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Journal of Digestive Cancer Research 2024; 12(3): 160-170

Published online December 20, 2024

https://doi.org/10.52927/jdcr.2024.12.3.160

© Korean Society of Gastrointestinal Cancer Research

Post-colonoscopy Colorectal Cancer: Causes and Prevention


Jong Yoon Lee


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Department of Internal Medicine, Dong-A University College of Medicine, Busan, Korea

Correspondence to :
Jong Yoon Lee
E-mail: ljyhateo@gmail.com
https://orcid.org/0000-0002-6542-8062

Received: November 18, 2024; Revised: December 9, 2024; Accepted: December 9, 2024

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0). which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

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Post-colonoscopy colorectal cancer (PCCRC), classified as colorectal cancer (CRC) diagnosed following a negative colonoscopy and prior to the recommended follow-up; despite advancements in the quality of colonoscopy, remains a significant concern. PCCRC accounts for 1.8 to 9.0% of CRC cases globally and 6.2% CRC cases in Korea. The predominant reasons for the incidence of PCCRC include procedural factors such as missed lesions and incomplete resections, and newly developed lesions. Few strategies that can mitigate PCCRC include improving adenoma detection rates to at least 25 to 35%, ensuring withdrawal times of ≥ 8 minutes, adequate bowel preparation, and cecal intubation rates exceeding 90 to 95%. For preventing PCCRC, advanced imaging technologies and enhanced polypectomy techniques, such as en bloc resection for larger or potentially malignant polyps are critical. This review highlights the multifactorial nature of PCCRC and the significance of quality assurance in colonoscopy for reducing its prevalence.

KeywordsColonoscopy Colorectal neoplasms Colonic polyp

INTRODUCTION

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Colorectal cancer (CRC) is one of the most commonly occurring cancers worldwide and a leading cause of cancer-related deaths [1]. This trend is also reflected in South Korea, where it remains a major health concern [2]. The effectiveness of colonoscopy as a preventive measure against CRC has been well established. Colonoscopy allows for the identification and removal of adenomas before they undergo malignant transformation, thereby significantly reducing the incidence of CRC [3-7]. According to the National Polyp Study, the first research on the preventive effects of colonoscopy for CRC, the incidence of CRC decreased by 90%, 88%, and 76% in three cohorts from the Mayo Clinic in the United States, St. Mark’s in the United Kingdom, and the National Cancer Institute in the United States, respectively, following the removal of polyps [3]. Subsequent studies have also confirmed a reduction in mortality rates by 53 to 67% [4-7]. Due to its effectiveness, colonoscopy has become the standard screening method for the diagnosis and prevention of CRC [8,9]. However, reports have emerged of what is known as post-colonoscopy colorectal cancer (PCCRC), referring to cases of CRC that develop within a short period after a colonoscopy did not find the cancer. This review aims to explore the causes and risk factors of PCCRC and to summarize preventive measures through a literature review.

MAIN SUBJECTS

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Definition of post-colonoscopy colorectal cancer

In 1997, Haseman et al. [10] reported 47 cases of CRC diagnosed within 3 years of a previous colonoscopy that had failed to detect the cancer, out of a total of 941 cases identified across 20 hospitals from 1988 to 1993. In follow-up studies on CRC initially undetected by a previous colonoscopy but later identified in subsequent colonoscopies, the interval between colonoscopy and cancer diagnosis has varied widely across studies, ranging from 36 to 120 months [11-24]. The terms “PCCRC” and “missed cancer” have been used interchangeably with “interval cancer.” In 2018, the World Endoscopy Organization (WEO) recommended the term “PCCRC” for cancers detected after a colonoscopy that failed to identify them, in order to establish clearer terminology. Additionally, the WEO proposed subdividing PCCRC into categories: cancers diagnosed before the recommended interval for the next colonoscopy are termed “interval cancers,” while those diagnosed after the recommended interval are referred to as “non-interval cancers” [25]. According to the WEO, PCCRC is defined as cancer detected within the recommended follow-up interval after a colonoscopy, although this interval may vary depending on different guidelines. The Korean guidelines recommend a 3-year surveillance interval for high-risk groups, which include cases with five or more adenomas, adenomas larger than 10 mm, villous adenomas, high-grade adenomas, or serrated polyps larger than 10 mm. For individuals with 3 to 4 tubular adenomas or serrated polyps under 10 mm, the recommended interval is between 3 to 5 years, while a 5-year interval is advised for those with normal findings or low-risk adenomas [26].

The incidence of PCCRC is reported to be approximately 1.8 to 9.0% of all CRC cases, depending on the study [11-24]. In a Korean study analyzing data from 482 CRC patients, PCCRC was found in 30 patients, accounting for 6.2% of cases [22]. Most studies indicate that PCCRC occurs more frequently in the right colon, with over half of the cases appearing there rather than in the left colon. A meta-analysis defining PCCRC within a 36-month colonoscopy found that PCCRC occurred 2.4 times more often in the right colon than in the left [27].

