Stamm, P.U. Heitz, G. Klöppel, Surgical pathology of gastrinoma. Site, size, multicentricity, association with multiple endocrine neoplasia type 1, and malignancy. Cancer 68, 1329–1334 (1991)PubMedCrossRef
13.
S. Wilkinson, B.T. Teh, K.R. Davey, J.P. McArdle, M. Young, J.J. Shepherd, Cause of death in multiple endocrine neoplasia type 1. Arch. Surg. 128, 683–690 (1993)PubMedCrossRef
14.
K.M. Hoffmann, M. Furukawa, R.T. Jensen, Duodenal neuroendocrine tumors: classification, functional syndromes, diagnosis and medical treatment.Best Pract. Res. Clin. Gastroenterol. 19, 675–697 (2005)PubMedCrossRef
15.
T. Ito, H. Igarashi, H. Uehara, M.J. Berna, R.T. Jensen, Causes of death and prognostic factors in multiple endocrine neoplasia type 1: a prospective study: comparison of 106 MEN1/Zollinger-Ellison syndrome patients with 1613 literature MEN1 patients with or without pancreatic endocrine tumors. Medicine 92, 135–181 (2013)PubMedPubMedCentralCrossRef
16.
M.J. Berna, K.M. Hoffmann, S.H. Long, J. Serrano, F. Gibril, R.T. Jensen, Serum gastrin in Zollinger-Ellison syndrome: II. Prospective study of gastrin provocative testing in 293 patients from the National Institutes of Health and comparison with 537 cases from the literature. Evaluation of diagnostic criteria, proposal of new criteria, and correlations with clinical and tumoral features. Medicine 85, 331–364 (2006)PubMedCrossRef
17.
P. Poitras, M.H. Gingras, J.F. Rehfeld, The Zollinger-Ellison syndrome: dangers and consequences of interrupting antisecretory treatment. Clin. Gastroenterol. Hepatol. 10, 199–202 (2012)PubMedCrossRef
18.
M. Falconi, B. Eriksson, G. Kaltsas, D.K. Bartsch, J. Capdevila, M. Caplin, B. Kos-Kudla, D. Kwekkeboom, G. Rindi, G. Klöppel, N. Reed, R. Kianmanesh, R.T. Jensen, ENETS consensus guidelines update for the management of patients with functional pancreatic neuroendocrine tumors and non-functional pancreatic neuroendocrine tumors. Neuroendocrinology 103, 153–171 (2016)PubMedPubMedCentralCrossRef
19.
S.A. Deppen, E. Liu, J.D. Blume, J. Clanton, C. Shi, L.B. Jones-Jackson, V. Lakhani, R.P. Baum, J. Berlin, G.T. Smith, M. Graham, M.P. Sandler, D. Delbeke, R.C. Walker, Safety and efficacy of 68Ga-DOTATATE PET/CT for diagnosis, staging and treatment management of neuroendocrine tumors. J. Nucl. Med. 57, 708–714 (2016)PubMedPubMedCentralCrossRef
20.
D.M. McCarthy, Report on the United States experience with cimetidine in Zollinger-Ellison syndrome and other hypersecretory states. Gastroenterology 74, 453–458 (1978)PubMed
21.
D.C. Metz, D.B. Strader, M. Orbuch, P.D. Koviack, K.M. Feigenbaum, R.T. Jensen, Use of omeprazole in Zollinger-Ellison syndrome: a prospective nine-year study of efficacy and safety. Aliment. Pharmacol. Ther. 7, 597–610 (1993)PubMedCrossRef
22.
P.S. Fox, J.W. Hofmann, J.J. Decosse, S.D. Wilson, The influence of total gastrectomy on survival in malignant Zollinger-Ellison tumors. Ann. Surg. 180, 558–566 (1974)PubMedPubMedCentralCrossRef
23.
R.M. Zollinger, E.C. Ellison, P.J. Fabri, J. Johnson, J. Sparks, L.C. Carey, Primary peptic ulcerations of the jejunum associated with islet cell tumors. Twenty-five-year appraisal. Ann. Surg. 192, 422–430 (1980)PubMedPubMedCentralCrossRef
24.
D.L. Fraker, J.A. Norton, Z.A. Saeed, P.N. Maton, J.D. Gardner, R.T. Jensen, A prospective study of perioperative and postoperative control of acid hypersecretion in patients with Zollinger-Ellison syndrome undergoing gastrinoma resection. Surgery 104, 1054–1063 (1988)PubMed
25.
C.J. Auernhammer, B. Göke, Medical treatment of gastrinomas. Wien. Klin. Wochenschr. 119, 609–615 (2007)PubMedCrossRef
