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Gopakumar H, Jahagirdar V, Koyi J, Dahiya DS, Goyal H, Sharma NR, Perisetti A. Role of Advanced Gastrointestinal Endoscopy in the Comprehensive Management of Neuroendocrine Neoplasms. Cancers (Basel) 2023; 15:4175. [PMID: 37627203 PMCID: PMC10453187 DOI: 10.3390/cancers15164175] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/17/2023] [Revised: 08/15/2023] [Accepted: 08/15/2023] [Indexed: 08/27/2023] Open
Abstract
Neuroendocrine neoplasms (NENs), also called neuroendocrine tumors (NETs), are relatively uncommon, heterogenous tumors primarily originating in the gastrointestinal tract. With the improvement in technology and increasing use of cross-sectional imaging and endoscopy, they are being discovered with increasing frequency. Although traditionally considered indolent tumors with good prognoses, some NENs exhibit aggressive behavior. Timely diagnosis, risk stratification, and management can often be a challenge. In general, small NENs without local invasion or lymphovascular involvement can often be managed using minimally invasive advanced endoscopic techniques, while larger lesions and those with evidence of lymphovascular invasion require surgery, systemic therapy, or a combination thereof. Ideal management requires a comprehensive and accurate understanding of the stage and grade of the tumor. With the recent advancements, a therapeutic advanced endoscopist can play a pivotal role in diagnosing, staging, and managing this rare condition. High-definition white light imaging and digital image enhancing technologies like narrow band imaging (NBI) in the newer endoscopes have improved the diagnostic accuracy of traditional endoscopy. The refinement of endoscopic ultrasound (EUS) over the past decade has revolutionized the role of endoscopy in diagnosing and managing various pathologies, including NENs. In addition to EUS-directed diagnostic biopsies, it also offers the ability to precisely assess the depth of invasion and lymphovascular involvement and thus stage NENs accurately. EUS-directed locoregional ablative therapies are increasingly recognized as highly effective, minimally invasive treatment modalities for NENs, particularly pancreatic NENs. Advanced endoscopic resection techniques like endoscopic submucosal dissection (ESD), endoscopic submucosal resection (EMR), and endoscopic full-thickness resection (EFTR) have been increasingly used over the past decade with excellent results in achieving curative resection of various early-stage gastrointestinal luminal lesions including NENs. In this article, we aim to delineate NENs of the different segments of the gastrointestinal (GI) tract (esophagus, gastric, pancreatic, and small and large intestine) and their management with emphasis on the endoscopic management of these tumors.
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Affiliation(s)
- Harishankar Gopakumar
- Department of Gastroenterology and Hepatology, University of Illinois College of Medicine at Peoria, Peoria, IL 61605, USA;
| | - Vinay Jahagirdar
- Department of Internal Medicine, University of Missouri-Kansas City, Kansas City, MO 64110, USA; (V.J.); (J.K.)
| | - Jagadish Koyi
- Department of Internal Medicine, University of Missouri-Kansas City, Kansas City, MO 64110, USA; (V.J.); (J.K.)
| | - Dushyant Singh Dahiya
- Division of Gastroenterology, Hepatology & Motility, The University of Kansas School of Medicine, Kansas City, KS 66160, USA;
| | - Hemant Goyal
- Department of Surgery, Center for Interventional Gastroenterology at UT (iGUT), The University of Texas Health Science Center, Houston, TX 77054, USA;
| | - Neil R. Sharma
- Advanced Interventional Endoscopy & Endoscopic Oncology (IOSE) Division, GI Oncology Tumor Site Team, Parkview Cancer Institute, 11104 Parkview Circle, Suite 310, Fort Wayne, IN 46845, USA;
| | - Abhilash Perisetti
- Division of Gastroenterology and Hepatology, Kansas City Veteran Affairs, Kansas City, MO 64128, USA
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Poston LM, Gupta S, Alvarado CE, Sinopoli J, Vargas LT, Linden PA, Towe CW. Contemporary outcomes of esophageal and gastroesophageal junction neuroendocrine tumors. Dis Esophagus 2023:6995427. [PMID: 36688874 DOI: 10.1093/dote/doad001] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/05/2022] [Revised: 11/28/2022] [Accepted: 12/31/2022] [Indexed: 01/24/2023]
Abstract
Adenocarcinoma and squamous cell esophageal cancers have been extensively studied in the literature. Esophageal neuroendocrine (NET)/carcinoid tumors are less commonly studied and have only been described in small series. The purpose of this study was to describe the demographics and natural history of esophageal NETs, as well as optimal treatments. We hypothesized that surgical resection would be the best treatment of esophageal NETs. The National Cancer Database was used to identify adult patients with esophageal or gastroesophageal junction (GEJ) cancer from 2004 to 2018. Patients were characterized as carcinoid/NET, adenocarcinoma, or squamous cell cancer. Clinical and demographic characteristics were compared between the histology groups. The primary outcome was overall survival, which was assessed by multivariable Cox analysis. Multivariable Cox analysis was also used to analyze factors associated with survival among NET patients who underwent surgery. Among 206,321 patients with esophageal cancer, 1,563 were NETs (<0.01%). Relative to the other two histologies, NETs were associated with younger age, female sex, and advanced clinical stage at diagnosis. Multivariate analysis suggested that NETs were less likely to be treated with surgical resection (OR 0.51, P < 0.001). Nonetheless, surgical resection was associated with improved survival (HR 0.64, P = 0.003). Among patients with NETs who received surgery, neoadjuvant therapy was associated with improved overall survival (HR 0.38, P = 0.013). NET of the esophagus presents with more advanced disease than other common histologies. Among patients with nonmetastatic cancer, surgical resection appears to be the best treatment. Neoadjuvant systemic therapy may offer survival benefit, but future studies are necessary.
