Colorectal cancer screening: Colonoscopy has disadvantages

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Colorectal cancer screening: Colonoscopy has disadvantages
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Joseph B. Weiss, MD
Nancy S. Cetel, MD
Danielle E. Weiss, MD

To the Editor: In the article, “Colorectal cancer screening: Choosing the right test,” the authors offer an excellent review, but restrict the discussion to just 2 of the many options. Screening compliance improves when clinicians and patients can select their preferred screening approach, and other noninvasive or minimally invasive approaches also deserve consideration and may well be superior. It is important that both the patient and the healthcare provider be fully aware of the advantages and disadvantages of each method.

The article is overly generous in its description of the accuracy and sensitivity of optical colonoscopy. The statement that colonoscopy visualizes the entire colon in more than 98% of cases is not supported by the biomedical literature or clinical experience. The measure of colonoscopy accuracy is best quantified by a review of more than 15,000 tandem colonoscopies that showed an average polyp miss rate of 22% using standard colonoscopes, and a 69% polyp miss rate compared with full-spectrum colonoscopes with greater fields of view.1–3 Between 5% and 10% of colonoscopies are technically incomplete and do not reach the cecum. Only 35% of colonoscopy bowel preps are excellent, and 21% are so poor that the procedure cannot be completed.4–8 Colorectal cancers are frequently missed at colonoscopy, with a rate of 7% quoted in the literature for interval cancer development.9–16 Studies of computed tomography colonography (virtual colonoscopy) have confirmed that between 10% and 20% of the colonic mucosa is hidden from view on optical colonoscopy by tall haustral mucosal folds.17,18 The operator variation measured by adenoma detection rates can exceed a 10-fold differential.

Colonoscopy is an important and valuable diagnostic and therapeutic tool. The disadvantages include significant cancer and polyp miss rates, high discomfort, high expense, potentially life-threatening complications, time- and resource-intensive utilization, high loss of patient work productivity, challenging and frequently inadequate preparation, higher risk of metachronous cancer and polyp spread, and high operator variability of quality.19–24 Unfortunately, while colonoscopy is an important tool, it does not come anywhere close to a score of 98% and should not be considered the gold standard for colorectal cancer screening.25

