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An international review of the main cost-effectiveness drivers of virtual colonography versus conventional colonoscopy for colorectal cancer screening: Is the tide changing due to adherence?
European Journal of Radiology 82 (2013) e629–e636
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European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Review
An international review of the main cost-effectiveness drivers of virtual colonography versus conventional colonoscopy for colorectal cancer screening: Is the tide changing due to adherence? Christine Kriza a,∗ , Martin Emmert b,1 , Philip Wahlster a , Charlotte Niederländer a , Peter Kolominsky-Rabas a a Interdisciplinary Centre for Health Technology Assessment and Public Health, University of Erlangen-Nuremberg, National BMBF-Cluster of Excellence, “Medical Technologies - Medical Valley EMN”, Schwabachanlage 6, 91054 Erlangen, Germany b School of Business and Economics, Institute of Management, University of Erlangen-Nuremberg, Lange Gasse 20, 90403 Nuremberg, Germany
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Article history: Received 29 April 2013 Received in revised form 16 July 2013 Accepted 19 July 2013 Keywords: Computerised tomographic colonography Colonoscopy Colorectal cancer Screening Cost-effectiveness Patient adherence Economics Modelling Simulation
a b s t r a c t Objectives: The majority of recent cost-effectiveness reviews concluded that computerised tomographic colonography (CTC) is not a cost-effective colorectal cancer (CRC) screening strategy yet. The objective of this review is to examine cost-effectiveness of CTC versus optical colonoscopy (COL) for CRC screening and identify the main drivers influencing cost-effectiveness due to the emergence of new research. Methods: A systematic review was conducted for cost-effectiveness studies comparing CTC and COL as a screening tool and providing outcomes in life-years saved, published between January 2006 and November 2012. Results: Nine studies were included in the review. There was considerable heterogeneity in modelling complexity and methodology. Different model assumptions and inputs had large effects on resulting costeffectiveness of CTC and COL. CTC was found to be dominant or cost-effective in three studies, assuming the most favourable scenario. COL was found to be not cost effective in one study. Conclusions: CTC has the potential to be a cost-effective CRC screening strategy when compared to COL. The most important assumptions that influenced the cost-effectiveness of CTC and COL were related to CTC threshold-based reporting of polyps, CTC cost, CTC sensitivity for large polyps, natural history of adenoma transition to cancer, AAA parameters and importantly, adherence. There is a strong need for a differential consideration of patient adherence and compliance to CTC and COL. Recent research shows that laxative-free CTC screening has the potential to become a good alternative screening method for CRC as it can improve patient uptake of screening. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Data from the Global Burden of Disease Study 2010 ranks CRC on fourth place in terms of leading causes of years of life lost for the Western European Region, ranking 10th for high-income North America [1]. The disease burden of CRC will increase in the coming years due to an ageing population, with considerable impact on health care costs [2]. In the last few years, colorectal cancer (CRC) screening using computerised tomographic colonography (CTC), also referred to as virtual colonography, has attracted considerable
∗ Corresponding author. Tel.: +49 9131 8535855; fax: +49 9131 8535854. E-mail addresses: [email protected], [email protected] (C. Kriza), [email protected] (M. Emmert), [email protected] (P. Wahlster), [email protected] (C. Niederländer), [email protected] (P. Kolominsky-Rabas). 1 Tel.: +49 911 5302 253; fax: +49 911 5302 285. 0720-048X/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejrad.2013.07.019
attention, discussion on screening methods and clinical comparisons [3], and was the basis for numerous cost-effectiveness reviews [4,5]. The majority of the reviews concluded that CTC is not a cost-effective screening strategy compared to other screening modalities yet. The objective of this review is to re-examine the cost-effectiveness of CTC as well as its major drivers, especially compared to conventional colonoscopy (COL) given the emergence of new research and data. The importance of the cost-effectiveness of CRC screening becomes all the more important, considering CRC is the third most common cancer worldwide [6]. 2. Methods For this review, studies had to compare CTC and COL as a primary screening tool, provide a related cost-effectiveness analysis for the two strategies and provide outcomes in life-years saved (LYS) in order to enable comparability. Studies published in peer reviewed
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Table 1 ICER results: overview. Study
More effective screening
Less costly screening
ICER of more effective to less effective
Assuming most favourable scenario for CTC
1 2 3 4 5 6 7 8 9
COL COL CTC CTC CTC COL COL COL COL
CTC CTC COL CTC COL CTC CTC COL CTC
COL vs CTC: D 15,091/LYS COL vs CTC: $63,900/LYS CTC vs COL: $156,000/LYS CTC dominates CTC vs COL: $2,144/LYS COL vs CTC: $498,668/LYS COL vs CTC: £42,000/LYS COL dominates CTC vs COL: $44,000/LYS
CTC 10yrs Scenario 2, CTC 10yrs Scenario 2, CTC 5yrs Scenario 3, CTC 10yrs CTC 10yrs Scenario 3, CTC 10yrs CTC 10yrs All scenarios assuming perfect adherence Scenario SIM-CRC, 50% adherence, CTC 5
journals between January 2006 and November 2012 were included in the review. The search methodology was in line with PRISMA guidelines [7], including the use of the PICOS review system (see details in the Annex). The selection criteria have been adapted from the CHEC-list (Consensus on health economic criteria) [8], and the CRD’s guidance for undertaking systematic reviews in health care, specifically the section on systematic reviews on economic evaluations (more details on methodology are provided in the Annex). The search results were independently reviewed and screened by two researchers who then independently extracted the relevant data. For each study included in the review, data was extracted on the parameters shown in the header columns in Supplementary Tables I and II. All studies that were included in the systematic review met the quality criteria according to the CRD’s checklist for assessing economic evaluations, sufficiently detailing study design, results and analysis. 3. Results
started from $498 for the American setting, ranging up to $877 (See supplementary Table I). When indirect costs were considered, COL costs ranged up to $1,100. CTC costs varied from $478 for the American setting, ranging up to $665, with Computer Assisted Detection (CAD) up to $715, and peaking at $814 when indirect costs were considered. CTC/COL cost ratios ranged from 0.26 to 0.98. Costs for COL and polypectomy ranged from $831 to $1,265. For the European setting, COL costs started from D 148 with CTC costs at D 101 and COL and polypectomy at D 229. The cost assumptions for cancer care varied between the studies in terms of cost components and sophistication of differentiating stages of cancer care. For the European setting, such costs started from D 14,940 for Early CRC and D 24,900 for Late CRC. For the American setting, cancer care costs started at $45,228 and ranged up to consideration of the societal perspective, considering CRC stages I–IV and phases of care, with costs for each combinations ranging from $2,719 up to $78,227, resulting in considerably higher care costs. In addition, studies differed in cost assumptions for cost of complications such as cost of treating colon perforation (ranges from $13,000 to $22,269), as well as consideration of extracolonic findings.
