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A Systematic Review of Repeat Fecal Occult Blood Tests for Colorectal Cancer Screening

Caitlin C. Murphy, Ahana Sen, Bianca Watson, Samir Gupta, Helen Mayo and Amit G. Singal
Caitlin C. Murphy
1Department of Population and Data Sciences, UT Southwestern Medical Center, Dallas, Texas.
2Harold C. Simmons Comprehensive Cancer Center, UT Southwestern Medical Center, Dallas, Texas.
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  • For correspondence: Caitlin.Murphy@UTSouthwestern.edu
Ahana Sen
3Department of Internal Medicine, UT Southwestern Medical Center, Dallas, Texas.
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Bianca Watson
4Department of Psychiatry and Behavioral Sciences, Tulane School of Medicine, New Orleans, Louisiana.
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Samir Gupta
5Veterans Affairs San Diego Healthcare System, UC San Diego, San Diego, California.
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Helen Mayo
6Health Sciences Digital Library and Learning Center, UT Southwestern Medical Center, Dallas Texas.
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Amit G. Singal
2Harold C. Simmons Comprehensive Cancer Center, UT Southwestern Medical Center, Dallas, Texas.
3Department of Internal Medicine, UT Southwestern Medical Center, Dallas, Texas.
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DOI: 10.1158/1055-9965.EPI-19-0775 Published February 2020
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  • Table 1.

    Definition of repeat FOBT outcomes across studies.

    OutcomeScreening roundsNumeratorDenominatorKey example
    Proportion of Round 1 participants who completed repeat FOBT in Round 22Completed FOBT in Round 2Completed FOBT with negative result in Round 1Baker, 2015 (26)
    Proportion of patients who completed two, consecutive FOBT2Completed consecutive FOBT in Rounds 1 and 2Eligible to complete FOBT in two screening rounds; negative result or did not complete FOBT in Round 1Singal, 2018 (20)
    Proportion of patients who completed FOBT in all screening rounds≥3Completed FOBT in all screening roundsEligible to complete FOBT in three or more screening rounds; negative result or did not complete FOBT in all but final roundDenis, 2015 (48)
  • Table 2.

    Characteristics of included studies (n = 27 unique studies reported in 35 articles).

