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Published in: Discover Oncology 1/2021

Open Access 01-12-2021 | Colorectal Cancer | Review

Clinicopathological factors and survival outcomes of signet-ring cell and mucinous carcinoma versus adenocarcinoma of the colon and rectum: a systematic review and meta-analysis

Authors: Michael G. Fadel, George Malietzis, Vasilis Constantinides, Gianluca Pellino, Paris Tekkis, Christos Kontovounisios

Published in: Discover Oncology | Issue 1/2021

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Abstract

Background

Histological subtypes of colorectal cancer may be associated with varied prognostic features. This systematic review and meta-analysis aimed to compare clinicopathological characteristics, recurrence and overall survival between colorectal signet-ring cell (SC) and mucinous carcinoma (MC) to conventional adenocarcinoma (AC).

Methods

A literature search of MEDLINE, EMBASE, Ovid and Cochrane Library was performed for studies that reported data on clinicopathological and survival outcomes on SC and/or MC versus AC from January 1985 to May 2020. Meta-analysis was performed using random-effect models and between-study heterogeneity was assessed.

Results

Thirty studies of 1,087,055 patients were included: 11,510 (1.06%) with SC, 110,179 (10.13%) with MC and 965,366 (88.81%) with AC. Patients with SC were younger than patients with AC (WMD − 0.47; 95% CI − 0.84 to –0.10; I2 88.6%; p = 0.014) and more likely to have right-sided disease (OR 2.12; 95% CI 1.72–2.60; I2 82.9%; p < 0.001). Locoregional recurrence at 5 years was more frequent in patients with SC (OR 2.81; 95% CI 1.40–5.65; I2 0.0%; p = 0.004) and MC (OR 1.92; 95% CI 1.18–3.15; I2 74.0%; p = 0.009). 5-year overall survival was significantly reduced when comparing SC and MC to AC (HR 2.54; 95% CI 1.98–3.27; I2 99.1%; p < 0.001 and HR 1.38; 95% CI 1.19–1.61; I2 98.6%; p < 0.001, respectively).

