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Aggregate Cost of Mammography Screening in the United States: Comparison of Current Practice and Advocated Guidelines

Cristina O'Donoghue, MD, MPH; Martin Eklund, PhD; Elissa M. Ozanne, PhD; and Laura J. Esserman, MD, MBA
[+] Article and Author Information

From University of California at San Francisco, San Francisco, California, and University of Illinois at Chicago, Chicago, Illinois.

Disclaimer: The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute or the National Institutes of Health.

Note: All authors had full access to all of the data in the study and take responsibility for the integrity of the data and accuracy of the data analysis. Each registry and the Statistical and Data Coordinating Center have received institutional review board approval for either active or passive consenting processes or a waiver of consent to enroll participants, link data, and perform analytic studies. All procedures are Health Insurance Portability and Accountability Act–compliant and all registries and the Statistical and Data Coordinating Center have received a Federal Certificate of Confidentiality and other protection for the identities of women, physicians, and facilities who are subjects of this research.

Acknowledgments: The authors thank the Breast Cancer Surveillance Consortium investigators, participating women, mammography facilities, and radiologists for the data they provided for this study. A list of the Breast Cancer Surveillance Consortium investigators and procedures for requesting Breast Cancer Surveillance Consortium data for research purposes are provided at: http://breastscreening.cancer.gov. They also thank Pamela Derish, MA, from the Department of Surgery at the University of California, San Francisco, for editing the manuscript and Karla Kerlikowske, MD, from the Department of Medicine and Epidemiology Biostatistics at the University of California, San Francisco, and Rebecca Hubbard, PhD, from the Group Health Research Institute and Department of Biostatistics at University of Washington, for reviewing the manuscript and giving valuable input.

Grant Support: This effort is part of the analysis proposed for breast cancer screening and prevention as part of the Athena Breast Health Network, a collaboration of the 5 University of California medical centers. Athena is supported by the University of California and Safeway Foundation. Data collection for this work was supported by a National Cancer Institute–funded Program Project (P01CA154292) and the Breast Cancer Surveillance Consortium (U01CA63740, U01CA86076, U01CA86082, U01CA63736, U01CA70013, U01CA69976, U01CA63731, U01CA70040, and HHSN261201100031C). Dr. O'Donoghue is funded in part by the University of Illinois at Chicago Eleanor B. Pillsbury Fellowship. Dr. Eklund is funded by the Swedish Council for Working Life and Social Research (FAS), project number 2012-0073. The collection of cancer data used in this study was supported in part by several state public health departments and cancer registries throughout the United States. For a full description of these sources, please visit www.breastscreening.cancer.gov/work/acknowledgment.html.

Potential Conflicts of Interest: None disclosed. Forms can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M13-1217.

Reproducible Research Statement: Study protocol: Available from Dr. O'Donoghue (e-mail, cristina.odonoghue@gmail.com). Statistical code: Available from Dr. Eklund (e-mail, martin.eklund@ucsfmedctr.org). Data set: Available from Drs. O'Donoghue and Eklund.

Requests for Single Reprints: Laura Esserman, MD, MBA, University of California, San Francisco Comprehensive Cancer Center, 1600 Divisadero Street, 2nd Floor, Box 1710, San Francisco, CA 94115; e-mail, Laura.esserman@ucsfmedctr.org.

Current Author Addresses: Dr. O'Donoghue: University of Illinois at Chicago Department of Surgery, 840 S. Wood Street, Suite 518-E Chicago, IL 60612.

Drs. Eklund and Esserman: University of California, San Francisco Comprehensive Cancer Center, 1600 Divisadero Street, 2nd Floor, Box 1710, San Francisco, CA 94115.

Dr. Ozanne: The Dartmouth Institute for Health Policy and Clinical Practice, Geisel School of Medicine at Dartmouth, 35 Centerra Parkway, Lebanon, NH 03766.

Author Contributions: Conception and design: C. O'Donoghue, M. Eklund, E.M. Ozanne, L.J. Esserman.

Analysis and interpretation of the data: C. O'Donoghue, M. Eklund, E.M. Ozanne, L.J. Esserman.

