Skip to main content
Top
Published in: BMC Surgery 1/2023

Open Access 01-12-2023 | Metastasis | Research

Clinicopathological characteristics of rectal multiple neuroendocrine neoplasms and literature review

Authors: Xiuli Zheng, Mingli Wu, Shengmian Li, Limian Er, Huiyan Deng, Shuo Guo, Zhihuan Liu

Published in: BMC Surgery | Issue 1/2023

Login to get access

Abstract

Background

There are only a few epidemiological reports available for reference. The clinicopathological features are not clear, so there is no consensus on treating rectal multiple neuroendocrine neoplasms. This study aims to summarize the clinicopathological characteristics and preliminarily discuss the clinical diagnosis and treatment of rectal multiple neuroendocrine neoplasms.

Methods

This study retrospectively analyzed rectal neuroendocrine neoplasm patients diagnosed and treated at the Fourth Hospital of Hebei Medical University from February 2007 to May 2021. The clinicopathological characteristics of rectal multiple neuroendocrine neoplasms were summarized and analyzed in combination with 14 studies on rectal multiple neuroendocrine neoplasms.

Results

The incidence of RM-NENs accounted for 3.8% of all R-NENs in this study. The number of tumors varied to some extent, the size of tumors was basically no more than 10 mm, and there were more G1 grade tumors. In the analysis of 46 cases with known lymph node metastasis, the difference in lymph node metastasis rate between the number of tumors < 8 and ≥ 8 was statistically significant (p = 0.002).