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Affiliation(s)
- Lauren M Poston
- Case Western Reserve University School of Medicine, Cleveland, OH, USA
| | - Shreya Gupta
- Division of Thoracic and Esophageal Surgery, Department of Surgery, University Hospitals Cleveland Medical Center, Cleveland, OH, USA
| | - Christine E Alvarado
- Division of Thoracic and Esophageal Surgery, Department of Surgery, University Hospitals Cleveland Medical Center, Cleveland, OH, USA
| | - Jillian Sinopoli
- Division of Thoracic and Esophageal Surgery, Department of Surgery, University Hospitals Cleveland Medical Center, Cleveland, OH, USA
| | - Leonidas T Vargas
- Division of Thoracic and Esophageal Surgery, Department of Surgery, University Hospitals Cleveland Medical Center, Cleveland, OH, USA
| | - Philip A Linden
- Division of Thoracic and Esophageal Surgery, Department of Surgery, University Hospitals Cleveland Medical Center, Cleveland, OH, USA
| | - Christopher W Towe
- Division of Thoracic and Esophageal Surgery, Department of Surgery, University Hospitals Cleveland Medical Center, Cleveland, OH, USA
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Sanghi V, Amin H, Sanaka MR, Thota PN. Resection of early esophageal neoplasms: The pendulum swings from surgical to endoscopic management. World J Gastrointest Endosc 2019; 11:491-503. [PMID: 31798770 PMCID: PMC6885444 DOI: 10.4253/wjge.v11.i10.491] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/11/2019] [Revised: 08/09/2019] [Accepted: 09/11/2019] [Indexed: 02/06/2023] Open
Abstract
Esophageal cancer is a highly lethal disease and is the sixth leading cause of cancer related mortality in the world. The standard treatment is esophagectomy which is associated with significant morbidity and mortality. This led to development of minimally invasive, organ sparing endoscopic therapies which have comparable outcomes to esophagectomy in early cancer. These include endoscopic mucosal resection and endoscopic submucosal dissection. In early squamous cell cancer, endoscopic submucosal dissection is preferred as it is associated with cause specific 5-year survival rates of 100% for M1 and M2 tumors and 85% for M3 and SM1 tumors and low recurrence rates. In early adenocarcinoma, endoscopic resection of visible abnormalities is followed by ablation of the remaining flat Barrett’s mucosa to prevent recurrences. Radiofrequency ablation is the most widely used ablation modality with others being cryotherapy and argon plasma coagulation. Focal endoscopic mucosal resection followed by radiofrequency ablation leads to eradication of neoplasia in 93.4% of patients and eradication of intestinal metaplasia in 73.1% of patients. Innovative techniques such as submucosal tunneling with endoscopic resection are developed for management of submucosal tumors of the esophagus. This review includes a discussion of various endoscopic techniques and their clinical outcomes in early squamous cell cancer, adenocarcinoma and submucosal tumors. An overview of comparison between esophagectomy and endoscopic therapy are also presented.
