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Biochemical curative surgery for gastrinoma in multiple endocrine neoplasia type-1 patients

Authors:
Masayuki Imamura
Masayuki Imamura
Masayuki Imamura
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Izumi Komoto at Kansai Electric Power Hospital
Izumi Komoto
  • Kansai Electric Power Hospital
Shuichi Ota
Shuichi Ota
Shuichi Ota
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Takuya Hiratsuka
Takuya Hiratsuka
Takuya Hiratsuka
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Abstract and Figures

To search for the optimal surgery for gastrinoma and duodenopancreatic neuroendocrine tumors in patients with multiple endocrine neoplasia type 1. Sixteen patients with genetically confirmed multiple endocrine neoplasia type 1 (MEN 1) and Zollinger-Ellison syndrome (ZES) underwent resection of both gastrinomas and duodenopancreatic neuroendocrine tumors (NETs) between 1991 and 2009. For localization of gastrinoma, selective arterial secretagogue injection test (SASI test) with secretin or calcium solution was performed as well as somatostatin receptor scintigraphy (SRS) and other imaging methods such as computed tomography (CT) or magnetic resonance imaging (MRI). The modus of surgery for gastrinoma has been changed over time, searching for the optimal surgery: pancreaticoduodenectomy (PD) was first performed guided by localization with the SAST test, then local resection of duodenal gastrinomas with dissection of regional lymph nodes (LR), and recently pancreas-preserving total duodenectomy (PPTD) has been performed for multiple duodenal gastrinomas. Among various types of preoperative localizing methods for gastrinoma, the SASI test was the most useful method. Imaging methods such as SRS or CT made it essentially impossible to differentiate functioning gastrinoma among various kinds of NETs. However, recent imaging methods including SRS or CT were useful for detecting both distant metastases and ectopic NETs; therefore they are indispensable for staging of NETs. Biochemical cure of gastrinoma was achieved in 14 of 16 patients (87.5%); that is, 100% in 3 patients who underwent PD, 100% in 6 patients who underwent LR (although in 2 patients (33.3%) second LR was performed for recurrence of duodenal gastrinoma), and 71.4% in 7 patients who underwent PPTD. Pancreatic NETs more than 1 cm in diameter were resected either by distal pancreatectomy or enucleations, and no hepatic metastases have developed postoperatively. Pathological study of the resected specimens revealed co-existence of pancreatic gastrinoma with duodenal gastrinoma in 2 of 16 patients (13%), and G cell hyperplasia and/or microgastrinoma in the duodenal Brunner's gland was revealed in all of 7 duodenal specimens after PPTD. Aggressive resection surgery based on accurate localization with the SASI test was useful for biochemical cure of gastrinoma in patients with MEN 1.
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... SASI testing is performed to localize pancreatic neuroendocrine tumors, including insulinoma [9] and gastrinoma [22]. This method is useful in guiding surgical decisions, especially for small tumors that remain elusive on imaging examinations, such as CT, MRI, scintigraphy, and endoscopic ultrasound. ...
