Incidence of advanced neoplasia during surveillance in high- and intermediate-risk groups of the European colorectal cancer screening guidelines

• Introduction
• Patients and methods
• Study design
• Definition of study groups
• Sources for data collection
• Outcome measures
• Dependent variables
• Sample size calculation
• Data analysis
• Results
• Baseline characteristics
• Incidence of advanced neoplasia
• Incidence of CRC
• Variables independently associated with the risk of advanced neoplasia detection at first colonoscopy
• Discussion
• References

Background and study aims: The European guidelines for quality assurance in colorectal cancer (CRC) screening have established high-risk (≥ 5 adenomas or an adenoma ≥ 20 mm) and intermediate-risk (3 – 4 adenomas or at least one adenoma 10 – 19 mm in size, or villous histology, or high grade dysplasia) groups with different endoscopic surveillance intervals. The aim of this study was to evaluate the difference in the incidence of advanced neoplasia (advanced adenoma or CRC) between the two risk groups.

Patients and methods: This retrospective group study included patients meeting high- or intermediate-risk criteria for adenomas detected in CRC screening programs and the COLONPREV study before European guidelines were adopted in Spain (June 2011) with a 3-year surveillance recommendation according to Spanish guidelines. The primary outcome measure was the incidence of advanced neoplasia in patients undergoing surveillance. The secondary outcome measure was the CRC incidence. We used an adjusted proportional hazards regression model to control confounding variables.

Results: The study included 5401 patients (3379 intermediate risk, 2022 high risk). Endoscopic surveillance was performed in 65.5 % of the patients (2.8 ± 1 years). The incidence of advanced neoplasia in the high- and intermediate-risk groups was 16.0 % (59.0 cases/1000 patient-years) and 12.3 % (41.2 cases/1000 patient-years), respectively. The CRC incidence was 0.5 % (1.4 cases/1000 patient-years) and 0.4 % (1 case/1000 patient-years), respectively. The advanced neoplasia and CRC attributable risk to the high risk group was of 3.7 % and 0.1 %, respectively. In the proportional hazards analysis, the risk of advanced neoplasia was greater in the high-risk group (hazard ratio [HR] 1.5, 95 % confidence interval [CI] 1.2 – 1.8), with no significant differences in the CRC incidence (HR 1.6, 95 %CI 0.6 – 3.8).

Conclusions: Patients meeting high-risk criteria have a higher incidence of advanced neoplasia during endoscopic surveillance. No differences were found in the CRC incidence at a 3-year surveillance recommendation.

Introduction

Population-based screening programs for colorectal cancer (CRC) have demonstrated effectiveness in reducing the mortality and incidence of CRC [1] [2] [3]. Similarly, they have been shown to be a highly cost-effective healthcare policy and can even reduce healthcare costs [4]. Most of the effect is related to the detection and resection of colorectal adenomas [5] [6]. Once a colorectal adenoma has been resected, patients require surveillance because of their increased risk of developing new neoplastic lesions in the colon. However, endoscopic surveillance is resource consuming and should therefore be adjusted to the risk of developing new advanced neoplasia. In this regard, several clinical guidelines have proposed different surveillance strategies [1] [2] [3] [7] [8]. In general, these guidelines have proposed a 5 – 10-year endoscopic surveillance interval for a low-risk group (adenomas < 10 mm and ≤ 2 in number and with an exclusively tubular histology) [9]. The remaining patients have traditionally been included in a high-risk group, with a 3-year endoscopic surveillance recommendation [1] [2].

The European guidelines for quality assurance in CRC screening and diagnosis subdivided the high-risk group into two groups according to the results of a combined analysis of eight surveillance studies [3] [10]. Consequently, three risk groups have been included in these guidelines: low risk (as mentioned above), intermediate risk (3 – 4 adenomas or at least one adenoma 10 – 19 mm in size, or villous histology, or high grade dysplasia [HGD]), and high risk (5 – 9 adenomas or an adenoma ≥ 20 mm in size) with different endoscopic surveillance recommendations. In the high- and intermediate-risk groups, a first colonoscopy surveillance is recommended within 1 and 3 years, respectively, after the complete removal of all the adenomas found at baseline colonoscopies [3].