    Author, yearStudy settingEligibility criteriaSample sizeFOBT/FITScreening delivery
    Tazi, 1997 (40)Burgundy, FranceAge 45–74 years45,642BiennialMailed outreach
    1988–1996Population-based
    Weller, 2007 (39)UK Colorectal Cancer Screening Pilot Evaluation, EnglandAge 50–69 years; completed negative index test107,434BiennialHema-screenMailed outreachPopulation-based
    2000–2004
    Fenton, 2010 (16)Group Health Cooperative, Seattle, WAAge 52–78 years; completed negative index test; continuously enrolled in health plan10,132BiennialOpportunistic
    2000–2003Hemoccult II SENSA
    Janda, 2010 (38)Queensland, AustraliaAge 50–74 years; completed negative index test3,406BiennialMailed outreach
    2000–2002Excluded hx SIG or COLPopulation-based
    Gellad, 2011 (51)Veterans Health Administration (136 sites), USAAge 50–75 years394,996AnnualOpportunistic
    1999–2005Excluded hx SIG, COL, or colorectal cancer
    Cole, 2012 (27)National Bowel Cancer Screening Pilot Program, AustraliaAge 55–74 years16,433AnnualDetectMailed outreach
    2003–2005Population-based
    Crotta, 2012 (50)Aosta Valley, ItalyAge 50–74 years2,959BiennialMailed outreach
    2001–2008Excluded hx SIG, COL, IBD, polyps, colorectal cancer, or severe comorbid conditionsOC-SensorPopulation-based
    Garcia, 2012 (37)Catalonia, SpainAge 50–69 years; completed negative index test11,969BiennialMailed outreach
    2004–2006Population-based
    Liss, 2013 (35)Erie Family FQHC, Chicago, ILAge 50–74 years; completed negative index test281AnnualOpportunistic
    2010–2011Excluded hx SIG, COL, IBD, colorectal cancer, or lower GI symptoms
    Bae, 2014 (25)University Hospital at Gangdong, South KoreaAge ≥50 years; completed ≥1 FOBT in prior decade; completed baseline survey237BiennialOpportunistic
    2002–2011
    Baker, 2014 (36)Erie Family FQHC, Chicago, ILAge 51–75 years; completed negative index test225AnnualOpportunistic
    2010–2011Excluded hx SIG, COL, IBD, or lower GI symptomsOC-Light
    Baker, 2014 (36)Erie Family FQHC, Chicago, ILAge 51–75 years; completed negative index test225AnnualMailed outreach
    2010–2011Excluded hx SIG, COL, IBD, or lower GI symptomsOC-Light
    Duncan, 2014 (49)Bowel Health Service, AustraliaAge 50–75 years; completed baseline survey1,540AnnualMailed outreach
    2008–2010Excluded hx SIG, COL, IBD, or colorectal cancer, family hx colorectal cancerOC-SensorPopulation-based
    McNamara, 2014 (28)Tallaght Hospital-Trinity College Colorectal Cancer Screening Program, IrelandAge 50–75 yearsExcluded hx COL, serious illness, or colorectal cancer9,863BiennialOC-SensorMailed outreach
    2008–2012
    Steele, 2014 (34)UK Colorectal Cancer Screening Pilot Evaluation, ScotlandAge 50–69 years251,578BiennialHema-screenMailed outreachPopulation-based
    2000–2006
    Wong, 2014 (30); Wong, 2013 (31)Hong KongAge 50–70 years5,832AnnualMailed outreach
    2008–2012Excluded hx SIG, COL, IBD, colorectal cancer, or lower GI symptomsHemosurePopulation-based
    Baker, 2015 (26)Erie Family FQHC, Chicago, ILAge 51–75 years; completed negative index test225AnnualMailed outreach
    2012–2013Excluded hx SIG, COL, or colorectal cancer in Round 1OC-Light
    Bujanda, 2015 (33)Basque, SpainAge 50–69 years; completed negative index test100,135BiennialMailed outreach
    2009–2013Excluded hx SIG, COL, IBD, or colorectal cancer, family hx colorectal cancerOC-SensorPopulation-based
    Denis, 2015 (48); Pornet, 2014 (52)Haut-Rhin, FranceAge 50–74 years242,271BiennialMailed outreach
    2003–2012Excluded hx of SIG, COL, serious illness, or high-risk colorectal cancer featuresHemoccult IIPopulation-based
    Lo, 2015 (29); Lo, 2016 (72); Lo, 2015 (73)NHS Bowel Cancer Screening Program, EnglandAge 60–64 years62,099BiennialHema-screenMailed outreachPopulation-based
    2006–2012
    Schlichting, 2015 (32)Veterans Health Administration, Iowa City, IAAge <65 years; completed negative index testExcluded self-reported screen up-to-date159AnnualOC FIT-CHEKMailed outreach
    2011–2013
    Paszat, 2016 (43)ColonCancerCheck Program, Ontario, CanadaAge 50–74 years; completed negative index test294,329BiennialOpportunistic
    2008–2012Excluded hx SIG, COL, or colorectal cancer, family hx colorectal cancerHema-Screen
    Telford, 2016 (42)Colon Check Program, British Columbia, CanadaAge 50–7416,234BiennialMailed outreach
    2009–2013Excluded hx SIG, COL, colorectal cancer, IBD, or rectal bleedingOC-Auto MicroPopulation-based
    Knudsen, 2017 (41)Bowel Cancer Screening in Norway, Southeast NorwayAge 50–74 years; completed negative index test; completed lifestyle survey3,114BiennialMailed outreachPopulation-based
    2012–2016Excluded hx SIG, COL, or colorectal cancer
    Saraste, 2017 (45)Stockholm-Gotland Region, SwedenAge 60–69 years; invited to ≥3 screening rounds48,959Biennial HemoccultMailed outreach
    2008–2015Population-based
    Singal, 2017 (47)Parkland Health & Hospital System, Dallas, TXAge 50–64 years; not up-to-date with screening Excluded hx SIG, COL, colorectal cancer, or IBD1,199AnnualOpportunistic
    2013–2016Hemoccult ICT
    Singal, 2017 (47)Parkland Health & Hospital System, Dallas, TXAge 50–64 years; not up-to-date with screening Excluded hx SIG, COL, colorectal cancer, or IBD2,400AnnualMailed outreach
    2013–2016FIT-CHEK
    van der Vlugt, 2017 (47);Southwest and Northwest NetherlandsAge 50–74 years; eligible for ≥2 screening rounds17,132BiennialMailed outreach
    Denters, 2013 (74); Grobbee, 2017 (75)2006–2014Excluded hx SIG, COL, IBD, colorectal cancer, or severe comorbid conditionsOC-SensorPopulation-based
    Singal, 2018 (20); Jensen, 2016 (6); Gordon, 2015 (21)Parkland Health & Hospital System, Dallas, TX; Kaiser Permanente Washington, Seattle, WA; Kaiser Permanente Northern and Southern CaliforniaAge 50–71 years; completed negative index test; 2–3 years follow-upExcluded hx SIG, COL, or colorectal cancer273,182Varied across sitesVaried across sites
    2010–2013
    Singal, 2018 (20); Jensen, 2016 (6); Gordon, 2015 (21)Parkland Health & Hospital System, Dallas, TX; Kaiser Permanente Washington, Seattle, WA; Kaiser Permanente Northern and Southern CaliforniaAge 50–71 years; completed negative index test; ≥3 years follow-upExcluded hx SIG, COL, or colorectal cancer344,103Varied across sitesVaried across sites
    2010–2013
    • Abbreviations: COL, colonoscopy; GI, gastrointestinal; hx, history; IBD, irritable bowel disease; SIG, sigmoidoscopy.

