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. 2024 Mar 3;38(2):523–530. doi: 10.21873/invivo.13470

Occurrence of Colorectal Cancer After a Negative Colonoscopy in Patients With Inflammatory Bowel Disease: A Systematic Review and Meta-analysis

GIORGIA BURRELLI SCOTTI 1, IMMACOLATA IANNONE 1, CRISTINA DE PADUA 1, DANIELE CROCETTI 1, GIULIA FIORI 1, PAOLO SAPIENZA 1, ENRICO FIORI 1, STEFANO AVENIA 1, ANTONIETTA LAMAZZA 1
PMCID: PMC10905472  PMID: 38418112

Abstract

Background/Aim

Despite the application of colorectal cancer (CRC) surveillance guidelines, the detection of early neoplastic lesions might be difficult in patients with inflammatory bowel disease (IBD). To explore the risk of post-colonoscopy CRC (PCCRC) in patients with IBD we performed a systematic review and meta-analysis.

Patients and Methods

A systematic literature search was performed (PROSPERO; no. CRD42023453049). We included studies reporting the 3-year PCCRC (PCCRC-3y) prevalence, according to World Endoscopy Organization (WEO)-endorsed definition, in IBD and non-IBD patients. As primary outcome we evaluated the PCCRC-3y prevalence, according to WEO definitions, in IBD- and non-IBD patients and calculated the odds ratio (OR). The secondary outcome was to assess risk factors for PCCRC development in IBD patients.

Results

Three retrospective observational cohort studies were included. The pooled PCCRC-3y rate in patients with IBD was 30.8% [95% confidence interval (CI)=24.4-37.5%] and in non-IBD patients was 6.8% (95%CI=6.2-7.4%). The PCCRC-3y occurrence in IBD patients was significantly higher than that in non-IBD patients (OR=6.04; 95%CI=4.04-9.4; I2=95%), but a high heterogeneity among studies was noted. Furthermore, patients with ulcerative colitis (UC) had a significantly higher prevalence of PCCRC than patients with Crohn’s Disease (CD): 30.9% (95%CI=27.8-34.2%) vs. 22.3% (95%CI=18-27%), respectively (OR=1.6, 95%CI=1.2-2.2; I2=0%).

Conclusion

One-third of CRC in IBD patients were PCCRC, and these numbers were significantly higher when compared with those in non-IBD patients. Furthermore, the prevalence of PCCRC in patients with UC was higher compared to those with CD. However, prospective studies are required to better characterize risk factors for PCCRC development in patients with IBD.

Keywords: Colorectal cancer, inflammatory bowel disease, colonoscopy, review

Colorectal cancer (CRC) is the third most common cancer and the second leading cause of cancer deaths worldwide (1). The introduction of screening tests and the early detection of gastrointestinal superficial lesions have been effective in reducing mortality and CRC incidence (2). Although colonoscopy is pivotal for the diagnosis and prevention of CRC, in some cases it may be diagnosed months or even years after a colonoscopy apparently negative for neoplasia.

A recent World Endoscopy Organization (WEO) consensus statement first used the term Post-Colonoscopy Colorectal Cancer (PCCRC) to define CRC developing after a colonoscopy negative for cancer (3). PCCRC may arise from missed cancers, missed or incompletely resected lesions, and rapidly growing new tumors (4-7). Even if the polyp-to-cancer sequence generally evolves in a long period (lasting up-to 25 years), the mean time of preclinical cancer progression to become a detectable cancer ranges between 4.5 and 5.8 years (3). According to the WEO consensus the PCCRC rate to compare endoscopic services should be settled at a 3-year follow-up period. The pooled 3-year PCCRC (PCCRC-3y) prevalence is 8.2% (8) and it comprises both “interval” and “non-interval” cancers following colonoscopy. Interval CRC occurs in the context of screening and surveillance when a CRC is identified before the next recommended examination. Non-interval PCCRCs occur when a CRC is identified either at or after a recommended screening or surveillance colonoscopy or following an examination for which no repeat was recommended, up-to 10-year after the colonoscopy (3).

In patients with inflammatory bowel disease (IBD patients) the risk of CRC is higher than in non-IBD patients. The standardized incidence ratios for developing CRC are 1.9 for patients with Crohn’s disease (CD) and 2.4 for those affected with ulcerative colitis (UC) patients, respectively (9). CRC rates in IBD patients decreased over the past decades, probably reflecting the improvement in medical therapies and endoscopic screening/surveillance (10). Regardless, CRC represents one of the main causes of death in IBD patients (15% of all deaths in IBD patients), while IBD-associated CRC only represents 1-2% of all CRC (11). In a recent multicenter study, the Authors (12) found that 53.3% of interval CRC in IBD patients were detected within the surveillance window, owing to non-adherence to guidelines. Noticeably, most of the IBD-patients had an active disease at the time of index colonoscopy (12). In a recent study which enrolled 1,273 IBD patients undergoing routine surveillance, 1.3% of IBD patients developed CRC, 70% of them caused by several factors, such as poor-quality colonoscopy, inadequate surveillance interval, and inadequate management of previous dysplasia (13).

