Estimation of Breast Cancer Overdiagnosis in a U.S. Breast Screening Cohort

Marc D. Ryser; Jane Lange; Lurdes Y.T. Inoue; Ellen S. O’Meara; Charlotte Gard; Diana L. Miglioretti; Jean Luc Bulliard; Andrew F. Brouwer; E. Shelley Hwang; Ruth B. Etzioni

doi:10.7326/M21-3577

Estimation of Breast Cancer Overdiagnosis in a U.S. Breast Screening Cohort

Marc D. Ryser, Jane Lange, Lurdes Y.T. Inoue, Ellen S. O’Meara, Charlotte Gard, Diana L. Miglioretti, Jean Luc Bulliard, Andrew F. Brouwer, E. Shelley Hwang, Ruth B. Etzioni

Research output: Contribution to journal › Article › peer-review

19 Scopus citations

Abstract

Background: Mammography screening can lead to overdiagnosis—that is, screen-detected breast cancer that would not have caused symptoms or signs in the remaining lifetime. There is no consensus about the frequency of breast cancer overdiagnosis. Objective: To estimate the rate of breast cancer overdiagnosis in contemporary mammography practice accounting for the detection of nonprogressive cancer. Design: Bayesian inference of the natural history of breast cancer using individual screening and diagnosis records, allowing for nonprogressive preclinical cancer. Combination of fitted natural history model with life-table data to predict the rate of overdiagnosis among screen-detected cancer under biennial screening. Setting: Breast Cancer Surveillance Consortium (BCSC) facilities. Participants: Women aged 50 to 74 years at first mammography screen between 2000 and 2018. Measurements: Screening mammograms and screen-detected or interval breast cancer. Results: The cohort included 35986 women, 82677 mammograms, and 718 breast cancer diagnoses. Among all preclinical cancer cases, 4.5% (95% uncertainty interval [UI], 0.1% to 14.8%) were estimated to be nonprogressive. In a program of biennial screening from age 50 to 74 years, 15.4% (UI, 9.4% to 26.5%) of screen-detected cancer cases were estimated to be overdiagnosed, with 6.1% (UI, 0.2% to 20.1%) due to detecting indolent preclinical cancer and 9.3% (UI, 5.5% to 13.5%) due to detecting progressive preclinical cancer in women who would have died of an unrelated cause before clinical diagnosis. Limitations: Exclusion of women with first mammography screen outside BCSC. Conclusion: On the basis of an authoritative U.S. population data set, the analysis projected that among biennially screened women aged 50 to 74 years, about 1 in 7 cases of screen-detected cancer is overdiagnosed. This information clarifies the risk for breast cancer overdiagnosis in contemporary screening practice and should facilitate shared and informed decision making about mammography screening.

Original language	English (US)
Pages (from-to)	471-478
Number of pages	8
Journal	Annals of internal medicine
Volume	175
Issue number	4
DOIs	https://doi.org/10.7326/M21-3577
State	Published - Apr 1 2022
Externally published	Yes

ASJC Scopus subject areas

Internal Medicine

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10.7326/M21-3577

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@article{453b2c4b742642bfa1d9762b40dd60de,

title = "Estimation of Breast Cancer Overdiagnosis in a U.S. Breast Screening Cohort",

abstract = "Background: Mammography screening can lead to overdiagnosis—that is, screen-detected breast cancer that would not have caused symptoms or signs in the remaining lifetime. There is no consensus about the frequency of breast cancer overdiagnosis. Objective: To estimate the rate of breast cancer overdiagnosis in contemporary mammography practice accounting for the detection of nonprogressive cancer. Design: Bayesian inference of the natural history of breast cancer using individual screening and diagnosis records, allowing for nonprogressive preclinical cancer. Combination of fitted natural history model with life-table data to predict the rate of overdiagnosis among screen-detected cancer under biennial screening. Setting: Breast Cancer Surveillance Consortium (BCSC) facilities. Participants: Women aged 50 to 74 years at first mammography screen between 2000 and 2018. Measurements: Screening mammograms and screen-detected or interval breast cancer. Results: The cohort included 35986 women, 82677 mammograms, and 718 breast cancer diagnoses. Among all preclinical cancer cases, 4.5% (95% uncertainty interval [UI], 0.1% to 14.8%) were estimated to be nonprogressive. In a program of biennial screening from age 50 to 74 years, 15.4% (UI, 9.4% to 26.5%) of screen-detected cancer cases were estimated to be overdiagnosed, with 6.1% (UI, 0.2% to 20.1%) due to detecting indolent preclinical cancer and 9.3% (UI, 5.5% to 13.5%) due to detecting progressive preclinical cancer in women who would have died of an unrelated cause before clinical diagnosis. Limitations: Exclusion of women with first mammography screen outside BCSC. Conclusion: On the basis of an authoritative U.S. population data set, the analysis projected that among biennially screened women aged 50 to 74 years, about 1 in 7 cases of screen-detected cancer is overdiagnosed. This information clarifies the risk for breast cancer overdiagnosis in contemporary screening practice and should facilitate shared and informed decision making about mammography screening.",