References
  1. Zhao S, Wang S, Pan P, et al. Magnitude, risk factors, and factors associated with adenoma miss rate of tandem colonoscopy: a systemic review and meta-analysis. Gastroenterology 2019; 156(6):1661–1674. doi:10.1053/j.gastro.2019.01.260
  2. van Rijn JC, Reitsma JB, Stoker J, Bossuyt PM, van Deventer SJ, Dekker E. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am J Gastroenterol 2006; 101(2):343–350. doi:10.1111/j.1572-0241.2006.00390.x
  3. Gralnek IM, Siersema PD, Halpern Z, et al. Standard forward-viewing colonoscopy versus full-spectrum endoscopy: an international, multicenter, randomised, tandem colonoscopy trial. Lancet Oncol 2014; 15(3):353–360. doi:10.1016/S1470-2045(14)70020-8
  4. Ness RM, Manam R, Hoen H, Chalasani N. Predictors of inadequate bowel preparation for colonoscopy. Am J Gastroenterol 2001; 96(6):1797–1802. doi:10.1111/j.1572-0241.2001.03874.x 
  5. Kluge M, Williams J, Wu C, et al. Inadequate Boston Bowel Preparation Scale scores predict the risk of missed neoplasia on the next colonoscopy. Gastrointest Endosc 2018; 87(3):744–751. doi:10.1016/j.gie.2017.06.012
  6. Gagneja H, Parekh P, Burleson D, et al. HyGIeaCare® preparation for colonoscopy – a technical update for success. J Gastrointest Dig Syst 2016; 6:4. doi:10.4172/2161-069X.1000458
  7. Das A, Parekh P, Bekal P, et al. Bowel preparation for colonoscopy: a comparative cost-effective analysis of traditional per os purgatory prep versus a novel method using high-volume colonic water irrigation. Gastroenterol Hepatol Int J 2017; 2(4):000132.
  8. D’Souza SM, Parekh PJ, Johnson DA. The dirty side of colonoscopy: predictors of poor bowel preparation and novel approaches to overcome the shortcomings. Br J Gastroenterol 2019: 1:1. https://hygieacare.com/wp-content/uploads/2019/06/The-Dirty-Side-of-Colonoscopy-PDF.pdf. Accessed October 23, 2019.
  9. Mouchli M, Ouk L, Scheitel M. Colonoscopy surveillance for high risk polyps does not always prevent colorectal cancer. World J Gastroenterol 2018; 24(8):905–916. doi:10.3748/wjg.v24.i8.905
  10. Adler J, Robertson DJ. Interval colorectal cancer after colonoscopy: exploring explanations and solutions. Am J Gastroenterol 2015; 110(12):1657–1664. doi:10.1038/ajg.2015.365
  11. Robertson DJ, Lieberman DA, Winawer SJ, et al. Colorectal cancers soon after colonoscopy: a pooled multi-cohort analysis. Gut 2014; 63(6):949–956. doi:10.1136/gutjnl-2012-303796
  12. Brenner H, Chang-Claude J, Seiler CM, Rickert A, Hoffmeister M. Protection from colorectal cancer after colonoscopy: a population-based, case-control study. Ann Intern Med 2011; 154(1):22–30. doi:10.7326/0003-4819-154-1-201101040-00004
  13. Brenner H, Chang-Claude J, Seiler CM, Hoffmeister M. Long-term risk of colorectal cancer after negative colonoscopy. J Clin Oncol 2011; 29(28):3761–3767. doi:10.1200/JCO.2011.35.9307
  14. Pohl H, Robertson DJ. Colorectal cancers detected after colonoscopy frequently result from missed lesions. Clin Gastroenterol Hepatol 2010; 8(10):858–864. doi:10.1016/j.cgh.2010.06.028
  15. Singh H, Nugent Z, Demers AA, Bernstein CN. Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study. Am J Gastroenterol 2010; 105(12):2588–2596. doi:10.1038/ajg.2010.390
  16. 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. doi:10.1056/NEJMoa1301969
  17. Thompson A, Jones R, Pou P, et al. Taller haustral folds in the proximal colon: a potential factor contributing to interval colorectal cancer. J Colon Rectal Cancer 2016; 1(1):45–54. doi:10.14302/issn.2471-7061.jcrc-15-899
  18. Zhu H, Barish M, Pickhardt P, et al. Haustral fold segmentation with curvature-guided level set evolution. IEEE Trans Biomed Eng 2013; 60(2):321–331. doi:10.1109/TBME.2012.2226242
  19. 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. doi:10.1016/j.gie.2012.11.012
  20. Reumkens A, Rondagh EJ, Bakker CM, et al. Post-colonoscopy complications: a systematic review, time trends, and meta-analysis of population-based studies. Am J Gastroenterol 2016; 111(8):1092–1101. doi:10.1038/ajg.2016.234
  21. ASGE Standards of Practice Committee, Fisher DA, Maple JT, Ben-Menachem T, et al. Complications of colonoscopy. Gastrointest Endosc 2011; 74(4):745–752. doi:10.1016/j.gie.2011.07.025
  22. 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. doi:10.7326/0003-4819-150-12-200906160-00008
  23. Whitlock EP, Lin JS, Liles E, et al. Screening for colorectal cancer: a targeted, updated systematic review for the U.S. Preventive Services Task Force. Ann Intern Med 2008; 149(9):638–658. doi:10.7326/0003-4819-149-9-200811040-00245
  24. Backes Y, Seerden T, van Gestel R, et al. Tumor seeding during colonoscopy as a possible cause for metachronous colorectal cancer. Gastroenterology 2019; Aug 13. pii: S0016-5085(19)41229-8. [Epub ahead of print] doi:10.1053/j.gastro.2019.07.062
  25. Lin JS, Piper MA, Perdue LA, et al. Screening for colorectal cancer: updated evidence report and systematic review for the US Preventive Services Task Force. JAMA 2016; 315(23):2576–2594. doi:10.1001/jama.2016.3332
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Joseph B. Weiss, MD
University of California San Diego

