Colorectal Cancer Survival in 50- to 69-Year-Olds after Introducing the Faecal Immunochemical Test

María Angeles Gutierrez-Stampa, Vanessa Aguilar, Cristina Sarasqueta, Joaquín Cubiella, Isabel Portillo, Luis Bujanda, María Angeles Gutierrez-Stampa, Vanessa Aguilar, Cristina Sarasqueta, Joaquín Cubiella, Isabel Portillo, Luis Bujanda

Abstract

Population screening has improved early diagnosis of colorectal cancer (CRC). Nonetheless, most cases are diagnosed in symptomatic patients. Faecal immunochemical testing has been recommended for assessing patients with lower gastrointestinal symptoms, but whether it improves patient survival is unknown. Our objective was to compare CRC survival in 50- to 69-year-olds between asymptomatic screen-detected patients and symptomatic patients by route to diagnosis.

Methods: We identified all cases of CRC diagnosed in 50-to 69-year-olds between 2009 and 2016, in Donostialdea (Gipuzkoa, Spain). Three groups were created: 1-screen-detected CRC; 2-CRC detected in symptomatic patients after a positive faecal immunochemical test(FIT); and 3-CRC detected in symptomatic patients without a FIT or after a negative result. We analysed survival using the Kaplan-Meier method and log-rank tests.

Results: Of 930 patients diagnosed with CRC, 433 cases were detected through screening and 497 in symptomatic patients, 7.9% after a positive FIT and 45.5% by other means. The 3-year CRC survival was significantly lower in group 3 (69.5%) than groups 1 (93%; p = 0.007) or 2 (87.5%; p = 0.02). The risk of death was lower in groups 1 (HR 0.42, 95% CI 0.30-0.58) and 2 (HR 0.51; 95% CI 0.29-0.87).

Conclusion: Half of CRC cases in 50- to 69-year-olds are diagnosed outside screening. Use of the FIT as a diagnostic strategy in symptomatic patients may improve survival.

Keywords: colorectal cancer; faecal immunochemical test; survival.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Flow diagram showing route to diagnosis of colorectal cancer (CRC) in groups 1, 2 and 3.
Figure 2
Figure 2
Kaplan-Meier overall survival curves by group. (Group 1: screen-detected CRC; Group 2: symptomatic patients with positive faecal immunochemical test results in the previous 12 months; Group 3: symptomatic patients who did not undergo faecal immunochemical testing or had a negative FIT result).