Conclusions

The incidence of rectal multiple neuroendocrine neoplasms accounted for 3.8% of all rectal neuroendocrine neoplasms. For rectal multiple neuroendocrine neoplasms, the lymph node metastasis rate was higher when the number of tumors was ≥ 8. The influence of the number of tumors on lymph node metastasis should be considered in the selection of treatment.
Literature
1.
go back to reference Hu P, Bai JA, Liu M, Xue J, Chen T, Li R, Kuai X, Zhao H, Li X, Tian Y, et al. Trends of incidence and prognosis of gastric neuroendocrine neoplasms: a study based on seer and our multicenter research. Gastric Cancer. 2020;23(4):591–9.PubMedPubMedCentralCrossRef Hu P, Bai JA, Liu M, Xue J, Chen T, Li R, Kuai X, Zhao H, Li X, Tian Y, et al. Trends of incidence and prognosis of gastric neuroendocrine neoplasms: a study based on seer and our multicenter research. Gastric Cancer. 2020;23(4):591–9.PubMedPubMedCentralCrossRef
2.
go back to reference Konishi T, Watanabe T, Muto T, Kotake K, Nagawa H. Site distribution of gastrointestinal carcinoids differs between races. Gut. 2006;55(7):1051–2.PubMedPubMedCentral Konishi T, Watanabe T, Muto T, Kotake K, Nagawa H. Site distribution of gastrointestinal carcinoids differs between races. Gut. 2006;55(7):1051–2.PubMedPubMedCentral
3.
go back to reference Fan JH, Zhang YQ, Shi SS, Chen YJ, Yuan XH, Jiang LM, Wang SM, Ma L, He YT, Feng CY, et al. A nation-wide retrospective epidemiological study of gastroenteropancreatic neuroendocrine neoplasms in china. Oncotarget. 2017;8(42):71699–708.PubMedPubMedCentralCrossRef Fan JH, Zhang YQ, Shi SS, Chen YJ, Yuan XH, Jiang LM, Wang SM, Ma L, He YT, Feng CY, et al. A nation-wide retrospective epidemiological study of gastroenteropancreatic neuroendocrine neoplasms in china. Oncotarget. 2017;8(42):71699–708.PubMedPubMedCentralCrossRef
4.
go back to reference Jetmore AB, Ray JE, Gathright JJ, Mcmullen KM, Hicks TC, Timmcke AE. Rectal carcinoids: the most frequent carcinoid tumor. Dis Colon Rectum. 1992;35(8):717–25.PubMedCrossRef Jetmore AB, Ray JE, Gathright JJ, Mcmullen KM, Hicks TC, Timmcke AE. Rectal carcinoids: the most frequent carcinoid tumor. Dis Colon Rectum. 1992;35(8):717–25.PubMedCrossRef
5.
go back to reference Modlin IM, Kidd M, Latich I, Zikusoka MN, Shapiro MD. Current status of gastrointestinal carcinoids. Gastroenterology. 2005;128(6):1717–51.PubMedCrossRef Modlin IM, Kidd M, Latich I, Zikusoka MN, Shapiro MD. Current status of gastrointestinal carcinoids. Gastroenterology. 2005;128(6):1717–51.PubMedCrossRef
6.
go back to reference Ramage JK, De Herder WW, Delle Fave G, Ferolla P, Ferone D, Ito T, Ruszniewski P, Sundin A, Weber W, Zheng-Pei Z, et al. Enets consensus guidelines update for colorectal neuroendocrine neoplasms. Neuroendocrinology. 2016;103(2):139–43.PubMedCrossRef Ramage JK, De Herder WW, Delle Fave G, Ferolla P, Ferone D, Ito T, Ruszniewski P, Sundin A, Weber W, Zheng-Pei Z, et al. Enets consensus guidelines update for colorectal neuroendocrine neoplasms. Neuroendocrinology. 2016;103(2):139–43.PubMedCrossRef
7.
go back to reference Sasou S, Suto T, Satoh T, Tamura G, Kudara N. Multiple carcinoid tumors of the rectum: report of two cases suggesting the origin of carcinoid tumors. Pathol Int. 2012;62(10):699–703.PubMedCrossRef Sasou S, Suto T, Satoh T, Tamura G, Kudara N. Multiple carcinoid tumors of the rectum: report of two cases suggesting the origin of carcinoid tumors. Pathol Int. 2012;62(10):699–703.PubMedCrossRef
8.
