LIVER TRANSPLANTATION IN A YOUNG PATIENT WITH SEVERE AND REFRACTORY CARCINOID SYNDROME
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1 Case Report LIVER TRANSPLANTATION IN A YOUNG PATIENT WITH SEVERE AND REFRACTORY CARCINOID SYNDROME Omalkhaire M. Alshaikh, MD 1 ; Sylvia L. Asa, MD, PhD 2 ; Ozgur Mete, MD 2 ; Paul D. Greig, MD 3 ; Ian McGilvray, MD 3 ; Shereen Ezzat, MD 4 ABSTRACT Objective: To report the role of liver transplantation in the management of refractory carcinoid syndrome. Methods: We describe the clinical course, biochemical, radiographic, and histopathologic features of a patient with severe refractory carcinoid syndrome due to a metastatic well-differentiated enterochromaffin cell neuroendocrine tumor of the jejunum. We also review and summarize the literature on liver transplantation in this setting. Results: An 18-year-old patient presented with a 3-year history of progressive palpitations, flushing, abdominal pain, and diarrhea. Initial imaging studies demonstrated multiple cystic liver lesions; biochemistry confirmed elevated 24-hour urinary 5-hydroxy-indolacetic acid (5-HIAA) levels. She was managed with somatostatin analogues followed by a partial small-bowel resection. Five sessions of liver embolization and escalating somatostatin analogues failed to control her symptoms or normalize urinary 5-HIAA levels. Cross-sectional imaging detected disease only in the liver. Due to progressively worsening symptoms, liver transplantation was offered as a therapeutic option at age 21 years. One year following the procedure, her condition improved clinically and biochemically with minimal disease outside the liver. Submitted for publication September 5, 2017 Accepted for publication December 7, 2017 From the 1 Department of Internal Medicine, Al Imam Mohammad Ibn Saud Islamic University, Riyadh, Saudi Arabia, and Departments of 2 Pathology, 3 Surgery, and 4 Medicine, Princess Margaret Cancer Centre, Toronto, Ontario Canada. Address correspondence to Dr. S. Ezzat, Princess Margaret Cancer Centre, University Health Network, 610 University Avenue, Room 7-327, Toronto, Ontario, M5G 2M9 Canada. shereen.ezzat@utoronto.ca. DOI: /ACCR To purchase reprints of this article, please visit: Conclusion: Liver transplantation represents a potential therapeutic option in selected patients with refractory carcinoid syndrome. (AACE Clinical Case Rep. 2018;4:e289-e293) Abbreviations: 5-HIAA = 5-hydroxy-indolacetic acid; CT = computed tomography; EC = enterochromaffin cell; MEN1 = multiple endocrine neoplasia type 1; NET = neuroendocrine tumor; OS = overall survival; SI-NET = small intestine neuroendocrine tumor INTRODUCTION Neuroendocrine tumors (NETs) are a complex group of endocrine neoplasms with wide-ranging clinical presentations. They can exhibit unpredictable behavior with uncertain clinical outcomes. The incidence of these tumors is increasing (1). Canadian data from the Ontario Cancer Registry indicate that the incidence of NETs among adult patients is 5.86 per 100,000 population per year, and metastatic disease is detected in 20.8% at the time of presentation (2). The gastrointestinal tract represents one of the more common sites of primary disease; the majority of gastrointestinal (GI)-NETs arise in the small intestine (SI-NET) and have an enterochromaffin cell (EC) origin, producing mainly serotonin (2). The clinical features of serotonin excess classically include diarrhea, flushing, and valvular heart disease. These carcinoid symptoms frequently worsen in the face of progressive liver metastases, as serotonin escapes hepatic metabolism to reach the systemic circulation. Histologic examination of the resected tumor and metastatic liver disease is essential to confirm tumor primary site, differentiation, grade, and stage. Grading and staging of the tumor are pivotal in designing manage- AACE CLINICAL CASE REPORTS Vol 4 No. 4 July/August 2018 e289
