Research progress of colorectal serrated adenocarcinoma of human

doi:10.3760/cma.j.issn.1007-1245.2022.13.007

Abstract

Abstract:

As a special clinical type of colorectal cancer, serrated adenocarcinoma (SAC) has attracted the interest of many researchers due to its special carcinogenesis pathway, poor detection, and poor treatment response and prognosis. The serrated pathway is characterized by BRAF mutation, microsatellite instability (MSI), and CpG island methylator phenotype (CIMP). Due to the special morphology, endoscopic characteristics, and occurrence site, it is easy to be missed during colonoscopy, and even easily ignored during pathological evaluation. When it is clinically diagnosed, the patients are often in the advanced stage, with poor prognosis and a low survival rate. This article reviews the epidemiology, risk factors, and clinical, pathological and molecular features of serrated colorectal adenocarcinoma.

Key words: Serrated colorectal adenocarcinoma, Epidemiology, Risk factors, Clinical features, Pathological features, Molecular features

摘要： 结直肠锯齿状腺癌（serrated adenocarcinoma，SAC）作为大肠癌的一种特殊临床类型，因其癌变途径的特殊性，检测以及较差的治疗反应和预后逐渐引起众多研究者的兴趣。其产生的途径主要为“锯齿状通路”途径，锯齿状通路途径以BRAF突变、微卫星体不稳定（microsatellite instability，MSI））和CpG岛的甲基化（CpG island methylator phenotype，CIMP）为特征。由于特殊的形态和内镜特征及特殊的发生部位，在结肠镜检查时很容易漏诊，甚至病理评估时也极易被忽视，临床确诊时往往已处于进展期，患者预后差，生存率低。本文针对锯齿状结直肠腺癌流行病学、危险因素、临床特征、病理学特征、分子特征等作一综述。

关键词: 锯齿状腺癌, 流行病学, 危险因素, 临床特征, 病理学特征, 分子特征

Wang Na, Jia Xingfang, Chu Linlin, Hao Jiahui, Liu Chengxia. Research progress of colorectal serrated adenocarcinoma of human [J]. International Medicine and Health Guidance News, 2022, 28(13): 1810-1814.

王娜　贾兴芳　储琳琳　郝佳慧　刘成霞. 人结直肠锯齿状腺癌的研究现状[J]. 国际医药卫生导报, 2022, 28(13): 1810-1814.