go back to reference Maruyama M, Fukayama M, Koike M. A case of multiple carcinoid tumors of the rectum with extraglandular endocrine cell proliferation. Cancer. 1988;61(1):131–6.PubMedCrossRef Maruyama M, Fukayama M, Koike M. A case of multiple carcinoid tumors of the rectum with extraglandular endocrine cell proliferation. Cancer. 1988;61(1):131–6.PubMedCrossRef
9.
go back to reference Kanter M, Lechago J. Multiple malignant rectal carcinoid tumors with immunocytochemical demonstration of multiple hormonal substances. Cancer. 1987;60(8):1782–6.PubMedCrossRef Kanter M, Lechago J. Multiple malignant rectal carcinoid tumors with immunocytochemical demonstration of multiple hormonal substances. Cancer. 1987;60(8):1782–6.PubMedCrossRef
10.
go back to reference Sung Sil Park NHJL. Multiple small rectal neuroendocrine tumors with numerous micronests. J Dig Dis. 2018;19(9):572–5.CrossRef Sung Sil Park NHJL. Multiple small rectal neuroendocrine tumors with numerous micronests. J Dig Dis. 2018;19(9):572–5.CrossRef
11.
go back to reference Winburn GB. Multiple rectal carcinoids: a case report. In: 1998–01–01. Atlanta: Southeastern Surgical Congress; 1998. p. 1200–3. Winburn GB. Multiple rectal carcinoids: a case report. In: 1998–01–01. Atlanta: Southeastern Surgical Congress; 1998. p. 1200–3.
12.
go back to reference Nishikawa Y, Chino A, Ide D, Saito S, Igarashi M, Takamatsu M, Fujisaki J, Igarashi Y. Clinicopathological characteristics and frequency of multiple rectal neuroendocrine tumors: a single-center retrospective study. Int J Colorectal Dis. 2019;34(11):1887–94.PubMedCrossRef Nishikawa Y, Chino A, Ide D, Saito S, Igarashi M, Takamatsu M, Fujisaki J, Igarashi Y. Clinicopathological characteristics and frequency of multiple rectal neuroendocrine tumors: a single-center retrospective study. Int J Colorectal Dis. 2019;34(11):1887–94.PubMedCrossRef
13.
go back to reference Toriyama K, Yamamura T, Nakamura M, Maeda K, Sawada T, Mizutani Y, Ishikawa E, Furukawa K, Ishikawa T, Ohno E, et al. An evaluation of resectability among endoscopic treatment methods for rectal neuroendocrine tumors <10 mm. Arab J Gastroenterol. 2021;22(2):104–10.PubMedCrossRef Toriyama K, Yamamura T, Nakamura M, Maeda K, Sawada T, Mizutani Y, Ishikawa E, Furukawa K, Ishikawa T, Ohno E, et al. An evaluation of resectability among endoscopic treatment methods for rectal neuroendocrine tumors <10 mm. Arab J Gastroenterol. 2021;22(2):104–10.PubMedCrossRef
14.
go back to reference Zhu H, Zhao S, Zhang C, Ji K, Wu W, Yin L, Yan H, Zhou J, Tang R, Miao L. Endoscopic and surgical treatment of t1n0m0 colorectal neuroendocrine tumors: a population-based comparative study. Surg Endosc. 2022;36(4):2488–98.PubMedCrossRef Zhu H, Zhao S, Zhang C, Ji K, Wu W, Yin L, Yan H, Zhou J, Tang R, Miao L. Endoscopic and surgical treatment of t1n0m0 colorectal neuroendocrine tumors: a population-based comparative study. Surg Endosc. 2022;36(4):2488–98.PubMedCrossRef
15.
go back to reference Haraguchi M, Kinoshita H, Koori M, Tsuneoka N, Kosaka T, Ito Y, Furui J, Kanematsu T. Multiple rectal carcinoids with diffuse ganglioneuromatosis. World J Surg Oncol. 2007;5:19.PubMedPubMedCentralCrossRef Haraguchi M, Kinoshita H, Koori M, Tsuneoka N, Kosaka T, Ito Y, Furui J, Kanematsu T. Multiple rectal carcinoids with diffuse ganglioneuromatosis. World J Surg Oncol. 2007;5:19.PubMedPubMedCentralCrossRef
16.
go back to reference Ghassemi KA, Ou H, Roth BE. Multiple rectal carcinoids in a patient with neurofibromatosis. Gastrointest Endosc. 2010;71(1):216–8.PubMedCrossRef Ghassemi KA, Ou H, Roth BE. Multiple rectal carcinoids in a patient with neurofibromatosis. Gastrointest Endosc. 2010;71(1):216–8.PubMedCrossRef