2 e290 Refractory Carcinoid Syndrome, AACE Clinical Case Rep. 2018;4(No. 4) ment recommendations (3). Resection of the primary intestinal tumor, which can sometimes be multifocal (3), and targeted therapy to metastatic liver disease represent the cornerstones of management. Adjuvant therapy with somatostatin analogues plays a role in control of hormonal excess while providing an antiproliferative effect in lowgrade disease (4). Primary tumor resection and low burden of liver involvement have been associated with promising response to somatostatin analogue therapy (4). In particular, the PROMID study reported longer disease stability in somatostatin analogue treated patients compared to placebo-treated patients when liver involvement was <10% (4); however, this treatment effect was not seen in those with more extensive disease (4,5). Other systemic therapies include the inhibitor of the mammalian target of rapamycin, everolimus, which has also been associated with favorable outcomes in GI-NETs, as shown in the RADIANT-4 study (1). Peptide radionuclide receptor therapy (PRRT) with 177 Lu-Dotatate has a promising role in the treatment of metastatic NETs. The recent NETTER-1 phase 3 trial showed progression-free survival of 65.2% at month 20 in the 177 Lu-Dotatate group, compared with only 10.8% in the control group (6). High rates of disease recurrence and lack of data that support and compare liver transplantation to other treatment modalities have been the major precluding factors for this type of surgical intervention. Here, we report a unique case of a young patient who presented with severe manifestations of the carcinoid syndrome. Failure to respond to standard-of-care approaches prompted consideration of liver transplantation. CASE REPORT A previously healthy 18-year-old female presented with palpitations, chest tightness, flushing, diarrhea, and weight loss. Over a 3-year period, her symptoms progressed to the point of frequent and recurrent syncope, precipitating multiple hospital admissions. Her heart rate was consistently 110 to 160 beats/minute. She was pale, cachectic, weighing only 41.1 kg, and had episodic diffuse flushing. Abdominal examination revealed diffuse tenderness but without discretely palpable masses, hepatomegaly, or rubs. Cardiac and neurologic examinations were unremarkable. Investigations identified iron deficiency anemia, while ultrasound examination of the abdomen showed multiple cystic liver lesions that were initially considered to be benign. Biochemical studies revealed elevated 24-hour urinary 5-hydroxy-indolacetic acid (5-HIAA) levels at 800 µmol/day (normal, 50 µmol/day), with elevated serum chromogranin-a at 497 ng/ml (normal, 100 ng/ ml). Computed tomography (CT) scanning of the abdomen revealed a possible mass in the small intestine and the previously noted cystic liver lesions. Echocardiography showed no evidence of valvular heart disease. Octreotide scanning demonstrated intense uptake corresponding to the midabdominal small intestine, but there was no uptake in the liver. Genetic testing for multiple endocrine neoplasia type 1 (MEN1) syndrome was negative. She was started on the somatostatin analogue octreotide LAR prior to surgical resection of the jejunum that identified a well-differentiated EC-NET (Fig. 1 A through C), positive for keratins, chromogranin-a (Fig. 1 D), caudal-related homeobox transcription factor 2 (CDX-2), and serotonin (Fig. 1 E), with intermediate-grade proliferative features (Ki-67 labeling index, 7.8%). Moreover, the tumor was negative for tyrosine hydroxylase, excluding paraganglioma. The tumor extended to the subserosa (Fig. 1 C) and exhibited lymphatic, vascular, and perineural invasion. Five of nine regional lymph nodes were involved, with metastatic tumor displaying extranodal extension. A biopsy of the liver at the time of surgery confirmed metastatic NET disease. She had transient improvement in her symptoms postoperatively, such that she did not require adjuvant therapy. However, 1 year later, her symptoms recurred, accompanied by elevated 24-hour urinary 5-HIAA levels with progression of size and number of the bilobar liver metastases. The largest tumor focus was in segment 2, measuring 2.1 cm. Liver biopsy revealed a well-differentiated NET with a Ki-67 labeling index of 2%. Both short- and long-acting somatostatin analogue therapy were