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Ogata Y, Hatta W, Kanno T, Saito M, Jin X, Asano N, Koike T, Imatani A, Yuan Y, Masamune A. Type 2 and type 3 gastric neuroendocrine tumors have high risk of lymph node metastasis: Systematic review and meta-analysis. Dig Endosc 2025. [PMID: 40170116 DOI: 10.1111/den.15026] [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: 11/27/2024] [Accepted: 03/05/2025] [Indexed: 04/03/2025]
Abstract
OBJECTIVES Lymph node metastasis (LNM) is crucial in determining treatment strategies for gastric neuroendocrine tumors (gNETs). While type 3 is considered more aggressive than types 1 and 2 within the clinical subtype of gNETs, the supporting data were insufficient, due to their rarity. We aimed to study the prevalence and risk factors associated with LNM in gNETs. METHODS We searched electronic databases from 1990 to 2023 to identify case-control and cohort studies regarding gNETs resected either endoscopically or surgically. The primary outcome measured was the pooled prevalence of LNM in gNETs. Secondary outcomes included categorizing the prevalence of LNM by clinical subtypes and identifying pathological risk factors associated with LNM in gNETs. RESULTS We included 28 studies, involving 1742 patients, among whom 240 had LNM (pooled prevalence rate, 11.8%; 95% confidence interval 7.6-17.9%). The pooled prevalence rates of LNM for type 1, type 2, and type 3 gNETs were 6.0%, 38.5%, and 23.2%, respectively. Type 2 (odds ratio [95% confidence interval] 11.53 [3.46-38.49]) and type 3 (6.88 [3.79-12.49]) gNETs exhibited a higher risk for LNM compared to type 1. Pathological risk factors for LNM included tumor size >10 mm (4.18 [1.91-9.17]), tumor invasion into the muscularis propria or deeper (11.21 [3.50-35.92]), grade 2/grade 3 (5.96 [2.65-13.40]), and lymphovascular invasion (34.50 [6.70-177.51]). CONCLUSION We demonstrated that type 2 gNETs, as well as type 3, had a high risk of LNM. Additionally, four pathological risk factors associated with LNM were identified.
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Affiliation(s)
- Yohei Ogata
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Miyagi, Japan
| | - Waku Hatta
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Miyagi, Japan
| | - Takeshi Kanno
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Miyagi, Japan
| | - Masahiro Saito
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Miyagi, Japan
| | - Xiaoyi Jin
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Miyagi, Japan
| | - Naoki Asano
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Miyagi, Japan
| | - Tomoyuki Koike
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Miyagi, Japan
| | - Akira Imatani
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Miyagi, Japan
| | - Yuhong Yuan
- Department of Medicine, London Health Science Centre, London, Ontario, Canada
| | - Atsushi Masamune
- Division of Gastroenterology, Tohoku University Graduate School of Medicine, Miyagi, Japan
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Son C, Kalapala J, Leya J, Popadiuk MM, Atieh MK, Havlichek D, Feldman L, Roach P, Banerjee P. Gastroesophageal Neuroendocrine Tumors: Outcomes and Management. J Clin Med 2025; 14:2148. [PMID: 40217599 PMCID: PMC11989656 DOI: 10.3390/jcm14072148] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/03/2025] [Revised: 03/14/2025] [Accepted: 03/15/2025] [Indexed: 04/14/2025] Open
Abstract
Background/Objectives: Neuroendocrine tumors (NETs) can arise in any organ and are most commonly found in the lungs and gastroenteropancreatic (GEP) system. GEP-NETs represent a small percentage of gastrointestinal cancers, and therefore, the standard treatment is not well-defined, especially for advanced disease. Our objective is to review GI NETs among veterans and analyze their therapeutic outcomes. Methods: A total of 61 GI NET cases were identified from our institution from 2019-2024. In total, twenty-seven review papers, ten population-based/multicenter/outcome studies, six case reports, and one case series were reviewed for the literature review. Results: The incidence of GI NETs at our institution was higher than the known epidemiology of GI NETs. Small intestine NETs were one of the most common sites of GEP-NETs at our institution, with only one of nineteen cases being grade 3 poorly differentiated neuroendocrine carcinoma. All cases of colonic and rectal NETs had good clinical outcomes consistent with findings from the literature. Most of the gastric NETs were type 1 and had benign courses of disease, except for one case with an intermediate grade and metastatic liver lesions. One case of esophageal neuroendocrine carcinoma (E-NEC) showed a complete response to chemotherapy despite a significant tumor burden on presentation and high-grade pathology, while another case of ENEC had recurrent disease despite systemic therapy. Conclusions: While the role of surgery or endoscopic resection is limited to localized tumors, combined treatment with chemoradiation can significantly improve patient outcomes, especially in high-grade, poorly differentiated tumors. Further studies are needed to establish systemic (i.e., chemotherapy and radiation) treatment strategies for poorly differentiated GI NETs.
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Affiliation(s)
- Christine Son
- Edward Hines VA Hospital, Hines, IL 60141, USA; (J.L.); (M.M.P.); (M.K.A.); (L.F.); (P.R.); (P.B.)
- Loyola Internal Medicine, University Medical Center, Maywood, IL 60153, USA
| | | | - Jeff Leya
- Edward Hines VA Hospital, Hines, IL 60141, USA; (J.L.); (M.M.P.); (M.K.A.); (L.F.); (P.R.); (P.B.)
| | - Michelle Marion Popadiuk
- Edward Hines VA Hospital, Hines, IL 60141, USA; (J.L.); (M.M.P.); (M.K.A.); (L.F.); (P.R.); (P.B.)
| | - Mohammed K. Atieh
- Edward Hines VA Hospital, Hines, IL 60141, USA; (J.L.); (M.M.P.); (M.K.A.); (L.F.); (P.R.); (P.B.)