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Affiliation(s)
- Vedha Sanghi
- Department of Internal Medicine, Cleveland Clinic, Cleveland, OH 44195, United States
| | - Hina Amin
- Department of Gastroenterology and Hepatology, Cleveland Clinic, Cleveland, OH 44195, United States
| | - Madhusudhan R Sanaka
- Department of Gastroenterology and Hepatology, Cleveland Clinic, Cleveland, OH 44195, United States
| | - Prashanthi N Thota
- Department of Gastroenterology and Hepatology, Cleveland Clinic, Cleveland, OH 44195, United States
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Okata T, Uno K, Fujishima F, Saito M, Jin X, Hatta W, Asanuma K, Asano N, Koike T, Imatani A, Masamune A. Difficult Preoperative Diagnosis of Lymphoepithelioma-Like Carcinoma of the Esophagus. ACG Case Rep J 2019; 6:e00163. [PMID: 31737702 PMCID: PMC6791625 DOI: 10.14309/crj.0000000000000163] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/20/2019] [Accepted: 06/04/2019] [Indexed: 01/13/2023] Open
Abstract
A 60-year-old man with a medical history of diabetes, liver cirrhosis, and distal gastrectomy was referred for further examination of a 10-mm pale-colored submucosal tumor around 40 cm from the incisors. Narrow band imaging-magnifying endoscopy revealed the lesion covered by smooth epithelium with irregular microvascular architecture in a sparse distribution. Endosonography showed an irregular-shaped hypoechoic lesion in the submucosa. With no evidence of metastases, we performed en bloc endoscopic submucosal dissection, whose specimen revealed esophageal lymphoepithelioma-like carcinoma invading up to 500 μm in the submucosa, a rare disease entity. Despite no additional treatment, he was alive without recurrence for longer than 88 months.
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Affiliation(s)
- Tomoki Okata
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
| | - Kaname Uno
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
| | | | - Masahiro Saito
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
| | - Xiaoyi Jin
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
| | - Waku Hatta
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
| | - Kiyotaka Asanuma
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
| | - Naoki Asano
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
| | - Tomoyuki Koike
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
| | - Akira Imatani
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
| | - Atsushi Masamune
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Miyagi, Japan
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Findeis SK, Agarwal A. Incidental neuroendocrine tumor of the esophagus: A case report and review of the literature. HUMAN PATHOLOGY: CASE REPORTS 2019. [DOI: 10.1016/j.ehpc.2019.02.005] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/27/2022] Open
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Giannetta E, Guarnotta V, Rota F, de Cicco F, Grillo F, Colao A, Faggiano A. A rare rarity: Neuroendocrine tumor of the esophagus. Crit Rev Oncol Hematol 2019; 137:92-107. [PMID: 31014519 DOI: 10.1016/j.critrevonc.2019.02.012] [Citation(s) in RCA: 35] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/30/2018] [Revised: 08/08/2018] [Accepted: 02/26/2019] [Indexed: 01/09/2023] Open
Abstract
Esophageal Neuroendocrine tumors (NETs) are rare, aggressive and lacking specific symptoms. This causes a diagnostic delay, worsening the prognosis. Numerous cases are reported in literature, without a consensus on the management. Our aim was to clarify epidemiology, clinical presentation, diagnostic, therapeutic management of esophageal NETs. Extensive literature search identified a total of 226 articles. One hundred twenty-five articles (n = 1676) met the inclusion criteria, showing that: the incidence of esophageal NET varies geographically; men (60-70 years) are more affected; smoking and alcohol abuse are the major risk factors; dysphagia, weight loss, appetite loss are the most common clinical features. The histotypes include high-grade small and large cell esophageal carcinomas and low-grade carcinoid tumors. Mixed neuroendocrine/non-neuroendocrine neoplasms are the most common. Often the diagnosis occurs randomly on endoscopic examination. Circulating markers, functional combined with conventional imaging contributes to the diagnosis and management. Treatment depends on type, grade and stage of the tumor.
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Affiliation(s)
- Elisa Giannetta
- Dept. of Experimental Medicine, "Sapienza" University of Rome, Italy.
