Multidirectional Colonoscopy Quality Improvement Increases Adenoma Detection Rate: Results of the Seoul National University Hospital Healthcare System Gangnam Center Colonoscopy Quality Upgrade Project (Gangnam-CUP)

  • Ji Yeon Seo
  • Eun Hyo Jin
  • Jung Ho Bae
  • Joo Hyun Lim
  • Goh Eun Chung
  • Changhyun Lee
  • Min-Sun Kwak
  • Hae Yeon Kang
  • Ji Hyun Song
  • Sun Young Yang
  • Jong In Yang
  • Seon Hee Lim
  • Jeong Yoon Yim
  • Joo Sung Kim
  • Su Jin ChungEmail author
Original Article



To prevent colorectal cancer, high-quality colonoscopy is advocated, undertaken by endoscopists with high adenoma detection rates (ADRs). Despite reports that various factors may impact ADRs, the significance of such factors is still unclear.


The analysis was aimed at quality-oriented interventions for boosting ADRs.


Study enrollees were adults subjected to screening colonoscopy between September 2013 and August 2016 at the Gangnam Center of Seoul National University Hospital Healthcare System. The investigation entailed six periods (P1–6) of 6 months each, during which serial multidirectional quality improvement efforts were instituted. In particular, we sought to further educate endoscopists, provide feedback on individual ADRs, and introduce a split-dose regimen, gauging results via the Boston Bowel Preparation Score. Changes in polyp detection rates (PDRs) and ADRs were then analyzed.


A total of 13,430 colonoscopies were undertaken by 15 experienced endoscopists. Overall, the ADR increased from 45.6% (P1) to 48.2% (P6, p < 0.001). The PDR, ADR, and advanced adenoma detection rate (AdvADR) showed the greatest increases between P3 and P4 [PDR 67.8% → 71.2% (p < 0.001); ADR 44.1% → 47.7% (p = 0.001); AdvADR 2.3% → 3.3% (p = 0.028)] in keeping with the introduction of a split-dose regimen. The sessile serrated adenoma detection rate (SSADR) increased substantially from 2.1% (P1) to 7.9% (P6, p < 0.001), with the largest gain between P1 and P2, just after education (p = 0.023).


Successful quality improvement in colonoscopy was achieved through comprehensive multidirectional efforts in education, feedback, and enhanced bowel preparation. Achieving high-level bowel preparation was paramount in ADR improvement. The SSADR was improved through education.


Adenoma detection rate Colonoscopy Quality improvement Education Feedback 



The authors wish to thank the entire staff of SNUH Gangnam Center for their joint support in this study and the endoscopy team for participating in this quality improvement program. The authors wish to thank Boram Park (Department of Public Health Science, Seoul National University, Seoul, Korea) for statistical support in this study.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflicts of interest for this article.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consents were accepted from all participating endoscopists.


