Advertisement

The predictive value of small versus diminutive adenomas for subsequent advanced neoplasia

Published:September 13, 2019DOI:https://doi.org/10.1016/j.gie.2019.08.047

      Background and Aims

      Patients with previous colorectal adenomas are at increased risk of colorectal cancer. Current guidelines for postpolypectomy surveillance intervals treat all tubular adenomas 1 to 9 mm in size with low-grade dysplasia as carrying the same level of risk. We evaluated whether 6 to 9 mm adenomas detected at colonoscopy are associated with greater risk of advanced neoplasia at follow-up compared with baseline 1 to 5 mm adenomas.

      Methods

      We retrospectively evaluated a colonoscopy database at a single U.S. academic center. Patients with baseline examinations demonstrating tubular adenomas 1 to 9 mm in size with low-grade dysplasia and no advanced adenomas were included. Follow-up colonoscopies were performed at least 200 days later and were assessed for incident advanced neoplasia (cancer, high-grade dysplasia, adenoma ≥10 mm in size, or villous elements).

      Results

      There were 2477 qualifying baseline colonoscopies. The absolute risk of metachronous advanced neoplasia increased from 3.6% in patients with 1 to 5 mm adenomas to 6.9% in patients with at least 1 adenoma of 6 to 9 mm (P = .001). Patients with 5 or more adenomas 1 of which was at least 6 to 9 mm had the highest risk of advanced neoplasia at follow-up (10.4%, P = .006). When only screening colonoscopies were considered, all baseline groups (1-2 adenomas, 3-4 adenomas, ≥5 adenomas) with adenomas 6 to 9 mm in size had an increased risk for metachronous advanced neoplasia (odds ratio [OR], 4.07; 95% confidence interval [CI], 1.50-11.04; OR, 4.91; 95% CI, 1.44-16.75; OR, 4.71; 95% CI, 1.30-17.05, respectively).

      Conclusions

      Patients with baseline small (6-9 mm) adenomas have an increased risk of advanced lesions on follow-up compared with patients with only diminutive (1-5 mm) adenomas. Postpolypectomy guidelines should consider risk stratification based on small versus diminutive adenomas.

      Abbreviations:

      ADR (adenoma detection rate), CI (confidence interval), OR (odds ratio), SSP (sessile serrated polyp)

      Introduction

      Patients with previous colorectal adenomas are at increased risk of colorectal cancer, although compared with the general population, the increased risk may be largely confined to those with advanced or multiple (3 or more) adenomas.
      • Winawer S.
      • Zauber A.
      • Ho M.
      • et al.
      Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps.
      • Martinez M.E.
      • Baron J.A.
      • Lieberman D.A.
      • et al.
      A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy.
      • Anderson J.C.
      • Baron J.A.
      • Ahnen D.J.
      • et al.
      Factors associated with shorter colonoscopy surveillance intervals for patients with low-risk colorectal adenomas and effects on outcome.
      • Hassan C.
      • Gimeno-Garcia A.
      • Kalager M.
      • et al.
      Systematic review with meta-analysis: the incidence of advanced neoplasia after polypectomy in patients with and without low-risk adenomas.
      • Dube C.
      • Yakubu M.
      • McCurdy B.R.
      • et al.
      Risk of advanced adenoma, colorectal cancer, and colorectal cancer mortality in people with low-risk adenomas at baseline colonoscopy: a systematic review and meta-analysis.
      • Gupta S.
      • Jacobs E.T.
      • Baron J.A.
      • et al.
      Risk stratification of individuals with low-risk colorectal adenomas using clinical characteristics: a pooled analysis.
      • Click B.
      • Pinsky P.F.
      • Hickey T.
      • et al.
      Association of colonoscopy adenoma findings with long-term colorectal cancer incidence.
      In current postpolypectomy surveillance guidelines,
      • Hassan C.
      • Quintero E.
      • Dumonceau J.M.
      • et al.
      Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) guideline.
      ,
      • Lieberman D.A.
      • Rex D.K.
      • Winawer S.J.
      • et al.
      Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer.
      patients are considered at higher risk if they have had an advanced conventional adenoma (adenoma ≥10 mm, or with high-grade dysplasia or villous elements), or 3 or more adenomas. High-risk patients are recommended to undergo their next surveillance colonoscopy at a shorter interval compared with those who have only 1 or 2 low-risk adenomas (tubular adenomas ≤9 mm in size with only low-grade dysplasia).
      Adenoma detection rates (ADRs) in clinical practice are increasing
      • Pike I.M.
      • Vicari J.
      Incorporating quality measurement and improvement into a gastroenterology practice.
      as a result of increased awareness of the importance of quality on prevention of interval cancers.
      • Kaminski M.F.
      • Regula J.
      • Kraszewska E.
      • et al.
      Quality indicators for colonoscopy and the risk of interval cancer.
      ,
      • Corley D.
      • Jensen C.D.
      • Marks A.R.
      • et al.
      Adenoma detection rate and risk of colorectal cancer and death.
      the availability of registries to facilitate ADR measurements,
      • Pike I.M.
      • Vicari J.
      Incorporating quality measurement and improvement into a gastroenterology practice.
      guidelines that endorse measurement of ADR,
      • Rex D.K.
      • Boland C.R.
      • Dominitz J.A.
      • et al.
      Colorectal cancer screening: recommendations for physicians and patients from the U.S. Multi-Society Task Force on Colorectal Cancer.
      ,
      • Rex D.K.
      • Schoenfeld P.S.
      • Cohen J.
      • et al.
      Quality indicators for colonoscopy.
      and the development of progressively higher-definition colonoscopes as well as add-on devices (eg, mucosal exposure devices).
      • Rex D.K.
      • Repici A.
      • Gross S.A.
      • et al.
      High-definition colonoscopy versus Endocuff versus EndoRings versus full-spectrum endoscopy for adenoma detection at colonoscopy: a multicenter randomized trial.
      As a result, tiny conventional adenomas are being detected in an increasingly large fraction of screening and surveillance populations. Patients with even tiny adenomas are assigned to shorter surveillance intervals, which results in increased cost, risks, and inconvenience to patients, with perhaps limited benefit in cancer protection. Further, the effectiveness of postpolypectomy surveillance is limited by marked variability in the quality of performance of the baseline colonoscopy.
      • Rex D.K.
      • Boland C.R.
      • Dominitz J.A.
      • et al.
      Colorectal cancer screening: recommendations for physicians and patients from the U.S. Multi-Society Task Force on Colorectal Cancer.
      ,
      • Rex D.K.
      • Schoenfeld P.S.
      • Cohen J.
      • et al.
      Quality indicators for colonoscopy.
      Currently, postpolypectomy surveillance guidelines do not account for baseline performance or the ADR of examiners, and generally assume that baseline colonoscopy has uniform performance. Future postpolypectomy surveillance guidelines might be specified to only apply for doctors with ADRs above a certain threshold, or could vary recommended intervals according to the ADR. Longer surveillance intervals could be particularly appropriate for doctors with high ADRs and patients with only tiny adenomas.
      For these reasons, we expect increasing pressure to expand surveillance intervals for patients with tiny adenomas. In this regard, in many postpolypectomy surveillance observational studies, low-risk adenomas include all tubular adenomas 1 to 9 mm in size with only low-grade dysplasia. However, adenoma size is a known predictor of subsequent risk, as has been repeatedly shown for adenomas ≥10 mm in size compared with 1 to 9 mm in size.
      • Winawer S.
      • Zauber A.
      • Ho M.
      • et al.
      Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps.
      • Martinez M.E.
      • Baron J.A.
      • Lieberman D.A.
      • et al.
      A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy.
      • Anderson J.C.
      • Baron J.A.
      • Ahnen D.J.
      • et al.
      Factors associated with shorter colonoscopy surveillance intervals for patients with low-risk colorectal adenomas and effects on outcome.
      • Hassan C.
      • Gimeno-Garcia A.
      • Kalager M.
      • et al.
      Systematic review with meta-analysis: the incidence of advanced neoplasia after polypectomy in patients with and without low-risk adenomas.
      • Dube C.
      • Yakubu M.
      • McCurdy B.R.
      • et al.
      Risk of advanced adenoma, colorectal cancer, and colorectal cancer mortality in people with low-risk adenomas at baseline colonoscopy: a systematic review and meta-analysis.
      • Gupta S.
      • Jacobs E.T.
      • Baron J.A.
      • et al.
      Risk stratification of individuals with low-risk colorectal adenomas using clinical characteristics: a pooled analysis.
      • Click B.
      • Pinsky P.F.
      • Hickey T.
      • et al.
      Association of colonoscopy adenoma findings with long-term colorectal cancer incidence.
      We hypothesized that adenomas 6 to 9 mm in size, often called “small adenomas,” could be associated with a greater risk of subsequent development of advanced neoplasia compared with diminutive adenomas (defined as 1-5 mm in size). Indeed, although most previous studies have lumped 1 to 5 mm and 6 to 9 mm adenomas together, some studies have suggested that small adenomas are associated with a higher risk of subsequent advanced neoplasia than are diminutive adenomas.
      • Moon C.M.
      • Jung S.A.
      • Eun C.S.
      • et al.
      The effect of small or diminutive adenomas at baseline colonoscopy on the risk of developing metachronous advanced colorectal neoplasia: KASID multicenter study.
      ,
      • Sneh Arbib O.
      • Zemser V.
      • Leibovici Weissman Y.
      • et al.
      Risk of advanced lesions at the first follow-up colonoscopy after polypectomy of diminutive versus small adenomatous polyps of low-grade dysplasia.
      In this report, we describe our experience with the risk of subsequent advanced neoplasia in patients with small versus only diminutive conventional adenomas.