The aim of our systematic review and meta-analysis was to evaluate the PCCRC rate in IBD patients when compared to non-IBD patients. Furthermore, we tried to identify risk factors affecting PCCRC development in this group of patients.

Patients and Methods

This systematic review was performed according to the Preferred reporting Item for Systematic Review and Meta-Analyses (PRISMA) statement (14). The review protocol was registered in PROSPERO (CRD42023453049).

The criteria for inclusion in the present systematic review and meta-analysis were as follows:

a. Inclusion criteria: Cohort and case-control studies; Studies including the PCCRC-3y prevalence according to the WEO-endorsed definition (3).

b. Type of participants: IBD patients and non-IBD patients.

c. Type of treatment: Colonoscopy.

The following primary outcomes were studied: 1) PCCRC-3y prevalence, according to WEO-endorsed definitions (3) in IBD- and non-IBD patients. Briefly, false-negative colonoscopies were divided into true positive and false negative colonoscopies, where false negatives refer to colonoscopy with CRC diagnosed between 6 and 36 months after the procedure and true positives refer to colonoscopy with CRC diagnosed at or within 6-month of the index colonoscopy. 2) Risk of PCCRC in IBD patients compared with non-IBD patients. 3) Risk of PCCRC between patients with UC and those with CD.

The secondary outcome studied was the following: risk factors for PCCRC development in IBD patients.

A systematic electronic literature search was conducted using PubMed, SCOPUS, and Web of Science (WOS) to identify all eligible studies. The last search was performed in August 2023, with no language restriction. The combination of the following keywords and medical subject headings (MeSH) terms were used: “Crohn’s disease” or “Ulcerative colitis” or “inflammatory bowel disease”, “interval cancer” or “post-colonoscopy colorectal cancer” or “PCCRC”.

Three Authors (GBS, IA, CDP) participated in the literature search, study selection, and data extraction independently. Inconsistency between researchers was resolved through discussion with a fourth Author (PS). Nonoriginal studies (i.e., case reports, commentaries, letters, and editorials), abstracts and animal studies were excluded. When overlapping was found between multiple articles published by the same authors and no difference in the examined time, only the most recent study was enclosed to avoid duplication. The PubMed function “related articles” and Google Scholar database were used to find further articles. A search on Google book was performed for the analysis of the grey literature (15).

Data extraction was conducted in duplicate by two reviewers (GBS and IA), independently extracting data from all included studies. A data collection electronic sheet based on the methods described in the Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses (16) was developed to confirm study relevance and to extract study characteristics. Study characteristics included: publication year, study design, country, number of patients included, age, sex, study period, number of colonoscopies, PCCRC. To ensure accurate data collection, each reviewer independently abstracted data to be compared. Any discrepancies and disagreements were discussed and resolved through a consensus session with a third researcher (PS).

Statistical analysis. The data analysis was performed using the meta-analysis software IBM® SPSS® 28.0.1.1 (IBM® Italia S.p.A. Circonvallazione Idroscalo 20090 Segrate, MI, Italy). Inter-reviewer agreement for inclusion eligibility was evaluated with the Cohen’s kappa (ĸ) statistic. A k value of 1.000 indicates perfect agreement, a k of 0.000 no agreement and a k of −1.000 complete disagreement. Furthermore, k values between 0.600 and 0.800 are considered to indicate ‘fair - good’ agreement and k values superior to 0.800 ‘excellent’ agreement beyond chance (17). Since there were few studies available for this analysis, and, therefore, an accurate estimate of the between-studies variance was difficult to obtain, we used a fixed or random-effect model. Briefly, in this model all differences reflect the sampling error. Therefore, any variance would come from within each study. The pooled estimate is calculated as a weighted average, where the weight assigned to each study is the inverse of that study’s variance. Specifically, in our study, larger studies had more weight than smaller studies. The odds ratio (OR) with a 95% confidence interval (CI) was used for the effect size measure. The method used for the fixed-effect model was the Mantel-Haenszel (18). All results are displayed in forest plot graphs. The I2 test was utilized for the heterogeneity assessment. A value greater than 50% was significant for heterogeneity. Publication bias was assessed through funnel plots and Egger’s test for asymmetry.

