Impact of surgical versus endoscopic management of complex nonmalignant polyps in a colorectal cancer screening program

• Abstract
• Introduction
• Methods
• MISCAN-Colon
• Population and screening program simulated
• Scenarios for management of complex nonmalignant polyps
• Complications with colonoscopy and surgery
• Utility losses
• Costs
• Outcomes
• Sensitivity analyses
• Results
• Prediction of annual outcomes in the Dutch CRC Screening Program (2014–2023)
• Prediction of lifetime outcomes of the Dutch CRC Screening Program
• One-way sensitivity analyses
• Threshold analysis and PSA
• Discussion
• Funding
• References

Abstract

Background When complex nonmalignant polyps are detected in colorectal cancer (CRC) screening programs, patients may be referred directly to surgery or may first undergo additional endoscopy for attempted endoscopic removal by an expert. We compared the impact of both strategies on screening effectiveness and costs.

Methods We used MISCAN-Colon to simulate the Dutch screening program, and projected CRC deaths prevented, quality-adjusted life-years (QALYs) gained, and costs for two scenarios: 1) surgery for all complex nonmalignant polyps; 2) attempted removal by an expert endoscopist first. We made the following assumptions: 3.9 % of screen-detected large nonmalignant polyps were complex; associated surgery mortality was 0.7 %; the rate of successful removal by an expert was 87 %, with 0.11 % mortality.

Results The screening program was estimated to prevent 11.2 CRC cases (–16.7 %) and 10.1 CRC deaths (–27.1 %), resulting in 32.9 QALYs gained (+ 17.2 %) per 1000 simulated individuals over their lifetimes compared with no screening. The program would also result in 2.1 surgeries for complex nonmalignant polyps with 0.015 associated deaths per 1000 individuals. If, instead, these patients were referred to an expert endoscopist first, only 0.2 patients required surgery, reducing associated deaths by 0.013 at the expense of 0.003 extra colonoscopy deaths. Compared with direct referral to surgery, referral to an expert endoscopist gained 0.2 QALYs and saved €12 500 per 1000 individuals in the target population.

Conclusion Referring patients with complex polyps to an expert endoscopist first reduced some surgery-related deaths while substantially improving cost-effectiveness of the screening program.

Introduction

Colorectal cancer (CRC) is the second leading cause of cancer-related death in the Western world [1]. Randomized controlled trials have shown that CRC screening can prevent deaths by detecting CRC at an earlier stage or by detecting and removing polyps that can be precursors to CRC [2]. Therefore, organized population-based CRC screening programs have been established worldwide. Many of these programs use fecal immunochemical testing (FIT) as a primary test, with referral to colonoscopy as a follow-up [3].

While most of the detected polyps in screening programs can be removed endoscopically, some complex nonmalignant polyps are referred for surgical resection [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20]. This is due to their large size, flat shape, location, or suspected submucosal invasion, which is a sign of malignant behavior. The negative impact of complex nonmalignant polyp surgery has been studied previously, and has shown that surgery for such polyps is associated with morbidity, mortality, and cost, which may eliminate the (cost-)effectiveness of screening programs. Because many CRC screening programs have been introduced recently, an increase in detection of complex nonmalignant polyps is expected.

The practice of surgery for complex nonmalignant polyps is debated [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20]. Several studies suggest that patients diagnosed with these polyps should first be referred to an endoscopist with experience in visual diagnosis and resection of complex nonmalignant polyps. Successful removal by the expert endoscopist may reduce surgery-related mortality, morbidity, and cost. However, endoscopic removal may harm patients if complex nonmalignant polyps are not resected radically and are subsequently diagnosed with CRC originating from this polyp. In addition, locoregional lymph nodes are not removed. The impact of management of complex polyps on screening effectiveness is currently unknown.

In this study, we estimated the impact of surgery for complex nonmalignant polyps on the (cost-)effectiveness of the Dutch national CRC FIT screening program and evaluated the extent to which referral to an expert endoscopist first is more cost-effective.

Methods

We used the Microsimulation Screening Analysis (MISCAN)-Colon model to simulate two management strategies for complex nonmalignant polyps in the Dutch national CRC screening program. The first strategy incorporated surgery only. The second strategy incorporated referral to an expert endoscopist first, with referral to surgery if the expert endoscopist was unsuccessful in removing the complex polyp. We compared the burden and (cost-)effectiveness of the two strategies.

MISCAN-Colon

MISCAN-Colon is a microsimulation model for CRC developed at the Department of Public Health of the Erasmus Medical Centre (Rotterdam, the Netherlands). The model’s structure, underlying assumptions, calibration, and validation have been described in previous publications [21] and are summarized in Supplement 1 of the online-only Supplementary material. In brief, MISCAN-Colon simulates the life histories of a large population of individuals from birth to death. As each simulated individual ages, one or more adenomas may develop. These adenomas can progress in size from small (≤ 5 mm in diameter) to medium (6–9 mm) to large (≥ 10 mm). Some adenomas can develop into preclinical cancer, which may progress through stages I to IV. During each stage, CRC may be diagnosed because of symptoms. Survival after clinical diagnosis is determined by the stage at diagnosis, the location of the cancer, and the person’s age.

Screening will alter some of the simulated life histories: some cancers will be prevented by the detection and removal of adenomas; other cancers will be detected at an earlier stage with more favorable survival. However, screening can also result in serious complications, overdiagnosis, and overtreatment. The morbidity, mortality, and costs caused by colonoscopy complications and CRC treatment are already incorporated into MISCAN-Colon. For the current study, we also incorporated the patient burden and harms caused by surgery for complex nonmalignant polyps. By comparing life histories following screening with the corresponding life histories without screening, MISCAN-Colon quantifies the effectiveness and efficiency of screening.

MISCAN-Colon is calibrated using Dutch age-, stage-, and location-specific CRC incidence and survival data, together with data on adenoma prevalence and size distribution. The validity of the MISCAN-colon model has been demonstrated using the results of large screening and surveillance studies. Details regarding the quantification of the model validation and calibration are described in Supplement 1.

Population and screening program simulated

We simulated the Dutch population from 2014 with age distribution and life expectancy in accordance with data from Statistics Netherlands [22]. Subsequently, we simulated the Dutch CRC screening program according to its observed implementation and design. The program started in 2014, with a gradual increase in the number of invited age cohorts during the initial phase (2014–2018). The simulated population was offered biennial FIT (screening between ages 55 and 75 years) with a cutoff of 47 μg Hb/g feces (in accordance with the real-world program, the initial cutoff simulated in 2014 was 15 μg Hb/g, and this was raised to 47 μg Hb/g after 6 months. The reason for the cutoff increment has been described elsewhere [23]). FIT characteristics were calibrated to the positivity rates and detection rates of CRCs and adenomas as observed in the first screening round of the screening program [24]. Those with a positive test were offered a colonoscopy. Details regarding sensitivity, specificity, and reach of FIT and follow-up colonoscopies can be found in Supplement 2. We simulated age-specific adherence rates for the first round of FIT screening and follow-up colonoscopy as observed in the Dutch CRC screening program in 2014–2016 (Supplement 2). Participants in whom adenomas were removed were assumed to undergo colonoscopy surveillance according to Dutch guidelines [25].

Scenarios for management of complex nonmalignant polyps

We defined complex nonmalignant polyps as adenomas that were detected during follow-up colonoscopy after a positive FIT but could not be removed by the endoscopist. Results from the CORERO-trial (personal communication trial leaders) [26] indicated that this was the case for 3.9 % of large adenomas detected at screening. We incorporated this percentage for complex nonmalignant polyps into MISCAN-Colon.

In the first scenario, we estimated the impact on costs and benefits of direct referral to surgery of all patients with complex nonmalignant polyps ([Table 1], [Fig. 1a]). In the second scenario, we evaluated the impact if these patients were first referred to an expert endoscopist ([Table 1], [Fig. 1b]). We defined an expert endoscopist as an endoscopist performing high numbers of complex polyp removals and who is therefore expected to have a higher success rate than endoscopists performing none or low numbers of complex polyp removals. We defined an expert colonoscopy as a colonoscopy performed by an expert endoscopist. We assumed that the nonmalignant nature of the polyp was not completely certain at the time of referral to an expert endoscopist. We assumed that 4.6 % of all screen-detected CRCs were misclassified as nonmalignant and referred for expert endoscopic removal. We based this percentage on the rate of nonmalignant vs. malignant polyps removed by the expert endoscopist in Friedland et al. [4].

We considered referral to an expert endoscopist to be successful when the polyp was considered completely removed by the expert endoscopist and the resected specimen was confirmed as nonmalignant by pathology examination. This was the case in 71 % of the referrals in Friedland et al. We assumed that for half of successful referrals, two expert colonoscopies were needed [4]. In addition, we assumed that the patients with these nonmalignant polyps received an extra surveillance colonoscopy for inspection of the scar [4]. We assumed that in 6 % of those patients, the resection was not radical after all, such that 0.2 % of all patients with referred complex nonmalignant polyps developed CRC within 2 years ([Fig. 1b]) [27]. For the remaining 29 % of patients with unsuccessful referrals, we distinguished three groups, based on Friedland et al. [4]: 1) patients with nonmalignant complex polyps that were, by visual inspection of the expert endoscopist, suspected to be malignant or considered too difficult to remove (11 %). We assumed that these polyps were referred to surgery and after surgery it was concluded from pathological examination of the specimen that the patient had a nonmalignant polyp; 2) patients with malignant complex polyps that were correctly diagnosed, by visual inspection of the expert endoscopist, as malignant (11 %); 3) patients in whom complex polyps were removed by the expert endoscopist that were later diagnosed by pathological examination as malignant (8 %). The estimate of 71 % successful referrals is equal to an estimate of 87 % successful referrals of nonmalignant polyps: 71 % divided by the total percentage of referred nonmalignant polyps (71 % removed plus 11 % not removed). In the base case, we assumed that all unsuccessful referrals received surgery after all, and that referral to an expert endoscopy first did not impact the prognosis of these patients.

Complications with colonoscopy and surgery

Considering only colonoscopy complications necessitating hospitalization or presentation at an emergency department, we assumed a complication rate of 0.24 % and a fatality rate of 0.00329 % for a regular colonoscopy with polypectomy (Supplement 2). We assumed a complication rate of 8.0 % for the expert colonoscopy in cases of polypectomy of a complex nonmalignant polyp [27]. For expert colonoscopies, we assumed that the fatality rate per complication was the same as for follow-up colonoscopies; this resulted in a fatality rate of 0.11 % per expert colonoscopy [28]. For surgery, we assumed a risk of perioperative death of 0.7 % [5].

Utility losses

We assumed no utility loss for an FIT, a utility loss equal to 2 days per colonoscopy with or without removal of a complex polyp (0.0055 QALYs), and a utility loss of 2 weeks per colonoscopy complication (0.0384 QALYs). We also assigned a utility loss to each life-year with CRC care (Supplement 2). Furthermore, we assumed that the utility loss for patients due to surgery of complex nonmalignant polyps was equivalent to the average utility loss in the first year after CRC stage I diagnosis (i. e. 0.12 QALYs). This utility loss includes patient burden by complications.

Costs

We included screening and treatment costs from a third-party payer perspective (Supplement 2). We based our cost estimation for diagnostic and expert colonoscopies on the rates in 2020 from the Dutch Health Care Authority. We assumed the surgery costs for complex nonmalignant polyps per patient to be equivalent to the average treatment costs per surgically treated patient in the first year of CRC stage I.

Outcomes

We estimated annual and lifetime outcomes of the Dutch CRC screening program, comparing surgery for complex nonmalignant polyps with expert colonoscopy first for these polyps. First, we estimated the annual results of the first 10 years of the Dutch FIT-based screening program, including the estimated annual number of colonoscopies, (fatal) complications from colonoscopy, complex nonmalignant polyps detected, surgeries for complex nonmalignant polyps, (fatal) complications from this surgery and from expert colonoscopy.

Second, we estimated the following lifetime outcomes of CRC screening: CRC cases and deaths prevented, (fatal) complications from colonoscopy and surgery, QALYs gained, and costs of the Dutch CRC screening program compared with no screening per 1000 population. When appropriate, we calculated the incremental cost-effectiveness ratio (ICER), using the Dutch willingness-to-pay threshold of €20 000. Costs and QALYs were discounted at an annual rate of 3 % from 2014 onwards. Outcomes were compared between both scenarios of management of complex nonmalignant polyps.

Sensitivity analyses

Given uncertainty in our assumptions, we performed one-way sensitivity and threshold analyses for all key assumptions ([Table 1], Supplement 2), as well as a probabilistic sensitivity analysis (PSA) (Supplement 3).

Results

Prediction of annual outcomes in the Dutch CRC Screening Program (2014–2023)

In 2014, the first year of the screening program, the model predicted that 0.8 million people were invited to the program, of whom 0.5 million participated ([Table 2]). These numbers increased to the level of 2.2 million invitees and 1.6 million participants by 2023. Per 100 000 participants in screening, the number of colonoscopies decreased from 6185 in 2014 to 4148 in 2023.

When all complex nonmalignant polyps were directly referred for surgery, 111 surgeries for complex nonmalignant polyps were performed in 2014, per 100 000 participants in screening. The number of surgeries decreased to 44 in 2023. Similarly, 0.78 deaths due to surgery for complex nonmalignant polyps occurred in 2014, decreasing to 0.31 in 2023 ([Fig. 2]).

If complex nonmalignant polyps were first referred to an expert endoscopist, in 2014 352 expert colonoscopies were performed (including follow-up colonoscopies after first attempt), decreasing to 141 in 2023 ([Table 2]). Together with the additional follow-up and surveillance colonoscopies needed, this scenario required 4 % more colonoscopies than the surgery scenario in 2014, decreasing to 2.7 % in 2023 in the Dutch CRC screening program. Consequently, in the program the total number of colonoscopy complications increased by 87 % in 2014, and by 50 % in 2023. Conversely, the number of surgeries and associated deaths were lower in this scenario, by 87 % ([Fig. 2]).

Prediction of lifetime outcomes of the Dutch CRC Screening Program

We estimated that without screening 67.0 CRC cases would have been diagnosed per 1000 individuals over their lifetimes, 37.3 CRC deaths would have occurred, 191 QALYs would have been lost, and CRC treatment would have cost €873 100.

With the implementation of the screening program, 11.2 of the 67.0 CRC cases were prevented (–16.7 %) and 10.1 of the 37.3 CRC deaths were prevented (–27.1 %). Consequently, 32.9 QALYs of the 191 QALYs lost to CRC were saved (+ 17.2 %) per 1000 individuals. The cost of surgery for complex nonmalignant polyps was €19 100 per 1000 individuals. Total extra costs (including those of screening, surveillance, and treatment) of the screening program compared with a situation without screening were €72 700. Regarding the necessary resources for the program, we estimated that 122.5 follow-up and 110.9 surveillance colonoscopies would be performed per 1000 individuals in the population during their lifetimes ([Table 3]). In addition, 0.6 colonoscopy complications occurred, of which 0.008 were fatal. A total of 2.1 surgeries for complex nonmalignant polyps were performed, with 0.015 fatal incidents per 1000 individuals.

Referring individuals with complex nonmalignant polyps to an expert endoscopist first before considering surgery resulted in negligible changes in the number of prevented CRC cases and CRC deaths ([Table 2]). The number of QALYs gained increased from 32.9 to 33.1 (+ 0.6 %) per 1000 individuals. Although expert colonoscopies incurred an additional cost of €4600, costs for surgery decreased from €19 100 to €1900, and referral to an expert endoscopist thus resulted in a net savings of €12 500 per 1000 individuals. This is a savings of 17.1 % compared with the scenario of surgery only. Consequently, the management of complex nonmalignant polyps with expert endoscopy first was found to be more cost-effective than surgery only. We estimated that over a lifetime, 6.4 extra colonoscopies per 1000 individuals were needed. Consequently, the number of complications from colonoscopy increased by 0.2 and the number of fatalities by 0.003. On the other hand, the number of surgeries for complex nonmalignant polyps decreased by 1.9 and the number of associated deaths decreased by 0.013.

One-way sensitivity analyses

With higher and lower assumed values of the various parameters in the sensitivity analysis, cost and utility loss altered proportionally or less than proportionally (Supplement 2). The sensitivity analyses did not alter the conclusion that referral of complex nonmalignant polyps to an expert endoscopist first gained more QALYs and cost less compared with immediate referral to surgery.

Threshold analysis and PSA

Direct referral to surgery could only become a cost-effective management strategy if the cost for surgery decreased by over 70 % or the cost for expert colonoscopy increased by more than fivefold (Supplement 2). Varying the remaining assumptions within plausible limits did not result in surgery only being identified as a cost-effective strategy. The PSA showed that referral to expert endoscopy for suspected complex nonmalignant polyps was preferrable to direct referral to surgery in 99.7 % of all instances, as it was consistently associated with lower costs and more QALYs gained ([Fig. 3]).

Discussion

Our analyses demonstrated that the negative impact of surgery for complex nonmalignant polyps on CRC screening effectiveness was modest, as only a few patients will be diagnosed with complex nonmalignant polyps relative to a large numbers of CRC deaths prevented and QALYs gained by screening. However, despite the low number of patients, the impact of this practice can be substantial on program costs. The approach of first referring patients with complex nonmalignant polyps to an expert endoscopist for attempted endoscopic polyp removal led to a substantial improvement in the cost-effectiveness of CRC screening. Sensitivity analyses showed that cost savings of referral to an expert endoscopist compared with surgery were highly robust for alternative assumptions.

This study provides three additional insights. First, the study showed that the number of deaths due to surgery for complex nonmalignant polyps may be about two times higher than the number of deaths due to colonoscopy complications. While complications and fatalities due to follow-up colonoscopies are routinely registered in screening programs [29], management of complex nonmalignant polyps occurs outside the structure of organized screening programs, and its complications and fatalities are therefore not routinely registered in these programs [30] [31]. Second, the negative impact of complex nonmalignant polyp surgeries is largest in the implementation phase of a CRC screening program, because screening occurs in a screen-naïve population. Age-specific prevalence of advanced neoplasia overall, including complex nonmalignant polyps, is higher in screen-naïve individuals than in individuals who have already attended one or more CRC screening rounds previously [32]. Third, the predicted number of extra expert colonoscopies relative to the total number of colonoscopies performed in the screening program is modest, even in the implementation years.

Our findings are in line with previous studies comparing endoscopic resection versus surgery of complex polyps [15] [16] [17] [18] [19] [20] (see also Supplement 4). The current findings provide three important additions to the literature. First, we quantified the impact on the cost-effectiveness of a CRC screening program. Second, we incorporated long-term risks of incomplete treatment of nonmalignant polyps. Third, we incorporated potential worse outcomes for patients with misclassified malignant polyps that were referred to an expert endoscopist first. Despite these strengths, some limitations are noteworthy. First, several underlying model assumptions are uncertain. For instance, the expert endoscopist success rate of 71 % (87 % when considering only nonmalignant polyps) was based on a small study by Friedland et al. [4]. Other studies involving expert endoscopies demonstrated higher success rates of over 90 % [8]; however, such studies included patients treated at tertiary centers for complex polyps that may have been, on average, less complex and appeared less malignant than the complex polyps that are referred directly to surgery by screening endoscopists [9] [10] [11]. In Friedland et al., patients with polyps were already referred to surgery, and afterwards these polyps were reassessed by an expert endoscopist at the request of the surgeon. A more conservative approach is therefore needed. In a study by Saade et al., which had a design similar to the current study, the expert endoscopy success rate was estimated to be lower, at 80 % [13]. Even with our conservative approach, the practice of expert colonoscopy was highly cost-effective. Our sensitivity analyses showed that our conclusions were highly robust for variability in the success rate. Second, we did not vary the complication and mortality rates with age. Third, due to the model structure, we varied referral rate to surgery as a proportion of polyps ≥ 10 mm in size, whereas most difficult polyps are defined as ≥ 20 mm; however, we consider that presenting the referrals as a proportion of ≥ 10 mm polyps still provides valid estimates. Finally, the estimated 3.9 % of complex nonmalignant polyps referred to surgery may have been an overestimate, as techniques and skills of endoscopists may have improved; however, a review of the literature did not indicate that this percentage has increased [14] (see also Supplement 5). Moreover, in our sensitivity analyses we demonstrated that our analyses were highly robust to variations in this percentage.

Notwithstanding these limitations, this study has four important implications for current practice. First, to support accurate decision making, it is necessary to register and monitor surgery referrals of complex polyps and associated mortality in a large-scale screening program; the same holds for the success rate of expert colonoscopies and associated mortality. Second, decision analyses evaluating the benefits and harms of screening should include the management of complex polyp. Third, this management should be incorporated into all CRC screening guidelines. Finally, a training program for a selection of endoscopists to learn to remove complex nonmalignant polyps and distinguish them from malignant polyps is currently lacking [7]; such a program could potentially gain QALYs and reduce costs.

The implications of our findings go beyond large screening programs, as surgery for nonmalignant polyps is performed outside of the screening setting [10] [11]. Moreover, although the impact on mortality in a screening program is modest, for an individual patient with a complex polyp, this impact is highly relevant. This practice has not yet fully changed for several reasons, including insufficient knowledge of advanced methods for polyp removal by endoscopists, fear of malignancy, and lack of availability of expert endoscopists in the patient’s geographic area [9] [10] [11] [12]. Meanwhile in many countries, waiting lists for surgery exist.

In conclusion, our study demonstrated that although the impact of surgery for complex nonmalignant polyps on the long-term effectiveness of a CRC screening program was modest, referring patients with complex nonmalignant polyps first to an expert endoscopist reduced the harms from screening and could substantially improve the cost-effectiveness of the screening program. With implementation of guidelines on the management of complex nonmalignant polyps and active monitoring of outcomes, deaths may be prevented and money can be saved.

Funding

Dutch National Institute for Public Health and the Environment (RIVM)

Competing interests

The authors declare that they have no conflict of interest.

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Corresponding author

Publication History

Received: 04 May 2021

Accepted: 29 November 2021

Article published online:
07 February 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

• References

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