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No Polyp Left Behind: Defining Bowel Preparation Adequacy to Avoid Missed Polyps

  • Philip Schoenfeld
    Correspondence
    Reprint requests Address requests for reprints to: Philip Schoenfeld, MD, MSEd, MSc (Epi), Professor of Medicine, University of Michigan School of Medicine Room 111-D, 2215 Fuller Road Ann Arbor, Michigan.
    Affiliations
    Ann Arbor Veterans Health Care System, University of Michigan School of Medicine, Ann Arbor, Michigan
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  • Jason A. Dominitz
    Affiliations
    VA Puget Sound Health Care System, University of Washington School of Medicine, Seattle, Washington
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Published:December 20, 2015DOI:https://doi.org/10.1053/j.gastro.2015.12.024
      See “Quantification of adequate bowel preparation for screening or surveillance colonoscopy in men,” by Clark BT, Protiva P, Nagar A, et al, on page 396.
      A major goal of colorectal cancer (CRC) screening with colonoscopy is to minimize CRC incidence, and this is accomplished by identifying and completely resecting 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.
      • Levin B.
      • Lieberman D.A.
      • McFarland B.
      • et al.
      Screening and surveillance for 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.
      In recent years, considerable attention has been focused on the adenoma detection rate (ADR) as a measure of the quality of colonoscopy.
      • Rex D.K.
      • Schoenfeld P.
      • Cohen J.
      • et al.
      Quality indicators for colonoscopy.
      Higher ADRs are associated with lower rates of interval CRC,
      • Corley D.A.
      • Jensen C.D.
      • Marks A.R.
      • et al.
      Adenoma detection rate and risk of colorectal cancer and death.
      which are defined as CRC diagnosed after a prior colonoscopy but before the next scheduled screening or surveillance colonoscopy. This is partly because endoscopists with a high ADR seem less likely to “miss” adenomas during colonoscopy. Endoscopists also intuitively understand that suboptimal bowel preparation obscures some colonic mucosa and increases the risk of “missing” an adenoma.
      • Johnson D.A.
      • Barkun A.N.
      • Cohen L.B.
      • et al.
      Optimizing adequacy of bowel cleansing for colonoscopy: recommendations from the US Multi-Society Task Force on Colorectal Cancer.
      • Menees S.B.
      • Kim H.M.
      • Elliott E.E.
      • et al.
      The impact of fair colonoscopy preparation on colonoscopy use and adenoma miss rates in patients undergoing outpatient colonoscopy.
      So, when bowel preparation is suboptimal, endoscopists are more likely to vary from guidelines and recommend shorter follow-up intervals for fear of missing important neoplasia.
      • Menees S.B.
      • Kim H.M.
      • Elliott E.E.
      • et al.
      The impact of fair colonoscopy preparation on colonoscopy use and adenoma miss rates in patients undergoing outpatient colonoscopy.
      • Johnson M.R.
      • Grubber J.
      • Grambow S.C.
      • et al.
      Physician non-adherence to colonoscopy interval guidelines in the Veterans Affairs Healthcare System.
      • Menees S.B.
      • Elliott E.E.
      • Govani S.
      • et al.
      The impact of bowel cleansing on follow-up recommendations in average-risk patients with a normal colonoscopy.
      Current guidelines state that the bowel preparation should be reported to be “adequate” if it allows visualization of polyps >5 mm.
      • Johnson D.A.
      • Barkun A.N.
      • Cohen L.B.
      • et al.
      Optimizing adequacy of bowel cleansing for colonoscopy: recommendations from the US Multi-Society Task Force on Colorectal Cancer.
      Up until now, this concept has been poorly defined, leading to substantial variability in endoscopists’ interpretation of what constitutes an “adequate” bowel preparation and its impact on recommendations for timing of future screening or surveillance colonoscopy.
      • Menees S.B.
      • Elliott E.E.
      • Govani S.
      • et al.
      The impact of bowel cleansing on follow-up recommendations in average-risk patients with a normal colonoscopy.
      • Menees S.B.
      • Elliott E.E.
      • Govani S.
      • et al.
      Adherence to recommended intervals for surveillance colonoscopy in average-risk patients with 1-2 small (< 1cm) polyps on screening colonoscopy.
      • Larsen M.
      • Hills N.
      • Terdiman J.
      The impact of the quality of colon preparation on follow-up colonoscopy recommendations.
      Therefore, endoscopists need a quantifiable, validated, and reproducible guide to determine when bowel cleansing is good enough. The findings of a new study address this.
      In this issue of Gastroenterology, Clark et al
      • Clark B.T.
      • Protiva P.
      • Nagar A.