      Methods

      A database of colonoscopies conducted at a single center (Indiana University Hospital and an associated outpatient endoscopy center) from 1999 to 2016 was used. The database is updated periodically with procedure information, and we have reported previously on surveillance findings collected from this database.
      • Vemulapalli K.C.
      • Rex D.K.
      Risk of advanced lesions at first follow-up colonoscopy in high-risk groups as defined by the United Kingdom post-polypectomy surveillance guideline: data from a single U.S. center.
      Briefly, the database contains patient demographics, polyp findings, including histology and size, and procedure characteristics, including indication. Completion of the procedure and bowel preparation quality were added to the database in 2012. Permission to review the database for the current study was obtained from the Institutional Review Board at Indiana University on November 21, 2018. The database at this time consisted of procedures from January 1999 to June 2016.
      We identified patients with only diminutive or small adenomas (<10 mm) and categorized them into either having diminutive adenomas or small adenomas and then into 6 groups: 1 to 2 adenomas both ≤5 mm, 1 to 2 adenomas with 1 at least 6 to 9 mm, 3 to 4 adenomas all ≤5 mm, 3 to 4 adenomas with 1 at least 6 to 9 mm, 5 or more adenomas all ≤5 mm, 5 or more adenomas with 1 at least 6 to 9 mm. Polyp size was estimated by the endoscopist at the time of the procedure. Patients with concomitant serrated lesions at baseline were not excluded.
      We excluded patients with inflammatory bowel disease, colon cancer syndromes (familial adenomatous polyposis, hereditary nonpolyposis colorectal cancer, serrated polyposis syndrome), advanced adenomas (≥10 mm tubular adenoma, villous component, high-grade dysplasia), or cancer at or before the baseline colonoscopy. We only included patients who had at least 1 follow-up examination at our institution at least 200 days later than the baseline colonoscopy.

      Outcome measures

      Advanced neoplasia at follow-up was defined as finding a conventional adenoma that was 10 mm or larger, with high-grade dysplasia or villous elements or cancer. We also included sensitivity analyses with an expanded definition of advanced neoplasia that considered a sessile serrated polyp (SSP) with cytological dysplasia or SSP ≥10 mm along with the above-mentioned criteria as the definition for advanced neoplasia. We also performed subgroup analyses first limiting the sample to screening patients and then limiting the sample to patients who had 1 to 2 adenomas with a follow-up interval between 4.5 and 5.5 years.

      Statistical analysis

      We report demographics, interval to follow-up colonoscopy, and advanced neoplasia at follow-up for each group. Analysis of variance was used for continuous variables and chi-squared tests were used for categorical variables. We then assessed the effects of age, gender, bowel preparation quality, indication for baseline colonoscopy, time to follow-up, and our baseline adenoma categories for risk of advanced neoplasia at follow-up using a logistic regression model. We report odds ratios (ORs) with 95% confidence intervals (CIs). All analyses were performed with IBM SPSS Statistics, Version 25 (IBM Corp, Armonk, NY, USA).