Nancy S. Cetel, MD
Speaking of Health Inc., San Diego, CA

Danielle E. Weiss, MD
University of California San Diego

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Cleveland Clinic Journal of Medicine - 86(12)
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colorectal cancer, screening, colonoscopy, Joseph Weiss, Nancy Cetel, Danielle Weiss
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Nancy S. Cetel, MD
Danielle E. Weiss, MD
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Nancy S. Cetel, MD
Danielle E. Weiss, MD
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University of California San Diego

Nancy S. Cetel, MD
Speaking of Health Inc., San Diego, CA

Danielle E. Weiss, MD
University of California San Diego

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University of California San Diego

Nancy S. Cetel, MD
Speaking of Health Inc., San Diego, CA

Danielle E. Weiss, MD
University of California San Diego

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In reply: Colorectal cancer screening
Colorectal cancer screening: Choosing the right test

To the Editor: In the article, “Colorectal cancer screening: Choosing the right test,” the authors offer an excellent review, but restrict the discussion to just 2 of the many options. Screening compliance improves when clinicians and patients can select their preferred screening approach, and other noninvasive or minimally invasive approaches also deserve consideration and may well be superior. It is important that both the patient and the healthcare provider be fully aware of the advantages and disadvantages of each method.

The article is overly generous in its description of the accuracy and sensitivity of optical colonoscopy. The statement that colonoscopy visualizes the entire colon in more than 98% of cases is not supported by the biomedical literature or clinical experience. The measure of colonoscopy accuracy is best quantified by a review of more than 15,000 tandem colonoscopies that showed an average polyp miss rate of 22% using standard colonoscopes, and a 69% polyp miss rate compared with full-spectrum colonoscopes with greater fields of view.1–3 Between 5% and 10% of colonoscopies are technically incomplete and do not reach the cecum. Only 35% of colonoscopy bowel preps are excellent, and 21% are so poor that the procedure cannot be completed.4–8 Colorectal cancers are frequently missed at colonoscopy, with a rate of 7% quoted in the literature for interval cancer development.9–16 Studies of computed tomography colonography (virtual colonoscopy) have confirmed that between 10% and 20% of the colonic mucosa is hidden from view on optical colonoscopy by tall haustral mucosal folds.17,18 The operator variation measured by adenoma detection rates can exceed a 10-fold differential.

Colonoscopy is an important and valuable diagnostic and therapeutic tool. The disadvantages include significant cancer and polyp miss rates, high discomfort, high expense, potentially life-threatening complications, time- and resource-intensive utilization, high loss of patient work productivity, challenging and frequently inadequate preparation, higher risk of metachronous cancer and polyp spread, and high operator variability of quality.19–24 Unfortunately, while colonoscopy is an important tool, it does not come anywhere close to a score of 98% and should not be considered the gold standard for colorectal cancer screening.25

To the Editor: In the article, “Colorectal cancer screening: Choosing the right test,” the authors offer an excellent review, but restrict the discussion to just 2 of the many options. Screening compliance improves when clinicians and patients can select their preferred screening approach, and other noninvasive or minimally invasive approaches also deserve consideration and may well be superior. It is important that both the patient and the healthcare provider be fully aware of the advantages and disadvantages of each method.

The article is overly generous in its description of the accuracy and sensitivity of optical colonoscopy. The statement that colonoscopy visualizes the entire colon in more than 98% of cases is not supported by the biomedical literature or clinical experience. The measure of colonoscopy accuracy is best quantified by a review of more than 15,000 tandem colonoscopies that showed an average polyp miss rate of 22% using standard colonoscopes, and a 69% polyp miss rate compared with full-spectrum colonoscopes with greater fields of view.1–3 Between 5% and 10% of colonoscopies are technically incomplete and do not reach the cecum. Only 35% of colonoscopy bowel preps are excellent, and 21% are so poor that the procedure cannot be completed.4–8 Colorectal cancers are frequently missed at colonoscopy, with a rate of 7% quoted in the literature for interval cancer development.9–16 Studies of computed tomography colonography (virtual colonoscopy) have confirmed that between 10% and 20% of the colonic mucosa is hidden from view on optical colonoscopy by tall haustral mucosal folds.17,18 The operator variation measured by adenoma detection rates can exceed a 10-fold differential.

