breast cancer a systematic literature review

A Systematic Literature Review of Breast Cancer Diagnosis Using Machine Intelligence Techniques

• Review article
• Published: 11 April 2022
• Volume 29 , pages 4401–4430, ( 2022 )

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• Varsha Nemade 1 ,
• Sunil Pathak 1 &
• Ashutosh Kumar Dubey 2  

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21 Citations

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Breast cancer is one of the most common diseases in women; it can have long-term implications and can even be fatal. However, early detection, achieved through recent advancements in technology, can help reduce mortality. In this paper, different machine intelligence techniques [machine learning (ML), and deep learning (DL)] were analysed in the context of breast cancer. In addition, the classification of breast cancer into malignant and benign using different breast cancer image modalities were discussed. Furthermore, the diagnosis of breast cancer using various publicly and privately available image datasets, pre-processing techniques, feature extraction techniques, comparison between conventional ML and different convolutional neural network (CNN) architectures, and transfer learning techniques were discussed in detail. It also correlates the parameters and attributes impact in case of different methods applied. Advantages and the limitations of the machine intelligence approaches were highlighted based on the discussion and analysis. A total of 162 research publications was considered for the time period of 2015–2021. These are in the chronological order of their appearance. This systematic literature review will be helpful to the researchers due to the detailed analysis of different methodologies and in conducting further investigations.

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Nemade, V., Pathak, S. & Dubey, A.K. A Systematic Literature Review of Breast Cancer Diagnosis Using Machine Intelligence Techniques. Arch Computat Methods Eng 29 , 4401–4430 (2022). https://doi.org/10.1007/s11831-022-09738-3

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• v.64; 2022 Aug

Global guidelines for breast cancer screening: A systematic review ☆

a Department of Cancer Epidemiology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China

Mingyang Chen

b Center for Global Health, School of Population Medicine and Public Health, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, China

Youlin Qiao

Fanghui zhao.

Breast cancer screening guidelines could provide valuable tools for clinical decision making by reviewing the available evidence and providing recommendations. Little information is known about how many countries have issued breast cancer screening guidelines and the differences among existing guidelines. We systematically reviewed current guidelines and summarized corresponding recommendations, to provide references for good clinical practice in different countries.

Systematic searches of MEDLINE, EMBASE, Web of Science, and Scopus from inception to March 27th, 2021 were conducted and supplemented by reviewing the guideline development organizations. The quality of screening guidelines was assessed from six domains of the Appraisal of Guidelines for Research and Evaluation Ⅱ (AGREE Ⅱ) instrument by two appraisers. The basic information and recommendations of the issued guidelines were extracted and summarized.

A total of 23 guidelines issued between 2010 and 2021 in 11 countries or regions were identified for further review. The content and quality varied across the guidelines. The average AGREE Ⅱ scores of the guidelines ranged from 33.3% to 87.5%. The highest domain score was "clarity of presentation" while the domain with the lowest score was "applicability". For average-risk women, most of the guidelines recommended mammographic screening for those aged 40–74 years, specifically, those aged 50–69 years were regarded as the optimal age group for screening. Nine of 23 guidelines recommended against an upper age limit for breast cancer screening. Mammography (MAM) was recommended as the primary screening modality for average-risk women by all included guidelines. Most guidelines suggested annual or biennial mammographic screening. Risk factors of breast cancer identified in the guidelines mainly fell within five categories which could be broadly summarized as the personal history of pre-cancerous lesions and/or breast cancer; the family history of breast cancer; the known genetic predisposition of breast cancer; the history of mantle or chest radiation therapy; and dense breasts. For women at higher risk, there was a consensus among most guidelines that annual MAM or annual magnetic resonance imaging (MRI) should be given, and the screening should begin earlier than the average-risk group.