References

[1] Siegel RL, Miller KD, Jemal A, et al. Colorectal cancer statistics, 2020 [J]. CA Cancer J Clin, 2020, 70(3): 145-164. DOI:10.3322/caac.21601.
[2] 郑荣寿,孙可欣,张思维,等. 2015年中国恶性肿瘤流行情况分析[J]. 中华肿瘤杂志,2019,41(1):19-28. DOI:10.3760/cma.j.issn.0253-3766.2019.01.008.
[3] Bleijenberg AGC, van Leerdam ME, Bargeman M, et al. Substantial and sustained improvement of serrated polyp detection after a simple educational intervention: results from a prospective controlled trial [J]. Gut, 2020, 69(12): 2150-2158. DOI:10.1136/gutjnl-2019-319804.
[4] Erichsen R, Baron JA, Hamilton-Dutoit SJ, et al. Increased risk of colorectal cancer development among patients with serrated polyps [J]. Gastroenterology, 2016, 150(4): 895-902.e5. DOI: 10.1053/j.gastro.2015.11.046.
[5] Keum N, Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies [J]. Nat Rev Gastroenterol Hepatol, 2019, 16(12):713-732. DOI:10.1038/s41575-019-0189-8.
[6] East JE, Atkin WS, Bateman AC, et al. British society of gastroenterology position statement on serrated polyps in the colon and rectum [J]. Gut, 2017, 66(7):1181-1196. DOI:10.1136/gutjnl-2017-314005.
[7] Bettington M, Walker N, Clouston A, et al. The serrated pathway to colorectal carcinoma: current concepts and challenges [J]. Histopathology, 2013, 62(3):367-386. DOI:10.1111/his.12055.
[8] Dekker E, Tanis PJ, Vleugels JLA, et al. Colorectal cancer [J]. Lancet, 2019, 394(10207):1467-1480. DOI: 10.1016/S0140-6736(19)32319-0.
[9] Huang CS, O'brien MJ, Yang S, et al. Hyperplastic polyps, serrated adenomas, and the serrated polyp neoplasia pathway [J]. Am J Gastroenterol, 2004, 99(11): 2242-2255. DOI: 10.1111/j.1572-0241.2004.40131.x.
[10] Leggett B, Whitehall V. Role of the serrated pathway in colorectal cancer pathogenesis [J]. Gastroenterology, 2010, 138(6):2088-2100. DOI: 10.1053/j.gastro.2009. 12.066.
[11] IJspeert JE, Vermeulen L, Meijer GA, et al. Serrated neoplasia-role in colorectal carcinogenesis and clinical implications [J]. Nat Rev Gastroenterol Hepatol, 2015, 12:401-409. DOI:10.1038/nrgastro.2015.73.
[12] 陆宝钿,李兆滔,崔西玉,等. 佛山地区大肠锯齿状腺癌临床流行病学特征研究[J]. 现代医药卫生,2020,36(8):1138-1141. DOI:10.3969/j.issn.1009-5519.2020.08.006.
[13] Tuppurainen K, Mäkinen JM, Junttila O, et al. Morphology and microsatellite instability in sporadic serrated and non-serrated colorectal cancer [J]. J Pathol, 2005, 207(3):285-294. DOI: 10.1002/path.1850.
[14] Kanzaki H, Hirasaki S, Suzuki S, et al. Early stage of colonic adenocarcinoma associated with traditional serrated adenoma [J]. Intern Med, 2007, 46(23): 1911-1914. DOI:10.2169/internalmedicine.46.0388.
[15] 刘喜波. 中国人结直肠锯齿状腺癌RAS/RAF突变及结直肠癌预后模型的研究[D]. 杭州:浙江大学,2017.
[16] García-Solano J, Pérez-Guillermo M, Conesa-Zamora P, et al. Clinicopathologic study of 85 colorectal serrated adenocarcinomas: further insights into the full recognition of a new subset of colorectal carcinoma [J]. Hum Pathol, 2010, 41(10): 1359-1368. DOI:10.1016/j.humpath.2010.04.002
[17] East JE, Atkin WS, Bateman AC, et al. British Society of Gastroenterology position statement on serrated polyps in the colon and rectum [J]. Gut, 2017, 66(7):1181-1196. DOI: 10.1136/gutjnl-2017-314005.
[18] Bailie L, Loughrey MB, Coleman HG. Lifestyle risk factors for serrated colorectal polyps: a systematic review and meta-analysis [J]. Gastroenterology, 2017,152(1): 92-104. DOI:10.1053/j.gastro.2016.09.003.
[19] Zorron Cheng Tao Pu L, Rana K, Singh G, et al. Different factors are associated with conventional adenoma and serrated colorectal neoplasia [J]. Nagoya J Med Sci, 2020, 82(2):335-343. DOI:10.18999/nagjms.82.2.335.
[20] Kanth P, Yu Z, Keener MB, et al. Cancer risk in patients with and relatives of serrated polyposis syndrome and sporadic sessile serrated sessions [J]. Am J Gastroenterol, 2022, 117(2): 336-342. DOI: 10.14309/ajg. 00000000- 00001572.
