Advertisement
Review Article| Volume 55, ISSUE 3, P336-341, March 2023

Impact of colorectal cancer screening on incidence, mortality and surgery rates: Evidences from programs based on the fecal immunochemical test in Italy

Published:August 20, 2022DOI:https://doi.org/10.1016/j.dld.2022.08.013

      Abstract

      Fecal immunochemical tests (FIT) are among the most commonly used tests for colorectal cancer (CRC) screening programs worldwide. However, no randomised controlled trials have been carried out evaluating the impact of FIT-based screening programs (FIT-progr) on CRC incidence and mortality rates. Italian FIT-progr represent one of the most widespread and established experience worldwide. This paper reviews the evidence on the impact of FIT-progr on CRC incidence, tumor stage at diagnosis, mortality and surgery rates, deriving from Italian routine programs, i.e., outside the research setting. Unfortunately, the application of FIT-progr in Italy can be considered as an unplanned experimental model, due to the differences between Regions, both in health system management and adherence of the target population to the screening programs. The analysis of the manuscripts considered in the review, confirms that FIT-progr are effective in reducing CRC incidence and mortality rates and in improving the rate of endoscopic treatment of early invasive lesions. The review also highlights that FIT-progr are less performing for proximal colon than for distal colon and rectum.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Digestive and Liver Disease
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bray F.
        • Ferlay J.
        • Soerjomataram I.
        • et al.
        Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
        CA Cancer J Clin. 2018; 68: 394-424
        • Hewitson P.
        • Glasziou P.
        • Irwig L.
        • et al.
        Screening for colorectal cancer using the faecal occult blood test.
        Cochrane Database Syst Rev. 2007; 24CD001216
        • Atkin W.S.
        • Edwards R.
        • Kralj-Hans I.
        • et al.
        Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomized controlled trial.
        Lancet. 2010; 375: 1624-1633
        • Holme Ø.
        • Løberg M.
        • Kalager M.
        • et al.
        Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial.
        JAMA. 2014; 312: 606-615
        • Schoen R.E.
        • Pinsky P.F.
        • Weissfeld J.L.
        • et al.
        Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy.
        N Engl J Med. 2012; 366: 2345-2357
        • Segnan N.
        • Armaroli P.
        • Bonelli L.
        • et al.
        Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian randomized controlled trial-SCORE.
        J Natl Cancer Inst. 2011; 103: 1310-1322
        • Kaminski M.F.
        • Bretthauer M.
        • Zauber A.G.
        • et al.
        The NordICC study: rationale and design of a randomized trial on colonoscopy screening for colorectal cancer.
        Endoscopy. 2012; 444: 695-702
        • Quintero E.
        • Castells A.
        • Bujanda L.
        • et al.
        Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening.
        N Engl J Med. 2012; 366 (2012): 697-706
        • Randel K.R.
        • Schult A.L.
        • Botteri E.
        • et al.
        Colorectal cancer screening with repeated fecal immunochemical test versus sigmoidoscopy: baseline results from a randomized trial.
        Gastroenterology. 2021; 160: 1085-1096
        • Buskermolen M Cenin D.R.
        • Helsingen L.M.
        • et al.
        Colorectal cancer screening with faecal immunochemical testing, sigmoidoscopy or colonoscopy: a microsimulation modelling study.
        BMJ. 2019; 367: l5383
        • Brenner H.
        • Tao S.
        Superior diagnostic performance of faecal immunochemical tests for haemoglobin in a head-to-head comparison with guaiac based faecal occult blood test among 2235 participants of screening colonoscopy.
        Eur J Cancer. 2013; 49: 3049-3054
        • Dancourt V.
        • Lejeune C.
        • Lepage C.
        • et al.
        Immunochemical faecal occult blood tests are superior to guaiac-based tests for the detection of colorectal neoplasms.
        Eur J Cancer. 2008; 44: 2254-2258
        • Hassan C.
        • Giorgi Rossi P.
        • Camilloni L.
        • et al.
        Meta-analysis: adherence to colorectal cancer screening and the detection rate for advanced neoplasia, according to the type of screening test.
        Aliment Pharmacol Ther. 2012; 36: 929-940
        • Hol L.
        • van Leerdam M.E.
        • van Ballegooijen M.
        • et al.
        Screening for colorectal cancer: randomised trial comparing guaiac-based and immunochemical faecal occult blood testing and flexible sigmoidoscopy.
        Gut. 2010; 59: 62-68
        • Segnan N.
        • Patnick J.
        • von Karsa L.
        European guidelines for quality assurance in colorectal cancer screening and diagnosis.
        1st ed. Publications Office of the European Union, Luxembourg2010
        • von Karsa L.
        • Patnick J.
        • Segnan N.
        • 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
        • Bibbins-Domingo K.
        • Grossman D.C.
        • et al.
        • US Preventive Services Task Force
        Screening for colorectal cancer: US preventive services task force recommendation statement.
        JAMA. 2016; 315: 2564-2575
      1. Osservatorio Nazionale Screening. Rapporto sul 2019. Available from: Rapportosul2019.pdf(osservatorionazionalescreening.it) [Italian].