Conclusion

SC and MC are associated with right-sided lesions, advanced stage at presentation, higher rates of recurrence and poorer overall survival. This has strong implications towards surgical and oncological management and surveillance of colorectal cancer.
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Literature
1.
2.
go back to reference Franzè E, Dinallo V, Rizzo A, et al. Interleukin-34 sustains pro-tumorigenic signals in colon cancer tissue. Oncotarget. 2018;9:3432–45.PubMed Franzè E, Dinallo V, Rizzo A, et al. Interleukin-34 sustains pro-tumorigenic signals in colon cancer tissue. Oncotarget. 2018;9:3432–45.PubMed
3.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.PubMed Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.PubMed
5.
go back to reference Brenner DR, Heer E, Sutherland RL, et al. National trends in colorectal cancer incidence among older and younger adults in Canada. JAMA Netw Open. 2019;2:e198090.PubMedPubMedCentral Brenner DR, Heer E, Sutherland RL, et al. National trends in colorectal cancer incidence among older and younger adults in Canada. JAMA Netw Open. 2019;2:e198090.PubMedPubMedCentral
6.
go back to reference Abualkhair WH, Zhou M, Ahnen D, et al. Trends in incidence of early-onset colorectal cancer in the United States among those approaching screening age. JAMA Netw Open. 2020;3:e1920407.PubMedPubMedCentral Abualkhair WH, Zhou M, Ahnen D, et al. Trends in incidence of early-onset colorectal cancer in the United States among those approaching screening age. JAMA Netw Open. 2020;3:e1920407.PubMedPubMedCentral
7.
go back to reference Davis DM, Marcet JE, Frattini JC, et al. Is it time to lower the recommended screening age for colorectal cancer? J Am Coll Surg. 2011;213:352.PubMed Davis DM, Marcet JE, Frattini JC, et al. Is it time to lower the recommended screening age for colorectal cancer? J Am Coll Surg. 2011;213:352.PubMed
8.
go back to reference Meester RGS, Mannalithara A, Lansdorp-Vogelaar I, Ladabaum U. Trends in incidence and stage at diagnosis of colorectal cancer in adults aged 40 through 49 years, 1975–2015. JAMA. 2019;321:1933.PubMedPubMedCentral Meester RGS, Mannalithara A, Lansdorp-Vogelaar I, Ladabaum U. Trends in incidence and stage at diagnosis of colorectal cancer in adults aged 40 through 49 years, 1975–2015. JAMA. 2019;321:1933.PubMedPubMedCentral
9.
go back to reference Siegel RL, Miller KD, Goding Sauer A, et al. Colorectal cancer statistics, 2020. CA Cancer J Clin. 2020;70:145.PubMed Siegel RL, Miller KD, Goding Sauer A, et al. Colorectal cancer statistics, 2020. CA Cancer J Clin. 2020;70:145.PubMed
10.
go back to reference Sheng H, Wei X, Mao M, et al. Adenocarcinoma with mixed subtypes is a rare but aggressive histologic subtype in colorectal cancer. BMC Cancer. 2019;19(1):1071.PubMedPubMedCentral Sheng H, Wei X, Mao M, et al. Adenocarcinoma with mixed subtypes is a rare but aggressive histologic subtype in colorectal cancer. BMC Cancer. 2019;19(1):1071.PubMedPubMedCentral
11.
go back to reference Nozoe T, Anai H, Nasu S, Sugimachi K. Clinicopathological characteristics of mucinous carcinoma of the colon and rectum. J Surg Oncol. 2000;75(2):103–7.PubMed Nozoe T, Anai H, Nasu S, Sugimachi K. Clinicopathological characteristics of mucinous carcinoma of the colon and rectum. J Surg Oncol. 2000;75(2):103–7.PubMed
12.
go back to reference Du W, Mah JTL, Lee J, Sankila R, Sankaranarayanan R, Chia KS. Incidence and survival of mucinous adenocarcinoma of the colorectum: a population-based study from an Asian country. Dis Colon Rectum. 2004;47(1):78–85.PubMed Du W, Mah JTL, Lee J, Sankila R, Sankaranarayanan R, Chia KS. Incidence and survival of mucinous adenocarcinoma of the colorectum: a population-based study from an Asian country. Dis Colon Rectum. 2004;47(1):78–85.PubMed
14.
go back to reference 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):294–8.PubMed 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):294–8.PubMed
15.
go back to reference Bӧrger ME, Gosens MJEM, Jeuken JWM, et al. Signet ring cell differentiation in mucinous colorectal carcinoma. J Pathol. 2007;212(3):278–86. Bӧrger ME, Gosens MJEM, Jeuken JWM, et al. Signet ring cell differentiation in mucinous colorectal carcinoma. J Pathol. 2007;212(3):278–86.
