Colorectal cancer (CRC) remains a major cause of cancer-related deaths worldwide [1]. CRC screening programs aim to reduce CRC-related mortality through early detection of cancer [2]. As most CRC develops gradually from adenomatous polyps through the adenoma-carcinoma sequence, it has been suggested that detection and removal of pre-cancerous lesions by colonoscopy can prevent development of CRC and reduce mortality associated with CRC [3,4]. Colonoscopy is the most sensitive tool for colorectal adenoma detection, and the detected adenoma can be resected during the procedure [5].

Although colonoscopy is regarded as the standard to detect and prevent CRC, this procedure has some limitations. Back-to-back colonoscopy revealed that the miss rate for adenomas of any size was 20% [6]. In addition, there are marked variations in polyp detection, complete polyp resection, and cancer prevention effects among fully trained colonoscopists [7-9]. Therefore, a high-quality colonoscopy is necessary to reduce CRC-related mortality. The American Society for Gastrointestinal Endoscopy guidelines provide quality indicators including cecal intubation rate ≥ 90%, adequate bowel preparation ≥ 85%, adenoma detection rate (ADR) ≥ 25%, and average withdrawal time ≥ 6 minutes to ensure adequate colonoscopy quality [10].

Colonoscopy is now widely used in various clinical practice settings not only in academic medical centers, but also in community hospitals and nonhospital facilities. In Korea, the National Endoscopy Quality Improvement Program exists for colonoscopy quality control [11]. However, little is known regarding the substantive quality of colonoscopy in real-life practice settings. It is important to maintain a similar level of colonoscopy quality among various clinical care settings in a population-based screening program. Therefore, we aimed to evaluate the quality of colonoscopies performed in community hospitals and nonhospital facilities in real-life practice.

In the present work, we found that the quality of colonoscopies performed in community hospitals and nonhospital facilities was suboptimal. Approximately one-third of colonoscopies were withdrawn within 6 minutes and had incomplete photo-documentation. Although the overall rate of cecal intubation exceeded 90%, the cecal intubation rate of non-board-certified endoscopists was 85.2%. Moreover, a large number of polyps were newly detected on follow-up exams within a short period of time.

According to previous studies conducted in Spain and the United States comparing the quality of colonoscopies between various practice settings, both academic and non-academic centers provided high-quality colonoscopies [14,15]. Our results, unlike previous studies, showed that the quality of colonoscopies in community hospitals and nonhospital facilities was suboptimal. In addition, community hospitals tend to perform colonoscopies of higher quality than nonhospital facilities. This disparity may be difficult to explain, given that there are numerous factors affecting the quality of care in medical practice environments [16]. In Korea, there is no medical budget for quality of care, and reimbursement for medical care is relatively low for nonhospital facilities. Indeed, the cost of a colonoscopy in Korea is approximately $72.6 (1100.3 Korean won = 1 US dollar by an annual exchange rate in 2018) [17], which is significantly lower than the cost of approximately $899 in the United States [18]. In addition, small-volume endoscopy units lack staff fully responsible for endoscopy and quality management. Meanwhile, it is also necessary to consider the possibility that excessive endoscopic workloads may result in suboptimal quality. Previous studies on the relationship between colonoscopy volume and quality have been inconclusive [19,20]. However, a recent study on the capacity for colonoscopies in Korea showed that there is a heavy colonoscopy workload and lack of capacity [21]. Further research and discussion on appropriate cost and colonoscopy workload is needed.

Interval CRCs, generally defined as CRCs after index colonoscopy before the next surveillance schedule, account for 1.8% to 9.0% of all CRCs [22]. Although the etiology of interval CRCs is unclear, the majority of interval CRCs originates from missed lesions [23]. Non-gastroenterologists and incomplete exams are associated with an increased risk of interval CRCs [24]. In our results, non-board-certified endoscopists had a higher rate of incomplete exams than board-certified endoscopists, although it was not an independent risk factor for missed polyps. It is worth noting that KSGE provides board certification to both internists and surgeons who have completed training at a designated training endoscopy center and have passed a qualifying examination [25]. In addition, to maintain qualifications, endoscopists should complete an annual education program including quality management [25]. This suggests that qualified endoscopists who were systematically trained in endoscopy and quality management are important for high-quality colonoscopies, regardless of their specialty in medical practice.