      2. Decreto del Presidente del Consiglio dei Ministri. Ulteriori disposizioni attuative del decreto-legge 23 febbraio 2020, n. 6, recante misure urgenti in materia di contenimento e gestione dell'emergenza epidemiologica da COVID-19, applicabili sull'intero territorio nazionale. Gazzetta Ufficiale Serie Generale n. 62, 9 marzo 2020.[Italian]

        • Hamilton W.
        Cancer diagnostic delay in the COVID-19 era: what happens next?.
        Lancet Oncol. 2020; 21: 1000-1002
        • Battisti F.
        • Falini P.
        • Gorini G.
        • et al.
        Cancer screening programmes in Italy during the COVID-19 pandemic: an update of a nationwide survey on activity volumes and delayed diagnoses.
        Ann Ist Super Sanità. 2022; 58: 16-24
      3. Osservatorio Nazionale Screening. Rapporto sui ritardi accumulati dai programmi di screening Italiani in seguito alla pandemia da Covid 19. Quarto Rapporto al 31 Maggio 2021. Available from: https://www.osservatorionazionalescreening.it/content/rapportosulla-ripartenza-maggio-2021.

        • Seniori Costantini A.
        • Martini A.
        • et al.
        Colorectal cancer mortality in two areas of Tuscany with different screening exposures.
        J Natl Cancer Inst. 2008; 100: 1818-1821
        • Zorzi M.
        • Fedeli U.
        • Schievano E.
        • et al.
        Impact on colorectal cancer mortality of screening programmes based on the faecal immunochemical test.
        Gut. 2015; 64: 784-790
        • Giorgi Rossi P.
        • Vicentini M.
        • Sacchettini C.
        • et al.
        Impact of screening program on incidence of colorectal cancer: a cohort study in Italy.
        Am J Gastroenterol. 2015; 110: 1359
        • Ventura L.
        • Mantellini P.
        • Grazzini G.
        • et al.
        The impact of immunochemical faecal occult blood testing on colorectal cancer incidence.
        Dig Liver Dis. 2014; 46: 82-86
        • Bucchi L.
        • Mancini S.
        • Baldacchini F.
        • et al.
        How a faecal immunochemical test screening programme changes annual colorectal cancer incidence rates: an Italian intention-to-screen study.
        Br J Cancer. 2022; 20 (Epub ahead of print): 541-548
        • Zorzi M.
        • Zappa M.
        Synthetic indicator of the impact of colorectal cancer screening programmes on incidence rates.
        Gut. 2020; 69: 311-316
        • Zorzi M.
        • Mangone L.
        • Sassatelli R.
        • et al.
        Incidence trends of colorectal cancer in the early 2000s in Italy. Figures from the IMPACT study on colorectal cancer screening.
        Epidemiol Prev. 2015; 39: 115-125
        • Zorzi M.
        • Mangone L.
        • Anghinoni E.
        • et al.
        Characteristics of the colorectal cancers diagnosed in the early 2000s in Italy. Figures from the IMPACT study on colorectal cancer screening.
        Epidemiol Prev. 2015; 39: 108-114
        • Vicentini M.
        • Zorzi M.
        • Bovo E.
        • et al.
        Impact of screening program based on the faecal immunochemical test on stage of colorectal cancer. Results from the IMPATTO study.
        Int J Cancer. 2019; 145: 110-121
        • Zorzi M.
        • Fedato C.
        • Del Sole A.M.
        • et al.
        I programmi di screening oncologici del veneto.
        CLEUP [Italian], Padova, Italy2015 (Rapporto 2013-2014)
        • Zorzi M.
        • Hassan C.
        • Capodaglio G.
        • et al.
        Divergent long-term detection rates of proximal and distal advanced neoplasia in fecal immunochemical test screening programs: a retrospective cohort study.
        Ann Intern Med. 2018; 169: 602-609
      4. GISCoR Working Group “Interval cancers and sensitivity estimate”. Detection of the interval cancers and estimate of the sensitivity of colorectal cancer screening programmes. Epid Prev 2013; 37(2–3) [Italian]. Available at https://www.giscor.it/Documenti/doc_giscor/GISCOR_2013_Ita.pdf.