Causes of post-colonoscopy colorectal cancer

Identifying the causes of PCCRC is very challenging. It is difficult to accurately measure the growth rate of cancer, to determine whether lesions that could have been detected in a completed colonoscopy were missed, and to confirm that polypectomy procedures fully removed all residual lesions. However, several studies have proposed the following three hypotheses as primary explanations for the occurrence of PCCRC.

Missed lesions

Studies have evaluated the adenoma miss rate (AMR) by considering cases in which adenomas, initially undetected, are identified during an immediate repeat colonoscopy. First reported by Rex et al. [28] in 1997, this approach, known as tandem colonoscopy, involves performing two consecutive colonoscopies on the same day to measure the rate of adenomas missed in the first examination. The AMR was found to be 24% in these studies. In subsequent studies evaluating AMR, the most recent meta-analysis found an overall AMR of approximately 26%, with an advanced AMR of 9% for adenomas larger than 10 mm, high-grade adenomas, and villous adenomas [29]. Factors identified as contributing to missed adenomas included a flat adenoma shape, inadequate bowel preparation, small adenoma size, withdrawal times of less than six minutes, procedures conducted by less experienced endoscopists, and adenomas located in the right colon [30,31]. In studies analyzing the causes of PCCRC, cases with a short diagnosis interval of within three years post-colonoscopy, smaller or early-stage cancers, or a history of endoscopic resection of advanced adenomas, where the location of the resected adenoma differs from the location of the diagnosed cancer, are considered likely to result from missed lesions. Based on these analyses, missed lesions are estimated to account for more than half of the causes of PCCRC [19,32].

Incomplete resection

Incomplete resection of adenomas is another cause of PCCRC. According to the Complete Adenoma Resection (CARE) study published in 2013, approximately 10.1% of polyps showed incomplete resection at the resection margin after polypectomy using electrocautery [33]. The European Society of Gastrointestinal Endoscopy (ESGE) guidelines published in 2017 recommended cold snare polypectomy (CSP) for polyps smaller than 10 mm [34] and subsequent studies have investigated the impact of this method on incomplete resection rates. In a study by Matsuura et al. [35], the incomplete resection rate for polyps ≤ 9 mm treated with CSP was 3.9%. A prospective randomized trial comparing complete resection rates between CSP and hot snare polypectomy (HSP) for polyps 6 to 10 mm in size found no statistically significant difference (CSP: 92.8%, HSP: 96.3%, p = 0.50 [36]. For polyps ≤ 10 mm, incomplete resection rates for both CSP and HSP were reported to be under 10%. However, for larger polyps, only HSP is performed, and the CARE study reported an incomplete resection rate of 23.3% for polyps sized 15 to 20 mm, indicating a significant increase in incomplete resection with larger polyps [33]. Additionally, flat morphology, sessile serrated lesions, and piecemeal resection were identified as factors associated with incomplete resection. Although it is difficult to precisely measure the contribution of incomplete resection to PCCRC, studies analyzing PCCRC cases have suggested that when high-risk adenomas such as those ≥ 10 mm, villous adenomas, or high-grade adenomas were resected at prior colonoscopies and PCCRC occurred at the same site, incomplete resection was likely the cause. Based on these analyses, PCCRCs attributed to incomplete resection are estimated to account for approximately 20% of cases [19,32].

New lesions

The natural progression of adenomas to cancer has been reported to take 7.6 to 24.2 years, and it takes 10.6 to 25.8 years for cancer to develop with symptoms [37]. Another study reported that the annual progression rate of advanced adenomas to cancer ranges from 2.6% to 5.6%, while the lifetime cumulative risk of non-advanced adenomas progressing to cancer is 30%, though it is only 2% between the ages of 75 and 80 [38]. These wide-ranging estimates of adenoma progression and age-dependent growth rates suggest the possibility of rapidly growing tumors leading to PCCRC. This difference in growth rates may also be closely related to the carcinogenic pathways of CRC. Known pathways include chromosomal instability (CIN), microsatellite instability (MSI), and the CpG island methylator phenotype (CIMP). CIN, which accounts for 60 to 70% of CRC, primarily contributes to left-sided CRCs, while MSI and CIMP are more associated with right-sided CRCs [39-41]. In PCCRCs, MSI was observed in 30.4% of cases compared to 10.3% in non-PCCRCs, and another study reported similar results (29% vs. 11%) [42], and another study reported similar results (29% vs. 11%) [11]. Similarly, CIMP was significantly higher in PCCRCs (57%) than in non-PCCRCs (33%), while BRAF mutations were more frequent in PCCRCs (28%) than non-PCCRCs (19%). However, KRAS mutations were significantly less common in PCCRCs (12.9%) compared to non-PCCRCs (28.9%) [11,43,44]. CRC does not follow a single carcinogenic pathway, with different pathways being predominant depending on the tumor location. Furthermore, PCCRCs and non-PCCRCs may differ in their carcinogenic pathways. These molecular differences suggest that rapidly growing tumors may contribute to the development of PCCRCs [11,45]. However, these pathways are also associated with serrated lesions that are flat and translucent, making them difficult to detect, suggesting that the characteristics of overlooked polyps rather than rapid growth rates may explain their progression to PCCRC [46,47]. Studies analyzing the causes of PCCRC have suggested that when the interval between the previous colonoscopy and diagnosis approaches the recommended maximum duration of 3 to 4 years or more, and the patient has a history of resected advanced adenomas, cancers diagnosed at a location different from the site of the previously resected adenomas are likely due to new lesions. Based on these analyses, approximately 20% of PCCRCs are estimated to arise from new lesions [19,32].