Drafting of the article: C. O'Donoghue.

Critical revision of the article for important intellectual content: C. O'Donoghue, M. Eklund, E.M. Ozanne, L.J. Esserman.

Final approval of the article: C. O'Donoghue, M. Eklund, E.M. Ozanne, L.J. Esserman.

Statistical expertise: M. Eklund, E.M. Ozanne.

Obtaining of funding: L.J. Esserman.

Administrative, technical, or logistic support: C. O'Donoghue, M. Eklund, E.M. Ozanne, L.J. Esserman.

Collection and assembly of data: C. O'Donoghue, M. Eklund.

Ann Intern Med. 2014;160(3):145-153. doi:10.7326/M13-1217
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Background: Controversy exists over how often and at what age mammography screening should be implemented. Given that evidence supports less frequent screening, the cost differences among advocated screening policies should be better understood.

Objective: To estimate the aggregate cost of mammography screening in the United States in 2010 and compare the costs of policy recommendations by professional organizations.

Design: A model was developed to estimate the cost of mammography screening in 2010 and 3 screening strategies: annual (ages 40 to 84 years), biennial (ages 50 to 69 years), and U.S. Preventive Services Task Force (USPSTF) guidelines (biennial for those aged 50 to 74 years and personalized based on risk for those younger than 50 years and based on comorbid conditions for those 75 years and older).

Setting: United States.

Patients: Women aged 40 to 85 years.

Intervention: Mammography annually, biennially, or following USPSTF guidelines.

Measurements: Cost of screening per year, using Medicare reimbursements.

Results: The estimated cost of mammography screening in the United States in 2010 was $7.8 billion, with approximately 70% of women screened. The simulated cost of screening 85% of women was $10.1 billion, $2.6 billion, and $3.5 billion for annual, biennial, and USPSTF guidelines, respectively. The largest drivers of cost (in order) were screening frequency, percentage of women screened, cost of mammography, percentage of women screened with digital mammography, and percentage of mammography recalls.

Limitation: Cost estimates and assumptions used in the model were conservative.

Conclusion: The cost of mammography varies by at least $8 billion per year on the basis of screening strategy. The USPSTF guidelines are based on the scientific evidence to date to maximize patient benefit and minimize harm but also result in far more effective use of resources.

Primary Funding Source: University of California and the Safeway Foundation.


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Figure 1.

Comparison of the costs of screening strategies per year.

Each bar represents the total cost of mammography screening per year, demarcating the costs from screening mammography and the subsequent recalls and biopsies. USPSTF = U.S. Preventive Services Task Force.

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Figure 2.

Sensitivity analyses of mammography screening practice and advocated screening strategies.

Tornado diagrams depict sensitivity analyses done for the largest determinants of cost for each strategy. The x-axis shows the cost of mammography screening per year. The vertical line within each tornado diagram is the point estimate of cost for each strategy, and the horizontal bars represent the effect on cost the input ranges have in the sensitivity analyses. Frequency is the largest driver of cost as demonstrated by the wide range of cost between the least frequent strategy, biennial screening, versus the most frequent strategy, annual screening. The next largest drivers of cost, by decreasing level of effect, were the variation of the percentage of women screened, the cost of individual mammography screenings, percentage of film versus digital mammography, the number of recalls, and the recall cost. USPSTF = U.S. Preventive Services Task Force.