26.
C.M. Wilcox, T. Seay, J.T. Arcury, J. Mohnen, B.I. Hirschowitz, Zollinger-Ellison syndrome: presentation, response to therapy, and outcome. Dig. Liver Dis. 43, 439–443 (2011)PubMedCrossRef
27.
28.
M.F. Brennan, R.T. Jensen, R.A. Wesley, J.L. Doppman, D.M. McCarthy, The role of surgery in patients with Zollinger-Ellison syndrome managed medically. Ann. Surg. 196, 239–245 (1982)PubMedPubMedCentralCrossRef
29.
E.C. Ellison, B.S. Sparks, Zollinger-Ellison syndrome in the era of effective acid suppression: are we unknowingly growing tumors? Am. J. Surg. 186, 245–248 (2003)PubMedCrossRef
30.
J.A. Norton, R.T. Jensen, Role of Surgery in Zollinger-Ellison Syndrome. J. Am. Coll. Surg. 205, 834–837 (2007)CrossRef
31.
J.A. Norton, H.R. Alexander, D.L. Fraker, D.J. Venzon, F. Gibril, R.T. Jensen, Does the use of routine duodenotomy (DUODX) affect rate of cure, development of liver metastases, or survival in patients with Zollinger-Ellison syndrome? Ann. Surg. 239, 617–625 (2004)PubMedPubMedCentralCrossRef
32.
G.W. Krampitz, J.A. Norton, Current management of the Zollinger-Ellison syndrome. Adv. Surg. 47, 59–79 (2013)PubMedCrossRef
33.
J.A. Norton, D.L. Fraker, H.R. Alexander, D.J. Venzon, J.L. Doppman, J. Serrano, S.U. Goebel, P.L. Peghini, P.K. Roy, F. Gibril, R.T. Jensen, Surgery to cure the Zollinger-Ellison syndrome. N. Eng. J. Med. 341, 635–644 (1999)CrossRef
34.
J.A. Norton, R.T. Jensen, Resolved and unsolved controversies in the surgical management of patients with Zollinger-Ellison syndrome. Ann. Surg. 240, 757–773 (2004)PubMedPubMedCentralCrossRef
35.
N.W. Thompson, A.I. Vinik, F.E. Eckhauser, Microgastrinoma of the duodenum a cause of failed operations for the Zollinger-Ellison syndrome. Ann. Surg. 209, 396–404 (1989)PubMedPubMedCentralCrossRef
36.
F. Maire, A. Sauvanet, A. Couvelard, V. Rebours, M.P. Vullierme, R. Lebtahi, O. Hentic, J. Belghiti, P. Hammel, P. Lévy, P. Ruszniewski, Recurrence after surgical resection of gastrinoma: who, when, where and why? Eur. J. Gastroenterol. Hepatol. 24, 368–374 (2012)PubMed
37.
J.A. Norton, D.L. Fraker, H.R. Alexander, F. Gibril, D.J. Liewehr, D.J. Venzon, R.T. Jensen, Surgery increases survival in patients with gastrinoma. Ann. Surg. 244, 410–419 (2006)PubMedPubMedCentral
38.
J.A. Norton, D.L. Fraker, H.R. Alexander, R.T. Jensen, Value of surgery in patients with negative imaging and sporadic Zollinger-Ellison syndrome. Ann. Surg. 25, 509–517 (2012)CrossRef
39.
C.L. Lopez, M. Falconi, J. Waldmann, L. Boninsegna, V. Fendrich, P.K. Goretzki, P. Langer, P.H. Kann, S. Partelli, D.K. Bartsch, Partial pancreaticoduodenectomy can provide cure for duodenal gastrinoma associated with multiple endocrine neoplasia type 1. Ann. Surg. 257, 308–314 (2013)PubMedCrossRef
40.
J.A. Norton, T.D. Fang, R.T. Jensen, Surgery for gastrinoma and insulinoma in multiple endocrine neoplasia type 1. J. Natl. Compr. Cancer Netw. 4, 148–153 (2006)CrossRef
41.
42.
C.M. Wilcox, B.I. Hirschowitz, Treatment strategies for Zollinger-Ellison syndrome. Expert Opin. Pharmacother. 10, 1145–1157 (2009)PubMedCrossRef
43.
J.M. Nieto, J.R. Pisegna, The role of proton pump inhibitors in the treatment of Zollinger-Ellison syndrome. Expert. Opin. Pharmacother. 7, 169–175 (2006)PubMedCrossRef
44.
J.A. Ziemniak, M. Madura, A.J. Adamonis, E.J. Olinger, M. Dreyer, J.J. Schentag, Failure of cimetidine in Zollinger-Ellison syndrome. Dig. Dis. Sci. 28, 976–980 (1983)PubMedCrossRef
45.
R.T. Jensen, M.J. Collen, S.J. Pandol, H.D. Allende, J.P. Raufman, B.M. Bissonnette, W.C. Duncan, P.L. Durgin, J.C. Gillin, J.D. Gardner, Cimetidine-induced impotence and breast changes in patients with gastric hypersecretory states. N. Eng. J. Med. 308, 883–887 (1983)CrossRef