The results of the pooled analysis performed by Martínez et al. [10] showed the heterogeneity in the risk of detecting adenomas during surveillance examinations. These differences have mainly been linked to the quality of the initial colonoscopy [1] [2] [11] [12]. In this regard, several colonoscopy quality indicators have been established, and the compliance with these criteria has been associated with an increase in the adenoma detection rate and a decrease in the incidence of CRC and its associated mortality [12] [13] [14] [15]. For this reason, CRC screening programs apply quality control policies based on colonoscopy quality indicators [12] [13].

Within the Spanish network of CRC screening programs and the COLONPREV study [16], we have carried out a cohort study comparing the incidence of advanced neoplasia and CRC in patients meeting the high- and intermediate-risk criteria established by the European guidelines for lesions detected and removed at baseline colonoscopy. The aim of the study was to determine whether there are differences in the incidence of advanced neoplasia and CRC detection at the first endoscopic surveillance between the two risk groups at a 3-year interval recommendation that would confirm the recommendations included in the European guidelines.

Patients and methods

Study design

We designed a retrospective cohort study performed within the Spanish network of CRC screening programs and the COLONPREV study (ClinicalTrials.gov NCT00906997) [16]. All of these screening programs apply quality control policies based on colonoscopy quality indicators [12] [13]. Only patients who met high-risk criteria according to American and Spanish guidelines were included in the study: at least one advanced adenoma (≥ 10 mm, or villous histology, or HGD) or more than two adenomas of any characteristic [1] [2]. After reviewing the available databases, we excluded patients with missing data, multiple colorectal adenomas (≥ 10 adenomas) or non-high-risk adenomas. The inclusion period started with the initial implementation of population-based screening programs in Spain (2000) and ended when the European guidelines were adopted by the Spanish CRC screening programs (June 2011). The study protocol was approved by the Clinical Research Ethic’s Committee of Hospital Virgen de la Arrixaca, Murcia, Spain (Act number 512012).

Definition of study groups

Two groups were defined on the basis of the European guidelines for quality assurance in CRC screening and diagnosis: intermediate-risk group and high-risk group. The first surveillance study in both groups was recommended to take place 3 years after the complete resection of the baseline adenomas [1] [2].

Sources for data collection

The information was gathered from the screening programs, information system (Spanish network of CRC screening programs, database of the COLONPREV study) and medical records. For patients who did not undergo endoscopic surveillance, we used the National Health System’s Hospital Discharge Records Database (CMBD in Spanish) to identify the incidence of CRC. The CMBD database receives notifications from approximately 98 % of the Spanish public hospitals [17]. Compulsory health insurance covers an estimated 99.5 % of the Spanish population, although patients who are not covered by health insurance can still receive treatment in public hospitals. Since 2005, the CMBD has also had partial coverage from private hospitals [18]. Codes 153 – 4 of the International Classification of Diseases, Ninth Revision, Clinical Modification were used to identify cases of CRC [19].

Outcome measures

The primary outcome measure of the study was the incidence of advanced neoplasia defined as CRC or advanced adenoma in the first surveillance colonoscopy examination [20]. The incidence of advanced neoplasia was expressed as cumulative incidence or incidence density ratio (number of cases per 1000 patient-years) of the population that underwent endoscopic surveillance.

The secondary outcome measure of the study consisted of the incidence of CRC, indicated as the cumulative incidence or incidence density ratio of the population with high- or intermediate-risk adenomas regardless of whether they underwent endoscopic surveillance or not.