Colonoscopy is an important and valuable diagnostic and therapeutic tool. The disadvantages include significant cancer and polyp miss rates, high discomfort, high expense, potentially life-threatening complications, time- and resource-intensive utilization, high loss of patient work productivity, challenging and frequently inadequate preparation, higher risk of metachronous cancer and polyp spread, and high operator variability of quality.19–24 Unfortunately, while colonoscopy is an important tool, it does not come anywhere close to a score of 98% and should not be considered the gold standard for colorectal cancer screening.25

References
  1. Zhao S, Wang S, Pan P, et al. Magnitude, risk factors, and factors associated with adenoma miss rate of tandem colonoscopy: a systemic review and meta-analysis. Gastroenterology 2019; 156(6):1661–1674. doi:10.1053/j.gastro.2019.01.260
  2. van Rijn JC, Reitsma JB, Stoker J, Bossuyt PM, van Deventer SJ, Dekker E. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am J Gastroenterol 2006; 101(2):343–350. doi:10.1111/j.1572-0241.2006.00390.x
  3. Gralnek IM, Siersema PD, Halpern Z, et al. Standard forward-viewing colonoscopy versus full-spectrum endoscopy: an international, multicenter, randomised, tandem colonoscopy trial. Lancet Oncol 2014; 15(3):353–360. doi:10.1016/S1470-2045(14)70020-8
  4. Ness RM, Manam R, Hoen H, Chalasani N. Predictors of inadequate bowel preparation for colonoscopy. Am J Gastroenterol 2001; 96(6):1797–1802. doi:10.1111/j.1572-0241.2001.03874.x 
  5. Kluge M, Williams J, Wu C, et al. Inadequate Boston Bowel Preparation Scale scores predict the risk of missed neoplasia on the next colonoscopy. Gastrointest Endosc 2018; 87(3):744–751. doi:10.1016/j.gie.2017.06.012
  6. Gagneja H, Parekh P, Burleson D, et al. HyGIeaCare® preparation for colonoscopy – a technical update for success. J Gastrointest Dig Syst 2016; 6:4. doi:10.4172/2161-069X.1000458
  7. Das A, Parekh P, Bekal P, et al. Bowel preparation for colonoscopy: a comparative cost-effective analysis of traditional per os purgatory prep versus a novel method using high-volume colonic water irrigation. Gastroenterol Hepatol Int J 2017; 2(4):000132.
  8. D’Souza SM, Parekh PJ, Johnson DA. The dirty side of colonoscopy: predictors of poor bowel preparation and novel approaches to overcome the shortcomings. Br J Gastroenterol 2019: 1:1. https://hygieacare.com/wp-content/uploads/2019/06/The-Dirty-Side-of-Colonoscopy-PDF.pdf. Accessed October 23, 2019.
  9. Mouchli M, Ouk L, Scheitel M. Colonoscopy surveillance for high risk polyps does not always prevent colorectal cancer. World J Gastroenterol 2018; 24(8):905–916. doi:10.3748/wjg.v24.i8.905
  10. Adler J, Robertson DJ. Interval colorectal cancer after colonoscopy: exploring explanations and solutions. Am J Gastroenterol 2015; 110(12):1657–1664. doi:10.1038/ajg.2015.365
  11. Robertson DJ, Lieberman DA, Winawer SJ, et al. Colorectal cancers soon after colonoscopy: a pooled multi-cohort analysis. Gut 2014; 63(6):949–956. doi:10.1136/gutjnl-2012-303796
  12. Brenner H, Chang-Claude J, Seiler CM, Rickert A, Hoffmeister M. Protection from colorectal cancer after colonoscopy: a population-based, case-control study. Ann Intern Med 2011; 154(1):22–30. doi:10.7326/0003-4819-154-1-201101040-00004
  13. Brenner H, Chang-Claude J, Seiler CM, Hoffmeister M. Long-term risk of colorectal cancer after negative colonoscopy. J Clin Oncol 2011; 29(28):3761–3767. doi:10.1200/JCO.2011.35.9307
  14. Pohl H, Robertson DJ. Colorectal cancers detected after colonoscopy frequently result from missed lesions. Clin Gastroenterol Hepatol 2010; 8(10):858–864. doi:10.1016/j.cgh.2010.06.028