Successful Superficial Blood Sampling to Localize a Fibroblast Growth Factor-23-Producing Tumor
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  • Feb 2024
Patient: Male, 64-year-old Final Diagnosis: Tumor-induced osteomalacia Symptoms: Arthralgia • bone fractures • bone pain • gait disturbance Clinical Procedure: — Specialty: Endocrinology and Metabolic • Oncology • Orthopedics and Traumatology Objective Rare disease Background Tumor-induced osteomalacia (TIO) is a paraneoplastic syndrome caused by aberrant fibroblast growth factor-23 (FGF-23)-producing tumors. Early surgical resection is the optimal strategy for preventing TIO progression. Thus, tumor localization is a priority for successful treatment. A simple and safe examination method to identify functional endocrine tumors is essential to achieve better outcomes in patients with TIO. Case Report A 64-year-old Japanese man with recurrent fractures, hypophosphatemia, and elevated alkaline phosphatase and FGF-23 levels (109 pg/mL) was admitted to our university hospital and was diagnosed with FGF23-related hypophosphatemic osteomalacia. Notably, the superficial dorsal vein in the patient’s left foot exhibited a high FGF-23 level (7510 pg/mL). Octreotide and ¹⁸F-fluorodeoxyglucose (FDG) scintigraphy and systemic venous sampling revealed that the tumor in the third basal phalanx of the left foot was responsible for FGF-23 overproduction. Tumor resection resulted in a rapid decrease in serum FGF-23 levels and an increase in serum phosphorus levels. Conclusions Octreotide scintigraphy, FDG-positron emission tomography, and systemic venous sampling are the standard methods for localizing functional endocrine tumors. However, the limited availability and invasive nature of these examinations hinder effective treatment. Here, we highlight the importance of peripheral superficial blood sampling as an alternative to conventional systemic methods for confirming the presence of FGF-23-producing tumors. Clinicians should consider TIO as a potential cause of acquired hypophosphatemic osteomalacia. Furthermore, peripheral superficial vein blood sampling may be useful for confirming the localization of FGF-23-producing tumors.
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A RARE CASE OF GASTRIC GASTRINOMA IN MEN-1 SYNDROME
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  • Jan 2024
We report here the rare case of life threatening multiple gastric gastrinomas in MEN-1 syndrome. The patient not responded to medical management, with on & off symptoms for past 4years, with multiple, >2cm size gastric gastrinomas associated with intussusception. Metastasis of this multiple gastric gastrinomas risk was high, and management was complex. A total gastrectomy was performed in order to prevent metastasis in this frial patient who was not eligible for further medical management
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Individualized approach for MEN1-associated duodenopancreatic neuroendocrine neoplasms
Article
  • Jan 2024
Multiple endocrine neoplasia type 1 (MEN1)-associated duodenopancreatic neuroendocrine neoplasms (dpNEN) represent the most frequent syndrome-associated cause of death, but the adequate treatment is sometimes considered controversial. Presentation of possible diagnostic and therapeutic options for MEN1-associated dpNENs. In this review article retrospective case studies, expert recommendations, national and international guidelines as well as personal experiences were analyzed and evaluated. Due to early detection programs and the use of the most modern imaging techniques, dpNEN are nowadays diagnosed much earlier. Nonfunctional pNENs currently represent the most frequent dpNENs with about 70%, followed by gastrinomas and insulinomas. Regardless of their functional activity, dpNENs with a size of > 2 cm are generally an indication for surgery. The choice of the optimal treatment strategy, however, in most cases remains the subject of controversial discussions, although nowadays surgery should always be performed in an organ-preserving and minimally invasive way when feasible. Recurrences or new dpNENs are expected in more than 60% of cases, necessitating a reoperation in up to 40% of these cases. Duodenopancreatic resections and reoperations can be carried out safely by experienced practitioners and with an acceptable level of risk. The planning of treatment requires careful consideration of the suitable timing, the extent of the operation, the risk of recurrence and potential morbidities. Furthermore, preserving pancreatic function and the quality of life is of utmost importance. In view of the complexity of the disease, MEN1 patients should be treated in specialized centers.