3.1. Overall study features 3.3. Incremental cost effectiveness ratios Due to the strict application of quality criteria, a total of nine studies were included in the systematic review. A majority of 7 studies were based on US data, with 1 study based on Italian and 1 study based on British data. All studies focused on a screening population at average risk of CRC (for full information on study features, see supplementary Table I). The majority of seven studies used either Markov cohort modelling or state transition type Markov models as methodology. Two studies used micro simulation methods which are based on a hybrid modelling approaches, using discrete event and Markov modelling aspects. All of the studies included COL and CTC in their screening scenario, but there was a large variety in the scenarios used in the studies. As such, different scenarios were used for management and reporting of polyps for CTC and time frames for CTC were either every five or ten years. Two studies applied inclusion of extra colonic finding benefits, specifically related to abdominal aortic aneurisms (AAA) for CTC in their scenarios. One study differentiated between CTC without CAD (Computer Assisted Detection) and with CAD, and also between experienced and inexperienced readers. One study used data for CTC accuracy from different sources, thereby creating separate scenarios. Two studies included scenarios from different microsimulation models, and one of these studies specified data from a 50% adherence scenario. Additional polypectomy costs as a follow-up of colonography were considered in the review studies. 3.2. Costs Costs for both screening strategies were influenced by the study perspective and consideration of direct and indirect costs. COL costs
All of the studies included in the review found CTC to be costeffective compared to “no screening” (this was not applicable in study 7, as a ‘no screening’ option was not considered). Costeffectiveness thresholds were used in most studies, although there were differences in which these thresholds were calculated. Assuming the most favourable scenario for CTC and disregarding other screening modalities except for COL and CTC, the results still varied considerably between the nine studies (see Table 1, ICER results). COL dominated in study 8 [9], although only the scenarios assuming perfect adherence were considered, as outcome data for less than perfect adherence was not indicated. CTC dominated in study 4 [10], considering the scenario for CTC every 10 years. COL was the more effective screening strategyin four studies: 1, 2, 6 and 7 [11–14]. The ICERs of COL vs. CTC in these studies ranged from D 15,091/LYS up to $498,668/LYS. In two studies, 3 and 5 [12,15], CTC was the more effective screening strategy. The ICERs of CTC vs. COL in these studies ranged from $2,144/LYS up to §156,000/LYS. Further factors had a major influence on the cost-effectiveness of COL and CTC, such as clinical management of CTC-detected polyps, screening accuracy, extracolonic findings, CRC national history assumptions and adherence related issues. 3.4. Sensitivity of COL and CTC and threshold reporting Sensitivity for COL was indicated according to polyp sizes. Sensitivity for polyps ≤5 mm ranged from 75-92.4%, for polyps sizes 6–9 mm: 85–95%, polyp size ≥10 mm: 88.3–95% and CRC: 88.3–95%. Sensitivity for CTC was also indicated according to polyp
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sizes, and in most studies, sensitivity for polyps ≤5 mm was not applicable due to the reporting threshold of polyps measuring at least 6 mm. Sensitivity for polyps sizes 6–9 mm ranged from 57 to 88%, polyp size ≥10 mm: 84–92% and CRC: 84–95%. Seven of the nine studies included a referral/reporting threshold for CTC of polyps measuring at least 6 mm in at least one of their scenarios. This practice has been widely discussed [4,16] and is not without its controversies [17]. However, in recent years, this practice has been established in order to address over-detection and apply a cost-effective approach [18]. Details on specificity of the screening approaches are given in Supplementary table I. 3.5. Extra-colonic findings, AAA Two studies included assumptions on the benefits of extracolonic findings in their modelling (4 and 5). Primarily, these benefits referred to the detection of abdominal aortic aneurisms (AAA), rather than extra colonic cancers in the lung, liver, pancreas and ovaries. Whereas screening of such cancers has not proved to be effective, there is strong data on screening effectiveness for AAA [19,20]. Incorporating the benefits of these assumptions had a considerable impact on showing CTC to be either dominant over COL, or cost-effective. 3.6. Natural history of colorectal cancer The most important assumptions on the natural history of CRC in the studies referred to polyp growth and speed of cancer development, overall prevalence of polyps before screening by age and the development of de novo cancer. The studies which based their models on Markov-type methods, used different approaches for natural history than the micro simulation models. For the former, natural history assumptions evolved by publication date in terms of more detail used and sophistication of assumptions. Six such studies indicated adenoma/polyp prevalence at age 50, ranging from 15 to 20%/age 65:40%. A new polyp rate for the periods 50–60y, 60–70y and 70–80y was considered in addition, with rates ranging from 1.9 to 3.3%. Annual transition rates from diminutive polyp sizes to small polyp sizes, from small to large and from large to early CRC were indicated, i.e. from ≤5 mm to 6–9 mm: 2–4; from 6 to 9 mm to ≥10 mm: 2–4; from ≥10 mm to early CRC: 3–4. Rates from early CRC to late CRC, or regional CRC to distant CRC ranged from 30 to 40 and rates for de novo cancer ranged from 0.008 to 0.16 (age specific). De novo prevalence rates of CRC ranged from 85 to 90. One study used a different methodology for annual probability of progression and disease classification (See Supplementary Table I, Study 7). Two studies considered the natural history of abdominal aortic aneurism. The two studies which used micro simulation approaches based their natural history assumptions on complex functional forms for adenoma growth and progression. (See Supplementary Table I, Studies 8 and 9). 3.7. Screening adherence, compliance and safety The term adherence is used to describe uptake of initial testing, whereas the term compliance relates to follow-up testing-used according to [11] and [12]. Screening assumptions for adherence and compliance varied across the studies. Most studies used a baseline scenario, with specific assumptions, ranging from 60% to 100% for adherence and 80–100% for compliance with both CTC and COL screening. Differential adherence scenarios were then modelled, ranging from 20 to 100%. However, only one study considered differential adherence scenarios between CTC and COL screening specifically (Study 8). These assumptions have a major impact on the simulation outcomes and will be analysed further in the discussion.