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Quantifying the Conflict-of-Interest in Promoting Screening Mammography
Posted on February 8, 2014
John D. Keen, MD, MBA
Stroger Hospital of Cook County
Conflict of Interest: None Declared
O’Donoghue et al have conservatively estimated the aggregate cost of screening mammography in the United State (U.S) under several scenarios(1). Screening advocates will certainly argue a difference in number of lives extended under an aggressive annual screening scenario rather than the USPSTF recommendations. Although the authors cite a cost-effectiveness (C/E) ratio of annual screening compared to biennial screening of more than $340,00/QALY, the real ratio including indirect costs and overdiagnosis is more likely double or triple that estimate.(2)
Furthermore, Hubbard et al have shown that annual screening in the U.S. has not reduced the proportion of advanced cancers compared to biennial screening. (3) Bleyer et al have shown only a marginal reduction in the rate of advanced breast cancer in the U.S. since the introduction of screening mammography, with probably half of screen-detected cancers overdiagnosis of pseudodisease.(4) There cannot be a benefit from screening (a reduction in mortality rates or mastectomy rates) if the rate of advanced cancers does not decrease. Instead of promoting screening participation by claiming the status quo falls short of “national goals”, the authors should acknowledge the possibility that the entire $8 billion consumed annually by screening mammography would be better spent on something else-the opportunity cost of the resources.
If physicians believe in promoting informed choice (insight) regarding cancer screening, given the substantial personal harm from overdiagnosis of healthy women and false-positive recalls and biopsies, then targeted participation rates (uptake) become irrelevant. As an alternative to a participation rate of 85%, the authors should model lower uptake to account for the current lack of insight among screening mammography participants regarding the trade-off of harms to benefit, and the uncertainty of their magnitude. Screening advocates including the American Cancer Society and some professional groups who benefit from screening (including breast imagers, oncologists, and surgeons) will probably continue to advocate the status quo or an aggressive annual screening schedule instead of the USPSTF recommendations.(5) This marketing of mammography no doubt increases screening participation and makes sense from a business perspective. The authors conservatively estimate $4.4 billion in additional revenue that the breast imaging community receives from the status quo each year.
One person’s cost is another person’s income. The authors have quantified the financial conflict-of-interest among those most stridently defending aggressive annual screening mammography: an extra $2.3 billion in revenue beyond the status quo. Financial considerations best explain the organized resistance to the implementation of the reasonable USPSTF recommendations.

1. O'Donoghue C, Eklund M, Ozanne EM, Esserman LJ. Aggregate Cost of Mammography Screening in the United States: Comparison of Current Practice and Advocated Guidelines. Annals of Internal Medicine;160(3):145-153.
2. Keen JD. Analysis of health benefits and cost-effectiveness of mammography for breast cancer. Ann Intern Med. 2011;155(8):566; author reply 566-7.
3. Hubbard RA, Kerlikowske K, Flowers CI, Yankaskas BC, Zhu W, Miglioretti DL. Cumulative probability of false-positive recall or biopsy recommendation after 10 years of screening mammography: a cohort study. Ann Intern Med. 2011;155(8):481-92.
4. Bleyer A, Welch HG. Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med. 2012;367(21):1998-2005.
5. Keen JD. The ACR/SBI Breast Cancer Screening Guidelines are Wrong. Medscape Radiology. March 2, 2012. Accessed at http://www.medscape.com/viewarticle/759429 on 6 February 2014.

Harms and Costs of Not Screening
Posted on February 27, 2014
Mark A. Helvie, MD
University of Michigan Health System, Comprehensive Cancer Center
Conflict of Interest: Institutional Grant support, General Electric Healthcare, Inc.
O’Donoghue et al compare insurer monetary costs of several mammographic screening regimen and conclude the added cost of more aggressive screening is not justified as clinical outcomes are implied to be similar (1). However, there are substantial outcome differences which significantly impact the cost analysis. The referenced Cancer Intervention and Surveillance Modeling Network (CISNET) model results show large outcome differences for both life years gained (LYG) and mortality reduction when annual mammographic screening from age 40 to 84 (A40-84) is compared to biennial screening age 50-74 (B50-74) (2, 3). These CISNET data show:

1. There is a 72% improvement in LYG when A40-84 mammographic screening is compared to B50-74 screening. Life years gained increases from 110/1000 for B50-74 to 189/1000 for A40-84. Mortality reduction nearly doubles, from 23% to 40% (2).
2. There is a 42% improvement in LYG when comparing annual screening to biennial screening. CISNET models for digital mammography show LYG increasing from 36/1000 for biennial screening to 51/1000 for annual screening women age 40-49 years (3).
3. The LYG per decade for screening women in their 40s (51/1000) with annual mammography exceeds the LYG per decade for B50-74 (44/1000) (3).