Prevention of post-colonoscopy colorectal cancer

Missed lesions and incomplete resections, which are among the causes of PCCRCs, are factors related to the colonoscopist performing the procedure. While it may not be possible to prevent all PCCRCs, a significant proportion caused by procedural factors can be prevented through high-quality examinations and complete polyp resection. Strategies to reduce the incidence of PCCRCs can be categorized into the following three approaches.

Improving the quality of colonoscopy

High-quality colonoscopy must meet certain quality indicators. These indicators include bowel preparation, cecal intubation rate, adenoma detection rate (ADR), and withdrawal time. The guidelines provided by the American Society of Gastrointestinal Endoscopy (ASGE) and the American College of Gastroenterology (ACG), along with those jointly published by the U.S. Multi-Society Task Force (which includes the American Gastroenterological Association), as well as the guidelines from the ESGE, will be reviewed to examine these indicators in detail.

Bowel preparation scores are measured using methods such as the Boston Bowel Preparation Scale (BBPS), Ottawa Scale, and Aronchick Scale. Adequate bowel preparation is defined as a BBPS score of ≥ 6 (range: 0–9), an Ottawa Scale score of ≤ 7 (range: 0–14), or an Aronchick Scale rating of “Fair” or better (Excellent, Good, Fair, Poor). Inadequate bowel preparation decreases ADR while increasing AMR, contributing to the occurrence of PCCRCs [48-50]. To improve bowel preparation, split-dose regimens are recommended [51-54], and educating patients on proper intake methods can enhance preparation quality [55,56]. Special attention should be given to individuals at risk of inadequate bowel preparation, such as the elderly, patients with diabetes or cerebrovascular disease, and hospitalized individuals [57,58]. Both the U.S. Multi-Society Task Force guidelines and the ESGE recommend maintaining adequate bowel preparation in at least 90% of all procedures [59,60]

Cecal intubation serves as an indicator not only for observing the right colon but also as a measure of the endoscopist’s technical ability to achieve complete insertion. Failure to intubate the cecum indicates an incomplete examination of the entire colon, increasing the likelihood of missed lesions and thus correlating with PCCRC risk. According to Baxter et al. [17], when the odds ratio (OR) for PCCRC incidence was set to 1 for endoscopists with a cecal intubation rate below 80%, those with an intubation rate of 90 to 94% had a reduced OR of 0.66 for proximal PCCRC and 0.71 for distal PCCRC. Endoscopists achieving a cecal intubation rate of 95% or higher demonstrated an OR of 0.72 for proximal PCCRC and 0.73 for distal PCCRC, signifying that increased cecal intubation rates significantly reduce the risk of PCCRC in both proximal and distal regions of the colon (p = 0.03). The ESGE recommends achieving a cecal intubation rate of at least 90%, while the U.S. Multi-Society Task Force advises a target of 95% or higher [59,61].

The ADR is a critical quality indicator associated with PCCRC. When comparing the PCCRC incidence based on varying ADRs, studies have shown a significant increase in PCCRC rates among endoscopists with lower ADRs. In a study that used an ADR of 20% or higher as a reference (hazard ratio [HR] of 1), the PCCRC HRs were 10.94 (confidence interval [CI]: 1.37–87.01) for an ADR of 15.0–19.9%, 10.75 (CI: 1.36–85.06) for 11 to 14.9%, and 12.50 (CI: 1.51–103.43) for ADRs below 11% [62]. Another study divided ADRs into quintiles and set the lowest quintile (≤ 19.05%) as the reference HR (HR = 1). As ADR increased, the PCCRC HR decreased substantially, with the highest quintile (≥ 33.51%) showing a HR of 0.52 (CI: 0.39–0.69), indicating a strong inverse relationship between ADR and PCCRC risk [16]. Additionally, a high ADR correlates with improved detection rates of serrated lesions, which often present on the right side of the colon and are challenging to detect [63]. The ESGE recommends maintaining an ADR of at least 25% during screening colonoscopies [59]. However, the most recent update from the U.S. Multi-Society Task Force recommends achieving an ADR of at least 35% for colonoscopies performed in individuals aged 45 and older [60].