- Loyola Internal Medicine, University Medical Center, Maywood, IL 60153, USA
| | - Daniel Havlichek
- Edward Hines VA Hospital, Hines, IL 60141, USA; (J.L.); (M.M.P.); (M.K.A.); (L.F.); (P.R.); (P.B.)
- Loyola Internal Medicine, University Medical Center, Maywood, IL 60153, USA
| | - Lawrence Feldman
- Edward Hines VA Hospital, Hines, IL 60141, USA; (J.L.); (M.M.P.); (M.K.A.); (L.F.); (P.R.); (P.B.)
- UI Health, University of Illinois in Chicago Hospital Health Sciences System, UIC Medical Center, Chicago, IL 60612, USA
| | - Paul Roach
- Edward Hines VA Hospital, Hines, IL 60141, USA; (J.L.); (M.M.P.); (M.K.A.); (L.F.); (P.R.); (P.B.)
| | - Promila Banerjee
- Edward Hines VA Hospital, Hines, IL 60141, USA; (J.L.); (M.M.P.); (M.K.A.); (L.F.); (P.R.); (P.B.)
- Loyola Internal Medicine, University Medical Center, Maywood, IL 60153, USA
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3
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Ortigão R, Afonso LP, Pimentel-Nunes P, Dinis-Ribeiro M, Libânio D. Predictors of Outcomes in Gastric Neuroendocrine Tumors: A Retrospective Cohort. GE PORTUGUESE JOURNAL OF GASTROENTEROLOGY 2024; 31:236-245. [PMID: 39022301 PMCID: PMC11250119 DOI: 10.1159/000530684] [Citation(s) in RCA: 1] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Received: 09/30/2022] [Accepted: 02/02/2023] [Indexed: 07/20/2024]
Abstract
INTRODUCTION/AIM Gastric neuroendocrine tumors (GNETs) frequently have an indolent clinical course, despite their metastatic potential. The aim of the study was to identify prognostic factors associated with overall survival and risk of metastases and to evaluate the impact of serial measurements of chromogranin A (CgA). METHODS The authors performed a retrospective cohort study including consecutive patients with GNET diagnosed between 2010 and 2019, with a minimum follow-up of 1 year. Univariate and multivariate analyses were performed. RESULTS We included 132 patients with GNET (type I, 113 patients; type II, 1 patient; type III, 14 patients; type IV, 2 patients; not classifiable, 2 patients), with 61% being female and a mean age at diagnosis of 66 years. During the follow-up period (median 66 months), 3 (2.3%) patients died due to metastatic disease (1 patient with type III and 2 patients with type IV). Male gender (p = 0.030), type III/IV (p < 0.001), Ki-67 index >20% (p < 0.001), grade 2/3 (p < 0.001), invasion beyond the submucosa (p < 0.001), and presence of metastases (p < 0.001) were identified as risk factors for mortality in the univariate analysis. Metastasis developed in 7 patients (5.3%). Multivariable analysis revealed that Ki-67 >20% (p = 0.016) was an independent risk factor for metastasis. Overall, CgA showed a sensitivity of 20% for detection of recurrence and a specificity of 79% (sensitivity of 8% and specificity of 71% in type I GNETs). CONCLUSION Identification of risk factors for the presence of metastases and for mortality in these groups of patients can help in individualizing the therapeutic strategy. CgA seems to be a weak marker for monitoring patients with GNET.
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Affiliation(s)
- Raquel Ortigão
- Gastroenterology Department, Portuguese Oncology Institute of Porto, Porto, Portugal
| | - Luís Pedro Afonso
- Department of Pathology, Portuguese Oncology Institute of Porto, Porto, Portugal
| | - Pedro Pimentel-Nunes
- Department of Surgery and Physiology, Faculty of Medicine, University of Porto (FMUP), Porto, Portugal
- RISE@CI-IPOP (Health Research Network, IPO Porto), Porto Comprehensive Cancer Center (Porto.CCC), Porto, Portugal
- Unilabs Portugal, Porto, Portugal
| | - Mário Dinis-Ribeiro
- Gastroenterology Department, Portuguese Oncology Institute of Porto, Porto, Portugal
- MEDCIDS, Faculty of Medicine, University of Porto, Porto, Portugal
| | - Diogo Libânio
- Gastroenterology Department, Portuguese Oncology Institute of Porto, Porto, Portugal
- MEDCIDS, Faculty of Medicine, University of Porto, Porto, Portugal
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Dell’Unto E, Marasco M, Mosca M, Gallo C, Esposito G, Rinzivillo M, Pilozzi E, Orrù F, Campana D, Massironi S, Annibale B, Panzuto F. Clinical Outcome of Patients with Gastric, Duodenal, or Rectal Neuroendocrine Tumors after Incomplete Endoscopic Resection. J Clin Med 2024; 13:2535. [PMID: 38731064 PMCID: PMC11084244 DOI: 10.3390/jcm13092535] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/18/2024] [Revised: 04/16/2024] [Accepted: 04/23/2024] [Indexed: 05/13/2024] Open
Abstract
Objectives: Our aim was to investigate the clinical outcome of patients with well-differentiated gastric, duodenal, and rectal neuroendocrine tumors after treatment with incomplete endoscopic resection due to the finding of microscopic positive resection margins (R1). Methods: This is a retrospective analysis of consecutive patients with type 1 gastric, non-ampullary non-functioning duodenal, or rectal neuroendocrine neoplasms with positive R1 margins after endoscopic resection. The rate of tumor recurrence and progression-free survival were considered to be the study's main endpoints. Statistical analysis was performed using MedCalc® v.17 software and a p-value of <0.05 was considered significant. A Cox proportional-hazard regression was performed to identify risk factors for disease recurrence/progression. Results: After evaluating 110 patients, a total of 58 patients were included in the final analysis (15 gastric NENs, 12 duodenal NENs, and 31 rectal NENs). After evidence of endoscopic R1 resection had been gathered, 26 patients (44.8%) underwent an endoscopic/surgical extension of the previous resection. Tumor progression (all local recurrences) occurred in five out of fifty-eight patients (8.6%) with a median PFS of 36 months. There were no tumor-related deaths. G2 grading and the gastric primary tumor site were the only features significantly associated with the risk of recurrence of the disease (HR: 11.97 [95% CI: 1.22-116.99], HR: 12.54 [95% CI: 1.28-122.24], respectively). Conclusions: Tumor progression rarely occurs in patients with microscopic positive margin excision (R1) after endoscopic resection and does not seem to affect patients' clinical outcomes.