In addition, while there are costs and harms of screening, there are also costs and harms of not screening which are not estimated in the study. The financial cost of medical treatment for a woman with metastatic breast cancer is $250,000 (4). The financial cost due to lost productivity secondary to death of a woman in her 40s is $1.4 million (5). Hence the financial cost of one excessive breast cancer death due to not screening is very large. The aggregate costs of these two factors, when attributed to excessive deaths from not screening based upon CISNET model results, approach or exceed the authors’ estimates of mammographic screening costs.

Medical insurers do not insure the large financial costs of lost productivity which are shifted to patients and their families. Insurers’ financial interests may not necessarily align with patient interests.

1. O'Donoghue C, Eklund M, Ozanne EM, Esserman LJ. Aggregate Cost of Mammography Screening in the United States: Comparison of Current Practice and Advocated Guidelines. Ann Intern Med. 2014;160(3):145-53.
2. Mandelblatt JS, Cronin KA, Bailey S, Berry DA, de Koning HJ, Draisma G, et al. Effects of mammography screening under different screening schedules: model estimates of potential benefits and harms. Ann Intern Med. 2009;151(10):738-47.
3. van Ravesteyn NT, Miglioretti DL, Stout NK, Lee SJ, Schechter CB, Buist DS, et al. Tipping the Balance of Benefits and Harms to Favor Screening Mammography Starting at Age 40 Years: A Comparative Modeling Study of Risk. Ann Intern Med. 2012;156(9):609-17.
4. Montero AJ, Eapen S, Gorin B, Adler P. The economic burden of metastatic breast cancer: a U.S. managed care perspective. Breast Cancer Res Treat. 2012;134(2):815-22.
5. Bradley CJ, Yabroff KR, Dahman B, Feuer EJ, Mariotto A, Brown ML. Productivity costs of cancer mortality in the United States: 2000-2020. J Natl Cancer Inst. 2008;100(24):1763-70.
More Light and Less Heat on the Breast Cancer Screening Debate
Posted on April 3, 2014
Martin Eklund, PhD, Cristina O'Donoghue, MD, MPH, Laura Esserman, MD, MBA
University of California San Francisco, University of Illinois at Chicago
Conflict of Interest: None Declared
We agree with Dr. Keen that the estimates we present are conservative; this is by design, in order to provide a lower bound of the likely cost implications of different approaches to screening.
Dr. Helvie expressed concern that the US Preventive Task Force (USPSTF) guidelines would lead to loss of life based on the CISNET models, the very analysis upon which the USPSTF based its guidelines for biennial screening[1]. In fact, the CISNET model shows that, over the same age range, the mortality reduction and life-years-gained by annual screening are virtually zero.[1] The evidence of benefit of annual over biennial screening is marginal[2] to none.[3] Outside of the US, the same data has led to adoption of policies for biennial screening starting at the age of 49. Despite annual screening, breast cancer mortality is not lower in the US than in comparable countries.[4] Dr. Helvie is also concerned that eliminating or reducing screening will increase metastatic disease. However, screening has not reduced the rates of primary presentation of metastatic disease, and the rate of stage 2 and 3 cancers has not dropped as much as we would have hoped with aggressive annual screening[5]. Nevertheless, there are likely population subgroups that benefit from annual screening[2] - but certainly not everyone[3].
There is a long-standing debate over mammography’s risks, who benefits most and who will not. More arguing over studies started decades ago will not improve our current approach or change polarized beliefs.
The opportunity before us today is to stop screening as if everyone has the same risk or is even at risk for the same kind of breast cancer. Not all women will benefit from the same screening strategy. Given the variability in women’s risk and the types of breast cancer (ranging from slow growing to aggressive) that arise, the opportunity is to use scientific advances in inherited risk, density, cancer biology, and imaging techniques to learn how to tailor screening accordingly.
Today, we individualize patient care based on tumor biology. It is time to design screening trials to enable us to harness this knowledge to shed more light and less heat on how best to screen in the modern era. The Athena Breast Health Network is planning such a personalized screening trial. Dr. Keen’s letter and our aggregate cost of mammography analysis suggest that the opportunity cost of annual screening is high; the money to study new approaches is already in the system.
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