The time taken to withdraw the colonoscope from the cecum to the anus is measured to assess the total observation time during a colonoscopy. In a study by Barclay et al. [64], analyzing 2,053 screening colonoscopies performed by 12 endoscopists, the ADR was significantly higher among endoscopists with an average withdrawal time of 6 minutes or more (28.3%) compared to those with a withdrawal time of less than 6 minutes (11.8%, p = 0.01). Additionally, Shaukat et al. [65] reported that colonoscopies with a withdrawal time of less than 6 minutes were associated with a 2.3-fold higher incidence of PCCRC compared to those with a withdrawal time of 6 minutes or more. Past guidelines from both the U.S. and Europe recommended a withdrawal time of at least 6 minutes [59,61]. However, recent studies have suggested that the optimal withdrawal time may be 8 to 9 minutes [66-68]. Reflecting these findings, the most recent update from the U.S. Multi-Society Task Force now recommends a withdrawal time of at least 8 minutes [60].

Appropriate polypectomy techniques

To prevent incomplete polyp resection, it is essential to select appropriate techniques and improve procedural skills. For non-pedunculated polyps measuring ≥ 20 mm, en bloc resection using endoscopic mucosal resection (EMR) is achieved in only 16 to 48%. Therefore, for large non-pedunculated lesions, endoscopic submucosal dissection (ESD) is recommended as a more suitable approach [69-72]. In cases where malignancy or submucosal invasion is suspected, achieving en bloc resection is crucial. For polyps larger than 10 mm, advanced imaging techniques, such as narrow-band imaging (NBI) or magnifying endoscopy, are recommended for evaluating submucosal invasion before resection [73,74]. This evaluation helps guide the selection of the appropriate resection technique based on the malignancy potential or submucosal invasion. Tools such as the NBI International Colorectal Endoscopic (NICE) and the Japan NBI Expert Team classification using NBI [75-78], as well as pit pattern classification via magnifying chromoendoscopy, as described by Kudo [79-82], can predict the pathology of deep submucosal invasion. For polyps suspected to be malignant, en bloc resection techniques should be employed; if this is not feasible, referral to a specialized center should be considered to ensure proper management.

Image-enhanced endoscopy and emerging technologies

Studies have been conducted to determine whether image-enhanced endoscopy (IEE) and emerging technologies contribute to improved ADRs or reduced AMRs. A representative IEE technique, NBI, uses optical filters to project selected narrow wavelength bands (415 ± 30 nm and 540 ± 30 nm), enabling detailed visualization of surface microstructures and mucosal patterns [83]. Early studies on NBI reported no significant benefit in ADR or AMRs compared to conventional methods [84,85]. However, nearly two decades after its introduction in 2004, recent meta-analyses of accumulated studies have demonstrated a statistically significant improvement in ADR with NBI compared to white light imaging (WLI) (WLI-ADR: 42.3%, NBI-ADR: 45.2%, p = 0.04) [86]. Additionally, studies have investigated novel technologies designed to enhance observation, such as Third Eye, FUSE, EndoRings, and EndoCuff, and have reported their potential to improve ADR [87-90]. Studies utilizing artificial intelligence (AI) have reported that AI-assisted colonoscopy can improve ADRs while simultaneously reducing AMRs [91-93]. These emerging technologies are expected to reduce the incidence of PCCRC through indirect evidence, such as improved ADR and reduced AMR. However, direct evidence demonstrating a decrease in PCCRC incidence is currently lacking, necessitating further research in this area.

CONCLUSION

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PCCRC is defined as CRC not detected during a colonoscopy but diagnosed before the next recommended surveillance. PCCRC accounts for 1.8 to 9.0% of all CRCs globally and 6.2% in Korea. It is more commonly detected in the right colon than in the left and is associated with molecular pathways such as MSI, CIMP, and BRAF mutations. While a significant proportion of PCCRC cases result from procedural factors, such as missed lesions or incomplete resections, new lesions also contribute to its occurrence. Since procedural factors are preventable through high-quality colonoscopy practices, efforts to improve colonoscopy quality are essential. Key strategies include maintaining adequate bowel preparation, achieving a cecal intubation rate of 90 to 95% or higher, ensuring a withdrawal time of at least eight minutes for thorough observation, and achieving an ADR of at least 25 to 35%. Additionally, improving polypectomy techniques and utilizing advanced imaging technologies can aid in detecting and appropriately managing lesions with malignant potential or suspected submucosal invasion, with particular attention to achieving en bloc resection.

CONFLICTS OF INTEREST

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No potential conflict of interest relevant to this article was reported.