17.
go back to reference Park CS, Lee SH, Kim SB, Kim KO, Jang BI. Multiple rectal neuroendocrine tumors: report of five cases. Korean J Gastroenterol. 2014;64(2):103.PubMedCrossRef Park CS, Lee SH, Kim SB, Kim KO, Jang BI. Multiple rectal neuroendocrine tumors: report of five cases. Korean J Gastroenterol. 2014;64(2):103.PubMedCrossRef
18.
go back to reference Zhou J, Lin G, Zhao D, Zhong G, Qiu H. Resection of multiple rectal carcinoids with transanal endoscopic microsurgery: case report. World J Gastroenterol. 2015;21(7):2220–4.PubMedPubMedCentralCrossRef Zhou J, Lin G, Zhao D, Zhong G, Qiu H. Resection of multiple rectal carcinoids with transanal endoscopic microsurgery: case report. World J Gastroenterol. 2015;21(7):2220–4.PubMedPubMedCentralCrossRef
19.
go back to reference Hua B, Fandong M, Xun Y. Multiple carcinoid of rectum: a case report and literature review. Zhong Guo Yi Yao Dao Kan. 2016;18(12):1282–3. Hua B, Fandong M, Xun Y. Multiple carcinoid of rectum: a case report and literature review. Zhong Guo Yi Yao Dao Kan. 2016;18(12):1282–3.
20.
go back to reference Doi M, Ikawa O, Taniguchi H, Kawamura T, Katsura K. Multiple rectal carcinoid tumors in monozygotic twins. Clin J Gastroenterol. 2016;9(4):215–21.PubMedCrossRef Doi M, Ikawa O, Taniguchi H, Kawamura T, Katsura K. Multiple rectal carcinoid tumors in monozygotic twins. Clin J Gastroenterol. 2016;9(4):215–21.PubMedCrossRef
21.
go back to reference Xie R, Fu K, Chen S, Tuo B, Wu H. Neurofibromatosis type 1-associated multiple rectal neuroendocrine tumors: a case report and review of the literature. World J Gastroenterol. 2018;24(33):3806–12.PubMedPubMedCentralCrossRef Xie R, Fu K, Chen S, Tuo B, Wu H. Neurofibromatosis type 1-associated multiple rectal neuroendocrine tumors: a case report and review of the literature. World J Gastroenterol. 2018;24(33):3806–12.PubMedPubMedCentralCrossRef
22.
go back to reference Kato M, Yonemura Y, Sugiyama K, Hashimoto T, Shima Y, Miyazaki I, Sugiura H, Kurumaya H, Hoso M, Yao T. Multiple rectal carcinoids–with special reference to the histogenesis of these lesions. Gan No Rinsho. 1986;32(14):1894.PubMed Kato M, Yonemura Y, Sugiyama K, Hashimoto T, Shima Y, Miyazaki I, Sugiura H, Kurumaya H, Hoso M, Yao T. Multiple rectal carcinoids–with special reference to the histogenesis of these lesions. Gan No Rinsho. 1986;32(14):1894.PubMed
23.
go back to reference Okamoto Y, Fujii M, Tateiwa S, Sakai T, Ochi F, Sugano M, Oshiro K, Masai K, Okabayashi Y. Treatment of multiple rectal carcinoids by endoscopic mucosal resection using a device for esophageal variceal ligation. Endoscopy. 2004;36(5):469–70.PubMedCrossRef Okamoto Y, Fujii M, Tateiwa S, Sakai T, Ochi F, Sugano M, Oshiro K, Masai K, Okabayashi Y. Treatment of multiple rectal carcinoids by endoscopic mucosal resection using a device for esophageal variceal ligation. Endoscopy. 2004;36(5):469–70.PubMedCrossRef
24.
go back to reference Ning L, Chen H, Kunnimalaiyaan M. Focal adhesion kinase, a downstream mediator of raf-1 signaling, suppresses cellular adhesion, migration, and neuroendocrine markers in bon carcinoid cells. Mol Cancer Res. 2010;8(5):775–82.PubMedPubMedCentralCrossRef Ning L, Chen H, Kunnimalaiyaan M. Focal adhesion kinase, a downstream mediator of raf-1 signaling, suppresses cellular adhesion, migration, and neuroendocrine markers in bon carcinoid cells. Mol Cancer Res. 2010;8(5):775–82.PubMedPubMedCentralCrossRef
25.
