CALCITONIN-SECRETING PANCREATIC NEUROENDOCRINE TUMOR IN A PATIENT WITH MULTIPLE ENDOCRINE NEOPLASIA TYPE 1

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1 Case Report CALCITONIN-SECRETING PANCREATIC NEUROENDOCRINE TUMOR IN A PATIENT WITH MULTIPLE ENDOCRINE NEOPLASIA TYPE 1 Umer A. Ansari, BS 1 ; Christine L. Ramirez, MD 1 ; Eric C. Feliberti, MD 1 ; Aaron I. Vinik, MD, PhD 2 ; Roger R. Perry, MD, MS 1 ABSTRACT Objective: To present a patient with multiple endocrine neoplasia type 1 (MEN1) syndrome recently diagnosed with a calcitonin-secreting pancreatic neuroendocrine tumor. Methods: Clinical and diagnostic evaluation, along with intervention, is presented. The relevant literature is reviewed. Results: The patient was a 52-year-old Caucasian man with a history of known MEN1 who had a right parathyroidectomy 10 years prior to admission, completion parathyroidectomy and total thyroidectomy for C cell hyperplasia 3 years prior, and removal of a pituitary adenoma 4 years prior. He was asymptomatic but had persistently elevated serum calcitonin levels. Venous sampling and positron emission tomography computerized tomography indicated several lesions in the pancreas as the most likely cause of ectopic calcitonin secretion. The patient underwent pylorus-sparing pancreaticoduodenectomy (Whipple procedure). Several well-differentiated neuroendocrine lesions of the pancreas were noted, with lymphatic invasion and spread to a peripancreatic lymph node. Postoperatively, the patient s calcitonin levels returned to the normal range. Submitted for publication September 11, 2016 Accepted for publication December 1, 2016 From the 1 Departments of Surgery, and 2 Medicine/Pathology/Neurobiology, Eastern Virginia Medical School, Norfolk, Virginia. Address correspondence to Dr. Roger R. Perry, EVMS Department of Surgery, 825 Fairfax Avenue, Norfolk, VA DOI: /EP CR To purchase reprints of this article, please visit: Conclusion: Calcitonin-secreting pancreatic neuroendocrine tumors are relatively rare entities that are even more rare in familial syndromes such as MEN1. Due to the clinically silent nature of these lesions, they are often discovered incidentally and late in their clinical course. More data are needed in order to establish a consensus on ideal management. Calcitonin elevation even in MEN1 may herald non-thyroid malignancy, therefore demanding an aggressive approach to evaluation and treatment. (AACE Clinical Case Rep. 2017;3:e317-e321) Abbreviations: CT = computerized tomography; MEN1 = multiple endocrine neoplasia type 1; PNETs = pancreatic neuroendocrine tumors; PP = pancreatic polypeptide; VIP = vasoactive intestinal peptide INTRODUCTION Multiple endocrine neoplasia type 1 (MEN1) is an autosomal dominant familial syndrome involving genetic loss of the MEN1 gene on chromosome 11q13 and its downstream protein menin. The loss of menin, which normally serves as a tumor suppressor and as a regulator of cellular growth and function, leads to neoplastic proliferation in multiple organs (1,2). Cases of MEN1 usually present with pituitary, parathyroid, and pancreatic neoplasms, although the loss of the menin gene has been associated with tumors in over 20 different endocrine and nonendocrine organs (3). In MEN1, a variety of pancreatic neuroendocrine tumors (PNETs) may occur (3,4). Individuals with MEN1 are predisposed to multifocal pancreatic neoplasms which, in the majority, are small, nonfunctioning, and asymptomatic. The most common functioning lesions are gastrinomas (55 to 70%) and insulinomas (20%). PNETs such as glucagonomas, vasoactive intestinal peptide AACE CLINICAL CASE REPORTS Vol 3 No. 4 Autumn 2017 e317