16.
go back to reference Giacchero A, Aste H, Baracchini P, et al. Primary signet-ring carcinoma of the large bowel. Report of nine cases. Cancer. 1985;56(11):2723–6.PubMed Giacchero A, Aste H, Baracchini P, et al. Primary signet-ring carcinoma of the large bowel. Report of nine cases. Cancer. 1985;56(11):2723–6.PubMed
17.
go back to reference Consorti F, Lorenzotti A, Midiri G, Di Paola M. Prognostic significance of mucinous carcinoma of colon and rectum: a prospective case-control study. J Surg Oncol. 2000;73(2):70–4.PubMed Consorti F, Lorenzotti A, Midiri G, Di Paola M. Prognostic significance of mucinous carcinoma of colon and rectum: a prospective case-control study. J Surg Oncol. 2000;73(2):70–4.PubMed
18.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG, Group P, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8(5):336–41.PubMed Moher D, Liberati A, Tetzlaff J, Altman DG, Group P, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8(5):336–41.PubMed
20.
go back to reference Hamilton S, Aaltonen LA, editors. Pathology and genetics of tumours of the digestive system, in WHO classification of tumours. Lyon: IARC; 2000. p. 104–9. Hamilton S, Aaltonen LA, editors. Pathology and genetics of tumours of the digestive system, in WHO classification of tumours. Lyon: IARC; 2000. p. 104–9.
21.
go back to reference Amin MB, Edge SB, Greene FL, et al. AJCC cancer staging manual. 8th ed. New York: Springer; 2017. Amin MB, Edge SB, Greene FL, et al. AJCC cancer staging manual. 8th ed. New York: Springer; 2017.
22.
go back to reference Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998;17(24):2815–34.PubMed Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998;17(24):2815–34.PubMed
24.
go back to reference Bittorf B, Merkel S, Matzel KE, Wein A, Dimmler A, Hohenberger W. Primary signet-ring cell carcinoma of the colorectum. Langenbecks Arch Surg. 2004;389(3):178–83.PubMed Bittorf B, Merkel S, Matzel KE, Wein A, Dimmler A, Hohenberger W. Primary signet-ring cell carcinoma of the colorectum. Langenbecks Arch Surg. 2004;389(3):178–83.PubMed
25.
go back to reference Chew MH, Yeo SAE, 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):1221–9.PubMed Chew MH, Yeo SAE, 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):1221–9.PubMed
26.
go back to reference Chen JS, Hsieh PS, Hung SY, et al. Clinical significance of signet ring cell rectal carcinoma. Int J Colorectal Dis. 2004;19(2):102–7.PubMed Chen JS, Hsieh PS, Hung SY, et al. Clinical significance of signet ring cell rectal carcinoma. Int J Colorectal Dis. 2004;19(2):102–7.PubMed
27.
go back to reference Chen JS, Hsieh PS, Chian JM, et al. Clinical outcome of signet ring cell carcinoma and mucinous adenocarcinoma of the colon. Chang Gung Med J. 2010;33(1):51–7.PubMed Chen JS, Hsieh PS, Chian JM, et al. Clinical outcome of signet ring cell carcinoma and mucinous adenocarcinoma of the colon. Chang Gung Med J. 2010;33(1):51–7.PubMed
28.
go back to reference Connelly JH, Robey-Cafferty SS, Cleary KR. Mucinous carcinomas of the colon and rectum. An analysis of 62 stage B and C lesions. Arch Pathol Lab Med. 1991;115(10):1022–5.PubMed Connelly JH, Robey-Cafferty SS, Cleary KR. Mucinous carcinomas of the colon and rectum. An analysis of 62 stage B and C lesions. Arch Pathol Lab Med. 1991;115(10):1022–5.PubMed
29.
go back to reference Enriquez JM, Díez M, Tobaruela E, et al. Clinical, histopathological, cytogenetic and prognostic differences between mucinous and nonmucinous colorectal adenocarcinomas. Rev Esp Enferm Dig. 1998;90(8):563–772.PubMed Enriquez JM, Díez M, Tobaruela E, et al. Clinical, histopathological, cytogenetic and prognostic differences between mucinous and nonmucinous colorectal adenocarcinomas. Rev Esp Enferm Dig. 1998;90(8):563–772.PubMed
30.
go back to reference Green JB, Timmcke AE, Mitchell WT, Hicks TC, Gathright JB Jr, Ray JE. Mucinous carcinoma–just another colon cancer? Dis Colon Rectum. 1993;36(1):49–54.PubMed Green JB, Timmcke AE, Mitchell WT, Hicks TC, Gathright JB Jr, Ray JE. Mucinous carcinoma–just another colon cancer? Dis Colon Rectum. 1993;36(1):49–54.PubMed
31.
go back to reference 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):333–9.PubMed 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):333–9.PubMed
