Importance
Colorectal cancer (CRC) remains a significant cause of morbidity and mortality in the United States.
Objective
To systematically review the effectiveness, diagnostic accuracy, and harms of screening for CRC.
Data Sources
Searches of MEDLINE, PubMed, and the Cochrane Central Register of Controlled Trials for relevant studies published from January 1, 2008, through December 31, 2014, with surveillance through February 23, 2016.
Study Selection
English-language studies conducted in asymptomatic populations at general risk of CRC.
Data Extraction and Synthesis
Two reviewers independently appraised the articles and extracted relevant study data from fair- or good-quality studies. Random-effects meta-analyses were conducted.
Main Outcomes and Measures
Colorectal cancer incidence and mortality, test accuracy in detecting CRC or adenomas, and serious adverse events.
Results
Four pragmatic randomized clinical trials (RCTs) evaluating 1-time or 2-time flexible sigmoidoscopy (n = 458 002) were associated with decreased CRC-specific mortality compared with no screening (incidence rate ratio, 0.73; 95% CI, 0.66-0.82). Five RCTs with multiple rounds of biennial screening with guaiac-based fecal occult blood testing (n = 419 966) showed reduced CRC-specific mortality (relative risk [RR], 0.91; 95% CI, 0.84-0.98, at 19.5 years to RR, 0.78; 95% CI, 0.65-0.93, at 30 years). Seven studies of computed tomographic colonography (CTC) with bowel preparation demonstrated per-person sensitivity and specificity to detect adenomas 6 mm and larger comparable with colonoscopy (sensitivity from 73% [95% CI, 58%-84%] to 98% [95% CI, 91%-100%]; specificity from 89% [95% CI, 84%-93%] to 91% [95% CI, 88%-93%]); variability and imprecision may be due to differences in study designs or CTC protocols. Sensitivity of colonoscopy to detect adenomas 6 mm or larger ranged from 75% (95% CI, 63%-84%) to 93% (95% CI, 88%-96%). On the basis of a single stool specimen, the most commonly evaluated families of fecal immunochemical tests (FITs) demonstrated good sensitivity (range, 73%-88%) and specificity (range, 90%-96%). One study (n = 9989) found that FIT plus stool DNA test had better sensitivity in detecting CRC than FIT alone (92%) but lower specificity (84%). Serious adverse events from colonoscopy in asymptomatic persons included perforations (4/10 000 procedures, 95% CI, 2-5 in 10 000) and major bleeds (8/10 000 procedures, 95% CI, 5-14 in 10 000). Computed tomographic colonography may have harms resulting from low-dose ionizing radiation exposure or identification of extracolonic findings.
Conclusions and Relevance
Colonoscopy, flexible sigmoidoscopy, CTC, and stool tests have differing levels of evidence to support their use, ability to detect cancer and precursor lesions, and risk of serious adverse events in average-risk adults. Although CRC screening has a large body of supporting evidence, additional research is still needed.
Although colorectal cancer (CRC) incidence has been declining over the past 20 years in the United States, it still causes significant morbidity and mortality.1Quiz Ref ID Despite increases in screening rates over the past 30 years, in 2012 an estimated 28% of eligible US adults had never been screened for CRC.2 A variety of tests are available for screening, including stool-based tests (eg, guaiac-based fecal occult blood testing [gFOBT], immunochemical-based fecal occult blood testing [FIT], stool DNA [sDNA] testing), endoscopy (eg, flexible sigmoidoscopy [SIG], colonoscopy), and imaging (eg, double-contrast barium enema, computed tomographic colonography [CTC]).
Quiz Ref IDCurrently, most US guideline organizations, including the US Preventive Services Task Force (USPSTF), recommend that options for CRC screening include colonoscopy every 10 years, an annual high-sensitivity gFOBT or FIT, and SIG every 5 years with high-sensitivity gFOBT or FIT.3,4 In 2008, the USPSTF recommended CRC screening using fecal occult blood testing, sigmoidoscopy, or colonoscopy beginning at age 50 years and continuing until age 75 years (A recommendation); selectively offering screening in adults aged 76 to 85 years (C recommendation); and against screening for colorectal cancer in adults older than 85 years (D recommendation). At that time, the USPSTF had insufficient evidence to assess the benefits and harms of CTC and sDNA testing as screening modalities. A systematic review was conducted to update relevant evidence since 2008 and to help inform a separate modeling exercise, which together were used by the USPSTF in its process of updating the 2008 CRC screening recommendations.
This review addressed 3 key questions (KQs) as shown in Figure 1. Additional methodological details regarding search strategies, detailed study inclusion criteria, quality assessment, excluded studies, and description of data analyses are publicly available in the full evidence report at http://www.uspreventiveservicestaskforce.org/Page/Document/final-evidence-review/colorectal-cancer-screening2.5
Data Sources and Searches
MEDLINE, PubMed, and the Cochrane Central Register of Controlled Trials were searched to locate primary studies informing the key questions (eMethods in the Supplement) that were published from the end of the previous review6 (January 1, 2008) through December 31, 2014. The database searches were supplemented with expert suggestions and by reviewing reference lists from all other relevant systematic reviews, including the 2008 USPSTF evidence report. The search also included selected gray literature sources, including ClinicalTrials.gov and the World Health Organization International Clinical Trials Registry Platform, for ongoing trials. Since December 2014, we continued to conduct ongoing surveillance through article alerts and targeted searches of high-impact journals to identify major studies published in the interim that may affect the conclusions or understanding of the evidence and therefore the related USPSTF recommendation. The last surveillance was conducted on February 23, 2016. Although several potentially relevant new studies were identified,7-9 none of these studies would substantively change the review’s interpretation of findings or conclusions.
Two investigators independently reviewed 8492 titles and abstracts and 696 articles against the specified inclusion criteria (Figure 2). Discrepancies were resolved through consensus and consultation with a third investigator. Inclusion criteria were fair- and good-quality English-language studies of asymptomatic screening populations of individuals who were 40 years or older, either at average risk for CRC or not selected for inclusion based on CRC risk factors. Studies were included that evaluated the following screening tests: colonoscopy, SIG, CTC, gFOBT, FIT, FIT plus sDNA, or a blood test for methylated SEPT9 DNA (mSEPT9).
For KQ1, randomized clinical trials (RCTs) or otherwise controlled trials of CRC screening vs no screening, as well as trials comparing screening tests, that included outcomes of cancer incidence, CRC-specific mortality, or all-cause mortality were reviewed for inclusion. For tests without trial-level evidence (ie, colonoscopy, FIT), well-conducted prospective cohort or population-based nested case-control studies were examined.
For KQ2, diagnostic accuracy studies that used colonoscopy as a reference standard were included. Studies whose design was subject to a high risk of bias were generally excluded, including studies that did not apply colonoscopy to at least a random subset of screen-negative persons (verification bias)10 and studies without an adequate representation of a full spectrum of patients (spectrum bias), such as case-control studies.10-14 Selected well-conducted FIT diagnostic accuracy studies that used robust registry follow-up for screen-negative participants were included.
For KQ3, all trials and observational studies that reported serious adverse events requiring unexpected or unwanted medical attention or resulting in death were included. These events included, but were not limited to, perforation, major bleeding, severe abdominal symptoms, and cardiovascular events. Studies designed to assess for extracolonic findings (ie, incidental findings on CTC) and the resultant diagnostic yield and harms of workup were also included. Studies reporting extracolonic findings generally used the CT Colonography Reporting and Data System (C-RADS). Under C-RADS, extracolonic findings are categorized as E0 (limited examination), E1 (normal examination or normal variant), E2 (clinically unimportant finding in which no workup is required), E3 (likely unimportant or incompletely characterized in which workup may be required), or E4 (potentially important finding requiring follow-up).15
Data Extraction and Quality Assessment
Two reviewers each critically appraised all articles that met inclusion criteria using the USPSTF design-specific quality criteria16 supplemented by the National Institute for Health and Clinical Excellence methodology checklists,17 A Measurement Tool to Assess Systematic Reviews (AMSTAR) for systematic reviews,18 Newcastle Ottawa Scales for cohort and case-control studies,19 and Quality Assessment of Diagnostic Accuracy (QUADAS) and QUADAS-2 for studies of diagnostic accuracy (eTable 1 in the Supplement).20,21 Poor-quality studies and those with a single fatal flaw or multiple important limitations that could invalidate results were excluded from this review. Disagreements about critical appraisal were resolved by consensus and, if needed, consultation with a third independent reviewer. One reviewer extracted key data from included studies; a second reviewer checked the data for accuracy.
Data Synthesis and Analysis
For each KQ, the number and design of included studies, overall results, consistency or precision of results, reporting bias, study quality, limitations of the body of evidence, and applicability of findings were summarized. The results were synthesized by KQ, type of screening test, and study design. Studies from the 2008 review that met the updated inclusion criteria were incorporated. The analyses for test performance focused primarily on per-person (ie, by individual patient rather than by lesion) test sensitivity and specificity to detect adenomas (by size, where reported, <6 mm, ≥6 mm, ≥10 mm), advanced adenomas (as defined by the study), and CRC. The studies used several kinds of FITs, which were grouped as qualitative (fixed cutoff) or quantitative (adjustable cutoff), as well as into families (tests produced by the same manufacturer, using the same components and method, or compatible with different automated analyzers). Tests were compared using similar cutoff values expressed in μg hemoglobin (Hb)/g feces.
Because of the limited number of studies and the clinical heterogeneity of studies, the analyses were largely descriptive. Random-effects meta-analyses were conducted using the profile likelihood method22 to estimate the effect of SIG based on the pooled incidence rate ratio (events/person-year) for CRC incidence and mortality across the 4 major SIG trials. Random-effects models were also conducted using the restricted maximum likelihood estimation method to estimate rates of serious adverse events for colonoscopy and SIG. The presence and magnitude of statistical heterogeneity were assessed among pooled studies using the I2 statistic. All tests were 2-sided with a P value less than .05 indicating statistical significance. Meta-analyses were performed using R version 3.0.2 (R Project for Statistical Computing).23,24
Effectiveness of Screening
Key Question 1. What is the effectiveness of screening programs based on the prespecified screening tests (alone or in combination) in reducing incidence of and mortality from colorectal cancer?
Twenty-five unique fair- or good-quality studies25-49 (published in 47 articles25-71) were found that assessed the effectiveness or comparative effectiveness of screening tests on CRC incidence and mortality. These studies included 1 cohort study of screening colonoscopy,36 4 RCTs of SIG (in 7 articles),25,39,41,50,60,66,71 and 6 trials (in 11 articles) of Hemoccult II gFOBT.29,33-35,40,44,59,62-64,67 In addition, 15 comparative effectiveness studies (in 22 articles) were found that were primarily designed to assess the relative uptake and CRC yield between different screening modalities.26-28,30-32,37,38,42,43,45-49,54-58,65,69 Due to limitations in study designs, the observational colonoscopy study and comparative effectiveness studies are not discussed further in this article. Summarized below are the results for CRC-specific mortality, as results for CRC incidence were consistent with CRC mortality findings.