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Article

Review Article

Journal of Digestive Cancer Research 2024; 12(3): 160-170

Published online December 20, 2024 https://doi.org/10.52927/jdcr.2024.12.3.160

Copyright © Korean Society of Gastrointestinal Cancer Research.

Post-colonoscopy Colorectal Cancer: Causes and Prevention

Jong Yoon Lee

Department of Internal Medicine, Dong-A University College of Medicine, Busan, Korea

Correspondence to:Jong Yoon Lee
E-mail: ljyhateo@gmail.com
https://orcid.org/0000-0002-6542-8062

Received: November 18, 2024; Revised: December 9, 2024; Accepted: December 9, 2024

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0). which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Post-colonoscopy colorectal cancer (PCCRC), classified as colorectal cancer (CRC) diagnosed following a negative colonoscopy and prior to the recommended follow-up; despite advancements in the quality of colonoscopy, remains a significant concern. PCCRC accounts for 1.8 to 9.0% of CRC cases globally and 6.2% CRC cases in Korea. The predominant reasons for the incidence of PCCRC include procedural factors such as missed lesions and incomplete resections, and newly developed lesions. Few strategies that can mitigate PCCRC include improving adenoma detection rates to at least 25 to 35%, ensuring withdrawal times of ≥ 8 minutes, adequate bowel preparation, and cecal intubation rates exceeding 90 to 95%. For preventing PCCRC, advanced imaging technologies and enhanced polypectomy techniques, such as en bloc resection for larger or potentially malignant polyps are critical. This review highlights the multifactorial nature of PCCRC and the significance of quality assurance in colonoscopy for reducing its prevalence.

Keywords: Colonoscopy, Colorectal neoplasms, Colonic polyp

INTRODUCTION

Colorectal cancer (CRC) is one of the most commonly occurring cancers worldwide and a leading cause of cancer-related deaths [1]. This trend is also reflected in South Korea, where it remains a major health concern [2]. The effectiveness of colonoscopy as a preventive measure against CRC has been well established. Colonoscopy allows for the identification and removal of adenomas before they undergo malignant transformation, thereby significantly reducing the incidence of CRC [3-7]. According to the National Polyp Study, the first research on the preventive effects of colonoscopy for CRC, the incidence of CRC decreased by 90%, 88%, and 76% in three cohorts from the Mayo Clinic in the United States, St. Mark’s in the United Kingdom, and the National Cancer Institute in the United States, respectively, following the removal of polyps [3]. Subsequent studies have also confirmed a reduction in mortality rates by 53 to 67% [4-7]. Due to its effectiveness, colonoscopy has become the standard screening method for the diagnosis and prevention of CRC [8,9]. However, reports have emerged of what is known as post-colonoscopy colorectal cancer (PCCRC), referring to cases of CRC that develop within a short period after a colonoscopy did not find the cancer. This review aims to explore the causes and risk factors of PCCRC and to summarize preventive measures through a literature review.

MAIN SUBJECTS

Definition of post-colonoscopy colorectal cancer

In 1997, Haseman et al. [10] reported 47 cases of CRC diagnosed within 3 years of a previous colonoscopy that had failed to detect the cancer, out of a total of 941 cases identified across 20 hospitals from 1988 to 1993. In follow-up studies on CRC initially undetected by a previous colonoscopy but later identified in subsequent colonoscopies, the interval between colonoscopy and cancer diagnosis has varied widely across studies, ranging from 36 to 120 months [11-24]. The terms “PCCRC” and “missed cancer” have been used interchangeably with “interval cancer.” In 2018, the World Endoscopy Organization (WEO) recommended the term “PCCRC” for cancers detected after a colonoscopy that failed to identify them, in order to establish clearer terminology. Additionally, the WEO proposed subdividing PCCRC into categories: cancers diagnosed before the recommended interval for the next colonoscopy are termed “interval cancers,” while those diagnosed after the recommended interval are referred to as “non-interval cancers” [25]. According to the WEO, PCCRC is defined as cancer detected within the recommended follow-up interval after a colonoscopy, although this interval may vary depending on different guidelines. The Korean guidelines recommend a 3-year surveillance interval for high-risk groups, which include cases with five or more adenomas, adenomas larger than 10 mm, villous adenomas, high-grade adenomas, or serrated polyps larger than 10 mm. For individuals with 3 to 4 tubular adenomas or serrated polyps under 10 mm, the recommended interval is between 3 to 5 years, while a 5-year interval is advised for those with normal findings or low-risk adenomas [26].

The incidence of PCCRC is reported to be approximately 1.8 to 9.0% of all CRC cases, depending on the study [11-24]. In a Korean study analyzing data from 482 CRC patients, PCCRC was found in 30 patients, accounting for 6.2% of cases [22]. Most studies indicate that PCCRC occurs more frequently in the right colon, with over half of the cases appearing there rather than in the left colon. A meta-analysis defining PCCRC within a 36-month colonoscopy found that PCCRC occurred 2.4 times more often in the right colon than in the left [27].