46.
M.J. Collen, J.M. Howard, K.E. McArthur, J.P. Raufman, M.J. Cornelius, C.A. Ciarleglio, J.D. Gardner, R.T. Jensen, Comparison of ranitidine and cimetidine in the treatment of gastric hypersecretion. Ann. Intern. Med. 100, 52–58 (1984)PubMedCrossRef
47.
J.M. Howard, A.N. Chremos, M.J. Collen, K.E. McArthur, J.A. Cherner, P.N. Maton, C.A. Ciarleglio, M.J. Cornelius, J.D. Gardner, R.T. Jensen, Famotidine, a new, potent, long-acting histamine H2-receptor antagonist: comparison with cimetidine and ranitidine in the treatment of Zollinger-Ellison syndrome. Gastroenterology 88, 1026–1033 (1985)PubMedCrossRef
48.
B.I. Hirschowitz, J. Simmons, J. Mohnen, Clinical outcome using lansoprazole in acid hypersecretors with and without Zollinger-Ellison syndrome: a 13-year prospective study. Clin. Gastroenterol. Hepatol. 3, 39–48 (2005)PubMedCrossRef
49.
V.D. Corleto, B. Annibale, F. Gibril, S. Angeletti, J. Serrano, D.J. Venzon, G. Delle Fave, R.T. Jensen, Does the widespread use of proton pump inhibitors mask, complicate and /or delay the diagnosis of Zollinger-Ellison syndrome? Aliment. Pharmacol. Ther. 15, 1555–1561 (2001)PubMedCrossRef
50.
P. Shah, M.H. Singh, Y.X. Yang, D.C. Metz, Hypochlorhydria and achlorhydria are associated with false-positive secretin stimulation testing for Zollinger-Ellison syndrome. Pancreas 42, 932–936 (2013)PubMedPubMedCentralCrossRef
51.
T. Ito, R.T. Jensen, Association of long-term proton pump inhibitor therapy with bone fractures and effects on absorption of calcium, vitamin B12, iron, and magnesium. Curr. Gastroenterol. Rep. 12, 448–457 (2010)PubMedPubMedCentralCrossRef
52.
J.M. Ruscin, R.L. Page II, R.J. Valuck, Vitamin B(12) deficiency associated with histamine(2)-receptor antagonists and a proton-pump inhibitor. Ann. Pharmacother. 36, 812–816 (2002)PubMedCrossRef
53.
R.J. Valuck, J.M. Ruscin, A case–control study on adverse effects: H2 blocker or proton pump inhibitor use and risk of vitamin B12 deficiency in older adults. J. Clin. Epidemiol. 57, 422–428 (2004)PubMedCrossRef
54.
W.P. den Elzen, Y. Groeneveld, W. de Ruijter, J.H. Souverijn, S. le Cessie, W.J. Assendelft, J. Gussekloo, Long-term use of proton pump inhibitors and vitamin B12 status in elderly individuals. Aliment. Pharmacol. Ther. 27, 491–497 (2008)CrossRef
55.
J.R. Lam, J.L. Schneider, W. Zhao, D.A. Corley, Proton pump inhibitor and histamine 2 receptor antagonist use and vitamin B12 deficiency. JAMA 310, 2435–2442 (2013)PubMedCrossRef
56.
B. Termanini, F. Gibril, V.E. Sutliff, F. Yu, D.J. Venzon, R.T. Jensen, Effect of long-term gastric acid suppressive therapy on serum vitamin B12 levels in patients with Zollinger-Ellison syndrome. Am. J. Med. 104, 422–430 (1998)PubMedCrossRef
57.
V.R. Sharma, M.A. Brannon, E.A. Carloss, Effect of omeprazole on oral iron replacement in patients with iron deficiency anemia. South. Med. J. 97, 887–889 (2004)PubMedCrossRef
58.
C. Hutchinson, C.A. Geissler, J.J. Powell, A. Bomford, Proton pump inhibitors suppress absorption of dietary non-haem iron in hereditary haemochromatosis. Gut 56, 1291–1295 (2007)PubMedPubMedCentralCrossRef
59.
C.A. Stewart, B. Termanini, V.E. Sutliff, J. Serrano, F. Yu, F. Gibril, R.T. Jensen, Assessment of the risk of iron malabsorption in patients with Zollinger-Ellison syndrome treated with long-term gastric acid antisecretory therapy. Aliment. Pharmacol. Ther. 12, 83–98 (1998)PubMedCrossRef
60.
