Review article 141
Health system costs of skin cancer and cost-effectiveness of skin cancer prevention and screening: a systematic review Louisa G. Gordona,b and David Rowella The objective of this study was to review the literature for malignant melanoma, basal and squamous cell carcinomas to understand: (a) national estimates of the direct health system costs of skin cancer and (b) the cost-effectiveness of interventions for skin cancer prevention or early detection. A systematic review was performed using Medline, Cochrane Library and the National Health Service Economic Evaluation Databases as well as a manual search of reference lists to identify relevant studies up to 31 August 2013. A narrative synthesis approach was used to summarize the data. National cost estimates were adjusted for country-specific inflation and presented in 2013 euros. The CHEERS statement was used to assess the quality of the economic evaluation studies. Sixteen studies reporting national estimates of skin cancer costs and 11 costeffectiveness studies on skin cancer prevention or early detection were identified. Relative to the size of their respective populations, the annual direct health system costs for skin cancer were highest for Australia, New Zealand, Sweden and Denmark (2013 euros). Skin cancer prevention initiatives are highly cost-effective and may also be cost-saving. Melanoma early detection programmes
Introduction
aimed at high-risk individuals may also be cost-effective; however, updated analyses are needed. There is a significant cost burden of skin cancer for many countries and health expenditure for this disease will grow as incidence increases. Public investment in skin cancer prevention and early detection programmes show strong potential for health and economic benefits. European Journal of Cancer Prevention 24:141–149 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. European Journal of Cancer Prevention 2015, 24:141–149 Keywords: cost of illness, cost-effectiveness, keratinocyte skin cancer, melanoma, screening a
School of Medicine, Centre for Applied Health Economics and bPopulation and Social Health Research Program, Griffith Health Institute, Griffith University, Logan Campus, Queensland, Australia Correspondence to Louisa G. Gordon, PhD, School of Medicine, Centre for Applied Health Economics, Griffith University, Logan Campus, University Drive, Meadowbrook, QLD 4131, Australia Tel: + 61 7 3382 1320; fax: + 61 7 3382 1160; e-mail: [email protected] Received 24 January 2014 Accepted 15 May 2014
In many countries with fair-skinned populations, the incidence of skin cancers is increasing (Garbe and Leiter, 2009). Exposure to ultraviolet radiation, either naturally from the sun or artificially through solarium use, is the main cause of skin cancers. Incidence will continue to increase as nations with ageing populations enter the prime ages for onset of keratinocyte skin cancers (i.e. squamous and basal cell carcinomas). Malignant melanoma, the most serious of all skin cancers, is also increasing in incidence and not only arises in older adults but also in young adults. Consequently, the healthcare costs of managing skin cancers are set to expand quickly. These costs are fuelled not only by ageing demographics but also by health price inflation, more expensive health services and new technologies, and a higher frequency of health services per person (Australian Institute of Health and Welfare, 2012; OECD, 2013). Individuals will also be carrying the burden of disease through direct copayments or losses in income.
Healthcare systems face increasing pressure to meet the higher demand for medical services with constrained budgets. Economists in Europe believe that the current growth in healthcare spending is not sustainable at current levels (OECD, 2013). They propose that governments should not support harsh cost-cutting initiatives but rather focus on innovative ways to improve efficiencies and eliminate wasteful spending. In effect, this requires decisions to redistribute funding from relatively inefficient to more efficient health services. Costeffectiveness analysis provides a framework for a systematic comparison of the relative healthcare costs and benefits of alternative strategies for the purpose of informing decision-makers about whether interventions show good value for money. This process of assessing cost-effectiveness requires the synthesis of data on the natural history of the disease, current clinical practice and management patterns, medical costs and health outcomes of the interventions. Cost-effectiveness analysis is an essential component of decision-making about new services and medicines in many health systems.
All supplementary digital content is available directly from the corresponding author.
There are very few studies investigating the costeffectiveness of interventions designed to control
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DOI: 10.1097/CEJ.0000000000000056
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142 European Journal of Cancer Prevention 2015, Vol 24 No 2
keratinocyte skin cancers and actinic keratosis and relatively more for malignant melanoma where chemotherapy options are available (Higashi et al., 2004). To understand the economic burden of skin cancer management and the relative economic literature of skin cancer prevention and early diagnosis across different health systems, we performed a review of the health economic literature for malignant melanoma, basal and squamous cell carcinomas. Specifically, we have consolidated the literature on (a) the direct health system costs of skin cancer at a country level and (b) the costeffectiveness analyses for prevention or screening interventions for skin cancer. The PRISMA statement was used to guide the review (Liberati et al., 2009).
Materials and methods Search strategy
A search was performed using Medline, The Cochrane Library and the National Health Service Economic Evaluation Database. A manual search of reference lists in the selected studies was performed as was a brief search for cost reports on Google search engine. No limitations on dates were imposed and only Englishlanguage articles were extracted. Searches were limited to the title/abstract fields and available full-text articles. Search terms included ‘costs’ ‘cost-effectiveness’ ‘costutility’ ‘economic evaluation’ ‘burden’ ‘cost-of-illness’ and combinations of ‘skin cancer’ ‘skin carcinoma’ ‘melanoma’ ‘non-melanoma’ ‘SCC & BCC’ ‘basal cell carcinoma’ ‘squamous cell carcinoma’ ‘BCC’ ‘SCC’ and ‘keratinocyte’. Cost studies were excluded if they were single-centre studies or did not include a wide range of costs (e.g. if they focused on one category of cost such as ‘adverse events’ of treatment or included a subgroup of patients such as those with organ transplants) or they did not report national cost estimates. Cost-effectiveness studies were excluded if they were not for the purpose of skin cancer prevention or early detection or were not a full economic evaluation [i.e. they did not assess both the relative costs and effects between an intervention and an alternative option(s)]. Two researchers performed the searches, and discrepancies in the chosen studies were resolved by further discussion.
reviewed according to each criterion and judged to be either fully, partially or not fulfilling the criteria. A narrative synthesis of the studies was performed to summarize the findings as it was not appropriate to use meta-analysis techniques. However, to ease the interpretation of the cost results when multiple currencies were reported across the studies and at different time periods, costs were first inflated to 2012/2013 prices using countryspecific inflation rates and then converted into Euros using exchange rates (http://www.xe.com, August 2013).
Results A total of 124 unique articles were identified in the database searches. Of these, 88 were immediately excluded after screening titles and abstracts. This was mostly because it was not a cost or cost-effectiveness study or studies related to treatments or diagnostic technologies for skin cancer control (Fig. 1). Closer assessment of the remaining 36 studies led to the exclusion of a further 12 studies because they did not report national estimates or they reported only partial costs. Three studies were added to the review after searching the internet for cost reports (O’dea, 2009; H. Krueger & Associates Inc., 2010) or manually searching reference lists of the chosen studies. In all, 27 studies were included in this review: 16 cost-ofillness studies, seven cost-effectiveness studies relating to prevention of skin cancer and four studies on the costeffectiveness of early detection (screening) of melanoma. A summary of the main features of studies included in the review is provided in Table 1 for cost-of-illness studies with national estimates and Table 2 for the costeffectiveness studies. Fig. 1
Potentially relevant studies identified in the search (n=124) Studies excluded (n=88) Not skin cancer (13) Not cost studies or economic evaluations (21) Studies assessing diagnosis/imaging (13) Studies assessing treatments (35) Studies assessing surveillance (3) Wrong study type (3) Studies retrieved for more detailed evaluation (n=36) Studies excluded (n=12) Partial costs only (8) Superseded study (1) National cost estimates not reported (3)
Synthesis and study quality
The results of the studies were combined into a spreadsheet, listing the major features of the studies. The data extracted were year of publication, setting, cost perspective, price year, cost estimates, strengths and limitations. For the cost-effectiveness studies, an assessment of their reporting quality was performed using the Consolidated Health Economic Reporting Standards (CHEERS) checklist (Husereau et al., 2013). The CHEERS statement recommends that 24 criteria be included in any report of a full economic evaluation (e.g. cost-effectiveness or cost-utility analysis). Studies were
Added studies identified through grey literature (2) or reference lists (1) Total identified = 3
Studies selected for review (n=27) Cost-analyses (n=16) Cost-effectiveness analysis (n=11)
Flow chart of literature search outcomes.