[21] Lieberman DA, Rex DK, Winawer SJ, et al. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer [J]. Gastroenterology, 2012, 143(3): 844-857. DOI:10.1053/j.gastro. 2012. 06.001.
[22] Lash RH, Genta RM, Schuler CM. Sessile serrated adenomas: prevalence of dysplasia and carcinoma in 2139 patients [J]. J Clin Pathol, 2010, 63(8): 681-686. DOI:10.1136/jcp.2010.075507.
[23] Nagtegaal ID, Odze RD, Klimstra D, et al. The 2019 WHO classification of tumours of the digestive system [J]. Histopathology, 2020, 76: 182-188. DOI:10.1111/his. 13975
[24] Jass JR, Smith M. Sialic acid and epithelial differentiation in colorectal polyps and cancer--a morphological, mucin and lectin histochemical study. Pathology. 1992;24(4):233-242. DOI:10.3109/00313029209068874
[25] Mäkinen MJ, George SM, Jernvall P, et al. Colorectal carcinoma associated with serrated adenoma-prevalence, histological features, and prognosis [J]. J Pathol, 2001, 193(3):286-294. DOI:10.1002/1096-9896(2000)9999:9999<::AID-PATH800>3.0.CO;2-2.
[26] Aust DE. WHO classification 2010 for the lower gastrointestinal tract: what is new? [J]. Pathologe, 2011, 32 Suppl 2:326-331. DOI:10.1007/s00292-011-1505-4
[27] Budinska E, Popovici V, Tejpar S, et al. Gene expression patterns unveil a new level of molecular heterogeneity in colorectal cancer [J]. J Pathol, 2013, 231: 63-76. DOI: 10.1002/path.4212
[28] Roepman P, Schlicker A, Tabernero J, et al. Colorectal cancer intrinsic subtypes predict chemotherapy benefit, deficient mismatch repair and epithelial-to-mesenchymal transition [J]. Int J Cancer, 2014, 134:552-562. DOI:10.1002/ijc.28387.
[29] Sadanandam A, Lyssiotis CA, Homicsko K, et al. A colorectal cancer classification system that associates cellular phenotype and responses to therapy [J]. Nat Med, 2013, 19:619-625. DOI:10.1038/nm.3175.
[30] De Sousa EMF, Wang X, Jansen M, et al. Poor-prognosis colon cancer is defined by a molecularly distinct subtype and develops from serrated precursor lesions [J]. Nat Med, 2013, 19:614-618. DOI:10.1038/nm.3174.
[31] Nakanishi Y, Diaz-Meco MT, Moscat J. Serrated colorectal cancer: the road less travelled? [J]. Trends Cancer, 2019, 5(11): 742-754. DOI: 10.1016/j.trecan.2019.09.004.
[32] Garces S, Yin CC, Patel KP, et al. Focal Rosai-Dorfman disease coexisting with lymphoma in the same anatomic site: a localized histiocytic proliferation associated with MAPK/ERK pathway activation [J]. Mod Pathol, 2019, 32(1): 16-26. DOI:10.1038/s41379-018-0152-1.
[33] Murcia O, Juárez M, Hernández-Illán E, et al. Serrated colorectal cancer: molecular classification, prognosis, and response to chemotherapy [J]. World J Gastroenterol, 2016, 22(13): 3516-3530. DOI:10.3748/wjg.v22.i13.3516.
[34] Murakami T, Sakamoto N, Nagahara A. Clinicopathological features, diagnosis, and treatment of sessile serrated adenoma/polyp with dysplasia/carcinoma [J]. J Gastroenterol Hepatol, 2019, 34(10): 1685-1695. DOI: 10.1111/jgh.14752.
[35] Sugai T, Eizuka M, Fujita Y, et al. Molecular profiling based on KRAS/BRAF mutation, methylation, and microsatellite statuses in serrated lesions [J]. Dig Dis Sci, 2018, 63(10): 2626-2638. DOI:10.1007/s10620-018-5167-4.
[36] Janjua HG, Høgdall E, Linnemann D. Hyperplastic polyps of the colon and rectum - reclassification, BRAF and KRAS status in index polyps and subsequent colorectal carcinoma [J]. APMIS, 2015, 123(4): 298-304. DOI: 10.1111/apm.12355.
[37] Stefanius K, Ylitalo L, Tuomisto A, et al. Frequent mutations of KRAS in addition to BRAF in colorectal serrated adenocarcinoma [J]. Histopathology, 2011, 58(5): 679-692. DOI: 10.1111/j.1365-2559.2011.03821.x.
[38] Toyota M, Issa JP. The role of DNA hypermethylation in human neoplasia [J]. Electrophoresis, 2000, 21(2): 329-333. DOI:10.1017/S0029665118000150.