2 e318 Calcitonin-secreting PNET in MEN1, AACE Clinical Case Rep. 2017;3(No. 4) (VIP)-secreting tumors (VIPomas), and somatostatinomas are less commonly reported, comprising less than 3% of cases. Rare functioning PNETs producing hormones such as adrenocorticotropic hormone, α-endorphin, neurotensin, pancreatic polypeptide, serotonin, and calcitonin are seldom reported and occur in less than 1% of all cases (1,5,6). Very rare instances of calcitonin-secreting PNETs have been reported, with those being associated with familial syndromes such as MEN1 being rarer still (6,7). This being such a rare entity, there is a paucity of data on which to base management (1,8-11). We present a case of a calcitonin-secreting PNET in a patient with known MEN1, discuss management, and review the scant literature. CASE REPORT A 52-year-old Caucasian male with known MEN1 was referred to surgical oncology for evaluation of pancreatic lesions in the setting of elevated calcitonin levels. He had a right parathyroidectomy 10 years prior to admission, followed by a completion parathyroidectomy. He was noted to be hypertensive, so the patient was later workedup for MEN type 2. Elevated serum calcitonin levels were noted, ranging from 22 to 47 pg/ml. The patient was found to have C cell hyperplasia, and consequently underwent total thyroidectomy 7 years later. Early postoperative calcitonin levels remained elevated at 28 pg/ml. He also underwent removal of a pituitary adenoma 4 years prior to admission. Further evaluation revealed that the patient was positive for a MEN1 gene mutation. Two siblings had clinical features suggestive of MEN1 but were deceased and could not be studied. He was being followed by his endocrinologist for stable adrenal adenomas, several pancreatic lesions, and persistently elevated serum calcitonin levels, ranging from 17 to 74 pg/ml. Of note, the patient was completely asymptomatic, and calcium and phosphorus levels remained normal. A sestamibi scan showed no evidence of parathyroid lesions as a potential source of the elevated calcitonin (Fig. 1), and magnetic resonance imaging (MRI) showed no obvious neck mass. A computerized tomography (CT) scan and MRI indicated several lesions throughout the pancreas; however, this only identified the masses and not the culprit secreting calcitonin. Therefore, the patient underwent venous sampling for calcitonin and parathyroid hormone (PTH) via trans-hepatic approach at the portal vein and its branches, as well as venous sampling of the head and neck. Sampling showed markedly elevated calcitonin levels in the gastrocolic trunk, splenic vein, and superior mesenteric vein around the pancreatic head (Fig. 2). The patient then underwent gallium-68 enhanced positron emission tomography (PET)/CT which showed 6 lesions in the pancreas (3 in the head), suggestive of neuroendocrine tumors, and 2 subcentimeter indeterminate lung nodules (Fig. 3). It was concluded that a pancreatic head lesion was the most likely source of calcitonin secretion in this patient. The patient was discussed at a multidisciplinary conference and, after much discussion, was deemed a good candidate for surgery. The patient was surgically explored. Intra-operative ultrasound revealed at least one of the pancreatic head masses abutting the main pancreatic duct. Therefore, enucleation was not possible given the proximity to the duct and the multiplicity of the lesions in the head. A pylorus-sparing pancreaticoduodenectomy (Whipple procedure) was performed. No hepatic or distant metastases were observed. The pathology report indicated 3 well-differentiated neuroendocrine tumors located in the pancreatic head, neck, and uncinate process. They displayed a low mitotic index (<2/high-power field) and Ki67 <2%. However, there was evidence of lymphovascular invasion, and 1 of 16 peripancreatic nodes sampled was positive for metastasis. None of the tumors stained for calcitonin. His postoperative course was uncomplicated, and calcitonin levels on postoperative day 7 were less than 2.0 pg/ml. He was discharged home on postoperative day Fig. 1. Sestamibi scan was negative for parathyroid lesions.