  • Table 3.

    Prevalence of repeat FOBT across studies (n = 27 unique studies reported in 35 articles) by screening delivery.

    Author, yearData sourceScreening roundsRelevant outcomeSample sizePrevalence (95% CI)
    Mailed outreach, population-based
     Tazi, 1997 (40)Population registry5% completed among Round 1 participants36,573/43,85283.4% (83.1%–83.7%)
    % completed across all screening rounds13,951/37,50237.2% (36.7%–37.7%)
     Weller, 2007 (39)Government health plan2% completed among Round 1 participants87,129/107,43481.1% (80.9%–81.3%)
     Janda, 2010 (38)Population registry2% completed among Round 1 participants874/1,16375.2% (72.7%–77.6%)
    % completed two, consecutive tests874/3,40625.7% (24.2%–27.1%)
     Cole, 2012 (27)Government health plan2% completed among Round 1 participants6,656/8,34579.8% (78.9%–80.6%)
    % completed two, consecutive tests6,656/16,43340.5% (39.8%–41.3%)
     Crotta, 2012 (50)Population registry4% completed across all screening rounds713/2,10933.8% (31.8%–35.8%)
     Garcia, 2012 (37)Population registry2% completed among Round 1 participants10,415/11,96987.0% (86.4%–87.6%)
    % completed two, consecutive tests10,415/63,68516.4% (16.1%–16.6%)
     Duncan, 2014 (49)Government health plan3% completed across all screening rounds860/1,54055.8% (53.4%–58.3%)
     Steele, 2014 (34)Government health plan3% completed among Round 1 participants114,063/139,27481.9% (81.7%–82.1%)
    % completed two, consecutive tests114,063/251,57845.3% (45.1%–45.5%)
    % completed across all screening rounds98,494/251,57839.2% (39.0%–39.3%)
     Denis, 2015 (48); Pornet, 2014 (52)Government health plan4% completed across all screening rounds34,556/242,27114.3% (14.1%–14.4%)
     Wong, 2014 (30); Wong, 2013 (31)Government health plan3% completed among Round 1 participants4,426/5,39182.1% (81.1%–83.1%)
    % completed two, consecutive tests4,426/5,53480.0% (78.9%–81.0%)
    % completed across all screening rounds3,519/5,48864.1% (62.9%–65.4%)
     Bujanda, 2015 (33)Government health plan2% completed among Round 1 participants69,193/100,13569.1% (68.8%–69.4%)
     Lo, 2015 (29); Lo, 2016 (72); Lo, 2015 (73)Government health plan3% completed among Round 1 participants30,182/35,61184.8% (84.4%–85.1%)
    % completed two, consecutive tests30,182/62,09948.6% (48.2%–49.0%)
    % completed across all screening rounds27,587/62,09944.4% (44.0%–44.8%)
     Telford, 2016 (42)Population registry2% completed among Round 1 participants5,378/6,25586.0% (85.1%–86.8%)
     Knudsen, 2017 (41)Population registry2% completed among Round 1 participants2,574/3,11482.7% (81.3%–84.0%)
     Saraste, 2017 (45)Population registry3% completed among Round 1 participants26,098/29,11389.6% (89.3%–90.0%)
    % completed two, consecutive tests26,098/48,95953.3% (52.9%–53.7%)
    % completed across all screening rounds24,373/48,95949.8% (49.3%–50.2%)
     van der Vlugt, 2017 (47); Denters, 2013 (74); Grobbee, 2017 (75)Population registry4% completed two, consecutive tests2,561/5,23248.9% (47.6%–50.3%)
    % completed across all screening rounds4,345/8,79549.4% (48.4%–50.4%)
    % completed in 3 of 3 screening rounds1,365/3,28541.6% (39.9%–43.2%)
    Mailed outreach, integrated health care systems
     Baker (intervention), 2014 (36)EHR2% completed among Round 1 participants185/21984.5% (79.7%–89.3%)
     McNamara, 2014 (28)EHR2% completed among Round 1 participants3,767/4,54982.8% (81.7%–83.9%)
    % completed two, consecutive tests3,767/9,35940.3% (39.3%–41.2%)
     Baker, 2015 (26)EHR2% completed among Round 1 participants114/12988.4% (82.8%–93.9%)
    % completed two, consecutive tests114/18960.3% (53.3%–67.3%)
     Schlichting, 2015 (32)EHR2% completed among Round 1 participants126/15979.2% (72.9%–85.5%)
     Singal (intervention), 2017 (47)EHR3% completed across all screening rounds395/2,00719.7% (17.9%–21.4%)
    Opportunistic
     Fenton, 2010 (16)EHR2% completed among Round 1 participants4,928/10,13248.6% (47.7%–49.6%)
     Gellad, 2011 (51)EHR5% completed in 4 of 5 screening rounds55,652/394,99614.1% (14.0%–14.2%)
     Liss, 2013 (35)EHR2% completed among Round 1 participants69/28124.6% (19.5%–29.6%)
     Bae, 2014 (25)Self-report5% completed across all screening rounds105/23744.3% (38.0%–50.6%)
     Baker (usual care), 2014 (36)EHR2% completed among Round 1 participants84/21938.3% (31.9%–44.8%)
     Paszat, 2016 (43)Government health plan2% completed among Round 1 participants101,526/294,32934.5% (34.3%–34.7%)
     Singal (usual care), 2017 (47)EHR3% completed across all screening rounds8/1,044
    • 0.8% (0.2%–1.3%)