required to manage her symptoms of palpitations and diarrhea. Despite this, she required frequent hospitalizations for carcinoid crises. These remained difficult to manage even with the addition of intravenous somatostatin therapy. Over-the-counter cyproheptadine use had minimal effect on her flushing and diarrhea. Surgical resection of her liver disease was not deemed an option, given the extensive bilobar involvement. Instead, she underwent four sessions of transarterial bland embolization over 5 months to address the metastatic liver disease. Despite this and maximal somatostatin analogue therapy (octreotide-lar and lanreotide-sr), 24-hour urinary 5-HIAA levels could only be reduced to 211 µmol/ day (normal, 50 µmol/day), with a serum chromogranin A of 357 ng/ml. Follow-up CT scanning showed mixed responses, with focal reduction and stabilization of most of the liver lesions but negligible effect on the frequency and severity of her carcinoid crises. Liver transplantation was considered. The compelling indications included the patient s age, the low tumor grade, local control of the primary tumor, the progression despite treatment, and her intractable, disabling symptoms. The features of the original tumor that were concerning for recurrence included the vascular, perineural and lymphatic invasion, and loco-regional nodal involvement. The consensus opinion was that transplantation would provide symptom improvement and possibly prolongation of life. The patient accepted the recommendation for liver transplantation, and she was listed with model
3 A Refractory Carcinoid Syndrome, AACE Clinical Case Rep. 2018;4(No. 4) e291 B C D E F G Fig. 1. The small bowel segmental resection showed a well-differentiated enterochromaffin cell (EC) neuroendocrine tumor (A-C) extending into subserosa (C). The tumor cells were diffusely positive for chromogranin-a (D) and serotonin (E). The liver resection specimen showed multifocal metastatic well-differentiated EC neuroendocrine tumor (F) with diffuse serotonin expression (G).
4 e292 Refractory Carcinoid Syndrome, AACE Clinical Case Rep. 2018;4(No. 4) for end-stage liver disease exception points awarded to patients with liver tumors. Only one living donor volunteered, and after careful assessment, she underwent livingdonor liver transplant 27 months from the time of her initial diagnosis. The resected liver contained multifocal metastatic well-differentiated NET that was positive for keratins, chromogranin-a, CDX-2, and serotonin, consistent with a metastatic EC-NET of midgut origin (Fig. 1 F, G). Mitoses were inconspicuous, and the Ki-67 labeling index was less than 1%. Embolization material was also noted within the tumor and in the vascular spaces, with accompanying foreign body giant cell reaction. Additional studies were performed to determine possible underlying mechanisms of tumorigenesis, given the young age of this patient. The tumor cells showed intact staining for menin, p27, succinate dehydrogenase, subunit B, and mismatch repair (MMR) proteins (e.g., MLH-1, MSH-2, MSH-6, and PMS-2), making the possibility of MEN1-, cyclin-dependent kinase inhibitor 1B (MEN4)-, succinate dehydrogenase, and MMR-related pathogenesis unlikely. Within the first 24 hours postoperatively, the patient noted resolution of her symptoms, especially palpitations, flushing, and diarrhea. Six months postoperatively, she had gained 7 kg and was able to return to work. At nearly 1-year post liver transplant, urinary 5-HIAA was normalized at 24 µmol/day, with a reduced serum chromogranin A of 131 ng/ml. Magnetic resonance imaging of the abdomen showed no evidence of disease in the liver and only a small (1 cm) mesenteric lymph node detectable on gallium-68 dotatate scanning. DISCUSSION We report an unusual case of a metastatic SI-NET in a young patient with multiple management challenges and atypical features of interest. Our patient presented at the young age of 18 years with symptoms of serotonin excess that included palpitations, flushing, and diarrhea. Lack of specificity of these symptoms, absence of structural heart disease, and the low incidence of NETs at such a young