Four large, fair-quality, pragmatic RCTs (n = 458 002) evaluated the effectiveness of 1 or 2 rounds of SIG in average-risk adults aged 50 to 74 years (Table 1).25,39,41,50,60,66,71 Adherence to SIG in these trials ranged from 58% to 84%, and rates of diagnostic colonoscopy ranged from 5% to 33% due to differences in referral criteria. Based on pooled intention-to-treat analyses, SIG was associated with lower CRC-specific mortality compared with no screening at 11 to 12 years of follow-up (incidence rate ratio, 0.73; 95% CI, 0.66-0.82; I2 = 0%) (Figure 3); however, the association with mortality benefit was limited to distal CRC (incidence rate ratio, 0.63; 95% CI, 0.49-0.84; I2 = 44%) (eFigure 1 in the Supplement). In 1 trial, conducted in Norway, half of the participants randomized to SIG also received a single FIT test; the SIG-plus-FIT group had lower CRC mortality than the SIG-only group did (hazard ratio, 0.62; 95% CI, 0.42-0.90).60
Five older, large, pragmatic RCTs (n = 419 966) with 11 to 30 years of follow-up evaluated the effectiveness of annual or biennial screening programs with Hemoccult II (Table 1).29,33,34,40,44,59,63,64,67 Based on intention-to-treat analyses, compared with no screening, biennial screening with Hemoccult II resulted in a reduction in CRC-specific mortality after 2 to 9 rounds of screening (relative risk [RR], 0.91; 95% CI, 0.84-0.98, at 19.5 years to RR, 0.78; 95% CI, 0.65-0.93, at 30 years). Based on 1 trial, conducted in the United States, annual screening with Hemoccult II after 11 rounds of screening resulted in greater reductions (RR, 0.68; 95% CI, 0.56-0.82) than biennial screening at 30 years did (RR, 0.78; 95% CI, 0.65-0.93).44
Diagnostic Accuracy of Screening
Key Question 2. What are the test performance characteristics of the prespecified screening tests (alone or in combination) for detecting colorectal cancer, advanced adenomas, or adenomatous polyps based on size?
Thirty-three unique diagnostic accuracy studies72-104 (published in 44 articles72-115) were found that evaluated the 1-time test performance of a screening test compared with an adequate reference standard, including 9 studies of screening CTC (in 10 articles),81,82,85-87,89,93,99,101,114 3 studies of gFOBT Hemoccult Sensa,72,73,90 20 studies of various FITs72-78,80,82-84,88,90,91,94-98,100,102-104 (1 of which evaluated a FIT plus sDNA test83), and 1 study of a blood test to detect circulating mSEPT9.79 The study of mSEPT9 (not approved by the US Food and Drug Administration [FDA] for screening) and studies evaluating Hemoccult Sensa and FITs that only applied the colonoscopy reference standard to positive stool tests are not discussed further in this article.
Direct Visualization Tests
Nine fair- or good-quality studies (n = 6497) evaluated the diagnostic accuracy of multidetector CTC in average-risk screening populations (Table 2).81,82,85-87,89,93,99,101,114 The 2 largest and best-quality studies were multicenter trials conducted in the United States evaluating CTC with bowel preparation and fecal tagging.85,99 Overall, the studies were not powered to estimate test performance to detect CRC. Based on 7 studies of CTC with bowel preparation (n = 5328), the per-person sensitivity to detect adenomas 10 mm and larger ranged from 67% (95% CI, 45%-84%) to 94% (95% CI, 84%-98%), and specificity ranged from 98% (95% CI, 96%-99%) to 96% (95% CI, 95%-97%). The per-person sensitivity to detect adenomas 6 mm and larger ranged from 73% (95% CI, 58%-84%) to 98% (95% CI, 91%-100%), and specificity ranged from 89% (95% CI, 84%-93%) to 91% (95% CI, 88%-93%). Two studies (N = 1169) evaluated CTC without bowel preparation.81,101 Although the data were limited, the sensitivity of CTC without bowel preparation to detect adenomas 6 mm and larger appeared to be lower than the sensitivity of CTC protocols including bowel preparation.
Four (n = 4821) of the 9 CTC studies allowed for the estimation of sensitivity of colonoscopy generalizable to community practice.85,86,99,101 Compared with CTC or colonoscopy plus CTC (eg, segmental unblinding), the sensitivity for colonoscopy to detect adenomas 10 mm and larger ranged from 89% (95% CI, 78%-96%) to 98% (95% CI, 74%-100%) and for adenomas 6 mm and larger ranged from 75% (95% CI, 63%-84%) to 93% (95% CI, 88%-96%) (see full report5). Therefore, CTC with bowel preparation had sensitivity to detect adenomas 6 mm and larger comparable with colonoscopy, albeit with wider variability in estimated performance. It is unclear whether the observed variation in CTC performance was due to differences in study design, populations, bowel preparation, CTC technologies, or differences in reader experience or reading protocols.
Fourteen fair- or good-quality studies (n = 59 425) that used colonoscopy reference standard in all participants reported sensitivity and specificity for 19 different types of qualitative or quantitative FITs, including 1 FIT plus sDNA test (Table 3).74,77,78,80,82,83,91,94,95,97,98,100,103,104,107,108,115 Overall, the sensitivity for CRC and advanced adenomas varied widely, including a discontinued test with very low sensitivity.100 Given the heterogeneity among FITs and their test performance, focus was placed on the performance characteristics of currently available tests evaluated in more than 1 study. Two families of FDA-cleared tests, OC-Light (qualitative, No. of studies = 3, n = 25 924) and OC FIT-CHEK (eg, OC-Sensor Diana, OC-Micro, OC-Auto) (quantitative, No. of studies = 5, n = 12 794), had relatively high sensitivity and specificity. With a single stool specimen, the lowest sensitivity demonstrated for CRC was 73% (95% CI, 48%-90%) and specificity was 96% (95% CI, 95%-96%). Similarly, the highest sensitivity with paired specificity for CRC was 88% (95% CI, 55%-99%) and 91% (95% CI, 89%-92%), respectively. In the largest studies, sensitivity ranged from 74% (95% CI, 62%-83%) for quantitative test categories (n = 9989) to 79% (95% CI, 61%-90%) for qualitative test categories (n = 18 296). In a small study (n = 770) that tested 3 stool specimens, sensitivity was 92% (95% CI, 69%-99%), but specificity was 87% (95% CI, 85%-89%). OC-Light or OC FIT-CHEK test sensitivity and specificity for advanced adenomas ranged from 22% (95% CI, 17%-28%) to 40% (95% CI, 30%-51%), and specificity ranged from 97% (95% CI, 97%-98%) to 91% (95% CI, 91%-92%). Although higher sensitivities to detect advanced adenomas were obtained for certain other FITs or by using 3 stool specimens, the corresponding specificities were lower.
Cologuard (Exact Sciences) is an FDA-approved stool test that combines stool DNA with a proprietary FIT component. One fair-quality diagnostic accuracy study (n = 9989) evaluated Cologuard compared with OC FIT-CHEK.83 In that study, Cologuard had a statistically significant higher sensitivity to detect CRC and advanced adenoma compared with OC FIT-CHEK. The higher sensitivity for CRC (92%; 95% CI, 84%-97%) and for advanced adenoma (42%; 95% CI, 39%-46%) was accompanied by lower specificity (84%; 95% CI, 84%-85% for CRC and 87%; 95% CI, 86%-87% for advanced adenoma). In our active surveillance of the literature, we identified 1 additional diagnostic accuracy study of FIT plus sDNA (n = 661) in asymptomatic Alaska Native adults.9 This study was not powered to find a difference in detection of CRC; nonetheless, findings were generally consistent with the included study on FIT plus sDNA.83
Key Question 3a. What are the adverse effects of the different screening tests (either as single application or in a screening program)?
Key Question 3b. Do adverse effects vary by important subpopulations (eg, age)?
Ninety-eight fair- or good-quality studies27,29,37-39,45,48,64,66,77,78,81,82,85-87,89,92,93,97,99,101,116-191 in 113 articles27,29,34,37-39,44,45,48,50,53,64,66,70,77,78,81,82,85-87,89,92,93,97,99,101,114,116-200 were included that evaluated the harms of CRC screening. These studies included 14 studies of screening programs using stool testing or SIG, 55 studies of colonoscopy in asymptomatic adults,37,45,77,78,85,97,101,116,117,119-124,126,128-131,133,136,140,142,144,147,148,150,151,153-156,158,159,161-163,170-178,180-183,187-190 18 studies of screening SIG,27,38,39,43,48,50,66,143,146,151,157,162,176,183,185,186,191-194,200 and 15 studies of screening CTC in asymptomatic adults.45,81,82,85,87,89,101,118,135,145,150,162,169,179 Twelve CTC studies provided estimates of radiation exposure per examination,81,82,85-87,89,93,99,101,118,135,162 and another 21 CTC studies reported information on extracolonic findings.45,85,99,101,114,125,127,134,137-139,141,150,152,160,164,166-168,184,195,198
Approximately half of colonoscopy harms studies (29/55 studies) were in explicitly screening or asymptomatic populations (eTable 2 in the Supplement). By pooling 26 studies (n = 3 414 108) in screening populations or generally asymptomatic persons,37,45,77,78,85,97,101,120,121,124,126,130,131,136,150,156,163,170,174,176,180-182,188-190 it was estimated that the risk of perforations from colonoscopy was 4 in 10 000 procedures (95% CI, 2-5 in 10 000; I2 = 86%) (Figure 4). On the basis of 22 of those studies (n = 3 347 101),37,45,77,85,97,101,120,121,124,126,130,131,156,163,170,174,180-182,188-190 it was estimated that the risk of major bleeding from colonoscopy was 8 in 10 000 procedures (95% CI, 5-14 in 10 000; I2 = 97%) (Figure 5). Only eight studies (n = 204 614) explicitly reported if perforation or major bleeding was related to polypectomy or biopsy.45,85,120,136,158,173,177,178 Based on this limited subset of studies reporting adequate information, 36% (15/42) of perforations and 96% (49/51) of major bleeding events were from polypectomy.
All 18 SIG harms studies were conducted in general-risk screening populations (eTable 3 in the Supplement). Based on the results of 16 studies (n = 329 698),38,39,43,48,50,66,143,146,151,157,176,183,185,186,191,192 perforations from SIG in average-risk screening populations were relatively uncommon: the pooled point estimate was 1 in 10 000 procedures (95% CI, 0.4-1.4 in 10 000; I2 = 18.4%). In 10 studies (n = 137 987),27,38,48,50,66,143,146,157,185,186 major bleeding episodes from SIG were also relatively uncommon, with a pooled point estimate of 2 in 10 000 procedures (95% CI, 0.7-4 in 10 000; I2 = 52.5%) (Figure 6 and Figure 7). Flexible sigmoidoscopy, however, may require follow-up diagnostic or therapeutic colonoscopy. From 5 SIG screening trials, the pooled estimate was 14 perforations per 10 000 (95% CI, 9-26 in 10 000) and 34 major bleeds per 10 000 (95% CI, 5-63 in 10 000) for follow-up colonoscopy for positive screening SIG from 4 trials.