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Both SCC and BCC
USA
Sweden
Germany
France
New Zealand
Brazil
USA
Canada
Brazil
USA
Australia
Denmark
UK
Housman et al. (2003)
Tinghög et al. (2008)
Stang et al. (2008)
Chevalier et al. (2008)
O’dea (2009)
Souza et al. (2009)
Seidler et al. (2010)
H. Krueger & Associates Inc. (2010) Souza et al. (2011)
Rogers and Coldiron (2013)
Fransen et al. (2012)
Bentzen et al. (2013)
Vallejo-Torres et al. (2013)
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of the article is prohibited. Top-down, Australia Medicare, estimated hospital costs Population registers, linked data, matched controls, bootstrapping Top-down and bottom-up, administrative reports, national statistics, unit costs
Top-down, unit costs applied to incidence, n = 42 184, Sao Paulo state Top-down, US Medicare and Medicaid
Top-down, cancer registries
Bottom-up, unit costs applied to NCCN pathways Top-down, US Medicare linked to SEER (n = 1858)
Bottom-up, hospitalization data, unit costs
Top-down, Hospital database – national, n = 7000 prevalent costs
Top-down and bottom-up, unit costs applied to national statistics Top-down, hospitalization data on inpatients only
Bottom-up, unit costs applied to pathways – steady state model Top-down, US Medicare Top-down, hospitalization and other statistics (n = 26 848) Top-down, US Medicare, ICD codes, mostly > 65 years
Approach/datasets
1998–2010 2007–2008
Health system (NHS) UK
1997–2010
1996–2008
2000–2007
2004 + projected
1991–1996
2000–2007
2006
2004
2003
2005
1992–1995
1992–1995 1999
1997
Timing
Societal
Health system
Institution
Health system
Societal
Institution
Health system
Societal
Institution
Institution
Societal
Health system
Institution Societal
Health system
Perspective
Key results of direct costs per year (price year)
€33.3 million for SCC and BCC and MM (2010), 59% costs for MM, 0.2% of Danish health budget £112.4 million for SCC and BCC and MM (2008) top-down, 20% costs for MM, £106 million bottom-up (including benign)
€50–60 million for MM, €105–130 million for SCC and BCC, SCC and BCC to MM ratio: 2.2 men and 1.9 women, MM and SCC and BCC are 2% of all cancer hospitalizations, 20 455 MM, 41 929 SCC and BCC hospitalizations €59 million (2004), €27 million for metastasized MM, 1% of hospital costs, components: chemotherapy 17%, hospital costs 38%, followup evaluations 20% NZ$5.7 million for MM (2007/08), $51.4 million for SCC and BCC, $2 million for prevention activities by Cancer Society R$33 million for MM in public sector (2007), R$76 million for MM in private sector, very high costs for advanced stage III and IV MM US$249 million for MM in > 65 year olds (1996), $28 000 per patient lifetime cost, expensive in late stage, comparable with other terminal cancers CAN$36.5 million for SCC and BCC (2004), CAN$29.6 million for MM R$37 million for SCC and BCC in public sector, R$26 million for SCC and BCC in private sector US$633.4 million in 2008, 90% of skin cancers treated in office-based settings, Medicare part B charges increased 137% over time AU$511 million for SCC and BCC (2010), 767 347 treatments
$US562 million (1998) for SCC and BCC, SCC and BCC is the fifth most costly cancer, US$28 million for MM, cost per patient nearly doubled 1995–1998 €22 million for MM (2005), €31 million for SCC and BCC
$US563 million for MM (1997), 11% costs for stage I and II, 89% costs for stage III and IV, $30 000 for interferon treatment per year $US426 million SEK 23 064 000 for MM (1999), SEK 17 584 000 for SCC and BCC
BCC, basal cell carcinoma; ICD, international classification of disease; MM, malignant melanoma; NHS, National Health Service; SCC, squamous cell carcinoma.
Both plus benign
Both
SCC and BCC
Both
MM
MM
Both
MM
Both plus benign Both
SCC and BCC Both plus benign Both
USA Sweden
Chen et al. (2001) Nilsson et al. (2003)
MM
MM or SCC and BCC
USA
Country
Key features of studies reporting national estimates of the direct healthcare costs of skin cancer
Tsao et al. (1998)
Reference
Table 1
Cost-effectiveness of skin cancer prevention Gordon and Rowell 143
MM focus
USA
USA
Losina et al. (2007)
BCC, basal cell carcinoma; MM, malignant melanoma; SCC, squamous cell carcinoma.
Routine use
MM focus
Australia
Sunscreen – regular use
SCC and BCC
Australia
Gordon et al. (2009) Hirst et al. (2012)
Routine use
All skin cancer All skin cancer
Australia Australia
Hirst et al. (2009) Shih et al. (2009)
Do nothing
Sunscreen – regular use
School-based programme
All skin cancer
Do nothing
Do nothing Current programme
Educational campaign
MM focus
Do nothing
No screening
No screening
No screening
No screening
Comparator
Solaria regulation SunSmart – multifaceted
Health campaign – early detect
MM focus
Screening individuals > 50 years of age, by GP, 2-yearly screen Screening high-risk, by dermatologist, onetime screen Screening by dermatologist white population average risk Screening general population, biannual, family history
Intervention and comparator(s)
Skin cancer prevention Cristofolini et al. Italy (1993) Garattini et al. Italy (1996) Kyle et al. (2008) USA
MM focus
MM focus
USA
MM focus
MM or SCC and BCC
Freedberg et al. (1999) Beddingfield (2002)
Melanoma screening Girgis et al. (1996) Australia
Setting
Key results of studies on the cost-effectiveness of skin cancer screening and prevention
References
Table 2
Government + individuals
Government + individuals
Government Government + individuals
Government + productivity
Government
Government + individuals
Government
Government
Government
Government
Perspective
Lifetime model
1992–1996
Lifetime model 1998–2006, high low investments
1999–2015
Pre 1977–1982, post 1977–1981, 1982–1985 1993
Lifetime model
Lifetime model
Lifetime model
Lifetime model
Timing
AU$40 890 per QALY
US $31.2 million cost-savings, return on investment $1.95–4.02 Cost-savings to government AU$680 per life-year saved, $180million net cost-savings, return on investment $2.30 Cost saving to government
$US3 357 per life-year saved (1993)
$400 per life-year saved
$51 481 per life-year saved, one time, lower in over 50s $80 700 per quality-adjusted life-year
$12 137 per life-year saved for men 50 years $39 600 per life-year saved (1996 US)
Incremental cost-effectiveness ratio
144 European Journal of Cancer Prevention 2015, Vol 24 No 2
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Cost-effectiveness of skin cancer prevention Gordon and Rowell 145
Cost studies Yield and study setting
Sixteen studies reported the direct health system costs of skin cancer at a country level (Table 1), and were published from 1996 to 2013. Studies were located in the following countries: Australia (Fransen et al., 2012); New Zealand (O’dea, 2009), Brazil (Souza et al., 2009; Souza et al., 2011), USA (Chen et al., 2001; Housman et al., 2003; Seidler et al., 2010; Rogers and Coldiron, 2013), UK (Vallejo-Torres et al., 2013), Denmark (Bentzen et al., 2013), Sweden (Nilsson et al., 2003; Tinghög et al., 2008), Germany (Stang et al., 2008), France (Chevalier et al., 2008), Italy (Johnston et al., 2012; Maio et al., 2012) and Canada (H. Krueger & Associates Inc., 2010). Unpublished reports were provided for cost studies in New Zealand and Canada (O’dea, 2009; H. Krueger & Associates Inc., 2010). Perspective and scope
Generally, studies adopted a health system perspective for the resources included and others had an institutional (e.g. public hospital or US Medicare) perspective. In most studies, the major direct treatment costs of skin cancers included were doctor visits, biopsies, surgical excisions, cryotherapy and hospital stays. Several studies also included indirect costs such as lost productivity, Fig. 2
future health and mortality costs. Some studies that examined resources for skin cancers also included resources for benign skin lesions (O’dea, 2009; Vallejo-Torres et al., 2013). All studies recognized and acknowledged limitations with the scope or quality of their datasets. These limitations were because of the unavailability of all possible cost components and/or were broad estimates only. Costing methods
The costing methods can be grouped into a ‘top-down’ or a ‘bottom-up’ approach. The top-down method is where large administrative datasets were analysed and distilled down to pertain only to skin cancer costs for the final estimation (Housman et al., 2003; Stang et al., 2008; Souza et al., 2011; Fransen et al., 2012). The bottom-up approach was used when patterns of care and management resources were determined and unit costs were assigned to each service and aggregated ‘up’ to a final total. Some studies used both approaches (Tsao et al., 1998; O’dea, 2009; Vallejo-Torres et al., 2013). To obtain national estimates, costs were often extrapolated according to national incidence or prevalence data. This in itself created further uncertainty in estimates as squamous and basal cell carcinomas are not formally registered in many countries. Costs were descriptive and one study provided cost findings in the form of ‘attributable’ costs by including a matched control group and calculating the difference between cancer and noncancer groups (Bentzen et al., 2013).