Conclusions

The majority of 23 included international guidelines were issued by developed countries which contained roughly the same but not identical recommendations on breast cancer screening age, methods, and intervals. Most guidelines recommended annual or biennial mammographic screening between 40 and 74 years for average-risk populations and annual MAM or annual MRI starting from a younger age for high-risk populations. Current guidelines varied in quality and increased efforts are needed to improve the methodological quality of guidance documents. Due to lacking clinical practice guidelines tailored to different economic levels, low- and middle-income countries (LMICs) should apply and implement the evidence-based guidelines with higher AGREE Ⅱ scores considering local adaption.

• • This systematic review comprehensively maps the recommendations of the latest international breast screening guidelines, providing valuable tools for clinical decision making in different settings.
• • Most guidelines recommend annual or biennial mammographic screening between 40 and 74 years for the average-risk populations and annual MAM or annual MRI starting from a younger age for the high-risk populations. However, there are indeed discrepancies in screening age, methods, and intervals among countries.
• • High-quality evidence and rigorous methodology are the keys to guidance development, but current guidelines vary in methodological quality.

1. Introduction

In 2021, breast cancer has overtaken lung cancer to be the world's most commonly diagnosed cancer, accounting for the severe burden globally, especially among women [ 1 ]. Screening for breast cancer is an effective measure to detect early-stage disease and improve the survival rate of cancer patients [ [2] , [3] ]. Population-based breast cancer screening programs have been implemented in many developed countries over the last decades, which contributed to reducing the mortality and the advanced cancer rate [ [4] , [5] , [6] ].

Screening guidelines could provide valuable tools for clinical decision making by reviewing the available evidence and providing recommendations. To date, several breast cancer screening guidelines have been issued in many developed countries [ [7] , [8] , [9] ]. However, the recommendations about screening age, methods, and intervals varied from different guidelines due to different institutions, based evidence, and development processes. This may confuse the clinical practice when they are applied to other countries. To our knowledge, it is currently unknown how many countries have issued breast cancer screening guidelines and the differences among these issued guidelines. Additionally, previous systematic reviews of international breast cancer screening guidelines were limited by publication date and screening population and did not systematically review screening recommendations for the population with different breast cancer risks [ [10] , [11] , [12] ].

Accordingly, our study reviewed existing breast cancer screening guidelines and summarized corresponding recommendations, in order to provide references for good clinical practice in different countries.

2. Material and methods

2.1. data sources and searches.

A search strategy was designed for MEDLINE, EMBASE, Web of Science, and Scopus from inception to March 27th, 2021 using variations on the search terms "breast cancer", "screening" and "guidelines/recommendations" ( Appendix A ). We also sought the additional guidelines by searching guideline development organizations, such as Guideline International Network (GIN), World Health Organization (WHO), Cancer Australia, Ministry of Health (MOH) Malaysia, and China Guideline Clearinghouse (CGC). Moreover, we meticulously examined the references of documents obtained above to further access potentially eligible articles.

2.2. Study selection and data extraction

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram is presented in Fig. 1 . Two reviewers (MYC and WHR) independently reviewed the titles and abstracts of the included guidelines. Any discrepancies were resolved by discussion. Finally, both reviewers determined the included guidelines based on the full text. We included guidelines following inclusion criteria: (1) originally published guidelines, consensus, or position papers related to breast cancer screening; (2) the latest versions of the updated guidelines; (3) English or Chinese guidelines; and (4) full text was available. We excluded guidelines if they were: summaries or interpreted versions of guidelines.

Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram.

Two independent reviewers (MYC and WHR) extracted information using a predesigned template. The information extracted included: (1) basic information (countries or regions, publication years, publication organizations, names of guidelines, number of updated versions, and publication years of old versions); (2) screening recommendations for the population at average risk and higher risk (screening age, screening methods, screening intervals, level of evidence, and strength of recommendation).

