Factors influencing the miss rate of polyps in a back-to-back colonoscopy study

• Introduction
• Patients and methods
• Statistical analysis
• Results
• Discussion
• References

Background and study aims: In patients undergoing colonoscopy, 22 % – 28 % of polyps and 20 % – 24 % of adenomas are missed. It is unclear which factors contribute to polyp miss rates, but colorectal cancer detected within 3 years after colonoscopy may originate from missed lesions. The aim of the current study was to determine patient- and polyp-related factors that influence the miss rates of polyps and adenomas during colonoscopy.

Patients and methods: Data from 406 patients were obtained from a multicenter, randomized back-to-back colonoscopy study investigating the Third Eye Retroscope (TER) in improving polyp detection rate by visualizing hidden areas such as folds and curves. Patients were randomized to undergo standard colonoscopy followed by colonoscopy with TER, or vice versa. Miss rates were calculated for all polyps and adenomas. All lesions were categorized for size and location within the colon/rectum. Odds ratios (ORs) were computed using adjusted logistic regression models to identify factors independently associated with missed lesions.

Results: The miss rate was 25 % (150 /611) for all polyps and 26 % (90 /350) for adenomas. Miss rates were significantly lower (21 % vs. 29 %) in patients randomized to TER as the first procedure (P < 0.03). Taking all groups together, > 2 polyps compared with ≤ 2 polyps detected during the first colonoscopy increased the risk of missing additional polyps (adjusted OR = 2.83; 95 % confidence interval [CI] 1.22 – 6.70). Adenomas in the left colon compared with adenomas in the right colon were also more frequently missed (adjusted OR = 1.65; 95 %CI 1.06 – 2.58).

Conclusions: A quarter of polyps were missed during colonoscopy. Physicians should be aware that the risk of missing a polyp is related to patient factors (presence of > 2 polyps) and polyp factors (left colon location).

Introduction

Colorectal cancer (CRC) is the fourth most prevalent cancer in men and the third most prevalent in women [1]. Worldwide it accounts for about one million new cases and over half a million deaths per year [1]. Colonoscopy is regarded as the gold standard for the detection of cancers and precancerous polyps in the colorectum [2] [3] [4] [5]. Previous research has indicated that polypectomy performed during colonoscopy results in a 76 % – 90 % reduced risk of developing CRC [6] [7].

Several studies have reported that a significant number of polyps are missed during routine colonoscopy [6] [7] [8], with interval CRCs being detected after recent colonoscopy most likely originating from missed lesions [9]. A systematic review that included six tandem colonoscopy studies with a total of 465 patients reported a pooled miss rate of 22 % for all polyps and 26 % for polyps smaller than 5 mm in size [10]. In this review, no risk factors associated with missing polyps were reported. This was mainly due to the fact that several factors, such as patient-related factors, polyp location, and adequacy of bowel preparation, were often not systematically registered.

A recent prospective multicenter study [11] that included 294 patients in 11 centers reported a miss rate of 28 % for polyps and 20 % for adenomas of all sizes. Moreover, 9 % of adenomas ≥ 5 mm and 11 % of advanced adenomas were reported to have been missed. The authors found that polyp diameter and detecting three or more polyps were significantly associated with a reduced polyp miss rate, whereas sessile or flat polyps and polyps in the left colon were associated with an increased polyp miss rate. No association between miss rates and adequacy of bowel cleansing or withdrawal time was found; the latter also included the time needed to perform polypectomy.

Until now, only a few studies have investigated risk factors for missing polyps during colonoscopy and in these studies only small numbers of patients were included, the studies were heterogeneous in study design, and/or were limited in their ability to determine which factors influenced the risk of missing a polyp. In order to investigate patient- and polyp-related factors that influence miss rates during colonoscopy, the database of the Third Eye Retroscope Randomized Clinical Evaluation (TERRACE) study was used; TERRACE examined the clinical value of the Third Eye Retroscope (TER) using back-to-back colonoscopy.

Patients and methods

The database of the TERRACE study, a prospective study comparing the diagnostic yield of the TER plus standard colonoscopy with standard colonoscopy alone during same-day, back-to-back colonoscopies (ClinicalTrials.gov, identifier NCT01044732) [12], was scrutinized for the purpose of identifying risk factors for missed lesions. TER is a retrograde imaging device that was designed to improve visualization of “hidden areas” during colonoscopy, such as the proximal side of haustral folds and behind curves, and which complements the antegrade view of the colonoscope [5].