Causes of post-colonoscopy colorectal cancer

Identifying the causes of PCCRC is very challenging. It is difficult to accurately measure the growth rate of cancer, to determine whether lesions that could have been detected in a completed colonoscopy were missed, and to confirm that polypectomy procedures fully removed all residual lesions. However, several studies have proposed the following three hypotheses as primary explanations for the occurrence of PCCRC.

Missed lesions

Studies have evaluated the adenoma miss rate (AMR) by considering cases in which adenomas, initially undetected, are identified during an immediate repeat colonoscopy. First reported by Rex et al. [28] in 1997, this approach, known as tandem colonoscopy, involves performing two consecutive colonoscopies on the same day to measure the rate of adenomas missed in the first examination. The AMR was found to be 24% in these studies. In subsequent studies evaluating AMR, the most recent meta-analysis found an overall AMR of approximately 26%, with an advanced AMR of 9% for adenomas larger than 10 mm, high-grade adenomas, and villous adenomas [29]. Factors identified as contributing to missed adenomas included a flat adenoma shape, inadequate bowel preparation, small adenoma size, withdrawal times of less than six minutes, procedures conducted by less experienced endoscopists, and adenomas located in the right colon [30,31]. In studies analyzing the causes of PCCRC, cases with a short diagnosis interval of within three years post-colonoscopy, smaller or early-stage cancers, or a history of endoscopic resection of advanced adenomas, where the location of the resected adenoma differs from the location of the diagnosed cancer, are considered likely to result from missed lesions. Based on these analyses, missed lesions are estimated to account for more than half of the causes of PCCRC [19,32].

Incomplete resection

Incomplete resection of adenomas is another cause of PCCRC. According to the Complete Adenoma Resection (CARE) study published in 2013, approximately 10.1% of polyps showed incomplete resection at the resection margin after polypectomy using electrocautery [33]. The European Society of Gastrointestinal Endoscopy (ESGE) guidelines published in 2017 recommended cold snare polypectomy (CSP) for polyps smaller than 10 mm [34] and subsequent studies have investigated the impact of this method on incomplete resection rates. In a study by Matsuura et al. [35], the incomplete resection rate for polyps ≤ 9 mm treated with CSP was 3.9%. A prospective randomized trial comparing complete resection rates between CSP and hot snare polypectomy (HSP) for polyps 6 to 10 mm in size found no statistically significant difference (CSP: 92.8%, HSP: 96.3%, p = 0.50 [36]. For polyps ≤ 10 mm, incomplete resection rates for both CSP and HSP were reported to be under 10%. However, for larger polyps, only HSP is performed, and the CARE study reported an incomplete resection rate of 23.3% for polyps sized 15 to 20 mm, indicating a significant increase in incomplete resection with larger polyps [33]. Additionally, flat morphology, sessile serrated lesions, and piecemeal resection were identified as factors associated with incomplete resection. Although it is difficult to precisely measure the contribution of incomplete resection to PCCRC, studies analyzing PCCRC cases have suggested that when high-risk adenomas such as those ≥ 10 mm, villous adenomas, or high-grade adenomas were resected at prior colonoscopies and PCCRC occurred at the same site, incomplete resection was likely the cause. Based on these analyses, PCCRCs attributed to incomplete resection are estimated to account for approximately 20% of cases [19,32].

New lesions

The natural progression of adenomas to cancer has been reported to take 7.6 to 24.2 years, and it takes 10.6 to 25.8 years for cancer to develop with symptoms [37]. Another study reported that the annual progression rate of advanced adenomas to cancer ranges from 2.6% to 5.6%, while the lifetime cumulative risk of non-advanced adenomas progressing to cancer is 30%, though it is only 2% between the ages of 75 and 80 [38]. These wide-ranging estimates of adenoma progression and age-dependent growth rates suggest the possibility of rapidly growing tumors leading to PCCRC. This difference in growth rates may also be closely related to the carcinogenic pathways of CRC. Known pathways include chromosomal instability (CIN), microsatellite instability (MSI), and the CpG island methylator phenotype (CIMP). CIN, which accounts for 60 to 70% of CRC, primarily contributes to left-sided CRCs, while MSI and CIMP are more associated with right-sided CRCs [39-41]. In PCCRCs, MSI was observed in 30.4% of cases compared to 10.3% in non-PCCRCs, and another study reported similar results (29% vs. 11%) [42], and another study reported similar results (29% vs. 11%) [11]. Similarly, CIMP was significantly higher in PCCRCs (57%) than in non-PCCRCs (33%), while BRAF mutations were more frequent in PCCRCs (28%) than non-PCCRCs (19%). However, KRAS mutations were significantly less common in PCCRCs (12.9%) compared to non-PCCRCs (28.9%) [11,43,44]. CRC does not follow a single carcinogenic pathway, with different pathways being predominant depending on the tumor location. Furthermore, PCCRCs and non-PCCRCs may differ in their carcinogenic pathways. These molecular differences suggest that rapidly growing tumors may contribute to the development of PCCRCs [11,45]. However, these pathways are also associated with serrated lesions that are flat and translucent, making them difficult to detect, suggesting that the characteristics of overlooked polyps rather than rapid growth rates may explain their progression to PCCRC [46,47]. Studies analyzing the causes of PCCRC have suggested that when the interval between the previous colonoscopy and diagnosis approaches the recommended maximum duration of 3 to 4 years or more, and the patient has a history of resected advanced adenomas, cancers diagnosed at a location different from the site of the previously resected adenomas are likely due to new lesions. Based on these analyses, approximately 20% of PCCRCs are estimated to arise from new lesions [19,32].

