Research advances of primary colorectal signet-ring cell carcinoma_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

WANG Yan ¹ , FANG Chao ¹ ,  YU Yongyang ² , HU Xu ¹

1. West China Hospital of Sichuan University, West China Medical School, Chengdu 610041, P. R. China;
2. Department of Gastrointestinal Surgery, West China Hospital of Sichuan University, Chengdu 610041, P. R. China;

Corresponding?author：

YU Yongyang, Email: yuyongyang@hotmail.com

Keywords：

colorectal signet-ring cell carcinoma; research advance; review

DOI：

10.7507/1007-9424.201801038

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the current research advances of colorectal signet-ring cell carcinoma (SRCC). Methods In this paper, the related literatures of colorectal SRCC in recent years were collected and reviewed. Results Colorectal SRCC was a pathological subtype of colorectal adenocarcinoma, with extremely low incidence but high malignancy and poor prognosis. At present, its molecular mechanism was still not very clear and the clinicopathological manifestations were not specific. Surgical treatment was the major treatmen. Conclusions Although we already have a certain degree of understanding about colorectal SRCC, due to the limitations in the results of some related researches because of the small sample size or the single-center study, we still need more researches to improve the cognition of colorectal SRCC.

Citation： WANG Yan, FANG Chao, YU Yongyang, HU Xu. Research advances of primary colorectal signet-ring cell carcinoma. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2018, 25(7): 883-888. doi: 10.7507/1007-9424.201801038 Copy

