PMCCPMCCPMCC

Search tips
Search criteria 

Advanced


 
Formats
Article sections
Authors
Related links
Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
 
Best Pract Res Clin Gastroenterol. Author manuscript; available in PMC 2011 August 1.
Published in final edited form as:
PMCID: PMC2939039
NIHMSID: NIHMS208585
Copyright notice and Disclaimer
Cost-effectiveness of colorectal cancer screening – an overview
Iris Lansdorp-Vogelaar, PhD,1 Amy Knudsen, PhD,2 and Prof. Hermann Brenner, MD, PhD3
1 Department of Public Health, Erasmus MC, University Medical Center Rotterdam, the Netherlands
2 Institute for Technology Assessment, Massachusetts General Hospital, Boston, Massachusetts, USA
3 Division of Clinical Epidemiology and Aging Research, German Cancer Research Centre, Heidelberg, Germany
Iris Lansdorp-Vogelaar, PhD (corresponding author), Erasmus MC, University Medical Center, Department of Public Health, PO Box 2040, 3000 CA Rotterdam, The Netherlands, Tel: +31-10-7043124, Fax: +31-10-7038474, i.vogelaar/at/erasmusmc.nl
Amy B. Knudsen, PhD, Massachusetts General Hospital, Institute for Technology Assessment, 101 Merrimac Street, 10th Floor, Boston, MA 02114, USA, Tel: +1-617-724-4445, aknudsen/at/mgh-ita.org
Prof. Herman Brenner, MD, PhD, German Cancer Research Centre, Division of Clinical Epidemiology and Aging Research, Bergheimer Str. 20, D-69115 Heidelberg, Germany, Tel: +49-06221-548140, Fax: +49-06221-548142, h.brenner/at/Dkfz-Heidelberg.de
Small right arrow pointing to: The publisher's final edited version of this article is available at Best Pract Res Clin Gastroenterol
Small right arrow pointing to: See other articles in PMC that cite the published article.
Publisher's Disclaimer
Abstract
There are several modalities available for a colorectal cancer (CRC) screening program. When determining which CRC screening program to implement, the costs of such programs should be considered in comparison to the health benefits they are expected to provide. Cost-effectiveness analysis provides a tool to do this. In this paper we review the evidence on the cost-effectiveness of CRC screening. Published studies universally indicate that when compared with no CRC screening, all screening modalities provide additional years of life at a cost that is deemed acceptable by most industrialized nations. Many recent studies even find CRC screening to be cost-saving. However, when the alternative CRC screening strategies are compared against each other in an incremental cost-effectiveness analysis, no single optimal strategy emerges across the studies. There is consensus that the new technologies of stool DNA testing, computed tomographic colonography and capsule endoscopy are not yet cost-effective compared with the established CRC screening tests.
Keywords: colorectal neoplasms, mass screening, cost-benefit analysis, occult blood, colonoscopy, sigmoidoscopy, colonography, computed tomographic, stool DNA, capsule endoscopy
The aim of population screening, such as colorectal cancer (CRC) screening, is to discover latent disease in its early stages to treat it adequately before it poses a threat to the individual.[1] As such, screening is a commendable method to fight disease. However, a screening program targets an (apparently) healthy population, and should therefore only be implemented after a careful consideration of both the harms and benefits of such a program. Cost-effectiveness analysis provides a tool to weigh and synthesize benefits, harms and costs of interventions and thus can inform the decision process for adopting population screening. In this paper we provide a brief overview of cost-effectiveness analysis and summarize the evidence on the cost-effectiveness of CRC screening in the average-risk population.
Cost-effectiveness analysis, a form of decision analysis, is an analytic tool that formally compares the health and economic consequences of different interventions, thereby assisting decision makers to identify the interventions that will yield the greatest health benefits, given their resource constraints.[2] Cost-effectiveness analysis cannot determine which the optimal intervention is, but rather which intervention will provide the greatest health benefits, given the decision maker’s willingness to pay for a unit of benefit. In a cost-effectiveness analysis, a mathematical model is typically used to track the benefits and harms of an intervention. These effects are then weighed against each other to determine the net benefit (or net harm). The model also tracks the costs associated with the intervention, including those of side effects. The results of a cost-effectiveness analysis are summarized in a cost-effectiveness ratio. The (quality-adjusted) life-years gained with a particular strategy (compared with an alternative) are included in the denominator, and the additional costs of that strategy (compared with the same alternative) are included in the numerator, yielding an incremental cost per (quality-adjusted) life-year gained.[2]
Two types of cost-effectiveness ratios are often reported in the literature: 1) a cost-effectiveness ratio comparing each intervention strategy with the standard of care, often a “no intervention” scenario; and 2) an incremental cost-effectiveness ratio comparing each strategy with the next most effective alternative which may or may not be a “no intervention” scenario. Incremental cost-effectiveness ratios are only calculated for strategies that are efficient or economically rational, which means that no other strategy or combination of strategies provides more life-years for the same or lower costs.[3] Non-efficient strategies are “dominated”. There are two ways in which a strategy can be dominated. A strategy is strongly dominated if an alternative strategy provides more life-years at the same or lower cost. A strategy is weakly dominated if a combination of alternative strategies provides more life-years at the same or lower cost. For more insight in this complex matter, see the visualization of cost-effectiveness analyses in Mark, 2002.[4]
The World Health Organization principles for population screening state that screening should only be implemented when there is a good balance between costs and benefits.[1] Unfortunately there is no universal definition for “good balance” and different institutions may have different assessments of whether the incremental cost of one intervention over another is warranted by the additional benefits it provides. An intervention that provides an additional year of life at an incremental cost of $50,000 or less is deemed acceptable in most industrialized countries, but thresholds of even $100,000 per life-year gained have been argued to be acceptable in some settings.[5]
To ensure efficient use of resources, the incremental cost-effectiveness ratio, not the ratio of each strategy compared to standard of care, should be compared to the threshold cost per (quality-adjusted) life-year gained.[6, 7] This requirement is illustrated by the following example: a recent US study found that the cost-effectiveness ratio of stool DNA testing for CRC compared with no CRC screening is $13,000–$18,000 per life-year gained.[8] With this ratio, stool DNA testing would be considered cost-effective even if the decision-maker is only willing to pay $20,000 per life-year gained. One might therefore recommend implementing a stool DNA screening program. However, annual screening with a faecal occult blood test (FOBT) was estimated to save more life-years than stool DNA testing at a lower cost and therefore strongly dominated stool DNA testing. Implementing a stool DNA screening program would therefore lead to higher costs and fewer life-years gained compared with an FOBT screening program.