Prevention of post-colonoscopy colorectal cancer

Missed lesions and incomplete resections, which are among the causes of PCCRCs, are factors related to the colonoscopist performing the procedure. While it may not be possible to prevent all PCCRCs, a significant proportion caused by procedural factors can be prevented through high-quality examinations and complete polyp resection. Strategies to reduce the incidence of PCCRCs can be categorized into the following three approaches.

Improving the quality of colonoscopy

High-quality colonoscopy must meet certain quality indicators. These indicators include bowel preparation, cecal intubation rate, adenoma detection rate (ADR), and withdrawal time. The guidelines provided by the American Society of Gastrointestinal Endoscopy (ASGE) and the American College of Gastroenterology (ACG), along with those jointly published by the U.S. Multi-Society Task Force (which includes the American Gastroenterological Association), as well as the guidelines from the ESGE, will be reviewed to examine these indicators in detail.

Bowel preparation scores are measured using methods such as the Boston Bowel Preparation Scale (BBPS), Ottawa Scale, and Aronchick Scale. Adequate bowel preparation is defined as a BBPS score of ≥ 6 (range: 0–9), an Ottawa Scale score of ≤ 7 (range: 0–14), or an Aronchick Scale rating of “Fair” or better (Excellent, Good, Fair, Poor). Inadequate bowel preparation decreases ADR while increasing AMR, contributing to the occurrence of PCCRCs [48-50]. To improve bowel preparation, split-dose regimens are recommended [51-54], and educating patients on proper intake methods can enhance preparation quality [55,56]. Special attention should be given to individuals at risk of inadequate bowel preparation, such as the elderly, patients with diabetes or cerebrovascular disease, and hospitalized individuals [57,58]. Both the U.S. Multi-Society Task Force guidelines and the ESGE recommend maintaining adequate bowel preparation in at least 90% of all procedures [59,60]

Cecal intubation serves as an indicator not only for observing the right colon but also as a measure of the endoscopist’s technical ability to achieve complete insertion. Failure to intubate the cecum indicates an incomplete examination of the entire colon, increasing the likelihood of missed lesions and thus correlating with PCCRC risk. According to Baxter et al. [17], when the odds ratio (OR) for PCCRC incidence was set to 1 for endoscopists with a cecal intubation rate below 80%, those with an intubation rate of 90 to 94% had a reduced OR of 0.66 for proximal PCCRC and 0.71 for distal PCCRC. Endoscopists achieving a cecal intubation rate of 95% or higher demonstrated an OR of 0.72 for proximal PCCRC and 0.73 for distal PCCRC, signifying that increased cecal intubation rates significantly reduce the risk of PCCRC in both proximal and distal regions of the colon (p = 0.03). The ESGE recommends achieving a cecal intubation rate of at least 90%, while the U.S. Multi-Society Task Force advises a target of 95% or higher [59,61].

The ADR is a critical quality indicator associated with PCCRC. When comparing the PCCRC incidence based on varying ADRs, studies have shown a significant increase in PCCRC rates among endoscopists with lower ADRs. In a study that used an ADR of 20% or higher as a reference (hazard ratio [HR] of 1), the PCCRC HRs were 10.94 (confidence interval [CI]: 1.37–87.01) for an ADR of 15.0–19.9%, 10.75 (CI: 1.36–85.06) for 11 to 14.9%, and 12.50 (CI: 1.51–103.43) for ADRs below 11% [62]. Another study divided ADRs into quintiles and set the lowest quintile (≤ 19.05%) as the reference HR (HR = 1). As ADR increased, the PCCRC HR decreased substantially, with the highest quintile (≥ 33.51%) showing a HR of 0.52 (CI: 0.39–0.69), indicating a strong inverse relationship between ADR and PCCRC risk [16]. Additionally, a high ADR correlates with improved detection rates of serrated lesions, which often present on the right side of the colon and are challenging to detect [63]. The ESGE recommends maintaining an ADR of at least 25% during screening colonoscopies [59]. However, the most recent update from the U.S. Multi-Society Task Force recommends achieving an ADR of at least 35% for colonoscopies performed in individuals aged 45 and older [60].