References

    1. GLOBOCAN Global Cancer Observatory. [(accessed on 20 February 2019)];Cancer Today [Internet] Available online:
    1. Zorzi M., Fedeli U., Schievano E., Bovo E., Guzzinati S., Baracco S., Fedato C., Saugo M., Dei Tos A.P. Impact on colorectal cancer mortality of screening programmes based on the faecal immunochemical test. Gut. 2015;64:784–790. doi: 10.1136/gutjnl-2014-307508.
    1. Idigoras I., Arrospide A., Portillo I., Arana-Arri E., Martínez-Indart L., Mar J., de Koning H.J., Lastra R., Soto-Gordoa M., van der Meulen M., et al. Evaluation of the colorectal cancer screening Programme in the Basque Country (Spain) and its effectiveness based on the Miscan-colon model. BMC Public Health. 2017;18:189. doi: 10.1186/s12889-017-4639-3.
    1. Elmunzer B.J., Singal A.G., Sussman J.B., Deshpande A.R., Sussman D.A., Conte M.L., Dwamena B.A., Rogers M.A.M., Schoenfeld P.S., Inadomi J.M., et al. Comparing the effectiveness of competing tests for reducing colorectal cancer mortality: A network meta-analysis. Gastroint. Endosc. 2015;81:700–709. doi: 10.1016/j.gie.2014.10.033.
    1. Council of the European Union Council Recommendation of 2 December 2003 on cancer screening (2003/878/EC) Off. J. Eur. Union. 2003;L327:34–38.
    1. Cancer Strategy of the Spanish National Health System 2009. Ministry of Health, Social Services and Equality; Madrid, Spain: 2009. [(accessed on 4 April 2020)]. Available online: .
    1. Mansouri D., McMillan D.C., Crearie C., Morrison D.S., Crighton E.M., Horgan P.G. Temporal trends in mode, site and stage of presentation with the introduction of colorectal cancer screening: A decade of experience from the West of Scotland. Br. J. Cancer. 2015;113:556–561. doi: 10.1038/bjc.2015.230.
    1. Morris E.J.A., Whitehouse L.E., Farrell T., Nickerson C., Thomas J.D., Quirke P., Rutter M.D., Rees C., Finan P.J., Wilkinson J.R., et al. A retrospective observational study examining the characteristics and outcomes of tumours diagnosed within and without of the English NHS Bowel Cancer Screening Programme. Br. J. Cancer. 2012;107:757–764. doi: 10.1038/bjc.2012.331.
    1. Pin Vieito N., Zarraquiños S., Cubiella J. High-risk symptoms and quantitative faecal immunochemical test accuracy: Systematic review and meta-analysis. World J. Gastroenterol. 2019;25:2383–2401. doi: 10.3748/wjg.v25.i19.2383.
    1. Westwood M., Lang S., Armstrong N., van Turenhout S., Cubiella J., Stirk L., Ramos I.C., Luyendijk M., Zaim R., Kleijnen J., et al. Faecal immunochemical tests (FIT) can help to rule out colorectal cancer in patients presenting in primary care with lower abdominal symptoms: A systematic review conducted to inform new NICE DG30 diagnostic guidance. BMC Med. 2017;15:189. doi: 10.1186/s12916-017-0944-z.
    1. Katsoula A., Paschos P., Haidich A.B., Tsapas A., Giouleme O. Diagnostic accuracy of fecal immunochemical test in patients at increased risk for colorectal cancer: A meta-analysis. JAMA Intern. Med. 2017;177:1110–1118. doi: 10.1001/jamainternmed.2017.2309.
    1. Stonestreet J., Chandrapalan S., Woolley D., Uthman U., Arasaradnam R.P. Systematic review and meta-analysis: Diagnostic accuracy of faecal immunochemical testing for haemoglobin (FIT) in detecting colorectal cancer for both symptomatic and screening population. Acta Gastroenterol. Belg. 2019;82:291–299.
    1. Cubiella J., Salve M., Díaz-Ondina M., Vega P., Alves M.T., Iglesias F., Sánchez E., Macía P., Blanco I., Bujanda L., et al. Diagnostic accuracy of the faecal immunochemical test for colorectal cancer in symptomatic patients: Comparison with NICE and SIGN referral criteria. Colorectal Dis. 2014;16:273–282. doi: 10.1111/codi.12569.
    1. Meklin J., SyrjÄnen K., Eskelinen M. Fecal Occult Blood Tests in Colorectal Cancer Screening: Systematic Review and Meta-analysis of Traditional and New-generation Fecal Immunochemical Tests. Anticancer Res. 2020;40:3591–3604. doi: 10.21873/anticanres.14349.