2.3. Quality assessment

The methodological quality of guidelines was evaluated using the Appraisal of Guidelines for Research and Evaluation Ⅱ (AGREE Ⅱ) instrument. This is a standardized tool for evaluating the methodological framework of guideline development which consists of 23 main items in six domains (scope and purpose, stakeholder involvement, rigour of development, clarity of presentation, applicability, and editorial independence) and two global rating items [ 13 ]. Each item is rated on a seven-point Likert-type scale from one (strongly disagree) to seven (strongly agree) according to the criteria and considerations articulated in the User's Manual. Scores are assigned depending on the completeness and quality of reporting. Scores increase as more criteria are met and considerations are addressed. Domain scores are calculated by summing up all the scores of the individual items in that domain and by scaling the total as a percentage of the maximum possible score for that domain. Two reviewers (MYC and WHR) independently scored each guideline. Evaluation results were compared and discrepancies of more than two points per item were discussed to reach a consensus. According to prior studies, the quality of guidelines was classified as high if the total score was 60% or higher and low if the score was less than 60% [ 14 , 15 ].

A total of 7417 citations were included during the preliminary literature search process, but most were excluded after deleting duplicates and applying the inclusion and exclusion criteria. Of these, 23 guidelines were identified for further review ( Fig. 1 ).

3.1. Guideline characteristics

Table 1 displays the general characteristics of 23 included guidelines that were published between 2010 and 2021 [ [7] , [8] , [9] , [16] , [17] , [18] , [19] , [20] , [21] , [22] , [23] , [24] , [25] , [26] , [27] , [28] , [29] , [30] , [31] , [32] , [33] , [34] , [35] ]. The majority of guidelines (17 of 23) were drawn from developed countries or regions. Guidelines from the United States accounted for the largest proportion, reaching 39.1%. One was developed by WHO, and four in Europe ( Fig. 2 ). 12 of 23 guidelines have been updated.

Characteristics of 23 included guidelines on screening for breast cancer.

Abbreviations: ACOG: American College of Obstetricians and Gynecologists; ACP: American College of Physicians; ACR: American College of Radiology; ACS: American Cancer Society; AWMF: German Association of Scientific Medical Societies; CBR: Brazilian College of Radiology and Diagnostic Imaging; CEWG: Cancer Expert Working Group; CTFPHC: Canadian Task Force on Preventive Health Care; DKG: German Cancer Society; DKH: German Cancer Aid; ECIBC: European Commission Initiative on Breast Cancer; ESMO: European Society for Medical Oncology; EUSOMA: European Society of Breast Cancer Specialists; FEBRASGO: Brazilian Federation of Gynecological and Obstetrical Associations; MOH: Ministry of Health; NCC: National Cancer Centre; NCCN: National Comprehensive Cancer Network; SBI: Society of Breast Imaging; SBM: Brazilian Society for Breast Disease; USPSTF: U.S. Preventive Services Task Force; WHO: World Health Organization.

Geographical distribution of the included breast cancer screening guidelines.

3.2. Quality assessment

The included 23 guidelines were appraised using AGREE II Criteria ( Fig. 3 ). The average AGREE II scores varied from 33.3% to 87.5%. 12 guidelines were scored over 60.0% [ [7] , [8] , [16] , [17] , [23] , [24] , [25] , [27] , [30] , [31] , [32] , [34] ]. Among these, the guideline issued by Canadian Task Force on Preventive Health Care (CTFPHC) [ 27 ] was scored the highest (87.5%), followed by European Commission Initiative on Breast Cancer (ECIBC) [ 25 ], American Cancer Society (ACS) [ 23 ], United States Preventive Services Taskforce (USPSTF) [ 7 ], and WHO [ 16 ]. The highest domain score was "clarity of presentation" (domain 4), with an average score of 81.9%, followed by "scope and purpose" (domain 1). The domain with the lowest score was "applicability" (domain 5) with an average score of 21.3%, followed by "stakeholder involvement" (domain 2).

Quality of the included guidelines for the six domains of the AGREE Ⅱ instrument.