1.	李道娟, 李倩, 賀宇彤. 結直腸癌流行病學趨勢. 腫瘤防治研究, 2015, 42(3): 305-310.
2.	Tan Y, Fu J, Li X, et al. A minor (<50%) signet-ring cell component associated with poor prognosis in colorectal cancer patients: a 26-year retrospective study in China. PLoS One, 2015, 10(3): e0121944.
3.	Laufman H, Saphir O. Primary linitis plastica type of carcinoma of the colon. AMA Arch Surg, 1951, 62(1): 79-91.
4.	曲輝, 車旭, 王成鋒, 等. 結直腸印戒細胞癌. 中華普通外科雜志, 2008, 23(6): 422-424.
5.	Kang H, O’Connell JB, Maggard MA, et al. A 10-year outcomes evaluation of mucinous and signet-ring cell carcinoma of the colon and rectum. Dis Colon Rectum, 2005, 48(6): 1161-1168.
6.	Hyngstrom JR, Hu CY, Xing Y, et al. Clinicopathology and outcomes for mucinous and signet ring colorectal adenocarcinoma: analysis from the National Cancer Data Base. Ann Surg Oncol, 2012, 19(9): 2814-2821.
7.	Hugen N, Verhoeven RH, Lemmens VE, et al. Colorectal signet-ring cell carcinoma: benefit from adjuvant chemotherapy but a poor prognostic factor. Int J Cancer, 2015, 136(2): 333-339.
8.	Nitsche U, Friess H, Agha A, et al. Prognosis of mucinous and signet-ring cell colorectal cancer in a population-based cohort. J Cancer Res Clin Oncol, 2016, 142(11): 2357-2366.
9.	Chen JS, Hsieh PS, Chiang JM, et al. Clinical outcome of signet ring cell carcinoma and mucinous adenocarcinoma of the colon. Chang Gung Med J, 2010, 33(1): 51-57.
10.	Liang Z, Yan D, Li G, et al. Clinical analysis of primary colorectal signet-ring cell carcinoma. Clin Colorectal Cancer, 2018, 17(1): e39-e44.
11.	Lee WS, Chun HK, Lee WY, et al. Treatment outcomes in patients with signet ring cell carcinoma of the colorectum. Am J Surg, 2007, 194(3): 294-298.
12.	Chew MH, Yeo SA, Ng ZP, et al. Critical analysis of mucin and signet ring cell as prognostic factors in an Asian population of 2, 764 sporadic colorectal cancers. Int J Colorectal Dis, 2010, 25(10): 1221-1229.
13.	Tung SY, Wu CS, Chen PC. Primary signet ring cell carcinoma of colorectum: an age- and sex-matched controlled study. Am J Gastroenterol, 1996, 91(10): 2195-2199.
14.	Sasaki S, Masaki T, Umetani N, et al. Characteristics in primary signet-ring cell carcinoma of the colorectum, from clinicopathological observations. Jpn J Clin Oncol, 1998, 28(3): 202-206.
15.	Kim HJ, Ha HK, Cho KS, et al. CT features of primary colorectal signet-ring cell carcinoma. J Comput Assist Tomogr, 2001, 25(2): 225-230.
16.	Song W, Wu SJ, He YL, et al. Clinicopathologic features and survival of patients with colorectal mucinous, signet-ring cell or non-mucinous adenocarcinoma: experience at an institution in southern China. Chin Med J (Engl), 2009, 122(13): 1486-1491.
17.	Cai X, Qi WX, Wang L, et al. Correlation of multiple proteins with clinic-pathological features and its prognostic significance in colorectal cancer with signet-ring cell component. Eur Rev Med Pharmacol Sci, 2016, 20(16): 3358-3367.
18.	李振輝, 董興祥, 高德培, 等. 結直腸原發印戒細胞癌與腺癌的 CT 表現比較. 中國醫學影像學雜志, 2015, 23(11): 834-838.
19.	劉騫, 王成鋒, 趙東兵, 等. 結直腸印戒細胞癌與黏液腺癌的臨床病理分析. 中華醫學雜志, 2010, 90(44): 3124-3126.
20.	Pozos-Ochoa LI, Lino-Silva LS, León-Takahashi AM, et al. Prognosis of signet ring cell carcinoma of the colon and rectum and their distinction of mucinous adenocarcinoma with signet ring cells. A comparative study. Pathol Oncol Res, 2017, [Epub ahead of print].
21.	Yamamoto H, Imai K. Microsatellite instability: an update. Arch Toxicol, 2015, 89(6): 899-921.
22.	Kawakami H, Zaanan A, Sinicrope FA. Microsatellite instability testing and its role in the management of colorectal cancer. Curr Treat Options Oncol, 2015, 16(7): 30.
23.	Ogino S, Brahmandam M, Cantor M, et al. Distinct molecular features of colorectal carcinoma with signet ring cell component and colorectal carcinoma with mucinous component. Mod Pathol, 2006, 19(1): 59-68.