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Affiliation(s)
- Elisabetta Dell’Unto
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy; (E.D.); (M.M.); (G.E.); (M.R.); (B.A.)
- Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy
| | - Matteo Marasco
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy; (E.D.); (M.M.); (G.E.); (M.R.); (B.A.)
- Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy
- PhD School in Translational Medicine and Oncology, Sapienza University of Rome, 00189 Rome, Italy
| | - Mirta Mosca
- Department of Experimental, Diagnostic & Specialty Medicine (DIMES), University of Bologna, 40138 Bologna, Italy; (M.M.); (D.C.)
- Medical Oncology, IRCCS Azienda Ospedaliero, Universitaria of Bologna, 40138 Bologna, Italy
| | - Camilla Gallo
- Division of Gastroenterology, Fondazione IRCCS San Gerardo dei Tintori, 20900 Monza, Italy; (C.G.); (S.M.)
| | - Gianluca Esposito
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy; (E.D.); (M.M.); (G.E.); (M.R.); (B.A.)
- Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy
| | - Maria Rinzivillo
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy; (E.D.); (M.M.); (G.E.); (M.R.); (B.A.)
| | - Emanuela Pilozzi
- Department of Clinical and Molecular Medicine, UOC Anatomic Pathology, Sant’Andrea Hospital, Sapienza University of Rome, 00189 Rome, Italy; (E.P.); (F.O.)
| | - Federica Orrù
- Department of Clinical and Molecular Medicine, UOC Anatomic Pathology, Sant’Andrea Hospital, Sapienza University of Rome, 00189 Rome, Italy; (E.P.); (F.O.)
| | - Davide Campana
- Department of Experimental, Diagnostic & Specialty Medicine (DIMES), University of Bologna, 40138 Bologna, Italy; (M.M.); (D.C.)
- Medical Oncology, IRCCS Azienda Ospedaliero, Universitaria of Bologna, 40138 Bologna, Italy
| | - Sara Massironi
- Division of Gastroenterology, Fondazione IRCCS San Gerardo dei Tintori, 20900 Monza, Italy; (C.G.); (S.M.)
| | - Bruno Annibale
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy; (E.D.); (M.M.); (G.E.); (M.R.); (B.A.)
- Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy
| | - Francesco Panzuto
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence or Rome, 00189 Rome, Italy; (E.D.); (M.M.); (G.E.); (M.R.); (B.A.)
- Department of Medical, Surgical Sciences and Translational Medicine, Sapienza University of Rome, 00189 Rome, Italy
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5
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Huang J, Liu H, Yang D, Xu T, Wang J, Li J. Personalized treatment of well-differentiated gastric neuroendocrine tumors based on clinicopathological classification and grading: A multicenter retrospective study. Chin Med J (Engl) 2024; 137:720-728. [PMID: 38384175 PMCID: PMC10950134 DOI: 10.1097/cm9.0000000000003029] [Citation(s) in RCA: 2] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/17/2023] [Indexed: 02/23/2024] Open
Abstract
BACKGROUND The incidence of well-differentiated gastric neuroendocrine tumors (G-NET) is increasing annually, and while they have a good prognosis and low mortality rate, their high recurrence rate makes treatment options controversial. This study aims to determine the relationship between individualized treatment plans and the recurrence of G-NET. METHODS We performed a multicenter, retrospective study of 94 patients with highly differentiated G-NET and treated at Peking Union Medical College Hospital, Yantai Yuhuangding Hospital, and Beijing Zhong-Neng-Jian Hospital from November 2015 to September 2023. Risk factors for recurrence of G-NETs were investigated using chi-squared test and multifactorial logistic regression analysis. RESULTS After a median follow-up of 49 months, the overall recurrence rate among the 94 G-NET patients was 14% (13/94). The recurrence rates of endoscopic mucosal resection (EMR), endoscopic submucosal dissection (ESD), somatostatin analog (SSA) therapy, and surgery were 43% (6/14), 10% (5/49), 5% (1/22), and 11% (1/9), respectively. Post-treatment recurrence rates were significantly different ( P = 0.014) among four treatments (EMR, ESD, SSA, and surgery), and further subgroup comparisons revealed lower recurrence rates in the ESD and SSA groups than in the EMR group. From the second month onward, SSA therapy considerably reduced the gastrin levels from 1081.0 (571.5, 2472.8) pg/mL to 461.5 (255.3, 795.0) pg/mL ( Z = -3.521, P <0.001). Both chi-squared test and multifactorial logistic regression analysis suggested that among the clinicopathological parameters studied, only the pre-treatment gastrin level ( P = 0.018 and 0.005) and the type of treatment ( P = 0.014 and 0.017) were significantly associated with G-NET recurrence. CONCLUSIONS Individualized treatment strategies may reduce the risk of relapse after G-NET treatment. Long-term SSA therapy may be a secure and efficacious treatment option for type 1 G-NET with more than six lesions, and it substantially decreases the incidence of post-treatment recurrence.
