Colonoscopic removal of adenomatous polyps decreases the incidence of colorectal cancer (CRC) [1,2] and prevents CRC-related death [3]. Colonoscopy has been accepted as one of the most effective screening methods for colorectal neoplasia [4].

Nonetheless, CRCs are often diagnosed after a negative colonoscopy. Recent clinical studies suggest that etiology of these interval CRCs includes missed polyps, incompletely removed polyps, and de novo interval CRCs [5]. More than 50% of interval CRCs can be explained by missed lesions [6]. Therefore, emphasis has been placed on measures to increase the quality of colonoscopy. The indicators of high quality colonoscopy are classified as pre-procedural quality metrics (bowel preparation), procedural quality metrics (cecal intubation rate, withdrawal time, and adenoma detection rate [ADR]), and post-procedural quality metrics (surveillance interval) [7].

Although ADR is regarded as one of the most important quality metrics [8], a high ADR is not sufficient to guarantee a low adenoma miss rate (AMR), which may be more directly related to the development of interval CRC [9]. AMR can be measured by using back-to-back colonoscopy, which is almost impossible to perform in real-world practice.

Approximately 2.6 million cases of colonoscopy were performed in 2010 in Korea according to data from the Korean Health Insurance Review and Assessment Service [10]. Yet, little is known about colonoscopy quality of primary care clinics in Korea. According to a questionnaire-based study in Korea, only 57% and 87% of endoscopists in non-tertiary or non-academic hospital experienced EMR or polypectomy for colonic lesions [11]. When primary physicians detect polyps requiring snare polypectomy or endoscopic submucosal dissection during screening colonoscopy, it is a common practice to transfer the patient to secondary or tertiary hospitals for polypectomy. On the other hand, endoscopists in referral hospitals frequently detect missed polyps during therapeutic colonoscopy.

We performed this study to estimate colonoscopy quality of polypectomy-referring hospitals in Korea by evaluating polyp miss rate, AMR, and advanced neoplasm miss rate during colonoscopy for polypectomy. Risk factors associated with adenoma-missing were also explored.

ADR is inversely associated with the incidence of interval CRC [14] and CRC mortality [15]. Although ADR has been accepted as a priority quality metric for colonoscopy [8], it is not a perfect metric. It cannot differentiate an endoscopist who consistently finds multiple adenomas from an endoscopist who only finds one adenoma (“one and done” phenomenon). To better measure the quality of colonoscopy, adenomas detected per colonoscopy, adenomas per positive participant, and the number of additional adenomas found after the first adenoma per colonoscopy (ADR-Plus) were adopted [16].

To best of our knowledge, there has not been any real-world study of colonoscopy quality in Korea using quality metrics. If AMR could be measured in daily practice, it would be a more appropriate quality metric for colonoscopy, since the majority of interval CRCs are associated with missed adenomas. Presently, we measured AMRs of polypectomy-referring hospitals by comparing their colonoscopic findings and our findings during colonoscopy for polypectomy. Many primary care physicians doing colonoscopy do not perform snare polypectomy in Korea because of the limited procedure time for an individual patient, difficulties in post-polypectomy care including management of bleeding or perforation, concerns about legal issues, and other reasons. Certainly, this is an irrational use of medical resources, since the prevalence of colorectal neoplasms among asymptomatic patients who are screened was reported as 33% in Korea [17]. This indicates that a number of patients requiring polypectomy should have a repeat consecutive colonoscopy within a short period of time.

AMRs has been reported as 17% to 25% [9,18,19] and our pooled miss rate for adenomas, which is compatible with AMR of other studies, was measured 37%. Our miss rate could be augmented since all the study subjects had polyps and meticulous endoscopic examination or documentation in primary care clinics might be omitted after detection of a polyp requiring referral. We believe that better preparation and longer withdrawal time of our therapeutic colonoscopies compared to the initial colonoscopies may also have contributed to the high AMR of the present study.

Our results show that smaller adenomas are more frequently missed, which is consistent with previous studies [18-21]. Diminutive or small adenomas are frequently undetected when they are located behind a fold or submerged in the luminal fluid. Although study results for adenoma location and miss rate are controversial, it was reported that adenomas in the right colon were more frequently missed [19,20,22,23]. Adenoma detection could be interfered by higher mucosal folds of the right colon.

Even though the AMR of this study might be augmented, the miss rate of adenoma per patient 48% was still very high. That means that almost half the patients referred for polypectomy harbored missed adenomas. Moreover, the 7% miss rate of advanced neoplasia per patient indicates that approximately one of 13 subjects harbored a missed advanced neoplasm or more. This clearly suggests that the quality of colonoscopy delivered by primary care clinics needs to be improved in Korea.

Various factors influencing AMR per patient were suggested in previous studies as follows: number of adenoma detected during initial colonoscopy [18,19,23], characteristics of individual endoscopists [9,24], and age of patient [24,25]. Our multivariate analysis showed only age of patient and number of adenoma on initial colonoscopy were significantly related with presence of missed adenoma. It is unclear why age of patient is related with AMR. The positive relationship between the number of adenoma during initial colonoscopy and AMR can be explained by a reduced attention after having already detected polyps and time pressure on endoscopists due to a remained endoscopy list for that day [23].

Our multivariate analysis revealed that withdrawal time and bowel preparation of initial colonoscopy were not significantly related with presence of missed adenoma. Increased number of polyps including adenomas itself could be related with prolonged withdrawal time. Even though time spent for biopsy and polypectomy was excluded, extra time for photodocumentation and close observation should be spent. Prolonged withdrawal time of initial colonoscopy might be related with the time for already-detected polyps rather than undetected polyps. Regarding preparation scale of initial colonoscopy, advanced age is an independent risk factor for inadequate bowel preparation [26]. Thus the effect of bowel preparation scale of initial colonoscopy could be reduced in multivariate analysis.

This study has several limitations. First, it is a retrospective study based on review of medical records. Aronchick bowel preparation scale should be scored before any attempt of washing and suctioning. Thus, another bowel preparation scale such as Boston bowel preparation score [27] might be more suitable for assessment of bowel preparation in polypectomy-referring hospitals. However, retrospective assessment of each colonic segment in Boston score was not easy. Moreover, at the time of the study, all the bowel preparation scale in our institution was scored using Aronchick scale. Thus we decided to apply Aronchick scare to compare bowel preparation scale between polypectomy-referring hospitals and our institution. Estimation of accurate withdrawal time was also limited since it was based on retrospective review of the electronic images. Second, we cannot evaluate the AMR according to characteristics of individual endoscopist or polypectomy-referring hospital because of limited information. Finally, the AMR could be overestimated by the “one-and-done phenomenon.” On the contrary, exclusion of cases with unidentifiable procedure time or incomplete documentation, which might be associated with poor quality colonoscopy, could lead to underestimation of the AMR.

In conclusion, the AMR of polypectomy-referring hospitals is high in Korea. Meticulous total colon exploration should be performed during therapeutic colonoscopy and nation-wide monitoring of colonoscopy quality is definitely necessary.