Other serious harms from endoscopy were not routinely reported or consistently defined. Only 2 studies compared harms other than perforation and bleeding in persons who had a colonoscopy vs those who had not.180,187 Both of these studies found no statistically significant higher risks of serious harms (including myocardial infarction, cerebrovascular accident, other cardiovascular events, and mortality) attributable to colonoscopy. Because of reporting bias around serious harms other than perforation and bleeding, as well as the lack of evidence for other serious harms attributable to colonoscopy in the few studies with control groups, these data were not quantitatively pooled.
Nineteen studies examined differential harms of colonoscopy by age group.116,119,122,123,128,129,131,136,140,154,156,159,161,170,172,174,187,189,190 These studies generally found increasing rates of serious adverse events with increasing age, including perforation and bleeding.
Fifteen fair- or good-quality studies addressed serious adverse effects of screening CTC (eTable 4 in the Supplement).45,81,82,85,87,89,101,118,135,145,150,162,169,179 Evidence suggested little to no risk of serious adverse events, including perforation, from CTC based on 11 prospective studies (n = 10 272) performed in screening populations.45,81,82,85,87,89,101,118,135,145,150,162,169,179
Many of the CTC studies in this review did not report actual radiation exposure or provide sufficient information to calculate it. Based on 4 included diagnostic accuracy studies of CTC,81,82,85,101 the estimated radiation dose for 1 full-screening CTC examination (dual positioning supine and prone) was about 4.5 to 7 mSv. In 3 additional recent CTC screening studies118,135,162 (2004-2008), the estimated radiation dose decreased to a range of 1 to less than 5 mSv.
CTC Extracolonic Findings
Incidental extracolonic findings detected on CTC can be beneficial or harmful depending on the finding. Twenty-one studies (n = 38 293)45,85,99,101,125,127,134,137-139,141,150,152,160,164,166-168,184,195,198 in 22 articles45,85,99,101,114,125,127,134,137-139,141,150,152,160,164,166-168,184,195,198 (7 studies with overlapping populations reported different types extracolonic findings) reported on extracolonic findings in asymptomatic persons (eTable 5 in the Supplement). In general, these studies varied greatly in their ability to accurately assess follow-up and the duration of follow-up.
Overall, extracolonic findings were common, occurring in 27% to 69% of examinations. Similarly, the studies suggested a very wide range of findings needing additional workup: 5% to 37% had E3 or E4 findings, and 1.7% to 12% had E4 findings. Among the studies that also reported medical follow-up of extracolonic findings, 1.4% to 11% went on to diagnostic evaluation, which is similar to the prevalence of E4 category findings. Among studies that adequately reported subsequent treatment, only up to 3% required definitive medical or surgical treatment. Extracolonic cancers were not common, occurring in 0.5% of persons undergoing CTC examinations. In the largest series of examinations (n = 10 286), which had about 4 years of follow-up, 0.35% of examinations revealed an extracolonic malignancy, 32 of which received definitive treatment.167 Abdominal aortic aneurysms were identified in 1.4% of persons or fewer. In our active surveillance of the literature, we identified 1 additional study evaluating extracolonic findings in screening CTC (n = 7952).7 This study’s population overlapped with several already included studies and reported that 2.5% of examinations had E4 category findings, consistent with findings from included studies.150,164,166-168,195,198
Colorectal cancer screening continues to be a necessary and active field of research. Since the 2008 USPSTF recommendation was published, 95 new studies were identified, including more evidence on (1) the effectiveness of SIG for reducing CRC mortality, (2) the test performance of screening CTC and decreasing radiation exposure from CTC, and (3) the test performance of a number of FDA-approved FITs (including 1 FIT plus sDNA test). Colonoscopy, SIG, CTC, and stool testing (gFOBT, FIT, and FIT plus sDNA test) each have differing levels of evidence to support their use, ability to detect cancer and precursor lesions, and risk of serious adverse events in screening average-risk adults for CRC (Table 4).
To date, no CRC screening modality has been shown to reduce all-cause mortality. Robust data from well-conducted population-based screening RCTs have demonstrated that both Hemoccult II and SIG can reduce CRC mortality, although neither of these tests is widely used for screening in the United States. Therefore, the empirical data on the performance of CRC screening programs using modalities used in clinical practice today are limited. Expensive, large population-based RCTs of newer stool tests may not always be necessary, as evidence-based reasoning supports that screening with stool tests with sensitivity and specificity that are both as good as, or better than, Hemoccult II would result in CRC mortality reductions similar to or better than reductions shown in existing trials.201 Based on this review, stool tests that meet those requirements are available, including specific single-stool sample FITs. However, FITs are not homogenous: they use different assays and have different diagnostic performance levels. The FDA-approved OC-Light and OC FIT-CHEK tests have the most evidence to support their use. Stool tests that maximize sensitivity (eg, FIT plus sDNA test, multiple sample FITs, or quantitative FIT using lower cutoffs) have lower specificity and therefore need new trials or modeling exercises to understand the tradeoff of higher false-positive findings. In addition, stool tests vary in cost; for example, the Centers for Medicare & Medicaid Services reimbursement is $23 per FIT vs $493 per FIT plus sDNA test.202
Even though its superiority in a program of screening has not been empirically established, colonoscopy remains the criterion standard for assessing the test performance of other CRC screening tests. Quiz Ref IDMoreover, colonoscopy is significantly more invasive than other available tests and thus carries a greater possibility of procedural complications, as well as harms of overdiagnosis and overtreatment of smaller lesions (ie, <10 mm). Three large RCTs of screening colonoscopy in average-risk adults are under way and will provide information about the long-term CRC incidence and mortality outcomes: the Northern European Initiative on Colorectal Cancer (NordICC) trial, comparing screening colonoscopy with usual care (estimated primary completion date, June 2026)203; COLONPREV, comparing colonoscopy with biennial FIT in Spain (estimated primary completion date, November 2021)37,204,205; and CONFIRM, comparing colonoscopy vs annual FIT in the United States (estimated primary completion date, September 2027).206
Quiz Ref IDEvidence continues to accrue that CTC adequately detects CRC and large potential precursor lesions. Although the risk of immediate harms from screening CTC (eg, bowel perforation from insufflation) is very low, it is unclear what (if any) true harm is posed by cumulative exposure to low-dose radiation or detection of extracolonic findings. Although the radiation dose appears to be decreasing over time due to technological and protocol advancements, it still ranges as high as 7 mSv per examination (dual positioning). Given that the average amount of radiation one is exposed to from background sources in the United States is about 3 mSv per year,207 ionizing radiation from a single CTC examination is low. However, current expert recommendations are to repeat CTC every 5 years, and even low doses of ionizing radiation could cumulatively convey a small excess risk of cancer.208,209 From empirical evidence to date, it remains unclear whether detection of extracolonic findings represents a net benefit or harm.
Quiz Ref IDThis evidence report and systematic review did not address several important issues: screening in high-risk adults (ie, those with known family history of CRC), risk assessment to tailor screening, test acceptability, availability of or access to screening tests, methods to increase screening adherence, potential harms of overdiagnosis or unnecessary polypectomy, overuse or misuse of screening, and surveillance after adenoma detection. This review was commissioned along with a separate set of microsimulation decision models from the Cancer Intervention and Surveillance Modeling Network (CISNET) that addressed other important gaps in evidence, including ages to start and stop screening, screening intervals, and targeted or tailored screening.210 The review was limited to evidence conducted in countries with the highest applicability to US practice; in addition, only articles published in English were considered for inclusion.
Unlike other routinely recommended or conducted cancer screening, there are multiple viable options for CRC screening. These options have various levels of evidence to support their use, aims (eg, to detect cancers, potential precursor lesions, or both), test acceptability and adherence, intervals of time to repeat screening, need for follow-up testing (including surveillance incurred), associated serious harms, availability in practice, cost, and advocacy for their use. This complexity is compounded by testing whose quality is more operator-dependent (eg, colonoscopy, CTC), as well as rapid technologic advancements in improving existing tests or developing new tests.
Empirical studies, trials, or well-designed cohort studies with average-risk populations are still needed to evaluate programs of screening using colonoscopy, the best-performing stool tests, and effect of CTC on cancer mortality and cancer incidence. Also needed are studies of diagnostic accuracy to confirm the screening test performance of promising stool tests based on high sensitivity to detect CRC or advanced adenomas with thus far limited reproducibility (ie, only 1 study). Diagnostic accuracy studies, particularly those evaluating new or more complex technologies, should report percentages of inadequate or indeterminate results. It is also important to understand the contribution of technological advancements to existing technology (eg, enhancements to optical colonoscopy or CTC) on test performance in average-risk adults as well as on reducing harms (eg, decreasing radiation exposure, less aggressive bowel preparation). More complete and consistent reporting regarding downstream benefits and harms from initial detection (ie, subsequent workup and definitive treatment) of C-RADS E3 and E4 findings need to be published in observational studies or trials with longer-term follow-up. Data are still needed on the differential uptake of and adherence to screening modalities and on continued adherence to repeated rounds of screening and diagnostic follow-up to screening over longer periods.
Colonoscopy, flexible sigmoidoscopy, CTC, and various stool tests have differing levels of evidence to support their use in CRC screening, ability to detect CRC and precursor lesions, and risk of serious adverse events in average-risk adults. Although CRC screening has a large body of supporting evidence, additional research is still needed to weigh the relative benefits and harms of each test in within a program of screening.
Corresponding Author: Jennifer S. Lin, MD, MCR, Center for Health Research, Kaiser Permanente Northwest, 3800 N Interstate Ave, Portland, OR 97227 (jennifer.s.lin@kpchr.org).
Correction: This article was corrected online August 2, 2016, to fix an incomplete URL for the full report and on October 4, 2016, to fix alignment of a row in Table 3 and correct numbers in the gFOBT row in Table 4.
Published Online: June 15, 2016. doi:10.1001/jama.2016.3332
Author Contributions: Dr Lin had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Lin, Piper, Perdue, Whitlock.
Acquisition, analysis, or interpretation of data: All authors.
Drafting of the manuscript: Lin, Piper, Rutter, Webber.
Critical revision of the manuscript for important intellectual content: Lin, Piper, Perdue, Rutter, O’Connor, Smith, Whitlock.
Statistical analysis: Lin, Piper, Rutter, O’Connor, Smith.
Obtained funding: Lin, Whitlock.
Administrative, technical, or material support: Piper, Perdue, Webber.
Study supervision: Lin, Whitlock.
Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported.
Funding/Support: This research was funded by the Agency for Healthcare Research and Quality (AHRQ) under a contract to support the USPSTF.