author = "Ryser, {Marc D.} and Jane Lange and Inoue, {Lurdes Y.T.} and O{\textquoteright}Meara, {Ellen S.} and Charlotte Gard and Miglioretti, {Diana L.} and Bulliard, {Jean Luc} and Brouwer, {Andrew F.} and Hwang, {E. Shelley} and Etzioni, {Ruth B.}",

note = "Funding Information: By grants R00CA207872, R01CA242735, and R01CA192492 from the National Institutes of Health. Data collection was additionally supported by the BCSC (www.bcsc-research. org/) with funding from the National Cancer Institute (grants P01CA154292 and U54CA163303) and the Patient-Centered Outcomes Research Institute (grant PCS-1504-30370). Cancer and vital status data collection were supported in part by several U.S. state public health departments and cancer registries (www.bcscresearch.org/about/work-acknowledgement). Funding Information: Financial Support: By grants R00CA207872, R01CA242735, and R01CA192492 from the National Institutes of Health. Data collection was additionally supported by the BCSC (www.bcsc-research. org/) with funding from the National Cancer Institute (grants P01CA154292 and U54CA163303) and the Patient-Centered Outcomes Research Institute (grant PCS-1504-30370). Cancer and vital status data collection were supported in part by several U.S. state public health departments and cancer registries (www.bcsc-research.org/about/work-acknowledgement). Funding Information: This study was funded by the National Cancer Institute, which had no role in design, analysis, manuscript preparation, or the decision to submit the manuscript for publication. Publisher Copyright: {\textcopyright} 2022 American College of Physicians. All rights reserved.",

year = "2022",

month = apr,

day = "1",

doi = "10.7326/M21-3577",

language = "English (US)",

volume = "175",

pages = "471--478",

journal = "Annals of Internal Medicine",

issn = "0003-4819",

publisher = "American College of Physicians",

number = "4",

}

TY - JOUR

T1 - Estimation of Breast Cancer Overdiagnosis in a U.S. Breast Screening Cohort

AU - Ryser, Marc D.

AU - Lange, Jane

AU - Inoue, Lurdes Y.T.

AU - O’Meara, Ellen S.

AU - Gard, Charlotte

AU - Miglioretti, Diana L.

AU - Bulliard, Jean Luc

AU - Brouwer, Andrew F.

AU - Hwang, E. Shelley

AU - Etzioni, Ruth B.

N1 - Funding Information: By grants R00CA207872, R01CA242735, and R01CA192492 from the National Institutes of Health. Data collection was additionally supported by the BCSC (www.bcsc-research. org/) with funding from the National Cancer Institute (grants P01CA154292 and U54CA163303) and the Patient-Centered Outcomes Research Institute (grant PCS-1504-30370). Cancer and vital status data collection were supported in part by several U.S. state public health departments and cancer registries (www.bcscresearch.org/about/work-acknowledgement). Funding Information: Financial Support: By grants R00CA207872, R01CA242735, and R01CA192492 from the National Institutes of Health. Data collection was additionally supported by the BCSC (www.bcsc-research. org/) with funding from the National Cancer Institute (grants P01CA154292 and U54CA163303) and the Patient-Centered Outcomes Research Institute (grant PCS-1504-30370). Cancer and vital status data collection were supported in part by several U.S. state public health departments and cancer registries (www.bcsc-research.org/about/work-acknowledgement). Funding Information: This study was funded by the National Cancer Institute, which had no role in design, analysis, manuscript preparation, or the decision to submit the manuscript for publication. Publisher Copyright: © 2022 American College of Physicians. All rights reserved.