32.
go back to reference 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):2814–21.PubMedPubMedCentral 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):2814–21.PubMedPubMedCentral
33.
go back to reference Kanemitsu Y, Kato T, Hirai T, et al. Survival after curative resection for mucinous adenocarcinoma of the colorectum. Dis Colon Rectum. 2003;46(2):160–7.PubMed Kanemitsu Y, Kato T, Hirai T, et al. Survival after curative resection for mucinous adenocarcinoma of the colorectum. Dis Colon Rectum. 2003;46(2):160–7.PubMed
34.
go back to reference Kang H, O’Connell JB, Maggard MA, Sack J, Ko CY. A 10-year outcomes evaluation of mucinous and signet-ring cell carcinoma of the colon and rectum. Dis Colon Rectum. 2005;48(6):1161–8.PubMed Kang H, O’Connell JB, Maggard MA, Sack J, Ko CY. A 10-year outcomes evaluation of mucinous and signet-ring cell carcinoma of the colon and rectum. Dis Colon Rectum. 2005;48(6):1161–8.PubMed
35.
go back to reference 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):332–8.PubMedPubMedCentral 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):332–8.PubMedPubMedCentral
36.
go back to reference Leopoldo S, Lorena B, Cinzia A, et al. Two subtypes of mucinous adenocarcinoma of the colorectum: clinicopathological and genetic features. Ann Surg Oncol. 2008;15(5):1429–39.PubMed Leopoldo S, Lorena B, Cinzia A, et al. Two subtypes of mucinous adenocarcinoma of the colorectum: clinicopathological and genetic features. Ann Surg Oncol. 2008;15(5):1429–39.PubMed
37.
go back to reference Min BS, Kim NK, Ko YT. Clinicopathological features of signet-ring cell carcinoma of the colon and rectum: a case-matched study. Hepatogastroenterology. 2009;56(93):984–8.PubMed Min BS, Kim NK, Ko YT. Clinicopathological features of signet-ring cell carcinoma of the colon and rectum: a case-matched study. Hepatogastroenterology. 2009;56(93):984–8.PubMed
38.
go back to reference Minsky BD, Mies C, Rich TA, Recht A, Chaffey JT. Colloid carcinoma of the colon and rectum. Cancer. 1987;60(12):3103–12.PubMed Minsky BD, Mies C, Rich TA, Recht A, Chaffey JT. Colloid carcinoma of the colon and rectum. Cancer. 1987;60(12):3103–12.PubMed
39.
go back to reference Mizushima T, Nomura M, Fujii M. Primary colorectal signet-ring cell carcinoma: clinicopathological features and postoperative survival. Surg Today. 2010;40(3):234–8.PubMed Mizushima T, Nomura M, Fujii M. Primary colorectal signet-ring cell carcinoma: clinicopathological features and postoperative survival. Surg Today. 2010;40(3):234–8.PubMed
40.
go back to reference Nissan A, Guillem JG, Paty PB, Wong WD, Cohen AM. Signet-ring cell carcinoma of the colon and rectum: a matched control study. Dis Colon Rectum. 1999;42(9):1176–80.PubMed Nissan A, Guillem JG, Paty PB, Wong WD, Cohen AM. Signet-ring cell carcinoma of the colon and rectum: a matched control study. Dis Colon Rectum. 1999;42(9):1176–80.PubMed
41.
go back to reference Psathakis D, Schiedeck TH, Krug F, Oovermann E, Kujath P, Bruch HP. Ordinary colorectal adenocarcinoma vs. primary colorectal signet-ring cell carcinoma: study matched for age, gender, grade, and stage. Dis Colon Rectum. 1999;42(12):1618–25.PubMed Psathakis D, Schiedeck TH, Krug F, Oovermann E, Kujath P, Bruch HP. Ordinary colorectal adenocarcinoma vs. primary colorectal signet-ring cell carcinoma: study matched for age, gender, grade, and stage. Dis Colon Rectum. 1999;42(12):1618–25.PubMed
42.
go back to reference Razenberg LGEM, van Gestel YRBM, Lemmens VEPP, de Wilt JHW, Creemers GJ, Hingh IHJT. The prognostic relevance of histological subtype in patients with peritoneal metastases from colorectal cancer: a nationwide population-based study. Clinic Colorectal Cancer. 2015;14(4):e13–9. Razenberg LGEM, van Gestel YRBM, Lemmens VEPP, de Wilt JHW, Creemers GJ, Hingh IHJT. The prognostic relevance of histological subtype in patients with peritoneal metastases from colorectal cancer: a nationwide population-based study. Clinic Colorectal Cancer. 2015;14(4):e13–9.
43.
go back to reference Secco GB, Fardelli R, Campora E, et al. Primary mucinous adenocarcinomas and signet-ring cell carcinomas of colon and rectum. Oncology. 1994;51(1):30–4.PubMed Secco GB, Fardelli R, Campora E, et al. Primary mucinous adenocarcinomas and signet-ring cell carcinomas of colon and rectum. Oncology. 1994;51(1):30–4.PubMed