Role of the Funder/Sponsor: Investigators worked with USPSTF members and AHRQ staff to develop the scope, analytic framework, and key questions for this review. AHRQ staff provided project oversight; reviewed the report to ensure that the analysis met methodological standards; and distributed the draft for peer review. AHRQ reviewed and approved the manuscript before submission, but had no role in the design and conduct of the study including study selection, quality assessment, analysis, and interpretation of the data; preparation of the manuscript; and decision to submit the manuscript for publication.
Additional Contributions: We gratefully acknowledge the following individuals for their contributions to this project: Smyth Lai, MLS; Kevin Lutz, MFA; and Elizabeth Hess, MA, ELS(D), at the Kaiser Permanente Center for Health Research; Jennifer Croswell, MD, MPH, at the Agency for Healthcare Research and Quality; and current and former members of the US Preventive Services Task Force who contributed to topic deliberations. USPSTF members, peer reviewers, and federal partner reviewers did not receive financial compensation for their contributions.
Additional Information: A draft version of this evidence report underwent external peer review from 6 content experts (James Allison, MD, University of California, San Francisco; Samir Gupta, MD, MSCS, University of California, San Diego; Theodore R. Levin, MD, Kaiser Permanente; David Lieberman, MD, Oregon Health & Science University; Perry Pickhardt, MD, MPH, University of Wisconsin; David Ransohoff, MD, University of North Carolina at Chapel Hill) and 4 federal partners: Centers for Disease Control and Prevention, National Institutes of Health, US Department of Veterans Affairs, and Indian Health Service. Comments were presented to the USPSTF during its deliberation of the evidence and were considered in preparing the final evidence review.
Editorial Disclaimer: This evidence report is presented as a document in support of the accompanying USPSTF Recommendation Statement. It did not undergo additional peer review after submission to JAMA.
2.Centers for Disease Control and Prevention (CDC). Vital signs: colorectal cancer screening test use: United States, 2012.
MMWR Morb Mortal Wkly Rep. 2013;62(44):881-888.
PubMedGoogle Scholar 3.US Preventive Services Task Force. Screening for colorectal cancer: US Preventive Services Task Force recommendation statement.
Ann Intern Med. 2008;149(9):627-637.
PubMedGoogle ScholarCrossref 4.Levin
B, Lieberman
DA, McFarland
B,
et al; American Cancer Society Colorectal Cancer Advisory Group; US Multi-Society Task Force; American College of Radiology Colon Cancer Committee. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology.
CA Cancer J Clin. 2008;58(3):130-160.
PubMedGoogle ScholarCrossref 5.Lin
JS, Piper
MA, Perdue
LA,
et al. Screening for Colorectal Cancer: A Systematic Evidence Review for the US Preventive Services Task Force: Evidence Synthesis No. 135. Rockville, MD: Agency for Healthcare Research and Quality; 2016. AHRQ publication 14-05203-EF-1.
6.Whitlock
EP, Lin
J, Liles
E,
et al. Screening for Colorectal Cancer: An Updated Systematic Review. Rockville, MD: Agency for Healthcare Research and Quality; 2008.
7.Pooler
BD, Kim
DH, Pickhardt
PJ. Potentially important extracolonic findings at screening CT colonography: incidence and outcomes data from a clinical screening program.
AJR Am J Roentgenol. 2016;206(2):313-318.
PubMedGoogle ScholarCrossref 8.Sali
L, Mascalchi
M, Falchini
M,
et al; SAVE Study Investigators. Reduced and full-preparation CT colonography, fecal immunochemical test, and colonoscopy for population screening of colorectal cancer: a randomized trial.
J Natl Cancer Inst. 2015;108(2):108.
PubMedGoogle Scholar 9.Redwood
DG, Asay
ED, Blake
ID,
et al. Stool DNA testing for screening detection of colorectal neoplasia in Alaska Native people.
Mayo Clin Proc. 2016;91(1):61-70.
PubMedGoogle ScholarCrossref 10.Lijmer
JG, Mol
BW, Heisterkamp
S,
et al. Empirical evidence of design-related bias in studies of diagnostic tests.
JAMA. 1999;282(11):1061-1066.
PubMedGoogle ScholarCrossref 11.Whiting
P, Rutjes
AW, Reitsma
JB, Glas
AS, Bossuyt
PM, Kleijnen
J. Sources of variation and bias in studies of diagnostic accuracy: a systematic review.
Ann Intern Med. 2004;140(3):189-202.
PubMedGoogle ScholarCrossref 12.Leeflang
MM, Bossuyt
PM, Irwig
L. Diagnostic test accuracy may vary with prevalence: implications for evidence-based diagnosis.
J Clin Epidemiol. 2009;62(1):5-12.
PubMedGoogle ScholarCrossref 13.Ransohoff
DF, Feinstein
AR. Problems of spectrum and bias in evaluating the efficacy of diagnostic tests.
N Engl J Med. 1978;299(17):926-930.
PubMedGoogle ScholarCrossref 14.Rutjes
AW, Reitsma
JB, Di Nisio
M, Smidt
N, van Rijn
JC, Bossuyt
PM. Evidence of bias and variation in diagnostic accuracy studies.
CMAJ. 2006;174(4):469-476.
PubMedGoogle ScholarCrossref 15.Zalis
ME, Barish
MA, Choi
JR,
et al; Working Group on Virtual Colonoscopy. CT colonography reporting and data system: a consensus proposal.
Radiology. 2005;236(1):3-9.
PubMedGoogle ScholarCrossref 16.Harris
RP, Helfand
M, Woolf
SH,
et al; Methods Work Group, Third US Preventive Services Task Force. Current methods of the US Preventive Services Task Force: a review of the process.
Am J Prev Med. 2001;20(3)(suppl):21-35.
PubMedGoogle ScholarCrossref 17.National Institute for Health and Clinical Excellence. The Guidelines Manual. London, UK: National Institute for Health and Clinical Excellence; 2006.
18.Shea
BJ, Grimshaw
JM, Wells
GA,
et al. Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews.
BMC Med Res Methodol. 2007;7:10.
PubMedGoogle ScholarCrossref 20.Whiting
P, Rutjes
AW, Reitsma
JB, Bossuyt
PM, Kleijnen
J. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews.
BMC Med Res Methodol. 2003;3:25.
PubMedGoogle ScholarCrossref 21.Whiting
PF, Rutjes
AW, Westwood
ME,
et al; QUADAS-2 Group. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies.
Ann Intern Med. 2011;155(8):529-536.
PubMedGoogle ScholarCrossref 25.Atkin
WS, Edwards
R, Kralj-Hans
I,
et al; UK Flexible Sigmoidoscopy Trial Investigators. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial.
Lancet. 2010;375(9726):1624-1633.
PubMedGoogle ScholarCrossref 26.Berry
DP, Clarke
P, Hardcastle
JD, Vellacott
KD. Randomized trial of the addition of flexible sigmoidoscopy to faecal occult blood testing for colorectal neoplasia population screening.
Br J Surg. 1997;84(9):1274-1276.
PubMedGoogle ScholarCrossref 27.Brevinge
H, Lindholm
E, Buntzen
S, Kewenter
J. Screening for colorectal neoplasia with faecal occult blood testing compared with flexible sigmoidoscopy directly in a 55-56 years’ old population.
Int J Colorectal Dis. 1997;12(5):291-295.
PubMedGoogle ScholarCrossref 28.Faivre
J, Dancourt
V, Denis
B,
et al. Comparison between a guaiac and three immunochemical faecal occult blood tests in screening for colorectal cancer.
Eur J Cancer. 2012;48(16):2969-2976.
PubMedGoogle ScholarCrossref 29.Faivre
J, Dancourt
V, Lejeune
C,
et al. Reduction in colorectal cancer mortality by fecal occult blood screening in a French controlled study.
Gastroenterology. 2004;126(7):1674-1680.
PubMedGoogle ScholarCrossref 30.Guittet
L, Bouvier
V, Mariotte
N,
et al. Comparison of a guaiac and an immunochemical faecal occult blood test for the detection of colonic lesions according to lesion type and location.
Br J Cancer. 2009;100(8):1230-1235.
PubMedGoogle ScholarCrossref 31.Hamza
S, Dancourt
V, Lejeune
C, Bidan
JM, Lepage
C, Faivre
J. Diagnostic yield of a one sample immunochemical test at different cut-off values in an organised screening programme for colorectal cancer.
Eur J Cancer. 2013;49(12):2727-2733.
PubMedGoogle ScholarCrossref 32.Hol
L, van Leerdam
ME, 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(1):62-68.
PubMedGoogle ScholarCrossref 33.Kronborg
O, Jørgensen
OD, Fenger
C, Rasmussen
M. Randomized study of biennial screening with a faecal occult blood test: results after nine screening rounds.
Scand J Gastroenterol. 2004;39(9):846-851.
PubMedGoogle ScholarCrossref 34.Lindholm
E, Brevinge
H, Haglind
E. Survival benefit in a randomized clinical trial of faecal occult blood screening for colorectal cancer.
Br J Surg. 2008;95(8):1029-1036.
PubMedGoogle ScholarCrossref 35.Malila
N, Palva
T, Malminiemi
O,
et al. Coverage and performance of colorectal cancer screening with the faecal occult blood test in Finland.
J Med Screen. 2011;18(1):18-23.
PubMedGoogle ScholarCrossref 36.Nishihara
R, Wu
K, Lochhead
P,
et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy.
N Engl J Med. 2013;369(12):1095-1105.
PubMedGoogle ScholarCrossref 37.Quintero
E, Castells
A, Bujanda
L,
et al; COLONPREV Study Investigators. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening.
N Engl J Med. 2012;366(8):697-706.
PubMedGoogle ScholarCrossref 38.Rasmussen
M, Kronborg
O, Fenger
C, Jørgensen
OD. Possible advantages and drawbacks of adding flexible sigmoidoscopy to Hemoccult-II in screening for colorectal cancer: a randomized study.
Scand J Gastroenterol. 1999;34(1):73-78.
PubMedGoogle ScholarCrossref 39.Schoen
RE, Pinsky
PF, Weissfeld
JL,
et al; PLCO Project Team. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy.
N Engl J Med. 2012;366(25):2345-2357.
PubMedGoogle ScholarCrossref 40.Scholefield
JH, Moss
SM, Mangham
CM, Whynes
DK, Hardcastle
JD. Nottingham trial of faecal occult blood testing for colorectal cancer: a 20-year follow-up.
Gut. 2012;61(7):1036-1040.
PubMedGoogle ScholarCrossref 41.Segnan
N, Armaroli
P, Bonelli
L,
et al; SCORE Working Group. Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian Randomized Controlled Trial: SCORE.
J Natl Cancer Inst. 2011;103(17):1310-1322.
PubMedGoogle ScholarCrossref 42.Segnan
N, Senore
C, Andreoni
B,
et al; SCORE3 Working Group-Italy. Comparing attendance and detection rate of colonoscopy with sigmoidoscopy and FIT for colorectal cancer screening.
Gastroenterology. 2007;132(7):2304-2312.