    Varied
     Singal, 2018 (20); Jensen, 2016 (6); Gordon, 2015 (21)EHR2% completed two, consecutive tests127,188/273,18246.6% (46.4%–46.7%)
     Singal, 2018 (20); Jensen, 2016 (6); Gordon, 2015 (21)EHR3% completed two, consecutive tests160,252/344,10346.6% (46.4%–46.7%)
    • Note: For studies with three or more screening rounds (e.g., Saraste, 2017; ref. 45), the outcome describing completion of two, consecutive tests corresponds to FOBT completion in the first two screening rounds (i.e., in Rounds 1 and 2); confidence intervals estimated using Wald method based on a normal approximation.Abbreviation: EHR, electronic health records.

  • Table 4.

    Proposed checklist for reporting studies of repeat stool-based screening.

    Outcome variable
    • Explicitly defined, with numerator and denominator
    Test characteristics
    • Test name, manufacturer
    • Quantitative or qualitative
    • Number of samples
    • Cutoff concentration
    Study population
    • Age at study entry
    • Number with high-risk features: family history, personal history, IBD, or UC
    • Proportion previously screened
    Screening round
    • Number of screening rounds
    • Follow-up period
    • Distinguish new invitees from previous participants
    • Number ineligible: positive FOBT or diagnostic colonoscopy in prior screening round, aged out, moved away from health care system or geographic region, colonoscopy for other reason, colorectal cancer diagnosis, death
    Screening delivery
    • Organized outreach versus opportunistic
    • Frequency, timing, and intensity of patient reminders
    • Patient education materials (if any)
    • Out-of-pocket costs or financial incentives
    • Abbreviations: IBD, inflammatory bowel disease; UC, ulcerative colitis.

Additional Files

  • Tables
  • Supplementary Data

    • Supplementary Table 1 - Completeness of reporting across categories of representativeness, intervention, outcome ascertainment, follow-up, and eligibility
    • Supplementary Figure 1 - Supplementary Figure 1. PRISMA flow diagram: selection of systematic review.
    • Supplementary Figure 2 - Supplementary Figure 2. Prevalence of repeat FOBT in Round 2 among those completing in Round 1, by screening delivery (mailed outreach vs. opportunistic.)
    • Supplementary Figure 3 - Supplementary Figure 3. Prevalence of repeat FOBT in Round 2 among those completing in Round 1, by screening interval (annual vs. biennial.)
    • Supplementary Figure 4 - Supplementary Figure 4. Prevalence of repeat FOBT in Round 2 among those completing in Round 1, by test type (FIT vs. gFOBT.)
    • Supplementary Materials and Methods - Supplementary Material: search strategies for MEDLINE, Embase, and Cochrane Library.
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Cancer Epidemiology Biomarkers & Prevention: 29 (2)
February 2020
Volume 29, Issue 2
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A Systematic Review of Repeat Fecal Occult Blood Tests for Colorectal Cancer Screening
Caitlin C. Murphy, Ahana Sen, Bianca Watson, Samir Gupta, Helen Mayo and Amit G. Singal
Cancer Epidemiol Biomarkers Prev February 1 2020 (29) (2) 278-287; DOI: 10.1158/1055-9965.EPI-19-0775

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A Systematic Review of Repeat Fecal Occult Blood Tests for Colorectal Cancer Screening
Caitlin C. Murphy, Ahana Sen, Bianca Watson, Samir Gupta, Helen Mayo and Amit G. Singal
Cancer Epidemiol Biomarkers Prev February 1 2020 (29) (2) 278-287; DOI: 10.1158/1055-9965.EPI-19-0775
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