PY - 2022/4/1

Y1 - 2022/4/1

N2 - Background: Mammography screening can lead to overdiagnosis—that is, screen-detected breast cancer that would not have caused symptoms or signs in the remaining lifetime. There is no consensus about the frequency of breast cancer overdiagnosis. Objective: To estimate the rate of breast cancer overdiagnosis in contemporary mammography practice accounting for the detection of nonprogressive cancer. Design: Bayesian inference of the natural history of breast cancer using individual screening and diagnosis records, allowing for nonprogressive preclinical cancer. Combination of fitted natural history model with life-table data to predict the rate of overdiagnosis among screen-detected cancer under biennial screening. Setting: Breast Cancer Surveillance Consortium (BCSC) facilities. Participants: Women aged 50 to 74 years at first mammography screen between 2000 and 2018. Measurements: Screening mammograms and screen-detected or interval breast cancer. Results: The cohort included 35986 women, 82677 mammograms, and 718 breast cancer diagnoses. Among all preclinical cancer cases, 4.5% (95% uncertainty interval [UI], 0.1% to 14.8%) were estimated to be nonprogressive. In a program of biennial screening from age 50 to 74 years, 15.4% (UI, 9.4% to 26.5%) of screen-detected cancer cases were estimated to be overdiagnosed, with 6.1% (UI, 0.2% to 20.1%) due to detecting indolent preclinical cancer and 9.3% (UI, 5.5% to 13.5%) due to detecting progressive preclinical cancer in women who would have died of an unrelated cause before clinical diagnosis. Limitations: Exclusion of women with first mammography screen outside BCSC. Conclusion: On the basis of an authoritative U.S. population data set, the analysis projected that among biennially screened women aged 50 to 74 years, about 1 in 7 cases of screen-detected cancer is overdiagnosed. This information clarifies the risk for breast cancer overdiagnosis in contemporary screening practice and should facilitate shared and informed decision making about mammography screening.

AB - Background: Mammography screening can lead to overdiagnosis—that is, screen-detected breast cancer that would not have caused symptoms or signs in the remaining lifetime. There is no consensus about the frequency of breast cancer overdiagnosis. Objective: To estimate the rate of breast cancer overdiagnosis in contemporary mammography practice accounting for the detection of nonprogressive cancer. Design: Bayesian inference of the natural history of breast cancer using individual screening and diagnosis records, allowing for nonprogressive preclinical cancer. Combination of fitted natural history model with life-table data to predict the rate of overdiagnosis among screen-detected cancer under biennial screening. Setting: Breast Cancer Surveillance Consortium (BCSC) facilities. Participants: Women aged 50 to 74 years at first mammography screen between 2000 and 2018. Measurements: Screening mammograms and screen-detected or interval breast cancer. Results: The cohort included 35986 women, 82677 mammograms, and 718 breast cancer diagnoses. Among all preclinical cancer cases, 4.5% (95% uncertainty interval [UI], 0.1% to 14.8%) were estimated to be nonprogressive. In a program of biennial screening from age 50 to 74 years, 15.4% (UI, 9.4% to 26.5%) of screen-detected cancer cases were estimated to be overdiagnosed, with 6.1% (UI, 0.2% to 20.1%) due to detecting indolent preclinical cancer and 9.3% (UI, 5.5% to 13.5%) due to detecting progressive preclinical cancer in women who would have died of an unrelated cause before clinical diagnosis. Limitations: Exclusion of women with first mammography screen outside BCSC. Conclusion: On the basis of an authoritative U.S. population data set, the analysis projected that among biennially screened women aged 50 to 74 years, about 1 in 7 cases of screen-detected cancer is overdiagnosed. This information clarifies the risk for breast cancer overdiagnosis in contemporary screening practice and should facilitate shared and informed decision making about mammography screening.

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JO - Annals of Internal Medicine

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ER -

Estimation of Breast Cancer Overdiagnosis in a U.S. Breast Screening Cohort

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