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Surgical management of pancreatic neuroendocrine neoplasms膵神経内分泌腫瘍の術式選択
Article
  • Dec 2023
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Imaging modalities for pancreatic NEN膵NENの画像診断: -Focusing on EUS-―EUSを中心に―
Article
  • Dec 2023
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A case of MEN1 presenting with multiple pancreatic neuroendocrine tumors with large cyst-like morphology difficult to differentiate from mucinous cystic neoplasm (MCN)MEN1に合併し，粘液性嚢胞腫瘍（MCN）との鑑別困難な大型の嚢胞様形態を伴った多発性膵神経内分泌腫瘍の1例
Article
  • Oct 2023
After undergoing prolactin-producing pituitary adenoma removal surgery at age 9, a 34-year-old female was diagnosed with adult growth hormone deficiency and began hormone replacement therapy. Four months later, abdominal CT showed an incidental cystic lesion 50mm in diameter in the pancreatic tail. In addition to hypergastrinemia and hyperglucagonemia, the patient had mildly elevated intact PTH. Somatostatin receptor scintigraphy revealed high levels of accumulation in the lesion. Although pancreatic neuroendocrine tumor (pNET) was suspected, a definitive diagnosis by EUS-FNA was difficult because the lesion was predominantly cystic. Based on ultrasound endoscopy, the preoperative diagnosis was mucinous cystic tumor followed by laparoscopic resection of the pancreatic body tail tumor. Because gastrin-producing tumors were observed in areas other than the thickened wall and limbs of the cyst, the patient was diagnosed with MEN1 presenting with pNET. Differential diagnosis of pancreatic tumors with cysts is difficult and requires multiple viewpoints. A large number of cases of pNET should be accumulated to build up evidence for postoperative adjuvant treatment.
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Multiple endocrine neoplasia type 1 with Zollinger–Ellison syndrome: clinicopathological analysis of a Japanese family with focus on menin immunohistochemistry
Article
Full-text available
  • Oct 2023
Background Multiple endocrine neoplasia type 1 (MEN1) is an autosomal dominant disorder characterized by the occurrence of multiple epithelial neuroendocrine tumors (NETs) and non-NETs in various organs. MEN1 encodes a 610-amino acid-long tumor suppressor protein, menin. The optimal treatment for multiple tumors, identification of the most critical tumors for patient prognosis, and menin immunohistochemistry findings remain controversial. Therefore, we aimed to elucidate these issues through a histological analysis of tumors and tumor-like lesions in a Japanese family, comprising a father and his two sons, who had MEN1 with Zollinger–Ellison syndrome (ZES). Patients and methods All family members had a germline alteration in exon 10, c.1714-1715 del TC of MEN1 , and exhibited multiple synchronous and metachronous tumors. The patients had pulmonary NETs, hyperparathyroidism, hypergastrinemia, pituitary adenomas, pancreaticoduodenal NETs, adrenocortical adenoma with myelolipoma, nodular goiter of the thyroid, lipomas, and angiofibroma. Most tumors were resected and histologically examined. We compared their clinical courses and tumor histology, and conducted menin immunohistochemistry (IHC). Results Two patients died of pulmonary NET G2. One patient who underwent pancreaticoduodenectomy was cured of ZES; however, the two other patients who did not undergo pancreaticoduodenectomy suffered persistent ZES despite treatment with octreotide. Menin IHC revealed varying NET intensities, ranging from positive to negative stains. Conclusion Pancreaticoduodenectomy is the most effective treatment for ZES. Long-term follow-up is essential for pulmonary NET G2 owing to the risk of distant metastasis and/or multiplicity. Moreover, the variability of menin IHC in MEN1-related tumors may indicate the pattern of tumor formation rather than the diagnostic utility of menin in MEN1.
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Indikation und operative Verfahren bei MEN1-assoziierten duodenopankreatischen neuroendokrinen Neoplasien
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  • Aug 2023
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Gastrinomas in the Duodenums of Patients with Multiple Endocrine Neoplasia Type 1 and the Zollinger-Ellison Syndrome
Article
Full-text available
  • Apr 1990
In patients with multiple endocrine neoplasia type 1 (MEN-1), gastrinomas are common and thought to occur predominantly in the pancreas. We describe eight patients with MEN-1 and hypergastrinemia (seven with the Zollinger-Ellison syndrome) in whom we searched for neuroendocrine tumors in the pancreas and duodenum. Tumors were found in the proximal duodenum in all eight patients: solitary tumors (diameter, 6 to 20 mm) in three patients and multiple microtumors (diameter, 2 to 6 mm) in the other five. Paraduodenal lymph-node metastases were detected in four patients. Immunocytochemical analysis revealed the presence of gastrin in all the duodenal tumors and in their lymph-node metastases. In contrast, no immunoreactivity for gastrin was present in the endocrine tumors found in the seven pancreatic specimens available for study, except for one tumor with scattered gastrin-positive cells. In four of the six patients whose duodenal gastrinomas were removed, serum gastrin levels returned to normal; in the other two patients gastrin concentrations decreased toward normal. We conclude that in patients with MEN-1 and the Zollinger-Ellison syndrome, gastrinomas occur in the duodenum, but the tumors may be so small that they escape detection.