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All studies considered bowel perforation and bleeding as a medical complication arising from COL and CTC. The safety parameters referring toperforation rates for CTC and COL ranged from 0.002 to 0.1%, with clear advantages of CTC regarding the safety profile. One study included assumptions of CTC radiation exposure and related cancer risk, concluding that the numbers of deaths as a result of radiation-related cancer were less than due to serious complications resulting from COL screening [10]. 3.8. Sensitivity analysis All nine studies included in the review used univariate sensitivity analysis in order to examine uncertainty, with a majority of studies applying multivariate sensitivity analysis through Monte-Carlo methodology. The most important assumptions that influenced the cost-effectiveness of CTC and COL were related to CTC threshold-based reporting of polyps, CTC/COL cost ratio, CTC sensitivity for small and large polyps, natural history of adenoma transition to cancer, AAA parameters, time intervals of screening and importantly, adherence. 4. Discussion There was considerable heterogeneity in modelling complexity and methodology, but especially in the model assumptions and inputs mentioned above. These all had large effects on resulting cost-effectiveness of CTC and COL. We will discuss the main drivers that are likely to affect CTC cost-effectiveness and examine related assumptions in the light of new research data. The main cost-effectiveness drivers can be identified in the area of costs, natural history, diagnostic sensitivity and importantly adherence and compliance. In our discussion, we attempt to focus on issue of adherence while also considering the impact of new research in the area of non-laxative CTC methods which suggest improvements of screening patients’ uptake to participate. 4.1. Costs and effects Overall, CTC was found to be dominant or cost effective in three studies, assuming specific scenarios. COL was found to be not cost effective in one study with a specific scenario. In the remaining studies where CTC was found to be not cost-effective, it would be possible to transform CTC towards cost-effectiveness when altering assumptions on costs, adherence and for some studies, natural history assumptions and CTC accuracy. Considering the results presented in this review, it is important to highlight the importance of cost data used for CTC and COL. For the European setting, it has been previously pointed out that costs appear to be lower for CTC due to different health system settings [11]. New research by de Haan [21] has concluded that Dutch costs of CTC are considerably lower than cost assumptions previously used in cost-effectiveness models. The research findings point out average costs per participant within an invitational population-based screening programme at D 169.40. When considering indirect costs, the advantages for CTC become more pronounced. Due to the increasing use of costly biological agents for the treatment of CRC, the consideration of a changing pattern in the Cost of illness of CRC becomes important [22]. The implications are increasing costs and the possibility to avert costs incurred for CRC treatment through screening programmes. 4.2. Natural history Microsimulation methodology allows for dynamic modelling of growth, which has potential advantages for realistically simulating natural history. It enables for the simulation of multiple
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adenoma/polyp sizes and locations, as opposed to more rigid adenoma states in the Markov models. However, comparing natural history assumptions of CRC becomes difficult as a result. In addition, different data sources were used for polyp/adenoma prevalence and other assumptions. Importantly, varying categories and the rate at which adenomas progress to cancer seem to be the most crucial aspects of natural history assumptions [23]. Consideration of abdominal aortic aneurism natural history and its related benefits of CTC screening seem to also have an important impact, which necessitates further critical review and research. New data has been presented on the risk of progression of advanced adenomas to CRC by age and sex which suggest that transition rates in older age groups are in line with previous estimates but considerably lower for younger age groups [24]. The impact of new research related to the understanding of polyp and CRC natural history needs to be considered for the design of future cost-effectiveness studies. 4.3. Sensitivity New data from larger CTC studies is emerging which points towards higher sensitivity and specificity rates than used in most of the studies included in the review [25,26], with findings also valid for older age groups [27]. In addition, updated meta-analysis also support the validity of higher CTC sensitivity and specificity than those used in the reviewed studies [28,29]. The use of CAD either concurrently or as a second reader has been connected with a considerable increase in sensitivity for detecting large polyps (6 mm and above). Relevant increases vary according to the experience of the reader and is indeed higher in those without specific experience in CTC (Regge et al.). However, there is a significant need to improve the training and expertise in CTC readers in addition to CAD. For consistently high senstitivity results, health policy makers would be required to address training and expertise improvements for CTC reading. 4.4. Adherence and compliance and the impact of new research The adherence and compliance levels used in the model assumptions of all of the studies are overestimating real-life data on uptake of COL and CTC. According to a similar review by van Gils for an earlier time period, this trend of modelling to use higher adherence rates than data from trials indicate has been highlighted, with average adherence in models at 78%, while data from trials regarding the adherence of colonoscopy and CTC refer to rates often under 30% [30]. The theoretical threshold of 50% participation for effective mass screening is often not realistic in clinical practice. While in a US setting, adherence per se has been cited to be as high as 50–60% [26,31], the figures for a European setting are much lower. In the German setting, data from 2010 indicates that only 3% of those entitled per year participated in colonoscopies that are an integral element of CRC screening according to German guidelines [32–34]. In addition, screening uptake rates are also often cited in different manners, sometimes referring to annual participation rates of eligible patients, in Germany below 3%, cumulated rates for a 5 year period (in Germany, such figures rise up to 20%), or screening participation ever (in Germany, up to 55%) [32,35,36]. Knudsen et al. suggest in their study that CTC could be a costeffective CRC screening option for Medicare enrollees CTC costs are substantially lower than those of COL, or if 25% of otherwise unscreened persons opted for CTC screening [9]. In response to this study [9], Pickhardt [37] argued that the latter condition would be met as data from the largest CTC screening experience in the US shows that nearly 40% of individuals screened by CTC would have foregone screening if CTC had not been offered [38]. In another study, roughly 80% of a nonadherent urban cohort indicated their