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Affiliation(s)
- Ju Huang
- Department of Gastroenterology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing 100730, China
- Key Laboratory of Gut Microbiota Translational Medicine Research, Chinese Academy of Medical Sciences, Beijing 100730, China
| | - Huimin Liu
- Department of Gastroenterology, Affiliated Yantai Yuhuangding Hospital of Qingdao University Medical College, Yantai, Shandong 264000, China
| | - Dekun Yang
- Department of Gastroenterology, Beijing Zhong-Neng-Jian Hospital, Beijing 102401, China
| | - Tianming Xu
- Department of Gastroenterology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing 100730, China
- Key Laboratory of Gut Microbiota Translational Medicine Research, Chinese Academy of Medical Sciences, Beijing 100730, China
| | - Jing Wang
- Department of Gastroenterology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing 100730, China
- Key Laboratory of Gut Microbiota Translational Medicine Research, Chinese Academy of Medical Sciences, Beijing 100730, China
| | - Jingnan Li
- Department of Gastroenterology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing 100730, China
- Key Laboratory of Gut Microbiota Translational Medicine Research, Chinese Academy of Medical Sciences, Beijing 100730, China
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Sok C, Ajay PS, Tsagkalidis V, Kooby DA, Shah MM. Management of Gastric Neuroendocrine Tumors: A Review. Ann Surg Oncol 2024; 31:1509-1518. [PMID: 38062290 PMCID: PMC10922891 DOI: 10.1245/s10434-023-14712-9] [Citation(s) in RCA: 14] [Impact Index Per Article: 14.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/18/2023] [Accepted: 11/20/2023] [Indexed: 01/30/2024]
Abstract
Gastric neuroendocrine tumors (G-NET) are rare tumors arising from enterochromaffin-like cells of the gastric mucosa. They belong to a larger group called gastroenteropancreatic neuroendocrine tumors and are classified as low, intermediate, or high-grade tumors based on their proliferative indices. They are further categorized into three subtypes based on their morphologic characteristics, pathogenesis, and behavior. Types 1 and 2 tumors are characterized by elevated serum gastrin and are usually multifocal. They typically occur in the setting of atrophic gastritis or MEN1/Zollinger Ellison syndrome, respectively. Type 2 tumors are associated with the most symptoms, such as abdominal pain and diarrhea. Type 3 tumors are associated with normal serum gastrin, are usually solitary, and occur sporadically. This type has the most aggressive phenotype and metastatic potential. Treatment and prognosis for G-NET is dependent on their type, size, and stage. Type 1 has the best prognosis, and Type 3 has the worst. This review discusses the presentation, workup, and surgical management of these tumors.
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Affiliation(s)
- Caitlin Sok
- Division of Surgical Oncology, Department of Surgery, Emory University School of Medicine, Atlanta, GA, USA
| | - Pranay S Ajay
- Division of Surgical Oncology, Department of Surgery, Emory University School of Medicine, Atlanta, GA, USA
| | - Vasileios Tsagkalidis
- Division of Surgical Oncology, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, USA
| | - David A Kooby
- Division of Surgical Oncology, Department of Surgery, Emory University School of Medicine, Atlanta, GA, USA
| | - Mihir M Shah
- Division of Surgical Oncology, Department of Surgery, Emory University School of Medicine, Atlanta, GA, USA.
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Guo X, Zhao X, Huang G, Yu Y. Advances in Endoscopic Diagnosis and Treatment of Gastric Neuroendocrine Neoplasms. Dig Dis Sci 2024; 69:27-35. [PMID: 37971578 DOI: 10.1007/s10620-023-08180-0] [Citation(s) in RCA: 2] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/12/2023] [Accepted: 11/01/2023] [Indexed: 11/19/2023]
Abstract
Gastric neuroendocrine neoplasms refer to a group of diseases that are relatively rare. They can be classified into three subtypes based on their clinical and histopathological features, and there are significant differences in diagnosis, treatment, and prognosis among the different subtypes. The incidence of gastric neuroendocrine neoplasms has been increasing globally in recent years with the localized disease being particularly evident. Gastrointestinal endoscopy is of irreplaceable importance for the diagnosis and management of g-NENs. Endoscopy with biopsy is the gold standard for the diagnosis of g-NENs. Ultrasound endoscopy can assess the depth of tumor invasion and the presence of lymphatic metastases, which is important for the development of treatment strategies. Meanwhile, for some small and low-risk lesions, endoscopic surveillance or endoscopic resection has satisfactory therapeutic results and prognosis. This means that even though the incidence has increased, advances in endoscopic techniques have allowed more patients to adopt a relatively conservative treatment strategy. However, the criteria for patients suitable for endoscopic surveillance or endoscopic resection remain controversial.