Dependent variables

In order to establish the variables associated with the risk of advanced neoplasia detection and to control for the confounding variables, we collected data on several factors: age, sex, initial CRC screening test (colonoscopy, fecal immunochemical test, guaiac fecal test), quality of the colonoscopy (cecal intubation and bowel cleansing measured with the Aronchick scale) [21], and the characteristics of the adenomas detected at the baseline colonoscopies. Bowel cleansing was considered to be adequate if more than 90 % of the colonic mucosa could be evaluated. We determined the total number of adenomas as well as their size, location (distal or proximal to the splenic flexure), villous histology (> 20 %), HGD, and serrated lesions (traditional serrated adenomas) [22].

For the surveillance studies, we included information on the first colonoscopic surveillance: date, quality of the colonoscopy, characteristics of the adenomas detected and, in those cases in which CRC was detected, the date, the location relative to the splenic flexure, and the tumor stage according to the American Joint Committee on Cancer, 7th edition [23]. In patients who did not undergo endoscopic surveillance, the last date of the follow-up evaluation was determined on the basis of the CRC diagnosis date or the last follow-up information available on CMBD if no CRC was detected.

Sample size calculation

This study was based on the assumption that the incidence of advanced neoplasia in the high-risk group following a 3-year interval would not be greater than that of the intermediate-risk group. The calculation was performed considering a surveillance compliance of 80 %, an estimated incidence of advanced neoplasia in the high-risk group of 15 %, and a 1:2 ratio between the high- and intermediate-risk groups [10] [24]. By accepting a nonsuperiority condition if the absolute difference between both groups was lower than 2.44 % [10], a sample size of 5525 (1879 high-risk patients and 3647 intermediate-risk patients) would provide 80 % power at a 5 % significance level using a one-tailed test of proportions.

Data analysis

A descriptive analysis of the patients was performed based on their risk group, including baseline characteristics of the study population and the endoscopic findings of their diagnostic colonoscopy. Thereafter, we calculated the cumulative incidence of advanced neoplasia and the incidence density rate in the population who underwent endoscopic surveillance examinations. We also determined the attributable risk to the high-risk group, defined as the cumulative incidence in the high-risk group minus that in the intermediate-risk group [25]. The chi-squared test was used to determine whether the cumulative incidence rate in the intermediate-risk group was equal to that of the high-risk group. The differences between the two risk groups were expressed as risk ratio (RR) with 95 % confidence intervals (95 %CI). The Kaplain–Meier one minus survival curves were drawn, and a Cox’s proportional hazards model was used to compare the differences in the incidence of advanced neoplasia between the groups, adjusted for potential confounders (age, sex, CRC screening program, initial screening test, cecal intubation rate, and bowel cleansing). The differences were expressed as hazard ratios (HR) with a 95 %CI. In addition, a secondary analysis was conducted to estimate the differences in the incidence of CRC between the two risk groups.

Finally, we determined which demographic and baseline endoscopic variables, including time to the first surveillance colonoscopy, were independently associated with the incidence of advanced neoplasia at the first surveillance colonoscopy. We used a multivariable logistic regression analysis to determine which variables were independently associated with advanced neoplasia detection and the differences were expressed as odds ratio (OR) with a 95 %CI. Differences of P < 0.05 were considered to be statistically significant. Statistical analyses were performed with IBM SPSS Statistics for Windows, Version 22.0 (IBM Corp., Armonk, New York, USA).

Results

Baseline characteristics

We identified a total of 5872 patients who could be considered for inclusion during the study period. After reviewing their characteristics, 471 patients were excluded because they did not meet inclusion criteria (missing data n = 98, low risk adenomas n = 200, more than 10 adenomas n = 173). Thus, the study finally included 5401 patients: 2022 meeting high-risk criteria and 3379 meeting intermediate-risk criteria ([Fig. 1]). As shown in [Table 1], the groups differed in terms of sex and primary screening test results. Patients in the intermediate-risk group required fewer baseline colonoscopies for complete removal of all lesions (1.1 ± 0.3) than patients in the high-risk group (1.3 ± 0.6; P < 0.001). No differences were found in terms of age, bowel cleansing results, and cecal intubation rate.  [Table2] includes the characteristics of the adenomas detected at the baseline colonoscopies.