24.	Lee HS, Soh JS, Lee S, et al. Clinical features and prognosis of resectable primary colorectal signet-ring cell carcinoma. Intest Res, 2015, 13(4): 332-338.
25.	Hartman DJ, Nikiforova MN, Chang DT, et al. Signet ring cell colorectal carcinoma: a distinct subset of mucin-poor microsatellite-stable signet ring cell carcinoma associated with dismal prognosis. Am J Surg Pathol, 2013, 37(7): 969-977.
26.	Sung CO, Seo JW, Kim KM, et al. Clinical significance of signet-ring cells in colorectal mucinous adenocarcinoma. Mod Pathol, 2008, 21(12): 1533-1541.
27.	Kakar S, Deng G, Smyrk TC, et al. Loss of heterozygosity, aberrant methylation, BRAF mutation and KRAS mutation in colorectal signet ring cell carcinoma. Mod Pathol, 2012, 25(7): 1040-1047.
28.	Umar A, Boland CR, Terdiman JP, et al. Revised Bethesda Guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. J Natl Cancer Inst, 2004, 96(4): 261-268.
29.	Hamilton SR, Aaltonen LA. Pathology and genetics of tumours of the digestive system. France: International Agency for Research on Cancer (IARC), 2000: 47-50.
30.	Joseph CG, Darrah E, Shah AA, et al. Association of the autoimmune disease scleroderma with an immunologic response to cancer. Science, 2014, 343(6167): 152-157.
31.	Wistuba II, Behrens C, Albores-Saavedra J, et al. Distinct K-ras mutation pattern characterizes signet ring cell colorectal carcinoma. Clin Cancer Res, 2003, 9(10 Pt 1): 3615-3619.
32.	Peyssonnaux C, Eychène A. The Raf/MEK/ERK pathway: new concepts of activation. Biol Cell, 2001, 93(1-2): 53-62.
33.	Seshimo I, Yamamoto H, Mishima H, et al. Expression and mutation of SMAD4 in poorly differentiated carcinoma and signet-ring cell carcinoma of the colorectum. J Exp Clin Cancer Res, 2006, 25(3): 433-442.
34.	Andreyev HJ, Norman AR, Cunningham D, et al. Kirsten ras mutations in patients with colorectal cancer: the multicenter " RASCAL” study. J Natl Cancer Inst, 1998, 90(9): 675-684.
35.	Inamura K, Yamauchi M, Nishihara R, et al. Prognostic significance and molecular features of signet-ring cell and mucinous components in colorectal carcinoma. Ann Surg Oncol, 2015, 22(4): 1226-1235.
36.	Alvi MA, Loughrey MB, Dunne P, et al. Molecular profiling of signet ring cell colorectal cancer provides a strong rationale for genomic targeted and immune checkpoint inhibitor therapies. Br J Cancer, 2017, 117(2): 203-209.
37.	Terada T. An immunohistochemical study of primary signet-ring cell carcinoma of the stomach and colorectum: Ⅲ. Expressions of EMA, CEA, CA19-9, CDX-2, p53, Ki-67 antigen, TTF-1, vimentin, and p63 in normal mucosa and in 42 cases. Int J Clin Exp Pathol, 2013, 6(4): 630-638.
38.	Mai KT, Isotalo PA, Guindi M, et al. Intestinal epithelial lesions associated with signet ring cell carcinoma of the colon and small intestine. Pathology, 2002, 34(1): 51-56.
39.	Rosai J. Rosai and ackerman’s surgical pathology. 9^th, New York: Mosby, 2004: 65-66.
40.	Cabibi D, Calascibetta A, Campione M, et al. Clinical relevance of thymidylate synthase expression in the signet ring cell histotype component of colorectal carcinoma. Eur J Cancer, 2004, 40(18): 2845-2850.
41.	Chu PG, Weiss LM. Immunohistochemical characterization of signet-ring cell carcinomas of the stomach, breast, and colon. Am J Clin Pathol, 2004, 121(6): 884-892.
42.	Biemer-Hüttmann AE, Walsh MD, McGuckin MA, et al. Immunohistochemical staining patterns of MUC1, MUC2, MUC4, and MUC5AC mucins in hyperplastic polyps, serrated adenomas, and traditional adenomas of the colorectum. J Histochem Cytochem, 1999, 47(8): 1039-1048.