go back to reference Wong M, Larson BK, Dhall D. Neuroendocrine proliferations in inflammatory bowel disease: differentiating neuroendocrine tumours from neuroendocrine cell micronests. Histopathology. 2019;74(3):415–23.PubMedCrossRef Wong M, Larson BK, Dhall D. Neuroendocrine proliferations in inflammatory bowel disease: differentiating neuroendocrine tumours from neuroendocrine cell micronests. Histopathology. 2019;74(3):415–23.PubMedCrossRef
26.
go back to reference Hiripi E, Bermejo JL, Sundquist J, Hemminki K. Familial gastrointestinal carcinoid tumours and associated cancers. Ann Oncol. 2009;20(5):950–4.PubMedCrossRef Hiripi E, Bermejo JL, Sundquist J, Hemminki K. Familial gastrointestinal carcinoid tumours and associated cancers. Ann Oncol. 2009;20(5):950–4.PubMedCrossRef
27.
go back to reference Caplin M, Sundin A, Nillson O, Baum RP, Klose KJ, Kelestimur F, Plöckinger U, Papotti M, Salazar R, Pascher A. Enets consensus guidelines for the management of patients with digestive neuroendocrine neoplasms: colorectal neuroendocrine neoplasms. Neuroendocrinology. 2012;95(2):88–97.PubMedCrossRef Caplin M, Sundin A, Nillson O, Baum RP, Klose KJ, Kelestimur F, Plöckinger U, Papotti M, Salazar R, Pascher A. Enets consensus guidelines for the management of patients with digestive neuroendocrine neoplasms: colorectal neuroendocrine neoplasms. Neuroendocrinology. 2012;95(2):88–97.PubMedCrossRef
28.
go back to reference Konishi T, Watanabe T, Kishimoto J, Kotake K, Muto T, Nagawa H. Prognosis and risk factors of metastasis in colorectal carcinoids: results of a nationwide registry over 15 years. Gut. 2007;56(6):863–8.PubMedPubMedCentralCrossRef Konishi T, Watanabe T, Kishimoto J, Kotake K, Muto T, Nagawa H. Prognosis and risk factors of metastasis in colorectal carcinoids: results of a nationwide registry over 15 years. Gut. 2007;56(6):863–8.PubMedPubMedCentralCrossRef
29.
go back to reference Lee J, Park YE, Choi JH, Heo NY, Park J, Park SH, et al. Comparison between cap-assisted and ligation-assisted endoscopic mucosal resection for rectal neuroendocrine tumors. Ann Gastroenterol. 2020;33(4):385–90. Lee J, Park YE, Choi JH, Heo NY, Park J, Park SH, et al. Comparison between cap-assisted and ligation-assisted endoscopic mucosal resection for rectal neuroendocrine tumors. Ann Gastroenterol. 2020;33(4):385–90.
31.
go back to reference Park SJ. Tips and tricks for better endoscopic treatment of colorectal tumors: usefulness of cap and band in colorectal endoscopic mucosal resection. Clin Endosc. 2013;46(5):492.PubMedPubMedCentralCrossRef Park SJ. Tips and tricks for better endoscopic treatment of colorectal tumors: usefulness of cap and band in colorectal endoscopic mucosal resection. Clin Endosc. 2013;46(5):492.PubMedPubMedCentralCrossRef
32.
go back to reference Park SS, Kim BC, Lee DE, Han KS, Kim B, Hong CW, Sohn DK. Comparison of endoscopic submucosal dissection and transanal endoscopic microsurgery for t1 rectal neuroendocrine tumors: a propensity score-matched study. Gastrointest Endosc. 2021;94(2):408-415.e2.PubMedCrossRef Park SS, Kim BC, Lee DE, Han KS, Kim B, Hong CW, Sohn DK. Comparison of endoscopic submucosal dissection and transanal endoscopic microsurgery for t1 rectal neuroendocrine tumors: a propensity score-matched study. Gastrointest Endosc. 2021;94(2):408-415.e2.PubMedCrossRef
33.
go back to reference He L, Wen W, Ye L, Liao K, Hu B. Endoscopic mucosal resection with double band ligation for small rectal neuroendocrine tumors. Am J Gastroenterol. 2021;116(9):1827–8.PubMedCrossRef He L, Wen W, Ye L, Liao K, Hu B. Endoscopic mucosal resection with double band ligation for small rectal neuroendocrine tumors. Am J Gastroenterol. 2021;116(9):1827–8.PubMedCrossRef