700
Healthcare cost estimates Melanoma SCC/BCC
600
500
400
300
200
100
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Annual direct healthcare costs for melanoma and keratinocyte skin cancers (€2013 million). Note: Fransen et al. (2012) (Australia) did not report costs for melanoma. These were estimated as a proportional extrapolation from an earlier report (Australian Institute of Health and Welfare, 2005). BCC, basal cell carcinoma; SCC, squamous cell carcinoma.
Figure 2 provides the results of annual direct healthcare costs by country in 2013 Euros. Each country is represented once in Figs 2 and 3 using the most current study when more than one existed for that country. In absolute terms, the USA spends the most healthcare funding on skin cancer, followed by Australia, Germany and the UK. However, relative to the size of their respective populations (Fig. 3), Australia and New Zealand have the highest reported cost burden for skin cancer, followed by Denmark and Sweden, whereas Brazil and Canada had the lowest. The total direct medical costs for squamous and basal cell cancers were considerably higher than for malignant melanoma in Australia, New Zealand, USA, UK and Germany, whereas in other nations, melanoma costs were higher or relatively similar to squamous and basal cell carcinomas. For studies breaking down costs by cancer severity, considerably higher costs were consistently reported (Alexandrescu, 2009; Johnston et al., 2012, Maio et al., 2012; Reyes et al., 2013) for advancedstage melanoma (i.e. AJCC stages III and IV) compared with stage I melanoma. Cost-effectiveness of interventions for screening populations for skin cancer
In the 10 years between 1996 and 2007, four studies reported the economic value of melanoma screening
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146 European Journal of Cancer Prevention 2015, Vol 24 No 2
Fig. 3
Cost-effectiveness of interventions for the prevention of skin cancer
18.0 16.0
Melanoma SCC/BCC
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Cost to population ratio (millions) (€2013). Note: Fransen et al. (2012) (Australia) did not report costs for melanoma. These were estimated as a proportional extrapolation from an earlier report (Australian Institute of Health and Welfare, 2005). BCC, basal cell carcinoma; SCC, squamous cell carcinoma.
(Girgis et al., 1996; Freedberg et al., 1999; Beddingfield, 2002; Losina et al., 2007). Three studies were based in the USA and one in Australia. There were varied approaches to screening delivery in terms of the screening frequency, setting and who would perform the screening. Although all studies had a focus on melanoma screening and reported the expected downshifting of cancer stage, and subsequent link to improved survival prospects, the studies also included the cost implications for increased case finding of squamous and basal cell carcinomas and other skin lesions. Results showed that screening could be cost-effective if targeted to high-risk populations such as older men (Girgis et al., 1996) or those with a family history of melanoma (Losina et al., 2007). The overall quality of these studies is good; reports were mostly comprehensive and clearly document the modelling methods and assumptions made. The limitation of these studies was that no budgetary information was provided for the costs of health promotion or screening aimed at a very large segment of the population nor on the likely uptake required for screening to be effective and cost-effective. These factors may reduce the reported benefits of the interventions. In addition, these studies are somewhat dated, reducing their applicability today. The health-related quality-oflife data were also very limited at the time the studies were carried out and most analysts used life-years saved rather than quality-adjusted life-years saved (QALYs).
We identified seven studies evaluating the costeffectiveness of initiatives to prevent skin cancer (Table 2). These were all published from 1992, with five studies published since 2008. A variety of interventions were assessed in these studies and ranged from health educational campaigns (in different settings), a schoolbased programme (Kyle et al., 2008) to system-wide regulation for restricting solarium use (Hirst et al., 2009). Analyses were similarly different as were the outcome measures (e.g. skin cancers avoided, life-years saved, QALYs). Many studies reported that cost-savings and health benefits would arise from skin prevention strategies, that is, governments would receive a return on investment with skin prevention programmes and also reap health benefits for reductions in skin cancer (Table 2). Another three studies did not report costsavings but incremental cost-effectiveness ratios of US $400 per life-year saved (Cristofolini et al., 1993) for an early detection/education campaign, US$3357 per lifeyear saved for an educational campaign (Garattini et al., 1996) and AU$40 890 per QALY for regular sunscreen use (Hirst et al., 2012). These indicate that the programmes were highly cost-effective according to acceptable cost per QALY/life-years saved thresholds in their respective countries. A major challenge with these studies is the intermediate links that are necessary (but weak) between the intervention creating the desirable behaviour change and the expected lag to produce longer-term health outcomes.
Discussion Our review provides insights into health system costs of skin cancer at a national level across many countries and the economic value of skin cancer prevention efforts and early detection programmes. It is clear that management of skin cancer exerts a sizable burden on health systems and there is increasing concern for the increase in incidence and costs to manage skin cancers and associated benign skin lesions. Skin cancers are largely preventable with easy sun-protective behaviours. The results show that skin cancer prevention programmes or policies are consistently cost-effective and may even be cost-saving for governments in the near future. To our knowledge, this is the first time that national estimates of skin cancer treatment costs have been compared across countries. The very high relative costs observed for Australia and New Zealand are most likely attributed to the high incidence of skin cancer. Both these countries have high ambient UV environments year round, an outdoors lifestyle and a large proportion of fairskinned individuals. This is supported by extensive epidemiological studies on known risk factors for skin cancer and in migration studies (Green et al., 1999; Whiteman et al., 2001). The costs of treating skin cancers
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Cost-effectiveness of skin cancer prevention Gordon and Rowell 147
are not high per case (Fransen et al., 2012) but rather a determinant of the very high numbers of individuals developing skin cancer in later years. High costs in Denmark and Sweden can also be attributed in part to the relatively high incidence of skin cancer and large proportions of fair-skinned (easily sunburned) individuals. However, in these affluent Northern European countries, the source of UV radiation is more likely not because of ambient UV exposure but from high solarium use and intense sun exposure during vacations in sunny locations (Forsea et al., 2012). In Figs 2 and 3, the countries are ordered from left to right by high to low incidence, respectively. Studies from Brazil and Canada report the lowest national cost estimates, of all the studies in this review, as a proportion of their population size. It can be seen in Fig. 3 that the aggregate national costs spent on skin cancer clearly relate to incidence, notwithstanding any currency purchasing power differences in Brazil and Canada compared with Euros. A number of studies have also reported costs per skin cancer case or episode of care (Chen et al., 2001, Housman et al., 2003; Gordon et al., 2009). Although the costs of squamous or basal cell carcinomas per lesion are not high, the high numbers of cancers and benign lesions being treated produce high aggregate costs (Housman et al., 