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Affiliation(s)
- Xinrui Guo
- Department of Gastroenterology, Qilu Hospital of Shandong University, 107 Wenhuaxi Road, Jinan, 250012, Shandong, People's Republic of China
- Shandong Provincial Clinical Research Center for Digestive Disease, Qilu Hospital of Shandong University, Jinan, Shandong, People's Republic of China
| | - Xiaohan Zhao
- Department of Gastroenterology, Qilu Hospital of Shandong University, 107 Wenhuaxi Road, Jinan, 250012, Shandong, People's Republic of China
- Shandong Provincial Clinical Research Center for Digestive Disease, Qilu Hospital of Shandong University, Jinan, Shandong, People's Republic of China
| | - Gang Huang
- Department of Gastroenterology, Qilu Hospital of Shandong University, 107 Wenhuaxi Road, Jinan, 250012, Shandong, People's Republic of China
- Shandong Provincial Clinical Research Center for Digestive Disease, Qilu Hospital of Shandong University, Jinan, Shandong, People's Republic of China
| | - Yanbo Yu
- Department of Gastroenterology, Qilu Hospital of Shandong University, 107 Wenhuaxi Road, Jinan, 250012, Shandong, People's Republic of China.
- Shandong Provincial Clinical Research Center for Digestive Disease, Qilu Hospital of Shandong University, Jinan, Shandong, People's Republic of China.
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Cavalcoli F, Gallo C, Coltro LA, Rausa E, Cantù P, Invernizzi P, Massironi S. Therapeutic Challenges for Gastric Neuroendocrine Neoplasms: Take It or Leave It? MEDICINA (KAUNAS, LITHUANIA) 2023; 59:1757. [PMID: 37893475 PMCID: PMC10608689 DOI: 10.3390/medicina59101757] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 08/28/2023] [Revised: 09/23/2023] [Accepted: 09/28/2023] [Indexed: 10/29/2023]
Abstract
Background and Objectives: Gastric neuroendocrine neoplasms (gNENs) represent rare but increasingly recognized tumors. They are distinguished into three main clinical types (type-1, type-2, and type-3) according to gastrin level and at histological evaluation in well-differentiated G1, G2, or G3 lesions, as well as poorly-differentiated lesions. Small type-1 and type-2 neoplasms with low proliferation indices demonstrated excellent survival without progression during an extended follow-up period, and for these reasons, active endoscopic observation or endoscopic resection are feasible options. On the other hand, surgery is the treatment of choice for more aggressive type-3, G3, or infiltrating neoplasms. The present study aims to comprehensively review and compare the available therapeutic strategies for gNENs. Materials and Methods: A computerized literature search was performed using relevant keywords to identify all of the pertinent articles with particular attention to gNEN endoscopic treatment. Results: In recent years, different endoscopic resective techniques (such as endoscopic mucosal dissection, modified endoscopic mucosal resection, and endoscopic full-thickness resection) have been developed, showing a high rate of complete resection for advanced and more aggressive lesions. Conclusions: Overall, gNENs represent a heterogeneous group of lesions with varying behavior which require personalized management. The non-operative approach for small type-1 gNENs seems to be feasible and should be promoted. A step-up approach with minimally invasive endoscopic therapies might be proposed, particularly for type-1 gNEN. On the other hand, it is important to recognize the negative prognostic factors in order to identify those rare cases requiring more aggressive approaches. A possible therapeutic algorithm for localized gNEN management is provided.
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Affiliation(s)
- Federica Cavalcoli
- Gastroenterology and Digestive Endoscopy Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, 20133 Milan, Italy; (F.C.); (P.C.)
| | - Camilla Gallo
- Division of Gastroenterology, Fondazione IRCCS San Gerardo dei Tintori, University of Milano-Bicocca School of Medicine, 20900 Monza, Italy; (C.G.)
| | - Lorenzo Andrea Coltro
- Division of Gastroenterology, Fondazione IRCCS San Gerardo dei Tintori, University of Milano-Bicocca School of Medicine, 20900 Monza, Italy; (C.G.)
| | - Emanuele Rausa
- Unit of Hereditary Digestive Tract Tumours, Department of Surgery, Fondazione IRCCS Istituto Nazionale dei Tumori, 20133 Milan, Italy;
| | - Paolo Cantù
- Gastroenterology and Digestive Endoscopy Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, 20133 Milan, Italy; (F.C.); (P.C.)
| | - Pietro Invernizzi
- Division of Gastroenterology, Fondazione IRCCS San Gerardo dei Tintori, University of Milano-Bicocca School of Medicine, 20900 Monza, Italy; (C.G.)
| | - Sara Massironi
- Division of Gastroenterology, Fondazione IRCCS San Gerardo dei Tintori, University of Milano-Bicocca School of Medicine, 20900 Monza, Italy; (C.G.)
- Division of Gastroenterology, Center for Autoimmune Liver Diseases, Department of Medicine and Surgery, University of Milano-Bicocca, 20900 Monza, Italy
- European Reference Network on Hepatological Diseases (ERN RARE-LIVER), San Gerardo Hospital, ASST Monza, 20900 Monza, Italy
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Funatsu N, Hara K, Takagi M, Onodera A, Ueno K, Endo K, Cho H. Robotically assisted total gastrectomy for lymphadenopathy after long-term follow-up for multiple type 1 gastric neuroendocrine tumor (NET): a case report. Surg Case Rep 2023; 9:142. [PMID: 37556088 PMCID: PMC10412512 DOI: 10.1186/s40792-023-01725-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/28/2023] [Accepted: 08/01/2023] [Indexed: 08/10/2023] Open
Abstract
BACKGROUND Type 1 gastric neuroendrine tumor (NET) is usually associated with chronic atrophic gastritis and forms multiple lesions. While most cases of type 1 gastric NET are generally slowly growing, some develop regional lymph node metastases even after long-term dormancy. CASE PRESENTATION A 73-year-old male patient with a 32-year history of multiple gastric NET was being followed-up at the study center after endoscopic submucosal dissection (ESD) of a large gastric NET. A blood examination revealed high serum gastrin (> 3000 pg/ml). An endoscopic examination found atrophic mucosa and multiple, elevated lesions in the upper to lower stomach body. Computed tomography (CT) revealed regional lymphadenopathy in the greater omentum along the gastroepiploic artery. Robotically assisted total gastrectomy was performed with D2 lymphadenectomy and Roux-en-Y reconstruction. Pathological analysis revealed a large number of gastric NET (grade 1) with a maximum size of 4.5 mm invading the submucosal layer. A single lymph node metastasis was also detected pathologically at station #4d. The postoperative course was uneventful, and serum gastrin normalized postoperatively. At postoperative year 3, the patient has been doing well without any recurrences. CONCLUSIONS The present case of multiple gastric NET with a single regional lymph node metastasis at year 32 of follow-up was successfully treated with a robotically assisted total gastrectomy.