The time taken to withdraw the colonoscope from the cecum to the anus is measured to assess the total observation time during a colonoscopy. In a study by Barclay et al. [64], analyzing 2,053 screening colonoscopies performed by 12 endoscopists, the ADR was significantly higher among endoscopists with an average withdrawal time of 6 minutes or more (28.3%) compared to those with a withdrawal time of less than 6 minutes (11.8%, p = 0.01). Additionally, Shaukat et al. [65] reported that colonoscopies with a withdrawal time of less than 6 minutes were associated with a 2.3-fold higher incidence of PCCRC compared to those with a withdrawal time of 6 minutes or more. Past guidelines from both the U.S. and Europe recommended a withdrawal time of at least 6 minutes [59,61]. However, recent studies have suggested that the optimal withdrawal time may be 8 to 9 minutes [66-68]. Reflecting these findings, the most recent update from the U.S. Multi-Society Task Force now recommends a withdrawal time of at least 8 minutes [60].

Appropriate polypectomy techniques

To prevent incomplete polyp resection, it is essential to select appropriate techniques and improve procedural skills. For non-pedunculated polyps measuring ≥ 20 mm, en bloc resection using endoscopic mucosal resection (EMR) is achieved in only 16 to 48%. Therefore, for large non-pedunculated lesions, endoscopic submucosal dissection (ESD) is recommended as a more suitable approach [69-72]. In cases where malignancy or submucosal invasion is suspected, achieving en bloc resection is crucial. For polyps larger than 10 mm, advanced imaging techniques, such as narrow-band imaging (NBI) or magnifying endoscopy, are recommended for evaluating submucosal invasion before resection [73,74]. This evaluation helps guide the selection of the appropriate resection technique based on the malignancy potential or submucosal invasion. Tools such as the NBI International Colorectal Endoscopic (NICE) and the Japan NBI Expert Team classification using NBI [75-78], as well as pit pattern classification via magnifying chromoendoscopy, as described by Kudo [79-82], can predict the pathology of deep submucosal invasion. For polyps suspected to be malignant, en bloc resection techniques should be employed; if this is not feasible, referral to a specialized center should be considered to ensure proper management.

Image-enhanced endoscopy and emerging technologies

Studies have been conducted to determine whether image-enhanced endoscopy (IEE) and emerging technologies contribute to improved ADRs or reduced AMRs. A representative IEE technique, NBI, uses optical filters to project selected narrow wavelength bands (415 ± 30 nm and 540 ± 30 nm), enabling detailed visualization of surface microstructures and mucosal patterns [83]. Early studies on NBI reported no significant benefit in ADR or AMRs compared to conventional methods [84,85]. However, nearly two decades after its introduction in 2004, recent meta-analyses of accumulated studies have demonstrated a statistically significant improvement in ADR with NBI compared to white light imaging (WLI) (WLI-ADR: 42.3%, NBI-ADR: 45.2%, p = 0.04) [86]. Additionally, studies have investigated novel technologies designed to enhance observation, such as Third Eye, FUSE, EndoRings, and EndoCuff, and have reported their potential to improve ADR [87-90]. Studies utilizing artificial intelligence (AI) have reported that AI-assisted colonoscopy can improve ADRs while simultaneously reducing AMRs [91-93]. These emerging technologies are expected to reduce the incidence of PCCRC through indirect evidence, such as improved ADR and reduced AMR. However, direct evidence demonstrating a decrease in PCCRC incidence is currently lacking, necessitating further research in this area.

CONCLUSION

PCCRC is defined as CRC not detected during a colonoscopy but diagnosed before the next recommended surveillance. PCCRC accounts for 1.8 to 9.0% of all CRCs globally and 6.2% in Korea. It is more commonly detected in the right colon than in the left and is associated with molecular pathways such as MSI, CIMP, and BRAF mutations. While a significant proportion of PCCRC cases result from procedural factors, such as missed lesions or incomplete resections, new lesions also contribute to its occurrence. Since procedural factors are preventable through high-quality colonoscopy practices, efforts to improve colonoscopy quality are essential. Key strategies include maintaining adequate bowel preparation, achieving a cecal intubation rate of 90 to 95% or higher, ensuring a withdrawal time of at least eight minutes for thorough observation, and achieving an ADR of at least 25 to 35%. Additionally, improving polypectomy techniques and utilizing advanced imaging technologies can aid in detecting and appropriately managing lesions with malignant potential or suspected submucosal invasion, with particular attention to achieving en bloc resection.

FUNDING

None.

CONFLICTS OF INTEREST

No potential conflict of interest relevant to this article was reported.

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Journal Info

JDCR
Vol.12 No.3
December 20, 2024
eISSN : 2950-9505
pISSN : 2950-9394
Frequency: Triannual

open access

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