  15. Singh H, Nugent Z, Demers AA, Bernstein CN. Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study. Am J Gastroenterol 2010; 105(12):2588–2596. doi:10.1038/ajg.2010.390
  16. 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. doi:10.1056/NEJMoa1301969
  17. Thompson A, Jones R, Pou P, et al. Taller haustral folds in the proximal colon: a potential factor contributing to interval colorectal cancer. J Colon Rectal Cancer 2016; 1(1):45–54. doi:10.14302/issn.2471-7061.jcrc-15-899
  18. Zhu H, Barish M, Pickhardt P, et al. Haustral fold segmentation with curvature-guided level set evolution. IEEE Trans Biomed Eng 2013; 60(2):321–331. doi:10.1109/TBME.2012.2226242
  19. 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. doi:10.1016/j.gie.2012.11.012
  20. Reumkens A, Rondagh EJ, Bakker CM, et al. Post-colonoscopy complications: a systematic review, time trends, and meta-analysis of population-based studies. Am J Gastroenterol 2016; 111(8):1092–1101. doi:10.1038/ajg.2016.234
  21. ASGE Standards of Practice Committee, Fisher DA, Maple JT, Ben-Menachem T, et al. Complications of colonoscopy. Gastrointest Endosc 2011; 74(4):745–752. doi:10.1016/j.gie.2011.07.025
  22. 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. doi:10.7326/0003-4819-150-12-200906160-00008
  23. Whitlock EP, Lin JS, Liles E, et al. Screening for colorectal cancer: a targeted, updated systematic review for the U.S. Preventive Services Task Force. Ann Intern Med 2008; 149(9):638–658. doi:10.7326/0003-4819-149-9-200811040-00245
  24. Backes Y, Seerden T, van Gestel R, et al. Tumor seeding during colonoscopy as a possible cause for metachronous colorectal cancer. Gastroenterology 2019; Aug 13. pii: S0016-5085(19)41229-8. [Epub ahead of print] doi:10.1053/j.gastro.2019.07.062
  25. Lin JS, Piper MA, Perdue LA, et al. Screening for colorectal cancer: updated evidence report and systematic review for the US Preventive Services Task Force. JAMA 2016; 315(23):2576–2594. doi:10.1001/jama.2016.3332
References
  1. Zhao S, Wang S, Pan P, et al. Magnitude, risk factors, and factors associated with adenoma miss rate of tandem colonoscopy: a systemic review and meta-analysis. Gastroenterology 2019; 156(6):1661–1674. doi:10.1053/j.gastro.2019.01.260
  2. van Rijn JC, Reitsma JB, Stoker J, Bossuyt PM, van Deventer SJ, Dekker E. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am J Gastroenterol 2006; 101(2):343–350. doi:10.1111/j.1572-0241.2006.00390.x
  3. Gralnek IM, Siersema PD, Halpern Z, et al. Standard forward-viewing colonoscopy versus full-spectrum endoscopy: an international, multicenter, randomised, tandem colonoscopy trial. Lancet Oncol 2014; 15(3):353–360. doi:10.1016/S1470-2045(14)70020-8
  4. Ness RM, Manam R, Hoen H, Chalasani N. Predictors of inadequate bowel preparation for colonoscopy. Am J Gastroenterol 2001; 96(6):1797–1802. doi:10.1111/j.1572-0241.2001.03874.x 
  5. Kluge M, Williams J, Wu C, et al. Inadequate Boston Bowel Preparation Scale scores predict the risk of missed neoplasia on the next colonoscopy. Gastrointest Endosc 2018; 87(3):744–751. doi:10.1016/j.gie.2017.06.012
  6. Gagneja H, Parekh P, Burleson D, et al. HyGIeaCare® preparation for colonoscopy – a technical update for success. J Gastrointest Dig Syst 2016; 6:4. doi:10.4172/2161-069X.1000458
  7. Das A, Parekh P, Bekal P, et al. Bowel preparation for colonoscopy: a comparative cost-effective analysis of traditional per os purgatory prep versus a novel method using high-volume colonic water irrigation. Gastroenterol Hepatol Int J 2017; 2(4):000132.