PubMedGoogle ScholarCrossref 43.Segnan
N, Senore
C, Andreoni
B,
et al; SCORE2 Working Group-Italy. Randomized trial of different screening strategies for colorectal cancer: patient response and detection rates.
J Natl Cancer Inst. 2005;97(5):347-357.
PubMedGoogle ScholarCrossref 44.Shaukat
A, Mongin
SJ, Geisser
MS,
et al. Long-term mortality after screening for colorectal cancer.
N Engl J Med. 2013;369(12):1106-1114.
PubMedGoogle ScholarCrossref 45.Stoop
EM, de Haan
MC, de Wijkerslooth
TR,
et al. Participation and yield of colonoscopy versus non-cathartic CT colonography in population-based screening for colorectal cancer: a randomised controlled trial.
Lancet Oncol. 2012;13(1):55-64.
PubMedGoogle ScholarCrossref 46.van Roon
AH, Goede
SL, van Ballegooijen
M,
et al. Random comparison of repeated faecal immunochemical testing at different intervals for population-based colorectal cancer screening.
Gut. 2013;62(3):409-415.
PubMedGoogle ScholarCrossref 47.van Rossum
LG, van Rijn
AF, Laheij
RJ,
et al. Random comparison of guaiac and immunochemical fecal occult blood tests for colorectal cancer in a screening population.
Gastroenterology. 2008;135(1):82-90.
PubMedGoogle ScholarCrossref 48.Verne
JECW, Aubrey
R, Love
SB, Talbot
IC, Northover
JM. Population based randomized study of uptake and yield of screening by flexible sigmoidoscopy compared with screening by faecal occult blood testing.
BMJ. 1998;317(7152):182-185.
PubMedGoogle ScholarCrossref 49.Zubero
MB, Arana-Arri
E, Pijoan
JI,
et al. Population-based colorectal cancer screening: comparison of two fecal occult blood test.
Front Pharmacol. 2014;4:175.
PubMedGoogle ScholarCrossref 50.Atkin
WS, Cook
CF, Cuzick
J, Edwards
R, Northover
JM, Wardle
J; UK Flexible Sigmoidoscopy Screening Trial Investigators. Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial.
Lancet. 2002;359(9314):1291-1300.
PubMedGoogle ScholarCrossref 51.Atkin
WS, Cuzick
J, Northover
JM, Whynes
DK. Prevention of colorectal cancer by once-only sigmoidoscopy.
Lancet. 1993;341(8847):736-740.
PubMedGoogle ScholarCrossref 52.Bretthauer
M, Gondal
G, Larsen
K,
et al. Design, organization and management of a controlled population screening study for detection of colorectal neoplasia: attendance rates in the NORCCAP study (Norwegian Colorectal Cancer Prevention).
Scand J Gastroenterol. 2002;37(5):568-573.
PubMedGoogle ScholarCrossref 53.de Wijkerslooth
TR, de Haan
MC, Stoop
EM,
et al. Study protocol: population screening for colorectal cancer by colonoscopy or CT colonography: a randomized controlled trial.
BMC Gastroenterol. 2010;10:47.
PubMedGoogle ScholarCrossref 54.Denters
MJ, Deutekom
M, Bossuyt
PM, Stroobants
AK, Fockens
P, Dekker
E. Lower risk of advanced neoplasia among patients with a previous negative result from a fecal test for colorectal cancer.
Gastroenterology. 2012;142(3):497-504.
PubMedGoogle ScholarCrossref 55.Denters
MJ, Deutekom
M, Fockens
P, Bossuyt
PM, Dekker
E. Implementation of population screening for colorectal cancer by repeated fecal occult blood test in the Netherlands.
BMC Gastroenterol. 2009;9:28.
PubMedGoogle ScholarCrossref 56.Faivre
J, Dancourt
V, Manfredi
S,
et al. Positivity rates and performances of immunochemical faecal occult blood tests at different cut-off levels within a colorectal cancer screening programme.
Dig Liver Dis. 2012;44(8):700-704.
PubMedGoogle ScholarCrossref 57.Guittet
L, Bouvier
V, Guillaume
E,
et al. Colorectal cancer screening: why immunochemical faecal occult blood test performs as well with either one or two samples.
Dig Liver Dis. 2012;44(8):694-699.
PubMedGoogle ScholarCrossref 58.Guittet
L, Bouvier
V, Mariotte
N,
et al. Performance of immunochemical faecal occult blood test in colorectal cancer screening in average-risk population according to positivity threshold and number of samples.
Int J Cancer. 2009;125(5):1127-1133.
PubMedGoogle ScholarCrossref 59.Hardcastle
JD, Chamberlain
JO, Robinson
MH,
et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer.
Lancet. 1996;348(9040):1472-1477.
PubMedGoogle ScholarCrossref 60.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(6):606-615.
PubMedGoogle ScholarCrossref 61.Kewenter
J, Brevinge
H, Engarås
B, Haglind
E, Ahrén
C. Results of screening, rescreening, and follow-up in a prospective randomized study for detection of colorectal cancer by fecal occult blood testing: results for 68,308 subjects.
Scand J Gastroenterol. 1994;29(5):468-473.
PubMedGoogle ScholarCrossref 62.Malila
N, Oivanen
T, Malminiemi
O, Hakama
M. Test, episode, and programme sensitivities of screening for colorectal cancer as a public health policy in Finland: experimental design.
BMJ. 2008;337:a2261.
PubMedGoogle ScholarCrossref 63.Mandel
JS, Church
TR, Bond
JH,
et al. The effect of fecal occult-blood screening on the incidence of colorectal cancer.
N Engl J Med. 2000;343(22):1603-1607.
PubMedGoogle ScholarCrossref 64.Mandel
JS, Bond
JH, Church
TR,
et al. Reducing mortality from colorectal cancer by screening for fecal occult blood: Minnesota Colon Cancer Control Study.
N Engl J Med. 1993;328(19):1365-1371.
PubMedGoogle ScholarCrossref 65.Parra-Blanco
A, Nicolas-Perez
D, Gimeno-Garcia
A,
et al. The timing of bowel preparation before colonoscopy determines the quality of cleansing, and is a significant factor contributing to the detection of flat lesions: a randomized study.
World J Gastroenterol. 2006;12(38):6161-6166.
PubMedGoogle ScholarCrossref 66.Segnan
N, Senore
C, Andreoni
B,
et al; SCORE Working Group-Italy. Baseline findings of the Italian multicenter randomized controlled trial of “once-only sigmoidoscopy”: SCORE.
J Natl Cancer Inst. 2002;94(23):1763-1772.
PubMedGoogle ScholarCrossref 67.Thomas
W, White
CM, Mah
J, Geisser
MS, Church
TR, Mandel
JS. Longitudinal compliance with annual screening for fecal occult blood: Minnesota Colon Cancer Control Study.
Am J Epidemiol. 1995;142(2):176-182.
PubMedGoogle Scholar 68.Atkin
WS, Cook
CF, Cuzick
J, Edwards
R, Northover
JM, Wardle
J; UK Flexible Sigmoidoscopy Screening Trial Investigators. Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial.
Lancet. 2002;359(9314):1291-1300.
PubMedGoogle ScholarCrossref 69.van Roon
AH, Wilschut
JA, Hol
L,
et al. Diagnostic yield improves with collection of 2 samples in fecal immunochemical test screening without affecting attendance.
Clin Gastroenterol Hepatol. 2011;9(4):333-339.
PubMedGoogle ScholarCrossref 70.van Dam
L, de Wijkerslooth
TR, de Haan
MC,
et al. Time requirements and health effects of participation in colorectal cancer screening with colonoscopy or computed tomography colonography in a randomized controlled trial.
Endoscopy. 2013;45(3):182-188.
PubMedGoogle ScholarCrossref 71.Weissfeld
JL, Schoen
RE, Pinsky
PF,
et al; PLCO Project Team. Flexible sigmoidoscopy in the PLCO cancer screening trial: results from the baseline screening examination of a randomized trial.
J Natl Cancer Inst. 2005;97(13):989-997.
PubMedGoogle ScholarCrossref 72.Allison
JE, Sakoda
LC, Levin
TR,
et al. Screening for colorectal neoplasms with new fecal occult blood tests: update on performance characteristics.
J Natl Cancer Inst. 2007;99(19):1462-1470.
PubMedGoogle ScholarCrossref 73.Allison
JE, Tekawa
IS, Ransom
LJ, Adrain
AL. A comparison of fecal occult-blood tests for colorectal-cancer screening.
N Engl J Med. 1996;334(3):155-159.
PubMedGoogle ScholarCrossref 74.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(14):3049-3054.
PubMedGoogle ScholarCrossref 75.Castiglione
G, Visioli
CB, 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(11):1750-1754.
PubMedGoogle ScholarCrossref 76.Chen
LS, Yen
AM, Chiu
SY, Liao
CS, Chen
HH. Baseline faecal occult blood concentration as a predictor of incident colorectal neoplasia: longitudinal follow-up of a Taiwanese population-based colorectal cancer screening cohort.
Lancet Oncol. 2011;12(6):551-558.
PubMedGoogle ScholarCrossref 77.Cheng
TI, Wong
JM, Hong
CF,
et al. Colorectal cancer screening in asymptomatic adults: comparison of colonoscopy, sigmoidoscopy and fecal occult blood tests.
J Formos Med Assoc. 2002;101(10):685-690.
PubMedGoogle Scholar 78.Chiu
HM, Lee
YC, Tu
CH,
et al. Association between early stage colon neoplasms and false-negative results from the fecal immunochemical test.
Clin Gastroenterol Hepatol. 2013;11(7):832-8.e1,2.
PubMedGoogle ScholarCrossref 79.Church
TR, Wandell
M, Lofton-Day
C,
et al; PRESEPT Clinical Study Steering Committee, Investigators and Study Team. Prospective evaluation of methylated
SEPT9 in plasma for detection of asymptomatic colorectal cancer.
Gut. 2014;63(2):317-325.
PubMedGoogle ScholarCrossref 80.de Wijkerslooth
TR, Stoop
EM, Bossuyt
PM,
et al. Immunochemical fecal occult blood testing is equally sensitive for proximal and distal advanced neoplasia.
Am J Gastroenterol. 2012;107(10):1570-1578.
PubMedGoogle ScholarCrossref 81.Fletcher
JG, Silva
AC, Fidler
JL,
et al. Noncathartic CT colonography: image quality assessment and performance and in a screening cohort.
AJR Am J Roentgenol. 2013;201(4):787-794.
PubMedGoogle ScholarCrossref 82.Graser
A, Stieber
P, Nagel
D,
et al. Comparison of CT colonography, colonoscopy, sigmoidoscopy and faecal occult blood tests for the detection of advanced adenoma in an average risk population.
Gut. 2009;58(2):241-248.
PubMedGoogle ScholarCrossref 83.Imperiale
TF, Ransohoff
DF, Itzkowitz
SH,
et al. Multitarget stool DNA testing for colorectal-cancer screening.
N Engl J Med. 2014;370(14):1287-1297.