43.	Baldus SE, M?nig SP, Hanisch FG, et al. Comparative evaluation of the prognostic value of MUC1, MUC2, sialyl-Lewis(a) and sialyl-Lewis(x) antigens in colorectal adenocarcinoma. Histopathology, 2002, 40(5): 440-449.
44.	Walsh MD, Clendenning M, Williamson E, et al. Expression of MUC2, MUC5AC, MUC5B, and MUC6 mucins in colorectal cancers and their association with the CpG island methylator phenotype. Mod Pathol, 2013, 26(12): 1642-1656.
45.	Imai Y, Yamagishi H, Fukuda K, et al. Differential mucin phenotypes and their significance in a variation of colorectal carcinoma. World J Gastroenterol, 2013, 19(25): 3957-3968.
46.	Sunami E, Tsuno N, Osada T, et al. MMP-1 is a prognostic marker for hematogenous metastasis of colorectal cancer. Oncologist, 2000, 5(2): 108-114.
47.	Wang R, Ma X, Li Y, et al. The characteristics and prognostic effect of E-cadherin expression in colorectal signet ring cell carcinoma. PLoS One, 2016, 11(8): e0160527.
48.	Cabibi D, Calascibetta A, Aragona F, et al. Differing expression of metalloprotease and of adhesion molecules in signet-ring cell and intestinal colorectal carcinoma. Anticancer Res, 2009, 29(11): 4417-4422.
49.	Psathakis D, Schiedeck TH, Krug F, et al. Ordinary colorectal adenocarcinoma vs. primary colorectal signet-ring cell carcinoma: study matched for age, gender, grade, and stage. Dis Colon Rectum, 1999, 42(12): 1618-1625.
50.	Nitsche U, Zimmermann A, Sp?th C, et al. Mucinous and signet-ring cell colorectal cancers differ from classical adenocarcinomas in tumor biology and prognosis. Ann Surg, 2013, 258(5): 775-782.
51.	Ciarrocchi A. Rectal versus non-rectal primary signet ring cell carcinoma of the colorectum: a retrospective survival analysis controlled for confounders. J Gastrointest Cancer, 2014, 45(3): 312-318.
52.	Chen JS, Hsieh PS, Hung SY, et al. Clinical significance of signet ring cell rectal carcinoma. Int J Colorectal Dis, 2004, 19(2): 102-107.
53.	Bittorf B, Merkel S, Matzel KE, et al. Primary signet-ring cell carcinoma of the colorectum. Langenbecks Arch Surg, 2004, 389(3): 178-183.
54.	Thota R, Fang X, Subbiah S. Clinicopathological features and survival outcomes of primary signet ring cell and mucinous adenocarcinoma of colon: retrospective analysis of VACCR database. J Gastrointest Oncol, 2014, 5(1): 18-24.
55.	Pande R, Sunga A, Levea C, et al. Significance of signet-ring cells in patients with colorectal cancer. Dis Colon Rectum, 2008, 51(1): 50-55.
56.	Barresi V, Reggiani Bonetti L, Domati F, et al. Prognostic relevance of histopathological features in signet ring cell carcinoma of the colorectum. Virchows Arch, 2016, 469(3): 267-275.
57.	Kong X, Zhang X, Huang Y, et al. Characteristics and prognostic factors of colorectal mucinous adenocarcinoma with signet ring cells. Cancer Manag Res, 2017, 9: 573-580.
58.	Mora-Guzmán I, Di Martino M, Mu?oz de Nova JL, et al. Primary signet ring cell carcinoma of the colon: a rare condition with a poor prognosis. A report on two cases. Rev Gastroenterol Mex, 2017, [Epub ahead of print].
59.	Song BR, Xiao CC, Wu ZK. Predictors of lymph node metastasis and prognosis in pT1 colorectal cancer patients with signet-ring cell and mucinous adenocarcinomas. Cell Physiol Biochem, 2017, 41(5): 1753-1765.
60.	Gopalan V, Smith RA, Ho YH, et al. Signet-ring cell carcinoma of colorectum－current perspectives and molecular biology. Int J Colorectal Dis, 2011, 26(2): 127-133.
61.	NCCN. Clinical Practice Guidelines in Oncology: rectal cancer. 2015-05-25. https://www.nccn.org/professionals/physician_gls/default.aspx.
62.	劉德寶, 徐忠法, 范開席. 晚期結直腸癌的治療策略. 國際腫瘤學雜志, 2016, 43(5): 387-390.
63.	Tamhankar AS, Ingle P, Engineer R, et al. Signet ring colorectal carcinoma: do we need to improve the treatment algorithm? World J Gastrointest Oncol, 2016, 8(12): 819-825.