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Affiliation(s)
- Nozomi Funatsu
- Department of Gastric Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, 3-18-22 Honkomagome, Bunkyo-Ku, Tokyo, 113-8677, Japan
| | - Kentaro Hara
- Department of Gastric Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, 3-18-22 Honkomagome, Bunkyo-Ku, Tokyo, 113-8677, Japan.
| | - Maki Takagi
- Department of Gastric Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, 3-18-22 Honkomagome, Bunkyo-Ku, Tokyo, 113-8677, Japan
| | - Atsushi Onodera
- Department of Gastric Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, 3-18-22 Honkomagome, Bunkyo-Ku, Tokyo, 113-8677, Japan
| | - Kohdai Ueno
- Department of Gastric Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, 3-18-22 Honkomagome, Bunkyo-Ku, Tokyo, 113-8677, Japan
| | - Kazuya Endo
- Department of Gastric Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, 3-18-22 Honkomagome, Bunkyo-Ku, Tokyo, 113-8677, Japan
| | - Haruhiko Cho
- Department of Gastric Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital, 3-18-22 Honkomagome, Bunkyo-Ku, Tokyo, 113-8677, Japan
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10
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Panzuto F, Ramage J, Pritchard DM, van Velthuysen MLF, Schrader J, Begum N, Sundin A, Falconi M, O'Toole D. European Neuroendocrine Tumor Society (ENETS) 2023 guidance paper for gastroduodenal neuroendocrine tumours (NETs) G1-G3. J Neuroendocrinol 2023; 35:e13306. [PMID: 37401795 DOI: 10.1111/jne.13306] [Citation(s) in RCA: 62] [Impact Index Per Article: 31.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/27/2023] [Revised: 05/09/2023] [Accepted: 05/10/2023] [Indexed: 07/05/2023]
Abstract
The aim of the present guidance paper was to update the previous ENETS guidelines on well-differentiated gastric and duodenal neuroendocrine tumours (NETs), providing practical guidance for specialists in the diagnosis and management of gastroduodenal NETs. Type II gastric NETs, neuroendocrine carcinomas (NECs), and functioning duodenal NETs are not covered, since they will be discussed in other ENETS guidance papers.
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Affiliation(s)
- Francesco Panzuto
- Department of Medical-Surgical Sciences and Translational Medicine, Digestive Disease Unit, Sant'Andrea University Hospital, ENETS Center of Excellence, Sapienza University of Rome, Rome, Italy
| | - John Ramage
- Department of Gastroenterology, Hampshire Hospitals and ENETS Center, Kings Health Partners London, London, United Kingdom
| | - D Mark Pritchard
- Department of Molecular and Clinical Cancer Medicine, University of Liverpool, Liverpool, UK
| | | | - Joerg Schrader
- Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
| | - Nehara Begum
- Department for General-, Visceral-, Thoracic- and Endocrine Surgery, Johannes-Wesling-Klinikum Minden, University Hospital of the Ruhr-University Bochum, Bochum, Germany
| | - Anders Sundin
- Department of Surgical Sciences, Radiology & Molecular Imaging, Uppsala University, Uppsala, Sweden
| | - Massimo Falconi
- Pancreas Translational and Clinical Research Center, Pancreatic Surgery Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy
| | - Dermot O'Toole
- National Centre for Neuroendocrine Tumours, ENETS Centre of Excellence, St. Vincent's University Hospital, Dublin, Ireland
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11
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Exarchou K, Hu H, Stephens NA, Moore AR, Kelly M, Lamarca A, Mansoor W, Hubner R, McNamara MG, Smart H, Howes NR, Valle JW, Pritchard DM. Endoscopic surveillance alone is feasible and safe in type I gastric neuroendocrine neoplasms less than 10 mm in diameter. Endocrine 2022; 78:186-196. [PMID: 35895180 PMCID: PMC9474380 DOI: 10.1007/s12020-022-03143-3] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/05/2022] [Accepted: 07/09/2022] [Indexed: 11/28/2022]
Abstract
PURPOSE Type I gastric neuroendocrine neoplasms (g-NENs) have a low risk of metastasis and a generally favourable prognosis. Patients with small type I g-NENs (≤10 mm) frequently require no treatment, whereas those with larger polyps usually undergo resection. We evaluated the safety and outcomes of endoscopic surveillance after no initial treatment in selected patients with type I g-NENs. METHODS Retrospective analysis of type I g-NEN patients across two European Neuroendocrine Tumour Society Centers of Excellence 2003-2019. RESULTS Following initial assessment, 87 of 115 patients with type I g-NEN (75 with polyps ≤10 mm) received no initial treatment and underwent endoscopic surveillance. 79/87 (91%) demonstrated no clinically meaningful change in tumour size or grade over a median 62 month follow up. Only two patients developed NEN progression that required a change in management and two other patients developed gastric adenocarcinoma/high grade dysplasia; all four initially had ≥11 mm g-NENs. CONCLUSIONS Patients with ≤10 mm type I g-NENs were unlikely to develop clinically significant tumour progression and in most cases, resection was not needed. The endoscopic surveillance interval could therefore potentially be safely increased to every 2-3 years in such patients. However, lifelong surveillance is still advocated due to the additional risk of developing gastric adenocarcinoma.