44.
go back to reference Song W, Wu S, He Y, 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. 2009;122(13):1486–91.PubMed Song W, Wu S, He Y, 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. 2009;122(13):1486–91.PubMed
45.
go back to reference 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):1753–65.PubMed 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):1753–65.PubMed
46.
go back to reference Umpleby HC, Ranson DL, Williamson RC. Peculiarities of mucinous colorectal carcinoma. Br J Surg. 1985;72(9):715–8.PubMed Umpleby HC, Ranson DL, Williamson RC. Peculiarities of mucinous colorectal carcinoma. Br J Surg. 1985;72(9):715–8.PubMed
47.
go back to reference Wu X, Lin H, Shaotang L. Prognoses of different pathological subtypes of colorectal cancer at different stages: a population-based retrospective cohort study. BMC Gastroenterol. 2019;19(1):164.PubMedPubMedCentral Wu X, Lin H, Shaotang L. Prognoses of different pathological subtypes of colorectal cancer at different stages: a population-based retrospective cohort study. BMC Gastroenterol. 2019;19(1):164.PubMedPubMedCentral
48.
go back to reference Yamamoto S, Mochizuki H, Hase K, et al. Assessment of clinicopathologic features of colorectal mucinous adenocarcinoma. Am J Surg. 1993;166(3):257–61.PubMed Yamamoto S, Mochizuki H, Hase K, et al. Assessment of clinicopathologic features of colorectal mucinous adenocarcinoma. Am J Surg. 1993;166(3):257–61.PubMed
49.
go back to reference Yun SO, Cho YB, Lee WY, et al. Clinical significance of signet-ring-cell colorectal cancer as a prognostic factor. Ann Coloproctol. 2017;33(6):232–8.PubMedPubMedCentral Yun SO, Cho YB, Lee WY, et al. Clinical significance of signet-ring-cell colorectal cancer as a prognostic factor. Ann Coloproctol. 2017;33(6):232–8.PubMedPubMedCentral
50.
go back to reference Luzietti E, Pellino G, Nikolaou S, et al. Comparison of guidelines for the management of rectal cancer. BJS Open. 2018;2(6):433–51.PubMedPubMedCentral Luzietti E, Pellino G, Nikolaou S, et al. Comparison of guidelines for the management of rectal cancer. BJS Open. 2018;2(6):433–51.PubMedPubMedCentral
51.
go back to reference Pellino G, Warren O, Mills S, Rasheed S, Tekkis PP, Kontovounisios C. Comparison of western and Asian guidelines concerning the management of colon cancer. Dis Colon Rectum. 2018;61(2):250–9.PubMed Pellino G, Warren O, Mills S, Rasheed S, Tekkis PP, Kontovounisios C. Comparison of western and Asian guidelines concerning the management of colon cancer. Dis Colon Rectum. 2018;61(2):250–9.PubMed
52.
go back to reference De Simone V, Ronchetti G, Franzè E, et al. Interleukin-21 sustains inflammatory signals that contribute to sporadic colon tumorigenesis. Oncotarget. 2015;6(12):9908–23.PubMedPubMedCentral De Simone V, Ronchetti G, Franzè E, et al. Interleukin-21 sustains inflammatory signals that contribute to sporadic colon tumorigenesis. Oncotarget. 2015;6(12):9908–23.PubMedPubMedCentral
53.
go back to reference Nigam AK, Savage FJ, Boulos PB, Stamp GW, Liu D, Pignatelli M. Loss of cell-cell and cell-matrix adhesion molecules in colorectal cancer. Br J Cancer. 1993;68(3):507–14.PubMedPubMedCentral Nigam AK, Savage FJ, Boulos PB, Stamp GW, Liu D, Pignatelli M. Loss of cell-cell and cell-matrix adhesion molecules in colorectal cancer. Br J Cancer. 1993;68(3):507–14.PubMedPubMedCentral
54.
go back to reference Becker KF, Atkinson MJ, Reich U, et al. E-cadherin gene mutations provide clues to diffuse type gastric carcinomas. Cancer Res. 1994;54(14):3845–52.PubMed Becker KF, Atkinson MJ, Reich U, et al. E-cadherin gene mutations provide clues to diffuse type gastric carcinomas. Cancer Res. 1994;54(14):3845–52.PubMed
55.
go back to reference Shino Y, Watanabe A, Yamada Y, et al. Clinicopathologic evaluation of immunohistochemical E-cadherin expression in human gastric carcinomas. Cancer. 1995;76(11):2193–201.PubMed Shino Y, Watanabe A, Yamada Y, et al. Clinicopathologic evaluation of immunohistochemical E-cadherin expression in human gastric carcinomas. Cancer. 1995;76(11):2193–201.PubMed
56.