( Abbreviations: ACOG: American College of Obstetricians and Gynecologists; ACP: American College of Physicians; ACR: American College of Radiology; ACS: American Cancer Society; AWMF: German Association of Scientific Medical Societies; CBR: Brazilian College of Radiology and Diagnostic Imaging; CEWG: Cancer Expert Working Group; CTFPHC: Canadian Task Force on Preventive Health Care; ECIBC: European Commission Initiative on Breast Cancer; ESMO: European Society for Medical Oncology; EUSOMA: European Society of Breast Cancer Specialists; MOH: Ministry of Health; NCC: National Cancer Centre; NCCN: National Comprehensive Cancer Network; SBI: Society of Breast Imaging; USPSTF: U.S. Preventive Services Task Force; WHO: World Health Organization).

3.3. Strength of recommendations and quality of evidence

17 of 23 guidelines reported eight applied grading systems. Grading of Recommendations, Assessment, Development and Evaluations (GRADE) was the common system that was applied in six guidelines [ 16 , 23 , 25 , 27 , 32 , 34 ]. Four guidelines used the self-designated grading system [ 8 , 9 , 18 , 30 ]. The details about the strength of recommendations and the quality of evidence varied in different grading systems. The information of evidence and recommendation about the included guidelines is shown in Table 2 .

Grading systems used in the included guidelines.

Abbreviations: ACOG: American College of Obstetricians and Gynecologists; ACS: American Cancer Society; ACR: American College of Radiology; AWMF: German Association of Scientific Medical Societies; CBR: Brazilian College of Radiology and Diagnostic Imaging; CTFPHC: Canadian Task Force on Preventive Health Care; DKG: German Cancer Society; DKH: German Cancer Aid; ECIBC: European Commission Initiative on Breast Cancer; ESMO: European Society for Medical Oncology; EUSOMA: European Society of Breast Cancer Specialists; FEBRASGO: Brazilian Federation of Gynecological and Obstetrical Associations; GPP: Good Practice Points; GRADE: Grading of Recommendations, Assessment, Development and Evaluations; JRGCSG: Japanese Research Group for the Development of Cancer Screening Guidelines; MOH: Ministry of Health; NCC: National Cancer Centre; NCCN: National Comprehensive Cancer Network; OCEBM: Oxford Centre for Evidence-based Medicine; RAM: RAND/UCLA Appropriateness Method; SBM: Brazilian Society for Breast Disease; USPSTF: U.S. Preventive Services Task Force; WHO: World Health Organization.

3.4. The screening recommendations for women at average risk

The detailed information of recommendations for average-risk women is shown in Table 3 , which summarized screening age, screening methods, screening intervals, and other recommended screening methods ( Fig. 4 ).

The screening recommendations in average-risk women in eligible guidelines.

Abbreviations: ABUS: Automated Breast Ultrasonography; ACOG: American College of Obstetricians and Gynecologists; ACP: American College of Physicians; ACR: American College of Radiology; ACS: American Cancer Society; AWMF: German Association of Scientific Medical Societies; BSE: Breast Self-Examination; CBE: Clinical Breast Examination; CBR: The Brazilian College of Radiology and Diagnostic Imaging; CTFPHC: Canadian Task Force on Preventive Health Care; DKG: German Cancer Society; DKH: German Cancer Aid; DBT: Digital Breast Tomosynthesis; ECIBC: European Commission Initiative on Breast Cancer; ESMO: European Society for Medical Oncology; FEBRASGO: Brazilian Federation of Gynecological and Obstetrical Associations; HHUS: Hand-Held Ultrasound; MAM: Mammography; MBI: Molecular Breast Imaging; MOH: Ministry of Health; MRI: Magnetic Resonance Imaging; NCC: National Cancer Centre; NCCN: National Comprehensive Cancer Network; NR: No Recommendation; SBM: The Brazilian Society for Breast Disease; SDM: Shared Decision Making; US: Ultrasound; USPSTF: U.S. Preventive Services Task Force; WHO: World Health Organization.