  1. 1.
    Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66:683–691. Scholar
  2. 2.
    Loberg M, Kalager M, Holme O, Hoff G, Adami HO, Bretthauer M. Long-term colorectal-cancer mortality after adenoma removal. N Engl J Med. 2014;371:799–807. Scholar
  3. 3.
    Zauber AG, Winawer SJ, O’Brien MJ, et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med. 2012;366:687–696. Scholar
  4. 4.
    Winawer SJ, Zauber AG, Ho MN, et al. Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. N Engl J Med. 1993;329:1977–1981. Scholar
  5. 5.
    Lakoff J, Paszat LF, Saskin R, Rabeneck L. Risk of developing proximal versus distal colorectal cancer after a negative colonoscopy: a population-based study. Clin Gastroenterol Hepatol. 2008;6:1117–1121. (quiz 064).CrossRefPubMedGoogle Scholar
  6. 6.
    Baxter NN, Goldwasser MA, Paszat LF, Saskin R, Urbach DR, Rabeneck L. Association of colonoscopy and death from colorectal cancer. Ann Intern Med. 2009;150:1–8.CrossRefGoogle Scholar
  7. 7.
    Singh H, Nugent Z, Demers AA, Kliewer EV, Mahmud SM, Bernstein CN. The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. Gastroenterology. 2010;139:1128–1137. Scholar
  8. 8.
    Pohl H, Srivastava A, Bensen SP, et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology. 2013;144:74e1–80e1. Scholar
  9. 9.
    Ketwaroo GA, Sawhney MS. Quality measures and quality improvements in colonoscopy. Curr Opin Gastroenterol. 2015;31:56–61. Scholar
  10. 10.
    Kaminski MF, Regula J, Kraszewska E, et al. Quality indicators for colonoscopy and the risk of interval cancer. N Engl J Med. 2010;362:1795–1803. Scholar
  11. 11.
    Rex DK, Schoenfeld PS, Cohen J, et al. Quality indicators for colonoscopy. Gastrointest Endosc. 2015;81:31–53. Scholar
  12. 12.
    Corley DA, Jensen CD, Marks AR, et al. Adenoma detection rate and risk of colorectal cancer and death. N Engl J Med. 2014;370:1298–1306. Scholar
  13. 13.
    Sherer EA, Imler TD, Imperiale TF. The effect of colonoscopy preparation quality on adenoma detection rates. Gastrointest Endosc. 2012;75:545–553. Scholar
  14. 14.
    Harewood GC, Sharma VK, de Garmo P. Impact of colonoscopy preparation quality on detection of suspected colonic neoplasia. Gastrointest Endosc. 2003;58:76–79. Scholar
  15. 15.
    Anderson JC, Butterly LF, Robinson CM, Goodrich M, Weiss JE. Impact of fair bowel preparation quality on adenoma and serrated polyp detection: data from the New Hampshire colonoscopy registry by using a standardized preparation-quality rating. Gastrointest Endosc. 2014;80:463–470. Scholar
  16. 16.
    Hong SN, Sung IK, Kim JH, et al. The effect of the bowel preparation status on the risk of missing polyp and adenoma during screening colonoscopy: a tandem colonoscopic study. Clin Endosc. 2012;45:404–411. Scholar
  17. 17.
    Martel M, Barkun AN, Menard C, Restellini S, Kherad O, Vanasse A. Split-dose preparations are superior to day-before bowel cleansing regimens: a meta-analysis. Gastroenterology. 2015;149:79–88. Scholar
  18. 18.
    Chan WK, Azmi N, Mahadeva S, Goh KL. Split-dose vs same-day reduced-volume polyethylene glycol electrolyte lavage solution for morning colonoscopy. World J Gastroenterol. 2014;20:14488–14494. Scholar
  19. 19.
    Radaelli F, Paggi S, Hassan C, et al. Split-dose preparation for colonoscopy increases adenoma detection rate: a randomised controlled trial in an organised screening programme. Gut. 2017;66:270–277. Scholar
  20. 20.
    Flemming JA, Green J, Melicharkova A, Vanner S, Hookey L. Low-residue breakfast during the preparation for colonoscopy using a polyethylene glycol electrolyte solution: a randomised non-inferiority trial. BMJ Open Gastroenterol. 2015;2:e000029. Scholar
  21. 21.
    Kurlander JE, Sondhi AR, Waljee AK, et al. How efficacious are patient education interventions to improve bowel preparation for colonoscopy? A systematic review. PLoS ONE. 2016;11:e0164442. Scholar