The first endoscopic surveillance was performed in 3536 patients (65.5 %) after a mean period of 2.8 ± 1 years (median 3.1, interquartile range [IQR] 2.5 – 3.4 years). More patients with high-risk lesions at baseline examination underwent the first endoscopic surveillance than those with intermediate-risk lesions (high-risk 69.4 %, intermediate-risk 63.1 %; RR 1.1, 95 %CI 1.06 – 1.14). Furthermore, less time elapsed between the last baseline colonoscopy and the endoscopic surveillance in the high-risk group (high-risk 2.7 ± 1 years, intermediate-risk 2.9 ± 0.9; P < 0.001). The first surveillance colonoscopy was performed before 1, 2, 3, 4, and 5 years after baseline colonoscopy in 6.5 %, 28.2 %, 47.9 %, 94.1 %, and 99.2 % of the high-risk patients and in 3.6 %, 15.0 %, 37.6 %, 94.5 %, and 98.5 % of the intermediate-risk patients who underwent surveillance colonoscopy, respectively.

The baseline characteristics of patients who underwent endoscopic surveillance are shown in [Table 1]. There were baseline differences between patients who underwent endoscopic surveillance and those who did not undergo endoscopic surveillance. In this respect, patients meeting high-risk criteria with endoscopic surveillance had a lower proportion of inadequate bowel cleansing (0.4 % vs. 1.5 %; P = 0.006), had more adenomas located both distal and proximal to the splenic flexure (56.0 % vs. 51.0 %; P = 0.04), had more advanced adenomas (≥ 2) (19.5 % vs. 15.5 %; P = 0.03), and more adenomas with villous histology (62.3 % vs. 56.6 %; P = 0.02) than those patients meeting high-risk criteria who did not undergo any surveillance colonoscopy. Patients meeting intermediate-risk criteria who underwent endoscopic surveillance had a lower proportion of inadequate bowel cleansing (0.4 vs. 1.1 %; P = 0.01), more serrated lesions (4.1 % vs. 2.6 %; P = 0.02), and more adenomas with villous histology (48.9 % vs. 45 %; P = 0.03) compared with intermediate-risk groups who did not undergo surveillance colonoscopy.

Incidence of advanced neoplasia

Advanced neoplasia was detected in 487 patients of the total of 3536 patients who underwent their first endoscopic surveillance, with a cumulative incidence of 13.8 % and an incidence density rate of 47.9 cases/1000 patient-years (95 %CI 43.6 – 52.1). The univariate analysis showed that the cumulative incidence of advanced neoplasia was slightly greater in the high-risk group (high-risk 16.0 %, intermediate-risk 12.3 %; RR 1.3, 95 %CI 1.1 – 1.5). The attributable risk of advanced neoplasia to the high-risk group during the endoscopic surveillance was 3.7 % (95 %CI 1.3 % – 6.1 %). The differences between the two risk groups were statistically significant after adjusting the analysis for confounders (HR 1.5, 95 %CI 1.2 – 1.8) as shown in [Fig. 2]. The incidence density rate is shown in  [Fig.2] and [Table 3].

Incidence of CRC

A CRC was detected in 19 patients at a mean (SD) of 2.9 (1.1) years (median 3.2, IQR 1.8 – 3.5) after the baseline colonoscopy. After searching the health system databases, we identified and confirmed three additional cases of CRC with a period from baseline colonoscopy ranging between 3.9 and 6.8 years. The location of the detected tumors was distal to the splenic flexure in 13 patients, proximal in 7 patients, and undefined in 2 patients. The tumor stage was I in 8, II in 4, III in 5, and IV in 5. The cumulative incidence of CRC in the global group was of 0.4 % and the incidence density rate was 1.1 cases/1000 patient-years (95 %CI 1.6 – 0.6). We found no statistically significant differences between the two groups in the cumulative incidence of CRC (high-risk 0.5 %, intermediate-risk 0.4 %; RR 1.4, 95 %CI 0.6 – 3.2), with a 0.1 % (95 %CI – 0.2 to + 0.5) attributable risk to the high-risk group. This result was confirmed after controlling for potential confounders in the Cox regression analysis (HR 1.6, 95 %CI 0.6 – 3.8), as shown in  [Fig.3]. The incidence density rate is shown in [Fig. 3] and [Table 3].