age delayed diagnosis. Sinus tachycardia was also atypical in not being a common manifestation of carcinoid heart disease (7). This patient presented with multiple liver cysts, which is also an unusual finding in a young patient that should prompt further investigation (8). At a certain point, patient symptoms appeared to worsen even while on somatostatin analogue therapy. This raised concerns regarding possible hypersensitivity reaction to the medication itself. Dadzie et al (9) reported a single case of an acromegalic patient who developed cutaneous hypersensitivity reaction to octreotide which required desensitization. However, our patient did not exhibit any skin or other signs of a hypersensitivity reaction, diminishing the likelihood of this possibility. Functional imaging such as octreotide scanning has been a valuable tool to localize primary and metastatic NETs. Avid disease may indicate favorable response to future therapy such as PRRT. Lymphatic metastasis of SI-NETs may preclude complete surgical cure, and more than half of NET patients have synchronous liver metastasis, while up to 75% of patients develop them at some point during the course of their disease (3,10,11). Low survival rate and poor prognosis correlate with liver metastasis, with 5-year survival rates ranging from 13 to 54%. This compares with the much higher 75 to 99% survival in those without liver involvement (11,12). Liver transplantation for NETs has been reported in only 0.3% of cases in Europe and in only 0.1% in the United States (13,14). The indication criteria for liver transplantation for NET patients were first reported in 2007 by Mazzaferro et al (15) and are now referred to as the Milan criteria. Subsequently, the European Neuroendocrine Tumor Society guidelines in 2012 articulated specific details (16). These include: (1) patient age 50 years or younger; (2) resection of the primary tumor; (3) no lesion other than the liver as detected by positron emission tomography/ct; (4) predicted mortality rate of patients undergoing liver transplantation less than 10%; (5) well-differentiated tumor of grade 1 or 2; and (6) low Ki-67 index. Mazzaferro et al (15) had additional criteria of (1) venous blood of the primary lesion flowing into the portal vein; (2) not exceeding 50% of the liver; (3) at least 6 months of disease stability. In 2014, Alagusundaramoorthy et al (17) performed a literature review comparing the outcome of liver transplantation among six studies between 1982 and They noted an overall 5-year survival rate of 44 to 59%. Fiveyear progression disease-free survival was 30 to 39% (17). The largest among these studies was the systematic review of the European Liver Transplant Registry, which included 213 patients. In that study, the median overall survival (OS) following liver transplantation was 67 months; at 5 years after transplant, OS was 52%, and disease-free survival was 30% (14). To our knowledge, there are few reports that exclusively studied SI-NETs with liver metastasis. Norlen et al (18) described their experience and the survival rate among 78 patients who had multimodal liver-directed therapies. They also performed a literature review of survival rate among 26 patients who had liver transplant as their main therapy for metastatic SI-NET. In their study, patients had a median follow-up of 7.4 years. Patients were divided into three groups, each of which was further divided into (A) all patients regardless of type of therapy they received, and
5 Refractory Carcinoid Syndrome, AACE Clinical Case Rep. 2018;4(No. 4) e293 (B) those who had not received any type of liver-directed therapy. Among patients <65 years of age, the 5-year OS rates were 84% in group 1A and 70% in group 1B. Among patients <55 years of age, the 5-year OS rates were 92% in group 2A and 75% in group 2B. Patients who fulfilled the Milan criteria had 5-year OS of 97% in group 3A and 89% in 3B. By comparison, their review of the literature, which included a mixed population, indicated that the 5-year OS among 26 patients who had liver transplant was 76% (18). Taken together, these findings are in line with survival