      • et al.
      Quantification of adequate bowel preparation for screening or surveillance colonoscopy in men.
      report on their tandem colonoscopy study to assess the impact of bowel cleansing on missing adenomas >5 mm. Study patients were average-risk, 50- to 75-year-old veterans undergoing colonoscopy for CRC screening or colon polyp surveillance. During an initial colonoscopy, all polyps were removed and the quality of bowel preparation in the right colon, transverse colon, and left colon was graded using the validated Boston Bowel Preparation Scale (BBPS) on a scale of 0-3 (Table 1). Then, a blinded endoscopist repeated the colonoscopy on that day or within 60 days and removed any residual polyps to determine if any adenomas were missed. The investigators hypothesized that a BBPS colon segment score of 2 was noninferior to a score of 3 for identifying adenomas >5 mm and that a BBPS colon-segment score of 1 would be inferior to scores of 2 or 3 during the initial colonoscopy. Their findings support this hypothesis: the miss rate for adenomas >5 mm was 15.9% when the BBPS segment score was 1, which was significantly higher than the miss rate when the BBPS score was 2 (5.2% miss rate) or 3 (5.6% miss rate). The authors suggest that if any colon segment has a BBPS score of 1, then the bowel preparation is inadequate because the miss rate for adenomas >5 mm is approximately 16%. Therefore, these patients should be told to return for repeat colonoscopy within 12 months, as per current guidelines.
      • Johnson D.A.
      • Barkun A.N.
      • Cohen L.B.
      • et al.
      Optimizing adequacy of bowel cleansing for colonoscopy: recommendations from the US Multi-Society Task Force on Colorectal Cancer.
      Conversely, as long as the BBPS score is 2 or 3 in all colon segments, bowel preparation is adequate and guidelines should be followed when recommending timing of repeat colonoscopy.
      Table 1Boston Bowel Preparation Scale
      The right colon and transverse colon, and left colon are each scored on a 0-3 scale, so total Boston Bowel Preparation Scale may be 0-9. Right colon is defined as cecum and ascending colon, transverse colon is defined as hepatic flexure to splenic flexure, and left colon is defined as the descending colon to rectum. Each colon segment is scored after all maneuvers have been performed to cleanse residual stool or fluid.
      ScoreDescription
      0Unprepared colon segment with mucosa not seen due to solid stool or thick liquid stool that cannot be cleared
      1Portion of mucosa of the colon segment seen, but other areas of the colon segment not well seen due to staining, residual stool and/or opaque liquid
      2Minor amount of residual staining, small fragments of stool and/or opaque liquid but mucosa of colon segment seen well
      3Entire mucosa of the colon segment seen well with no residual staining, small fragments of stool or opaque liquid
      a The right colon and transverse colon, and left colon are each scored on a 0-3 scale, so total Boston Bowel Preparation Scale may be 0-9. Right colon is defined as cecum and ascending colon, transverse colon is defined as hepatic flexure to splenic flexure, and left colon is defined as the descending colon to rectum. Each colon segment is scored after all maneuvers have been performed to cleanse residual stool or fluid.
      One of the primary strengths of this study is the use of the BBPS to grade the quality of bowel preparation. The BBPS meets the criteria for a validated instrument.
      • Lai E.J.
      • Calderwood A.H.
      • Doros G.
      • et al.
      The Boston Bowel Preparation Scale: a valid and reliable instrument for colonoscopy-oriented research.
      • Calderwood A.H.
      • Jacobson B.C.
      Comprehensive validation of the Boston Bowel Preparation Scale.
      It has demonstrated intraobserver reproducibility (ie, an individual endoscopist’s BBPS score is likely to remain stable when he or she views the same colon segment >1 time) and interobserver reliability (ie, ≥2 endoscopists are likely to report the same BBPS score when viewing the same colon segment). In prospective studies, higher BBPS score (≥5 vs < 5) correlates with clinically important outcomes, such as higher ADR.
      • Calderwood A.H.
      • Jacobson B.C.
      Comprehensive validation of the Boston Bowel Preparation Scale.
      Also, unlike some other bowel preparation rating scales, the quality of the bowel preparation is assessed after all cleansing of the colon is complete, which is the critical for assessing actual mucosal visualization. Finally, widespread implementation of the BBPS is feasible through publicly available training videos (eg, www.cori.org/bbps).
      However, Clark et al
      • Clark B.T.
      • Protiva P.
      • Nagar A.
      • et al.