Y.X. Yang, J.D. Lewis, S. Epstein, D.C. Metz, Long-term proton pump inhibitor therapy and risk of hip fracture. JAMA 296, 2947–2953 (2006)PubMedCrossRef
61.
C. Roux, K. Briot, L. Gossec, S. Kolta, T. Blenk, D. Felsenberg, D.M. Reid, R. Eastell, C.C. Glüer, Increase in vertebral fracture risk in postmenopausal women using omeprazole. Calcif. Tissue Int. 84, 13–19 (2009)PubMedCrossRef
62.
L.E. Targownik, L.M. Lix, C.J. Metge, H.J. Prior, S. Leung, W.D. Leslie, Use of proton pump inhibitors and risk of osteoporosis-related fractures. Can. Med. Assoc. J. 179, 319–326 (2008)CrossRef
63.
P.O. Lewis, J.M. Litchfield, J.L. Tharp, R.M. Garcia, M. Pourmorteza, C.M. Reddy, Risk and severity of hospital-acquired clostridium difficile infection in patients taking proton pump inhibitors. Pharmacotherapy 36, 986–993 (2016)PubMedCrossRef
64.
C. Giuliano, S.M. Wilhelm, P.B. Kale-Pradhan, Are proton pump inhibitors associated with the development of community-acquired pneumonia? A meta-analysis. Expert Rev. Clin. Pharmacol. 5, 337–344 (2012)PubMedCrossRef
65.
P.L. Peghini, B. Annibale, C. Azzoni, M. Milione, V.D. Corleto, F. Gibril, D.J. Venzon, G. Delle Fave, C. Bordi, R.T. Jensen, Effect of chronic hypergastrinemia on human enterochromaffin-like cells: insights from patients with sporadic gastrinomas. Gastroenterology 123, 68–85 (2002)PubMedCrossRef
66.
M.J. Berna, B. Annibale, M. Marignani, T.V. Luong, V. Corleto, A. Pace, T. Ito, D. Liewehr, D.J. Venzon, G. Delle Fave, C. Bordi, R.T. Jensen, A prospective study of gastric carcinoids and enterochromaffin-like cells changes in multiple endocrine neoplasia type 1 and Zollinger-Ellison syndrome: identification of risk factors. J. Clin. Endocrinol. Metabol. 93, 1582–1591 (2008)CrossRef
67.
P.N. Maton, E.E. Lack, M.J. Collen, M.J. Cornelius, E. David, J.D. Gardner, R.T. Jensen, The effect of Zollinger-Ellison syndrome and omeprazole therapy on gastric oxyntic endocrine cells. Gastroenterology 99, 943–950 (1990)PubMedCrossRef
68.
J.C. Yao, M.H. Shah, T. Ito, C.L. Bohas, E.M. Wolin, E. Van Cutsem, T.J. Hobday, T. Okusaka, J. Capdevila, E.G. de Vries, P. Tomassetti, M.E. Pavel, S. Hoosen, T. Haas, J. Lincy, D. Lebwohl, K. Öberg, RAD001 in advanced neuroendocrine tumors, third trial (RADIANT-3) study group. Everolimus for advanced pancreatic neuroendocrine tumors. N. Eng. J. Med. 364, 514–523 (2011)CrossRef
69.
E. Raymond, L. Dahan, J.L. Raoul, Y.J. Bang, I. Borbath, C. Lombard-Bohas, J. Valle, P. Metrakos, D. Smith, A. Vinik, J.S. Chen, D. Hörsch, P. Hammel, B. Wiedenmann, E. Van Cutsem, S. Patyna, D.R. Lu, C. Blanckmeister, R. Chao, P. Ruszniewski, Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N. Eng. J. Med. 364, 501–513 (2011)CrossRef
70.
T. Von Schrenck, J.M. Howard, J.L. Doppman, J.A. Norton, P.N. Maton, F.P. Smith, R. Vinayek, H. Frucht, S.A. Wank, J.D. Gardner et al. Prospective study of chemotherapy in patients with metastatic gastrinoma. Gastroenterology 94, 1326–1334 (1988)CrossRef
71.
J.R. Strosberg, R.L. Fine, J. Choi, A. Nasir, D. Coppola, D.T. Chen, J. Helm, L. Kvols, First-line chemotherapy with capecitabine and temozolomide in patients with metastatic pancreatic endocrine carcinomas. Cancer 117, 268–275 (2011)PubMedCrossRef
72.
A.V. Schally, Oncological applications of somatostatin analogues. Cancer Res. 48, 6977–6785 (1988)PubMed
73.
Pollak M.N., Schally A.V., Mechanisms of antineoplastic action of somatostatin analogs. Proc. Soc. Exp. Biol. Med. 217, 143–152 (1998)PubMedCrossRef
74.
S. Pyronnet, C. Bousquet, S. Najib, R. Azar, H. Laklai, C. Susini, Antitumor effects of somatostatin. Mol. Cell Endocrinol. 286, 230–237 (2008)PubMedCrossRef
75.