1. 李道娟, 李倩, 賀宇彤. 結直腸癌流行病學趨勢. 腫瘤防治研究, 2015, 42(3): 305-310.
2. Tan Y, Fu J, Li X, et al. A minor (<50%) signet-ring cell component associated with poor prognosis in colorectal cancer patients: a 26-year retrospective study in China. PLoS One, 2015, 10(3): e0121944.
3. Laufman H, Saphir O. Primary linitis plastica type of carcinoma of the colon. AMA Arch Surg, 1951, 62(1): 79-91.
4. 曲輝, 車旭, 王成鋒, 等. 結直腸印戒細胞癌. 中華普通外科雜志, 2008, 23(6): 422-424.
5. Kang H, O’Connell JB, Maggard MA, et al. A 10-year outcomes evaluation of mucinous and signet-ring cell carcinoma of the colon and rectum. Dis Colon Rectum, 2005, 48(6): 1161-1168.
6. Hyngstrom JR, Hu CY, Xing Y, et al. Clinicopathology and outcomes for mucinous and signet ring colorectal adenocarcinoma: analysis from the National Cancer Data Base. Ann Surg Oncol, 2012, 19(9): 2814-2821.
7. Hugen N, Verhoeven RH, Lemmens VE, et al. Colorectal signet-ring cell carcinoma: benefit from adjuvant chemotherapy but a poor prognostic factor. Int J Cancer, 2015, 136(2): 333-339.
8. Nitsche U, Friess H, Agha A, et al. Prognosis of mucinous and signet-ring cell colorectal cancer in a population-based cohort. J Cancer Res Clin Oncol, 2016, 142(11): 2357-2366.
9. Chen JS, Hsieh PS, Chiang JM, et al. Clinical outcome of signet ring cell carcinoma and mucinous adenocarcinoma of the colon. Chang Gung Med J, 2010, 33(1): 51-57.
10. Liang Z, Yan D, Li G, et al. Clinical analysis of primary colorectal signet-ring cell carcinoma. Clin Colorectal Cancer, 2018, 17(1): e39-e44.
11. Lee WS, Chun HK, Lee WY, et al. Treatment outcomes in patients with signet ring cell carcinoma of the colorectum. Am J Surg, 2007, 194(3): 294-298.
12. Chew MH, Yeo SA, Ng ZP, et al. Critical analysis of mucin and signet ring cell as prognostic factors in an Asian population of 2, 764 sporadic colorectal cancers. Int J Colorectal Dis, 2010, 25(10): 1221-1229.
13. Tung SY, Wu CS, Chen PC. Primary signet ring cell carcinoma of colorectum: an age- and sex-matched controlled study. Am J Gastroenterol, 1996, 91(10): 2195-2199.
14. Sasaki S, Masaki T, Umetani N, et al. Characteristics in primary signet-ring cell carcinoma of the colorectum, from clinicopathological observations. Jpn J Clin Oncol, 1998, 28(3): 202-206.
15. Kim HJ, Ha HK, Cho KS, et al. CT features of primary colorectal signet-ring cell carcinoma. J Comput Assist Tomogr, 2001, 25(2): 225-230.
16. Song W, Wu SJ, He YL, et al. Clinicopathologic features and survival of patients with colorectal mucinous, signet-ring cell or non-mucinous adenocarcinoma: experience at an institution in southern China. Chin Med J (Engl), 2009, 122(13): 1486-1491.
17. Cai X, Qi WX, Wang L, et al. Correlation of multiple proteins with clinic-pathological features and its prognostic significance in colorectal cancer with signet-ring cell component. Eur Rev Med Pharmacol Sci, 2016, 20(16): 3358-3367.
18. 李振輝, 董興祥, 高德培, 等. 結直腸原發印戒細胞癌與腺癌的 CT 表現比較. 中國醫學影像學雜志, 2015, 23(11): 834-838.
19. 劉騫, 王成鋒, 趙東兵, 等. 結直腸印戒細胞癌與黏液腺癌的臨床病理分析. 中華醫學雜志, 2010, 90(44): 3124-3126.
20. Pozos-Ochoa LI, Lino-Silva LS, León-Takahashi AM, et al. Prognosis of signet ring cell carcinoma of the colon and rectum and their distinction of mucinous adenocarcinoma with signet ring cells. A comparative study. Pathol Oncol Res, 2017, [Epub ahead of print].
21. Yamamoto H, Imai K. Microsatellite instability: an update. Arch Toxicol, 2015, 89(6): 899-921.
22. Kawakami H, Zaanan A, Sinicrope FA. Microsatellite instability testing and its role in the management of colorectal cancer. Curr Treat Options Oncol, 2015, 16(7): 30.
23. Ogino S, Brahmandam M, Cantor M, et al. Distinct molecular features of colorectal carcinoma with signet ring cell component and colorectal carcinoma with mucinous component. Mod Pathol, 2006, 19(1): 59-68.