Variables independently associated with the risk of advanced neoplasia detection at first colonoscopy

[Table 4] shows the incidence of advanced neoplasia according to the baseline variables as well as the multivariable logistic regression analysis to determine which baseline variables were associated with the risk of advanced neoplasia detection during surveillance examinations. Only four variables were independently associated with advanced neoplasia detection: guaiac fecal test as the primary screening test (OR 1.9, 95 %CI 1.1 – 3.4), more than five adenomas (OR 1.7, 95 %CI 1.2 – 2.3), at least one adenoma with a villous histology (OR 1.4, 95 %CI 1.1 – 1.7), and at least one adenoma with HGD (OR 0.7, 95 %CI 0.5 – 0.98).

Discussion

Results of this cohort study have shown that individuals meeting the high-risk criteria established by the European guidelines in CRC screening [3] have a slightly increased risk of advanced neoplasia detection following a 3-year surveillance recommendation compared with those classified as intermediate-risk subjects (16.0 % vs. 12.3 %). However, the attributable risk to this group was only 3.7 % and we found no differences in the incidence of CRC between both groups.

The study has several strengths. We gathered the information from six regional CRC population-based screening programs and the COLONPREV study. These programs were based on different primary screening tests: colonoscopy, guaiac and immunological fecal occult blood test, which met quality criteria of a common quality assurance policy that enabled the establishment of a continuous evaluation of quality indicators [12] [13] [26]. Thus, we had the opportunity to collect relevant information related to both the baseline findings at colonoscopy, the endoscopic surveillance, and the incidence of CRC from a large number of asymptomatic individuals. Another important issue that must be highlighted is that the abovementioned CRC screening programs based their endoscopic surveillance recommendations on the Spanish and American clinical practice guidelines until June 2011. Hence, a 3-year endoscopic surveillance recommendation was established in all patients with at least one advanced adenoma or more than two adenomas at their baseline evaluation [1] [2]. In fact, although less time elapsed until the surveillance assessment in the high-risk group, there was only a difference of 2.5 months between the high- and intermediate-risk groups. We did not evaluate the low-risk group because, based on the Spanish guidelines, a different surveillance recommendation (5-year interval) was established for this group. In this low-risk group, the European guidelines recommend that patients are re-introduced into the screening program rather than entering a specific endoscopic surveillance program.

The most relevant matter that arises from this study is a question about the main goal of surveillance programs after resection of an adenoma, especially in asymptomatic individuals. The aim of any surveillance strategy after an adenoma resection, as in the case of CRC screening, is to reduce the incidence and mortality of CRC [3] [7]. Although most patients with advanced or multiple adenomas have an increased risk of death from CRC, only one cohort study has shown that endoscopic surveillance reduces the incidence of CRC [27]. In fact, no randomized controlled trial has evaluated different surveillance intervals with the incidence of CRC or its associated mortality as an end point. The different post-polypectomy and colonoscopy surveillance recommendations available are based mainly on observational studies and a pooled analysis of randomized controlled trials with advanced neoplasia as their primary end point. As a matter of fact, in the study published by Martinez et al. the incidence of CRC after a median follow-up period of 47 months was 0.8 % in the American guidelines high-risk group, a value that is only slightly higher than the incidence of CRC found in the current study (0.4 %) [10].