R. Arnold, M.E. Trautmann, W. Creutzfeldt, R. Benning, M. Benning, C. Neuhaus, R. Jurgensen, K. Stein, H. Schafer, C. Bruns, H.J. Dennler, Somatostatin analogue octreotide and inhibition of tumour growth in metastatic endocrine gastroenteropancreatic tumours. Gut 38, 430–438 (1996)PubMedPubMedCentralCrossRef
76.
M. Di Bartolomeo, E. Bajetta, R. Buzzoni, L. Mariani, C. Carnaghi, L. Somma, N. Zilembo, A. Di Leo, Clinical efficacy of octreotide in the treatment of metastatic neuroendocrine tumors. A study by the Italian Trials in Medical Oncology Group. Cancer 77, 402–408 (1996)PubMedCrossRef
77.
T. Aparicio, M. Ducreux, E. Baudin, J.C. Sabourin, T. De Baere, E. Mitry, M. Schlumberger, P. Rougier, Antitumour activity of somatostatin analogues in progressive metastatic neuroendocrine tumours. Eur. J. Cancer 37, 1014–1019 (2001)PubMedCrossRef
78.
S. Faiss, U.F. Pape, M. Böhmig, Y. Dörffel, U. Mansmann, W. Golder, E.O. Riecken, B. Wiedenmann, Prospective, randomized, multicenter trial on the antiproliferative effect of lanreotide, interferon alfa, and their combination for therapy of metastatic neuroendocrine gastroenteropancreatic tumors-The International Lanreotide and Interferon Alfa Study Group. J. Clin. Oncol. 21, 2689–2696 (2003)PubMedCrossRef
79.
A. Rinke, H.H. Müller, C. Schade-Brittinger, K.J. Klose, P. Barth, M. Wied, C. Mayer, B. Aminossadati, U.F. Pape, M. Bläker, J. Harder, C. Arnold, T. Gress, R. Arnold, Placebo-controlled, double-blind, prospective, randomized study on the effect of octreotide LAR in the control of tumor growth in patients with metastatic neuroendocrine midgut tumors: a report from the PROMID Study. J. Clin. Oncol. 27, 4656–4663 (2009)PubMedCrossRef
80.
M.E. Caplin, M. Pavel, J.B. Ćwikła, A.T. Phan, M. Raderer, E. Sedláčková, G. Cadiot, E.M. Wolin, J. Capdevila, L. Wall, Lanreotide in metastatic enteropancreatic neuroendocrine tumors. N. Eng. J. Med. 371, 224–233 (2014)CrossRef
81.
D. Hoyer, H. Lubbert, C. Bruns, Molecular pharmacology of somatostatin receptors. Naunyn Schmiedeberg’s Arch. Pharmacol. 350, 441–453 (1994)CrossRef
82.
M. Vanetti, M. Kouba, X. Wang, G. Vogt, V. Hollt, Cloning and expression of a novel mouse somatostatin receptor (SSTR2B). FEBS Lett. 311, 290–294 (1992)PubMedCrossRef
83.
Y.C. Patel, M. Greenwood, G. Kent, R. Panetta, C.B. Srikant, Multiple gene transcripts of the somatostatin receptor SSTR2: tissue selective distribution and cAMP regulation. Biochem. Biophys. Res. Commun. 192, 288–294 (1993)PubMedCrossRef
84.
S.W. Lamberts, E.P. Krenning, J.C. Reubi, The role of somatostatin and its analogs in the diagnosis and treatment of tumors. Endocr. Rev. 12, 450–482 (1991)PubMedCrossRef
85.
L.J. Hofland, H.A. Visser-Wisselaar, S.W. Lamberts, Somatostatin analogs: clinical application in relation to human somatostatin receptor subtypes. Biochem. Pharmacol. 50, 287–297 (1995)PubMedCrossRef
86.
J.C. Reubi, J. Laissue, E. Krenning, S.W. Lamberts, Somatostatin receptors in human cancer: incidence, characteristics, functional correlates and clinical implications. J. Steroid Biochem. Mol. Biol. 43, 27–35 (1992)PubMedCrossRef
87.
J.C. Reubi, B. Waser, J.C. Schaer, J.A. Laissue, Somatostatin receptor sst1–sst5 expression in normal and neoplastic human tissues using receptor autoradiography with subtype-selective ligands. Eur. J. Nucl. Med. 28, 836–846 (2001)PubMedCrossRef
88.
S. Vikic-Topic, K.P. Raisch, L.K. Kvols, S. Vuk-Pavlovic, Expression of somatostatin receptor subtypes in breast carcinoma, carcinoid tumor, and renal cell carcinoma. J. Clin. Endocrinol. Metabol. 80, 2974–2979 (1995)
89.