24. Lee HS, Soh JS, Lee S, et al. Clinical features and prognosis of resectable primary colorectal signet-ring cell carcinoma. Intest Res, 2015, 13(4): 332-338.
25. Hartman DJ, Nikiforova MN, Chang DT, et al. Signet ring cell colorectal carcinoma: a distinct subset of mucin-poor microsatellite-stable signet ring cell carcinoma associated with dismal prognosis. Am J Surg Pathol, 2013, 37(7): 969-977.
26. Sung CO, Seo JW, Kim KM, et al. Clinical significance of signet-ring cells in colorectal mucinous adenocarcinoma. Mod Pathol, 2008, 21(12): 1533-1541.
27. Kakar S, Deng G, Smyrk TC, et al. Loss of heterozygosity, aberrant methylation, BRAF mutation and KRAS mutation in colorectal signet ring cell carcinoma. Mod Pathol, 2012, 25(7): 1040-1047.
28. Umar A, Boland CR, Terdiman JP, et al. Revised Bethesda Guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. J Natl Cancer Inst, 2004, 96(4): 261-268.
29. Hamilton SR, Aaltonen LA. Pathology and genetics of tumours of the digestive system. France: International Agency for Research on Cancer (IARC), 2000: 47-50.
30. Joseph CG, Darrah E, Shah AA, et al. Association of the autoimmune disease scleroderma with an immunologic response to cancer. Science, 2014, 343(6167): 152-157.
31. Wistuba II, Behrens C, Albores-Saavedra J, et al. Distinct K-ras mutation pattern characterizes signet ring cell colorectal carcinoma. Clin Cancer Res, 2003, 9(10 Pt 1): 3615-3619.
32. Peyssonnaux C, Eychène A. The Raf/MEK/ERK pathway: new concepts of activation. Biol Cell, 2001, 93(1-2): 53-62.
33. Seshimo I, Yamamoto H, Mishima H, et al. Expression and mutation of SMAD4 in poorly differentiated carcinoma and signet-ring cell carcinoma of the colorectum. J Exp Clin Cancer Res, 2006, 25(3): 433-442.
34. Andreyev HJ, Norman AR, Cunningham D, et al. Kirsten ras mutations in patients with colorectal cancer: the multicenter " RASCAL” study. J Natl Cancer Inst, 1998, 90(9): 675-684.
35. Inamura K, Yamauchi M, Nishihara R, et al. Prognostic significance and molecular features of signet-ring cell and mucinous components in colorectal carcinoma. Ann Surg Oncol, 2015, 22(4): 1226-1235.
36. Alvi MA, Loughrey MB, Dunne P, et al. Molecular profiling of signet ring cell colorectal cancer provides a strong rationale for genomic targeted and immune checkpoint inhibitor therapies. Br J Cancer, 2017, 117(2): 203-209.
37. Terada T. An immunohistochemical study of primary signet-ring cell carcinoma of the stomach and colorectum: Ⅲ. Expressions of EMA, CEA, CA19-9, CDX-2, p53, Ki-67 antigen, TTF-1, vimentin, and p63 in normal mucosa and in 42 cases. Int J Clin Exp Pathol, 2013, 6(4): 630-638.
38. Mai KT, Isotalo PA, Guindi M, et al. Intestinal epithelial lesions associated with signet ring cell carcinoma of the colon and small intestine. Pathology, 2002, 34(1): 51-56.
39. Rosai J. Rosai and ackerman’s surgical pathology. 9^th, New York: Mosby, 2004: 65-66.
40. Cabibi D, Calascibetta A, Campione M, et al. Clinical relevance of thymidylate synthase expression in the signet ring cell histotype component of colorectal carcinoma. Eur J Cancer, 2004, 40(18): 2845-2850.
41. Chu PG, Weiss LM. Immunohistochemical characterization of signet-ring cell carcinomas of the stomach, breast, and colon. Am J Clin Pathol, 2004, 121(6): 884-892.
42. Biemer-Hüttmann AE, Walsh MD, McGuckin MA, et al. Immunohistochemical staining patterns of MUC1, MUC2, MUC4, and MUC5AC mucins in hyperplastic polyps, serrated adenomas, and traditional adenomas of the colorectum. J Histochem Cytochem, 1999, 47(8): 1039-1048.
43. Baldus SE, M?nig SP, Hanisch FG, et al. Comparative evaluation of the prognostic value of MUC1, MUC2, sialyl-Lewis(a) and sialyl-Lewis(x) antigens in colorectal adenocarcinoma. Histopathology, 2002, 40(5): 440-449.