Patients in the TERRACE study were 18 years or older and were scheduled for colonoscopy for CRC screening, surveillance after previous polypectomy or for diagnostic work-up. Patients with inflammatory bowel disease, history of polyposis syndrome or colonic resection, suspected stricture potentially precluding complete colonoscopy, diverticulitis, toxic megacolon or a history of radiation therapy to the abdomen or pelvis were excluded. All patients who underwent both colonoscopies back-to-back were included in the analyses, regardless of the quality of bowel preparation. The protocol was approved by the ethical committees/institutional review boards of all nine participating hospitals, and all patients signed an informed consent form before enrolment.

Patients were randomized into two groups at the time of informed consent using a web-based randomization module stratified by center and by individual endoscopist. Patients in one group first underwent standard colonoscopy followed immediately by repeat colonoscopy with the TER. Patients in the other group underwent colonoscopy with the TER first, which was followed immediately by standard colonoscopy. Both procedures were performed by the same endoscopist. All procedures were performed by endoscopists with a long experience in performing colonoscopy.

During colonoscopies, all polyps were immediately removed after detection during intubation or withdrawal, except in cases of numerous small hyperplastic polyps in the rectum. Bowel preparation was recorded using the Ottawa bowel preparation quality score [13] [14]. Patients who did not undergo a second colonoscopy were not included in the analyses.

Withdrawal time was defined as the time of initiation of cecal inspection to the time when the colonoscope was withdrawn from the anus minus the time that was needed to perform polypectomy [15]. Polyp size was determined by comparison with an open biopsy forceps. Adenomas were subdivided depending on their histology (tubular, villous, tubulovillous or serrated), presence of dysplasia (none, low grade or high grade), size ( ≤ 5 mm, 6 – 9 mm, ≥ 10 mm), morphology (flat, flat-elevated, sessile or pedunculated), and location in the colon (right colon: cecum, ascending colon, hepatic flexure, transverse colon, and splenic flexure; or left colon: descending colon, sigmoid, and rectum).

A polyp was determined to be missed when it was detected only during the second colonoscopy. Similarly, in the per patient analyses, a patient was determined to have one or more missed polyps when these were detected during the second procedure and were not seen during the first colonoscopy. If no lesions were found during either colonoscopy, a patient was classified as being “without missed lesions.” All patients were contacted by telephone 24 – 72 hours after the investigation for evaluation of the procedure and to assess whether post-procedural complications had occurred.

Statistical analysis

Baseline characteristics were presented according to detection status using means with standard deviations, medians with ranges, or frequencies with percentages, where appropriate. Miss rates were calculated for all polyps and adenomas. P values were determined by chi-squared or Fisher’s exact testing for differences between groups, where appropriate.

Odds ratios (ORs) with 95 % confidence intervals (CIs) were computed using logistic regression models. Per-patient and per-polyp based univariate and multivariate analyses were performed. The following variables were considered for the per-patient based analyses: randomization group, sex, age, indication for colonoscopy, total number of polyps found during the first endoscopy, withdrawal time of the first procedure, start time of the first endoscopy (morning vs. afternoon), adverse events, pain during and after colonoscopy, and the Ottawa bowel preparation score. For the per-polyp based analyses histology, adenoma size, morphology, and location were considered.

All statistical analyses were performed using the statistical analyses system (SAS) software package, version 9.2 (SAS institute, Cary, North Carolina, USA). Two-sided P values of < 0.05 were considered to be statistically significant.

Results

In total, 448 patients were included between March 2009 and January 2010 in four European and five US centers. The cecum was reached in 98 % of patients. Only patients who did not undergo two complete colonoscopies were excluded from the database; however all others were included in the analyses (n = 406). Baseline characteristics of patients are shown in [Table 1]. Characteristics for polyps are shown in [Table 2]. A total of 611 polyps were detected, with 461 polyps (75 %) detected during the first procedure and 150 (25 %) during the second procedure. No CRCs were found.

Polyp miss rates, overall and separately for both randomization groups (colonoscopy followed by colonoscopy + TER, or vice versa) are shown in  [Table 3]. The polyp miss rate for all polyps together was 25 % and the rate for all adenomas was 26 %. Miss rates for polyps at the hepatic and splenic flexure, and in the sigmoid were relatively high (36 %, 67 %, and 33 %, respectively), compared with other locations in the colon. In the group that first underwent standard colonoscopy followed by colonoscopy + TER the total number of missed polyps was significantly higher compared with the group that first underwent colonoscopy + TER (P < 0.03). This was due to polyps with a size of 6 – 9 mm being found during the second procedure.