      Results

      Among 34,467 patients who underwent procedures from January 1999 to June 2016, we identified 2477 patients who had diminutive or small adenomas at baseline colonoscopy, who never had advanced neoplasia before this examination, and underwent a follow-up examination at least 200 days later at 1 of our institutions (Fig. 1). The largest fraction of the baseline cohort had only 1 or 2 diminutive adenomas (66%). The absolute risk of advanced neoplasia at follow-up was 3.6% among patients with only diminutive adenomas compared with 6.9% among patients with at least 1 small adenoma (71 of 1997 vs 33 of 480, P = .001) (Table 1). We performed 2 separate logistic regression analyses using different adenoma subgroups (Table 2). The first logistic regression indicated that age and the presence of a small adenoma were risk factors for metachronous advanced neoplasia, whereas gender and time to follow-up colonoscopy were not (Table 2). The fraction of baseline bowel preparations that were excellent or good was 89.2%. In the multivariable analysis, excellent or good preparation at baseline was not associated with advanced neoplasia at follow-up colonoscopy (OR, 0.65; 95% CI, 0.32-1.31; P = .229; Table 2).
      Figure thumbnail gr1
      Figure 1Patients excluded from the study. IBD, Inflammatory bowel disease.
      Table 1Demographic features and advanced neoplasia at follow-up in patients with diminutive adenomas (1-5 mm) only and patients with at least 1 small adenoma (6-9 mm) at baseline colonoscopy
      TotalPatients with diminutive adenomas only at baseline colonoscopyPatients with at least 1 small adenoma at baseline colonoscopyP value
      Number24771997480
      Age, years (SD)58.6 (9.7)58.3 (9.7)59.8 (9.5).002
      Male gender, n (%)1382 (55.8)1083 (54.2)299 (62.3).001
      Time to follow-up examination, years (SD)4.5 (2.4)4.6 (2.4)3.8 (2.2)<.001
      6 months to 1 year, n (%)70 (2.8)49 (2.5)21 (4.4)
      1-3 years554 (22.4)413 (20.7)141 (29.4)
      3-5 years884 (35.7)675 (33.8)209 (43.5)
      5+ years969 (39.1)860 (43.1)109 (22.7)
      Excellent or good bowel preparation, n (%)
      Information available for 1740 patients (70.2%).
      1552 (89.2)1242 (90.1)310 (85.6).014
      Indication, n (%).673
      Screening1144 (46.2)931 (46.6)213 (44.4)
      Surveillance767 (31)614 (30.7)153 (31.9)
      Diagnostic566 (22.9)452 (22.6)114 (23.8)
      Advanced neoplasia at follow-up, n (%)104 (4.2)71 (3.6)33 (6.9).001
      Cancer4 (0.2)4 (0.2)0
      HGD7 (0.3)5 (0.3)2 (0.4)
      VA ≥10 mm11 (0.4)8 (0.4)3 (0.6)
      VA<10 mm11 (0.4)7 (0.4)4 (0.8)
      TA ≥10 mm71 (2.9)47 (2.4)24 (5)
      SD, Standard deviation; HGD, high-grade dysplasia; VA, villous or tubulovillous adenoma; TA, tubular adenoma.
      Information available for 1740 patients (70.2%).
      Table 2Risk factors for advanced neoplasia at follow-up in multivariable analysis
      Logistic regression using the enter method.
      FactorOdds ratio (95% confidence interval)P value
      Age (yearly increment)
      Results from the first logistic regression.
      1.05 (1.02-1.08).001
      Gender
      Results from the first logistic regression.
       Female1
       Male0.96 (0.58-1.56).854
      Time to follow-up (per year increment)
      Results from the first logistic regression.
      1.06 (0.94-1.18).353
      Preparation quality
      Results from the first logistic regression.
       Poor/fair1
       Excellent/good0.65 (0.32-1.31).229
      Indication
      Logistic regression using the enter method.
       Screening1
       Polyp surveillance1.44 (0.84-2.47).185
       Diagnostic0.81 (0.38-1.73).581
      Baseline adenoma findings
      Results from the first logistic regression.
       All adenomas ≤5 mm1
       Any adenoma 6-9 mm2.29 (1.38-3.80).001
      Baseline adenoma findings
      Results from the second logistic regression. Results for age, gender, time to follow-up, bowel preparation quality, and indication were nearly identical to the first analysis. Therefore, only the results for adenoma subgroups are shown for the second analysis.
       1-2 adenomas both ≤5 mm1
       1-2 adenomas one 6-9 mm1.63 (0.78-3.39).193
       3-4 adenomas all ≤5 mm0.94 (0.41-2.18).889
       3-4 adenomas one 6-9 mm2.71 (1.14-6.43).024
       ≥5 adenomas all ≤ 5 mm0.99 (0.29-3.36).992
       ≥5 adenomas one 6-9 mm3.31 (1.51-7.28).003
      Logistic regression using the enter method.
      Results from the first logistic regression.
      Results from the second logistic regression. Results for age, gender, time to follow-up, bowel preparation quality, and indication were nearly identical to the first analysis. Therefore, only the results for adenoma subgroups are shown for the second analysis.
      We performed a second logistic regression using more adenoma subgroups (Table 2). In the second analysis, there was only minimal difference in the results for age, gender, years to follow-up, bowel preparation quality, or indication from the first analysis, and the results are only shown for these factors for the first logistic regression in Table 2. The second logistic regression indicated that age (results not shown) and the subcategories of patients with at least 3 adenomas 1 of which was ≥6 mm in size predicted advanced neoplasia at follow-up colonoscopy (Table 2).
      The absolute risk of metachronous advanced neoplasia was 10.4% (11 of 106) among patients with ≥5 adenomas at least 1 of which was a small adenoma (Table 3). Patients who only had 1 to 2 diminutive adenomas had an absolute risk of 3.3% (54 of 1625) for advanced neoplasia at follow-up.
      Table 3Advanced lesions at follow-up according to the baseline colonoscopy findings
      1-2 both ≤5 mm1-2 at least one 6-9 mm3-4 all ≤5 mm3-4 at least one 6-9 mm5 or more all ≤5 mm5 or more at least one 6-9 mmP value
      Number1625272271102101106
      Male, n (%)854 (53)156 (57)159 (59)64 (63)70 (69)79 (75)<.001
      Age, years (SD)57.5 (9.7)58.2 (9.5)61.2 (8.8)60.9 (9.7)61.6 (8.8)62.9 (9.3)<.001
      Time to follow-up, years (SD)4.7 (2.4)4.1 (2.3)4.3 (2.2)3.9 (2.2)3.5 (1.9)2.9 (1.7)<.001
       6 months to 1 year, n (%)43 (2.6)9 (3.3)4 (1.5)3 (2.9)2 (2)9 (8.5)
       1-3 years321 (19.8)68 (25)56 (20.7)28 (27.5)36 (35.6)45 (42.5)
       3-5 years506 (31.1)110 (40.4)121 (44.6)54 (52.9)48 (47.5)45 (42.5)
       5+ years755 (46.5)85 (31.3)90 (33.2)17 (16.7)15 (14.9)7 (6)
      Excellent/good bowel preparation, n (%)982 (90)161 (83)182 (90.5)65 (83.3)78 (90.7)84 (93.3).019
      Indication at baseline colonoscopy, n (%).003
       Screening754 (46.4)117 (43)130 (48)48 (47.1)47 (46.5)48 (45.3)
       Surveillance480 (29.5)79 (29)95 (35.1)29 (28.4)39 (38.6)45 (42.5)
       Diagnostic391 (24.1)76 (27.9)46 (17)25 (24.5)15 (14.9)13 (12.3)
      Patients with advanced neoplasms, n (%)54 (3.3)15 (5.5)12 (4.4)7 (6.9)5 (5)11 (10.4).006
      Fisher exact test.
       Cancer2 (0.1)01 (0.4)01 (1)0
       HGD4 (0.2)1 (0.4)1 (0.4)001 (0.9)
       VA ≥ 10 mm8 (0.5)2 (0.7)0001 (0.9)
       VA < 10 mm7 (0.4)1 (0.4)02 (2)01 (0.9)
       TA ≥ 10 mm33 (2)11 (4)13 (4.8)5 (4.9)4 (4)8 (7.5)
      SD, Standard deviation; HGD, high-grade dysplasia; VA, villous or tubulovillous adenoma; TA, tubular adenoma.
      Fisher exact test.