PubMedGoogle ScholarCrossref 84.Itoh
M, Takahashi
K, Nishida
H, Sakagami
K, Okubo
T. Estimation of the optimal cut off point in a new immunological faecal occult blood test in a corporate colorectal cancer screening programme.
J Med Screen. 1996;3(2):66-71.
PubMedGoogle Scholar 85.Johnson
CD, Chen
MH, Toledano
AY,
et al. Accuracy of CT colonography for detection of large adenomas and cancers.
N Engl J Med. 2008;359(12):1207-1217.
PubMedGoogle ScholarCrossref 86.Johnson
CD, Fletcher
JG, MacCarty
RL,
et al. Effect of slice thickness and primary 2D versus 3D virtual dissection on colorectal lesion detection at CT colonography in 452 asymptomatic adults.
AJR Am J Roentgenol. 2007;189(3):672-680.
PubMedGoogle ScholarCrossref 87.Kim
YS, Kim
N, Kim
SH,
et al. The efficacy of intravenous contrast-enhanced 16-raw multidetector CT colonography for detecting patients with colorectal polyps in an asymptomatic population in Korea.
J Clin Gastroenterol. 2008;42(7):791-798.
PubMedGoogle ScholarCrossref 88.Launoy
GD, Bertrand
HJ, Berchi
C,
et al. Evaluation of an immunochemical fecal occult blood test with automated reading in screening for colorectal cancer in a general average-risk population.
Int J Cancer. 2005;115(3):493-496.
PubMedGoogle ScholarCrossref 89.Lefere
P, Silva
C, Gryspeerdt
S,
et al. Teleradiology based CT colonography to screen a population group of a remote island; at average risk for colorectal cancer.
Eur J Radiol. 2013;82(6):e262-e267.
PubMedGoogle ScholarCrossref 90.Levi
Z, Birkenfeld
S, Vilkin
A,
et al. A higher detection rate for colorectal cancer and advanced adenomatous polyp for screening with immunochemical fecal occult blood test than guaiac fecal occult blood test, despite lower compliance rate: a prospective, controlled, feasibility study.
Int J Cancer. 2011;128(10):2415-2424.
PubMedGoogle ScholarCrossref 91.Levy
BT, Bay
C, Xu
Y,
et al. Test characteristics of faecal immunochemical tests (FIT) compared with optical colonoscopy.
J Med Screen. 2014;21(3):133-143.
PubMedGoogle ScholarCrossref 92.Lin
JS, Webber
EM, Beil
TL, Goddard
KA, Whitlock
EP. Fecal DNA Testing in Screening for Colorectal Cancer in Average-Risk Adults. Rockville, MD: Agency for Healthcare Research and Quality; 2012. AHRQ publication 12-EHC022-EF.
93.Macari
M, Bini
EJ, Jacobs
SL,
et al. Colorectal polyps and cancers in asymptomatic average-risk patients: evaluation with CT colonography.
Radiology. 2004;230(3):629-636.
PubMedGoogle ScholarCrossref 94.Morikawa
T, Kato
J, Yamaji
Y, Wada
R, Mitsushima
T, Shiratori
Y. A comparison of the immunochemical fecal occult blood test and total colonoscopy in the asymptomatic population.
Gastroenterology. 2005;129(2):422-428.
PubMedGoogle ScholarCrossref 95.Nakama
H, Yamamoto
M, Kamijo
N,
et al. Colonoscopic evaluation of immunochemical fecal occult blood test for detection of colorectal neoplasia.
Hepatogastroenterology. 1999;46(25):228-231.
PubMedGoogle Scholar 96.Nakama
H, Kamijo
N, Abdul Fattah
AS, Zhang
B. Validity of immunochemical faecal occult blood screening for colorectal cancer: a follow up study.
J Med Screen. 1996;3(2):63-65.
PubMedGoogle Scholar 97.Ng
SC, Ching
JY, Chan
V,
et al. Diagnostic accuracy of faecal immunochemical test for screening individuals with a family history of colorectal cancer.
Aliment Pharmacol Ther. 2013;38(7):835-841.
PubMedGoogle ScholarCrossref 98.Park
DI, Ryu
S, Kim
YH,
et al. Comparison of guaiac-based and quantitative immunochemical fecal occult blood testing in a population at average risk undergoing colorectal cancer screening.
Am J Gastroenterol. 2010;105(9):2017-2025.
PubMedGoogle ScholarCrossref 99.Pickhardt
PJ, Choi
JR, Hwang
I,
et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults.
N Engl J Med. 2003;349(23):2191-2200.
PubMedGoogle ScholarCrossref 100.Sohn
DK, Jeong
SY, Choi
HS,
et al. Single immunochemical fecal occult blood test for detection of colorectal neoplasia.
Cancer Res Treat. 2005;37(1):20-23.
PubMedGoogle ScholarCrossref 101.Zalis
ME, Blake
MA, Cai
W,
et al. Diagnostic accuracy of laxative-free computed tomographic colonography for detection of adenomatous polyps in asymptomatic adults: a prospective evaluation.
Ann Intern Med. 2012;156(10):692-702.
PubMedGoogle ScholarCrossref 102.Chiang
TH, Chuang
SL, Chen
SL,
et al. Difference in performance of fecal immunochemical tests with the same hemoglobin cutoff concentration in a nationwide colorectal cancer screening program.
Gastroenterology. 2014;147(6):1317-1326.
PubMedGoogle ScholarCrossref 103.Hernandez
V, Cubiella
J, Gonzalez-Mao
MC,
et al; COLONPREV Study Investigators. Fecal immunochemical test accuracy in average-risk colorectal cancer screening.
World J Gastroenterol. 2014;20(4):1038-1047.
PubMedGoogle ScholarCrossref 104.Lee
YH, Hur
M, Kim
H,
et al. Optimal cut-off concentration for a faecal immunochemical test for haemoglobin by Hemo Techt NS-Plus C15 system for the colorectal cancer screening.
Clin Chem Lab Med. 2015;53(3):e69-e71.
PubMedGoogle ScholarCrossref 106.Ahlquist
DA, Sargent
DJ, Loprinzi
CL,
et al. Stool DNA and occult blood testing for screen detection of colorectal neoplasia.
Ann Intern Med. 2008;149(7):441-450,W81.
PubMedGoogle ScholarCrossref 107.Brenner
H, Haug
U, Hundt
S. Inter-test agreement and quantitative cross-validation of immunochromatographical fecal occult blood tests.
Int J Cancer. 2010;127(7):1643-1649.
PubMedGoogle ScholarCrossref 108.Brenner
H, Haug
U, Hundt
S. Sex differences in performance of fecal occult blood testing.
Am J Gastroenterol. 2010;105(11):2457-2464.
PubMedGoogle ScholarCrossref 109.Grazzini
G, Castiglione
G, Ciabattoni
C,
et al. Colorectal cancer screening programme by faecal occult blood test in Tuscany: first round results.
Eur J Cancer Prev. 2004;13(1):19-26.
PubMedGoogle ScholarCrossref 110.Haug
U, Kuntz
KM, Knudsen
AB, Hundt
S, Brenner
H. Sensitivity of immunochemical faecal occult blood testing for detecting left- vs right-sided colorectal neoplasia.
Br J Cancer. 2011;104(11):1779-1785.
PubMedGoogle ScholarCrossref 111.Haug
U, Hillebrand
T, Bendzko
P,
et al. Mutant-enriched PCR and allele-specific hybridization reaction to detect K-ras mutations in stool DNA: high prevalence in a large sample of older adults.
Clin Chem. 2007;53(4):787-790.
PubMedGoogle ScholarCrossref 112.Hundt
S, Haug
U, Brenner
H. Comparative evaluation of immunochemical fecal occult blood tests for colorectal adenoma detection.
Ann Intern Med. 2009;150(3):162-169.
PubMedGoogle ScholarCrossref 113.Imperiale
TF, Ransohoff
DF, Itzkowitz
SH, Turnbull
BA, Ross
ME; Colorectal Cancer Study Group. Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population.
N Engl J Med. 2004;351(26):2704-2714.
PubMedGoogle ScholarCrossref 114.Johnson
CD, Herman
BA, Chen
MH,
et al. The National CT Colonography Trial: assessment of accuracy in participants 65 years of age and older.
Radiology. 2012;263(2):401-408.
PubMedGoogle ScholarCrossref 115.Morikawa
T, Kato
J, Yamaji
Y,
et al. Sensitivity of immunochemical fecal occult blood test to small colorectal adenomas.
Am J Gastroenterol. 2007;102(10):2259-2264.
PubMedGoogle ScholarCrossref 116.Adeyemo
A, Bannazadeh
M, Riggs
T, Shellnut
J, Barkel
D, Wasvary
H. Does sedation type affect colonoscopy perforation rates?
Dis Colon Rectum. 2014;57(1):110-114.
PubMedGoogle ScholarCrossref 117.Adler
A, Wegscheider
K, Lieberman
D,
et al. Factors determining the quality of screening colonoscopy: a prospective study on adenoma detection rates, from 12,134 examinations (Berlin colonoscopy project 3, BECOP-3).
Gut. 2013;62(2):236-241.
PubMedGoogle ScholarCrossref 118.An
S, Lee
KH, Kim
YH,
et al. Screening CT colonography in an asymptomatic average-risk Asian population: a 2-year experience in a single institution.
AJR Am J Roentgenol. 2008;191(3):W100-W106.
PubMedGoogle ScholarCrossref 119.Arora
G, Mannalithara
A, Singh
G, Gerson
LB, Triadafilopoulos
G. Risk of perforation from a colonoscopy in adults: a large population-based study.
Gastrointest Endosc. 2009;69(3 pt 2):654-664.
PubMedGoogle ScholarCrossref 120.Bair
D, Pham
J, Seaton
MB, Arya
N, Pryce
M, Seaton
TL. The quality of screening colonoscopies in an office-based endoscopy clinic.
Can J Gastroenterol. 2009;23(1):41-47.
PubMedGoogle ScholarCrossref 121.Berhane
C, Denning
D. Incidental finding of colorectal cancer in screening colonoscopy and its cost effectiveness.
Am Surg. 2009;75(8):699-703.
PubMedGoogle Scholar 122.Bielawska
B, Day
AG, Lieberman
DA, Hookey
LC. Risk factors for early colonoscopic perforation include non-gastroenterologist endoscopists: a multivariable analysis.
Clin Gastroenterol Hepatol. 2014;12(1):85-92.
PubMedGoogle ScholarCrossref 123.Blotière
PO, Weill
A, Ricordeau
P, Alla
F, Allemand
H. Perforations and haemorrhages after colonoscopy in 2010: a study based on comprehensive French health insurance data (SNIIRAM).
Clin Res Hepatol Gastroenterol. 2014;38(1):112-117.
PubMedGoogle ScholarCrossref 124.Bokemeyer
B, Bock
H, Hüppe
D,
et al. Screening colonoscopy for colorectal cancer prevention: results from a German online registry on 269000 cases.
Eur J Gastroenterol Hepatol. 2009;21(6):650-655.