L.J. Hofland, Q. Liu, P.M. van Koetsveld, J. Zuijderwijk, F. van der Ham, R.R. de Krijger, A. Schonbrunn, S.W. Lamberts, Immunohistochemical detection of somatostatin receptor subtypes sst1 and sst2A in human somatostatin receptor positive tumors. J. Clin. Endocrinol. Metab. 84, 775–780 (1999)PubMedCrossRef
90.
J.C. Reubi, J. Laissue, B. Waser, U. Horisberger, J.C. Schaer, Expression of somatostatin receptors in normal, inflamed, and neoplastic human gastrointestinal tissues. Ann. N. Y. Acad. Sci. 733, 122–137 (1994)PubMedCrossRef
91.
H. Kulaksiz, R. Eissele, D. Rössler, S. Schulz, V. Hollt, Y. Cetin, R. Arnold, Identification of somatostatin receptor subtypes 1, 2A, 3, and 5 in neuroendocrine tumours with subtypespecific antibodies. Gut 50, 52–60 (2002)PubMedPubMedCentralCrossRef
92.
S.W. Lamberts, A.J. van der Lely, W.W. de Herder, L.J. Hofland, Octreotide. N. Eng. J. Med. 334, 246–254 (1996)CrossRef
93.
E.J. Mozell, A.L. Cramer, T.M. O’Dorisio, E.A. Woltering, Long-term efficacy of octreotide in the treatment of Zollinger-Ellison syndrome. Arch. Surg. 127, 1019–1024 (1992)PubMedCrossRef
94.
E.P. Krenning, D.J. Kwekkeboom, W.H. Bakker, W.A. Breeman, P.P. Kooij, H.Y. Oei, M. van Hagen, P.T. Postema, M. de Long, J.C. Reubi et al. Somatostatin receptor scintigraphy with [1 l ‘In-DTPA-D-Phe’]- and [123I-Tyr3]- octreotide: the Rotterdam experience with more than 1000 patients. Eur. J. Nucl. Med. 20, 716–731 (1993)PubMedCrossRef
95.
E. de Kerviler, G. Cadiot, R. Lebtahi, M. Faraggi, D. Le Guludec, M. Mignon, Somatostatin receptor scintigraphy in forty-eight patients with Zollinger-Ellison syndrome. GRESZE: Group d’Etude du Syndrome de Zollinger-Ellison. Eur. J. Nucl. Med. 21, 1191–1197 (1994)PubMedCrossRef
96.
R.T. Jensen, F. Gibril, Somatostatin receptor scintigraphy in gastrinomas. Ital. J. Gastroenterol. Hepatol. 31, S179–85 (1993)
97.
F. Gibril, J.C. Reynolds, J.L. Doppmann, C.C. Chen, D.J. Venzon, B. Termanini, H.C. Weber, C.A. Steward, R.T. Jensen, Somatostatin receptor scintigraphy: its sensitivity compared with that of other imaging methods in detecting primary and metastatic gastrinomas. A prospective study. Ann. Intern. Med. 125, 26–34 (1996)PubMedCrossRef
98.
J.C. Reubi, J.C. Schär, B. Waser, S. Wenger, A. Heppeler, J.S. Schmitt, H.R. Mäcke, Affinity profiles for human somatostatin receptor subtypes SST1–SST5 of somatostatin radiotracers selected for scintigraphic and radiotherapeutic use. Eur. J. Nucl. Med. 27, 273–282 (2000)PubMedCrossRef
99.
A. Mojtahedi, S. Thamake, I. Tworowska, D. Ranganathan, E.S. Delpassand, The value of (68)Ga-DOTATATE PET/CT in diagnosis and management of neuroendocrine tumors compared to current FDA approved imaging modalities: a review of literature. Am. J. Nucl. Med. Mol. Imaging 4, 426–434 (2014)PubMedPubMedCentral
100.
N. Naswa, P. Sharma, R. Soundararajan, S. Karunanithi, A.H. Nazar, R. Kumar, A. Malhotra, C. Bal, Diagnostic performance of somatostatin receptor PET/CT using 68 Ga DOTANOC in gastrinoma patients with negative or equivocal CT findings. Abdom. Imaging 38, 552–560 (2013)PubMedCrossRef
101.
J.C. Reubi, H.R. Mäcke, E.P. Krenning, Candidates for peptide receptor radiotherapy today and in the future. J. Nucl. Med. 46, 67S–75S (2005)PubMed
102.
D.J. Kwekkeboom, J.J. Teunissen, W.H. Bakker, P.P. Kooij, W.W. de Herder, R.A. Feelders, C.H. van Eijck, J.P. Esser, B.L. Kam, E.P. Krenning, Radiolabeled somatostatin analog [177Lu-DOTA0,Tyr3]octreotate in patients with endocrine gastroenteropancreatic tumors. J. Clin. Oncol. 23, 2754–2762 (2005)PubMedCrossRef
103.