      Sensitivity analysis

      When SSPs ≥10 mm were also considered as advanced neoplasia, the analysis showed similar results (Supplementary Table 1, Supplementary Table 2, Supplementary Table 3, Supplementary Table 4, available online at www.giejournal.org). Similar results were observed when we removed 29 patients who had ≥10 adenomas at the baseline colonoscopy (Supplementary Table 5, Supplementary Table 6, Supplementary Table 7, Supplementary Table 8, available online at www.giejournal.org).
      Tables 4 and 5 show findings at follow-up colonoscopy according to baseline screening colonoscopies only. When the analysis was confined to baseline screening examinations only, multivariable analyses showed that all subgroups with adenomas 6 to 9 mm had a higher incidence of advanced neoplasia at follow-up compared with 1 to 2 adenomas <6 mm in size, regardless of the total number of adenomas (Table 5).
      Table 4Advanced lesions among 6 baseline groups limited to screening indication only
      Baseline adenoma findingsP value
      1-2 both ≤5 mm1-2 at least one 6-9 mm3-4 all ≤5 mm3-4 at least one 6-9 mm5 or more all ≤5 mm5 or more at least one 6-9 mm
      Number754117130484748
      Male, n (%)416 (55.2)77 (65.8)79 (60.8)32 (66.7)34 (72.3)39 (81.3).001
      Age, years (SD)57.2 (8.2)57.1 (8.1)61.4 (7.9)59.7 (7.9)60.7 (7.9)61.7 (7.4)<.001
      Time to follow-up, years (SD)5.1 (2.2)4.5 (2.0)4.8 (2.3)4.2 (2.4)3.6 (1.7)3 (1.6)<.001
       6 months to 1 year, n (%)13 (1.7)5 (4.3)1 (0.8)01 (2.1)1 (2.1)
       1-3 years91 (12.1)15 (12.8)16 (12.3)14 (29.2)14 (29.2)14 (29.8)
       3-5 years228 (30.2)50 (42.7)14 (29.2)24 (50)24 (50)26 (55.3)
       5+ years422 (56)47 (40.2)24 (50)10 (20.8)10 (20.8)6 (12.8)
      Excellent/good bowel preparation, n (%)525 (91)85 (85.9)96 (91.4)35 (85.4)36 (85.7)38 (92.7).377
      Fisher exact test.
      Patients with advanced neoplasms, n (%)12 (1.6)8 (6.8)5 (3.8)4 (8.3)3 (6.4)4 (8.3)<.001
      Fisher exact test.
       Cancer00001 (2.1)0
       HGD2 (0.3)10000
       VA ≥10 mm000000
       VA <10 mm2 (0.3)1 (0.9)0000
       TA ≥10 mm8 (1.1)6 (5.1)5 (3.8)4 (8.3)2 (4.3)4 (8.3)
      SD, Standard deviation; HGD, high-grade dysplasia; VA, villous or tubulovillous adenoma; TA, tubular adenoma.
      Fisher exact test.
      Table 5Risk factors for advanced neoplasia (screening patients only) in the multivariable analysis
      Logistic regression using the enter method.
      FactorOdds ratio (95% confidence interval)P value
      Age (yearly increment)1.09 (1.04-1.13)<.001
      Gender
       Female1
       Male0.89 (0.42-1.92).774
      Time to follow-up (per year increment)1.06 (0.88-1.26).553
      Preparation quality
       Poor/fair1
       Excellent/good0.62 (0.31-1.27).191
      Baseline adenoma findings
       1-2 adenomas both ≤5 mm1
       1-2 adenomas one 6-9 mm4.07 (1.50-11.04).006
       3-4 adenomas all ≤5 mm1.12 (0.30-4.19).861
       3-4 adenomas one 6-9 mm4.91 (1.44-16.75).011
       ≥ 5 adenomas all ≤5 mm3.24 (0.83-12.62).091
       ≥ 5 adenomas one 6-9 mm4.71 (1.30-17.05).018
      Logistic regression using the enter method.
      Tables 6 and 7 show an analysis limited to patients with 1 to 2 baseline adenomas and who had a follow-up examination between 4.5 and 5.5 years. Patients with a small adenoma had a significantly higher risk of advanced neoplasia at follow-up compared with patients with diminutive adenomas only (OR, 5.23; 95% CI, 1.55-17.68).
      Table 6Advanced lesions at follow-up according to baseline colonoscopy findings limited to patients with 1-2 adenomas at baseline whose follow-up colonoscopy was at 5 ± 0.5 years
      1-2 both ≤5 mm1-2 at least one 6-9 mmP value
      Number46153
      Male, n (%)854 (53)156 (57)<.001
      Age, years (SD)58.3 (9.1)58.7 (9.1).745
      Time to follow-up, years (SD)5.1 (0.2)5.0 (0.2).104
       3-5 years, n (%)128 (27.8)20 (37.7)
       5+ years, n (%)333 (72.2)33 (62.3)
      Excellent/good bowel preparation, n (%)361 (96)42 (93.3).425
      Fisher exact test.
      Indication at baseline colonoscopy, n (%).457
       Screening264 (57.3)35 (66)
       Surveillance116 (25.2)10 (18.9)
       Diagnostic81 (17.6)8 (15.1)
      Patients with advanced neoplasms, n (%)14 (3)6 (11.3).011
      Fisher exact test.
       Cancer1 (0.2)0
       HGD2 (0.4)1 (1.9)
       VA ≥10 mm1 (0.2)1 (1.9)
       VA <10 mm3 (0.7)0
       TA ≥10 mm7 (1.5)4 (7.5)
      SD, Standard deviation; HGD, high-grade dysplasia; VA, villous or tubulovillous adenoma; TA, tubular adenoma.
      Fisher exact test.
      Table 7Risk factors for advanced neoplasia at follow-up (limited to patients with 1-2 adenomas at baseline whose follow-up colonoscopy was at 5 ± 0.5 years) in the multivariable analysis
      Logistic regression using the enter method.
      FactorOdds ratio (95% confidence interval)P value
      Age (yearly increment)1.06 (0.99-1.13).063
      Gender
       Female1
       Male0.83 (0.26-2.73).764
      Time to follow-up (per year increment)0.25 (0.02-4.07)0.329
      Preparation quality
       Poor/fair1
       Excellent/good0.57 (0.06-5.87).633
      Indication
       Screening1
       Polyp surveillance1.8 (0.53-6.03).344
       Diagnostic
      Odds ratio could not be calculated (too few events).
      .997
      Baseline adenoma findings
       1-2 both ≤5 mm1
       1-2 at least one 6-9 mm5.23 (1.55-17.68).008
      Logistic regression using the enter method.
      Odds ratio could not be calculated (too few events).