PubMedGoogle ScholarCrossref 125.Cash
BD, Riddle
MS, Bhattacharya
I,
et al. CT colonography of a Medicare-aged population: outcomes observed in an analysis of more than 1400 patients.
AJR Am J Roentgenol. 2012;199(1):W27-W34.
PubMedGoogle ScholarCrossref 126.Castro
G, Azrak
MF, Seeff
LC, Royalty
J. Outpatient colonoscopy complications in the CDC’s Colorectal Cancer Screening Demonstration Program: a prospective analysis.
Cancer. 2013;119(suppl 15):2849-2854.
PubMedGoogle ScholarCrossref 127.Chin
M, Mendelson
R, Edwards
J, Foster
N, Forbes
G. Computed tomographic colonography: prevalence, nature, and clinical significance of extracolonic findings in a community screening program.
Am J Gastroenterol. 2005;100(12):2771-2776.
PubMedGoogle ScholarCrossref 128.Chukmaitov
A, Bradley
CJ, Dahman
B, Siangphoe
U, Warren
JL, Klabunde
CN. Association of polypectomy techniques, endoscopist volume, and facility type with colonoscopy complications.
Gastrointest Endosc. 2013;77(3):436-446.
PubMedGoogle ScholarCrossref 129.Cooper
GS, Kou
TD, Rex
DK. Complications following colonoscopy with anesthesia assistance: a population-based analysis.
JAMA Intern Med. 2013;173(7):551-556.
PubMedGoogle ScholarCrossref 130.Cotterill
M, Gasparelli
R, Kirby
E. Colorectal cancer detection in a rural community: development of a colonoscopy screening program.
Can Fam Physician. 2005;51:1224-1228.
PubMedGoogle Scholar 131.Crispin
A, Birkner
B, Munte
A, Nusko
G, Mansmann
U. Process quality and incidence of acute complications in a series of more than 230,000 outpatient colonoscopies.
Endoscopy. 2009;41(12):1018-1025.
PubMedGoogle ScholarCrossref 132.Dancourt
V, Lejeune
C, Lepage
C, Gailliard
MC, Meny
B, Faivre
J. Immunochemical faecal occult blood tests are superior to guaiac-based tests for the detection of colorectal neoplasms.
Eur J Cancer. 2008;44(15):2254-2258.
PubMedGoogle ScholarCrossref 133.Dominitz
JA, Baldwin
LM, Green
P, Kreuter
WI, Ko
CW. Regional variation in anesthesia assistance during outpatient colonoscopy is not associated with differences in polyp detection or complication rates.
Gastroenterology. 2013;144(2):298-306.
PubMedGoogle ScholarCrossref 134.Durbin
JM, Stroup
SP, Altamar
HO, L’esperance
JO, Lacey
DR, Auge
BK. Genitourinary abnormalities in an asymptomatic screening population: findings on virtual colonoscopy.
Clin Nephrol. 2012;77(3):204-210.
PubMedGoogle ScholarCrossref 135.Edwards
JT, Mendelson
RM, Fritschi
L,
et al. Colorectal neoplasia screening with CT colonography in average-risk asymptomatic subjects: community-based study.
Radiology. 2004;230(2):459-464.
PubMedGoogle ScholarCrossref 136.Ferlitsch
M, Reinhart
K, Pramhas
S,
et al. Sex-specific prevalence of adenomas, advanced adenomas, and colorectal cancer in individuals undergoing screening colonoscopy.
JAMA. 2011;306(12):1352-1358.
PubMedGoogle ScholarCrossref 137.Flicker
MS, Tsoukas
AT, Hazra
A, Dachman
AH. Economic impact of extracolonic findings at computed tomographic colonography.
J Comput Assist Tomogr. 2008;32(4):497-503.
PubMedGoogle ScholarCrossref 138.Ginnerup Pedersen
B, Rosenkilde
M, Christiansen
TE, Laurberg
S. Extracolonic findings at computed tomography colonography are a challenge.
Gut. 2003;52(12):1744-1747.
PubMedGoogle ScholarCrossref 139.Gluecker
TM, Johnson
CD, Wilson
LA,
et al. Extracolonic findings at CT colonography: evaluation of prevalence and cost in a screening population.
Gastroenterology. 2003;124(4):911-916.
PubMedGoogle ScholarCrossref 140.Hamdani
U, Naeem
R, Haider
F,
et al. Risk factors for colonoscopic perforation: a population-based study of 80118 cases.
World J Gastroenterol. 2013;19(23):3596-3601.
PubMedGoogle ScholarCrossref 141.Hara
AK, Johnson
CD, MacCarty
RL, Welch
TJ. Incidental extracolonic findings at CT colonography.
Radiology. 2000;215(2):353-357.
PubMedGoogle ScholarCrossref 142.Ho
JM, Gruneir
A, Fischer
HD,
et al. Serious events in older Ontario residents receiving bowel preparations for outpatient colonoscopy with various comorbidity profiles: a descriptive, population-based study.
Can J Gastroenterol. 2012;26(7):436-440.
PubMedGoogle ScholarCrossref 143.Hoff
G, Thiis-Evensen
E, Grotmol
T, Sauar
J, Vatn
MH, Moen
IE. Do undesirable effects of screening affect all-cause mortality in flexible sigmoidoscopy programmes? experience from the Telemark Polyp Study 1983-1996.
Eur J Cancer Prev. 2001;10(2):131-137.
PubMedGoogle ScholarCrossref 144.Hsieh
TK, Hung
L, Kang
FC, Lan
KM, Poon
PW, So
EC. Anesthesia does not increase the rate of bowel perforation during colonoscopy: a retrospective study.
Acta Anaesthesiol Taiwan. 2009;47(4):162-166.
PubMedGoogle ScholarCrossref 145.Iafrate
F, Iussich
G, Correale
L,
et al. Adverse events of computed tomography colonography: an Italian National Survey.
Dig Liver Dis. 2013;45(8):645-650.
PubMedGoogle ScholarCrossref 146.Jain
A, Falzarano
J, Jain
A, Decker
R, Okubo
G, Fujiwara
D. Outcome of 5,000 flexible sigmoidoscopies done by nurse endoscopists for colorectal screening in asymptomatic patients.
Hawaii Med J. 2002;61(6):118-120.
PubMedGoogle Scholar 147.Kamath
AS, Iqbal
CW, Sarr
MG,
et al. Colonoscopic splenic injuries: incidence and management.
J Gastrointest Surg. 2009;13(12):2136-2140.
PubMedGoogle ScholarCrossref 149.Kao
KT, Jain
A, Sheinbaum
A. Ischemic colitis following routine screening colonoscopy: a case report.
Endoscopy. 2009;41(suppl 2):E100.
PubMedGoogle ScholarCrossref 150.Kim
DH, Pickhardt
PJ, Taylor
AJ,
et al. CT colonography versus colonoscopy for the detection of advanced neoplasia.
N Engl J Med. 2007;357(14):1403-1412.
PubMedGoogle ScholarCrossref 151.Kim
JS, Kim
BW, Kim
JI,
et al. Endoscopic clip closure versus surgery for the treatment of iatrogenic colon perforations developed during diagnostic colonoscopy: a review of 115,285 patients.
Surg Endosc. 2013;27(2):501-504.
PubMedGoogle ScholarCrossref 152.Kim
YS, Kim
N, Kim
SY,
et al. Extracolonic findings in an asymptomatic screening population undergoing intravenous contrast-enhanced computed tomography colonography.
J Gastroenterol Hepatol. 2008;23(7 pt 2):e49-e57.
PubMedGoogle ScholarCrossref 153.Ko
CW, Riffle
S, Shapiro
JA,
et al. Incidence of minor complications and time lost from normal activities after screening or surveillance colonoscopy.
Gastrointest Endosc. 2007;65(4):648-656.
PubMedGoogle ScholarCrossref 154.Korman
LY, Overholt
BF, Box
T, Winker
CK. Perforation during colonoscopy in endoscopic ambulatory surgical centers.
Gastrointest Endosc. 2003;58(4):554-557.
PubMedGoogle ScholarCrossref 155.Layton
JB, Klemmer
PJ, Christiansen
CF,
et al. Sodium phosphate does not increase risk for acute kidney injury after routine colonoscopy, compared with polyethylene glycol.
Clin Gastroenterol Hepatol. 2014;12(9):1514-1521.
PubMedGoogle ScholarCrossref 156.Levin
TR, Zhao
W, Conell
C,
et al. Complications of colonoscopy in an integrated health care delivery system.
Ann Intern Med. 2006;145(12):880-886.
PubMedGoogle ScholarCrossref 157.Levin
TR, Conell
C, Shapiro
JA, Chazan
SG, Nadel
MR, Selby
JV. Complications of screening flexible sigmoidoscopy.
Gastroenterology. 2002;123(6):1786-1792.
PubMedGoogle ScholarCrossref 158.Loffeld
RJ, Engel
A, Dekkers
PE. Incidence and causes of colonoscopic perforations: a single-center case series.
Endoscopy. 2011;43(3):240-242.
PubMedGoogle ScholarCrossref 159.Lorenzo-Zúñiga
V, Moreno de Vega
V, Doménech
E, Mañosa
M, Planas
R, Boix
J. Endoscopist experience as a risk factor for colonoscopic complications.
Colorectal Dis. 2010;12(10 online):e273-e277.
PubMedGoogle ScholarCrossref 160.Macari
M, Nevsky
G, Bonavita
J, Kim
DC, Megibow
AJ, Babb
JS. CT colonography in senior versus nonsenior patients: extracolonic findings, recommendations for additional imaging, and polyp prevalence.
Radiology. 2011;259(3):767-774.
PubMedGoogle ScholarCrossref 161.Mansmann
U, Crispin
A, Henschel
V,
et al. Epidemiology and quality control of 245 000 outpatient colonoscopies.
Dtsch Arztebl Int. 2008;105(24):434-440.
PubMedGoogle Scholar 162.Multicentre Australian Colorectal-neoplasia Screening (MACS) Group. A comparison of colorectal neoplasia screening tests: a multicentre community-based study of the impact of consumer choice.
Med J Aust. 2006;184(11):546-550.
PubMedGoogle Scholar 163.Nelson
DB, McQuaid
KR, Bond
JH, Lieberman
DA, Weiss
DG, Johnston
TK. Procedural success and complications of large-scale screening colonoscopy.
Gastrointest Endosc. 2002;55(3):307-314.
PubMedGoogle ScholarCrossref 164.O’Connor
SD, Pickhardt
PJ, Kim
DH, Oliva
MR, Silverman
SG. Incidental finding of renal masses at unenhanced CT: prevalence and analysis of features for guiding management.
AJR Am J Roentgenol. 2011;197(1):139-145.
PubMedGoogle ScholarCrossref 165.Parente
F, Boemo
C, Ardizzoia
A,
et al. Outcomes and cost evaluation of the first two rounds of a colorectal cancer screening program based on immunochemical fecal occult blood test in northern Italy.
Endoscopy. 2013;45(1):27-34.