        • Campari C.
        • Sassatelli R.
        • Paterlini L.
        • et al.
        Sensibilità del test immunochimico e del programma nello screening del cancro del colon retto nella provincia di Reggio Emilia [Test and programme sensitivities of screening for colorectal cancer in Reggio Emilia].
        Epidemiol Prev. 2011; 35 (Mar-Apr[Italian]): 118-124
        • Castiglione G.
        • Visioli C.B.
        • Ciatto S.
        • et al.
        Sensitivity of latex agglutination faecal occult blood test in the Florence district population-based colorectal cancer screening programme.
        Br J Cancer. 2007; 96: 1750-1754
        • Mancini S.
        • Bucchi L.
        • Giuliani O.
        • et al.
        Proportional incidence of interval colorectal cancer in a large population-based faecal immunochemical test screening programme.
        Dig Liver Dis. 2020; 52: 452-456
        • Zorzi M.
        • Fedato C.
        • Grazzini G.
        • et al.
        High sensitivity of five colorectal screening programmes with faecal immunochemical test in the Veneto Region, Italy.
        Gut. 2011; 60: 944-949
        • Zorzi M.
        • Hassan C.
        • Senore C.
        • et al.
        Interval colorectal cancers after negative faecal immunochemical test in a 13-year screening programme.
        J Med Screen. 2021; 28: 131-139
        • Giorgi Rossi P.
        • Carretta E.
        • Mangone L.
        • et al.
        Incidence of interval cancers in faecal immunochemical test colorectal screening programmes in Italy.
        J Med Screen. 2018; 25 (Epub 2017 Feb 14. PMID: 28195508): 32-39https://doi.org/10.1177/0969141316686391
        • van de Ven S.E.M.
        • Backes Y.
        • Hilbink M.
        • Seerden T.C.J.
        • Kessels K.
        • de Vos Tot Nederveen Cappel W.H.
        • Groen J.N.
        • Wolfhagen F.H.J.
        • Geesing J.M.J.
        • Borg F.T.
        • van Bergeijk J.
        • Spanier B.W.M.
        • Mundt M.W.
        • Pullens H.J.M.
        • Boonstra J.J.
        • Opsteeg B.
        • van Lent A.U.G.
        • Schrauwen R.W.M.
        • Laclé M.M.
        • Moons L.M.G.
        • Terhaar Sive Droste J.S.
        Periprocedural adverse events after endoscopic resection of T1 colorectal carcinomas.
        Gastrointest Endosc. 2020; 91 (Dutch T1 CRC Working Group) (142–52.e3)
        • Zorzi M.
        • Gennaro N.
        • Capodaglio G.
        • et al.
        Colorectal cancer screening: the surgery rates they are a-changing. A nationwide study on surgical resections in Italy.
        Dig Liver Dis. 2019; 51: 304-309
        • AIRTUM Working Group
        New incidence and mortality data 2003–2005.
        Epidemiol Prev. 2009; 33: 1-30
        • Fedeli U.
        • Zorzi M.
        • Urso E.D.
        • et al.
        Impact of fecal immunochemical test-based screening programs on proximal and distal colorectal cancer surgery rates: a natural multiple-baseline experiment.
        Cancer. 2015; 121: 3982-3989
      5. Definizione dei livelli essenziali di assistenza. Decreto del Presidente del Consiglio dei Ministri 29 Novembre 2001. Gazzetta Ufficiale Serie Generale n.33 del 08-02-2002 -Suppl. Ordinario n. 26. Available from http://www.gazzettaufficiale.it/eli/id/2002/02/08/02A00907/sg

        • Imperiale T.F.
        • Ransohoff D.F.
        • et al.
        Multitarget stool DNA testing for colorectal-cancer screening.
        N Engl J Med. 2014; 370: 1287-1297
        • Prince M.
        • Lester L.
        • Chiniwala R.
        • et al.
        Multitarget stool DNA tests increases colorectal cancer screening among previously noncompliant medicare patients.
        World J Gastroenterol. 2017; 23: 464-471
        • Kim D.H.
        • Lubner M.G.
        • et al.
        Flat serrated polyps at CT colonography: relevance, appearance, and optimizing interpretation.
        Radiographics. 2018; 38: 60-74
        • Spada C.
        • Hassan C.
        • Bellini D.
        • et al.
        Imaging alternatives to colonoscopy: CT colonography and colon capsule. European Society of Gastrointestinal Endoscopy (ESGE) and European Society of Gastrointestinal and Abdominal Radiology (ESGAR) guideline - update 2020.
        Endoscopy. 2020; 52: 1127-1141
        • Backes Y.
        • Moss A.
        • Reitsma J.B.
        • et al.
        Narrow band imaging, magnifying chromoendoscopy, and gross morphological features for the optical diagnosis of T1 colorectal cancer and deep submucosal invasion: a systematic review and meta-analysis.
        Am J Gastroenterol. 2017; 112: 54-64
        • Gkolfakis P.
        • Tziatzios G.
        • Spartalis E.
        • et al.
        Colonoscopy attachments for the detection of precancerous lesions during colonoscopy: a review of the literature.
        World J Gastroenterol. 2018; 24: 4243-4253
        • Matsuda T.
        • Kawano H.
        • Chiu H.M.
        Screening colonoscopy: what is the most reliable modality for the detection and characterization of colorectal lesions?.
        Dig Endosc. 2015; 27: 25-29
        • Rex D.K.
        Polyp detection at colonoscopy: endoscopist and technical factors.
        Best Pract Res Clin Gastroenterol. 2017; 31: 425-433