      Discussion

      In this study, we describe experience from a single U.S. center of the impact of small versus diminutive adenomas at colonoscopy on the risk of advanced neoplasia at follow-up. Among patients with ≥5 adenomas, the risk for advanced neoplasia at follow-up was greater for patients who had at least 1 small adenoma compared with patients with all diminutive adenomas Thus, we found that adenomas in the 6 to 9 mm size range increase the risk of subsequent advanced neoplasia compared with diminutive adenomas. Our results suggest that caution is appropriate in lumping all adenomas of 1 to 9 mm together in postpolypectomy surveillance guidelines.
      • Lieberman D.A.
      • Rex D.K.
      • Winawer S.J.
      • et al.
      Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer.
      In addition to 6 to 9 mm adenomas predicting subsequent advanced neoplasia compared with having only diminutive adenomas in our entire study population, we also found that the discriminating effect of 6 to 9 mm polyps on the subsequent risk of advanced neoplasia was present when only baseline colonoscopies performed for screening were considered. Thus, when only baseline screening colonoscopies were considered, each of the 3 subgroups of adenomas organized by number of lesions (1-2 adenomas, 3-4 adenomas, and ≥5 adenomas) and containing at least 1 adenoma 6 to 9 mm in size had a significantly higher risk of advanced neoplasia at follow-up compared with the subgroup with the same number of adenomas composed of only diminutive adenomas. The predictive value of 6 to 9 mm adenomas in screening patients was more striking than the same effect for the entire study population. The explanation for this finding is uncertain, but one possibility is that patients undergoing baseline surveillance examinations had previous examinations at other centers that removed high-risk adenoma findings, but of which we were unaware and could not identify from our database. Such patients would remain at increased risk of advanced neoplasia despite an intervening surveillance examination at our center showing only low-risk adenomas.
      • Lieberman D.A.
      • Rex D.K.
      • Winawer S.J.
      • et al.
      Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer.
      Most previous studies of risk stratification for subsequent advanced lesions based on baseline findings have not stratified lesions 1 to 9 mm in size.
      • Winawer S.
      • Zauber A.
      • Ho M.
      • et al.
      Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps.
      • Martinez M.E.
      • Baron J.A.
      • Lieberman D.A.
      • et al.
      A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy.
      • Anderson J.C.
      • Baron J.A.
      • Ahnen D.J.
      • et al.
      Factors associated with shorter colonoscopy surveillance intervals for patients with low-risk colorectal adenomas and effects on outcome.
      • Hassan C.
      • Gimeno-Garcia A.
      • Kalager M.
      • et al.
      Systematic review with meta-analysis: the incidence of advanced neoplasia after polypectomy in patients with and without low-risk adenomas.
      • Dube C.
      • Yakubu M.
      • McCurdy B.R.
      • et al.
      Risk of advanced adenoma, colorectal cancer, and colorectal cancer mortality in people with low-risk adenomas at baseline colonoscopy: a systematic review and meta-analysis.
      • Gupta S.
      • Jacobs E.T.
      • Baron J.A.
      • et al.
      Risk stratification of individuals with low-risk colorectal adenomas using clinical characteristics: a pooled analysis.
      • Click B.
      • Pinsky P.F.
      • Hickey T.
      • et al.
      Association of colonoscopy adenoma findings with long-term colorectal cancer incidence.
      However, 2 small studies that did stratify risk by small versus diminutive size of adenomas at baseline suggested an increased risk of subsequent advanced lesions in those with small baseline adenomas.
      • Moon C.M.
      • Jung S.A.
      • Eun C.S.
      • et al.
      The effect of small or diminutive adenomas at baseline colonoscopy on the risk of developing metachronous advanced colorectal neoplasia: KASID multicenter study.
      ,
      • Sneh Arbib O.
      • Zemser V.
      • Leibovici Weissman Y.
      • et al.
      Risk of advanced lesions at the first follow-up colonoscopy after polypectomy of diminutive versus small adenomatous polyps of low-grade dysplasia.
      Thus, the observations we made here have been made previously.
      During the study interval, endoscopists in our group consistently had ADRs above the recommended thresholds.
      • Rex D.K.
      • Ponugoti P.L.
      Calculating the adenoma detection rate in screening colonoscopies only: Is it necessary? Can it be gamed?.
      Because ADRs have been increasing in recent years,
      • Pike I.M.
      • Vicari J.
      Incorporating quality measurement and improvement into a gastroenterology practice.
      we suspect that our results have good generalizability. Our results may not apply in settings where ADRs are low because the absolute risk of advanced neoplasia could be substantially higher even in individuals with very low-risk findings (because more high-risk lesions are missed when ADRs are low). Many of the studies that underlie current postpolypectomy surveillance recommendations
      • Pike I.M.
      • Vicari J.
      Incorporating quality measurement and improvement into a gastroenterology practice.
      were performed before the current emphasis on ADRs and before high-definition colonoscopes were available. Thus, the prevalence of patients with only tiny adenomas may be substantially different in the current study from earlier studies. Indeed, the difference in risk of subsequent advanced neoplasia observed in the current study between the baseline small versus diminutive adenoma groups may largely reflect the current study identifying a large and distinct cohort of very low-risk tiny adenomas that were less-frequently observed in earlier studies. This suggestion warrants additional evaluation.
      Limitations of our study include that it is a retrospective analysis of a prospectively developed and maintained database. The number of patients in certain of the risk groups was small. Nevertheless, the results supporting the predictive value of adenomas in the 6 to 9 mm size range compared with the 1 to 5 mm size range reached statistical significance. ADRs in our unit are likely to be relatively high, which suggests that our findings will be increasingly relevant as detection improves in community-based colonoscopy. Another potential limitation might be that we did not choose to systematically exclude patients with serrated lesions at baseline. Further, we did not present data on the impact of concomitant SSPs at baseline, primarily because our pathology department has not consistently interpreted SSPs versus hyperplastic polyps over the study interval, as we have twice demonstrated.
      • Abdeljawad K.
      • Vemulapalli K.C.
      • Kahi C.J.
      • et al.
      Sessile serrated polyp prevalence determined by a colonoscopist with a high lesion detection rate and an experienced pathologist.
      ,
      • Khalid O.
      • Radaideh S.
      • Cummings O.W.
      • et al.
      Reinterpretation of histology of proximal colon polyps called hyperplastic in 2001.
      Finally, polyp size was estimated endoscopically, which may be subject to operator error
      • Eichenseer P.J.
      • Dhanekula R.
      • Jakate S.
      • et al.
      Endoscopic mis-sizing of polyps changes colorectal cancer surveillance recommendations.
      ,
      • Schoen R.E.
      • Gerber L.D.
      • Margulies C.
      The pathologic measurement of polyp size is preferable to the endoscopic estimate.
      and terminal digit rounding,
      • Plumb A.A.
      • Nickerson C.
      • Wooldrage K.
      • et al.
      Terminal digit preference biases polyp size measurements at endoscopy, computed tomographic colonography, and histopathology.
      but these effects are common to postpolypectomy surveillance studies generally.
      In conclusion, these data indicate that lumping small and diminutive adenomas together in postpolypectomy surveillance guidelines may create a risk for some patients with 6 to 9 mm adenomas and/or increase procedure-related costs and risks for patients with 1 to 5 mm adenomas. We recommend that additional groups evaluate the impact of small versus diminutive adenomas on the subsequent risk of advanced neoplasia in postpolypectomy surveillance cohorts.