3 Calcitonin-secreting PNET in MEN1, AACE Clinical Case Rep. 2017;3(No. 4) e319 Marker # Splenic Vein Venous Sampling: Calcitonin (normal pg/ml) Calcitonin (pg/ml) Marker # Calcitonin (pg/ml) Superior Mesenteric Vein A A A A Gastrocolic Trunk Inferior Mesenteric Vein Fig. 2. Results of trans-hepatic portal vein sampling for serum calcitonin levels. Results indicated the highest levels in the splenic vein, superior mesenteric vein, and gastrocolic trunk (underlined values). With several pancreatic lesions noted on imaging, this pattern was highly suggestive of ectopic pancreatic calcitonin secretion. 10. At that time, he was ambulating, voiding, tolerating a regular diet, and having normal bowel function. Follow-up PET/CT of the chest 5 months after discharge showed a 1 cm pulmonary nodule in the left upper lobe with uptake of 68-gallium-dotatate. The nodule was highly suspicious for metastasis. Subsequent imaging has shown stability of this lung lesion for greater than 1 year, and calcitonin levels remain less than 2 pg/ml. DISCUSSION The majority of disease-specific mortality in MEN1 now occurs as a malignant sequelae of PNETs (2,12,13). PNETs in the setting of MEN1 are usually small, multifocal, occur in a background of diffuse pancreatic adenomatosis, tend to be more aggressive, and less likely to be cured via surgical resection than sporadic PNETs. Unlike our patient, the majority of PNETs in MEN1 patients are nonfunctioning and do not release hormones into the Fig. 3. T1-weighted magnetic resonance imaging with contrast demonstrating enhancement of several lesions, including those in the pancreatic head (arrow). circulation. Nonfunctioning PNETs occur in approximately 95% of MEN1 cases, with fewer than 15% of tumors being symptomatic (1). The lack of symptoms often causes a delay in diagnosis. Patients with nonsecreting tumors usually present with a large tumor burden and often at an advanced stage, but may lack the hormone-related morbidity associated with smaller, peptide-secreting tumors. Thus, patients with nonsecreting tumors are often diagnosed with a large pancreatic mass or enlarged liver during a routine physical examination. In contrast, small but hormonally active tumors can have significant debilitating symptoms that prompt diagnostic evaluation earlier in their course (4,7,14). The most common functioning lesions, including gastrinomas, insulinomas, and VIPomas, tend to present with significant symptoms such as recurrent peptic ulcer disease, symptomatic hypoglycemia, and watery diarrhea, respectively (4,7). These symptoms can be an early clue for clinicians to initiate proper diagnostic investigation. Pancreatic polypeptide (PP)-secreting tumors occur with a similar frequency to gastrinomas and insulinomas, and are confined to the head of the pancreas. However, PP has little bioactivity and hence elevated levels result in few if any symptoms (15). Calcitonin-producing PNETs are exceedingly rare and very few cases of their co-occurrence with MEN1 have been reported (1,6,7,13,16,17). Lesions often produce several hormones simultaneously, such as VIP, PP, corticotropin-releasing factor, insulin, gastrin, and somatostatin, which can be responsible for associated symptoms (6,7). However, tumors that produce only calcitonin are more insidious in their presentation, since they may have no symptoms or nonspecific symptoms. Calcitonin is a small (32 amino acid) peptide hormone normally secreted by thyroid C cells (16). C cells are present not only in the thyroid, but in the parathyroid glands,

4 e320 Calcitonin-secreting PNET in MEN1, AACE Clinical Case Rep. 2017;3(No. 4) lungs, thymus, small intestine, liver, and bladder (8). Despite the abnormal secretion of calcitonin, up to one half of patients with tumors that produce the hormone may be asymptomatic (4,6,7,16,18). Classically, high circulating calcitonin levels are associated with medullary thyroid carcinoma, but may also be elevated in patients with chronic kidney disease, especially those with secondary hyperparathyroidism (6-8,16). Our patient had previously been operated on and found to have C cell hyperplasia, which can produce watery diarrhea, abdominal pain, and flushing, and is best treated surgically, as he was. Paradoxically, the persistent elevation in calcitonin levels did not derive from C cells in the thyroid but from an ectopic source in the pancreas. Elevated calcitonin levels have also been rarely noted in other neoplasms such as pheochromocytomas, mucosal neuromas, lung carcinomas, melanomas, breast cancer, and colorectal cancer (6,16,18,19). Venous sampling did, however, direct us to the venous drainage from the head of the pancreas. The patient s calcitonin levels returned to normal after