    1. Cubiella J., Marzo-Castillejo M., Mascort-Roca J.J., Amador-Romero F.J., Bellas-Beceiro B., Clofent-Vilaplana J., Carballal S., Ferrándiz-Santos J., Gimeno-García A.Z., Jover R., et al. Clinical practice guideline. Diagnosis and prevention of colorectal cancer. 2018 Update. Gastroenterol. Hepatol. 2018;41:585–596. doi: 10.1016/j.gastrohep.2018.07.012.
    1. National Institute for Health and Care Excellence (NICE) Quantitative Faecal Immunochemical Tests to Guide Referral for Colorectal Cancer in Primary Care. Diagnostics Guidance DG30. [(accessed on 20 February 2019)];2017 Available online: .
    1. Gutierrez-Stampa M.A., Aguilar V., Sarasqueta C., Cubiella J., Portillo I., Bujanda L. Impact of the faecal immunochemical test on colorectal cancer survival. BMC Cancer. 2020;20:616. doi: 10.1186/s12885-020-07074-y.
    1. Mosquera I., Mendizabal N., Martín U., Bacigalupe A., Aldasoro E., Portillo I. Inequalities in participation in colorectal cancer screening programmes: A systematic review. Eur. J. Public Health. 2020;30:558–567. doi: 10.1093/eurpub/ckz236.
    1. Portillo I., Arana-Arri E., Gutiérrez-Ibarluzea I., Bilbao I., Luis Hurtado J., Sarasqueta C., Idigoras I., Bujanda L., Hurtado J.L., de No C., et al. Factors related to the participation and detection of lesions in colorectal cancer screening programme-based faecal immunochemical test. Eur. J. Public Health. 2018;28:1143–1148. doi: 10.1093/eurpub/cky109.
    1. Portillo I., Idígoras I., Ojembarrena E., Arana-Arri E., Zubero M.B., Pijoán J.I., López Urrutia A., Marqués M.L. [Main results of the colorectal cancer screening program in the Basque Country (Spain)] Gac. Sanit. 2013;27:358–361. doi: 10.1016/j.gaceta.2012.12.013.
    1. Clarke N., Sharp L., Osborne A., Kearney P.M. Comparison of Uptake of Colorectal Cancer Screening Based on Fecal Immunochemical Testing (FIT) in Males and Females: A Systematic Review and Meta-analysis. Cancer Epidemiol. Biomarkers Prev. 2015;24:39–47. doi: 10.1158/1055-9965.EPI-14-0774.
    1. Frederiksen B.L., Jørgensen T., Brasso K., Holten I., Osler M. Socioeconomic position and participation in colorectal cancer screening. Br. J. Cancer. 2010;103:1496–1501. doi: 10.1038/sj.bjc.6605962.
    1. Hurtado J.L., Bacigalupe A., Calvo M., Esnaola S., Mendizabal N., Portillo I., Idigoras I., Millán E., Arana-Arri E. Social inequalities in a population based colorectal cancer screening programme in the Basque Country. BMC Public Health. 2015;15 doi: 10.1186/s12889-015-2370-5.
    1. Von Wagner C., Baio G., Raine R., Snowball J., Morris S., Atkin W., Obichere A., Handley G., Logan R.F., Rainbow S., et al. Inequalities in participation in an organized national colorectal cancer screening programme: Results from the first 2.6 million invitations in England. Int. J. Epidemiol. 2011;40:712–718. doi: 10.1093/ije/dyr008.
    1. European Colorectal Cancer Screening Guidelines Working Group. von Karsa L., Patnick J., Segnan N., Atkin W., Halloran S., Lansdorp-Vogelaar I., Malila N., Minozzi S., Moss S., et al. European guidelines for quality assurance in colorectal cancer screening and diagnosis: Overview and introduction to the full supplement publication. Endoscopy. 2013;45:51–59. doi: 10.1055/s-0032-1325997.
    1. Borowski D.W., Cawkwell S., Zaidi S.M.A., Toward M., Maguire N., Garg D.K., Gill T.S. The NHS Bowel cancer screening programme achieves the anticipated survival improvement, but participation must be improved. Int. J. Health Care Qual. Assur. 2018;31:106–115. doi: 10.1108/IJHCQA-11-2016-0169.
    1. Idigoras Rubio I., Arana-Arri E., Portillo Villares I., Bilbao Iturribarrria I., Martínez-Indart L., Imaz-Ayo N., de la Cruz M., de Castro V., López de Munain A., Torrejón Perez I., et al. Participation in a population-based screening for colorectal cancer using the faecal immunochemical test decreases mortality in 5 years. Eur. J. Gastroenterol. Hepatol. 2019;31:197–204. doi: 10.1097/MEG.0000000000001338.