2003; Fransen et al., 2012). Several studies have examined costs for advanced malignant melanoma (John Chen et al., 2006; Alexandrescu, 2009; Johnston et al., 2012; Maio et al., 2012; Reyes et al., 2013), with a focus on quantifying costs during metastatic disease where emerging pharmaceutical agents (e.g. ipilimumab, vemurafenib) are competing with traditional supportive care options for public reimbursement. In 2012, the Australian Government approved public funding of ipilimumab for individuals with metastatic melanoma (and previously failed existing treatments) at AU$47 584/patient. The incremental cost-effectiveness ratio was over $100 000 per QALY gained and in survival terms is predicted to prolong life by around 3½ months (PBAC, 2012). In the UK, the cost of ipilimumab is £75 000 and price negotiations are underway. These very high costs for malignant melanoma treatment raise the issue that screening for high-risk individuals should be revisited to include updated treatment patterns, incidence and more accurately reflect and highlight the trade-offs between early detection and treatment. Investing in population programmes to prevent skin cancer is challenging even in high-incidence countries. Policy efforts at reducing the toll of skin cancer now compete with other major behavioural health issues for obesity, harmful alcohol consumption and smoking. In Australia, where SunSmart messages have been repeatedly promoted in mass campaigning since the 1980s, sun protection marketing may be waning and the Australian population is confused about the harms of possibly too little sun exposure causing vitamin D deficiency (Bilinski
and Boyages, 2012). In all health systems, and particularly in Europe, vitamin D deficiency is a concern for individuals and the issue will be important to address in future skin cancer prevention efforts. There is currently an absence of robust randomized clinical trial evidence on whether vitamin D levels, as measured by circulating levels of 25-hydroxyvitamin D, are linked to various chronic diseases or on the overall risks and benefits of vitamin D supplementation. However, a large-scale trial, with mortality and common cancers as primary outcomes, is currently underway in Australia (Tran et al., 2012). The quality of the cost-effectiveness studies in this review was relatively good, with most salient features transparent, analytical approaches sound and sufficient details provided to enable scrutiny (Supplementary file). Despite some studies being dated, most studies carried out thorough sensitivity analyses and used the best available epidemiological or observational data. Clear reporting of the methods and results of cost-effectiveness studies can be challenging because considerable information must be provided within journal word limits (Husereau et al., 2013). There are a number of limitations with this review. Comparison of economic outcomes across studies is problematic because there are different currencies, time periods involved and health system structures. Although it is reasonable to assume that the relative prices for common skin cancer diagnoses and treatments might be similar across countries, the mix of resources used may differ across countries. For example, for keratinocyte cancers, patients are often treated in high-cost dermatologist settings in the USA, whereas in New Zealand and Australia, they are more likely to be treated in general practitioner settings and therefore face different consultation fees. It is beyond the scope of this review to analyse the particular cost drivers within each country. Further research is required to understand where efficiencies can be gained for the large numbers of patients needing skin cancer treatments in future years. In light of this, we have provided a snapshot of this literature and identified commonalities in outcome measures, approaches adopted and scope of resources measured. Most studies underestimated resources and the attendant costs of skin cancer because study investigators could not exhaust all possible outlays. Because of nonregistration of keratinocyte cancers, methods used for determining incidence were different, that is, some use International Classification of Disease codes (Rogers and Coldiron, 2013), laboratory records (O’dea, 2009) or national administrative codes (Fransen et al., 2012). In addition, there is considerable heterogeneity among the cost studies where benign lesions (e.g. actinic keratosis) are included in ‘skin cancer’ costs. Indeed, this does reflect the economic burden of ultraviolet radiation skin damage where suspected skin lesions are excised, but later found
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148 European Journal of Cancer Prevention 2015, Vol 24 No 2
to be benign. However, we recommend that cost studies report these separately to distinguish clearly between actual skin cancer and related healthcare resources. Conclusion
This review summarizes the current body of knowledge of healthcare expenditure by governments for populations commonly diagnosed with skin cancer. The costeffectiveness studies provide an understanding of the economic value of prevention and early detection activities. In an era of economic austerity measures throughout many developed nations and the urgent need for efficient healthcare services, investments in skin cancer prevention and possibly early detection programmes show strong health and economic dividends.
Acknowledgements D.R. was funded by a postdoctoral research fellowship from the National Health and Medical Research Council Centre for Research Excellence in Sun and Health (CRESH). Conflicts of interest
There are no conflicts of interest.
References Alexandrescu DT (2009). Melanoma costs: a dynamic model comparing estimated overall costs of various clinical stages. Dermatol Online J 15:1. Australian Institute of Health and Welfare (2012). Health expenditure Australia 2010-11. AIHW cat. no. HWE 56. Health and Welfare Expenditure Series No. 47. Canberra: Australian Institute of Health and Welfare. Australian Institute of Health and Welfare (2005). Health system expenditures on cancer and other neoplasms in Australia, 2000-01. AIHW cat. no. HWE 29. Health and Welfare Expenditure Series No. 22. Canberra: Australian Institute of Health and Welfare. Beddingfield FC III (2002). Melanoma: a decision analysis to estimate the effectiveness and cost-effectiveness of screening and an analysis of the relevant epidemiology of the disease. DTIC Document, RAND Graduate School, USA. Bentzen J, Kjellberg J, Thorgaard C, Engholm G, Phillip A, Storm HH (2013). Costs of illness for melanoma and nonmelanoma skin cancer in Denmark. Eur J Cancer Prev 22:569–576. Bilinski KL, Boyages SC (2012). The rising cost of vitamin D testing in Australia: time to establish guidelines for testing. Med J Aust 197:90. Chen JG, Fleischer AB Jr, Smith ED, Kancler C, Goldman ND, Williford PM, Feldman SR (2001). Cost of nonmelanoma skin cancer treatment in the United States. Dermatol Surg 27:1035–1038. Chevalier J, Bonastre J, Avril MF (2008). The economic burden of melanoma in France: assessing healthcare use in a hospital setting. Melanoma Res 18:40–46. Cristofolini M, Bianchi R, Boi S, Decarli A, Hanau C, Micciolo R, Zumiani G (1993). Analysis of the cost-effectiveness ratio of the health campaign for the early diagnosis of cutaneous melanoma in Trentino, Italy. Cancer 71:370–374. Forsea AM, Del Marmol V, de Vries E, Bailey EE, Geller AC (2012). Melanoma incidence and mortality in Europe: new estimates, persistent disparities. Br J Dermatol 167:1124–1130. Fransen M, Karahalios A, Sharma N, English DR, Giles GG, Sinclair RD (2012). Non-melanoma skin cancer in Australia. Med J Aust 197:565–568. Freedberg KA, Geller AC, Miller DR, Lew RA, Koh HK (1999). Screening for malignant melanoma: a cost-effectiveness analysis. J Am Acad Dermatol 41:738–745. Garattini L, Cainelli T, Tribbia G, Scopelliti D (1996). Economic evaluation of an educational campaign for early diagnosis of cutaneous melanoma. Pharmacoeconomics 9:146–155. Garbe C, Leiter U (2009). Melanoma epidemiology and trends. Clin Dermatol 27:3–9.