| | - Valentina Guarnotta
- Biomedical Department of Internal and Specialist Medicine (DIBIMIS), Section of Endocrine-Metabolic Diseases, University of Palermo, Italy
| | - Francesca Rota
- Unit of Endocrinology, San Camillo-Forlanini Hospital, Rome, Italy
| | - Federica de Cicco
- Department of Clinical Medicine and Surgery, University "Federico II", Naples, Italy
| | - Federica Grillo
- Pathology Unit, Department of Surgical Sciences and Integrated Diagnostics (DISC), University of Genova and Ospedale Policlinico San Martino, Genova, Italy
| | - Annamaria Colao
- Department of Clinical Medicine and Surgery, University "Federico II", Naples, Italy
| | - Antongiulio Faggiano
- Thyroid and Parathyroid Surgery Unit, Istituto Nazionale per lo Studio e la Cura dei Tumori "Fondazione G. Pascale", IRCCS, Naples, Italy
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Carcinoid tumour of the oesophagus: a systematic review. GASTROENTEROLOGY REVIEW 2018; 13:196-199. [PMID: 30302162 PMCID: PMC6173072 DOI: 10.5114/pg.2018.78285] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 08/25/2017] [Accepted: 01/04/2018] [Indexed: 01/15/2023]
Abstract
Introduction Knowledge about oesophageal carcinoids is based primarily on case reports, and therefore information about them is incomplete. Aim To collect information on oesophageal carcinoid tumours in a systematic review study. Material and methods Databases including PubMed, Scopus, and Web of Science were searched for the characteristics of oesophageal carcinoid tumour. Studies included original articles, case series, or case reports, reporting at least one of the characteristics of benign carcinoid tumour or carcinoid tumour. Results Out of 670 studies searched, after evaluation and excluding non-relevant studies, 14 studies were included and analysed in the systematic review. These studies included 19 patients with carcinoid tumour of whom 57.9% were males with a mean age of 55.5 years. Dysphagia and weight loss were the most prevalent symptoms and signs in the patients. Lower oesophagus was the most prevalent site of tumour. Conclusions This meta-analysis showed that the mean age at diagnosis of oesophageal carcinoid was around 55 years, with 1.4 times greater prevalence among males, and located mainly in the distal oesophagus. The mean tumour size was 2.4 cm. The main symptoms and signs of this disease were dysphagia, weight loss, and reflux. The tumour behaviour was mainly non-aggressive except for cases associated with adenocarcinoma.
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Yazici C, Boulay BR. Evolving role of the endoscopist in management of gastrointestinal neuroendocrine tumors. World J Gastroenterol 2017; 23:4847-4855. [PMID: 28785139 PMCID: PMC5526755 DOI: 10.3748/wjg.v23.i27.4847] [Citation(s) in RCA: 15] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/29/2017] [Revised: 05/05/2017] [Accepted: 06/12/2017] [Indexed: 02/06/2023] Open
Abstract
Neuroendocrine tumors (NETs) are uncommon gastrointestinal neoplasms but have been increasingly recognized over the past few decades. Luminal NETs originate from the submucosa of the gastrointestinal tract and careful endoscopic exam is a key for accurate diagnosis. Despite their reputation as indolent tumors with a good prognosis, some NETs may have aggressive features with associated poor long-term survival. Management of NETs requires full understanding of tumor size, depth of invasion, local lymphadenopathy status, and location within the gastrointestinal tract. Staging with endoscopic ultrasound or cross-sectional imaging is important for determining whether endoscopic treatment is feasible. In general, small superficial NETs can be managed by endoscopic mucosal resection and endoscopic submucosal dissection (ESD). In contrast, NETs larger than 2 cm are almost universally treated with surgical resection with lymphadenectomy. For those tumors between 11-20 mm in size, careful evaluation can identify which NETs may be managed with endoscopic resection. The increasing adoption of ESD may improve the results of endoscopic resection for luminal NETs. However, enthusiasm for endoscopic resection must be tempered with respect for the more definitive curative results afforded by surgical treatment with more advanced lesions.
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Ma Z, Cai H, Cui Y. Progress in the treatment of esophageal neuroendocrine carcinoma. Tumour Biol 2017; 39:1010428317711313. [PMID: 28653897 DOI: 10.1177/1010428317711313] [Citation(s) in RCA: 25] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/14/2023] Open
Abstract
Esophageal neuroendocrine neoplasms are rare. With the improvement and popularization of diagnostic methods, the morbidity statistics have increased annually in recent years. There are currently no treatment guidelines for esophageal neuroendocrine neoplasms, and surgery is the only cure. This usually involves radical surgery when the tumor is limited to the primary site or when only regional lymph node metastasis occurs. Surgical treatment is key to treating esophageal neuroendocrine neoplasms, but combined treatment with chemotherapy and radiotherapy can significantly improve patient survival. The effect of radiotherapy alone on this disease is poor. However, targeted endocrine therapy can improve endocrine hormone symptoms. The prognosis of patients with esophageal neuroendocrine neoplasms is mainly determined by the pathological stage. With the development of molecular biology techniques, the combination of targeted drugs and traditional chemotherapy is expected to provide novel ideas and directions for the treatment of esophageal neuroendocrine neoplasms in the coming years. In this article, the status of esophageal neuroendocrine tumor treatments was reviewed in detail.