  8. D’Souza SM, Parekh PJ, Johnson DA. The dirty side of colonoscopy: predictors of poor bowel preparation and novel approaches to overcome the shortcomings. Br J Gastroenterol 2019: 1:1. https://hygieacare.com/wp-content/uploads/2019/06/The-Dirty-Side-of-Colonoscopy-PDF.pdf. Accessed October 23, 2019.
  9. Mouchli M, Ouk L, Scheitel M. Colonoscopy surveillance for high risk polyps does not always prevent colorectal cancer. World J Gastroenterol 2018; 24(8):905–916. doi:10.3748/wjg.v24.i8.905
  10. Adler J, Robertson DJ. Interval colorectal cancer after colonoscopy: exploring explanations and solutions. Am J Gastroenterol 2015; 110(12):1657–1664. doi:10.1038/ajg.2015.365
  11. Robertson DJ, Lieberman DA, Winawer SJ, et al. Colorectal cancers soon after colonoscopy: a pooled multi-cohort analysis. Gut 2014; 63(6):949–956. doi:10.1136/gutjnl-2012-303796
  12. Brenner H, Chang-Claude J, Seiler CM, Rickert A, Hoffmeister M. Protection from colorectal cancer after colonoscopy: a population-based, case-control study. Ann Intern Med 2011; 154(1):22–30. doi:10.7326/0003-4819-154-1-201101040-00004
  13. Brenner H, Chang-Claude J, Seiler CM, Hoffmeister M. Long-term risk of colorectal cancer after negative colonoscopy. J Clin Oncol 2011; 29(28):3761–3767. doi:10.1200/JCO.2011.35.9307
  14. Pohl H, Robertson DJ. Colorectal cancers detected after colonoscopy frequently result from missed lesions. Clin Gastroenterol Hepatol 2010; 8(10):858–864. doi:10.1016/j.cgh.2010.06.028
  15. Singh H, Nugent Z, Demers AA, Bernstein CN. Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study. Am J Gastroenterol 2010; 105(12):2588–2596. doi:10.1038/ajg.2010.390
  16. 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. doi:10.1056/NEJMoa1301969
  17. Thompson A, Jones R, Pou P, et al. Taller haustral folds in the proximal colon: a potential factor contributing to interval colorectal cancer. J Colon Rectal Cancer 2016; 1(1):45–54. doi:10.14302/issn.2471-7061.jcrc-15-899
  18. Zhu H, Barish M, Pickhardt P, et al. Haustral fold segmentation with curvature-guided level set evolution. IEEE Trans Biomed Eng 2013; 60(2):321–331. doi:10.1109/TBME.2012.2226242
  19. 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. doi:10.1016/j.gie.2012.11.012
  20. Reumkens A, Rondagh EJ, Bakker CM, et al. Post-colonoscopy complications: a systematic review, time trends, and meta-analysis of population-based studies. Am J Gastroenterol 2016; 111(8):1092–1101. doi:10.1038/ajg.2016.234
  21. ASGE Standards of Practice Committee, Fisher DA, Maple JT, Ben-Menachem T, et al. Complications of colonoscopy. Gastrointest Endosc 2011; 74(4):745–752. doi:10.1016/j.gie.2011.07.025
  22. 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. doi:10.7326/0003-4819-150-12-200906160-00008
  23. Whitlock EP, Lin JS, Liles E, et al. Screening for colorectal cancer: a targeted, updated systematic review for the U.S. Preventive Services Task Force. Ann Intern Med 2008; 149(9):638–658. doi:10.7326/0003-4819-149-9-200811040-00245
  24. Backes Y, Seerden T, van Gestel R, et al. Tumor seeding during colonoscopy as a possible cause for metachronous colorectal cancer. Gastroenterology 2019; Aug 13. pii: S0016-5085(19)41229-8. [Epub ahead of print] doi:10.1053/j.gastro.2019.07.062
  25. Lin JS, Piper MA, Perdue LA, et al. Screening for colorectal cancer: updated evidence report and systematic review for the US Preventive Services Task Force. JAMA 2016; 315(23):2576–2594. doi:10.1001/jama.2016.3332
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