S. Grozinski-Glasberg, D. Barak, M. Fraenkel, M.A. Walter, J. Müeller-Brand, J. Eckstein, L. Applebaum, I. Shimon, D.J. Gross, Peptide receptor radioligand therapy is an effective treatment for the long-term stabilization of malignant gastrinomas. Cancer 117, 1377–1385 (2011)CrossRef
104.
G. Delle Fave, D.J. Kwekkeboom, E. Van Cutsem, G. Rindi, B. Kos-Kudla, U. Knigge, H. Sasano, P. Tomassetti, R. Salazar, P. Ruszniewski, ENETS consensus guidelines for the management of patients with gastroduodenal neoplasms. Neuroendocrinology 95, 74–87 (2012)PubMedCrossRef
105.
R.T. Jensen, G. Cadiot, M.L. Brandi, W.W. de Herder, G. Kaltsas, P. Komminoth, J.Y. Scoazec, R. Salazar, A. Sauvanet, R. Kianmanesh, ENETS Consensus Guidelines for the management of patients with digestive neuroendocrine neoplasms: functional pancreatic endocrine tumor syndromes. Neuroendocrinology 95, 98–119 (2012)PubMedPubMedCentralCrossRef
106.
M. Pavel, E. Baudin, A. Couvelard, E. Krenning, K. Öberg, T. Steinmüller, M. Anlauf, B. Wiedenmann, B. Salazar, NETS Consensus Guidelines for the management of patients with liver and other distant metastases from neuroendocrine neoplasms of foregut, midgut, hindgut, and unknown primary. Neuroendocrinology 95, 157–176 (2012)PubMedCrossRef
107.
G. Delle Fave, D. O’Toole, A. Sundin, B. Taal, P. Ferolla, J.K. Ramage, D. Ferone, T. Ito, W. Weber, Z. Zheng-Pei, W.W. De Herder, A. Pascher, P. Ruszniewski, ENETS consensus guidelines update for gastroduodenal neuroendocrine neoplasms. Neuroendocrinology 103, 119–124 (2016)PubMedCrossRef
108.
M. Pavel, D. O’Toole, F. Costa, J. Capdevila, D. Gross, R. Kianmanesh, E. Krenning, U. Knigge, R. Salazar, U.F. Pape, K. Öberg, ENETS consensus guidelines update for the management of distant metastatic disease of intestinal, pancreatic, bronchial neuroendocrine neoplasms (NEN) and NEN of unknown primary site. Neuroendocrinology 103, 172–185 (2016)PubMedCrossRef
109.
M.H. Kulke, L.B. Anthony, D.L. Bushnell, W.W. de Herder, S.J. Goldsmith, D.S. Klimstra, S.J. Marx, J.L. Pasieka, R.F. Pommier, J.C. Yao, R.T. Jensen, NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas 39, 735–752 (2010)PubMedPubMedCentralCrossRef
110.
P.L. Kunz, D. Reidy-Lagunes, L.B. Anthony, E.M. Bertino, K. Brendtro, J.A. Chan, H. Chen, R.T. Jensen, M.K. Kim, D.S. Klimstra, M.H. Kulke, E.H. Liu, D.C. Metz, A.T. Phan, R.S. Sippel, J.R. Strosberg, J.C. Yao, Consensus guidelines for the management and treatment of neuroendocrine tumors. Pancreas 42, 557–577 (2013)PubMedPubMedCentralCrossRef
111.
K. Öberg, U. Knigge, D. Kwekkeboom, A. Perren, Neuroendocrine gastro-entero-pancreatic tumors: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 23, 124–130 (2012)
112.
B. Wormann, K. Kutz, R. Ottenjann, Treatment of relapsing bleeding peptic ulcers with the somatostatin analogue SMS 201 995 in a patient with Zollinger-Ellison syndrome. Hepatogastroenterology 32, 152–153 (1985)PubMed
113.
P. Ruszniewski, H. Laucournet, L. Elouaer-Blanc, M. Mignon, S. Bonfils, Long-acting somatostatin (SMS 201-995) in the management of Zollinger-Ellison syndrome: evidence for susteined efficacy. Pancreas 3, 145–152 (1988)PubMedCrossRef
114.
P. Ruszniewski, F. Girard, R. Benamouzig, M. Mignon, S. Bonfils, Long-acting somatostatin treatment of paraneoplastic Cushing’s syndrome in a case of Zollinger-Ellison syndrome. Gut 29, 838–842 (1988)PubMedPubMedCentralCrossRef
115.
R. Arnold, R. Benning, C. Neuhaus, M. Rolwage, M.E. Trautmann, Gastroenteropancreatic endocrine tumors: effect of sandostatin on tumor growth. Ger. Sandostatin Study Group Metabol. 41, 116–118 (1992)
116.