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Surgery versus surveillance of pancreaticoduodenal endocrine tumours in multiple endocrine neoplasia type 1
Article
  • Sep 2000
  • BRIT J SURG
Background Management of pancreaticoduodenal endocrine tumours remains controversial in multiple endocrine neoplasia type 1 (MEN1). The authors' experience with MEN1-related pancreaticoduodenal tumours has been reviewed in order to evaluate a rational therapeutic approach.Methods Twenty-one patients with MEN1 with pancreaticoduodenal endocrine tumours were analysed with special regard to outcome of surgery and surveillance. In addition, a phenotype/genotype analysis was performed based on MEN1 gene mutation analysis.ResultsTwelve of 21 patients had multiple tumours. Nine patients had gastrinomas, six non-functioning tumours, three insulinomas, two insulinomas and gastrinomas, and one had a vipoma. Six tumours were malignant with lymph node metastases (five gastrinomas, one vipoma). Seventeen patients were treated initially by either pancreatic left resection with tumour enucleation of the duodenum and/or pancreatic head (n = 9), tumour enucleation alone (n = 7) or pylorus-preserving partial pancreatectomy (PPPD; n = 1). Sixteen of 17 patients were cured biochemically after initial surgery and 11 remained free of disease after a median follow-up of 55 (range 2–197) months. Six patients underwent reoperation for recurrence and/or lymph node metastases, including two PPPDs in patients with gastrinoma. All six patients remained asymptomatic and three remained biochemically free of disease. Three of the 17 operated patients died from either unrelated causes (n = 2) or postoperative complications (n = 1). On the other hand, four asymptomatic patients with either gastrinomas (n = 2) or non-functioning tumours (n = 2) were closely surveyed and showed no progress or metastases on somatostatin (SMS) scans and computed tomography after 9–110 months. The genotype/phenotype analysis revealed that patients with truncating nonsense or frameshift MEN1 gene mutations in the N- or C-terminal regions (exons 2, 9 or 10) had a significantly higher rate of malignant tumours (55 versus 8 per cent; P = 0·04) and tended to have shorter disease-free intervals (28 versus 120 months; P = 0·11) than patients with other mutations.Conclusion An aggressive surgical approach is justified for pancreaticoduodenal tumours in patients with MEN1 since symptom-free long-term survival can be achieved. However, MEN1 gene mutations in exons 3–8 seem to be associated with mild behaviour of pancreaticoduodenal tumours which might allow close surveillance in asymptomatic patients with MEN1. © 2000 British Journal of Surgery Society Ltd
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Early surgical intervention and strategy in patients with multiple endocrine neoplasia type I
Article
  • Jun 2001
Patients with multiple endocrine neoplasia type 1 (MEN-1) are an unusual challenge to the endocrine surgeon. Pituitary disease is often treated without surgery, but nearly all patients will require parathyroidectomy for parathyroid hyperplasia. Subtotal parathyroidectomy can be accomplished with a very low rate of permanent hypoparathyroidism and an acceptable rate of recurrent hyperparathyroidism. The treatment of pancreaticoduodenal disease is quite controversial. Even when associated with the Zollinger–Ellison syndrome, early and aggressive surgical treatment should be considered to influence the hormonal syndrome as well as to address the malignant potential of both pancreatic and duodenal tumours. This includes distal pancreatectomy, enucleation of pancreatic head lesions, and duodenotomy with the resection of gastrinomas. Many patients may be completely cured of the manifestations of their disease. As MEN-1 is an uncommon entity, there are very few prospective, randomized data upon which to base surgical judgements.