Results

The PRISMA flow chart for systematic review is schematically reported in Figure 1. Briefly, after the screening for relevance, 110 articles remained for further assessment of eligibility, 107 of them were successively excluded and a total of 3 articles (19-21) were eligible for the present study. There was near-perfect agreement between reviewers on study eligibility (ĸ=0.96; 95%CI=0.92-1.00).

Figure 1. Preferred reporting items for systematic reviews and meta-analyses flow diagram.

Figure 1

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Quality assessment. The potential risk of bias in each of the articles included in this retrospective review is depicted in Table I and was calculated using the NOS criteria (16).

Table I. Methodological quality appraisal using the Newcastle-Ottawa Quality Assessment Scale (NOS) for cohort studies.

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– : Criteria not met; *1 point for meeting criteria; **2 points for meeting criteria. Overall score: 0-3 points: poor quality; 4-6 points: fair quality; 7-9 points: good quality.

Characteristics of the studies. Three studies were included in this systematic review. The articles were retrospective observational cohort studies all conducted in Northern Europe between 1995 and 2015. Overall, 172,030 colonoscopies for CRC detection were performed within 3 years and 12,748 (7.4%) PCCRC were noted. Demographics and characteristics of the population and of the studies are depicted in Table II.

Table II. Descriptive analysis of the population.

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CRC: Colorectal cancer; IBD: inflammatory bowel disease. *Εxpressed as median; NR: not reported; PCCRC: post-colonoscopy colorectal cancer within three years of colonoscopy according to World Endoscopy Organization definition.

Primary outcome. The pooled PCCRC-3y occurrence in IBD patients was 30.8% (95%CI=24.4-37.5%), and specifically, it was 30.9% (95%CI=27.8-34.2%) in patients with UC and 22.3% (95%CI=18-27%) in those with CD. Conversely, in non-IBD patients the pooled PCCRC-3y occurrence was 6.8% (95%CI=6.2-7.4%). We demonstrate a significant increase in PCCRC-3y rate in IBD patients when compared with non-IBD patients (p<0.0001). The odds ratio was 6.04 (95%CI=4.04-9.4). However, a high heterogeneity was demonstrated among studies (I2=95%) (Figure 2). Egger’s test failed to detect any publication bias (p = 0.2). Funnel plot is shown in Figure 3. The PCCRC-3y rate also showed a statistically significant (p<0.02) difference in patients affected with UC as compared to those affected with CD (OR=1.6, 95%CI=1.19-2.15) (Figure 4). Noticeably, a great homogeneity of the samples was registered (I2=0%).

Figure 2. Forest plot for risk of post-colonoscopy colorectal cancer in inflammatory bowel disease (IBD) compared with non-IBD patients. OR: Odds ratio; FN: false negative; TP: true positive.

Figure 2

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Figure 3. Funnel plot for risk of post-colonoscopy colorectal cancer in inflammatory bowel disease (IBD) compared with non-IBD.

Figure 3

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Figure 4. Forest plot for risk of post-colonoscopy colorectal cancer in ulcerative colitis (UC) compared with Crohn’s disease (CD). OR: Odds ratio; FN: false negative; TP: true positive.

Figure 4

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Secondary outcome. The present literature does not permit this analysis because of insufficient data to understand the role of specific risk factors, both patient- and disease-related, in the development of PCCRC in IBD patients.

Discussion

In the present systematic review and meta-analysis, we found that about one-third of CRC in IBD patients were discovered after a negative colonoscopy, with a significant higher risk of PCCRC among IBD patients when compared to non-IBD patients, as testified in our analysis by the elevated OR. Furthermore, the risk of PCCRC development was significantly higher in patients with UC as compared to those with CD.

Even if the overall cumulative incidence proportions of PCCRC is low either in non-IBD or IBD patients (0.2% and 0.4% of all patients undergoing colonoscopies) (21), these data require discussion. In the general population the specific characteristics of patients with PCCRC are: a prior diagnosis of CRC, prior polypectomy, high comorbidity index, diverticular disease and IBD (19,20). Specifically, in non-IBD patients, PCCRC arises from missed or incompletely resected lesions, and less commonly by rapidly growing CRC arising from de novo lesions (3-7). To what extent the risk of PCCRC in IBD patients is due to the quality of colonoscopy or to the aggressive nature of the tumor has not been yet established, because IBD-related CRC and sporadic CRC differ in presentation and molecular features (22-24), and because active inflammation hides dysplastic lesions that would otherwise be visible with high definition colonoscope and chromoendoscopy (25).