      Quantification of adequate bowel preparation for screening or surveillance colonoscopy in men.
      did not attempt to determine the impact of bowel cleansing on the miss rate of serrated polyps. This is understandable, because a much larger study would be needed to quantify the impact of colon-segment BBPS scores of 1-3 on serrated polyp miss rates. Nevertheless, this is still important to quantify in future studies because serrated polyps are often flat and found in the right side of the colon where it is more difficult to get excellent bowel cleansing. More important, these lesions are the precursor to the 20%-30% of CRC that follow the CpG island methylation pathway, which may progress from polyp to cancer much faster than the typical adenoma–carcinoma sequence.
      • Rex D.K.
      • Ahnen D.J.
      • Baron J.A.
      • et al.
      Serrated lesions of the colorectum: review and recommendations from an expert panel.
      We suspect that these serrated polyps are responsible for many interval CRCs, especially in the right side of the colon, and help to explain why the protective effect of colonoscopy is lower in the right colon compared with the left colon.
      • Nishihara R.
      • Wu K.
      • Lochhead P.
      • et al.
      Long-term colorectal cancer incidence and mortality after lower endoscopy.
      Currently, there is no clearly preferred bowel preparation scale. The US Multi-Society Task Force (USMSTF) on CRC does not specify a preferred bowel preparation scale. It simply states that an adequate bowel preparation should produce a recommendation for repeat colonoscopy that is consistent with guidelines for screening or surveillance intervals.
      • Johnson D.A.
      • Barkun A.N.
      • Cohen L.B.
      • et al.
      Optimizing adequacy of bowel cleansing for colonoscopy: recommendations from the US Multi-Society Task Force on Colorectal Cancer.
      The Aronchick scale,
      • Aronchick C.A.
      • Lipshutz W.H.
      • Wright S.H.
      • et al.
      A novel tableted purgative for colonoscopic preparation: efficacy and safety comparisons with colyte and fleet phosphor-soda.
      which classifies bowel cleansing as poor, fair, good, and excellent, is frequently used in the United States, but is not very helpful for meeting the USMSTF standard. In the Aronchick scale, the mid-scale qualitative descriptor “fair” is susceptible to interobserver variability, especially when compared with the extreme ends of the scale for “excellent” and “poor.”
      • Calderwood A.H.
      • Jacobson B.C.
      Comprehensive validation of the Boston Bowel Preparation Scale.
      • Ben-Horin S.
      • Bar-Meir S.
      • Avidan B.
      The impact of colon cleanliness assessment on endoscopists’ recommendations for follow-up colonoscopy.
      This has led to controversy about whether or not a “fair” bowel preparation is adequate to identify polyps >5 mm.
      • Clark B.T.
      • Rustagi T.
      • laine L.
      What level of bowel prep quality requires early repeat colonoscopy: systematic review and meta-analysis of the impact of prep quality on adenoma detection rate.
      • Liang P.S.
      • Dominitz J.A.
      Bowel preparation: is fair good enough?.
      What is not controversial is that “fair” bowel preparation is frequently associated with recommending a shorter interval for repeat colonoscopy
      • Menees S.B.
      • Kim H.M.
      • Elliott E.E.
      • et al.
      The impact of fair colonoscopy preparation on colonoscopy use and adenoma miss rates in patients undergoing outpatient colonoscopy.
      • Menees S.B.
      • Elliott E.E.
      • Govani S.
      • et al.
      The impact of bowel cleansing on follow-up recommendations in average-risk patients with a normal colonoscopy.
      • Menees S.B.
      • Elliott E.E.
      • Govani S.
      • et al.
      Adherence to recommended intervals for surveillance colonoscopy in average-risk patients with 1-2 small (< 1cm) polyps on screening colonoscopy.
      • Larsen M.
      • Hills N.
      • Terdiman J.
      The impact of the quality of colon preparation on follow-up colonoscopy recommendations.
      • Ben-Horin S.
      • Bar-Meir S.
      • Avidan B.
      The impact of colon cleanliness assessment on endoscopists’ recommendations for follow-up colonoscopy.
      (eg, recommending a repeat colonoscopy in 5 years instead of 10 years after a normal screening colonoscopy.) Therefore, the BBPS scale offers an alternative that may be more suitable to meet the USMSTF standard.
      Per the data from Clark et al,
      • Clark B.T.
      • Protiva P.
      • Nagar A.
      • et al.
      Quantification of adequate bowel preparation for screening or surveillance colonoscopy in men.
      a colon segment BBPS of 1 was associated with a 15.9% miss rate for adenomas >5 mm. Therefore, it is not surprising that the appropriate interval between colonoscopies would have changed from 10 years to 3 years in 10.9% of these patients if the findings from both colonoscopies were used to determine the appropriate timing for the next colonoscopy. However, when the BBPS ≥2 in each segment, adenomas were rarely missed on the initial colonoscopy and findings from the second colonoscopy rarely led to a change in the appropriate surveillance interval. This finding supports previous data that a BBPS of ≥2 in each segment is associated with 90% adherence to guideline recommendations. when no adenomas are found.