    1. Chiu H.-M., Chen S.L.-S., Yen A.M.-F., Chiu S.Y.-H., Fann J.C.-Y., Lee Y.-C., Pan S.-L., Wu M.-S., Liao C.-S., Chen H.-H., et al. Effectiveness of fecal immunochemical testing in reducing colorectal cancer mortality from the One Million Taiwanese Screening Program. Cancer. 2015;121:3221–3229. doi: 10.1002/cncr.29462.
    1. Gini A., Jansen E.E.L., Zielonke N., Meester R.G.S., Senore C., Anttila A., Segnan N., Mlakar D.N., de Koning H.J., Lansdorp-Vogelaar I., et al. Impact of colorectal cancer screening on cancer-specific mortality in Europe: A systematic review. Eur. J. Cancer. 2020 doi: 10.1016/j.ejca.2019.12.014.
    1. Rossi P.G., Vicentini M., Sacchettini C., Di Felice E., Caroli S., Ferrari F., Mangone L., Pezzarossi A., Roncaglia F., Campari C., et al. Impact of Screening Program on Incidence of Colorectal Cancer: A Cohort Study in Italy. Am. J. Gastroenterol. 2015;110:1359–1366. doi: 10.1038/ajg.2015.240.
    1. Ventura L., Mantellini P., Grazzini G., Castiglione G., Buzzoni C., Rubeca T., Sacchettini C., Paci E., Zappa M. The impact of immunochemical faecal occult blood testing on colorectal cancer incidence. Dig. Liver Dis. 2014;46:82–86. doi: 10.1016/j.dld.2013.07.017.
    1. Parente F., Vailati C., Boemo C., Bonoldi E., Ardizzoia A., Ilardo A., Tortorella F., Cereda D., Cremaschini M., Moretti R. Improved 5-year survival of patients with immunochemical faecal blood test-screen-detected colorectal cancer versus non-screening cancers in northern Italy. Dig. Liver Dis. 2015;47:68–72. doi: 10.1016/j.dld.2014.09.015.
    1. Van der Vlugt M., Grobbee E.J., Bossuyt P.M.M., Bos A., Bongers E., Spijker W., Kuipers E.J., Lansdorp-Vogelaar I., Spaander M.C.W., Dekker E. Interval Colorectal Cancer Incidence Among Subjects Undergoing Multiple Rounds of Fecal Immunochemical Testing. Gastroenterology. 2017;153:439–447. doi: 10.1053/j.gastro.2017.05.004.
    1. Gill M.D., Bramble M.G., Hull M.A., Mills S.J., Morris E., Bradburn D.M., Bury Y., Parker C.E., Lee T.J.W., Rees C.J. Screen-detected colorectal cancers are associated with an improved outcome compared with stage-matched interval cancers. Br. J. Cancer. 2014;111:2076–2081. doi: 10.1038/bjc.2014.498.
    1. Domènech X., Garcia M., Benito L., Binefa G., Vidal C., Milà N., Moreno V. Cánceres de intervalo y sensibilidad de los programas poblacionales de cribado de cáncer colorrectal. Gac Sanit. 2015;29:464–471. doi: 10.1016/j.gaceta.2015.07.002.
    1. Gingold-Belfer R., Leibovitzh H., Boltin D., Issa N., Tsadok Perets T., Dickman R., Niv Y. The compliance rate for the second diagnostic evaluation after a positive fecal occult blood test: A systematic review and meta-analysis. United Eur. Gastroenterol. J. 2019;7:424–448. doi: 10.1177/2050640619828185.
    1. Lee Y.-C., Fann J.C.-Y., Chiang T.-H., Chuang S.-L., Chen S.L.-S., Chiu H.-M., Yen A.M.-F., Chiu S.Y.-H., Hsu C.-Y., Hsu W.-F., et al. Time to Colonoscopy and Risk of Colorectal Cancer in Patients With Positive Results From Fecal Immunochemical Tests. Clin. Gastroenterol. Hepatol. 2019;17:1332–1340. doi: 10.1016/j.cgh.2018.10.041.
    1. Corley D.A., Jensen C.D., Quinn V.P., Doubeni C.A., Zauber A.G., Lee J.K., Schottinger J.E., Marks A.R., Zhao W.K., Ghai N.R., et al. Association Between Time to Colonoscopy After a Positive Fecal Test Result and Risk of Colorectal Cancer and Cancer Stage at Diagnosis. JAMA. 2017;317:1631. doi: 10.1001/jama.2017.3634.
    1. Meester R.G.S., Zauber A.G., Doubeni C.A., Jensen C.D., Quinn V.P., Helfand M., Dominitz J.A., Levin T.R., Corley D.A., Lansdorp-Vogelaar I. Consequences of Increasing Time to Colonoscopy Examination After Positive Result From Fecal Colorectal Cancer Screening Test. Clin. Gastroenterol. Hepatol. 2016;14:1445–1451. doi: 10.1016/j.cgh.2016.05.017.
    1. Benedict M., Galvao Neto A., Zhang X. Interval colorectal carcinoma: An unsolved debate. World J. Gastroenterol. 2015;21:12735–12741. doi: 10.3748/wjg.v21.i45.12735.
    1. Brierley J.D., Gospodarowicz M.K., Wittekind C., editors. TNM Classification of Malignant Tumours. 8th ed. Wiley-Blackwell; West Sussex, UK: 2017.

Source: PubMed

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