willingness to use CTC screening [39]. New research supports this argument as follows. CTC has one major advantage over COL in that it is less invasive in nature. Recent research findings suggest that CTC using noncathartic, or laxative-free, bowel preparation approaches together with faecal tagging, showed positive effects in terms of high sensitivity for advanced adenomas and high patient acceptability of the procedure [40,41]. Bowel preparation is reported to be one of the main sources of patient discomfort and a barrier to the uptake of screening [42,43]. A recent systematic review and meta-analysis of patient preference for COL versus CTC showed that screening patients preferred CTC, with studies featuring limited bowel preparations for CTC reporting marked CTC preference [44]. Further consideration on how to target specific subgroups of patients, for whom uptake of screening have been low can be crucial [43,45–48]. Research findings from a Dutch RCT comparing CTC and COL showed that participation in screening with CTC was significantly better than with COL [40]. The study demonstrates a 55% improvement in screening participation with CTC over COLfrom 22% for COL to 34% to CTC [49]. Although the iodinated contrast material was connected with some patient discomfort [50], different tagging methods led to improved patient experience [41]. A recent study on thediagnostic accuracy of laxative-freeCTC found high accuracy in detecting adenomas 10 mm larger but less so for smaller lesions [41]. Patient experience was better with laxative-free CT. Participants in the study indicated that laxative-free CTC is more comfortable and easier to prepare for, and it was the preferred screening method for 62% of respondents. According to Zalis, CTCs currently cost about one-third as much as COL, and it is to be expected that a laxative-free version would cost the same [41]. 4.5. Study limitations A major limitation of this review is the limited number of studies included due to very strict quality criteria. In addition, of the total of nine studies, 5 studies have been published by the same author group. Seven of the nine studies provide an analysis of scenarios from the United States, which reduces the aspect of the international perspective of the review. However, even given the specific limitations of the studies analysed, certain commonalities and trends could be extracted from the analysis of the different studies. The focus of the review was to highlight and discuss the most important findings.Issues that also have an impact of the cost-effectiveness, such as radiation and the impact of extra colonic findings have not been analysed in sufficient detail, but have been subject of previous research and reviews [51–53]. 5. Conclusion There has been an established development in the last years, whereby CTC is considered cost-effective compared to noscreening [5,23], which is also supported by this review. CTC has the potential to be a cost-effective CRC screening strategy when compared to COL. The main modelling assumptions that are likely to render CTC cost-effective are connected to natural history concepts, especially the rate in which large adenomas progress to CRC, a finding first suggested by [23] and confirmed by [54]. In addition, the consideration of AAAs for the benefits of CTC extracolonic findings are an important factor that positively influence CTC cost-effectiveness. Model inputs regarding CTC cost and accuracy aspects are also crucial, and current research is emerging that shows low CTC costs, especially in a European setting alongside higher accuracy for CTCs, also for older populations. The most important assumption highlighted in this review is the need for a differential consideration of patient adherence and compliance
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to CTC and COL. The importance of patient adherence has been pointed out previously [4,30,55–57], but the specific significance of non-laxative CTC methods is highlighted in this review. Recent research shows that laxative-free CTC screening has the potential to become a good alternative screening method for CRC as it can improve patient uptake of screening. Our review suggests that if cost-effectiveness modelling applies real adherence and compliance rates that have been observed in clinical practice, the cost-effectiveness balance is likely to be turned in favour of CTC methods. 6. Annex 6.1. Details on study selection The following databases were searched: Medline, PubMed, Science Direct, Cochrane Library and the York Centre for Reviews and Dissemination databases. A comprehensive search strategy has been developed, using appropriate disease-related MeSH terms and economic filters. Search terms included the following: colonography, virtual colonoscopy, colonoscopy, cost and economics. The keywords were combined and adapted to search the above mentioned databases. For the discussion on the major drivers of CTC cost-effectiveness, a separate search was undertaken in relation to patient preferences considering CTC and COL and the background of non-laxative CTC. Additional articles were found in the references and citations of the retrieved articles (citation snowballing). Sufficient details were required for modelling design and related assumptions, including the related economic and cost aspects. Studies that only included comparison between varying CTC modalities (for example different screening intervals) or a singular focus on clinical performance, were excluded. Studies that did not give enough detail about CTC or COL cost aspects were excluded from the review. A total of 350 full papers have been identified for screening for the review. After additional exclusion criteria were applied, 69 research articles were analysed further. However, a further 60 were excluded from the systematic review itself as they did not meet the full inclusion and exclusion criteria. Some of the articles excluded at this point were included in the general consideration for the review (n = 43), such as the discussion and conclusion. Existing systematic reviews of relevant cost-effectiveness studies have been automatically excluded from the review itself, however some of the findings are analysed in the discussion part of
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the research paper. Several Health Technology Assessments (HTAs) have been released on cost-effectiveness of CTC, however these have also been excluded as most followed an approach of a systematic review. In three HTA cases, these are based on a novel cost-effectiveness model, but the findings have been published in separate research articles and their inclusion or exclusion in the review is based on the published research articles [58–60]. 6.2. PICOS details The details for population, intervention, comparators, outcomes and study design criteria are as follows: Population: population from 50 or 65 years at average risk for colorectal cancer. Intervention: CTC. Comparators: OC. Outcomes: LYS, Cost, ICER. Study Design: Cost effectiveness study. The following criteria were used for study inclusion: • Study methods are described in adequate detail • The study population is clearly described • There is a well defined research question, posed in an answerable form • The disease differentiation is clearly laid out for colorectal cancer • The viewpoints of the analysis are clearly stated There is enough economic detail in the study: • All costs are measured appropriately, i.e. monetary values for disease-specific attributed costs • The chosen time-horizon is appropriate to include relevant costs and consequences • The differentiation of cost aspects and outcome measures in LYS is made appropriately and in physical units • The different cost components are described in sufficient detail The following exclusion criteria were used: • Cost-effectiveness studies only focusing on CTC scenarios • Reviews of existing economic studies related to CTC costefffectiveness • Non-English studies
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Flow chart of search process Titles and abstracts identified and screened n = 3,079 PubMed: n = 719 Science Direct: n = 2,271 CRD York: n = 76 Cochrance Library: n = 13 Excluded n = 2,720
Unable to obtain/further information required to make assessment n = 9
Full copies retrieved and assessed for eligibility n = 350
Excluded n = 273 Not relevant design n = 160 Background discussion n = 81 No relevant outcome n = 9 Duplicate publication n = 23
Studies identified from contact with experts n = 1 Studies identified from searching in reference list n = 3
Foreign language n = 11
Publications meeting inclusion criteria n = 69
Excluded n = 54 Comparison group not relevant n=4 Not relevant outcomes or details not indicated for all outcomes n = 3
Publications included in the review n = 43 Number of studies included in the review n = 9
Role of the funding source The research is supported by the German Federal Ministry of Education and Research (BMBF), project grant No. 01EX1013B, as part of the Centre of Excellence for Medical Technology.
Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ejrad.2013. 07.019.
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Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Review
An international review of the main cost-effectiveness drivers of virtual colonography versus conventional colonoscopy for colorectal cancer screening: Is the tide changing due to adherence? Christine Kriza a,∗ , Martin Emmert b,1 , Philip Wahlster a , Charlotte Niederländer a , Peter Kolominsky-Rabas a a Interdisciplinary Centre for Health Technology Assessment and Public Health, University of Erlangen-Nuremberg, National BMBF-Cluster of Excellence, “Medical Technologies - Medical Valley EMN”, Schwabachanlage 6, 91054 Erlangen, Germany b School of Business and Economics, Institute of Management, University of Erlangen-Nuremberg, Lange Gasse 20, 90403 Nuremberg, Germany
a r t i c l e
i n f o
Article history: Received 29 April 2013 Received in revised form 16 July 2013 Accepted 19 July 2013 Keywords: Computerised tomographic colonography Colonoscopy Colorectal cancer Screening Cost-effectiveness Patient adherence Economics Modelling Simulation
a b s t r a c t Objectives: The majority of recent cost-effectiveness reviews concluded that computerised tomographic colonography (CTC) is not a cost-effective colorectal cancer (CRC) screening strategy yet. The objective of this review is to examine cost-effectiveness of CTC versus optical colonoscopy (COL) for CRC screening and identify the main drivers influencing cost-effectiveness due to the emergence of new research. Methods: A systematic review was conducted for cost-effectiveness studies comparing CTC and COL as a screening tool and providing outcomes in life-years saved, published between January 2006 and November 2012. Results: Nine studies were included in the review. There was considerable heterogeneity in modelling complexity and methodology. Different model assumptions and inputs had large effects on resulting costeffectiveness of CTC and COL. CTC was found to be dominant or cost-effective in three studies, assuming the most favourable scenario. COL was found to be not cost effective in one study. Conclusions: CTC has the potential to be a cost-effective CRC screening strategy when compared to COL. The most important assumptions that influenced the cost-effectiveness of CTC and COL were related to CTC threshold-based reporting of polyps, CTC cost, CTC sensitivity for large polyps, natural history of adenoma transition to cancer, AAA parameters and importantly, adherence. There is a strong need for a differential consideration of patient adherence and compliance to CTC and COL. Recent research shows that laxative-free CTC screening has the potential to become a good alternative screening method for CRC as it can improve patient uptake of screening. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Data from the Global Burden of Disease Study 2010 ranks CRC on fourth place in terms of leading causes of years of life lost for the Western European Region, ranking 10th for high-income North America [1]. The disease burden of CRC will increase in the coming years due to an ageing population, with considerable impact on health care costs [2]. In the last few years, colorectal cancer (CRC) screening using computerised tomographic colonography (CTC), also referred to as virtual colonography, has attracted considerable
∗ Corresponding author. Tel.: +49 9131 8535855; fax: +49 9131 8535854. E-mail addresses: [email protected], [email protected] (C. Kriza), [email protected] (M. Emmert), [email protected] (P. Wahlster), [email protected] (C. Niederländer), [email protected] (P. Kolominsky-Rabas). 1 Tel.: +49 911 5302 253; fax: +49 911 5302 285. 0720-048X/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejrad.2013.07.019
attention, discussion on screening methods and clinical comparisons [3], and was the basis for numerous cost-effectiveness reviews [4,5]. The majority of the reviews concluded that CTC is not a cost-effective screening strategy compared to other screening modalities yet. The objective of this review is to re-examine the cost-effectiveness of CTC as well as its major drivers, especially compared to conventional colonoscopy (COL) given the emergence of new research and data. The importance of the cost-effectiveness of CRC screening becomes all the more important, considering CRC is the third most common cancer worldwide [6]. 2. Methods For this review, studies had to compare CTC and COL as a primary screening tool, provide a related cost-effectiveness analysis for the two strategies and provide outcomes in life-years saved (LYS) in order to enable comparability. Studies published in peer reviewed
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Table 1 ICER results: overview. Study
More effective screening
Less costly screening
ICER of more effective to less effective
Assuming most favourable scenario for CTC
1 2 3 4 5 6 7 8 9
COL COL CTC CTC CTC COL COL COL COL
CTC CTC COL CTC COL CTC CTC COL CTC
COL vs CTC: D 15,091/LYS COL vs CTC: $63,900/LYS CTC vs COL: $156,000/LYS CTC dominates CTC vs COL: $2,144/LYS COL vs CTC: $498,668/LYS COL vs CTC: £42,000/LYS COL dominates CTC vs COL: $44,000/LYS
CTC 10yrs Scenario 2, CTC 10yrs Scenario 2, CTC 5yrs Scenario 3, CTC 10yrs CTC 10yrs Scenario 3, CTC 10yrs CTC 10yrs All scenarios assuming perfect adherence Scenario SIM-CRC, 50% adherence, CTC 5
journals between January 2006 and November 2012 were included in the review. The search methodology was in line with PRISMA guidelines [7], including the use of the PICOS review system (see details in the Annex). The selection criteria have been adapted from the CHEC-list (Consensus on health economic criteria) [8], and the CRD’s guidance for undertaking systematic reviews in health care, specifically the section on systematic reviews on economic evaluations (more details on methodology are provided in the Annex). The search results were independently reviewed and screened by two researchers who then independently extracted the relevant data. For each study included in the review, data was extracted on the parameters shown in the header columns in Supplementary Tables I and II. All studies that were included in the systematic review met the quality criteria according to the CRD’s checklist for assessing economic evaluations, sufficiently detailing study design, results and analysis. 3. Results
started from $498 for the American setting, ranging up to $877 (See supplementary Table I). When indirect costs were considered, COL costs ranged up to $1,100. CTC costs varied from $478 for the American setting, ranging up to $665, with Computer Assisted Detection (CAD) up to $715, and peaking at $814 when indirect costs were considered. CTC/COL cost ratios ranged from 0.26 to 0.98. Costs for COL and polypectomy ranged from $831 to $1,265. For the European setting, COL costs started from D 148 with CTC costs at D 101 and COL and polypectomy at D 229. The cost assumptions for cancer care varied between the studies in terms of cost components and sophistication of differentiating stages of cancer care. For the European setting, such costs started from D 14,940 for Early CRC and D 24,900 for Late CRC. For the American setting, cancer care costs started at $45,228 and ranged up to consideration of the societal perspective, considering CRC stages I–IV and phases of care, with costs for each combinations ranging from $2,719 up to $78,227, resulting in considerably higher care costs. In addition, studies differed in cost assumptions for cost of complications such as cost of treating colon perforation (ranges from $13,000 to $22,269), as well as consideration of extracolonic findings.