34.
go back to reference Sun P, Zheng T, Hu C, Gao T, Ding X. Comparison of endoscopic therapies for rectal neuroendocrine tumors: endoscopic submucosal dissection with myectomy versus endoscopic submucosal dissection. Surg Endosc. 2021;35(11):6374–8.PubMedCrossRef Sun P, Zheng T, Hu C, Gao T, Ding X. Comparison of endoscopic therapies for rectal neuroendocrine tumors: endoscopic submucosal dissection with myectomy versus endoscopic submucosal dissection. Surg Endosc. 2021;35(11):6374–8.PubMedCrossRef
35.
go back to reference Wang X, Chai N, Linghu E, Li H, Zhai Y, Feng X, Zhang W, Zou J, Li L, Xiang J. Efficacy and safety of hybrid endoscopic submucosal dissection compared with endoscopic submucosal dissection for rectal neuroendocrine tumors and risk factors associated with incomplete endoscopic resection. Ann Transl Med. 2020;8(6):368–368.PubMedPubMedCentralCrossRef Wang X, Chai N, Linghu E, Li H, Zhai Y, Feng X, Zhang W, Zou J, Li L, Xiang J. Efficacy and safety of hybrid endoscopic submucosal dissection compared with endoscopic submucosal dissection for rectal neuroendocrine tumors and risk factors associated with incomplete endoscopic resection. Ann Transl Med. 2020;8(6):368–368.PubMedPubMedCentralCrossRef
36.
go back to reference Wang X, Chai N, Linghu E, Qiu S, Li L, Zou J, Xiang J, Li X. The outcomes of modified endoscopic mucosal resection and endoscopic submucosal dissection for the treatment of rectal neuroendocrine tumors and the value of endoscopic morphology classification in endoscopic resection. BMC Gastroenterol. 2020;20(1):1–2.CrossRef Wang X, Chai N, Linghu E, Qiu S, Li L, Zou J, Xiang J, Li X. The outcomes of modified endoscopic mucosal resection and endoscopic submucosal dissection for the treatment of rectal neuroendocrine tumors and the value of endoscopic morphology classification in endoscopic resection. BMC Gastroenterol. 2020;20(1):1–2.CrossRef
37.
go back to reference Ahmed Y, Othman M. Emr/esd: techniques, complications, and evidence. Curr Gastroenterol Rep. 2020;22(8):1–2.CrossRef Ahmed Y, Othman M. Emr/esd: techniques, complications, and evidence. Curr Gastroenterol Rep. 2020;22(8):1–2.CrossRef
39.
go back to reference Zilli A, Arcidiacono PG, Conte D, Massironi S. Clinical impact of endoscopic ultrasonography on the management of neuroendocrine tumors: lights and shadows. Dig Liver Dis. 2018;50(1):6–14.PubMedCrossRef Zilli A, Arcidiacono PG, Conte D, Massironi S. Clinical impact of endoscopic ultrasonography on the management of neuroendocrine tumors: lights and shadows. Dig Liver Dis. 2018;50(1):6–14.PubMedCrossRef
40.
go back to reference Gu Q, Lin Y, Cen L, Xu M, Li H, Lin X, Lu C. Endoscopic ultrasonography is useful in the diagnosis and treatment of rectal neuroendocrine neoplasms: a case series. J Zhejiang Univ Sci B. 2019;20(10):861–4.PubMedPubMedCentralCrossRef Gu Q, Lin Y, Cen L, Xu M, Li H, Lin X, Lu C. Endoscopic ultrasonography is useful in the diagnosis and treatment of rectal neuroendocrine neoplasms: a case series. J Zhejiang Univ Sci B. 2019;20(10):861–4.PubMedPubMedCentralCrossRef
41.
go back to reference Burke AP, Thomas RM, Elsayed AM, Sobin LH. Carcinoids of the jejunum and ileum: an immunohistochemical and clinicopathologic study of 167 cases. Cancer. 1997;79(6):1086–93.PubMedCrossRef Burke AP, Thomas RM, Elsayed AM, Sobin LH. Carcinoids of the jejunum and ileum: an immunohistochemical and clinicopathologic study of 167 cases. Cancer. 1997;79(6):1086–93.PubMedCrossRef