Patient factors associated with missed lesions are shown in [Table 1]. In patients with more than two polyps detected during the first endoscopy, the risk of missing an additional polyp was significantly increased (adjusted OR = 2.83; 95 %CI 1.22 – 6.70). Withdrawal time during the first endoscopy (OR = 0.91, 95 %CI 0.30 – 3.16 comparing withdrawal time of > 6 minutes with ≤ 6 minutes) and start time of the first endoscopy (OR = 1.06, 95 %CI 0.45 – 2.44 comparing colonoscopies after 1:00 p.m. vs. before 1:00 p.m.) had no effect on the risk of missing a polyp. A higher Ottawa bowel score (poorer bowel preparation) increased the risk of missing a polyp; however, this was not statistically significant after adjustment (adjusted OR = 1.94; 95 %CI 0.90 – 4.22).

Polyp factors associated with missed lesions are shown in [Table 2]. The risk of missing adenomas in the left colon was significantly increased compared with missing adenomas in the right colon (OR 1.65; 95 %CI 1.06 – 2.58). The risk of missing adenomas or hyperplastic polyps was not different. The risk of missing adenomas ≥ 10 mm in size was nonsignificantly lower compared with the risk of missing adenomas ≤ 5 mm (adjusted OR = 0.41; 95 %CI 0.06 – 1.54). The risk of missing flat lesions compared with sessile polyps was nonsignificantly increased (adjusted OR = 2.28; 95 %CI 0.43 – 11.18).

Discussion

In this prospective, multicenter back-to-back colonoscopy study investigating the clinical value of the TER in improving detection rates of lesions in the colon, the miss rate for all polyps was 25 % and the rate for adenomas was 26 %. It was found that in patients with more than two polyps detected during the first colonoscopy, the risk of missing an additional polyp was significantly increased, and that adenomas in the left colon were also more likely to be missed compared with those in the right colon.

The overall polyp and adenoma miss rates found in the study were comparable to previously published results from back-to-back colonoscopy studies (i. e. 22 % – 28 % for all polyps and 20 % – 24 % for adenomas of all sizes [4] [10] [11]). The finding in the current study that patients with more than two polyps during the first colonoscopy were more likely to have a polyp detected during the second procedure is supported by findings from Rex et al. [4], who reported a three-fold higher risk of detecting additional polyps after initially finding two or more adenomas during the first colonoscopy. In addition, Bensen et al. [16] reported that the number of polyps detected during the first procedure was a predictor of detecting one or more additional polyps during a second procedure. This is probably explained by a reduced attention of an endoscopist during the procedure after having already detected and removed polyps from the colon/rectum. Moreover, the presence of blood on the colonic mucosa as a consequence of an earlier polypectomy is another explanation that could reduce the ability to detect other polyps. Finally, as polypectomy can be time-consuming, it may be that there is time pressure on endoscopists due to a (long) endoscopy list for that day and this could be a factor contributing to the miss rate. Most of these factors are difficult to measure. Based on the current findings, we agree with previous suggestions that the reported increased adenoma recurrence rate in patients with multiple polyps may at least be partially related to missed polyps during previous colonoscopies [16].

In the current study, adenomas in the left colon were more likely to be missed than adenomas in the right colon. This is important, as a significant proportion of advanced pathologic characteristics have been reported in left-sided adenomas compared with right-sided adenomas (17 % vs. 8.9 %) [17] [18]. The current findings are in line with those from Heresbach et al. [11]. In contrast, Rex et al. [4] previously reported a nonsignificantly increased miss rate of right-sided adenomas. We speculate that the frequently cited publication by Rex et al. [4] has made endoscopists, including those in the study by Heresbach et al. [11] and our study, more alert to the possibility of missed polyps in the right colon. Another explanation for our finding could be that we included the splenic flexure as part of the left colon. Both the splenic flexure and the sigmoid are known to be difficult areas to completely visualize endoscopically compared with the right colon. Nonetheless, the hepatic flexure and to a lesser degree the cecum may also be challenging to fully inspect during colonoscopy. Contrary to the current findings are recent findings by Singh et al. [19] who reported a reduction in mortality from distal CRC after previous colonoscopy and only a nonsignificant mortality reduction for proximal colon cancer. This finding and those of Rex et al. [4] can be explained by a reported increased prevalence of nonpolypoid lesions (measuring less than 2.5 mm in height) in the proximal colon [20], and therefore these right-sided lesions might also not have been detected during the second colonoscopy. In the TERRACE database that we used for the current study, however, 94 % of all lesions in the proximal colon were of flat, flat elevated or sessile morphology compared with 90 % in the distal colon. In the studies by Rex [4] and Singh [19], information on the presence of nonpolypiod lesions was not reported.