  22. 22.
    Clark BT, Rustagi T, Laine L. What level of bowel prep quality requires early repeat colonoscopy: systematic review and meta-analysis of the impact of preparation quality on adenoma detection rate. Am J Gastroenterol. 2014;109:1714–1723. Scholar
  23. 23.
    Barclay RL, Vicari JJ, Doughty AS, Johanson JF, Greenlaw RL. Colonoscopic withdrawal times and adenoma detection during screening colonoscopy. N Engl J Med. 2006;355:2533–2541. Scholar
  24. 24.
    Sawhney MS, Cury MS, Neeman N, et al. Effect of institution-wide policy of colonoscopy withdrawal time > or = 7 minutes on polyp detection. Gastroenterology. 2008;135:1892–1898. Scholar
  25. 25.
    Lee SW, Chang JH, Ji JS, et al. Effect of dynamic position changes on adenoma detection during colonoscope withdrawal: a randomized controlled multicenter trial. Am J Gastroenterol. 2016;111:63–69. Scholar
  26. 26.
    Hanson JM, Atkin WS, Cunliffe WJ, et al. Rectal retroflexion: an essential part of lower gastrointestinal endoscopic examination. Dis Colon Rectum. 2001;44:1706–1708.CrossRefGoogle Scholar
  27. 27.
    Saad A, Rex DK. Routine rectal retroflexion during colonoscopy has a low yield for neoplasia. World J Gastroenterol. 2008;14:6503–6505.CrossRefGoogle Scholar
  28. 28.
    Chandran S, Parker F, Vaughan R, et al. Right-sided adenoma detection with retroflexion versus forward-view colonoscopy. Gastrointest Endosc. 2015;81:608–613. Scholar
  29. 29.
    Clark BT, Parikh ND, Laine L. Yield of repeat forward-view examination of the right side of the colon in screening and surveillance colonoscopy. Gastrointest Endosc. 2016;84:126–132. Scholar
  30. 30.
    Shaukat A, Oancea C, Bond JH, Church TR, Allen JI. Variation in detection of adenomas and polyps by colonoscopy and change over time with a performance improvement program. Clin Gastroenterol Hepatol. 2009;7:1335–1340. Scholar
  31. 31.
    Rajasekhar PT, Rees CJ, Bramble MG, et al. A multicenter pragmatic study of an evidence-based intervention to improve adenoma detection: the Quality Improvement in Colonoscopy (QIC) study. Endoscopy. 2015;47:217–224. Scholar
  32. 32.
    Seo JY, Lee C, Jin EH, et al. Is a split-dose regimen of 2 L polyethylene glycol plus ascorbic acid tolerable for colonoscopy in an early morning visit to a comprehensive medical check-up? World J Gastroenterol. 2017;23:1030–1037. Scholar
  33. 33.
    Rostom A, Jolicoeur E. Validation of a new scale for the assessment of bowel preparation quality. Gastrointest Endosc. 2004;59:482–486.CrossRefGoogle Scholar
  34. 34.
    Lai EJ, Calderwood AH, Doros G, Fix OK, Jacobson BC. The Boston bowel preparation scale: a valid and reliable instrument for colonoscopy-oriented research. Gastrointest Endosc. 2009;69:620–625. Scholar
  35. 35.
    Kluge MA, Williams JL, Wu CK, et al. Inadequate Boston Bowel Preparation Scale scores predict the risk of missed neoplasia on the next colonoscopy. Gastrointest Endosc. 2018;87:744–751. Scholar
  36. 36.
    Coe SG, Crook JE, Diehl NN, Wallace MB. An endoscopic quality improvement program improves detection of colorectal adenomas. Am J Gastroenterol. 2013;108:219–226. (quiz 27).CrossRefPubMedGoogle Scholar
  37. 37.
    Rex DK, Ahnen DJ, Baron JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol. 2012;107:1315–1329. (quiz 4, 30).CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Torlakovic EE, Gomez JD, Driman DK, et al. Sessile serrated adenoma (SSA) vs. traditional serrated adenoma (TSA). Am J Surg Pathol. 2008;32:21–29. Scholar
  39. 39.
    East JE, Saunders BP, Jass JR. Sporadic and syndromic hyperplastic polyps and serrated adenomas of the colon: classification, molecular genetics, natural history, and clinical management. Gastroenterol Clin North Am. 2008;37:25–46. Scholar