pancreaticoduodenectomy. Of note, the 3 tumors in the pathology specimen did not stain for calcitonin. Failure of positive staining may be due to production of a large form of calcitonin not recognized by the antiserum, or alternatively due to high rates of calcitonin secretion into the portal circulation, resulting in depleted tissue levels. Higher levels of calcitonin are considered to correlate with the presence of symptoms, but not all patients with high levels of the hormone will have symptoms (6-8,16,18). When symptoms do occur, the main manifestations of calcitonin-secreting PNETs are watery diarrhea (51.4%), abdominal pain (35.1%), and weight loss (6,7,16). Diarrhea may be explained by the hormone s effect on the gut in reducing gastrin and gastric acid secretion, and increasing secretion of sodium, potassium, chloride, and water (6,16). Due to the lack of symptoms produced by even large elevations in calcitonin, these tumors are often found incidentally, as part of diagnostic and laboratory workup for other reasons (6,7,18). In the case of our patient, he was free of any symptoms, and his lesions were only discovered as part of routine follow-up screening due to his known MEN1 and C cell hyperplasia. Most patients with calcitonin-producing PNETs (59.5 to 90%) are reported to present with metastatic spread at the time of diagnosis (6,8,11,19). Despite knowledge of our patient s MEN1 status, which prompted early monitoring and intervention, our patient was noted to have spread to a peripancreatic node. He also has 2 small indeterminate pulmonary nodules, one stable and one which has stabilized after initial growth. Patients with higher calcitonin levels at time of presentation (>250 ng/l) tend to have a worse prognosis and are more likely to have metastasis at the time of diagnosis (9). Due to the relatively silent nature of these lesions and advanced stage at diagnosis, better methods are needed to find calcitonin-secreting PNETs earlier. Some authors suggest screening for extrathyroidal calcitonin secretion in the presence of elevated calcitonin, or when there are symptoms suggestive of elevated calcitonin (watery diarrhea without flushing), particularly when thyroid examination and imaging are normal (7,18). Treatment of PNETs in familial syndromes such as MEN1 remains controversial (6,16,17). In calcitoninsecreting lesions, the rate of survival has been shown to be higher in patients who underwent more aggressive surgical therapies, such as distal pancreatectomy or pancreaticoduodenectomy, compared with local resection (6). Given our patient s young age, overall good health, and apparently localized disease at presentation, we felt an aggressive surgical approach was justified, in this case pancreaticoduodenectomy. We generally hold a very conservative posture in recommending surgery for PNETs in MEN1 patients, limiting surgery to those with symptomatic lesions or nonmetastatic lesions 3 cm or more in diameter. Indeed, surgery is to be avoided in most PNETs in MEN1, because the chance for cure is so slim. For a reasonable management scheme, see the North American Neuroendocrine Tumor Society guidelines (20). Recurrence of calcitonin-secreting PNETs is common even after surgical resection and adjuvant multimodal therapy (8,12). Somatostatin analogs have been proposed to slow the progression and symptoms of metastatic disease but have typically proved ineffective due to the advanced stage at which these lesions usually present (16). Although our patient underwent aggressive surgical resection, the presence of a lymph node metastasis at the time of resection and the initial progression of a pulmonary lesion suggest he is at risk of further metastasis, which is often the typical course. Should he develop clear evidence of recurrence, treatment with tyrosine kinase inhibitors may be helpful as we have shown in other cases (21). He will be closely followed as we have a biomarker in the form of calcitonin in addition to the other hormones he has produced, such as prolactin and PTH. He will likely receive additional treatment since the behavior of calcitonin-producing PNETs in MEN1 is far from benign. His prognosis is quite guarded. CONCLUSION Due to the paucity of data on calcitonin-secreting PNETs and, more specifically, those associated with MEN1 syndrome, little is known about the ideal surveillance and management of these lesions. They are often clinically silent and not diagnosed until advanced stages. These lesions are aggressive, as seen in this case report. Clinicians managing patients with familial syndromes such as MEN1 need to be aware of this uncommon entity, so that it may be diagnosed and treated at an earlier stage, hopefully resulting in a better prognosis.