go back to reference Kim HC, Kim HJ, Kim JC. Reduced E-cadherin expression as a cause of distinctive signet-ring cell variant in colorectal carcinoma. J Korean Med Sci. 2002;17(1):23–8.PubMedPubMedCentral Kim HC, Kim HJ, Kim JC. Reduced E-cadherin expression as a cause of distinctive signet-ring cell variant in colorectal carcinoma. J Korean Med Sci. 2002;17(1):23–8.PubMedPubMedCentral
57.
go back to reference Céspedes MV, Larriba MJ, Pavón MA, et al. Site-dependent E-cadherin cleavage and nuclear translocation in a metastatic colorectal cancer model. Am J Pathol. 2010;177(4):2067–79.PubMedPubMedCentral Céspedes MV, Larriba MJ, Pavón MA, et al. Site-dependent E-cadherin cleavage and nuclear translocation in a metastatic colorectal cancer model. Am J Pathol. 2010;177(4):2067–79.PubMedPubMedCentral
58.
go back to reference Efstathiou JA, Liu D, Wheeler JM, et al. Mutated epithelial cadherin is associated with increased tumorigenicity and loss of adhesion and of responsiveness to the motogenic trefoil factor 2 in colon carcinoma cells. Proc Natl Acad Sci USA. 1999;96(5):2316.PubMedPubMedCentral Efstathiou JA, Liu D, Wheeler JM, et al. Mutated epithelial cadherin is associated with increased tumorigenicity and loss of adhesion and of responsiveness to the motogenic trefoil factor 2 in colon carcinoma cells. Proc Natl Acad Sci USA. 1999;96(5):2316.PubMedPubMedCentral
59.
go back to reference Efstathiou JA, Noda M, Rowan A, et al. Intestinal trefoil factor controls the expression of the adenomatous polyposis coli-catenin and the E-cadherin-catenin complexes in human colon carcinoma cells. Proc Natl Acad Sci USA. 1998;95(6):3122–317.PubMedPubMedCentral Efstathiou JA, Noda M, Rowan A, et al. Intestinal trefoil factor controls the expression of the adenomatous polyposis coli-catenin and the E-cadherin-catenin complexes in human colon carcinoma cells. Proc Natl Acad Sci USA. 1998;95(6):3122–317.PubMedPubMedCentral
60.
go back to reference Sugarbaker PH. Mucinous colorectal carcinoma. J Surg Oncol. 2001;77(4):282–3.PubMed Sugarbaker PH. Mucinous colorectal carcinoma. J Surg Oncol. 2001;77(4):282–3.PubMed
61.
go back to reference Benedix F, Kube R, Meyer F, et al. Comparison of 17,641 patients with right- and left-sided colon cancer: differences in epidemiology, perioperative course, histology, and survival. Dis Colon Rectum. 2010;53(1):57–64.PubMed Benedix F, Kube R, Meyer F, et al. Comparison of 17,641 patients with right- and left-sided colon cancer: differences in epidemiology, perioperative course, histology, and survival. Dis Colon Rectum. 2010;53(1):57–64.PubMed
62.
go back to reference Benedix F, Meyer F, Kube Gastinger I, Lippert H. Right- and left-sided colonic cancer - different tumour entities. Zentralbl Chir. 2010;135(4):312–7.PubMed Benedix F, Meyer F, Kube Gastinger I, Lippert H. Right- and left-sided colonic cancer - different tumour entities. Zentralbl Chir. 2010;135(4):312–7.PubMed
63.
go back to reference Meguid RA, Slidell MB, Wolfgang CL, Chang DC, Ahuja N. Is there a difference in survival between right- versus left-sided colon cancers? Ann Surg Oncol. 2008;15(9):2388–94.PubMedPubMedCentral Meguid RA, Slidell MB, Wolfgang CL, Chang DC, Ahuja N. Is there a difference in survival between right- versus left-sided colon cancers? Ann Surg Oncol. 2008;15(9):2388–94.PubMedPubMedCentral
64.
go back to reference Wray CM, Ziogas A, Hinojoas W, Le H, Stamos MJ, Zell JA. Tumor subsite location within the colon is prognostic for survival after colon cancer diagnosis. Dis Colon Rectum. 2009;52(8):1359–66.PubMed Wray CM, Ziogas A, Hinojoas W, Le H, Stamos MJ, Zell JA. Tumor subsite location within the colon is prognostic for survival after colon cancer diagnosis. Dis Colon Rectum. 2009;52(8):1359–66.PubMed
Metadata
Title
Clinicopathological factors and survival outcomes of signet-ring cell and mucinous carcinoma versus adenocarcinoma of the colon and rectum: a systematic review and meta-analysis
Authors
Michael G. Fadel
George Malietzis
Vasilis Constantinides
Gianluca Pellino
Paris Tekkis
Christos Kontovounisios
Publication date
01-12-2021
Publisher
Springer US
Published in
Discover Oncology / Issue 1/2021
Print ISSN: 1868-8497
Electronic ISSN: 2730-6011
DOI
https://doi.org/10.1007/s12672-021-00398-6

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