Barclay et al. [21] recently reported a significantly increased detection rate of polyps when the mean withdrawal time of the colonoscope was 6 minutes or more. This was however disputed by Heresbach et al. [11], who reported that the miss rate of polyps > 5 mm and adenomas of any size was not affected by a longer withdrawal time. Similarly, no difference in miss rate of polyps was found in the current study when comparing procedures with a withdrawal time longer or shorter than 6 minutes. It is important to emphasize however that the number of patients with a withdrawal time shorter than 6 minutes was small in the current study (19.8 % of all colonoscopies). In addition, Chan et al. [22] recently reported an increased miss rate of polyps when procedures were performed after 1:00 p.m. compared with colonoscopies before 1:00 p.m. It is not possible to confirm these findings in the current study.

The miss rate of polyps in patients with a relatively poor bowel preparation was not different from those with good bowel preparation. This is in line with results from Barclay et al. [21] and Heresbach et al. [11], but contrary to those of Harewood et al. [23] and Froehlich et al. [24]. The main reason for our findings is probably that patients with inadequate bowel preparation (Ottawa bowel score of > 6) did not undergo a same-day second procedure and instead were scheduled for a second procedure after more thorough preparation.

The current study has several strengths, but also some limitations. The strengths include that this is the largest, prospective, multicenter study to date in which polyp and adenoma miss rates have been studied in a same-day back-to-back colonoscopy design. Second, by having the same endoscopist performing both colonoscopies, additional confounding variables that could result from differences in skill, experience, and technique between two endoscopists were eliminated. However, the same operator will likely use the same technique with the same mistakes or perhaps pays less attention to the presence of polyps either the first or the second time. Third, all endoscopists were experienced and the overall cecal intubation rate was 98 %.

A limitation of the study is that it was originally designed to compare polyp detection rates between standard colonoscopy and colonoscopy with the TER. The variable of randomization of the order of colonoscopies might have changed patient-based results to some extent. Second, back-to-back colonoscopies are known to be not 100 % accurate to estimate miss rates, as polyps can be missed during the second colonoscopy as well, despite the fact that the colon had already been cleaned during the first colonoscopy. In particular, serrated lesions could have been missed in both arms; however, this is true for all colonoscopies and should therefore be considered to be a constant factor. Third, it is not known whether missed lesions after the first colonoscopy were really precancerous lesions and indeed would have developed into CRC. Therefore the clinical implications of the current findings remain to be established.

In conclusion, patients with more than two polyps found during colonoscopy have an increased risk of an additional polyp being missed. In addition, adenomas in the left colon were also more frequently missed than adenomas in the right colon. Endoscopists should pay particular attention to the detection of polyps when polyps have already been detected during the colonoscopy and when inspecting the left colon.

Competing interests: None

Acknowledgments

We thank the TERRACE Study Group for their contribution to recruitment and endoscopy procedures. The TERRACE Study Group included: Daniel C. DeMarco, Elizabeth Odstrcil, and Bradley Creel (Baylor University Medical Center, Dallas, Texas, USA); Amit Rastogi and Vikas Singh (Kansas City Veterans Administration Medical Center, Kansas City, Missouri, USA); Paul A. Akerman (Bayside Endoscopy Center, Providence, Rhode Island, USA); Kassem Azzouzi, Olivier Dewit, and Pierre H. Deprez (Cliniques Universitaires Saint-Luc, Université Catholique de Louvain, Brussels, Belgium); Richard I. Rothstein (Dartmouth-Hitchcock Medical Center, Lebanon, New Hampshire, USA); Alessandro Repici and Giacomo Rando (Istituto Clinico Humanitas, Milan, Italy); Patrick I. Okolo, Anne Marie Lennon, and Anthony N. Kalloo (Johns Hopkins Hospital, Baltimore, Maryland, USA); Ana Ignjatovic, James East, and Brian P. Saunders (St. Mark’s Hospital, London, UK).

^* for the TERRACE Study Group

• References

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Corresponding author

• References

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  Search in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
• 10 van Rijn JC, Reitsma JB, Stoker J et al. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am J Gastroenterol 2006; 101: 343-350
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• 11 Heresbach D, Barrioz T, Lapalus MG et al. Miss rate for colorectal neoplastic polyps: a prospective multicenter study of back-to-back video colonoscopies. Endoscopy 2008; 40: 284-290
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  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  Thieme ConnectPubMedSearch in Google Scholar
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