Girgis A, Clarke P, Burton RC, Sanson-Fisher RW (1996). Screening for melanoma by primary health care physicians: a cost-effectiveness analysis. J Med Screen 3:47–53. Gordon LG, Scuffham PA, van der Pols JC, McBride P, Williams GM, Green AC (2009). Regular sunscreen use is a cost-effective approach to skin cancer prevention in subtropical settings. J Invest Dermatol 129:2766–2771. Green A, Williams G, Neale R, Hart V, Leslie D, Parsons P, et al. (1999). Daily sunscreen application and betacarotene supplementation in prevention of basal-cell and squamous-cell carcinomas of the skin: a randomised controlled trial. Lancet 354:723–729 [erratum Lancet 1999; 1354:1038]. H. Krueger & Associates Inc (2010). The economic burden of skin cancer in Canada: current and projected. British Columbia: Canadian Partnership against CancerAvailable at: http://www.cancercare.ns.ca/site-cc/media/can cercare/Economic%20Burden%20of%20Skin%20Cancer%20in% 20Canada%20Report.pdf. pp. 1–204. Available at: http://www.cancercare. ns.ca/site-cc/media/cancercare/Economic%20Burden%20of%20Skin% 20Cancer%20in%20Canada%20Report.pdf. Higashi MK, Veenstra DL, Langley PC (2004). Health economic evaluation of nonmelanoma skin cancer and actinic keratosis. Pharmacoeconomics 22:83–94. Hirst N, Gordon L, Gies P, Green AC (2009). Estimation of avoidable skin cancers and cost-savings to government associated with regulation of the solarium industry in Australia. Health Policy 89:303–311. Hirst NG, Gordon LG, Scuffham PA, Green AC (2012). Lifetime costeffectiveness of skin cancer prevention through promotion of daily sunscreen use. Value Health 15:261–268. Housman TS, Feldman SR, Williford PM, Fleischer AB Jr, Goldman ND, Acostamadiedo JM, Chen GJ (2003). Skin cancer is among the most costly of all cancers to treat for the Medicare population. J Am Acad Dermatol 48:425–429. Husereau D, Drummond M, Petrou S, Carswell C, Moher D, Greenberg D, et al. CHEERS Task Force (2013). Consolidated Health Economic Evaluation Reporting Standards (CHEERS) statement. Int J Technol Assess Health Care 29:117–122. John Chen G, Yelverton CB, Polisetty SS, Housman TS, Williford PM, Teuschler HV, Feldman SR (2006). Treatment patterns and cost of nonmelanoma skin cancer management. Dermatol Surg 32:1266–1271. Johnston K, Levy AR, Lorigan P, Maio M, Lebbe C, Middleton M, et al. (2012). Economic impact of healthcare resource utilisation patterns among patients diagnosed with advanced melanoma in the United Kingdom, Italy, and France: results from a retrospective, longitudinal survey (MELODY study). Eur J Cancer 48:2175–2182. Kyle JW, Hammitt JK, Lim HW, Geller AC, Hall-Jordan LH, Maibach EW, et al. (2008). Economic evaluation of the US Environmental Protection Agency’s SunWise program: sun protection education for young children. Pediatrics 121:e1074–e1084. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, et al. (2009). The PRISMA statement for reporting systematic reviews and metaanalyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 62:e1–e34. Losina E, Walensky RP, Geller A, Beddingfield FC 3rd, Wolf LL, Gilchrest BA, Freedberg KA (2007). Visual screening for malignant melanoma: a costeffectiveness analysis. Arch Dermatol 143:21–28. Maio M, Ascierto P, Testori A, Ridolfi R, Bajetta E, Queirolo P, et al. (2012). The cost of unresectable stage III or stage IV melanoma in Italy. J Exp Clin Cancer Res 31:91. Nilsson GH, Carlsson L, Dal H, Ullén H (2003). Skin diseases caused by ultraviolet radiation: the cost of illness. Int J Technol Assess Health Care 19:724–730. O’dea D (2009). The costs of skin cancer to New Zealand. Wellington: School of Medicine, University of Otago. pp. 1–76. Available at: http://www.cancernz. org.nz/assets/files/info/SunSmart/CostsofSkinCancer_NZ_22October2009. pdf [Accessed 19 December 2013]. OECD (2013). What Future for Health Spending? OECD Economics Department Policy Notes, 19 June. PBAC. Public Summary Document: Ipilimumab. Canberra: Department of Health. Available at: http://www.pbs.gov.au/industry/listing/elements/pbac-meetings/ psd/2012-11/ipilimumab.pdf [Accessed 19 December 2013]. Reyes C, DaCosta Byfield S, Linke R, Satram-Hoang S, Teitelbaum AH (2013). The burden of metastatic melanoma: treatment patterns, healthcare use (utilization), and costs. Melanoma Res 23:159–166. Rogers HW, Coldiron BM (2013). Analysis of skin cancer treatment and costs in the United States Medicare population, 1996–2008. Dermatol Surg 39:35–42. Seidler AM, Pennie ML, Veledar E, Culler SD, Chen SC (2010). Economic burden of melanoma in the elderly population: population-based analysis of the
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Cost-effectiveness of skin cancer prevention Gordon and Rowell 149
Surveillance, Epidemiology, and End Results (SEER) – Medicare data. Arch Dermatol 146:249–256. Shih ST, Carter R, Sinclair C, Mihalopoulos C, Vos T (2009). Economic evaluation of skin cancer prevention in Australia. Prev Med 49:449–453. Souza RJ, Mattedi AP, Rezende ML, Corrêa Mde P, Duarte EM (2009). An estimate of the cost of treating melanoma disease in the state of Sao Paulo – Brazil. An Bras Dermatol 84:237–243. Souza RJ, Mattedi AP, Corrêa MP, Rezende ML, Ferreira AC (2011). An estimate of the cost of treating non-melanoma skin cancer in the state of São Paulo, Brazil. An Bras Dermatol 86:657–662. Stang A, Stausberg J, Boedeker W, Kerek-Bodden H, Jöckel KH (2008). Nationwide hospitalization costs of skin melanoma and non-melanoma skin cancer in Germany. J Eur Acad Dermatol Venereol 22:65–72.
Tinghög G, Carlsson P, Synnerstad I, Rosdahl I (2008). Societal cost of skin cancer in Sweden in 2005. Acta Derm Venereol 88:467–473. Tran B, Armstrong BK, Carlin JB, Ebeling PR, English DR, Kimlin MG, et al. (2012). Recruitment and results of a pilot trial of vitamin D supplementation in the general population of Australia. J Clin Endocrinol Metab 97:4473–4480. Tsao H, Rogers GS, Sober AJ (1998). An estimate of the annual direct cost of treating cutaneous melanoma. J Am Acad Dermatol 38:669–680. Vallejo-Torres L, Morris S, Kinge JM, Poirier V, Verne J (2014). Measuring current and future cost of skin cancer in England. J Public Health (Oxf) 36:140–148. Whiteman DC, Whiteman CA, Green AC (2001). Childhood sun exposure as a risk factor for melanoma: a systematic review of epidemiologic studies. Cancer Causes Control 12:69–82.
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Health system costs of skin cancer and cost-effectiveness of skin cancer prevention and screening: a systematic review Louisa G. Gordona,b and David Rowella The objective of this study was to review the literature for malignant melanoma, basal and squamous cell carcinomas to understand: (a) national estimates of the direct health system costs of skin cancer and (b) the cost-effectiveness of interventions for skin cancer prevention or early detection. A systematic review was performed using Medline, Cochrane Library and the National Health Service Economic Evaluation Databases as well as a manual search of reference lists to identify relevant studies up to 31 August 2013. A narrative synthesis approach was used to summarize the data. National cost estimates were adjusted for country-specific inflation and presented in 2013 euros. The CHEERS statement was used to assess the quality of the economic evaluation studies. Sixteen studies reporting national estimates of skin cancer costs and 11 costeffectiveness studies on skin cancer prevention or early detection were identified. Relative to the size of their respective populations, the annual direct health system costs for skin cancer were highest for Australia, New Zealand, Sweden and Denmark (2013 euros). Skin cancer prevention initiatives are highly cost-effective and may also be cost-saving. Melanoma early detection programmes
Introduction
aimed at high-risk individuals may also be cost-effective; however, updated analyses are needed. There is a significant cost burden of skin cancer for many countries and health expenditure for this disease will grow as incidence increases. Public investment in skin cancer prevention and early detection programmes show strong potential for health and economic benefits. European Journal of Cancer Prevention 24:141–149 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. European Journal of Cancer Prevention 2015, 24:141–149 Keywords: cost of illness, cost-effectiveness, keratinocyte skin cancer, melanoma, screening a
School of Medicine, Centre for Applied Health Economics and bPopulation and Social Health Research Program, Griffith Health Institute, Griffith University, Logan Campus, Queensland, Australia Correspondence to Louisa G. Gordon, PhD, School of Medicine, Centre for Applied Health Economics, Griffith University, Logan Campus, University Drive, Meadowbrook, QLD 4131, Australia Tel: + 61 7 3382 1320; fax: + 61 7 3382 1160; e-mail: [email protected] Received 24 January 2014 Accepted 15 May 2014
In many countries with fair-skinned populations, the incidence of skin cancers is increasing (Garbe and Leiter, 2009). Exposure to ultraviolet radiation, either naturally from the sun or artificially through solarium use, is the main cause of skin cancers. Incidence will continue to increase as nations with ageing populations enter the prime ages for onset of keratinocyte skin cancers (i.e. squamous and basal cell carcinomas). Malignant melanoma, the most serious of all skin cancers, is also increasing in incidence and not only arises in older adults but also in young adults. Consequently, the healthcare costs of managing skin cancers are set to expand quickly. These costs are fuelled not only by ageing demographics but also by health price inflation, more expensive health services and new technologies, and a higher frequency of health services per person (Australian Institute of Health and Welfare, 2012; OECD, 2013). Individuals will also be carrying the burden of disease through direct copayments or losses in income.
Healthcare systems face increasing pressure to meet the higher demand for medical services with constrained budgets. Economists in Europe believe that the current growth in healthcare spending is not sustainable at current levels (OECD, 2013). They propose that governments should not support harsh cost-cutting initiatives but rather focus on innovative ways to improve efficiencies and eliminate wasteful spending. In effect, this requires decisions to redistribute funding from relatively inefficient to more efficient health services. Costeffectiveness analysis provides a framework for a systematic comparison of the relative healthcare costs and benefits of alternative strategies for the purpose of informing decision-makers about whether interventions show good value for money. This process of assessing cost-effectiveness requires the synthesis of data on the natural history of the disease, current clinical practice and management patterns, medical costs and health outcomes of the interventions. Cost-effectiveness analysis is an essential component of decision-making about new services and medicines in many health systems.