There is however a situation where the cost-effectiveness ratio compared to no screening could be considered the appropriate measure of cost-effectiveness of a screening test, namely if the test would entice a previously unscreened segment of the population to adhere to screening. For example, less than 60% of the population currently adheres to CRC screening.[9–13] Most cited reasons for nonparticipation are practical reasons (e.g., conflicts with work or family, inconvenience, being too busy, lack of interest, and cost) and not having any current health problems or symptoms of CRC.[14] These barriers exist regardless of the screening test. However, other reasons for nonparticipation are worry about pain, discomfort, or injury associated with the examination or that the test would be embarrassing or unpleasant.[14] New screening tests such as computed tomographic (CT) colonography, stool DNA tests, and serum tests aim to eliminate (some of) these barriers. If there is good evidence that these tests indeed are able to increase adherence among those who would otherwise remain unscreened, then the cost-effectiveness ratio compared to no screening would be an appropriate measure for decision-making since for these people no screening is the relevant comparator.
Since the demonstration of the efficacy of CRC screening with guaiac FOBT in 1993, [15] the economic impact of population screening for CRC has been evaluated in several cost-effectiveness analyses.
US studies
The majority of CRC screening cost-effectiveness analyses are based on the US population. CRC screening guidelines were first released in the US in 1997, recommending individuals at average risk be screened with any of the following methods: (1) annual guaiac FOBT; (2) 5-yearly sigmoidoscopy; (3) the combination of 5-yearly sigmoidoscopy and annual guaiac FOBT (4)5-yearly barium enema; or (5) 10-yearly colonoscopy.[16] These strategies are still included in the most recent US CRC screening guidelines, [17, 18] and we refer to them below as the “established screening strategies”.
To date, there has been one systematic review of the cost-effectiveness of CRC screening in the US.[19] That review showed that the cost-effectiveness ratios for all established screening strategies compared to no screening were less than $50,000 per life-year gained. For guaiac FOBT the estimates were between $5,691 and $17,805 per life-year gained, for sigmoidoscopy between $12,477 and $39,359, for the combination of guaiac FOBT and sigmoidoscopy between $13,792 and $22,518 and for colonoscopy screening between $9,038 and $22,012. When the established CRC screening strategies were compared against each other, no strategy was consistently found to be the most effective or to have the best incremental cost-effectiveness ratio:[19] approximately half of the studies found the combination strategy of flexible sigmoidoscopy and guaiac FOBT to be the most effective, while the other half found colonoscopy to be the most effective strategy. At a willingness-to-pay threshold of $20,000 per life-year gained, each established screening strategy emerged as the preferred screening strategy in at least one model.
Since 2001, several new cost-effectiveness analyses of CRC screening have been published.[20–23] These studies generally confirm the findings of the systematic review that CRC screening is cost-effective compared to no screening, but no single strategy is consistently found to be the most effective or to have the most attractive incremental cost-effectiveness ratio for a given willingness to pay per life-year gained.
Studies outside the US
Cost-effectiveness analyses have also been performed for CRC screening in Europe [24–34], Asia [35–40] Australia [41–43], and Canada [44]. The focus of European cost-effectiveness analyses has been much more on (guaiac) FOBT, [24, 25, 27–29, 34] and to a lesser extent sigmoidoscopy[30, 33]; only three European studies evaluated colonoscopy screening.[26, 31, 32] In many European countries colonoscopy is not considered an option for population CRC screening. Reasons include lack of endoscopic capacity, [45, 46] lack of evidence from randomized trials, [47] and population preference for non-invasive testing.[48, 49] Another potential explanation is the different mechanism by which screening recommendations and policies are set between the US and Europe. In the US, guidelines have been issued by professional societies and other organizations that are not incentivized to consider cost or capacity issues, merely effectiveness. In many European countries screening decisions are implemented by a national body that must consider issues such as capacity and costs, as well as effectiveness of alternative screening options.
In general, the cost-effectiveness of CRC screening in Europe and Asia is more favourable than in the US, with cost-effectiveness ratios compared with no screening mostly less than $10,000 per life-year gained, [24, 25, 27–30, 34, 39] and in many studies even cost-saving.[26, 31, 33, 35, 40] The lower test costs in Europe and Asia provide an important explanation for this difference. Studies in Australia and Canada find similar cost-effectiveness ratios as in the US.[41–44] These difference illustrate the necessity to tailor cost-effectiveness analyses for specific countries. Generalization of cost-effectiveness analyses from one country to another cannot be done, because screening costs, resource capacity and population preferences for different screening tests vary from country to country.
Two collaborative modelling efforts have been undertaken to identify reasons for differences in effectiveness and cost-effectiveness of CRC screening across models.
Institute of Medicine workshop on the cost-effectiveness of CRC screening
The Institute of Medicine organized a workshop in January 2004 in which researches from five modelling teams agreed to participate.[50]. Each model was used to estimated costs and life-years gained for five screening strategies. Each estimation was performed twice: once with the original assumptions used by the modeller and once with standardized input assumptions concerning test and treatment costs, test performance, adherence to screening, follow-up, and surveillance, and the surveillance protocol. As expected, there was quite some variation in the model outcomes with the original modellers’ assumptions (Table 1). No strategy was efficient in all five models, nor was there one strategy that was dominated in all five models. After standardization, there was still considerable variation in absolute levels of costs and life-years gained, but interestingly the ordering of strategies with respect to cost-effectiveness were comparable across models (Table 2). Based on these results, the workshop organizers concluded that variation in results between CRC models could be reduced when standardizing inputs for costs, test performance, adherence and surveillance. This implies that consensus is needed regarding the best estimates for these parameters.
TABLE 1
TABLE 1
Preferred CRC Screening Strategy at different levels of willingness to pay: Original Assumptions [50]
TABLE 2
TABLE 2
Preferred CRC Screening Strategy at Different Levels of Willingness to Pay: Standardized Assumptions [50]
Cancer Intervention and Surveillance Modeling Network
In September of 2000 the National Cancer Institute in the US established the Cancer Intervention and Surveillance Modeling Network (CISNET), a large-scale modelling effort with the goal of using comparative modelling to inform cancer-control interventions.[51] Three CRC models were funded by CISNET. The CISNET CRC models were developed independently, but the modellers collaborated to identify the best-available data to inform the natural history components of the models and to standardize assumptions about screening and surveillance. In spite of the fact that the three models are informed by a common set of data and yield similar predictions for adenoma prevalence, CRC incidence, and CRC mortality in the absence of screening, the models differ with respect to which screening strategy is the most effective in terms of the number of life-years saved.[23] They determined that this discrepancy is mainly caused by differences in the simulated duration of the adenoma-carcinoma sequence. It is difficult to measure this duration in patients because, by definition, it is the period during which the condition is undiagnosed. Longitudinal data of CRC incidence after a negative sigmoidoscopy and colonoscopy from randomized trials will shed light on the true duration of the adenoma carcinoma sequence.
Three factors are likely to greatly influence the cost-effectiveness of CRC screening in the coming years: new CRC screening tests, personalized screening recommendations based on CRC risk and rising CRC treatment costs.
New CRC screening tests
In the latest version of the US Multi-Society Task Force guidelines, immunochemical FOBT, CT colonography and stool DNA testing are included as viable options for CRC screening.[17] A fourth emerging test for CRC screening is capsule endoscopy.
Several studies have shown that immunochemical FOBT has a higher CRC and adenoma detection rate than Hemoccult II, while having the same or a better positive predictive value.[52–63] Its sensitivity is comparable to that of Hemoccult Sensa, while having better specificity.[64] However in the US, immunochemical FOBT is also considerably more expensive than these guaiac FOBTs. Approximately half of the cost-effectiveness analyses that evaluated immunochemical FOBT conclude that it is a cost-effective screening strategy, [20, 24, 35, 37] whereas in the other half it is dominated by Hemoccult Sensa.[23, 39] This result is mainly dependent on the price difference between the immunochemical FOBT and Hemoccult Sensa.
US studies have estimated that screening for CRC with a stool DNA test every 2–5 years has a cost-effectiveness ratio compared to no screening of $13,000–$30,000 per life-year gained. However, the established screening options are estimated to save more life-years at lower costs and therefore stool DNA testing is strongly dominated.[8, 65] In order for stool DNA testing to be cost-effective, its unit cost would need to fall and/or adherence with stool DNA testing would need to be substantially higher than with the established screening tests. There is some evidence that the price of stool DNA testing can be reduced: the first stool DNA assay that reached the market cost almost $800, whereas a more recent stool assay for vimentin methylation alone was introduced at a cost of $220.[66] These numbers offer hope that further technological refinements will permit significant cost reductions.
Screening for CRC with CT colonography every 5–10 years has been estimated to be more expensive and in many (US) cost-effectiveness studies also less effective than colonoscopy. It is either dominated by colonoscopy or has a high incremental cost-effectiveness ratio.[67] The studies suggest that if the cost of a CT scan were a quarter to half the cost of a colonoscopy, then the incremental cost-effectiveness ratio of CT colonography screening would be similar to colonoscopy and/or the established CRC screening techniques. An important deficiency of most cost-effectiveness analyses of CT colonography to date is that they have not incorporated the potential harms of the radiation exposure from CT exams and/or costs and potential health effects associated with extracolonic findings. Only one study incorporated health benefits of abdominal aortic aneurysm detection, extracolonic cancer detection, and long-term radiation effects. In this study, CT colonography was dominant over both colonoscopy and colonoscopy with 1-time ultrasonography.[68] However, this study did not include costs of follow-up of other extracolonic findings and the benefits of finding abdominal aortic aneurysms were very favourable. A more careful examination of radiation risks and extra-colonic findings is needed.[67]
Finally, capsule endoscopy is the least developed of the emerging CRC screening tests.[69, 70] To date, only one study has evaluated the cost-effectiveness of capsule endoscopy.[71] Although the cost-effectiveness ratio comparing capsule endoscopy to no screening was found to be $25,000–$29,000 per life-year gained, colonoscopy saved more life-years at a lower cost than capsule endoscopy and capsule endoscopy was therefore dominated. The authors concluded that the cost-effectiveness of capsule endoscopy was mainly dependent on its ability to improve adherence to CRC screening.
These studies show that there is general consensus that the developing screening methods are not cost-effective compared to the established screening strategies, but that they are cost-effective compared to no screening. Accordingly, from an efficiency perspective, these tests should only be implemented if they entice individuals who would not otherwise be screened to adopt screening. Although some studies suggest that patients prefer CT colonography or stool DNA testing over the established screening strategies, there is no direct evidence showing that CT colonography and stool DNA increase CRC screening uptake among subjects who have been unwilling to perform any of the established tests.[8, 23] Stool DNA testing still requires contact with stool and may therefore present the same barrier as FOBT. Although CT colonography and capsule endoscopy are less invasive than endoscopy, they both require extensive bowel preparation which is generally considered to be one of the most important barriers to CRC screening.
Personalized screening
Personalized medicine is a general trend in medical care. Separate CRC screening guidelines already exist for individuals at increased risk of the disease because of a family history of CRC, a genetic predisposition (e.g., familial adenomatous polyposis and hereditary nonpolyposis CRC), or a personal history of CRC, adenomas, or inflammatory bowel disease.[17, 18] But differences in CRC risk exist even within the average-risk population. African Americans and men have higher CRC risk than whites and women respectively.[72] Furthermore, several risk factors are known to increase CRC incidence, such as smoking, diet, obesity, and physical inactivity.[73] To date, screening recommendations have not been tailored across different subgroups of the average-risk population. However, the American College of Gastroenterology has advocated that screening should start earlier in blacks because of the higher incidence and younger age at presentation of CRC in this population subgroup.[74] Studies have shown that CRC screening in African Americans has a lower cost per life-year gained than in whites, [75–77] and that African Americans should be screened earlier in life and with higher frequency than whites.[75] However, the benefit of tailoring of screening strategies by race was modest. Personalization of CRC screening recommendations is complex, and it might confuse providers and consumers to the point of decreasing adherence. A decrease in adherence would easily offset the gains from personalization. Given the low adherence to current screening guidelines, more benefit could be obtained from increasing adherence to existing guidelines than from personalizing them. On the other hand, individualization of screening guidelines must be considered in the context of a general trend towards personalized medical care.[78, 79] If personalization of medical care becomes the standard, it would be only natural to account for risk differences by race and gender.
Rising treatment costs
CRC treatment costs have increased dramatically over the past years. From the early 1990s to 2003, treatment costs per person have increased by up to 200%, depending on the stage of disease at diagnosis, [80, 81] whereas unit screening costs have not.[65, 82] With the US Food and Drug Administration’s approval of oxaliplatin in 2003 and the monoclonal antibodies bevacizumab and cetuximab for metastatic CRC in 2004, treatment costs have risen even higher.[83] We do not expect to have seen the end of developments in chemotherapy for CRC. The second-line treatment of bevacizumab for recurrent disease is already being investigated as first-line treatment for stage IV disease [84] and as adjuvant therapy for stage III and advanced stage II disease.[85] An important consequence of this development is that the savings from preventing (advanced) CRC and CRC deaths by screening also increase dramatically. Two studies have explicitly evaluated the consequence of the increasing CRC treatment costs on the cost-effectiveness of CRC screening. They showed that the cost-effectiveness of CRC screening is becoming more favourable compared to no screening and that most CRC screening strategies even become cost-saving, because the treatment savings from preventing (advanced) CRC and CRC deaths by screening outweigh the screening costs.[20, 86] The vast majority of the cost-effectiveness analyses have not included this spectacular increase in treatment costs, and are therefore outdated.
The discrepancies in the outcomes of the different cost-effectiveness analyses seem to indicate that no conclusion can be drawn concerning which CRC screening program should be implemented. However, the fact that no strategy emerges across the models as being the most effective or having the best incremental cost-effectiveness ratio suggests that, assuming perfect adherence across all modalities, the differences in life-years gained between strategies are quite small. This result triggers the question of whether test-specific adherence predicts the best CRC screening strategy, rather than cost-effectiveness.[87] As the prominent gastroenterologist Dr. Sidney Winawer said a long time ago, the best test is the test that gets done.[Personal Communication]
Most cost-effectiveness analyses to date assume either perfect adherence or comparable imperfect adherence among all screening strategies. European randomized controlled trials have shown that adherence with immunochemical FOBT is significantly higher than with guaiac FOBT or endoscopy.[48, 49] However, these studies have only compared adherence with the first round of screening. FOBT is generally repeated every (other) year, whereas the recommended interval for colonoscopy screening is 10 years. Although trials have shown that initial adherence with immunochemical FOBT is higher than with colonoscopy, high adherence with repeat immunochemical FOBT is required to reach similar life-years gained as with colonoscopy screening.[88] Given the frequent nature of immunochemical FOBT testing, adherence may decline over time. If small advantages in adherence for FOBT are associated with better projected outcomes relative to colonoscopy, then trials that compare both adherence and clinical outcomes after invitation to an FOBT versus colonoscopy screening program are warranted. Longer-term trials measuring adherence with FOBT in repeat screening rounds are required to finally determine which test gets done and thus what the best CRC screening strategy is. Since attitudes toward screening may differ across countries, adherence patterns observed in one country may not be applicable to other countries and should therefore be evaluated in each country.
Although for any test to be effective it first must be done, there is another important aspect to the effectiveness of any screening program: quality. Efficacy of tests is established in trial settings, and cost-effectiveness analyses are almost always based on estimates from these trials. However, the efficacy of a screening test in a trial setting may differ from its effectiveness in real-world settings. Randomized controlled trials generally have detailed screening and follow-up protocols that include quality assurance and control measures; these high standards are not always followed in real-world screening settings. For example, while adherence to follow-up colonoscopy after a positive FOBT was over 80% in randomized trials, [10, 11, 15] only 50% undergo follow-up in US clinical practice.[89] Additionally, several studies have shown that there is wide variation in adenoma detection rates between endoscopists, even within a trial setting.[90, 91] Outside a trial setting, endoscopists generally perform fewer screening procedures and are less experienced. These provider-specific factors will influence detection rates and thus effectiveness of endoscopy screening. It is therefore important for any screening program to have good quality assurance protocols in place. Accordingly, Dr. Winawer has updated his quote to: “The best screening test is the test that gets done well”.[Personal Communication]
Cost-effectiveness analysis is a useful tool for weighing the costs and benefits of alternative screening programs. Many cost-effectiveness analyses have been performed for CRC screening. All studies show that when compared with no CRC screening, all screening modalities provide additional years of life at a cost that is deemed acceptable by most industrialized nations. However even with standardization of assumptions, no one screening program emerges as the most effective in terms of life-years saved or as the preferred strategy for a given willingness to pay. There is good consensus that CT colonography, stool DNA and capsule endoscopy testing are currently more costly than alternative strategies that provide comparable, if not greater, health benefits and accordingly are not cost-effective. Studies of test-specific adherence patterns are needed, as these strategies could be cost-effective if they entice previously unscreened individuals to adopt screening. With the dramatic rise in the costs of CRC screening, the cost-effectiveness of CRC screening programs will further improve and CRC screening is likely to become cost-saving. Assuming perfect adherence across all screening modalities, life-years gained with annual screening with a highly sensitivity FOBT, 10-yearly colonoscopy, or with a combination of annual FOBT and 5-yearly sigmoidoscopy are nearly equivalent. This result implies that test-specific adherence predicts the best CRC screening strategy, rather than cost-effectiveness. Longer-term trials measuring adherence and detection rates with FOBT in repeat screening rounds are required to determine the relative benefit of FOBT versus endoscopy.
Practice points
  • All CRC screening strategies are cost-effective compared to no screening
  • There is no consensus on what is the preferred CRC strategy for a given willingness to pay
  • Generalization of cost-effectiveness analyses from one country to another cannot be done, because screening costs, resource capacity and population preferences differ
  • CT colonography, stool DNA and capsule endoscopy are not (yet) cost-effective compared to FOBT and endoscopy screening
  • Rising CRC treatment costs will make CRC screening even more cost-effective and possibly cost-saving
  • Test-specific adherence may be the key determinant of the (cost-)effectiveness of a CRC screening strategy
Research agenda
  • Evidence is needed regarding whether stool DNA, CT colonography and/or capsule endoscopy entice a previously unscreened segment of the population to adhere to screening
  • Studies investigating the effect of personalized screening on CRC screening adherence are necessary
  • Detailed studies are required to determine the best estimates for CRC test and treatment costs, screening test performance, adherence and surveillance
  • Longitudinal data of CRC incidence after a negative sigmoidoscopy and colonoscopy from randomized trials are needed to obtain a better estimate of the duration of the adenoma carcinoma sequence
  • Longer-term trials measuring adherence and detection rates with FOBT in repeat screening rounds are required to determine the relative benefit of FOBT versus endoscopy
Acknowledgments
Drs. Lansdorp-Vogelaar and Knudsen are supported in part by Cancer Intervention and Surveillance Modeling Network grants from the National Cancer Institute: (U01-CA-097426 (Lansdorp-Vogelaar), U01-CA-115953 (Lansdorp-Vogelaar), and U01-CA-088204 (Knudsen)).
Footnotes
Conflict of interest: none
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
References
1. Wilson JM, Jungner YG. Principles and practice of mass screening for disease. Boletin de la Oficina Sanitaria Panamericana. 1968 Oct;65(4):281–393. [PubMed]
2. Goldie SJ. Chapter 15: Public health policy and cost-effectiveness analysis. J Natl Cancer Inst Monogr. 2003;(31):102–10. [PubMed]
3. Cantor SB. Cost-effectiveness analysis, extended dominance, and ethics: a quantitative assessment. Med Decis Making. 1994 Jul–Sep;14(3):259–65. [PubMed]
4. Mark DH. Visualizing cost-effectiveness analysis. JAMA. 2002 May 8;287(18):2428–9. [PubMed]
5. Weinstein MC. How much are Americans willing to pay for a quality-adjusted life year? Med Care. 2008 Apr;46(4):343–5. [PubMed]
6. Hollingsworth B, Dawson PJ, Maniadakis N. Efficiency measurement of health care: a review of non-parametric methods and applications. Health Care Manag Sci. 1999 Jul;2(3):161–72. [PubMed]
7. Johannesson M, Weinstein MC. On the decision rules of cost-effectiveness analysis. J Health Econ. 1993 Dec;12(4):459–67. [PubMed]
8. Special report: fecal DNA analysis for colon cancer screening. Technol Eval Cent Asses Program Exec Summ. 2006 Aug;21(6):1–2. [PubMed]
9. Deutekom M, van Rijn AF, Dekker E, Blaauwgeers H, et al. Uptake of faecal occult blood test colorectal cancer screening by different ethnic groups in the Netherlands. Eur J Public Health. 2009 Aug;19(4):400–2. [PubMed]
10. Hardcastle JD, Chamberlain JO, Robinson MH, Moss SM, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet. 1996 Nov 30;348(9040):1472–7. [PubMed]
11. Kronborg O, Fenger C, Olsen J, Jorgensen OD, et al. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet. 1996 Nov 30;348(9040):1467–71. [PubMed]
12. Masseria C. Colorectal cancer in Italy: a review of current national and regional practice on screening and treatment. Eur J Health Econ. 2010 Jan;10( Suppl 1):S41–9. [PubMed]
13. Shapiro JA, Seeff LC, Thompson TD, Nadel MR, et al. Colorectal cancer test use from the 2005 National Health Interview Survey. Cancer Epidemiol Biomarkers Prev. 2008 Jul;17(7):1623–30. [PubMed]
14. Vernon SW. Participation in colorectal cancer screening: a review. J Natl Cancer Inst. 1997 Oct 1;89(19):1406–22. [PubMed]
15. Mandel JS, Bond JH, Church TR, Snover DC, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. The New England journal of medicine. 1993 May 13;328(19):1365–71. [PubMed]
16. Winawer SJ, Fletcher RH, Miller L, Godlee F, et al. Colorectal cancer screening: clinical guidelines and rationale. Gastroenterology. 1997 Feb;112(2):594–642. [PubMed]
17. Levin B, Lieberman DA, McFarland B, Andrews KS, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology. 2008 May;134(5):1570–95. [PubMed]
18. U. S. Preventive Services Task Force. Screening for Colorectal Cancer: U.S. Preventive Services Task Force Recommendation Statement. Annals of internal medicine. 2008 Oct 6;149(9) [PubMed]
19. Pignone M, Saha S, Hoerger T, Mandelblatt J. Cost-effectiveness analyses of colorectal cancer screening: a systematic review for the U.S. Preventive Services Task Force. Annals of internal medicine. 2002 Jul 16;137(2):96–104. [PubMed]
20. Parekh M, Fendrick AM, Ladabaum U. As tests evolve and costs of cancer care rise: Reappraising stool-based screening for colorectal neoplasia. Alimentary Pharmacology and Therapeutics. 2008;27(8):697–712. [PMC free article] [PubMed]
21. Pickhardt PJ, Hassan C, Laghi A, Zullo A, et al. Cost-effectiveness of colorectal cancer screening with computed tomography colonography: the impact of not reporting diminutive lesions. Cancer. 2007 Jun 1;109(11):2213–21. [PubMed]
22. Vijan S, Hwang I, Inadomi J, Wong RK, et al. The cost-effectiveness of CT colonography in screening for colorectal neoplasia. Am J Gastroenterol. 2007 Feb;102(2):380–90. [PMC free article] [PubMed]
23. Zauber A, Knudsen AB, Rutter CM, Lansdorp-Vogelaar I, Savarino JE, van Ballegooijen M, Kuntz KM. Cost-effectiveness of CT Colonography to screen for colorectal cancer. 2009
24. Berchi C, Bouvier V, Reaud JM, Launoy G. Cost-effectiveness analysis of two strategies for mass screening for colorectal cancer in France. Health Econ. 2004 Mar;13(3):227–38. [PubMed]
25. Gyrd-Hansen D. The relative economics of screening for colorectal cancer, breast cancer and cervical cancer. Crit Rev Oncol Hematol. 1999 Nov;32(2):133–44. [PubMed]
26. Hassan C, Zullo A, Laghi A, Reitano I, et al. Colon cancer prevention in Italy: cost-effectiveness analysis with CT colonography and endoscopy. Dig Liver Dis. 2007 Mar;39(3):242–50. [PubMed]
27. Hristova L, Hakama M. Effect of screening for cancer in the Nordic countries on deaths, cost and quality of life up to the year 2017. Acta Oncol. 1997;36( Suppl 9):1–60. [PubMed]
28. Lejeune C, Arveux P, Dancourt V, Bejean S, et al. Cost-effectiveness analysis of fecal occult blood screening for colorectal cancer. Int J Technol Assess Health Care. 2004 Fall;20(4):434–9. [PubMed]
29. Macafee DAL, Waller M, Whynes DK, Moss S, et al. Population screening for colorectal cancer: The implications of an ageing population. British Journal of Cancer. 2008;99(12):1991–2000. [PMC free article] [PubMed]
30. Norum J. Prevention of colorectal cancer: a cost-effectiveness approach to a screening model employing sigmoidoscopy. Ann Oncol. 1998 Jun;9(6):613–8. [PubMed]
31. Sieg A, Brenner H. Cost-saving analysis of screening colonoscopy in Germany. Z Gastroenterol. 2007 Sep;45(9):945–51. [PubMed]
32. Steele RJ, Gnauck R, Hrcka R, Kronborg O, et al. Methods and Economic Considerations: Group 1 Report. ESGE/UEGF Colorectal Cancer--Public Awareness Campaign. The Public/Professional Interface Workshop: Oslo, Norway, June 20–22, 2003. fulfillment corporate. Endoscopy. 2004 Apr;36(4):349–53. [PubMed]
33. Tappenden P, Chilcott J, Eggington S, Patnick J, et al. Option appraisal of population-based colorectal cancer screening programmes in England. Gut. 2007 May;56(5):677–84. [PMC free article] [PubMed]
34. Whynes DK, Nottingham FOBST. Cost-effectiveness of screening for colorectal cancer: evidence from the Nottingham faecal occult blood trial. J Med Screen. 2004;11(1):11–5. [PubMed]
35. Chen LS, Liao CS, Chang SH, Lai HC, et al. Cost-effectiveness analysis for determining optimal cut-off of immunochemical faecal occult blood test for population-based colorectal cancer screening (KCIS 16) J Med Screen. 2007;14(4):191–9. [PubMed]
36. Leshno M, Halpern Z, Arber N. Cost-effectiveness of colorectal cancer screening in the average risk population. Health Care Manag Sci. 2003 Aug;6(3):165–74. [PubMed]
37. Shimbo T, Glick HA, Eisenberg JM. Cost-effectiveness analysis of strategies for colorectal cancer screening in Japan. Int J Technol Assess Health Care. 1994 Summer;10(3):359–75. [PubMed]
38. Tsoi KK, Ng SS, Leung MC, Sung JJ. Cost-effectiveness analysis on screening for colorectal neoplasm and management of colorectal cancer in Asia. Aliment Pharmacol Ther. 2008 Aug 1;28(3):353–63. [PubMed]
39. Wong SS, Leong AP, Leong TY. Cost-effectiveness analysis of colorectal cancer screening strategies in Singapore: a dynamic decision analytic approach. Stud Health Technol Inform. 2004;107(Pt 1):104–10. [PubMed]
40. Wu GH, Wang YM, Yen AM, Wong JM, et al. Cost-effectiveness analysis of colorectal cancer screening with stool DNA testing in intermediate-incidence countries. BMC Cancer. 2006;6:136. [PMC free article] [PubMed]
41. O’Leary BA, Olynyk JK, Neville AM, Platell CF. Cost-effectiveness of colorectal cancer screening: comparison of community-based flexible sigmoidoscopy with fecal occult blood testing and colonoscopy. J Gastroenterol Hepatol. 2004 Jan;19(1):38–47. [PubMed]
42. Salkeld G, Young G, Irwig L, Haas M, et al. Cost-effectiveness analysis of screening by faecal occult blood testing for colorectal cancer in Australia. Aust N Z J Public Health. 1996 Apr;20(2):138–43. [PubMed]
43. Stone CA, Carter RC, Vos T, St John J. Colorectal cancer screening in Australia: An economic evaluation of a potential biennial screening program using faecal occult blood tests. Australian and New Zealand Journal of Public Health. 2004;28(3):273–82. [PubMed]
44. Flanagan WM, Le Petit C, Berthelot JM, White KJ, et al. Potential impact of population-based colorectal cancer screening in Canada. Chronic Dis Can. 2003 Fall;24(4):81–8. [PubMed]
45. Macfarlane B, Leicester R, Romaya C, Epstein O. Colonoscopy services in the United Kingdom. Endoscopy. 1999 Aug;31(6):409–11. [PubMed]
46. van Putten PG, van Leerdam ME, Kuipers EJ. The views of gastroenterologists about the role of nurse endoscopists, especially in colorectal cancer screening. Aliment Pharmacol Ther. 2009 Apr 15;29(8):892–7. [PubMed]
47. Council of the European Union. COUNCIL RECOMMENDATION of 2 December 2003 on cancer screening. 2003
48. Hol L, van Leerdam ME, van Ballegooijen M, van Vuuren AJ, et al. Screening for colorectal cancer: randomised trial comparing guaiac-based and immunochemical faecal occult blood testing and flexible sigmoidoscopy. Gut. Jan;59(1):62–8. [PubMed]
49. Segnan N, Senore C, Andreoni B, Arrigoni A, et al. Randomized trial of different screening strategies for colorectal cancer: patient response and detection rates. J Natl Cancer Inst. 2005 Mar 2;97(5):347–57. [PubMed]
50. Pignone M, Russell L, Wagner J. Economic Models of Colorectal Cancer Screening in Average-Risk Adults: Workshop Summary. Washington DC: Institute of Medicine and National Research Council of the National Academies; 2005.
51. Cancer Intervention and Surveillance Modeling Network. Available from: http://cisnet.cancer.gov.
52. Allison JE, Tekawa IS, Ransom LJ, Adrain AL. A comparison of fecal occult-blood tests for colorectal-cancer screening. The New England journal of medicine. 1996 Jan 18;334(3):155–9. [PubMed]
53. Castiglione G, Zappa M, Grazzini G, Mazzotta A, et al. Immunochemical vs guaiac faecal occult blood tests in a population-based screening programme for colorectal cancer. Br J Cancer. 1996 Jul;74(1):141–4. [PMC free article] [PubMed]
54. Dancourt V, Lejeune C, Lepage C, Gailliard MC, et al. Immunochemical faecal occult blood tests are superior to guaiac-based tests for the detection of colorectal neoplasms. Eur J Cancer. 2008 Oct;44(15):2254–8. [PubMed]
55. Guittet L, Bouvier V, Mariotte N, Vallee JP, et al. Comparison of a guaiac based and an immunochemical faecal occult blood test in screening for colorectal cancer in a general average risk population. Gut. 2007 Feb;56(2):210–4. [PMC free article] [PubMed]
56. Hoepffner N, Shastri YM, Hanisch E, Rosch W, et al. Comparative evaluation of a new bedside faecal occult blood test in a prospective multicentre study. Aliment Pharmacol Ther. 2006 Jan 1;23(1):145–54. [PubMed]
57. Hughes K, Leggett B, Del Mar C, Croese J, et al. Guaiac versus immunochemical tests: faecal occult blood test screening for colorectal cancer in a rural community. Aust N Z J Public Health. 2005 Aug;29(4):358–64. [PubMed]
58. Ko CW, Dominitz JA, Nguyen TD. Fecal occult blood testing in a general medical clinic: comparison between guaiac-based and immunochemical-based tests. Am J Med. 2003 Aug 1;115(2):111–4. [PubMed]
59. Rozen P, Knaani J, Samuel Z. Comparative screening with a sensitive guaiac and specific immunochemical occult blood test in an endoscopic study. Cancer. 2000 Jul 1;89(1):46–52. [PubMed]
60. Smith A, Young GP, Cole SR, Bampton P. Comparison of a brush-sampling fecal immunochemical test for hemoglobin with a sensitive guaiac-based fecal occult blood test in detection of colorectal neoplasia. Cancer. 2006 Nov 1;107(9):2152–9. [PubMed]
61. van Rossum LG, van Rijn AF, Laheij RJ, van Oijen MG, et al. Random comparison of guaiac and immunochemical fecal occult blood tests for colorectal cancer in a screening population. Gastroenterology. 2008 Jul;135(1):82–90. [PubMed]
62. Wong BC, Wong WM, Cheung KL, Tong TS, et al. A sensitive guaiac faecal occult blood test is less useful than an immunochemical test for colorectal cancer screening in a Chinese population. Aliment Pharmacol Ther. 2003 Nov 1;18(9):941–6. [PubMed]
63. Zappa M, Castiglione G, Paci E, Grazzini G, et al. Measuring interval cancers in population-based screening using different assays of fecal occult blood testing: the District of Florence experience. Int J Cancer. 2001 Apr 1;92(1):151–4. [PubMed]
64. Allison JE, Sakoda LC, Levin TR, Tucker JP, et al. Screening for colorectal neoplasms with new fecal occult blood tests: update on performance characteristics. J Natl Cancer Inst. 2007 Oct 3;99(19):1462–70. [PubMed]
65. Zauber A, Lansdorp-Vogelaar I, Wilschut J, Knudsen AB, van Ballegooijen M, Kuntz KM. Cost-effectiveness of DNA stool testing to screen for colorectal cancer: Report to AHRQ and CMS from the Cancer Intervention and Surveillance Modeling Network (CISNET) for MISCAN and SimCRC Models. 2007