In the UK population, Burr et al. (19) stated that PCCRC rates were lower for colonoscopies performed under the English National Health Service (NHS) bowel cancer screening program, adhering to strict performance criteria (high standard with high adenoma detection and cecal intubation rates), as compared to those conducted by non-NHS providers (3.6% vs. 9.3%, respectively). In a recent study from a tertiary referral center in Australia with high key performance indicators the PCCRC-3y rate was 2.2% (26). However, in a multicentric study of IBD patients, Burke et al. (12) found no significant difference in colonoscopy quality measure between patients with and without IBD, and they also observed that IBD patients with interval CRC had a significantly younger age and active inflammation at the time of the index colonoscopy. Despite a significant reduction of the PCCRC rate in people without IBD over time, reflecting a better endoscopic technique and surveillance program, Burr et al. (19) demonstrated the PCCRC-3y rate was 38% in 2005 and 36% in 2013. Conversely, Troelsen et al. (21) found a decrease of PCCRC-3y rate in both IBD and non-IBD patients (from 43% in IBD and 27% in non-IBD in 1995 to 14% and 5% in 2015, respectively); we believe that a wider observation time might have determined this important reduction in CRC occurrence.

The studies included in our systematic review and meta-analysis had no sufficient data to extrapolate the role of specific risk factors, both patients- or disease-related, for the development of PCCRC in IBD patients. However, studies from the same Danish and Swedish cohorts indicated the following risk factors: primary sclerosing cholangitis in IBD patients, the young age, mismatch repair deficiency, metastatic presentation at diagnosis, proximal location, previously resected colorectal polyps and dysplasia for UC, and rectal location for CD (27,28). Troelsen et al. (21) found that the hazard ratio of PCCRC adjusted for age, sex, year of colonoscopy, and co-morbidities in IBD patients was similar to non-IBD patients, and it was calculated including all patients who underwent colonoscopies. They also observed an increased PCCRC-3y rate with the number of colonoscopies performed and that patients with IBD were generally more likely to have records of multiple colonoscopies than non-IBD patients, although it is unlikely that this accounts entirely for the increased PCCRC rates, that were also elevated regardless the number of colonoscopies performed.

Our study has several limitations including the application of a formal meta-analytic method to retrospective observational studies. Similarly, the diversity of study designs and populations makes the interpretation of simple summaries problematic. Despite these limitations, meta-analyses of observational studies continue to be one of the few methods for assessing efficacy and effectiveness. Therefore, we believe that our results can improve the comprehension of the most useful approach to these patients. Furthermore, these studies lack information on the quality of index colonoscopy (bowel preparation, cecal intubation rate), extent of colitis and disease duration, adherence to surveillance programs, and accurate description of polyps’ resection. However, the data from these three studies, all population-based cohorts, have a very important strength point, i.e., the same calculation method for PCCRC rate as recommended by WEO (29).

The higher risk of PCCRC in IBD patients compared to non-IBD patients could reflect an increased risk of overlooking subtle lesions especially in patients with active disease, despite modern endoscopic techniques, and a particularly aggressive CRC biology. The correction of modifiable factors, such as the quality of colonoscopy, the adherence to surveillance guidelines, the proper patient referral, especially those with high-risk, to high volume centers may reduce the risk of PCCRC (12,30,31). However, further observational or prospective studies are needed to identify risk factors of PCCRC in IBD patients in order to reduce their incidence.

In conclusion, we suggest a high-quality surveillance colonoscopy for the early detection of IBD-related cancers because appropriate surveillance measures contribute significantly to the reduction in the incidence of CRC and the associated mortality. However, early neoplastic lesion detection remains difficult in IBD patients, even if surveillance colonoscopy is routinely performed and despite the strict application of guidelines.

Funding

This research received no external funding.

Conflicts of Interest

The Authors have no conflicts of interest to declare regarding this study.

Authors’ Contributions

Giorgia Burrelli Scotti: conceptualization, design and writing the manuscript, collection and analysis of data; Immacolata Iannone: collection and analysis of data, design and writing the manuscript; Cristina De Padua: collection and analysis of data, design and writing the manuscript; Daniele Crocetti: collection and analysis of data, writing the manuscript; Giulia Fiori: collection and analysis of data, writing the manuscript; Paolo Sapienza: Conceptualization, design and writing the manuscript, collection and analysis of data, supervision; Enrico Fiori: Conceptualization, design and writing the manuscript, supervision; Stefano Avenia: collection and analysis of data, design and writing the manuscript; Antonietta Lamazza: Conceptualization, design, supervision. All Authors have approved the final submitted draft.

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