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Gastrinoma
Chapter
  • Apr 2009
In 1955, Zollinger and Ellison described two patients in whom jejunal peptic ulcers recurred, successively resistant to conventional ulcer operations including vagotomy and a few distal gastrectomies until a total gastrectomy was performed [1]. The first patient died of the disease. There was no doubt that these persistent peptic ulcers were caused by the extreme acid hypersecretion from a small remnant of stomach left after subtotal gastrectomy.
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Clinicopathological characteristics of duodenal microgastrinomas
Article
  • Jan 1992
Duodenal gastrinomas do not seem to behave as malignantly as sporadic pancreatic gastrinomas. Statistical analysis of 49 patients with sporadic pancreatic gastrinoma and 21 patients with sporadic duodenal gastrinoma reported since 1980 in Japan revealed that the incidence of hepatic metastasis was 57% in patients with sporadic pancreatic gastrinoma and only 9% in patients with sporadic duodenal gastrinoma (pLos gastrinomas duodenales (Goma-D) no parecen tener un comportamiento tan maligno como el de los gastrinomas pancreticos espordicos (Goma-P). El anlisis estadstico de 49 casos de Goma-P espordico y de 21 casos de Goma-D espordico reportados desde 1980 en el Japn, revel que la incidencia de metstasis hepticas fue de 57% en los Goma-P espordicos y apenas de 9% en los Goma-D espordicos (pLes gastrinomes duodnaux (D-Goma) ne semblent pas avoir le mme potentiel malin que les gastrinomes pancratiques sporadiques (P-Goma). L'analyse statistique de 49 cas de P-Goma sporadiques et de 21 cas de D-Goma sporadiques, rapports depuis 1980 au Japon, a montr que l'incidence des mtastases hpatiques tait de 57% dans les P-Goma sporadiques et seulement de 9% dans les D-Goma (p
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Risk Factors and Causes of Death in MEN1 Disease. A GTE (Groupe d’Etude des Tumeurs Endocrines) Cohort Study Among 758 Patients
Article
  • Dec 2009
  • WORLD J SURG
The natural history of multiple endocrine neoplasia type 1 (MEN1) is known through single-institution or single-family studies. We aimed to analyze the risk factors and causes of death in a large cohort of MEN1 patients. Overall, 758 symptomatic MEN1 patients were identified through the GTE network (Groupe d'étude des Tumeurs Endocrines), which involves French and Belgian genetics laboratories responsible for MEN1 diagnosis and 80 clinical reference centers. The causes of death were analyzed. A frailty model, including time-dependent variables, was used to assess the impact of each clinical lesion, except for hyperparathyroidism, on survival. The median follow-up was 6.3 years. Female gender, family history of MEN1, and recent diagnosis were associated with a lower risk of death. Compared with nonaffected patients, those with thymic tumors (hazard ratio [HR] = 4.64, 95% CI = 1.73-12.41), glucagonomas-vipomas-somatostatinomas (HR = 4.29, 95% CI = 1.54-11.93), nonfunctioning pancreatic tumors (HR = 3.43, 95% CI = 1.71-6.88), and gastrinoma (HR = 1.89, 95% CI = 1.09-3.25) had a higher risk of death after adjustment for age, gender, and diagnosis period. The increased risk of death among patients with adrenal tumors was not significant, but three patients died from aggressive adrenal tumors. Pituitary tumors, insulinomas, and bronchial tumors did not increase the risk of death. The proportion of MEN1-related deaths decreased from 76.8 to 71.4% after 1990. The prognosis of MEN1 disease has improved since 1980. Thymic tumors and duodenopancreatic tumors, including nonsecreting pancreatic tumors, increased the risk of death. Rare but aggressive adrenal tumors may also cause death. Most deaths were related to MEN1. New recommendations on abdominal and thoracic imaging are required.