outcomes reported in SI-NET patients undergoing multimodal liver-directed therapies (18). CONCLUSION In summary, our case is unique because of the patient s young age of presentation and the nature of her predominantly cardiac symptoms. The patient s rapid symptomatic improvement following liver transplantation points to this as a potential therapeutic option worthy of consideration in selected cases. The durability of such an approach and its long-term impact on quality of life, a critical outcome in this disease (19), remains to be cautiously determined. ACKNOWLEDGMENT We thank the patient for consent and allowing reporting of the case. DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Yao JC, Fazio N, Singh S, et al. Everolimus for the treatment of advanced, non-functional neuroendocrine tumours of the lung or gastrointestinal tract (RADIANT-4): a randomised, placebocontrolled, phase 3 study. Lancet. 2016;387: Singh S, Asa SL, Dey C, et al. Diagnosis and management of gastrointestinal neuroendocrine tumors: an evidence-based Canadian consensus. Cancer Treat Rev. 2016;47: Araujo PB, Cheng S, Mete O, et al. Evaluation of the WHO 2010 grading and AJCC/UICC staging systems in prognostic behavior of intestinal neuroendocrine tumors. PLoS One. 2013;8:e Rinke A, Müller HH, Schade-Brittinger C, et al. Placebocontrolled, 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 Group. J Clin Oncol. 2009;27: Rinke A, Wittenberg M, Schade-Brittinger C, et al. Placebocontrolled, double-blind, prospective, randomized study on the effect of octreotide LAR in the control of tumor growth in patients with metastatic neuroendocrine midgut tumors (PROMID): results of long-term survival. Neuroendocrinology. 2017;104: Strosberg J, El-Haddad G, Wolin E, et al. Phase 3 trial of 177Lu-Dotatate for midgut neuroendocrine tumors. N Engl J Med. 2017;376: Luis SA, Pellikka PA. Carcinoid heart disease: diagnosis and management. Best Pract Res Clin Endocrinol Metab. 2016;30: Fiori S, Del Gobbo A, Gaudioso G, et al. Hepatic pseudocystic metastasis of well-differentiated ileal neuroendocrine tumor: a case report with review of the literature. Diagn Pathol. 2013;8: Dadzie DD, Lee EJ, Monteleone CA, Schneider SH. Desensitization treatment for hypersensitivity reaction to octreotide in an acromegalic patient. Pituitary. 2012;15(suppl 1): S68-S Mignon M. Natural history of neuroendocrine enteropancreatic tumors. Digestion. 2000;62(suppl 1): Jagannath P, Chhabra D, Shrikhande S, Shah R. Surgical treatment of liver metastases in neuroendocrine neoplasms. Int J Hepatol. 2012;2012: Touzios JG, Kiely JM, Pitt SC, et al. Neuroendocrine hepatic metastases: does aggressive management improve survival? Ann Surg. 2005;241: ; discussion Gedaly R, Daily MF, Davenport D, et al. Liver transplantation for the treatment of liver metastases from neuroendocrine tumors: an analysis of the UNOS database. Arch Surg. 2011;146: Le Treut YP, Grégoire E, Klempnauer J, et al. Liver transplantation for neuroendocrine tumors in Europe-results and trends in patient selection: a 213-case European liver transplant registry study. Ann Surg. 2013;257: Mazzaferro V, Pulvirenti A, Coppa J. Neuroendocrine tumors metastatic to the liver: how to select patients for liver transplantation? J Hepatol. 2007;47: Pavel M, Baudin E, Couvelard A, et al. ENETS consensus guidelines for the management of patients with liver and other distant metastases from neuroendocrine neoplasms of foregut, midgut, hindgut, and unknown primary. Neuroendocrinology. 2012;95: Alagusundaramoorthy SS, Gedaly R. Role of surgery and transplantation in the treatment of hepatic metastases from neuroendocrine tumor. World J Gastroenterol. 2014;20: Norlén O, Daskalakis K, Öberg K, Åkerström G, Stålberg P, Hellman P. Indication for liver transplantation in young patients with small intestinal NETs is rare? World J Surg. 2014;38: Khan S, Krenning EP, van Essen M, Kam BL, Teunissen JJ, Kwekkeboom DJ. Quality of life in 265 patients with gastroenteropancreatic or bronchial neuroendocrine tumors treated with [177Lu-DOTA0,Tyr3]. J Nucl Med. 2011;52:
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