3.1. Overall study features 3.3. Incremental cost effectiveness ratios Due to the strict application of quality criteria, a total of nine studies were included in the systematic review. A majority of 7 studies were based on US data, with 1 study based on Italian and 1 study based on British data. All studies focused on a screening population at average risk of CRC (for full information on study features, see supplementary Table I). The majority of seven studies used either Markov cohort modelling or state transition type Markov models as methodology. Two studies used micro simulation methods which are based on a hybrid modelling approaches, using discrete event and Markov modelling aspects. All of the studies included COL and CTC in their screening scenario, but there was a large variety in the scenarios used in the studies. As such, different scenarios were used for management and reporting of polyps for CTC and time frames for CTC were either every five or ten years. Two studies applied inclusion of extra colonic finding benefits, specifically related to abdominal aortic aneurisms (AAA) for CTC in their scenarios. One study differentiated between CTC without CAD (Computer Assisted Detection) and with CAD, and also between experienced and inexperienced readers. One study used data for CTC accuracy from different sources, thereby creating separate scenarios. Two studies included scenarios from different microsimulation models, and one of these studies specified data from a 50% adherence scenario. Additional polypectomy costs as a follow-up of colonography were considered in the review studies. 3.2. Costs Costs for both screening strategies were influenced by the study perspective and consideration of direct and indirect costs. COL costs
All of the studies included in the review found CTC to be costeffective compared to “no screening” (this was not applicable in study 7, as a ‘no screening’ option was not considered). Costeffectiveness thresholds were used in most studies, although there were differences in which these thresholds were calculated. Assuming the most favourable scenario for CTC and disregarding other screening modalities except for COL and CTC, the results still varied considerably between the nine studies (see Table 1, ICER results). COL dominated in study 8 [9], although only the scenarios assuming perfect adherence were considered, as outcome data for less than perfect adherence was not indicated. CTC dominated in study 4 [10], considering the scenario for CTC every 10 years. COL was the more effective screening strategyin four studies: 1, 2, 6 and 7 [11–14]. The ICERs of COL vs. CTC in these studies ranged from D 15,091/LYS up to $498,668/LYS. In two studies, 3 and 5 [12,15], CTC was the more effective screening strategy. The ICERs of CTC vs. COL in these studies ranged from $2,144/LYS up to §156,000/LYS. Further factors had a major influence on the cost-effectiveness of COL and CTC, such as clinical management of CTC-detected polyps, screening accuracy, extracolonic findings, CRC national history assumptions and adherence related issues. 3.4. Sensitivity of COL and CTC and threshold reporting Sensitivity for COL was indicated according to polyp sizes. Sensitivity for polyps ≤5 mm ranged from 75-92.4%, for polyps sizes 6–9 mm: 85–95%, polyp size ≥10 mm: 88.3–95% and CRC: 88.3–95%. Sensitivity for CTC was also indicated according to polyp
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sizes, and in most studies, sensitivity for polyps ≤5 mm was not applicable due to the reporting threshold of polyps measuring at least 6 mm. Sensitivity for polyps sizes 6–9 mm ranged from 57 to 88%, polyp size ≥10 mm: 84–92% and CRC: 84–95%. Seven of the nine studies included a referral/reporting threshold for CTC of polyps measuring at least 6 mm in at least one of their scenarios. This practice has been widely discussed [4,16] and is not without its controversies [17]. However, in recent years, this practice has been established in order to address over-detection and apply a cost-effective approach [18]. Details on specificity of the screening approaches are given in Supplementary table I. 3.5. Extra-colonic findings, AAA Two studies included assumptions on the benefits of extracolonic findings in their modelling (4 and 5). Primarily, these benefits referred to the detection of abdominal aortic aneurisms (AAA), rather than extra colonic cancers in the lung, liver, pancreas and ovaries. Whereas screening of such cancers has not proved to be effective, there is strong data on screening effectiveness for AAA [19,20]. Incorporating the benefits of these assumptions had a considerable impact on showing CTC to be either dominant over COL, or cost-effective. 3.6. Natural history of colorectal cancer The most important assumptions on the natural history of CRC in the studies referred to polyp growth and speed of cancer development, overall prevalence of polyps before screening by age and the development of de novo cancer. The studies which based their models on Markov-type methods, used different approaches for natural history than the micro simulation models. For the former, natural history assumptions evolved by publication date in terms of more detail used and sophistication of assumptions. Six such studies indicated adenoma/polyp prevalence at age 50, ranging from 15 to 20%/age 65:40%. A new polyp rate for the periods 50–60y, 60–70y and 70–80y was considered in addition, with rates ranging from 1.9 to 3.3%. Annual transition rates from diminutive polyp sizes to small polyp sizes, from small to large and from large to early CRC were indicated, i.e. from ≤5 mm to 6–9 mm: 2–4; from 6 to 9 mm to ≥10 mm: 2–4; from ≥10 mm to early CRC: 3–4. Rates from early CRC to late CRC, or regional CRC to distant CRC ranged from 30 to 40 and rates for de novo cancer ranged from 0.008 to 0.16 (age specific). De novo prevalence rates of CRC ranged from 85 to 90. One study used a different methodology for annual probability of progression and disease classification (See Supplementary Table I, Study 7). Two studies considered the natural history of abdominal aortic aneurism. The two studies which used micro simulation approaches based their natural history assumptions on complex functional forms for adenoma growth and progression. (See Supplementary Table I, Studies 8 and 9). 3.7. Screening adherence, compliance and safety The term adherence is used to describe uptake of initial testing, whereas the term compliance relates to follow-up testing-used according to [11] and [12]. Screening assumptions for adherence and compliance varied across the studies. Most studies used a baseline scenario, with specific assumptions, ranging from 60% to 100% for adherence and 80–100% for compliance with both CTC and COL screening. Differential adherence scenarios were then modelled, ranging from 20 to 100%. However, only one study considered differential adherence scenarios between CTC and COL screening specifically (Study 8). These assumptions have a major impact on the simulation outcomes and will be analysed further in the discussion.