R. Arnold, C. Neuhaus, R. Benning, W.B. Schwerk, M.E. Trautmann, K. Joseph, C. Bruns, Somatostatin analog sandostatin and inhibition of tumor frowth in patients with metastatic endocrine gastroenteropancreatic tumors. World J. Surg. 17, 511–519 (1993)PubMedCrossRef
117.
S. Angeletti, V.D. Corleto, O. Schillaci, A. Moretti, F. Panzuto, B. Annobale, G. Delle Fave, Single dose of octreotide stabilize metastatic gastro-entero-pancreatic endocrine tumors. Ital. J. Gastroenterol. Hepatol. 31, 23–27 (1999)PubMed
118.
S. Gaztambide, J.A. Vazquez, Short-and long term effect of a long-acting somatostatin analogue, lanreotide (SR-L) on metastatic gastrinoma. J. Endocrinol. Invest. 22, 144–146 (1999)PubMedCrossRef
119.
A.N.M. Wymenga, B. Eriksson, P.I. Salmela, M.B. Jacobsen, E.J.D.G. Van Cutsem, R.H. Fiasse, M.J. Välimäki, J. Renstrup, E.G.E. de Vries, K.E. Öberg, Efficacy and safety of prolonged-release lanreotide in patients with gastrointestinal neuroendocrine tumors and hormone-related symptoms. J. Clin. Oncol. 17, 1111–1117 (1999)PubMedCrossRef
120.
P. Tomassetti, M. Migliori, R. Corinaldesi, L. Gullo, Treatment of gastroenteropancreatic neuroendocrine tumours with octreotide LAR. Aliment. Pharmacol. Ther. 14, 557–560 (2000)PubMedCrossRef
121.
H. Shojamanesh, F. Gibril, A. Louie, J.V. Ojeaburu, S. Bashir, A. Abou-Saif, R.T. Jensen, Prospective study of the antitumor efficacy of long-term octreotide treatment in patients with progressive metastatic gastrinoma. Cancer 94, 331–343 (2002)PubMedCrossRef
122.
F. Saijo, H. Naito, Y. Funayama, K. Fukushima, C. Shibata, A. Hashimoto, T. Kitayama, M. Nagao, S. Matsuno, I. Sasaki, Octreotide in control of liver metastases from gastrinoma. J. Gastroenterol. 38, 905–908 (2003)PubMedCrossRef
123.
D. Granberg, H. Jacobsson, K.E. Öberg, J. Gustavsson, M. Lehtihet, Regression of a large malignant gastrinoma on treatment with Sandostin LAR: a case report. Digestion 77, 92–95 (2008)PubMedCrossRef
124.
M. Yamaguchi, Y. Yamada, Y. Hosokawa, R. Iwamoto, S. Tamba, A. Ihara, K. Yamamoto, Y. Hoshida, Y. Matzuzawa, Long-term suppressive effect of Octreotide on progression of metastatic gastrinoma with multiple endocrine neoplasia type 1: seven-year follow up. Intern. Med. 49, 1557–1563 (2010)PubMedCrossRef
Metadata
Title
The Zollinger-Ellison syndrome: is there a role for somatostatin analogues in the treatment of the gastrinoma?
Authors
Valentina Guarnotta
Chiara Martini
Maria Vittoria Davì
Genoveffa Pizza
Annamaria Colao
Antongiulio Faggiano
on behalf of NIKE group
Publication date
01-04-2018
Publisher
Springer US
Published in
Endocrine / Issue 1/2018
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-017-1420-4

Other articles of this Issue 1/2018

Endocrine 1/2018 Go to the issue

Original Article

MiR-145 improves macrophage-mediated inflammation through targeting Arf6

Original Article

Female gonadal functions and ovarian reserve in patients with acromegaly: experience from a single tertiary center

Original Article

Long-term safety of long-acting octreotide in patients with diabetic retinopathy: results of pooled data from 2 randomized, double-blind, placebo-controlled phase 3 studies

Research Letter

Treatment of refractory and severe hypothyroidism with sublingual levothyroxine in liquid formulation

Original Article

Body composition and sarcopenia in patients with chronic obstructive pulmonary disease

Letter to the Editor

Comment on “The pros and cons of continuous glucose monitoring for patients with type 1 diabetes on multiple daily injections of insulin”. Authors’ reply

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits