Cost-utility analysis of colonoscopy or faecal immunochemical test for population-based organised colorectal cancer screening

Abstract

Background

Organised programmes for colorectal cancer screening demand a high burden of medical and economic resources. The preferred methods are the faecal immunochemical test and primary colonoscopy.

Objective

The purpose of this study was to perform an economic analysis and comparison between these tests in Europe.

Methods

We used a Markov cost-utility analysis from a societal perspective comparing biennial faecal immunochemical test or colonoscopy every 10 years screening versus non-screening in Portugal. The population was screened, aged from 50–74 years, and efficacy was evaluated in quality-adjusted life years. For the base-case scenario, the faecal immunochemical test cost was €3 with 50% acceptance and colonoscopy cost was €397 with 38% acceptance. The threshold was set at €39,760/quality-adjusted life years and the primary outcome was the incremental cost-effectiveness ratio.

Results

Screening by biennial faecal immunochemical test and primary colonoscopy every 10 years resulted in incremental utilities of 0.00151 quality-adjusted life years and 0.00185 quality-adjusted life years at additional costs of €4 and €191, respectively. The faecal immunochemical test was the most cost-effective option providing an incremental cost-effectiveness ratio of €2694/quality-adjusted life years versus €103,633/quality-adjusted life years for colonoscopy. Colonoscopy capacity would have to increase 1.3% for a faecal immunochemical test programme or 31% for colonoscopy.

Conclusion

Biennial faecal immunochemical test screening is better than colonoscopy as it is cost-effective, allows more individuals to get screened, and provides a more rational use of the endoscopic capacity available.

Keywords

Cost analysis cost-benefit analysis colorectal neoplasms early detection of cancer cancer screening occult blood colonoscopy

Key summary

Established knowledge on this subject

Colorectal cancer screening implementation is markedly different among countries.

The two preferred methods are faecal immunochemical test (FIT) and primary colonoscopy.

Many cost-effectiveness studies used unrealistic 100% adherence rates for the screening tests.

What are the significant and/or new findings of this study?

Under realistic worldwide adherence rates, biennial FIT screening is a more cost-effective choice than colonoscopy every 10 years.

A FIT programme also allows more individuals to get screened and provides a more rational use of endoscopic capacity (13,050 colonoscopies/year/million screened) than a colonoscopy programme (47,500 colonoscopies/year/million screened).

Our results support the progressive implementation of FIT-based programmes in Europe.

Introduction

Colorectal cancer (CRC) is a worldwide problem due to its high incidence and increasing burden reflecting population's growth, aging and lifestyle.¹ It is the second greatest cause of cancer mortality in Europe and the first in Portugal, representing nearly 16% of all cancer-related deaths.² Several European countries have already implemented population-based CRC screening programmes mainly based on the use of the faecal immunochemical test (FIT), due to higher accuracy and acceptability of such test, compared with previous guaiac-based faecal test. On the other hand, in the USA, as well as in a few European countries (such as Germany and Poland), a primary screening colonoscopy strategy is advocated at population level, due to the higher accuracy of such test for precancerous lesions.^3–5

Accuracy, however, is not necessarily the main determinant when choosing between a FIT or a primary colonoscopy approach, as other factors such as the acceptability of the test, costs and limited endoscopic capacity may play a critical role in the decision-making process. In addition, available clinical evidence is generally restricted to one-time testing, either with FIT or colonoscopy, while these tests are expected to be repeated at regular intervals with cumulative estimates of efficacy that are too complex to be simply derived from the outcomes of such trials.

Simulation models may attempt to address such uncertainty, by simultaneously considering the key factors required in the decision process, allowing a long-term estimation of life expectancy increase, as well as budget savings between screening costs and decreasing treatments.⁶ Although previous modelling has already addressed the comparison between FIT and colonoscopy, this was diluted in a more general comparison among several screening strategies, avoiding a clear and informative comparison between these two tests that are now implemented worldwide.^7–15

Primary aim of our analysis was to perform a cost-utility analysis in a European country, to compare a population-based CRC screening programme with FIT or primary colonoscopy versus no screening. Secondary aims were to explore the influence of adherence rates and costs on such cost-utility ratio, and to evaluate its impact on health resources, namely on the annual capacity for performing colonoscopies.

Materials and methods

Study population

Portuguese adults from age 50–74 years were considered at risk for developing CRC and were modelled in a cost-utility analysis comparing colorectal screening on a population-based nationwide programme versus no screening, according to European Union recommendations.^3,4 Two alternatives for screening were considered: biennial FIT followed by colonoscopy if positive (≥100 ng/ml or 20 µg/g) or primary colonoscopy every 10 years.^3,4 This means that for every 10 years of the screening programme, a patient with consecutive negative FIT tests would account for the costs of five FIT tests while a patient with a negative primary colonoscopy would account for the cost of one colonoscopy.

A societal perspective was adopted by including the costs to the healthcare system, patients, families and employers, in accordance with recommendations for cost-effectiveness analysis reporting.¹⁶

Model structure

A Markov model with a one-year cycle was chosen to compare both screening strategies (FIT or colonoscopy) versus no screening as reported in Supplementary Material Figure 1. Briefly, in the natural history model, we simulated three main states, namely no CRC, CRC and CRC death, progression from one status to the next being based on registry data. In the screening simulation, we used literature-based estimates from large cohort or randomised trials to estimate the reduction in CRC incidence and mortality, while we used endoscopic studies to provide an estimate of the prevalence of polyps at screening colonoscopy (either post-positive FIT or at primary colonoscopy screening). Such information on polyp prevalence was used only to assess the cost related to polypectomy while, as already outlined, estimates on efficacy were purely related to the degree of CRC prevention shown in already published cohorts.

Figure 1.

Cost-utility analysis of faecal immunochemical test (FIT) or colonoscopy screening versus no screening. The x-axis represents the effectiveness in quality-adjusted life years (QALY) and the y-axis represents the cost in Euros (€). The cost-effectiveness frontier is represented by the black line between strategies showing that the best colorectal screening strategy is FIT, presenting a better combination of increased effectiveness and at lesser costs, providing an incremental cost effectiveness ratio of €2694/QALY, well below the threshold set at €39,760/QALY. For colonoscopy the incremental cost effectiveness ratio is €103,633/QALY.

The currency used is the Euro (€) and costs are given in 2017 prices. Prices from previous years were adjusted for inflation with an online conversion tool available from Pordata.¹⁷ The discount rate was set at 3% for all cost and effectiveness data for the base-case scenario, ranging in sensitivity analysis between 0–5% in accordance with published guidelines that were used for reporting of this economic evaluation.^16,18–21 The software used was TreeAge Pro 2009 (TreeAge Software, Williamstown, Massachusetts, USA).

Clinical data

Clinical probabilities were obtained after an extensive review of the literature to find the best available estimates for rates of adherence to screening tests; distribution by cancer stage; colonoscopy efficacy, polyp detection, removal and complications; colorectal cancer treatments and adverse events; and disease-specific stage survival rates. This included average realistic adherence rates for screening tests and available ranges, from European and North American publications, namely FIT adherence rates between 35–68% and colonoscopy adherence rates between 18–38%.^7,22–24

Efficacy was evaluated in terms of CRC prevention and mortality reduction by detection of CRC in earlier stages of disease with better survival rates.

Cost data

Costs were estimated from Portuguese national sources for screening and surveillance costs (FIT, colonoscopy and bowel preparation, including the user fees if applicable, but without administrative related costs), healthcare state costs (depending on location of cancer in colon versus rectum, disease-stage and available treatments), adverse event costs (for colonoscopy, but also for colorectal cancer treatments such as surgery, chemotherapy or radiotherapy) and indirect costs (working days lost, visits to healthcare personnel and transport). No assumptions were made on issues such as dedicated nurse time, time lost for relatives or caregivers, or productivity changes.

For the current no screening strategy, costs are mainly derived from CRC treatments and further surveillance; for the FIT screening strategy, the FIT cost plus the colonoscopy cost (endoscopic exam plus bowel preparation) after a positive FIT test were added, while for the primary colonoscopy screening strategy the colonoscopy cost (endoscopic exam plus bowel preparation) was considered.

For the costs of both screening tests, some assumptions were made to allow a wide range of variation. As such, the colonoscopy cost was modelled with two values: €397 for the base-case setting (price already published to be paid for a colonoscopy with anaesthesia under a national screening colorectal cancer programme),²⁵ but also €150 which is the current price for an opportunistic colonoscopy with anaesthesia paid by the health service; FIT cost was modelled between €3–30, to accommodate a wider range with a very low base-case cost.

Assumptions were made on costs for employers and transportation expenses since no data were available for the Portuguese population. Accordingly, employers' costs were based on the cost per hour reported by the Portuguese Institute of Statistics, while transport expenses were based on a broad estimate of the distance between home and hospital for the general population.

Utility data

Utilities were obtained from the literature providing values for quality of life adjusted for disease location in terms of colon versus rectum, and by stage of disease from stage I–IV.^26,27

Cost-utility analysis

The outcome measure was the incremental cost effectiveness ratio (ICER) between the screening strategies, FIT or colonoscopy, versus no screening. Costs were included in the numerator and effectiveness in the denominator, in terms of quality-adjusted life years (QALYs). The willingness to pay was set at €39,760/QALY adopting the threshold of twice the gross national income per capita, as recommended by the Commission for Macroeconomics and Health of the World Health Organization.^28–30

Data on clinical probabilities and range for both costs and utilities are provided in Supplementary Material Table 1. Every point estimate is accompanied by a range and a distribution, to account for variability and allow sensitivity analysis, using deterministic and probabilistic approaches. For sensitivity analysis, when only a single value was available in the literature, the range was calculated for a 10% deviation and this applied mainly to costs.³¹ For probabilistic analysis, all distributions were calculated using an approximation of the mean and standard deviation provided by the TreeAge software.

Table 1.

Results of the cost-effectiveness model for the base-case scenario.

Strategy	Cost	Incremental cost	Effectiveness	Incremental effectiveness	Cost/ effectiveness	Incremental cost/effectiveness (ICER)
No screening	€7.9		25.79076 QALY		0 €/QALY
FIT screening €3 vs no screening	€11.9	€4.1	25.79227 QALY	0.00151 QALY	1 €/QALY	€2694/QALY
Colonoscopy screening €150 vs no screening	€96.8	€89.2	25.79261 QALY	0.00185 QALY	4 €/QALY	€48,285/QALY
Colonoscopy screening €397 vs no screening	€199.4	€191.6	25.79261 QALY	0.00185 QALY	8 €/QALY	€103,633/QALY
Colonoscopy screening €397 vs FIT screening	€199.4	€187.5	25.79261 QALY	0.00034 QALY	8 €/QALY	€549,433/QALY

FIT: faecal immunochemical test; QALY: quality adjusted life year.

Results

According to our model, a FIT-based screening programme would provide a 30% reduction in CRC incidence and mortality, while a colonoscopy-based screening programme would provide a further 8% reduction with an average 38% reduction in the CRC incidence and mortality. In terms of effectiveness this means that a FIT screening programme would provide 0.00151 extra QALYs, while a colonoscopy screening programme would provide 0.00185 extra QALYs.

Regarding costs, the average cost for CRC per person with the current no screening strategy is €8 per person; with a FIT screening programme the average cost per person would be €12, while in a colonoscopy screening programme the average cost would be €199 per person. This means that a FIT-based screening programme would require an incremental cost of €4 per person while a colonoscopy-based programme would require an incremental €191 per person.

The ICERs of the model for the base-case scenario, comparing both screening strategies, are presented in Table 1. Compared to no screening, FIT screening at a cost of €3 per FIT test is cost-effective, presenting an ICER of €2694/QALY, well below the threshold set at €39,760/QALY. For colonoscopy at a price of €397, screening is not cost-effective due to its very high cost (although presenting more effectiveness), resulting in an ICER of €103,633/QALY, 2.5 times above the adopted threshold. These results are better represented in Figure 1, which demonstrates that FIT screening is the most cost-effective strategy. Even for a colonoscopy price of €150 (current price in Portugal), screening is not cost-effective providing an ICER of €48.285/QALY, still above the adopted threshold.

One-way sensitivity analysis according to the cut-off points defined for the FIT test, varying between (≥50 ng/ml or 10 µg/g) to (≥200 ng/ml or 30 µg/g), would make an ICER variation between €4653/QALY and €1530/QALY, respectively. Also, modelling the adherence rate for FIT showed that for rates between 35–62% the FIT screening is more cost-effective than primary colonoscopy but for rates ≥63%, the FIT option will dominate the colonoscopy option by providing even more QALYs than colonoscopy, at a lower cost.

Moreover, considering the need for repeating a colonoscopy until 10% (due to inability to reach the caecum or an inadequate bowel preparation), a sensitivity analysis shows that the ICER values would remain similar for both the FIT option (€2965/QALY instead of €2694) and the colonoscopy option (€549,252/QALY instead of €549,433).

Two-way sensitivity analysis on cost of both screening alternatives is shown in Figure 2(a), demonstrating that, to be cost-effective, the price for a primary colonoscopy would have to be below €95. Three-way sensitivity analysis on colonoscopy cost versus colonoscopy and FIT adherence rates is presented in Figure 2(b), showing that for colonoscopy to be cost-effective the acceptance rate would have to be 100% for a colonoscopy cost of €90. For a FIT acceptance above 55% or a colonoscopy price above €100, colonoscopy is never cost-effective.

Figure 2.

(a) Sensitivity analysis on costs of both screening strategies. The x-axis represents the cost of faecal immunochemical test (FIT) and the y-axis represents the cost of colonoscopy, both in Euros (€). For colonoscopy to be more cost-effective than FIT it would have to cost less than €95 and FIT above €60. (b) Sensitivity analysis on colonoscopy cost and adherence rates of both screening strategies. The x-axis represents the cost of colonoscopy in Euros (€) and the y-axis represents the adherence rate for colonoscopy screening, at the assumption of a FIT screening adherence rate of 40%. For colonoscopy to be cost-effective the adherence rate for FIT would have to be as low as 40% and the colonoscopy adherence rates above 65% (for a colonoscopy cost of €50) or 100% (for a colonoscopy cost of €90). For a FIT acceptance above 55% or a colonoscopy cost above €100, colonoscopy would never be cost-effective.

Deterministic sensitivity analysis, representing the influence of each variable on the ICER is shown in Figure 3 as a tornado diagram. The results show that the most prominent variables in the model were the costs of screening tests (FIT and colonoscopy); the probabilities related to changes in stages of CRC (that relate to the efficacy of screening) and the performance of the FIT test in terms of sensitivity, specificity and adherence rate. For the base-case scenario with realistic ranges of adherence rates for both FIT and colonoscopy (35–68% for FIT and 18–38% for colonoscopy), neither of these values changed the model's conclusion, favouring FIT screening.

Figure 3.

Tornado diagram. Variables tested in one-way sensitivity analysis are displayed on the y-axis while the x-axis represents the net monetary benefit for a willingness to pay (WTP) of €39,790/QALY, with variables having the widest range for the result with a wider line at the top. Variables are followed by the values of their range considered in the analysis. Variables not displayed were even less relevant for the model. The most relevant variables in the model were the costs of both screening tests, the probabilities related to changes in stages of colorectal cancer and rates of adherence to screening tests.

Monte Carlo probabilistic multi-way analysis is shown in Figure 4, through 1000 simulations of the model comparing the FIT option versus no screening. Each point corresponds to one simulation, and cost-effective results for a FIT-based screening programme are reported as points below the willingness-to-pay dotted threshold line, comprising 96% of all simulations. Figure 5 represents the acceptability curves showing the probability of each option to be the best cost-effective strategy, comparing the 96% probability for FIT screening with a 4% probability for the no-screening strategy and 0% for colonoscopy screening.

Figure 4.

Scatter plot for probabilistic Monte Carlo sensitivity analysis for the faecal immunochemical test (FIT) screening versus no screening. Representation of 1000 simulations where each dot means one simulation, the x-axis represents the incremental effectiveness in terms of quality-adjusted life years (QALYs) and the y-axis represents incremental costs in Euros (€). The ellipse surrounds the estimates that fall within the 95% confidence intervals. Cost-effective simulations are situated below the dotted line representing the willingness-to-pay threshold, set at €39,760/QALY and comprise 96% of all simulations.

Figure 5.

Acceptability curve comparing the screening strategies of faecal immunochemical test (FIT) or colonoscopy versus no screening. The x-axis represents the willingness-to-pay in Euros (€) per quality-adjusted life year (QALY) and the y-axis represents the probability of cost-effectiveness, ranging from 0–100%. From left to right the intersection of the FIT screening line with the no screening line represents the point where the option for FIT screening starts to have a probability above 50% to be more cost-effective, at an incremental cost effectiveness ratio (ICER) of €2694/QALY. The dotted vertical line set for a willingness-to-pay of €39,760/QALY shows that the FIT screening option has a 96% probability of being cost effective versus 4% for no screening and 0% for colonoscopy screening.

Regarding the extra capacity in colonoscopy performance per year to accommodate the demands of a new screening programme, the increase of extra colonoscopies to perform per year, depending on the option of a FIT or colonoscopy screening test is shown in Figure 6. The actual number of colonoscopies performed per year in Portugal is 375,000 and most of them for symptoms or therapeutics; assuming that 5–10% of the actual colonoscopies are already performed for an opportunistic screening, the option of a FIT screening programme with a 50% adherence rate would represent an increase in extra colonoscopies capacity by just 1.3%, while for a colonoscopy screening programme with an adherence rate of 38%, extra colonoscopies capacity would have to increase by 31%.

Figure 6.

Number of extra colonoscopies to perform per year depending on the option of faecal immunochemical test (FIT) or colonoscopy as a screening test. The lower brighter bar corresponds to the actual number of colonoscopies performed per year, most of them for symptoms, surveillance or therapeutics; the top darker bars corresponds to the increase in colonoscopies per year if a screening programme is in place, assuming that 5–10% of the colonoscopies are already performed for opportunistic screening. This means that for a FIT screening programme the extra colonoscopies capacity would rise just 1.3% while for a colonoscopy screening programme the extra colonoscopies capacity would have to rise by 31%.

An extrapolation on the extra capacity of colonoscopies per gastroenterologist, per week, according to the screening options is provided in Supplementary Material Tables 2.1 and 2.2, depending on the population aged 50–74 years-old and the number of available gastroenterologists. Both assume a mean of 48 working weeks per year and for the FIT screening every two years an adherence rate of 50%, a positivity rate of 6% and an adherence rate for colonoscopy after a positive test of 87%; for colonoscopy screening every 10 years a 38% adherence rate was used. In a country like Portugal, with around 3 m people aged 50–74 years and about 400 gastroenterologists, this means that a FIT screening programme would require an extra two colonoscopies per week per gastroenterologist (13,050 colonoscopies/year/m screened), while a colonoscopy screening programme would require seven extra colonoscopies per week per gastroenterologist (47,500 colonoscopies/year/m screened).

Discussion

CRC is particularly suitable for screening and prevention of death, considering its long latency of progression, providing an excellent window of opportunity for early detection. The existence of available screening methods with adequate sensitivity and specificity rates, acceptable by an asymptomatic population and with few side effects, makes it the perfect oncological disease to be detected early or even prevented by screening. In Portugal, three regional pilot programmes based on FIT-screening are currently in place while Health government decisions are waited for a national population-based CRC screening programme.

The choice between screening tests should take in to account costs for the society, due to the large number of negative tests in asymptomatic people. On the other hand, effectiveness of detection and removal of polyps, preventing the disease's natural progression and early detection of an asymptomatic cancer would allow less invasive and costly treatments.

The present model for the Portuguese population compared the two most-used screening strategies for CRC in Europe, FIT and colonoscopy, and our results show that both strategies are effective compared to no screening. Moreover, in our study both screening strategies provide clinical relevant reductions in CRC incidence and mortality after 25 years of a screening programme in place. These results are in accordance with published results that report for faecal tests screening reductions between 15–35% at 30 years of follow-up^24,32–35 (30% in our model), while for primary endoscopic screening reduction rates are between 18–34% at 12 years for sigmoidoscopy and between 29–61% at 24 years for colonoscopy (38% in our model at 25 years).^34–37

Additionally, biennial FIT screening is the most cost-effective option. The ICER of just €2,694/QALY is far below the threshold of €39,760/QALY, even for a colonoscopy cost of €397 per exam. Also, the increase in colonoscopy capacity warranted by such a screening programme would be only 1.3%. These outcomes assume realistic available adherence rates for both screening options, 50% for FIT and 38% for colonoscopy. Besides, they are based on the latest cost for a colonoscopy performed under a national screening programme defined by the Portuguese Government (€397).

Colonoscopy screening on the other hand, is very costly for its effectiveness, with an ICER of €103,633/QALY (at a cost of €397). Even if the current price of €150 for a colonoscopy under anaesthesia outside a screening programme was used, the corresponding ICER would be €48,285/QALY, still above the €39,760/QALY threshold. Also, such a screening programme would require an extra colonoscopy capacity of 31% compared to the actual capacity of the country.

Our conclusions were robust in sensitivity analyses as relevant variables such as costs of screening tests (FIT and colonoscopy), different FIT cut-offs, changes in stages of the detected cancers and performance of the screening tests (sensitivity, specificity or adherence rates) did not change the conclusions of the model, favouring FIT screening, as this programme remained cost-effective in 96% of the simulations.

Comparing our model to other relevant studies, the main difference relates to the assumed adherence rates in other models (Supplementary Material Table 3). All models that concluded in favour of colonoscopy screening, assumed perfect but unrealistic adherence rates of 100% for both FIT and colonoscopy,^12,13,15 or equal but again unrealistic 50% adherence rates for both tests.¹⁴ On the other hand, three models in favour of FIT screening used more realistic adherence rates of 50–68% for FIT and 38–40% for colonoscopy,^6,7,9,10,16 while two others again used unrealistic similar adherence rates of 100% or 63% for both screening tests.^8,11 Of all these studies, both from the European setting favoured FIT screening versus colonoscopy, similar to our conclusion.^7,10 No screening programme exists with a perfect 100% adherence rate; also there is no published data with the same adherence rate for FIT and colonoscopy in the same population.

However, limitations to the present study need to be mentioned. Although an extensive literature research was performed for the best available evidence, studies on quality of life of patients with CRC specific for the Portuguese population are lacking. Ranges and distributions for some variables in sensitivity analysis are not available in the literature and estimates were used using the TreeAge software; it is crucial to recall that the model was conceived for the Portuguese population and adjustments need to be made for other populations to prove its generalisability.

In conclusion, biennial FIT screening for CRC is more cost-effective than primary colonoscopy screening in Portugal, presenting as a screening strategy affordable to the society, robust for a wide range of relevant clinical and cost variables and not requiring an extraordinary demand in extra colonoscopy capacity. This further supports the progressive implementation of FIT-based programmes in Europe. Future studies in other countries using realistic adherence rates are needed, to corroborate our conclusions.

Supplemental Material

Supplemental material for Cost-utility analysis of colonoscopy or faecal immunochemical test for population-based organised colorectal cancer screening

Supplemental material for Cost-utility analysis of colonoscopy or faecal immunochemical test for population-based organised colorectal cancer screening by Miguel Areia, Lorenzo Fuccio, Cesare Hassan, Evelien Dekker, António Dias-Pereira and Mário Dinis-Ribeiro in United European Gastroenterology Journal

Footnotes

Acknowledgements

The authors provided the following author contribution information: guarantor of article: M Areia. M Areia and M Dinis-Ribeiro created the model and conducted the systematic search. L Fuccio, C Hassan, E Dekker and A Dias-Pereira, verified model consistency and checked for coherence of results. M Areia wrote the manuscript. L Fuccio, C Hassan, E Dekker, A Dias-Pereira and M Dinis-Ribeiro provided a critical review of the manuscript. All authors approved the final version of the manuscript.

Declaration of conflicting interests

None declared.

Funding

This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Ethics approval

Not applicable.

Informed consent

Not applicable.

References

Jemal

Bray

Center

et al.

Global cancer statistics. CA Cancer J Clin 2011; 61: 69–90.

Ferlay

Steliarova-Foucher

Lortet-Tieulent

et al.

Cancer incidence and mortality patterns in Europe: Estimates for 40 countries in 2012. Eur J Cancer 2013; 49: 1374–1403.

von Karsa

Patnick

Segnan

. European guidelines for quality assurance in colorectal cancer screening and diagnosis. First edition – executive summary. Endoscopy 2012; 44: SE1–SE8.

Lansdorp-Vogelaar I, von Karsa L and International Agency for Research on Cancer. European guidelines for quality assurance in colorectal cancer screening and diagnosis. First edition – introduction. Endoscopy 2012; 44: SE15–SE30.

Schreuders

Ruco

Rabeneck

et al.

Colorectal cancer screening: A global overview of existing programmes. Gut 2015; 64: 1637–1649.

Arrospide

Idigoras

Mar

et al.

Cost-effectiveness and budget impact analyses of a colorectal cancer screening programme in a high adenoma prevalence scenario using MISCAN-Colon microsimulation model. BMC Cancer 2018; 18: 464.

Aronsson

Carlsson

Levin

et al.

Cost-effectiveness of high-sensitivity faecal immunochemical test and colonoscopy screening for colorectal cancer. Br J Surg 2017; 104: 1078–1086.

Heitman

Hilsden

et al.

Colorectal cancer screening for average-risk North Americans: An economic evaluation. PLoS Med 2010; 7: e1000370.

Kingsley

Karanth

Revere

et al.

Cost effectiveness of screening colonoscopy depends on adequate bowel preparation rates – a modeling study. PloS One 2016; 11: e0167452.

10.

Hassan

Benamouzig

Spada

et al.

Cost effectiveness and projected national impact of colorectal cancer screening in France. Endoscopy 2011; 43: 780–793.

11.

Ladabaum

Mannalithara

. Comparative effectiveness and cost effectiveness of a multitarget stool DNA test to screen for colorectal neoplasia. Gastroenterology 2016; 151: 427–439.e426.

12.

Telford

Levy

Sambrook

et al.

The cost-effectiveness of screening for colorectal cancer. CMAJ 2010; 182: 1307–1313.

13.

Coldman

Phillips

Brisson

et al.

Using the Cancer Risk Management Model to evaluate colorectal cancer screening options for Canada. Curr Oncol 2015; 22: e41–e50.

14.

Dan

Chuah

Koh

et al.

Screening based on risk for colorectal cancer is the most cost-effective approach. Clin Gastroenterol Hepatol 2012; 10: 266–271. .

15.

Knudsen

Lansdorp-Vogelaar

Rutter

et al.

Cost-effectiveness of computed tomographic colonography screening for colorectal cancer in the Medicare population. J Natl Cancer Inst 2010; 102: 1238–1252.

16.

Husereau

Drummond

Petrou

et al.

Consolidated Health Economic Evaluation Reporting Standards (CHEERS) – explanation and elaboration: A report of the ISPOR Health Economic Evaluation Publication Guidelines Good Reporting Practices Task Force. Value Health 2013; 16: 231–250.

17.

Pordata. Pordata, https://www.pordata.pt/PortugalHome.aspx (accessed 28 February 2018).

18.

Russell

Gold

Siegel

et al.

The role of cost-effectiveness analysis in health and medicine. Panel on Cost-Effectiveness in Health and Medicine. JAMA 1996; 276: 1172–1177.

19.

Weinstein

Siegel

Gold

et al.

Recommendations of the Panel on Cost-effectiveness in Health and Medicine. JAMA 1996; 276: 1253–1258.

20.

Siegel

Weinstein

Russell

et al.

Recommendations for reporting cost-effectiveness analyses. Panel on Cost-Effectiveness in Health and Medicine. JAMA 1996; 276: 1339–1341.

21.

Smith

Gravelle

. The practice of discounting in economic evaluations of healthcare interventions. Int J Technol Assess Health Care 2001; 17: 236–243.

22.

ASGE Fisher

Maple

et al.

Complications of colonoscopy. Gastrointest Endosc 2011; 74: 745–752.

23.

Centers for Disease Control and Prevention. Vital signs: Colorectal cancer screening test use–United States, 2012. MMWR Morb Mortal Wkly Rep 2013; 62: 881–888.

24.

Idigoras

Arrospide

Portillo

et al.

Evaluation of the colorectal cancer screening programme in the Basque Country (Spain) and its effectiveness based on the Miscan-colon model. BMC Public Health 2017; 18: 78.

25.

Portuguese Government. Tables of prices charged by the National Health Service (Portaria no. 207/2017). In: Portuguese Ministry of Health (ed.). Republic Diary: Portuguese Ministry of Health, 2017, pp. 3550–3708.

26.

Ness

Holmes

Klein

et al.

Utility valuations for outcome states of colorectal cancer. Am J Gastroenterol 1999; 94: 1650–1657.

27.

Djalalov

Rabeneck

Tomlinson

et al.

A review and meta-analysis of colorectal cancer utilities. Med Decision Making 2014; 34: 809–818.

28.

Garber

Phelps

. Economic foundations of cost-effectiveness analysis. J Health Econ 1997; 16: 1–31.

29.

Sachs JD. Macroeconomics and health: Investing in health for economic development. Geneva: World Health Organization, 2001.

30.

Tan-Torres Edejer T, Baltussen R, Adam T, et al. Making choices in health: WHO guide to cost-effectiveness analysis. 2003. Geneva: World Health Organization, 2003.

31.

Areia

Dinis-Ribeiro

Rocha Goncalves

. Cost-utility analysis of endoscopic surveillance of patients with gastric premalignant conditions. Helicobacter 2014; 19: 425–436.

32.

Ventura

Mantellini

Grazzini

et al.

The impact of immunochemical faecal occult blood testing on colorectal cancer incidence. Dig Liver Dis 2014; 46: 82–86.

33.

Zorzi

Fedeli

Schievano

et al.

Impact on colorectal cancer mortality of screening programmes based on the faecal immunochemical test. Gut 2015; 64: 784–790.

34.

Lin

Piper

Perdue

et al.

Screening for colorectal cancer: Updated evidence report and systematic review for the US Preventive Services Task Force. JAMA 2016; 315: 2576–2594.

35.

Lin JS, Piper MA, Perdue LA, et al. Screening for colorectal cancer: A systematic review for the U.S. Preventive Services Task Force. Report no. Evidence synthesis no. 135. Agency for Healthcare Research and Quality Publication No. 14-05203-EF-1. Rockville, MD, 2016.

36.

Brenner

Stock

Hoffmeister

. Effect of screening sigmoidoscopy and screening colonoscopy on colorectal cancer incidence and mortality: Systematic review and meta-analysis of randomised controlled trials and observational studies. BMJ 2014; 348: g2467.

37.

Nishihara

Lochhead

et al.

Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med 2013; 369: 1095–1105. .

Supplementary Material

Please find the following supplemental material available below.

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