The suboptimal colonoscopy quality seen in community hospitals and nonhospital facilities in our results calls for strengthening quality management systems. In Korea, the National Cancer Screening Program (NCSP) provides fecal occult blood testing for adults 50 years of age or older and colonoscopies for positive cases [26]. For endoscopy quality management, NCSP operates an Endoscopy Quality Improvement Program, and revised quality indicators were recently published by the KSGE [11]. Quality indicators consist of 34 items in six areas of the workforce, process, facilities and equipment, outcome, reprocessing, and sedation [11]. However, endoscopy quality evaluation criteria only assess the overall quality of the institution, not the performance indicators of the individual endoscopist. Therefore, an individual endoscopist’s cecal intubation rate, mean withdrawal time, and ADR are not measured. In addition, measurement of quality indicators depends on voluntary reporting by the endoscopist, and most end up with a document review without a field investigation. This suggests that current quality assessment and audit systems may be ineffective in real-life practice settings.

Poor-quality colonoscopies may cause not only interval CRCs and CRC-related deaths, but also overutilization, subsequent complications, and increased medical costs [27]. The cost for improving colonoscopy quality may be lower than the medical costs brought on by overutilization and subsequent complications associated with poor-quality colonoscopies. Cost-effective methods for quality improvement need to be discussed. In the United States, the Center for Medicare & Medicaid Services has a Physician Quality Reporting System in which physicians voluntarily report endoscopy quality indicators and receive incentives [28]. In Spain, all screening colonoscopy data are coded by the coordinating staff in the Basque Country CRC Screening Program. In this way, data on colonoscopy quality indicators including ADR, cecal intubation rate, complications, and bowel preparation quality can be collected [14,29].

Ultimately, a comprehensive approach is needed to further improve the quality of colonoscopies in Korea. The first step is to refine the reporting system. According to a study conducted in Ontario, Canada, a considerable proportion of the colonoscopy reports submitted by the endoscopists in the field were inappropriate in quality [30]. Feedback is another important factor associated with quality improvement [31]. Providing appropriate feedback rather than auditing alone contributes to quality improvement, and providing incentives further increases effectiveness [31]. In addition, because it is not realistic to field investigate all institutions, an electronic database of colonoscopy quality indicators needs to be established. Pathological results after polypectomies should be collected to automatically calculate ADR and provide periodic feedback. Above all, to create a virtuous circle for quality improvement, it is important to encourage endoscopists to participate in the process of reporting, auditing, and providing feedback. To do so, the reporting system should be easy to implement, and appropriate feedback and incentives need to be provided.

This study has some limitations. Because colonoscopy data were retrospectively collected, we were not able to identify the indications for colonoscopy. Therefore, this study included colonoscopies of various indications besides screening colonoscopies. It may be inappropriate to directly apply our results to quality indicators of screening colonoscopies. Second, we measured withdrawal time as cecal intubation time minus finish time minus time spent on biopsy or polypectomy, which was an arbitrary measurement. In fact, withdrawal time ≥ 6 minutes is a meaningful indicator in a negative study. Third, we were not able to investigate individual endoscopist ADR, which is an important indicator for endoscopist performance. The retrospective nature of the study limits the data collection; many colonoscopy pathologic reports were not available and a follow-up colonoscopy was not performed in all cases. Therefore, a complete assessment of adenoma detection could not be achieved. Fourth, bowel preparation was evaluated by the investigators, not by the operators. We used BBPS as a measure of bowel preparation, which relies on the degree of bowel visualization after sufficient washing and aspiration. Our method was limited in assessing bowel preparation accurately, because it was not possible to confirm that the pictures that the investigators used to evaluate bowel visualization were taken after sufficient washing and aspiration. Finally, we could not measure the level of experience of the endoscopist, nor the capacity and colonoscopy volume of each endoscopy unit. Future studies regarding colonoscopy quality indicators in non-academic centers including detailed information about endoscopists and endoscopy units are needed.

In conclusion, our results showed that the quality of colonoscopies performed in community hospitals and nonhospital facilities was suboptimal. Systematic reporting, auditing, and feedback are needed to establish a virtuous circle for colonoscopy quality improvement.