66. Chung DC. Stool DNA testing and colon cancer prevention: another step forward. Annals of internal medicine. 2008 Oct 7;149(7):509–10. [PubMed]
67. Special report: critical appraisal of CT colonography cost-effectiveness analyses. Technol Eval Cent Asses Program Exec Summ. 2009 Aug;24(2):1–2. [PubMed]
68. Hassan C, Pickhardt P, Laghi A, Kim D, et al. Computed tomographic colonography to screen for colorectal cancer, extracolonic cancer, and aortic aneurysm: model simulation with cost-effectiveness analysis. Archives of Internal Medicine. 2008;168(7):696–705. [PubMed]
69. Fireman Z, Kopelman Y. The colon - the latest terrain for capsule endoscopy. Dig Liver Dis. 2007 Oct;39(10):895–9. [PubMed]
70. Tran K. Capsule colonoscopy: PillCam Colon. Issues Emerg Health Technol. 2007 Oct;(106):1–4. [PubMed]
71. Hassan C, Zullo A, Winn S, Morini S. Cost-effectiveness of capsule endoscopy in screening for colorectal cancer. Endoscopy. 2008 May;40(5):414–21. [PubMed]
72. Ries L, Eisner MP, Kosary CL, Hankey BF, Miller BA, Clegg L, Mariotto A, Feuer EJ, Edwards BKe. SEER Cancer Statistics Review, 1975–2001. National Cancer Institute; 2004. Available from: http://seer.cancer.gov/csr/1975_2001/
73. Giovannucci E. Modifiable risk factors for colon cancer. Gastroenterol Clin North Am. 2002 Dec;31(4):925–43. [PubMed]
74. Agrawal S, Bhupinderjit A, Bhutani MS, Boardman L, et al. Colorectal cancer in African Americans. Am J Gastroenterol. 2005 Mar;100(3):515–23. discussion 4. [PubMed]
75. Lansdorp-Vogelaar I, van Ballegooijen M, Zauber AG, Boer R, et al. Individualizing colonoscopy screening by sex and race. Gastrointest Endosc. 2009 Jul;70(1):96–108. e1–24. [PMC free article] [PubMed]
76. Theuer CP, Taylor TH, Brewster WR, Anton-Culver H. Gender and race/ethnicity affect the cost-effectiveness of colorectal cancer screening. J Natl Med Assoc. 2006 Jan;98(1):51–7. [PMC free article] [PubMed]
77. Theuer CP, Wagner JL, Taylor TH, Brewster WR, et al. Racial and ethnic colorectal cancer patterns affect the cost-effectiveness of colorectal cancer screening in the United States. Gastroenterology. 2001 Mar;120(4):848–56. [PubMed]
78. Abrahams E, Ginsburg GS, Silver M. The Personalized Medicine Coalition: goals and strategies. Am J Pharmacogenomics. 2005;5(6):345–55. [PubMed]
79. Kalow W. Pharmacogenetics and pharmacogenomics: origin, status, and the hope for personalized medicine. Pharmacogenomics J. 2006 May–Jun;6(3):162–5. [PubMed]
80. Brown ML, Riley GF, Potosky AL, Etzioni RD. Obtaining long-term disease specific costs of care: application to Medicare enrollees diagnosed with colorectal cancer. Med Care. 1999 Dec;37(12):1249–59. [PubMed]
81. Yabroff KR, Lamont EB, Mariotto A, Warren JL, et al. Cost of care for elderly cancer patients in the United States. J Natl Cancer Inst. 2008 May 7;100(9):630–41. [PubMed]
82. Sonnenberg A, Delco F, Inadomi JM. Cost-effectiveness of colonoscopy in screening for colorectal cancer. Annals of internal medicine. 2000 Oct 17;133(8):573–84. [PubMed]
83. Schrag D. The price tag on progress--chemotherapy for colorectal cancer. The New England journal of medicine. 2004 Jul 22;351(4):317–9. [PubMed]
84. Kabbinavar FF, Hurwitz HI, Yi J, Sarkar S, et al. Addition of bevacizumab to fluorouracil-based first-line treatment of metastatic colorectal cancer: pooled analysis of cohorts of older patients from two randomized clinical trials. J Clin Oncol. 2009 Jan 10;27(2):199–205. [PubMed]
85. de Gramont A, Tournigand C, Andre T, Larsen AK, et al. Adjuvant therapy for stage II and III colorectal cancer. Semin Oncol. 2007 Apr;34(2 Suppl 1):S37–40. [PubMed]
86. Lansdorp-Vogelaar I, van Ballegooijen M, Zauber AG, Habbema JD, et al. Effect of rising chemotherapy costs on the cost savings of colorectal cancer screening. J Natl Cancer Inst. 2009 Oct 21;101(20):1412–22. [PMC free article] [PubMed]
87. Gupta S. Will test-specific adherence predict the best colorectal cancer screening strategy? Annals of internal medicine. 2009 Mar 3;150(5):359. author reply -60. [PubMed]
88. Zauber AG, Lansdorp-Vogelaar I, Knudsen AB, Wilschut J, et al. Evaluating test strategies for colorectal cancer screening: a decision analysis for the U.S. Preventive Services Task Force. Annals of internal medicine. 2008 Nov 4;149(9):659–69. [PMC free article] [PubMed]
89. Miglioretti DL, Rutter CM, Bradford SC, Zauber AG, et al. Improvement in the diagnostic evaluation of a positive fecal occult blood test in an integrated health care organization. Med Care. 2008 Sep;46(9 Suppl 1):S91–6. [PubMed]
90. Atkin W, Rogers P, Cardwell C, Cook C, et al. Wide variation in adenoma detection rates at screening flexible sigmoidoscopy. Gastroenterology. 2004 May;126(5):1247–56. [PubMed]
91. Shaukat A, Oancea C, Bond JH, Church TR, et al. Variation in detection of adenomas and polyps by colonoscopy and change over time with a performance improvement program. Clin Gastroenterol Hepatol. 2009 Dec;7(12):1335–40. [PubMed]