      Acknowledgments

      This work was supported by a gift from Scott Schurz of Bloomington, Indiana, and his children to the Indiana University Foundation in the name of Douglas K. Rex, MD.

      Appendix

      Supplementary Table 1Advanced neoplasia according to baseline findings and including sessile serrated polyps (SSPs) with cytological dysplasia and SSPs ≥10 mm as advanced lesions
      Patients with diminutive adenomas (1-5 mm) onlyPatients with at least one small adenoma (6-9 mm)P value
      Number1997480
      Age, years (SD)58.3 (9.7)59.8 (9.5).002
      Male gender (%)1083 (54.2)299 (62.3).001
      Time to follow-up examination, years (SD)4.6 (2.4)3.8 (2.2)<.001
       6 months to 1 year, n (%)49 (2.5)21 (4.4)
       1-3 years413 (20.7)141 (29.4)
       3-5 years675 (33.8)209 (43.5)
       5+ years860 (43.1)109 (22.7)
      Excellent or good bowel preparation, n (%)
      Bowel preparation quality information available for 1740 of 2477 patients (70.2%).
      1242 (90.1)310 (85.6).014
      Indication, n (%).673
       Screening931 (46.6)213 (44.4)
       Surveillance614 (30.7)153 (31.9)
       Diagnostic452 (22.6)114 (23.8)
      Advanced neoplasia at follow-up, n (%)92 (4.6)37 (7.7).006
       Cancer4 (0.2)0
       HGD or SSPCD5 (0.3)2 (0.4)
       VA ≥10 mm8 (0.4)3 (0.6)
       VA <10 mm7 (0.4)4 (0.8)
       TA or SSP ≥10 mm68 (3.4)28 (5.8)
      SD, Standard deviation; HGD, high-grade dysplasia; SSPCD, sessile serrated polyp with cytological dysplasia; VA, villous or tubulovillous adenoma; TA, tubular adenoma.
      Bowel preparation quality information available for 1740 of 2477 patients (70.2%).
      Supplementary Table 2Risk factors for advanced neoplasia according to the baseline findings and including sessile serrated polyps (SSPs) with cytological dysplasia and SSPs ≥10 mm as advanced lesions in the multivariable analysis
      Logistic regression using the enter method.
      FactorOdds ratio (95% confidence interval)P value
      Age (yearly increment)1.04 (1.01-1.06).004
      Gender (male/female).281
       Female1
       Male0.79 (0.51-1.21)
      Time to follow-up (per year increment)1.02 (0.92-1.13).756
      Preparation quality.344
       Poor/fair1
       Excellent/good0.73 (0.39-1.40)
      Indication
       Screening1
       Polyp surveillance1.47 (0.91-2.38).113
       Diagnostic0.80 (0.41-1.55).506
      Baseline adenoma findings
       All adenomas ≤5 mm1
       Any adenoma 6-9 mm1.96 (1.24-3.117).004
      Logistic regression using the enter method.
      Supplementary Table 3Advanced neoplasia according to the baseline findings and including sessile serrated polyps (SSPs) with cytological dysplasia and SSPs ≥10 mm as advanced lesions
      Baseline adenoma findingsP value
      1-2 both less than 6 mm1-2 at least one 6-9 mm3-4 all less than 6 mm3-4 at least one 6-9 mm5 or more all less than 6 mm5 or more at least one 6-9 mm
      Number1625272271102101106
      Male, n (%)854 (53)156 (57)159 (59)64 (63)70 (69)79 (75)<.001
      Age, years (SD)57.5 (9.7)58.2 (9.5)61.2 (8.8)60.9 (8.7)61.6 (8.8)62.9 (9.3)<.001
      Time to follow-up, years (SD)4.7 (2.4)4.1 (2.3)4.3 (2.2)3.9 (2.2)3.5 (1.9)2.9 (1.7)<.001
       6 months to 1 year, n (%)43 (2.6)9 (3.3)4 (1.5)3 (2.9)2 (2)9 (8.5)
       1-3 years321 (19.8)68 (25)56 (20.7)28 (27.5)36 (35.6)45 (42.5)
       3-5 years506 (31.1)110 (40.4)121 (44.6)54 (52.9)48 (47.5)45 (42.5)
       5+ years755 (46.5)85 (31.3)90 (33.2)17 (16.7)15 (14.9)7 (6)
      Excellent/good bowel preparation, n (%)982 (90)161 (83)182 (90.5)65 (83.3)78 (90.7)84 (93.3).019
      Indication at baseline colonoscopy, n (%).003
       Screening754 (46.4)117 (43)130 (48)48 (47.1)47 (46.5)48 (45.3)
       Surveillance480 (29.5)79 (29)95 (35.1)29 (28.4)39 (38.6)45 (42.5)
       Diagnostic391 (24.1)76 (27.9)46 (17)25 (24.5)15 (14.9)13 (12.3)
      Patients with advanced neoplasms, n (%)71 (4.4)17 (6.3)15 (5.5)7 (6.9)6 (5.9)13 (12.3).014
       Cancer2 (0.1)01 (0.4)01 (1)0
       HGD or SSPCD4 (0.2)1 (0.4)1 (0.4)001 (0.9)
       VA ≥10 mm8 (0.5)2 (0.7)0001 (0.9)
       VA <10 mm7 (0.4)1 (0.4)02 (2)01 (0.9)
       TA or SSP ≥10 mm50 (3.1)13 (4.8)13 (4.8)5 (4.9)5 (5)10 (9.4)
      SD, Standard deviation; HGD, high-grade dysplasia; SSPCD, sessile serrated polyp with cytological dysplasia; VA, villous or tubulovillous adenoma; TA, tubular adenoma.
      Supplementary Table 4Risk factors for advanced neoplasia according to the baseline findings and including sessile serrated adenomas/polyps (SSPs) with cytological dysplasia and SSPs ≥10 mm as advanced lesions in the multivariable analysis
      Logistic regression using the enter method.
      FactorOdds ratio (95% confidence interval)P value
      Age (yearly increment)1.04 (1.01-1.06).005
      Gender.254
       Female1
       Male0.78 (0.50-1.20)
      Time to follow-up (per year increment)1.03 (0.92-1.14).633
      Preparation quality
       Poor/fair1
       Excellent/good0.70 (0.37-1.34).282
      Indication
       Screening1
       Polyp surveillance1.46 (0.91-2.36).121
       Diagnostic0.82 (0.42-1.59).549
      Baseline adenoma findings