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The influence of surgery in MEN-1 syndrome: Observations over 150 years
Article
  • Oct 2008
Efficacy and timing of operative intervention in patients with multiple endocrine neoplasia type 1 (MEN-1) syndrome remains controversial. This report utilizes a novel approach to evaluate the influence of evolving operative interventions for patients with MEN-1 syndrome. Six generations from a large MEN-1 family pedigree were studied. The number of operations for MEN-1 related pathology was recorded according to birth eras over 150 years. Length of life was a primary outcome measurement. Inheritance of the MEN-1 trait was near 50%. There were no instances of a skipped generation. Affected individuals born before 1900 died from gastrointestinal hemorrhage and without any surgical intervention. After 1900, there were increasing numbers of gastric, parathyroid, and pancreatic operations in successive eras. Death occurred >20 years earlier in MEN-1 individuals than unaffected family members in eras 1 and 2. Family members with MEN-1 lived longer in succeeding eras with increasing number of operative and pharmacologic interventions. MEN-1 family members invariably have pathologic changes in pituitary, parathyroid, and pancreatic islets when long lived, the "all-or-none" phenomenon. Patients are not cured with operative interventions, although they may live longer and without symptoms with a good quality of life. This model may allow better comparisons with other MEN-1 patients when evaluating outcomes of new medical and operative management schemes and long-term follow-up.
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Secretin and calcium provocative tests in the Zollinger-Ellison syndrome: A prospective study
Article
  • Dec 1989
To evaluate criteria of positivity for and usefulness of both the secretin and calcium gastrin-provocative tests in patients with the Zollinger-Ellison syndrome. Prospective trial in consecutive patients. Referrals to a clinical research center. Consecutive sample of 80 patients with the Zollinger-Ellison syndrome. Kabi-secretin (2 U/kg body weight) given by intravenous bolus and calcium gluconate (10%) (54 mg/kg.h [5 mg/kg.h of calcium]) given by continuous intravenous infusion for 3 hours. Serum gastrin measured at -15, and -1 minutes before, and 2, 5, 10, 15, 20, and 30 minutes after secretin, or every 30 minutes for 3 hours during the calcium infusion. Serum calcium and serum gastrin were measured simultaneously during the calcium infusion. There was no significant difference in the responses of patients with different extents or locations of the tumor, presence or absence of multiple endocrine neoplasia, type-I, or with fasting gastrin less than or greater than 1000 pg/mL. In patients with fasting gastrin of less than 1000 pg/mL, the sensitivity of the secretin test using the criterion of an increase in gastrin of at least 110 pg/mL was 93% (CI, 76% to 99%) and for an increase of 200 pg/mL it was 85% (CI, 66% to 96%), (P greater than 0.05). With the calcium infusion test, the sensitivity using the criterion of an increase of 395 pg/mL was 43%, (CI, 23% to 66%) and for an increase of 50% was 74% (CI, 52% to 90%), (P less than 0.01). The calcium infusion test was positive in 33% of patients with a negative secretin test. With the secretin test, 75% of patients had a positive response by 5 minutes, 95% by 10 minutes, 100% by 15 minutes, and 6% only at 2 minutes. With calcium infusion, patients had positive responses at 120 to 180 minutes. The secretin test is preferred over the calcium test because of its greater sensitivity and simplicity. The recommended criteria are a 200 pg/mL increase for the secretin test and a 395 pg/mL increase for the calcium test. The calcium test should be reserved for patients having a negative secretin test, gastric acid hypersecretion, and a strong clinical suspicion of the Zollinger-Ellison syndrome.
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