      • Calderwood A.
      • Schroy P.C.
      • Lieberman D.
      • et al.
      Boston Bowel Preparation Scale scores provide a standard definition of “adequate” for describing bowel cleanliness.
      Given the results from the current study by Clark et al,
      • Clark B.T.
      • Protiva P.
      • Nagar A.
      • et al.
      Quantification of adequate bowel preparation for screening or surveillance colonoscopy in men.
      a strong argument can be made that the BBPS should become the standard bowel preparation scale used for clinical practice and research.
      Some readers might look at these data and state that the miss rate for adenomas >5 mm is still approximately 5% with BBPS of 2-3, so why shouldn’t these patients return early, too? The answer to this question is multifaceted. First, although “no polyp left behind” may be the objective of every endoscopist, it is currently an unrealistic goal. Regardless of bowel cleansing quality and endoscopist skill, adenomas will be missed until technologic improvements allow comprehensive visualization of the entire colonic mucosa. A meta-analysis of tandem colonoscopy studies finds that 2.1% of adenomas ≥10 mm and 13% of adenomas 6-9 mm are missed on a first colonoscopy, yet found on a second colonoscopy.
      • van Rijn J.C.
      • Reitsma J.B.
      • Stoker J.
      • et al.
      Polyp miss rate determined by tandem colonoscopy: a systematic review.
      Physicians and patients alike must remember that no screening test is foolproof; the risk of an interval cancer after a normal screening colonoscopy in an average risk patient is approximately 1 in 1000.
      • Brenner H.
      • Chang-Claude J.
      • Seiler C.
      • et al.
      Protection from colorectal cancer after colonoscopy.
      • Adler J.
      • Robertson D.J.
      Interval colorectal cancer after colonoscopy: exploring explanations and solutions.
      Fortunately, the vast majority of adenomas never progress to cancer. Second, the recently published multisociety position statement on Quality Indicators for Colonoscopy
      • Rex D.K.
      • Schoenfeld P.
      • Cohen J.
      • et al.
      Quality indicators for colonoscopy.
      does provide endoscopists with some flexibility to manage individual patients by allowing a 10% variance from guideline recommendations for timing of repeat screening and surveillance colonoscopy. Third, we should remember that more colonoscopy does not necessarily equal better patient care. In addition to substantial patient inconvenience and discomfort with bowel preparation and colonoscopy, the 7-day unplanned hospital visit rate (eg, emergency department visits, observation stays, or unplanned hospitalization) is 1.8% after outpatient colonoscopies per the Centers for Medicare and Medicaid Services,

      Public Comment Summary Report. Facility 7-day risk-standardized hospital visit rate after outpatient colonoscopy. Available: www.cms.gov/Medicare/Quality-Initiatives-Patient-AssessmentInstruments/MMS/CallforPublicComment.html. Accessed on November 15, 2015.

      whereas the cost effectiveness of CRC screening with colonoscopy is lost when patients routinely undergo colonoscopy sooner than recommended.
      • 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.
      • Levin B.
      • Lieberman D.A.
      • McFarland B.
      • et al.
      Screening and surveillance for 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.
      • Rex D.K.
      • Schoenfeld P.
      • Cohen J.
      • et al.
      Quality indicators for colonoscopy.
      Finally, in the era of Physician Quality Reporting System and increased emphasis on quality of care, provider performance on multiple quality indicators (including ADR, frequency of adequate bowel preparation, and adherence to guideline recommendations for timing of repeat colonoscopy) will be reported to payers, such as Centers for Medicare and Medicaid Services.
      Those who perform colonoscopy should use validated scoring systems to report the quality of bowel preparation and should adhere to guideline recommendations for surveillance when the preparation is deemed adequate. Thanks to Clark et al,
      • Clark B.T.
      • Protiva P.
      • Nagar A.
      • et al.
      Quantification of adequate bowel preparation for screening or surveillance colonoscopy in men.
      we now have long overdue data that define what qualifies for an “adequate” bowel preparation. Until and unless other bowel preparation scoring systems are likewise studied, these findings should encourage the widespread adoption of the BBPS, which is a validated, quantitative scale that can be easily learned.

      Acknowledgements

      This material is the result of work supported in part by resources from The Veterans Health Administration. The views expressed in this article are those of the authors and do not necessarily represent the views of the Department of Veterans Affairs.

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