PubMedGoogle Scholar 166.Pickhardt
PJ, Boyce
CJ, Kim
DH, Hinshaw
LJ, Taylor
AJ, Winter
TC. Should small sliding hiatal hernias be reported at CT colonography?
AJR Am J Roentgenol. 2011;196(4):W400-W404.
PubMedGoogle ScholarCrossref 167.Pickhardt
PJ, Kim
DH, Meiners
RJ,
et al. Colorectal and extracolonic cancers detected at screening CT colonography in 10,286 asymptomatic adults.
Radiology. 2010;255(1):83-88.
PubMedGoogle ScholarCrossref 168.Pickhardt
PJ, Kim
DH, Taylor
AJ, Gopal
DV, Weber
SM, Heise
CP. Extracolonic tumors of the gastrointestinal tract detected incidentally at screening CT colonography.
Dis Colon Rectum. 2007;50(1):56-63.
PubMedGoogle ScholarCrossref 169.Pickhardt
PJ. Incidence of colonic perforation at CT colonography: review of existing data and implications for screening of asymptomatic adults.
Radiology. 2006;239(2):313-316.
PubMedGoogle ScholarCrossref 170.Pox
CP, Altenhofen
L, Brenner
H, Theilmeier
A, Von Stillfried
D, Schmiegel
W. Efficacy of a nationwide screening colonoscopy program for colorectal cancer.
Gastroenterology. 2012;142(7):1460-1467.
PubMedGoogle ScholarCrossref 171.Quallick
MR, Brown
WR. Rectal perforation during colonoscopic retroflexion: a large, prospective experience in an academic center.
Gastrointest Endosc. 2009;69(4):960-963.
PubMedGoogle ScholarCrossref 172.Rabeneck
L, Paszat
LF, Hilsden
RJ,
et al. Bleeding and perforation after outpatient colonoscopy and their risk factors in usual clinical practice.
Gastroenterology. 2008;135(6):1899-1906.
PubMedGoogle ScholarCrossref 173.Rathgaber
SW, Wick
TM. Colonoscopy completion and complication rates in a community gastroenterology practice.
Gastrointest Endosc. 2006;64(4):556-562.
PubMedGoogle ScholarCrossref 174.Rutter
CM, Johnson
E, Miglioretti
DL, Mandelson
MT, Inadomi
J, Buist
DS. Adverse events after screening and follow-up colonoscopy.
Cancer Causes Control. 2012;23(2):289-296.
PubMedGoogle ScholarCrossref 175.Sagawa
T, Kakizaki
S, Iizuka
H,
et al. Analysis of colonoscopic perforations at a local clinic and a tertiary hospital.
World J Gastroenterol. 2012;18(35):4898-4904.
PubMedGoogle ScholarCrossref 176.Senore
C, Ederle
A, Fantin
A,
et al. Acceptability and side-effects of colonoscopy and sigmoidoscopy in a screening setting.
J Med Screen. 2011;18(3):128-134.
PubMedGoogle ScholarCrossref 177.Sieg
A, Hachmoeller-Eisenbach
U, Eisenbach
T. Prospective evaluation of complications in outpatient GI endoscopy: a survey among German gastroenterologists.
Gastrointest Endosc. 2001;53(6):620-627.
PubMedGoogle ScholarCrossref 178.Singh
H, Penfold
RB, DeCoster
C,
et al. Colonoscopy and its complications across a Canadian regional health authority.
Gastrointest Endosc. 2009;69(3 pt 2):665-671.
PubMedGoogle ScholarCrossref 179.Sosna
J, Blachar
A, Amitai
M,
et al. Colonic perforation at CT colonography: assessment of risk in a multicenter large cohort.
Radiology. 2006;239(2):457-463.
PubMedGoogle ScholarCrossref 180.Stock
C, Ihle
P, Sieg
A, Schubert
I, Hoffmeister
M, Brenner
H. Adverse events requiring hospitalization within 30 days after outpatient screening and nonscreening colonoscopies.
Gastrointest Endosc. 2013;77(3):419-429.
PubMedGoogle ScholarCrossref 181.Strul
H, Kariv
R, Leshno
M,
et al. The prevalence rate and anatomic location of colorectal adenoma and cancer detected by colonoscopy in average-risk individuals aged 40-80 years.
Am J Gastroenterol. 2006;101(2):255-262.
PubMedGoogle ScholarCrossref 182.Suissa
A, Bentur
OS, Lachter
J,
et al. Outcome and complications of colonoscopy: a prospective multicenter study in northern Israel.
Diagn Ther Endosc. 2012;2012:612542.
PubMedGoogle ScholarCrossref 183.Tam
MS, Abbas
MA. Perforation following colorectal endoscopy: what happens beyond the endoscopy suite?
Perm J. 2013;17(2):17-21.
PubMedGoogle ScholarCrossref 184.Veerappan
GR, Ally
MR, Choi
JH, Pak
JS, Maydonovitch
C, Wong
RK. Extracolonic findings on CT colonography increases yield of colorectal cancer screening.
AJR Am J Roentgenol. 2010;195(3):677-686.
PubMedGoogle ScholarCrossref 185.Viiala
CH, Olynyk
JK. Outcomes after 10 years of a community-based flexible sigmoidoscopy screening program for colorectal carcinoma.
Med J Aust. 2007;187(5):274-277.
PubMedGoogle Scholar 186.Wallace
MB, Kemp
JA, Meyer
F,
et al. Screening for colorectal cancer with flexible sigmoidoscopy by nonphysician endoscopists.
Am J Med. 1999;107(3):214-218.
PubMedGoogle ScholarCrossref 187.Warren
JL, Klabunde
CN, Mariotto
AB,
et al. Adverse events after outpatient colonoscopy in the Medicare population.
Ann Intern Med. 2009;150(12):849-857,W152.
PubMedGoogle ScholarCrossref 188.Xirasagar
S, Hurley
TG, Sros
L, Hebert
JR. Quality and safety of screening colonoscopies performed by primary care physicians with standby specialist support.
Med Care. 2010;48(8):703-709.
PubMedGoogle ScholarCrossref 189.Zafar
HM, Harhay
MO, Yang
J, Armstron
K. Adverse events following computed tomographic colonography compared to optical colonoscopy in the elderly.
Prev Med Rep. 2014;1:3-8.
PubMedGoogle ScholarCrossref 190.Ko
CW, Riffle
S, Michaels
L,
et al. Serious complications within 30 days of screening and surveillance colonoscopy are uncommon.
Clin Gastroenterol Hepatol. 2010;8(2):166-173.
PubMedGoogle ScholarCrossref 191.Atkin
WS, Hart
A, Edwards
R,
et al. Uptake, yield of neoplasia, and adverse effects of flexible sigmoidoscopy screening.
Gut. 1998;42(4):560-565.
PubMedGoogle ScholarCrossref 192.Gondal
G, Grotmol
T, Hofstad
B, Bretthauer
M, Eide
TJ, Hoff
G. The Norwegian Colorectal Cancer Prevention (NORCCAP) screening study: baseline findings and implementations for clinical work-up in age groups 50-64 years.
Scand J Gastroenterol. 2003;38(6):635-642.
PubMedGoogle ScholarCrossref 193.Hoff
G, Grotmol
T, Skovlund
E, Bretthauer
M; Norwegian Colorectal Cancer Prevention Study Group. Risk of colorectal cancer seven years after flexible sigmoidoscopy screening: randomised controlled trial.
BMJ. 2009;338:b1846.
PubMedGoogle ScholarCrossref 194.Hoff
G, Sauar
J, Vatn
MH,
et al. Polypectomy of adenomas in the prevention of colorectal cancer: 10 years’ follow-up of the Telemark Polyp Study I: a prospective, controlled population study.
Scand J Gastroenterol. 1996;31(10):1006-1010.
PubMedGoogle ScholarCrossref 195.Kim
DH, Pickhardt
PJ, Hanson
ME, Hinshaw
JL. CT colonography: performance and program outcome measures in an older screening population.
Radiology. 2010;254(2):493-500.
PubMedGoogle ScholarCrossref 196.Miles
A, Wardle
J, McCaffery
K, Williamson
S, Atkin
W. The effects of colorectal cancer screening on health attitudes and practices.
Cancer Epidemiol Biomarkers Prev. 2003;12(7):651-655.
PubMedGoogle Scholar 197.Pickhardt
PJ, Kim
DH, Robbins
JB. Flat (nonpolypoid) colorectal lesions identified at CT colonography in a US screening population.
Acad Radiol. 2010;17(6):784-790.
PubMedGoogle ScholarCrossref 198.Pickhardt
PJ, Hanson
ME, Vanness
DJ,
et al. Unsuspected extracolonic findings at screening CT colonography: clinical and economic impact.
Radiology. 2008;249(1):151-159.
PubMedGoogle ScholarCrossref 199.Regula
J, Polkowski
M. CT colonography versus colonoscopy for the detection of advanced neoplasia.
N Engl J Med. 2008;358(1):88-89.
PubMedGoogle ScholarCrossref 200.Thiis-Evensen
E, Hoff
GS, Sauar
J, Langmark
F, Majak
BM, Vatn
MH. Population-based surveillance by colonoscopy: effect on the incidence of colorectal cancer: Telemark Polyp Study I.
Scand J Gastroenterol. 1999;34(4):414-420.
PubMedGoogle ScholarCrossref 201.Lord
SJ, Irwig
L, Simes
RJ. When is measuring sensitivity and specificity sufficient to evaluate a diagnostic test, and when do we need randomized trials?
Ann Intern Med. 2006;144(11):850-855.
PubMedGoogle ScholarCrossref 203.Kaminski
MF, Bretthauer
M, Zauber
AG,
et al. The NordICC Study: rationale and design of a randomized trial on colonoscopy screening for colorectal cancer.
Endoscopy. 2012;44(7):695-702.
PubMedGoogle ScholarCrossref 205.Álvarez
C, Andreu
M, Castells
A,
et al; ColonPrev study investigators. Relationship of colonoscopy-detected serrated polyps with synchronous advanced neoplasia in average-risk individuals.
Gastrointest Endosc. 2013;78(2):333-341.
PubMedGoogle ScholarCrossref 207.Committee to Assess Health Risks from Exposure to Low Levels of Ionizing Radiation, Board on Radiation Effects Research, Division on Earth and Life Studies, National Research Council of the National Academies. Health Risks From Exposure to Low Levels of Ionizing Radiation: BEIR VII Phase 2. Washington, DC: National Academies Press; 2006.
208.Cardis
E, Vrijheid
M, Blettner
M,
et al. Risk of cancer after low doses of ionising radiation: retrospective cohort study in 15 countries.
BMJ. 2005;331(7508):77.
PubMedGoogle ScholarCrossref 210.Knudsen
AB, Zauber
AG, Rutter
CM,
et al. Estimation of benefits, burden, and harms of colorectal cancer screening strategies: modeling study for the US Preventive Services Task Force.
JAMA. doi:
10.1001/jama.2016.6828.
Google Scholar