All supplementary digital content is available directly from the corresponding author.
There are very few studies investigating the costeffectiveness of interventions designed to control
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DOI: 10.1097/CEJ.0000000000000056
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142 European Journal of Cancer Prevention 2015, Vol 24 No 2
keratinocyte skin cancers and actinic keratosis and relatively more for malignant melanoma where chemotherapy options are available (Higashi et al., 2004). To understand the economic burden of skin cancer management and the relative economic literature of skin cancer prevention and early diagnosis across different health systems, we performed a review of the health economic literature for malignant melanoma, basal and squamous cell carcinomas. Specifically, we have consolidated the literature on (a) the direct health system costs of skin cancer at a country level and (b) the costeffectiveness analyses for prevention or screening interventions for skin cancer. The PRISMA statement was used to guide the review (Liberati et al., 2009).
Materials and methods Search strategy
A search was performed using Medline, The Cochrane Library and the National Health Service Economic Evaluation Database. A manual search of reference lists in the selected studies was performed as was a brief search for cost reports on Google search engine. No limitations on dates were imposed and only Englishlanguage articles were extracted. Searches were limited to the title/abstract fields and available full-text articles. Search terms included ‘costs’ ‘cost-effectiveness’ ‘costutility’ ‘economic evaluation’ ‘burden’ ‘cost-of-illness’ and combinations of ‘skin cancer’ ‘skin carcinoma’ ‘melanoma’ ‘non-melanoma’ ‘SCC & BCC’ ‘basal cell carcinoma’ ‘squamous cell carcinoma’ ‘BCC’ ‘SCC’ and ‘keratinocyte’. Cost studies were excluded if they were single-centre studies or did not include a wide range of costs (e.g. if they focused on one category of cost such as ‘adverse events’ of treatment or included a subgroup of patients such as those with organ transplants) or they did not report national cost estimates. Cost-effectiveness studies were excluded if they were not for the purpose of skin cancer prevention or early detection or were not a full economic evaluation [i.e. they did not assess both the relative costs and effects between an intervention and an alternative option(s)]. Two researchers performed the searches, and discrepancies in the chosen studies were resolved by further discussion.
reviewed according to each criterion and judged to be either fully, partially or not fulfilling the criteria. A narrative synthesis of the studies was performed to summarize the findings as it was not appropriate to use meta-analysis techniques. However, to ease the interpretation of the cost results when multiple currencies were reported across the studies and at different time periods, costs were first inflated to 2012/2013 prices using countryspecific inflation rates and then converted into Euros using exchange rates (http://www.xe.com, August 2013).
Results A total of 124 unique articles were identified in the database searches. Of these, 88 were immediately excluded after screening titles and abstracts. This was mostly because it was not a cost or cost-effectiveness study or studies related to treatments or diagnostic technologies for skin cancer control (Fig. 1). Closer assessment of the remaining 36 studies led to the exclusion of a further 12 studies because they did not report national estimates or they reported only partial costs. Three studies were added to the review after searching the internet for cost reports (O’dea, 2009; H. Krueger & Associates Inc., 2010) or manually searching reference lists of the chosen studies. In all, 27 studies were included in this review: 16 cost-ofillness studies, seven cost-effectiveness studies relating to prevention of skin cancer and four studies on the costeffectiveness of early detection (screening) of melanoma. A summary of the main features of studies included in the review is provided in Table 1 for cost-of-illness studies with national estimates and Table 2 for the costeffectiveness studies. Fig. 1
Potentially relevant studies identified in the search (n=124) Studies excluded (n=88) Not skin cancer (13) Not cost studies or economic evaluations (21) Studies assessing diagnosis/imaging (13) Studies assessing treatments (35) Studies assessing surveillance (3) Wrong study type (3) Studies retrieved for more detailed evaluation (n=36) Studies excluded (n=12) Partial costs only (8) Superseded study (1) National cost estimates not reported (3)
Synthesis and study quality
The results of the studies were combined into a spreadsheet, listing the major features of the studies. The data extracted were year of publication, setting, cost perspective, price year, cost estimates, strengths and limitations. For the cost-effectiveness studies, an assessment of their reporting quality was performed using the Consolidated Health Economic Reporting Standards (CHEERS) checklist (Husereau et al., 2013). The CHEERS statement recommends that 24 criteria be included in any report of a full economic evaluation (e.g. cost-effectiveness or cost-utility analysis). Studies were
Added studies identified through grey literature (2) or reference lists (1) Total identified = 3
Studies selected for review (n=27) Cost-analyses (n=16) Cost-effectiveness analysis (n=11)
Flow chart of literature search outcomes.
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Both SCC and BCC
USA
Sweden
Germany
France
New Zealand
Brazil
USA
Canada
Brazil
USA
Australia
Denmark
UK
Housman et al. (2003)
Tinghög et al. (2008)
Stang et al. (2008)
Chevalier et al. (2008)
O’dea (2009)
Souza et al. (2009)
Seidler et al. (2010)
H. Krueger & Associates Inc. (2010) Souza et al. (2011)
Rogers and Coldiron (2013)
Fransen et al. (2012)
Bentzen et al. (2013)
Vallejo-Torres et al. (2013)
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of the article is prohibited. Top-down, Australia Medicare, estimated hospital costs Population registers, linked data, matched controls, bootstrapping Top-down and bottom-up, administrative reports, national statistics, unit costs
Top-down, unit costs applied to incidence, n = 42 184, Sao Paulo state Top-down, US Medicare and Medicaid
Top-down, cancer registries
Bottom-up, unit costs applied to NCCN pathways Top-down, US Medicare linked to SEER (n = 1858)
Bottom-up, hospitalization data, unit costs
Top-down, Hospital database – national, n = 7000 prevalent costs
Top-down and bottom-up, unit costs applied to national statistics Top-down, hospitalization data on inpatients only
Bottom-up, unit costs applied to pathways – steady state model Top-down, US Medicare Top-down, hospitalization and other statistics (n = 26 848) Top-down, US Medicare, ICD codes, mostly > 65 years
Approach/datasets
1998–2010 2007–2008
Health system (NHS) UK
1997–2010
1996–2008
2000–2007
2004 + projected
1991–1996
2000–2007
2006
2004
2003
2005
1992–1995
1992–1995 1999
1997
Timing
Societal
Health system
Institution
Health system
Societal
Institution
Health system
Societal
Institution
Institution
Societal
Health system
Institution Societal
Health system
Perspective
Key results of direct costs per year (price year)
€33.3 million for SCC and BCC and MM (2010), 59% costs for MM, 0.2% of Danish health budget £112.4 million for SCC and BCC and MM (2008) top-down, 20% costs for MM, £106 million bottom-up (including benign)
€50–60 million for MM, €105–130 million for SCC and BCC, SCC and BCC to MM ratio: 2.2 men and 1.9 women, MM and SCC and BCC are 2% of all cancer hospitalizations, 20 455 MM, 41 929 SCC and BCC hospitalizations €59 million (2004), €27 million for metastasized MM, 1% of hospital costs, components: chemotherapy 17%, hospital costs 38%, followup evaluations 20% NZ$5.7 million for MM (2007/08), $51.4 million for SCC and BCC, $2 million for prevention activities by Cancer Society R$33 million for MM in public sector (2007), R$76 million for MM in private sector, very high costs for advanced stage III and IV MM US$249 million for MM in > 65 year olds (1996), $28 000 per patient lifetime cost, expensive in late stage, comparable with other terminal cancers CAN$36.5 million for SCC and BCC (2004), CAN$29.6 million for MM R$37 million for SCC and BCC in public sector, R$26 million for SCC and BCC in private sector US$633.4 million in 2008, 90% of skin cancers treated in office-based settings, Medicare part B charges increased 137% over time AU$511 million for SCC and BCC (2010), 767 347 treatments
$US562 million (1998) for SCC and BCC, SCC and BCC is the fifth most costly cancer, US$28 million for MM, cost per patient nearly doubled 1995–1998 €22 million for MM (2005), €31 million for SCC and BCC
$US563 million for MM (1997), 11% costs for stage I and II, 89% costs for stage III and IV, $30 000 for interferon treatment per year $US426 million SEK 23 064 000 for MM (1999), SEK 17 584 000 for SCC and BCC
BCC, basal cell carcinoma; ICD, international classification of disease; MM, malignant melanoma; NHS, National Health Service; SCC, squamous cell carcinoma.