[39] Kang X, Zhang R, Kwong TN, et al. Serrated neoplasia in the colorectum: gut microbiota and molecular pathways [J]. Gut Microbes, 2021, 13(1):1-12. DOI:10.1080/19490976.2020.1863135.
[40] Yang S, Farraye FA, Mack C, et al. BRAF and KRAS mutations in hyperplastic polyps and serrated adenomas of the colorectum: relationship to histology and CpG island methylation status [J]. Am J Surg Pathol, 2004, 28(11): 1452-1459. DOI:10.1097/01.pas.0000141404. 56839.6a.
[41] Weisenberger DJ, Siegmund KD, Campan M, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer [J]. Nat Genet, 2006, 38(7): 787-793. DOI: 10.1038/ng1834.
[42] Cheng X, Xu X, Chen D, et al. Therapeutic potential of targeting the Wnt/β-catenin signaling pathway in colorectal cancer [J]. Biomed Pharmacother, 2019, 110: 473-481. DOI: 10.1016/j.biopha.2018.11.082.
[43] Kim S, Jeong S. Mutation hotspots in the β-catenin gene: lessons from the human cancer genome databases [J]. Mol Cells, 2019, 42(1): 8-16. DOI: 10.14348/molcells. 2018.0436.
[44] Borowsky J, Dumenil T, Bettington M, et al. The role of APC in WNT pathway activation in serrated neoplasia [J]. Mod Pathol, 2018, 31(3):495-504. DOI:10.1038/modpathol.2017.150.
[45] Dhir M, Yachida S, Van Neste L, et al. Sessile serrated adenomas and classical adenomas: an epigenetic perspective on premalignant neoplastic lesions of the gastrointestinal tract [J]. Int J Cancer, 2011, 129(8): 1889-1898. DOI:10.1002/ijc.25847.
[46] Fujita K, Yamamoto H, Matsumoto T, et al. Sessile serrated adenoma with early neoplastic progression: a clinicopathologic and molecular study [J]. Am J Surg Pathol, 2011, 35(2):295-304. DOI:10.1097/PAS.0b013e318205df36.
[47] Murakami T, Mitomi H, Saito T, et al. Distinct WNT/β-catenin signaling activation in the serrated neoplasia pathway and the adenoma-carcinoma sequence of the colorectum [J]. Mod Pathol, 2015, 28(1): 146-158. DOI: 10.1038/modpathol.2014.41.
[48] Yurgelun MB, Hampel H. Recent advances in lynch syndrome: diagnosis, treatment, and cancer prevention [J]. Am Soc Clin Oncol Educ Book, 2018, 38: 101-109. DOI:10.1200/EDBK_208341.
[49] Harada S, Morlote D. Molecular pathology of colorectal cancer [J]. Adv Anat Pathol, 2020, 27(1):20-26. DOI:10.1097/PAP.0000000000000247.
[50] De' Angelis GL, Bottarelli L, Azzoni C, et al. Microsatellite instability in colorectal cancer [J]. Acta Biomed, 2018, 89(9-S): 97-101. DOI:10.23750/abm.v89i9-S.7960.
[51] Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer [J]. Nature, 2012, 487(7407): 330-337. DOI:10.1038/nature11252.
[52] Huang CS, Farraye FA, Yang S, et al. The clinical significance of serrated polyps [J]. Am J Gastroenterol, 2011, 106(2):229-241. DOI:10.1038/ajg.2010.429.
[53] Murcia O, Juárez M, Hernández-Illán E, et al. Serrated colorectal cancer: molecular classification, prognosis, and response to chemotherapy [J]. World J Gastroenterol, 2016, 22(13): 3516-3530. DOI:10.3748/wjg.v22.i13.3516.
[54] Wong SH, Yu J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications [J]. Nat Rev Gastroenterol Hepatol, 2019, 16(11): 690-704. DOI:10.1038/s41575-019-0209-8
[55] Yu J, Chen Y, Fu X, et al. Invasive Fusobacterium nucleatum may play a role in the carcinogenesis of proximal colon cancer through the serrated neoplasia pathway [J]. Int J Cancer, 2016, 139(6): 1318-1326.DOI:10.1002/ijc.30168.
[56] Guinney J, Dienstmann R, Wang X, et al. The consensus molecular subtypes of colorectal cancer [J]. Nat Med, 2015, 21(11): 1350-1356. DOI:10.1038/nm.3967.
[57] Purcell RV, Visnovska M, Biggs PJ, et al. Distinct gut microbiome patterns associate with consensus molecular subtypes of colorectal cancer [J]. Sci Rep, 2017, 7(1):11590. DOI:10.1038/s41598-017-11237-6.