A prospective study, in which higher rates of surveillance in both the intermediate- and high-risk groups are achieved, and more information on the quality of the baseline colonoscopy, would be a far superior design to answer the questions of interest. In this respect, the European Polyp Surveillance (EPoS) trials (NCT02319928), which compare different surveillance intervals in terms of 10-year CRC incidence as the main end point will solve most of the uncertainty regarding endoscopic surveillance after adenoma resection [28]. In the meantime, expert recommendation documents and clinical practice guidelines should determine whether a CRC attributable risk of 0.1 % in the high-risk group justifies more frequent surveillance, with the consequent increase in risk of major complications, workload and, thus, the expenditure of medical and economical resources [7] [15] [29].

The current study also has several limitations. The main limitation relates to the difference in the surveillance rates between the two risk groups. First, the surveillance rate was lower than expected but comparable to that reported from other studies that have evaluated the use of surveillance colonoscopy on a community-wide basis [30]. However, we were aware that there could be differences both in the surveillance rate and in the length of time to the first surveillance colonoscopy. We have tried to mitigate any potential bias by limiting the analysis of advanced neoplasia incidence to the first colonoscopy in patients who performed at least one surveillance examination. Furthermore, we performed two different analyses, one based on the cumulative incidence and the other on the incidence density rate. As we have shown, there were no differences in the results obtained in both analyses, highlighting the strength of the findings.

We were unable to include several quality indicators related to the endoscopies: adenoma detection rate, withdrawal time, and number of baseline colonoscopies required, because this information was not available for all screening programs. Although these factors could potentially modify the risk of advanced neoplasia or CRC detection during the surveillance period, we believe that they do not change the differences in the incidence of advanced neoplasia or CRC detection between the two groups evaluated. We have not evaluated several demographic and epidemiological variables associated with the incidence of advanced neoplasia, such as smoking habit, family history of CRC, and body mass index. However, the aim of the study was to evaluate the European guidelines classification and not to determine which variables were independently associated with the risk of advanced neoplasia during surveillance.

The third limitation is related to the study design. The study was not designed to detect differences in the incidence of CRC. Indeed, we would need to include nearly 150 000 patients in the study in order to detect a statistically significant difference based on the incidence of CRC observed in the current study. In fact, we believe that, even if it was statistically significant, a 1/1000 attributable fraction risk is not a clinically relevant difference and not sufficient to justify subjecting patients to a more intensive endoscopic surveillance schedule. As an example, this increased risk is counterbalanced by the 1/1000 acceptable risk of perforation in the screening colonoscopy [15]. Finally, we were unable to assess whether all of the advanced adenomas detected during the surveillance period could be endoscopically resected or which proportion required surgical resection. Obviously, the decrease in the morbidity associated with colorectal surgery must also be an end point of any surveillance strategy implemented after an adenoma resection. Unfortunately, as in the case of the endoscopy quality indicators, this information was not systematically collected in all screening programs.

To conclude, the high-risk criteria established by the European guidelines for CRC screening are only associated with a slightly increased risk of detecting advanced neoplasia during surveillance examinations and a doubtful increase in the incidence of CRC. These differences may not be enough to justify modifications in the surveillance recommendations established in the European guidelines.

Competing interests: None.

Acknowledgments

This article was presented at the United European Gastroenterology Week that took place in Barcelona, Spain, 24 – 28 October 2015.

This study was supported by a grant (FFIS-DF-2013-1502) from the Foundation for Healthcare Training and Research of the Region of Murcia (Murcia, Spain) whose funds were donated by Norgine (Madrid, Spain) on the basis of an agreement (bases and guiding principles of the cooperation between Norgine and the Foundation for Healthcare Training and Research of the Region of Murcia). The funding institutions played no part in the study design; the collection, analysis, and interpretation of the collected data; the writing of the report; or in the decision to submit the article for publication.

J.C. and V.H. have received an intensification grant through the European Comission supported “BIOCAPS” project (FP-7-REGPOT 2012-2013-1, Grant agreement no. FP7 – 316265)

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Corresponding author

• References

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