Both plus benign
Both
SCC and BCC
Both
MM
MM
Both
MM
Both plus benign Both
SCC and BCC Both plus benign Both
USA Sweden
Chen et al. (2001) Nilsson et al. (2003)
MM
MM or SCC and BCC
USA
Country
Key features of studies reporting national estimates of the direct healthcare costs of skin cancer
Tsao et al. (1998)
Reference
Table 1
Cost-effectiveness of skin cancer prevention Gordon and Rowell 143
MM focus
USA
USA
Losina et al. (2007)
BCC, basal cell carcinoma; MM, malignant melanoma; SCC, squamous cell carcinoma.
Routine use
MM focus
Australia
Sunscreen – regular use
SCC and BCC
Australia
Gordon et al. (2009) Hirst et al. (2012)
Routine use
All skin cancer All skin cancer
Australia Australia
Hirst et al. (2009) Shih et al. (2009)
Do nothing
Sunscreen – regular use
School-based programme
All skin cancer
Do nothing
Do nothing Current programme
Educational campaign
MM focus
Do nothing
No screening
No screening
No screening
No screening
Comparator
Solaria regulation SunSmart – multifaceted
Health campaign – early detect
MM focus
Screening individuals > 50 years of age, by GP, 2-yearly screen Screening high-risk, by dermatologist, onetime screen Screening by dermatologist white population average risk Screening general population, biannual, family history
Intervention and comparator(s)
Skin cancer prevention Cristofolini et al. Italy (1993) Garattini et al. Italy (1996) Kyle et al. (2008) USA
MM focus
MM focus
USA
MM focus
MM or SCC and BCC
Freedberg et al. (1999) Beddingfield (2002)
Melanoma screening Girgis et al. (1996) Australia
Setting
Key results of studies on the cost-effectiveness of skin cancer screening and prevention
References
Table 2
Government + individuals
Government + individuals
Government Government + individuals
Government + productivity
Government
Government + individuals
Government
Government
Government
Government
Perspective
Lifetime model
1992–1996
Lifetime model 1998–2006, high low investments
1999–2015
Pre 1977–1982, post 1977–1981, 1982–1985 1993
Lifetime model
Lifetime model
Lifetime model
Lifetime model
Timing
AU$40 890 per QALY
US $31.2 million cost-savings, return on investment $1.95–4.02 Cost-savings to government AU$680 per life-year saved, $180million net cost-savings, return on investment $2.30 Cost saving to government
$US3 357 per life-year saved (1993)
$400 per life-year saved
$51 481 per life-year saved, one time, lower in over 50s $80 700 per quality-adjusted life-year
$12 137 per life-year saved for men 50 years $39 600 per life-year saved (1996 US)
Incremental cost-effectiveness ratio
144 European Journal of Cancer Prevention 2015, Vol 24 No 2
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Cost-effectiveness of skin cancer prevention Gordon and Rowell 145
Cost studies Yield and study setting
Sixteen studies reported the direct health system costs of skin cancer at a country level (Table 1), and were published from 1996 to 2013. Studies were located in the following countries: Australia (Fransen et al., 2012); New Zealand (O’dea, 2009), Brazil (Souza et al., 2009; Souza et al., 2011), USA (Chen et al., 2001; Housman et al., 2003; Seidler et al., 2010; Rogers and Coldiron, 2013), UK (Vallejo-Torres et al., 2013), Denmark (Bentzen et al., 2013), Sweden (Nilsson et al., 2003; Tinghög et al., 2008), Germany (Stang et al., 2008), France (Chevalier et al., 2008), Italy (Johnston et al., 2012; Maio et al., 2012) and Canada (H. Krueger & Associates Inc., 2010). Unpublished reports were provided for cost studies in New Zealand and Canada (O’dea, 2009; H. Krueger & Associates Inc., 2010). Perspective and scope
Generally, studies adopted a health system perspective for the resources included and others had an institutional (e.g. public hospital or US Medicare) perspective. In most studies, the major direct treatment costs of skin cancers included were doctor visits, biopsies, surgical excisions, cryotherapy and hospital stays. Several studies also included indirect costs such as lost productivity, Fig. 2
future health and mortality costs. Some studies that examined resources for skin cancers also included resources for benign skin lesions (O’dea, 2009; Vallejo-Torres et al., 2013). All studies recognized and acknowledged limitations with the scope or quality of their datasets. These limitations were because of the unavailability of all possible cost components and/or were broad estimates only. Costing methods
The costing methods can be grouped into a ‘top-down’ or a ‘bottom-up’ approach. The top-down method is where large administrative datasets were analysed and distilled down to pertain only to skin cancer costs for the final estimation (Housman et al., 2003; Stang et al., 2008; Souza et al., 2011; Fransen et al., 2012). The bottom-up approach was used when patterns of care and management resources were determined and unit costs were assigned to each service and aggregated ‘up’ to a final total. Some studies used both approaches (Tsao et al., 1998; O’dea, 2009; Vallejo-Torres et al., 2013). To obtain national estimates, costs were often extrapolated according to national incidence or prevalence data. This in itself created further uncertainty in estimates as squamous and basal cell carcinomas are not formally registered in many countries. Costs were descriptive and one study provided cost findings in the form of ‘attributable’ costs by including a matched control group and calculating the difference between cancer and noncancer groups (Bentzen et al., 2013).
700
Healthcare cost estimates Melanoma SCC/BCC
600
500
400
300
200
100
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Annual direct healthcare costs for melanoma and keratinocyte skin cancers (€2013 million). Note: Fransen et al. (2012) (Australia) did not report costs for melanoma. These were estimated as a proportional extrapolation from an earlier report (Australian Institute of Health and Welfare, 2005). BCC, basal cell carcinoma; SCC, squamous cell carcinoma.
Figure 2 provides the results of annual direct healthcare costs by country in 2013 Euros. Each country is represented once in Figs 2 and 3 using the most current study when more than one existed for that country. In absolute terms, the USA spends the most healthcare funding on skin cancer, followed by Australia, Germany and the UK. However, relative to the size of their respective populations (Fig. 3), Australia and New Zealand have the highest reported cost burden for skin cancer, followed by Denmark and Sweden, whereas Brazil and Canada had the lowest. The total direct medical costs for squamous and basal cell cancers were considerably higher than for malignant melanoma in Australia, New Zealand, USA, UK and Germany, whereas in other nations, melanoma costs were higher or relatively similar to squamous and basal cell carcinomas. For studies breaking down costs by cancer severity, considerably higher costs were consistently reported (Alexandrescu, 2009; Johnston et al., 2012, Maio et al., 2012; Reyes et al., 2013) for advancedstage melanoma (i.e. AJCC stages III and IV) compared with stage I melanoma. Cost-effectiveness of interventions for screening populations for skin cancer
In the 10 years between 1996 and 2007, four studies reported the economic value of melanoma screening
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146 European Journal of Cancer Prevention 2015, Vol 24 No 2
Fig. 3
Cost-effectiveness of interventions for the prevention of skin cancer
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al .( 20 12 (2 )( 0 nt Au 09 ze st ) n ( ra N et lia e Ti w al ) ng .( Z hö ea 20 g la 1 e n 3) Va ta d) (D lle l. jo en (2 -T 0 m or 08 ar re St k) )( s an Sw et g ed al et . en C (2 al he ) .( 01 H va 20 3) .K lie 0 (U ru 8 r )( et K) eg G al er Se er .( & m 20 id As a le ny 08 re so ) )( ci ta Fr at l. a es (2 nc 01 In e) 0) So c. (2 (U uz 01 SA a 0) et ) (C al an .( 20 ad 11 a) )( Br az il)
0.0
Cost to population ratio (millions) (€2013). Note: Fransen et al. (2012) (Australia) did not report costs for melanoma. These were estimated as a proportional extrapolation from an earlier report (Australian Institute of Health and Welfare, 2005). BCC, basal cell carcinoma; SCC, squamous cell carcinoma.