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All studies considered bowel perforation and bleeding as a medical complication arising from COL and CTC. The safety parameters referring toperforation rates for CTC and COL ranged from 0.002 to 0.1%, with clear advantages of CTC regarding the safety profile. One study included assumptions of CTC radiation exposure and related cancer risk, concluding that the numbers of deaths as a result of radiation-related cancer were less than due to serious complications resulting from COL screening [10]. 3.8. Sensitivity analysis All nine studies included in the review used univariate sensitivity analysis in order to examine uncertainty, with a majority of studies applying multivariate sensitivity analysis through Monte-Carlo methodology. The most important assumptions that influenced the cost-effectiveness of CTC and COL were related to CTC threshold-based reporting of polyps, CTC/COL cost ratio, CTC sensitivity for small and large polyps, natural history of adenoma transition to cancer, AAA parameters, time intervals of screening and importantly, adherence. 4. Discussion There was considerable heterogeneity in modelling complexity and methodology, but especially in the model assumptions and inputs mentioned above. These all had large effects on resulting cost-effectiveness of CTC and COL. We will discuss the main drivers that are likely to affect CTC cost-effectiveness and examine related assumptions in the light of new research data. The main cost-effectiveness drivers can be identified in the area of costs, natural history, diagnostic sensitivity and importantly adherence and compliance. In our discussion, we attempt to focus on issue of adherence while also considering the impact of new research in the area of non-laxative CTC methods which suggest improvements of screening patients’ uptake to participate. 4.1. Costs and effects Overall, CTC was found to be dominant or cost effective in three studies, assuming specific scenarios. COL was found to be not cost effective in one study with a specific scenario. In the remaining studies where CTC was found to be not cost-effective, it would be possible to transform CTC towards cost-effectiveness when altering assumptions on costs, adherence and for some studies, natural history assumptions and CTC accuracy. Considering the results presented in this review, it is important to highlight the importance of cost data used for CTC and COL. For the European setting, it has been previously pointed out that costs appear to be lower for CTC due to different health system settings [11]. New research by de Haan [21] has concluded that Dutch costs of CTC are considerably lower than cost assumptions previously used in cost-effectiveness models. The research findings point out average costs per participant within an invitational population-based screening programme at D 169.40. When considering indirect costs, the advantages for CTC become more pronounced. Due to the increasing use of costly biological agents for the treatment of CRC, the consideration of a changing pattern in the Cost of illness of CRC becomes important [22]. The implications are increasing costs and the possibility to avert costs incurred for CRC treatment through screening programmes. 4.2. Natural history Microsimulation methodology allows for dynamic modelling of growth, which has potential advantages for realistically simulating natural history. It enables for the simulation of multiple
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adenoma/polyp sizes and locations, as opposed to more rigid adenoma states in the Markov models. However, comparing natural history assumptions of CRC becomes difficult as a result. In addition, different data sources were used for polyp/adenoma prevalence and other assumptions. Importantly, varying categories and the rate at which adenomas progress to cancer seem to be the most crucial aspects of natural history assumptions [23]. Consideration of abdominal aortic aneurism natural history and its related benefits of CTC screening seem to also have an important impact, which necessitates further critical review and research. New data has been presented on the risk of progression of advanced adenomas to CRC by age and sex which suggest that transition rates in older age groups are in line with previous estimates but considerably lower for younger age groups [24]. The impact of new research related to the understanding of polyp and CRC natural history needs to be considered for the design of future cost-effectiveness studies. 4.3. Sensitivity New data from larger CTC studies is emerging which points towards higher sensitivity and specificity rates than used in most of the studies included in the review [25,26], with findings also valid for older age groups [27]. In addition, updated meta-analysis also support the validity of higher CTC sensitivity and specificity than those used in the reviewed studies [28,29]. The use of CAD either concurrently or as a second reader has been connected with a considerable increase in sensitivity for detecting large polyps (6 mm and above). Relevant increases vary according to the experience of the reader and is indeed higher in those without specific experience in CTC (Regge et al.). However, there is a significant need to improve the training and expertise in CTC readers in addition to CAD. For consistently high senstitivity results, health policy makers would be required to address training and expertise improvements for CTC reading. 4.4. Adherence and compliance and the impact of new research The adherence and compliance levels used in the model assumptions of all of the studies are overestimating real-life data on uptake of COL and CTC. According to a similar review by van Gils for an earlier time period, this trend of modelling to use higher adherence rates than data from trials indicate has been highlighted, with average adherence in models at 78%, while data from trials regarding the adherence of colonoscopy and CTC refer to rates often under 30% [30]. The theoretical threshold of 50% participation for effective mass screening is often not realistic in clinical practice. While in a US setting, adherence per se has been cited to be as high as 50–60% [26,31], the figures for a European setting are much lower. In the German setting, data from 2010 indicates that only 3% of those entitled per year participated in colonoscopies that are an integral element of CRC screening according to German guidelines [32–34]. In addition, screening uptake rates are also often cited in different manners, sometimes referring to annual participation rates of eligible patients, in Germany below 3%, cumulated rates for a 5 year period (in Germany, such figures rise up to 20%), or screening participation ever (in Germany, up to 55%) [32,35,36]. Knudsen et al. suggest in their study that CTC could be a costeffective CRC screening option for Medicare enrollees CTC costs are substantially lower than those of COL, or if 25% of otherwise unscreened persons opted for CTC screening [9]. In response to this study [9], Pickhardt [37] argued that the latter condition would be met as data from the largest CTC screening experience in the US shows that nearly 40% of individuals screened by CTC would have foregone screening if CTC had not been offered [38]. In another study, roughly 80% of a nonadherent urban cohort indicated their