42.
go back to reference Lundqvist M, Wilander E. A study of the histopathogenesis of carcinoid tumors of the small intestine and appendix. Cancer. 1987;60(2):201–6.PubMedCrossRef Lundqvist M, Wilander E. A study of the histopathogenesis of carcinoid tumors of the small intestine and appendix. Cancer. 1987;60(2):201–6.PubMedCrossRef
43.
go back to reference Iwai K, Yao T, Nakamura S, Matsumoto T, Nishiyama K, Iida M, Tsuneyoshi M. Multiple gastric carcinoids and endocrine cell micronests in type a gastritis: nuclear morphometric and immunohistochemical analysis. Oncol Rep. 2005;13(3):397.PubMed Iwai K, Yao T, Nakamura S, Matsumoto T, Nishiyama K, Iida M, Tsuneyoshi M. Multiple gastric carcinoids and endocrine cell micronests in type a gastritis: nuclear morphometric and immunohistochemical analysis. Oncol Rep. 2005;13(3):397.PubMed
44.
go back to reference Suzuki S, Kawakami H, Miike T, Yamamoto S, Abe H, Shimoda K, Ashizuka S, Inatsu H, Kubota Y, Ban T, et al. Single rectal neuroendocrine tumor associated with multiple endocrine cell micronests. Intern Med. 2020;59(5):619–23.PubMedCrossRef Suzuki S, Kawakami H, Miike T, Yamamoto S, Abe H, Shimoda K, Ashizuka S, Inatsu H, Kubota Y, Ban T, et al. Single rectal neuroendocrine tumor associated with multiple endocrine cell micronests. Intern Med. 2020;59(5):619–23.PubMedCrossRef
45.
go back to reference Mastracci L, Rindi G, Grillo F, Solcia E, Campora M, Fassan M, Parente P, Vanoli A, La Rosa S. Neuroendocrine neoplasms of the esophagus and stomach. Pathologica. 2021;113(1):5–11.PubMedPubMedCentralCrossRef Mastracci L, Rindi G, Grillo F, Solcia E, Campora M, Fassan M, Parente P, Vanoli A, La Rosa S. Neuroendocrine neoplasms of the esophagus and stomach. Pathologica. 2021;113(1):5–11.PubMedPubMedCentralCrossRef
46.
go back to reference Ishioka M, Hirasawa T, Kawachi H, Nakano K, Kunieda J, Yoshimizu S, Horiuchi Y, Ishiyama A, Yoshio T, Tsuchida T, et al. Enterochromaffin-like cell neuroendocrine tumor associated with parietal cell dysfunction. Gastrointest Endosc. 2019;90(5):841-845.e1.PubMedCrossRef Ishioka M, Hirasawa T, Kawachi H, Nakano K, Kunieda J, Yoshimizu S, Horiuchi Y, Ishiyama A, Yoshio T, Tsuchida T, et al. Enterochromaffin-like cell neuroendocrine tumor associated with parietal cell dysfunction. Gastrointest Endosc. 2019;90(5):841-845.e1.PubMedCrossRef
47.
go back to reference Tsolakis AV, Ragkousi A, Vujasinovic M, Kaltsas G, Daskalakis K. Gastric neuroendocrine neoplasms type 1: a systematic review and meta-analysis. World J Gastroenterol. 2019;25(35):5376–87.PubMedPubMedCentralCrossRef Tsolakis AV, Ragkousi A, Vujasinovic M, Kaltsas G, Daskalakis K. Gastric neuroendocrine neoplasms type 1: a systematic review and meta-analysis. World J Gastroenterol. 2019;25(35):5376–87.PubMedPubMedCentralCrossRef
48.
go back to reference Itsuno MWHIM. Multiple carcinoids and endocrine cell micronests in type a gastritis. Cancer. 1989;63(5):881–90.PubMedCrossRef Itsuno MWHIM. Multiple carcinoids and endocrine cell micronests in type a gastritis. Cancer. 1989;63(5):881–90.PubMedCrossRef
Metadata
Title
Clinicopathological characteristics of rectal multiple neuroendocrine neoplasms and literature review
Authors
Xiuli Zheng
Mingli Wu
Shengmian Li
Limian Er
Huiyan Deng
Shuo Guo
Zhihuan Liu
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Surgery / Issue 1/2023
Electronic ISSN: 1471-2482
DOI
https://doi.org/10.1186/s12893-023-02050-2

Other articles of this Issue 1/2023

BMC Surgery 1/2023 Go to the issue