       1-2 adenomas both ≤5 mm1
       1-2 adenomas with at least one 6-9 mm1.44 (0.74-2.78).284
       3-4 adenomas all ≤5 mm1.01 (0.50-2.06).973
       3-4 adenomas with at least one 6-9 mm1.99 (0.86-4.62).11
       ≥5 adenomas ≤5 mm0.72 (0.22-2.41).599
       ≥5 adenomas with at least one 6-9 mm2.97 (1.45-6.08).003
      Logistic regression using the enter method.
      Supplementary Table 5Advanced neoplasia according to the baseline findings after removing 29 patients with >10 adenomas at baseline
      Patients with diminutive adenomas (1-5 mm) onlyPatients with at least one small adenoma (6-9 mm)P value
      Number1992456
      Age, years (SD)58.3 (9.7)59.6 (9.3).009
      Male gender (%)1080 (54.2)280 (61.4).005
      Time to follow-up examination, years (SD)4.6 (2.4)3.8 (2.2)<.001
       6 months to 1 year, n (%)48 (2.4)15 (3.3)
       1-3 years409 (20.5)129 (28.3)
       3-5 years675 (33.9)204 (44.7)
       5+ years860 (43.2)108 (23.7)
      Excellent or good bowel preparation, n (%)1239 (90.2)291 (85.1).006
      Indication, n (%).76
       Screening928 (46.6)205 (45.0)
       Surveillance612 (30.7)141 (30.9)
       Diagnostic452 (22.7)110 (24.1)
      Advanced neoplasia at follow-up (%)71 (3.6)31 (6.8).002
       Cancer4 (0.2)
       HGD5 (0.3)2 (0.4)
       VA ≥10 mm8 (0.4)2 (0.4)
       VA <10 mm7 (0.4)4 (0.9)
       TA ≥10 mm47 (2.4)23 (5)
      SD, Standard deviation; HGD, high-grade dysplasia; VA, villous or tubulovillous adenoma; TA, tubular adenoma.
      Supplementary Table 6Risk factors for advanced neoplasia according to the baseline findings after removing 29 patients with more than 10 adenomas at baseline in the multivariable analysis
      Logistic regression using the enter method.
      FactorOdds ratio (95% confidence interval)P value
      Age (yearly increment)1.05 (1.03-1.08)<.001
      Gender
       Female1
       Male0.93 (0.57-1.53).783
      Time to follow-up (per year increment)1.06 (0.94-1.18).354
      Preparation quality
       Poor/fair1
       Excellent/good0.64 (0.31-1.30).214
      Indication
       Screening1
       Polyp surveillance1.38 (0.80-2.37).247
       Diagnostic0.80 (0.37-1.72).566
      Baseline findings
       All adenomas ≤5 mm1
       Any adenoma 6-9 mm2.34 (1.40-3.91).001
      Logistic regression using the enter method.
      Supplementary Table 7Advanced neoplasia according to baseline findings after removing 29 patients with more than 10 adenomas at baseline
      Baseline adenoma findingsP value
      1-2 both less than 6 mm1-2 at least one 6-9 mm3-4 all less than 6 mm3-4 at least one 6-9 mm5 or more all less than 6 mm5 or more at least one 6-9 mm
      Number16252722711029682
      Male, n (%)854 (53)156 (57)159 (59)64 (63)67 (70)60 (73)<.001
      Age, years (SD)57.5 (9.7)58.2 (9.5)61.2 (8.8)60.9 (8.7)61.6 (8.8)62.9 (9.3)<.001
      Time to follow-up, years (SD)4.7 (2.4)4.1 (2.3)4.3 (2.2)3.9 (2.2)3.6 (1.9)3.1 (1.8)<.001
       6 months to 1 year, n (%)43 (2.6)9 (3.3)4 (1.5)3 (2.9)1 (1)3 (3.7)
       1-3 years321 (19.8)68 (25)56 (20.7)28 (27.5)32 (33.3)33 (40.2)
       3-5 years506 (31.1)110 (40.4)121 (44.6)54 (52.9)48 (50)40 (48.8)
       5+ years755 (46.5)85 (31.3)90 (33.2)17 (16.7)15 (15.6)6 (7.3)
      Excellent/good bowel preparation, n (%)982 (90)161 (83)182 (90.5)65 (83.3)75 (92.6)65 (92.9).018
      Indication at baseline colonoscopy, n (%).009
       Screening754 (46.4)117 (43)130 (48)48 (47.1)44 (45.8)40 (48.8)
       Surveillance480 (29.5)79 (29)95 (35.1)29 (28.4)37 (38.5)33 (40.2)
       Diagnostic391 (24.1)76 (27.9)46 (17)25 (24.5)15 (15.6)9 (11)
      Patients with advanced neoplasms, n (%)54 (3.3)15 (5.5)12 (4.4)7 (6.9)5 (5.2)9 (11).01
      Fisher exact test.
       Cancer2 (0.1)01 (0.4)01 (1)0
       HGD4 (0.2)1 (0.4)1 (0.4)001 (0.9)
       VA ≥10 mm8 (0.5)2 (0.7)0000
       VA <10 mm7 (0.4)1 (0.4)02 (2)01 (1.2)
       TA ≥10 mm33 (2)11 (4)10 (3.7)5 (4.9)4 (4.2)7 (8.5)
      SD, Standard deviation; HGD, high-grade dysplasia; VA, villous or tubulovillous adenoma; TA, tubular adenoma.
      Fisher exact test.
      Supplementary Table 8Risk factors for advanced neoplasia according to the baseline findings after removing 29 patients with >10 adenomas at baseline in the multivariable analysis
      Logistic regression using the enter method.
      FactorOdds ratio (95% confidence interval)P value
      Age (yearly increment)1.05 (1.02-1.08)<.001
      Gender
       Female1
       Male0.91 (0.55-1.50).705
      Time to follow-up (per year increment)1.07 (0.95-1.19).269
      Preparation quality
       Poor/fair1
       Excellent/good0.61 (0.30-1.25).174
      Indication
       Screening1
       Polyp surveillance1.37 (0.80-2.37).255
       Diagnostic0.82 (0.38-1.77).618
      Baseline adenoma findings
       1-2 adenomas both ≤5 mm1
       1-2 adenomas one 6-9 mm1.62 (0.78-3.38).196
       3-4 adenomas all ≤5 mm0.93 (0.40-2.15).864
       3-4 adenomas one 6-9 mm2.68 (1.13-6.37).026
       ≥ 5 adenomas all ≤5 mm1.05 (0.31-3.57).935
       ≥ 5 adenomas one 6-9 mm3.86 (1.70-8.77).001
      Logistic regression using the enter method.