willingness to use CTC screening [39]. New research supports this argument as follows. CTC has one major advantage over COL in that it is less invasive in nature. Recent research findings suggest that CTC using noncathartic, or laxative-free, bowel preparation approaches together with faecal tagging, showed positive effects in terms of high sensitivity for advanced adenomas and high patient acceptability of the procedure [40,41]. Bowel preparation is reported to be one of the main sources of patient discomfort and a barrier to the uptake of screening [42,43]. A recent systematic review and meta-analysis of patient preference for COL versus CTC showed that screening patients preferred CTC, with studies featuring limited bowel preparations for CTC reporting marked CTC preference [44]. Further consideration on how to target specific subgroups of patients, for whom uptake of screening have been low can be crucial [43,45–48]. Research findings from a Dutch RCT comparing CTC and COL showed that participation in screening with CTC was significantly better than with COL [40]. The study demonstrates a 55% improvement in screening participation with CTC over COLfrom 22% for COL to 34% to CTC [49]. Although the iodinated contrast material was connected with some patient discomfort [50], different tagging methods led to improved patient experience [41]. A recent study on thediagnostic accuracy of laxative-freeCTC found high accuracy in detecting adenomas 10 mm larger but less so for smaller lesions [41]. Patient experience was better with laxative-free CT. Participants in the study indicated that laxative-free CTC is more comfortable and easier to prepare for, and it was the preferred screening method for 62% of respondents. According to Zalis, CTCs currently cost about one-third as much as COL, and it is to be expected that a laxative-free version would cost the same [41]. 4.5. Study limitations A major limitation of this review is the limited number of studies included due to very strict quality criteria. In addition, of the total of nine studies, 5 studies have been published by the same author group. Seven of the nine studies provide an analysis of scenarios from the United States, which reduces the aspect of the international perspective of the review. However, even given the specific limitations of the studies analysed, certain commonalities and trends could be extracted from the analysis of the different studies. The focus of the review was to highlight and discuss the most important findings.Issues that also have an impact of the cost-effectiveness, such as radiation and the impact of extra colonic findings have not been analysed in sufficient detail, but have been subject of previous research and reviews [51–53]. 5. Conclusion There has been an established development in the last years, whereby CTC is considered cost-effective compared to noscreening [5,23], which is also supported by this review. CTC has the potential to be a cost-effective CRC screening strategy when compared to COL. The main modelling assumptions that are likely to render CTC cost-effective are connected to natural history concepts, especially the rate in which large adenomas progress to CRC, a finding first suggested by [23] and confirmed by [54]. In addition, the consideration of AAAs for the benefits of CTC extracolonic findings are an important factor that positively influence CTC cost-effectiveness. Model inputs regarding CTC cost and accuracy aspects are also crucial, and current research is emerging that shows low CTC costs, especially in a European setting alongside higher accuracy for CTCs, also for older populations. The most important assumption highlighted in this review is the need for a differential consideration of patient adherence and compliance
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to CTC and COL. The importance of patient adherence has been pointed out previously [4,30,55–57], but the specific significance of non-laxative CTC methods is highlighted in this review. Recent research shows that laxative-free CTC screening has the potential to become a good alternative screening method for CRC as it can improve patient uptake of screening. Our review suggests that if cost-effectiveness modelling applies real adherence and compliance rates that have been observed in clinical practice, the cost-effectiveness balance is likely to be turned in favour of CTC methods. 6. Annex 6.1. Details on study selection The following databases were searched: Medline, PubMed, Science Direct, Cochrane Library and the York Centre for Reviews and Dissemination databases. A comprehensive search strategy has been developed, using appropriate disease-related MeSH terms and economic filters. Search terms included the following: colonography, virtual colonoscopy, colonoscopy, cost and economics. The keywords were combined and adapted to search the above mentioned databases. For the discussion on the major drivers of CTC cost-effectiveness, a separate search was undertaken in relation to patient preferences considering CTC and COL and the background of non-laxative CTC. Additional articles were found in the references and citations of the retrieved articles (citation snowballing). Sufficient details were required for modelling design and related assumptions, including the related economic and cost aspects. Studies that only included comparison between varying CTC modalities (for example different screening intervals) or a singular focus on clinical performance, were excluded. Studies that did not give enough detail about CTC or COL cost aspects were excluded from the review. A total of 350 full papers have been identified for screening for the review. After additional exclusion criteria were applied, 69 research articles were analysed further. However, a further 60 were excluded from the systematic review itself as they did not meet the full inclusion and exclusion criteria. Some of the articles excluded at this point were included in the general consideration for the review (n = 43), such as the discussion and conclusion. Existing systematic reviews of relevant cost-effectiveness studies have been automatically excluded from the review itself, however some of the findings are analysed in the discussion part of
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the research paper. Several Health Technology Assessments (HTAs) have been released on cost-effectiveness of CTC, however these have also been excluded as most followed an approach of a systematic review. In three HTA cases, these are based on a novel cost-effectiveness model, but the findings have been published in separate research articles and their inclusion or exclusion in the review is based on the published research articles [58–60]. 6.2. PICOS details The details for population, intervention, comparators, outcomes and study design criteria are as follows: Population: population from 50 or 65 years at average risk for colorectal cancer. Intervention: CTC. Comparators: OC. Outcomes: LYS, Cost, ICER. Study Design: Cost effectiveness study. The following criteria were used for study inclusion: • Study methods are described in adequate detail • The study population is clearly described • There is a well defined research question, posed in an answerable form • The disease differentiation is clearly laid out for colorectal cancer • The viewpoints of the analysis are clearly stated There is enough economic detail in the study: • All costs are measured appropriately, i.e. monetary values for disease-specific attributed costs • The chosen time-horizon is appropriate to include relevant costs and consequences • The differentiation of cost aspects and outcome measures in LYS is made appropriately and in physical units • The different cost components are described in sufficient detail The following exclusion criteria were used: • Cost-effectiveness studies only focusing on CTC scenarios • Reviews of existing economic studies related to CTC costefffectiveness • Non-English studies
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Flow chart of search process Titles and abstracts identified and screened n = 3,079 PubMed: n = 719 Science Direct: n = 2,271 CRD York: n = 76 Cochrance Library: n = 13 Excluded n = 2,720
Unable to obtain/further information required to make assessment n = 9
Full copies retrieved and assessed for eligibility n = 350
Excluded n = 273 Not relevant design n = 160 Background discussion n = 81 No relevant outcome n = 9 Duplicate publication n = 23
Studies identified from contact with experts n = 1 Studies identified from searching in reference list n = 3
Foreign language n = 11
Publications meeting inclusion criteria n = 69
Excluded n = 54 Comparison group not relevant n=4 Not relevant outcomes or details not indicated for all outcomes n = 3
Publications included in the review n = 43 Number of studies included in the review n = 9
Role of the funding source The research is supported by the German Federal Ministry of Education and Research (BMBF), project grant No. 01EX1013B, as part of the Centre of Excellence for Medical Technology.
Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ejrad.2013. 07.019.
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