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Affiliation(s)
- Klaire Exarchou
- Department of Molecular and Clinical Cancer Medicine, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, UK
- Department of Upper Gastrointestinal Surgery, Liverpool University Hospitals NHS Foundation Trust, Liverpool, UK
| | - Haiyi Hu
- Department of Molecular and Clinical Cancer Medicine, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, UK
- Department of Gastroenterology, Beijing Friendship Hospital, Capital Medical University; National Clinical Research Center for Digestive Diseases, Beijing, China
| | - Nathan A Stephens
- Department of Upper Gastrointestinal Surgery, Liverpool University Hospitals NHS Foundation Trust, Liverpool, UK
| | - Andrew R Moore
- Department of Gastroenterology, Liverpool University Hospitals NHS Foundation Trust, Liverpool, UK
| | - Mark Kelly
- Department of Gastroenterology, Manchester University NHS Foundation Trust, Manchester, UK
| | - Angela Lamarca
- Department of Oncology, The Christie NHS Foundation Trust, Manchester, UK
- Division of Cancer Sciences, University of Manchester, Oxford Rd, Manchester, UK
| | - Wasat Mansoor
- Department of Oncology, The Christie NHS Foundation Trust, Manchester, UK
- Division of Cancer Sciences, University of Manchester, Oxford Rd, Manchester, UK
| | - Richard Hubner
- Department of Oncology, The Christie NHS Foundation Trust, Manchester, UK
- Division of Cancer Sciences, University of Manchester, Oxford Rd, Manchester, UK
| | - Mairéad G McNamara
- Department of Oncology, The Christie NHS Foundation Trust, Manchester, UK
- Division of Cancer Sciences, University of Manchester, Oxford Rd, Manchester, UK
| | - Howard Smart
- Department of Gastroenterology, Liverpool University Hospitals NHS Foundation Trust, Liverpool, UK
| | - Nathan R Howes
- Department of Upper Gastrointestinal Surgery, Liverpool University Hospitals NHS Foundation Trust, Liverpool, UK
| | - Juan W Valle
- Department of Oncology, The Christie NHS Foundation Trust, Manchester, UK
- Division of Cancer Sciences, University of Manchester, Oxford Rd, Manchester, UK
| | - D Mark Pritchard
- Department of Molecular and Clinical Cancer Medicine, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, UK.
- Department of Gastroenterology, Liverpool University Hospitals NHS Foundation Trust, Liverpool, UK.
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12
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Esposito G, Cazzato M, Rinzivillo M, Pilozzi E, Lahner E, Annibale B, Panzuto F. Management of type-I gastric neuroendocrine neoplasms: A 10-years prospective single centre study. Dig Liver Dis 2022; 54:890-895. [PMID: 34903498 DOI: 10.1016/j.dld.2021.11.012] [Citation(s) in RCA: 18] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/16/2021] [Revised: 11/12/2021] [Accepted: 11/15/2021] [Indexed: 02/08/2023]
Abstract
BACKGROUND This study aimed to evaluate the outcome of patients with type 1 gastric neuroendocrine neoplasia (T1gNENs) treated with different endoscopic approaches. METHODS Patients were managed with endoscopic surveillance at regular intervals. Resection was performed by forceps or cold snare in tumours < 10 mm, otherwise mucosal resection (EMR) or submucosal dissection (ESD) were done. RESULTS 127 T1gNENs, detected in 80 patients, were included. 87.4% of them were <5 mm, whereas 8.7% were 6-10 mm, 3.1% were 11-20 mm, and 0.8% was >20 mm. Ki67 <3%% was found in 85.8% tumours, whereas it was 3%-20% in the remaining 14.2% lesions. Noninterventional management (surveillance without radical resection) was performed in 15 patients (18.7%) with T1gNENs <5 mm. None of them underwent disease progression during follow-up. among the 65 patients treated by radical endoscopic resection, 37 patients (56.9%) had disease recurrence. 48.5% T1gNENs were removed by forceps, 16.8% by cold snare, 31.7% by EMR and 3% by ESD. The recurrence rate was similar among the different endoscopic techniques used. CONCLUSIONS The management of T1gNENs may be planned based on tumour size. T1gNENs < 5 mm for which the initial removal is not radical could be followed up by noninterventional endoscopic surveillance.
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Affiliation(s)
- Gianluca Esposito
- Digestive Disease Unit, Sant'Andrea University Hospital, Sapienza University of Rome, ENETS Center of Excellence, Rome, Italy; Department of Medical-Surgical Sciences and Translational Medicine, Sapienza University of Rome, Rome, Italy
| | - Maria Cazzato
- Digestive Disease Unit, Sant'Andrea University Hospital, Sapienza University of Rome, ENETS Center of Excellence, Rome, Italy; Department of Medical-Surgical Sciences and Translational Medicine, Sapienza University of Rome, Rome, Italy
| | - Maria Rinzivillo
- Digestive Disease Unit, Sant'Andrea University Hospital, Sapienza University of Rome, ENETS Center of Excellence, Rome, Italy
| | - Emanuela Pilozzi
- Department of Clinical and Molecular Medicine, Sant'Andrea University Hospital, Sapienza University of Rome, ENETS Center of Excellence, Rome, Italy
| | - Edith Lahner
- Digestive Disease Unit, Sant'Andrea University Hospital, Sapienza University of Rome, ENETS Center of Excellence, Rome, Italy; Department of Medical-Surgical Sciences and Translational Medicine, Sapienza University of Rome, Rome, Italy
| | - Bruno Annibale
- Digestive Disease Unit, Sant'Andrea University Hospital, Sapienza University of Rome, ENETS Center of Excellence, Rome, Italy; Department of Medical-Surgical Sciences and Translational Medicine, Sapienza University of Rome, Rome, Italy
| | - Francesco Panzuto
- Digestive Disease Unit, Sant'Andrea University Hospital, Sapienza University of Rome, ENETS Center of Excellence, Rome, Italy.