  40. 40.
    Rex DK, Schoenfeld PS, Cohen J, et al. Quality indicators for colonoscopy. Am J Gastroenterol. 2015;110:72–90. Scholar
  41. 41.
    Gurudu SR, Ramirez FC, Harrison ME, Leighton JA, Crowell MD. Increased adenoma detection rate with system-wide implementation of a split-dose preparation for colonoscopy. Gastrointest Endosc. 2012;76:603e1–608e1. Scholar
  42. 42.
    Jover R, Zapater P, Polania E, et al. Modifiable endoscopic factors that influence the adenoma detection rate in colorectal cancer screening colonoscopies. Gastrointest Endosc. 2013;77:381e1–389e1. Scholar
  43. 43.
    Kilgore TW, Abdinoor AA, Szary NM, et al. Bowel preparation with split-dose polyethylene glycol before colonoscopy: a meta-analysis of randomized controlled trials. Gastrointest Endosc. 2011;73:1240–1245. Scholar
  44. 44.
    Enestvedt BK, Tofani C, Laine LA, Tierney A, Fennerty MB. 4-Liter split-dose polyethylene glycol is superior to other bowel preparations, based on systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2012;10:1225–1231. Scholar
  45. 45.
    Park JS, Sohn CI, Hwang SJ, et al. Quality and effect of single dose versus split dose of polyethylene glycol bowel preparation for early-morning colonoscopy. Endoscopy. 2007;39:616–619. Scholar
  46. 46.
    Johnson DA, Barkun AN, Cohen LB, et al. Optimizing adequacy of bowel cleansing for colonoscopy: recommendations from the U.S. multi-society task force on colorectal cancer. Gastrointest Endosc. 2014;80:543–562. Scholar
  47. 47.
    Overholt BF, Brooks-Belli L, Grace M, et al. Withdrawal times and associated factors in colonoscopy: a quality assurance multicenter assessment. J Clin Gastroenterol. 2010;44:e80–e86. Scholar
  48. 48.
    Kaminski MF, Anderson J, Valori R, et al. Leadership training to improve adenoma detection rate in screening colonoscopy: a randomised trial. Gut. 2016;65:616–624. Scholar
  49. 49.
    Nutalapati V, Kanakadandi V, Desai M, Olyaee M, Rastogi A. Cap-assisted colonoscopy: a meta-analysis of high-quality randomized controlled trials. Endosc Int Open. 2018;6:E1214–E1223. Scholar
  50. 50.
    Ussui V, Coe S, Rizk C, Crook JE, Diehl NN, Wallace MB. Stability of increased adenoma detection at colonoscopy. Follow-up of an endoscopic quality improvement program-EQUIP-II. Am J Gastroenterol. 2015;110:489–496. Scholar
  51. 51.
    Wallace MB, Crook JE, Thomas CS, Staggs E, Parker L, Rex DK. Effect of an endoscopic quality improvement program on adenoma detection rates: a multicenter cluster-randomized controlled trial in a clinical practice setting (EQUIP-3). Gastrointest Endosc. 2017;85:538e4–545e4. Scholar
  52. 52.
    Racho RG, Krishna M, Coe SG, et al. Impact of an endoscopic quality improvement program focused on adenoma detection on sessile serrated adenoma/polyp detection. Digest Dis Sci. 2017;62:1464–1471. Scholar
  53. 53.
    Anderson JC, Butterly LF, Weiss JE, Robinson CM. Providing data for serrated polyp detection rate benchmarks: an analysis of the New Hampshire Colonoscopy Registry. Gastrointest Endosc. 2017;85:1188–1194. Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Ji Yeon Seo
    • 1
  • Eun Hyo Jin
    • 1
  • Jung Ho Bae
    • 1
  • Joo Hyun Lim
    • 1
  • Goh Eun Chung
    • 1
  • Changhyun Lee
    • 1
  • Min-Sun Kwak
    • 1
  • Hae Yeon Kang
    • 1
  • Ji Hyun Song
    • 1
  • Sun Young Yang
    • 1
  • Jong In Yang
    • 1
  • Seon Hee Lim
    • 1
  • Jeong Yoon Yim
    • 1
  • Joo Sung Kim
    • 1
    • 2
  • Su Jin Chung
    • 1
    Email author
  1. 1.Department of Internal Medicine and Healthcare Research Institute, Healthcare System Gangnam CenterSeoul National University HospitalSeoulSouth Korea
  2. 2.Department of Internal Medicine and Liver Research InstituteSeoul National University College of MedicineSeoulSouth Korea

Personalised recommendations