(Girgis et al., 1996; Freedberg et al., 1999; Beddingfield, 2002; Losina et al., 2007). Three studies were based in the USA and one in Australia. There were varied approaches to screening delivery in terms of the screening frequency, setting and who would perform the screening. Although all studies had a focus on melanoma screening and reported the expected downshifting of cancer stage, and subsequent link to improved survival prospects, the studies also included the cost implications for increased case finding of squamous and basal cell carcinomas and other skin lesions. Results showed that screening could be cost-effective if targeted to high-risk populations such as older men (Girgis et al., 1996) or those with a family history of melanoma (Losina et al., 2007). The overall quality of these studies is good; reports were mostly comprehensive and clearly document the modelling methods and assumptions made. The limitation of these studies was that no budgetary information was provided for the costs of health promotion or screening aimed at a very large segment of the population nor on the likely uptake required for screening to be effective and cost-effective. These factors may reduce the reported benefits of the interventions. In addition, these studies are somewhat dated, reducing their applicability today. The health-related quality-oflife data were also very limited at the time the studies were carried out and most analysts used life-years saved rather than quality-adjusted life-years saved (QALYs).
We identified seven studies evaluating the costeffectiveness of initiatives to prevent skin cancer (Table 2). These were all published from 1992, with five studies published since 2008. A variety of interventions were assessed in these studies and ranged from health educational campaigns (in different settings), a schoolbased programme (Kyle et al., 2008) to system-wide regulation for restricting solarium use (Hirst et al., 2009). Analyses were similarly different as were the outcome measures (e.g. skin cancers avoided, life-years saved, QALYs). Many studies reported that cost-savings and health benefits would arise from skin prevention strategies, that is, governments would receive a return on investment with skin prevention programmes and also reap health benefits for reductions in skin cancer (Table 2). Another three studies did not report costsavings but incremental cost-effectiveness ratios of US $400 per life-year saved (Cristofolini et al., 1993) for an early detection/education campaign, US$3357 per lifeyear saved for an educational campaign (Garattini et al., 1996) and AU$40 890 per QALY for regular sunscreen use (Hirst et al., 2012). These indicate that the programmes were highly cost-effective according to acceptable cost per QALY/life-years saved thresholds in their respective countries. A major challenge with these studies is the intermediate links that are necessary (but weak) between the intervention creating the desirable behaviour change and the expected lag to produce longer-term health outcomes.
Discussion Our review provides insights into health system costs of skin cancer at a national level across many countries and the economic value of skin cancer prevention efforts and early detection programmes. It is clear that management of skin cancer exerts a sizable burden on health systems and there is increasing concern for the increase in incidence and costs to manage skin cancers and associated benign skin lesions. Skin cancers are largely preventable with easy sun-protective behaviours. The results show that skin cancer prevention programmes or policies are consistently cost-effective and may even be cost-saving for governments in the near future. To our knowledge, this is the first time that national estimates of skin cancer treatment costs have been compared across countries. The very high relative costs observed for Australia and New Zealand are most likely attributed to the high incidence of skin cancer. Both these countries have high ambient UV environments year round, an outdoors lifestyle and a large proportion of fairskinned individuals. This is supported by extensive epidemiological studies on known risk factors for skin cancer and in migration studies (Green et al., 1999; Whiteman et al., 2001). The costs of treating skin cancers
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Cost-effectiveness of skin cancer prevention Gordon and Rowell 147
are not high per case (Fransen et al., 2012) but rather a determinant of the very high numbers of individuals developing skin cancer in later years. High costs in Denmark and Sweden can also be attributed in part to the relatively high incidence of skin cancer and large proportions of fair-skinned (easily sunburned) individuals. However, in these affluent Northern European countries, the source of UV radiation is more likely not because of ambient UV exposure but from high solarium use and intense sun exposure during vacations in sunny locations (Forsea et al., 2012). In Figs 2 and 3, the countries are ordered from left to right by high to low incidence, respectively. Studies from Brazil and Canada report the lowest national cost estimates, of all the studies in this review, as a proportion of their population size. It can be seen in Fig. 3 that the aggregate national costs spent on skin cancer clearly relate to incidence, notwithstanding any currency purchasing power differences in Brazil and Canada compared with Euros. A number of studies have also reported costs per skin cancer case or episode of care (Chen et al., 2001, Housman et al., 2003; Gordon et al., 2009). Although the costs of squamous or basal cell carcinomas per lesion are not high, the high numbers of cancers and benign lesions being treated produce high aggregate costs (Housman et al., 2003; Fransen et al., 2012). Several studies have examined costs for advanced malignant melanoma (John Chen et al., 2006; Alexandrescu, 2009; Johnston et al., 2012; Maio et al., 2012; Reyes et al., 2013), with a focus on quantifying costs during metastatic disease where emerging pharmaceutical agents (e.g. ipilimumab, vemurafenib) are competing with traditional supportive care options for public reimbursement. In 2012, the Australian Government approved public funding of ipilimumab for individuals with metastatic melanoma (and previously failed existing treatments) at AU$47 584/patient. The incremental cost-effectiveness ratio was over $100 000 per QALY gained and in survival terms is predicted to prolong life by around 3½ months (PBAC, 2012). In the UK, the cost of ipilimumab is £75 000 and price negotiations are underway. These very high costs for malignant melanoma treatment raise the issue that screening for high-risk individuals should be revisited to include updated treatment patterns, incidence and more accurately reflect and highlight the trade-offs between early detection and treatment. Investing in population programmes to prevent skin cancer is challenging even in high-incidence countries. Policy efforts at reducing the toll of skin cancer now compete with other major behavioural health issues for obesity, harmful alcohol consumption and smoking. In Australia, where SunSmart messages have been repeatedly promoted in mass campaigning since the 1980s, sun protection marketing may be waning and the Australian population is confused about the harms of possibly too little sun exposure causing vitamin D deficiency (Bilinski
and Boyages, 2012). In all health systems, and particularly in Europe, vitamin D deficiency is a concern for individuals and the issue will be important to address in future skin cancer prevention efforts. There is currently an absence of robust randomized clinical trial evidence on whether vitamin D levels, as measured by circulating levels of 25-hydroxyvitamin D, are linked to various chronic diseases or on the overall risks and benefits of vitamin D supplementation. However, a large-scale trial, with mortality and common cancers as primary outcomes, is currently underway in Australia (Tran et al., 2012). The quality of the cost-effectiveness studies in this review was relatively good, with most salient features transparent, analytical approaches sound and sufficient details provided to enable scrutiny (Supplementary file). Despite some studies being dated, most studies carried out thorough sensitivity analyses and used the best available epidemiological or observational data. Clear reporting of the methods and results of cost-effectiveness studies can be challenging because considerable information must be provided within journal word limits (Husereau et al., 2013). There are a number of limitations with this review. Comparison of economic outcomes across studies is problematic because there are different currencies, time periods involved and health system structures. Although it is reasonable to assume that the relative prices for common skin cancer diagnoses and treatments might be similar across countries, the mix of resources used may differ across countries. For example, for keratinocyte cancers, patients are often treated in high-cost dermatologist settings in the USA, whereas in New Zealand and Australia, they are more likely to be treated in general practitioner settings and therefore face different consultation fees. It is beyond the scope of this review to analyse the particular cost drivers within each country. Further research is required to understand where efficiencies can be gained for the large numbers of patients needing skin cancer treatments in future years. In light of this, we have provided a snapshot of this literature and identified commonalities in outcome measures, approaches adopted and scope of resources measured. Most studies underestimated resources and the attendant costs of skin cancer because study investigators could not exhaust all possible outlays. Because of nonregistration of keratinocyte cancers, methods used for determining incidence were different, that is, some use International Classification of Disease codes (Rogers and Coldiron, 2013), laboratory records (O’dea, 2009) or national administrative codes (Fransen et al., 2012). In addition, there is considerable heterogeneity among the cost studies where benign lesions (e.g. actinic keratosis) are included in ‘skin cancer’ costs. Indeed, this does reflect the economic burden of ultraviolet radiation skin damage where suspected skin lesions are excised, but later found
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148 European Journal of Cancer Prevention 2015, Vol 24 No 2
to be benign. However, we recommend that cost studies report these separately to distinguish clearly between actual skin cancer and related healthcare resources. Conclusion
This review summarizes the current body of knowledge of healthcare expenditure by governments for populations commonly diagnosed with skin cancer. The costeffectiveness studies provide an understanding of the economic value of prevention and early detection activities. In an era of economic austerity measures throughout many developed nations and the urgent need for efficient healthcare services, investments in skin cancer prevention and possibly early detection programmes show strong health and economic dividends.
Acknowledgements D.R. was funded by a postdoctoral research fellowship from the National Health and Medical Research Council Centre for Research Excellence in Sun and Health (CRESH). Conflicts of interest
There are no conflicts of interest.
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