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Abstract
Purpose of Review Gastric neuroendocrine neoplasms (g-NENs) are a rare type of stomach cancer. The three main subtypes have different pathogeneses, biological behaviours and clinical characteristics, so they require different management strategies. This article will provide an overview of g-NENs and highlight recent advances in the field. Recent Findings Molecular profiling has revealed differences between indolent and aggressive g-NENs, as well as a new somatic mutation responsible for some familial type I g-NENs. Novel biomarkers have been developed which will hopefully improve diagnosis, treatment, risk stratification and follow-up. Patient treatment is also changing, as evidence supports the use of less aggressive options (e.g. endoscopic surveillance or resection) in some patients with more indolent tumours. Summary g-NEN heterogeneity poses challenges in understanding and managing this rare disease. More basic science research is needed to investigate molecular pathogenesis, and future larger clinical studies will hopefully also further improve treatment and patient outcomes.
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Yozgat A, Kekilli M, Altay M. Time to give up traditional methods for the management of gastrointestinal neuroendocrine tumours. World J Clin Cases 2021; 9:8627-8646. [PMID: 34734042 PMCID: PMC8546836 DOI: 10.12998/wjcc.v9.i29.8627] [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: 02/20/2021] [Revised: 05/19/2021] [Accepted: 08/24/2021] [Indexed: 02/06/2023] Open
Abstract
Neuroendocrine tumors (NETs) are a rare and heterogeneous disease group and constitute 0.5% of all malignancies. The annual incidence of NETs is increasing worldwide. The reason for the increase in the incidence of NETs is the detection of benign lesions, incidental detection due to the highest use of endoscopic and imaging procedures, and higher recognition rates of pathologists. There have been exciting developments regarding NET biology in recent years. Among these, first of all, somatostatin receptors and downstream pathways in neuroendocrine cells have been found to be important regulatory mechanisms for protein synthesis, hormone secretion, and proliferation. Subsequently, activation of the mammalian target of rapamycin pathway was found to be an important mechanism in angiogenesis and tumor survival and cell metabolism. Finally, the importance of proangiogenic factors (platelet-derived growth factor, vascular endothelial growth factor, fibroblastic growth factor, angiopoietin, and semaphorins) in the progression of NET has been determined. Using the combination of biomarkers and imaging methods allows early evaluation of the appropriateness of treatment and response to treatment.
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Affiliation(s)
- Ahmet Yozgat
- Department of Gastroenterology, Ufuk University, Ankara, 06510, Turkey
| | - Murat Kekilli
- Department of Gastroenterology, Gazi University, Ankara 06560, Turkey
| | - Mustafa Altay
- Department of Endocrinology and Metabolism, University of Health Sciences Turkey, Keçiören Health Administration and Research Center, Ankara 06190, Turkey
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15
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Panzuto F, Magi L, Esposito G, Rinzivillo M, Annibale B. Comparison of Endoscopic Techniques in the Management of Type I Gastric Neuroendocrine Neoplasia: A Systematic Review. Gastroenterol Res Pract 2021; 2021:1-6. [PMID: 33859684 PMCID: PMC8026302 DOI: 10.1155/2021/6679397] [Citation(s) in RCA: 22] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/29/2020] [Revised: 03/09/2021] [Accepted: 03/17/2021] [Indexed: 02/08/2023] Open
Abstract
Background. Endoscopic resection is considered the treatment of choice for type I gastric neuroendocrine neoplasia (gNEN) given its indolent behaviour; however, the favoured endoscopic technique to remove these tumours is not well established. Aims. This systematic review is aimed at investigating the best endoscopic management for type I gNEN. Methods. PubMed Central/Medline and Scopus were systematically searched for records up to August 31, 2020. Results. After screening the 675 retrieved records, 6 studies were selected for the final analysis. The main endoscopic resection techniques described were endoscopic mucosal resection (EMR) and endoscopic submucosal dissection (ESD). Overall, 112 gNENs were removed by EMR and 77 by ESD. Both techniques showed similar results for complete and en bloc resection (97.4% and 98.7%; 92.3% and 96.3% with ESD and EMR, respectively). ESD was associated with a higher rate of complications than EMR (11.7% vs. 5.4%), but this difference was not statistically significant (
). The rates of recurrence during follow-up were 18.2% and 11.5% for EMR and ESD, respectively. Conclusions. To date, there are no sufficient data showing superiority of a given endoscopic technique over others. Both ESD and EMR seem to be effective in the management of type I gNEN, with a relatively low rate of recurrence.
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Affiliation(s)
- Francesco Panzuto
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence, Rome, Italy
| | - Ludovica Magi
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence, Rome, Italy
- Department of Translational and Precision Medicine, Sapienza University of Rome, Italy
| | - Gianluca Esposito
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence, Rome, Italy
- Department of Medical-Surgical Sciences and Translational Medicine, Sapienza University of Rome, Italy
| | - Maria Rinzivillo
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence, Rome, Italy
| | - Bruno Annibale
- Digestive Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence, Rome, Italy
- Department of Medical-Surgical Sciences and Translational Medicine, Sapienza University of Rome, Italy
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