5 Calcitonin-secreting PNET in MEN1, AACE Clinical Case Rep. 2017;3(No. 4) e321 DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Sadowski SM, Triponez F. Management of pancreatic neuroendocrine tumors in patients with MEN 1. Gland Surg. 2015;4: Pieterman CRC, Conemans EB, Dreijerink KMA, et al. Thoracic and duodenopancreatic neuroendocrine tumors in multiple endocrine neoplasia type 1: natural history and function of menin in tumorigenesis. Endocr Relat Cancer. 2014;21:R121-R Jeong YJ, Oh HK, Bong JG. Multiple endocrine neoplasia type 1 associated with breast cancer: a case report and review of the literature. Oncol Lett. 2014;8: Ellison TA, Edil BH. The current management of pancreatic neuroendocrine tumors. Adv Surg. 2012;46: Yates CJ, Newey PJ, Thakker RV. Challenges and controversies in management of pancreatic neuroendocrine tumours in patients with MEN1. Lancet Diabetes Endocrinol. 2015;3: Schneider R, Waldmann J, Swaid Z, et al. Calcitonin-secreting pancreatic endocrine tumors: systematic analysis of a rare tumor entity. Pancreas. 2011;40: Fleury A, Fléjou JF, Sauvanet A, et al. Calcitonin-secreting tumors of the pancreas: about six cases. Pancreas. 1998;16: Nozières C, Chardon L, Goichot B, et al. Neuroendocrine tumors producing calcitonin: characteristics, prognosis and potential interest of calcitonin monitoring during follow-up. Eur J Endocrinol. 2016;174: Wuilmet L, Jovenin N, Larbre H, et al. Digestive calcitoninsecreting tumors of the foregut: comparison with non-calcitoninsecreting tumors. Eur J Gastroenterol Hepatol. 2006;18: Asa SL, Kovacs K, Killinger DW, Marcon N, Platts M. Pancreatic islet cell carcinoma producing gastrin, ACTH, alphaendorphin, somatostatin and calcitonin. Am J Gastroenterol. 1980;74: Sugimoto F, Sekiya T, Saito M, et al. Calcitonin-producing pancreatic somatostatinoma: report of a case. Surg Today. 1998;28: Kon T, Wada R, Suzuki R, Nakayama Y, Ebina Y, Yagihashi S. VIP and calcitonin-producing pancreatic neuroendocrine tumor with watery diarrhea: clinicopathological features and the effect of somatostatin analogue. JOP. 2012;13: Gut P, Komarowska H, Czarnywojtek A, et al. Familial syndromes associated with neuroendocrine tumours. Contemp Oncol (Pozn). 2015;19: Solcia E, Capella C, Fiocca R, Cornaggia M, Bosi F. The gastroenteropancreatic endocrine system and related tumors. Gastroenterol Clin North Am. 1989;18: Vinik AI. Advances in diagnosis and treatment of pancreatic neuroendocrine tumors. Endocr Pract. 2014;20: Toledo SPA, Lourenço DM Jr, Santos MA, Tavares MR, Toledo RA, de Menezes Correia-Deur JE. Hypercalcitoninemia is not pathognomonic of medullary thyroid carcinoma. Clinics (Sao Paulo). 2009;64: O Toole D, Salazar R, Falconi M, et al. Rare functioning pancreatic endocrine tumors. Neuroendocrinology. 2006;84: Giannetta E, Gianfrilli D, Pozza C, et al. Extrathyroidal calcitonin secreting tumors: pancreatic neuroendocrine tumors in patients with multinodular goiter: two case reports. Medicine (Baltimore). 2016;95:e Do Cao C, Mekinian A, Ladsous M, et al. Hypercalcitonemia revealing a somatostatinoma. Ann Endocrinol (Paris). 2010;71: Kulke MH, Anthony LB, Bushnell DL, et al. NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas. 2010;39: Bourcier ME, Vinik AI. Sunitinib for the treatment of metastatic paraganglioma and vasoactive intestinal polypeptide-producing tumor (VIPoma). Pancreas. 2013;42:

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