      References

        • Winawer S.
        • Zauber A.
        • Ho M.
        • et al.
        Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps.
        N Engl J Med. 1993; 328: 901-906
        • Martinez M.E.
        • Baron J.A.
        • Lieberman D.A.
        • et al.
        A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy.
        Gastroenterology. 2009; 136: 832-841
        • Anderson J.C.
        • Baron J.A.
        • Ahnen D.J.
        • et al.
        Factors associated with shorter colonoscopy surveillance intervals for patients with low-risk colorectal adenomas and effects on outcome.
        Gastroenterology. 2017; 152: 1933-1943.e5
        • Hassan C.
        • Gimeno-Garcia A.
        • Kalager M.
        • et al.
        Systematic review with meta-analysis: the incidence of advanced neoplasia after polypectomy in patients with and without low-risk adenomas.
        Aliment Pharmacol Ther. 2014; 39: 905-912
        • Dube C.
        • Yakubu M.
        • McCurdy B.R.
        • et al.
        Risk of advanced adenoma, colorectal cancer, and colorectal cancer mortality in people with low-risk adenomas at baseline colonoscopy: a systematic review and meta-analysis.
        Am J Gastroenterol. 2017; 112: 1790-1801
        • Gupta S.
        • Jacobs E.T.
        • Baron J.A.
        • et al.
        Risk stratification of individuals with low-risk colorectal adenomas using clinical characteristics: a pooled analysis.
        Gut. 2017; 66: 446-453
        • Click B.
        • Pinsky P.F.
        • Hickey T.
        • et al.
        Association of colonoscopy adenoma findings with long-term colorectal cancer incidence.
        JAMA. 2018; 319: 2021-2031
        • Hassan C.
        • Quintero E.
        • Dumonceau J.M.
        • et al.
        Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) guideline.
        Endoscopy. 2013; 45: 842-851
        • Lieberman D.A.
        • Rex D.K.
        • Winawer S.J.
        • et al.
        Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer.
        Gastroenterology. 2012; 143: 844-857
        • Pike I.M.
        • Vicari J.
        Incorporating quality measurement and improvement into a gastroenterology practice.
        Am J Gastroenterol. 2010; 105: 252-254
        • Kaminski M.F.
        • Regula J.
        • Kraszewska E.
        • et al.
        Quality indicators for colonoscopy and the risk of interval cancer.
        N Engl J Med. 2010; 362: 1795-1803
        • Corley D.
        • Jensen C.D.
        • Marks A.R.
        • et al.
        Adenoma detection rate and risk of colorectal cancer and death.
        N Engl J Med. 2014; 370: 1298-1306
        • Rex D.K.
        • Boland C.R.
        • Dominitz J.A.
        • et al.
        Colorectal cancer screening: recommendations for physicians and patients from the U.S. Multi-Society Task Force on Colorectal Cancer.
        Gastrointest Endosc. 2017; 86: 18-33
        • Rex D.K.
        • Schoenfeld P.S.
        • Cohen J.
        • et al.
        Quality indicators for colonoscopy.
        Gastrointest Endosc. 2015; 81: 31-53
        • Rex D.K.
        • Repici A.
        • Gross S.A.
        • et al.
        High-definition colonoscopy versus Endocuff versus EndoRings versus full-spectrum endoscopy for adenoma detection at colonoscopy: a multicenter randomized trial.
        Gastrointest Endosc. 2018; 88: 335-344 e2
        • Moon C.M.
        • Jung S.A.
        • Eun C.S.
        • et al.
        The effect of small or diminutive adenomas at baseline colonoscopy on the risk of developing metachronous advanced colorectal neoplasia: KASID multicenter study.
        Dig Liver Dis. 2018; 50: 847-852
        • Sneh Arbib O.
        • Zemser V.
        • Leibovici Weissman Y.
        • et al.
        Risk of advanced lesions at the first follow-up colonoscopy after polypectomy of diminutive versus small adenomatous polyps of low-grade dysplasia.
        Gastrointest Endosc. 2017; 86: 713-721.e2
        • Vemulapalli K.C.
        • Rex D.K.
        Risk of advanced lesions at first follow-up colonoscopy in high-risk groups as defined by the United Kingdom post-polypectomy surveillance guideline: data from a single U.S. center.
        Gastrointest Endosc. 2014; 80: 299-306
        • Rex D.K.
        • Ponugoti P.L.
        Calculating the adenoma detection rate in screening colonoscopies only: Is it necessary? Can it be gamed?.
        Endoscopy. 2017; 49: 1069-1074
        • Abdeljawad K.
        • Vemulapalli K.C.
        • Kahi C.J.
        • et al.
        Sessile serrated polyp prevalence determined by a colonoscopist with a high lesion detection rate and an experienced pathologist.
        Gastrointest Endosc. 2015; 81: 517-524
        • Khalid O.
        • Radaideh S.
        • Cummings O.W.
        • et al.
        Reinterpretation of histology of proximal colon polyps called hyperplastic in 2001.
        World J Gastroenterol. 2009; 15: 3767-3770
        • Eichenseer P.J.
        • Dhanekula R.
        • Jakate S.
        • et al.
        Endoscopic mis-sizing of polyps changes colorectal cancer surveillance recommendations.
        Dis Colon Rectum. 2013; 56: 315-321
        • Schoen R.E.
        • Gerber L.D.
        • Margulies C.
        The pathologic measurement of polyp size is preferable to the endoscopic estimate.
        Gastrointest Endosc. 1997; 46: 492-496
        • Plumb A.A.
        • Nickerson C.
        • Wooldrage K.
        • et al.
        Terminal digit preference biases polyp size measurements at endoscopy, computed tomographic colonography, and histopathology.
        Endoscopy. 2016; 48: 899-908

      Linked Article