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Affiliation(s)
- Zheng Ma
- Department of Thoracic Surgery, The First Hospital of Jilin University, Changchun, China
| | - Hongfei Cai
- Department of Thoracic Surgery, The First Hospital of Jilin University, Changchun, China
| | - Youbin Cui
- Department of Thoracic Surgery, The First Hospital of Jilin University, Changchun, China
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Tustumi F, Takeda FR, Uema RH, Pereira GLS, Sallum RAA, Cecconello I. Primary neuroendocrine neoplasm of the esophagus - Report of 14 cases from a single institute and review of the literature. ARQUIVOS DE GASTROENTEROLOGIA 2017; 54:4-10. [PMID: 28079231 DOI: 10.1590/s0004-2803.2017v54n1-01] [Citation(s) in RCA: 23] [Impact Index Per Article: 2.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/09/2016] [Accepted: 08/22/2016] [Indexed: 02/08/2023]
Abstract
BACKGROUND: Most prevalent esophageal neoplasm is squamous cell carcinoma and adenocarcinoma. Other tumors are uncommon and poorly studied. Primary neuroendocrine esophageal neoplasm is a rare carcinoma and most of its therapy management is based on lung neuroendocrine studies. Neuroendocrine tumors can be clustered in the following subtypes: high grade (small cell carcinoma or large cell carcinoma) and low grade (carcinoids). OBJECTIVE: The present study aims to assess clinical and pathological neuroendocrine esophageal tumors in a single oncologic center. METHODS: A retrospective analysis of patients and review of the literatures was performed. RESULTS: Fourteen patients were identified as neuroendocrine tumors, 11 male and 3 female patients. Mean age was 67.3 years old. Ten patients were classified as small cell, 3 as large cell and 1 as carcinoid. Four patients presented squamous cell carcinoma simultaneously and 1 also presented adenocarcinoma. Main sites of metastasis were liver, peritoneum, lung and bones. Most patients died before 2 years of follow-up. Patient with longer survival died at 35 months after diagnosis. CONCLUSION: Neuroendocrine esophageal tumors are rare; affect mainly men in their sixties or seventies. High grade tumors can be mixed to other subtypes neoplasms, such as adenocarcinoma and squamous cell carcinoma. Most of these patients have poor overall survival rates.
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Affiliation(s)
- Francisco Tustumi
- Cirurgia do Aparelho Digestivo, Faculdade de Medicina, Hospital das Clínicas, USP, SP, Brasil
| | | | - Rodrigo Hideki Uema
- Faculdade de Medicina, Hospital das Clínicas, Universidade de São Paulo, SP, Brasil
| | | | | | - Ivan Cecconello
- Cirurgia do Aparelho Digestivo, Faculdade de Medicina, Hospital das Clínicas, USP, SP, Brasil
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Huang YQ. Current progress in diagnosis and therapy of neuroendocrine neoplasms of the digestive system. Shijie Huaren Xiaohua Zazhi 2016; 24:2625-2636. [DOI: 10.11569/wcjd.v24.i17.2625] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/06/2023] Open
Abstract
Neuroendocrine neoplasms (NENs) are a group of heterogeneous, biologically diverse, rare malignancies originated from the peptidergic neurons and neuroendocrine cells. In recent years, the incidence of NENs has been increasing gradually. They typically arise in the pancreas and gastrointestinal tract. Chromogranin A (CgA) has long been used as an important broad-spectrum marker for the identification of NENs. The diagnosis is based on histopathology demonstrating neuroendocrine features such as positive staining for chromogranin A and specific hormones such as gastrin, proinsulin, vasoactive intestinal peptide (VIP) and glucagon. In addition, radiological modalities including computed tomography (CT), positron emission tomography and computed tomography (PET/CT), magnetic resonance imaging (MRI), ultrasound (US), endoscopic ultrasound (EUS), and somatostatin receptor scintigraphy (SRS) can help establish a diagnosis. Surgery is still one of the cornerstones in the management of NENs. This article reviews the current progress in the diagnosis and therapy of NENs of the digestive system, including the pathological features and clinical diagnostic modalities for primary esophageal, gastric, duodenal, small intestinal, appendiceal, colonic, rectal, hepatic, gallbladder, extrahepatic bile duct, and pancreatic NENs, according to a revised system of classification, nomenclature and grading of NENs proposed by the fourth edition of "World Health Organization (WHO) classification of tumours of the digestive system" in 2010, and consensus of diagnosis and treatment of gastroenteropancreatic NENs (GEP-NENs) proposed by the Chinese Society of Clinical Oncology (CSCO) in 2013.
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