44. Walsh MD, Clendenning M, Williamson E, et al. Expression of MUC2, MUC5AC, MUC5B, and MUC6 mucins in colorectal cancers and their association with the CpG island methylator phenotype. Mod Pathol, 2013, 26(12): 1642-1656.
45. Imai Y, Yamagishi H, Fukuda K, et al. Differential mucin phenotypes and their significance in a variation of colorectal carcinoma. World J Gastroenterol, 2013, 19(25): 3957-3968.
46. Sunami E, Tsuno N, Osada T, et al. MMP-1 is a prognostic marker for hematogenous metastasis of colorectal cancer. Oncologist, 2000, 5(2): 108-114.
47. Wang R, Ma X, Li Y, et al. The characteristics and prognostic effect of E-cadherin expression in colorectal signet ring cell carcinoma. PLoS One, 2016, 11(8): e0160527.
48. Cabibi D, Calascibetta A, Aragona F, et al. Differing expression of metalloprotease and of adhesion molecules in signet-ring cell and intestinal colorectal carcinoma. Anticancer Res, 2009, 29(11): 4417-4422.
49. Psathakis D, Schiedeck TH, Krug F, et al. Ordinary colorectal adenocarcinoma vs. primary colorectal signet-ring cell carcinoma: study matched for age, gender, grade, and stage. Dis Colon Rectum, 1999, 42(12): 1618-1625.
50. Nitsche U, Zimmermann A, Sp?th C, et al. Mucinous and signet-ring cell colorectal cancers differ from classical adenocarcinomas in tumor biology and prognosis. Ann Surg, 2013, 258(5): 775-782.
51. Ciarrocchi A. Rectal versus non-rectal primary signet ring cell carcinoma of the colorectum: a retrospective survival analysis controlled for confounders. J Gastrointest Cancer, 2014, 45(3): 312-318.
52. Chen JS, Hsieh PS, Hung SY, et al. Clinical significance of signet ring cell rectal carcinoma. Int J Colorectal Dis, 2004, 19(2): 102-107.
53. Bittorf B, Merkel S, Matzel KE, et al. Primary signet-ring cell carcinoma of the colorectum. Langenbecks Arch Surg, 2004, 389(3): 178-183.
54. Thota R, Fang X, Subbiah S. Clinicopathological features and survival outcomes of primary signet ring cell and mucinous adenocarcinoma of colon: retrospective analysis of VACCR database. J Gastrointest Oncol, 2014, 5(1): 18-24.
55. Pande R, Sunga A, Levea C, et al. Significance of signet-ring cells in patients with colorectal cancer. Dis Colon Rectum, 2008, 51(1): 50-55.
56. Barresi V, Reggiani Bonetti L, Domati F, et al. Prognostic relevance of histopathological features in signet ring cell carcinoma of the colorectum. Virchows Arch, 2016, 469(3): 267-275.
57. Kong X, Zhang X, Huang Y, et al. Characteristics and prognostic factors of colorectal mucinous adenocarcinoma with signet ring cells. Cancer Manag Res, 2017, 9: 573-580.
58. Mora-Guzmán I, Di Martino M, Mu?oz de Nova JL, et al. Primary signet ring cell carcinoma of the colon: a rare condition with a poor prognosis. A report on two cases. Rev Gastroenterol Mex, 2017, [Epub ahead of print].
59. Song BR, Xiao CC, Wu ZK. Predictors of lymph node metastasis and prognosis in pT1 colorectal cancer patients with signet-ring cell and mucinous adenocarcinomas. Cell Physiol Biochem, 2017, 41(5): 1753-1765.
60. Gopalan V, Smith RA, Ho YH, et al. Signet-ring cell carcinoma of colorectum－current perspectives and molecular biology. Int J Colorectal Dis, 2011, 26(2): 127-133.
61. NCCN. Clinical Practice Guidelines in Oncology: rectal cancer. 2015-05-25. https://www.nccn.org/professionals/physician_gls/default.aspx.
62. 劉德寶, 徐忠法, 范開席. 晚期結直腸癌的治療策略. 國際腫瘤學雜志, 2016, 43(5): 387-390.
63. Tamhankar AS, Ingle P, Engineer R, et al. Signet ring colorectal carcinoma: do we need to improve the treatment algorithm? World J Gastrointest Oncol, 2016, 8(12): 819-825.

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Research advances of primary colorectal signet-ring cell carcinoma

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