The main screening recommendations in average-risk women in the eligible guidelines.

( Abbreviations: CBE: Clinical Breast Examination; MAM: Mammography; US: Ultrasound)

3.4.1. Screening age

The majority of guidelines recommended mammographic screening for average-risk individuals aged 40–74 years [ [7] , [8] , [9] , 16 , 17 , 29 , 35 ], and recommended women aged 50–69 years as the optimal age group for screening with strong recommendation [ 8 , 16 , 25 , 28 , 30 , 34 ]. National Comprehensive Cancer Network (NCCN) [ 18 ] and American College of Obstetricians and Gynecologists (ACOG) [ 24 ] suggested starting screening at age 25 by clinical encounter or clinical breast examination (CBE).

Nine of 23 guidelines did not recommend an upper age limit for breast cancer screening [ 8 , 9 , 16 , 18 , 20 , 25 , 27 , 31 , 32 ]. Some guidelines, including American College of Radiology (ACR) [ 21 ], ACR and Society of Breast Imaging (SBI) [ 22 ], and ACS [ 23 ] suggested that the age to end screening should be determined based on the women's health status, for example, stopping screening for women with life expectancy lower than 5–7 years or 10 years. Other guidelines, like USPSTF [ 7 ], American College of Physicians (ACP) [ 17 ], and Brazilian College of Radiology and Diagnostic Imaging (CBR)/Brazilian Society for Breast Disease (SBM)/Brazilian Federation of Gynecological and Obstetrical Associations (FEBRASGO) [ 35 ] did not recommend breast cancer screening for women aged over 75 years unless their life expectancy were higher than 7 years or 10 years. German Association German Cancer Society of Scientific Medical Societies (AWMF)/German Cancer Society (DKG)/German Cancer Aid (DKH) [ 28 ] and MOH of Singapore [ 30 ] recommended stopping screening at age 70.

3.4.2. Screening methods and intervals

Mammography (MAM) was recommended as the primary screening modality for average-risk women by all included guidelines [ [7] , [8] , [9] , [16] , [17] , [18] , [19] , [21] , [22] , [23] , [24] , [25] , [26] , [27] , [28] , [29] , [30] , [31] , [32] , [34] , [35] ]. Most guidelines suggested annual or biennial mammographic screening [ 7 , 16 , 17 , 29 , 31 ]. Three guidelines recommended screening every 1–2 years [ [8] , [23] , [32] ]. Some guidelines agreed that screening intervals should be determined based on age [ 18 , 24 ]. ACS [ 23 ] recommended screening with MAM annually for women aged 40–54 years and every 1–2 years for women aged 55 years or older. ECIBC [ 25 ] recommended screening every 2–3 years for women aged 40–49 years and for women aged 70–74 years. For the priority screening groups (women aged 50–69 years), annual screening was not recommended, and biennial screening is better than triennial screening.

The recommendations of each guideline on CBE and ultrasound (US) were different in detail. NCCN [ 18 ] and ACOG [ 24 ] suggested that CBE should be given every 1–3 years for women aged 25–39 years and annually for women older than 40 years, but ACS [ 23 ] and CTFPHC [ 27 ] did not recommend CBE as a primary screening method. Among the included screening guidelines, only National Cancer Centre (NCC) of China [ 32 ] recommended screening every 1–2 years for women older than 45 years using US alone.

All guidelines did not recommend using breast self-examination (BSE), magnetic resonance imaging (MRI), and computed tomography (CT) to screen for average-risk women because of lacking evidence of benefit.

3.5. The screening recommendations for women at higher risk

Risk factors of breast cancer identified in the guidelines mainly fell within five categories which could be broadly summarized as the personal history of pre-cancerous lesions and/or breast cancer; the family history of breast cancer; the known genetic predisposition of breast cancer; the history of mantle or chest radiation therapy; and dense breasts. For women at higher risk, there was a consensus among most guidelines that annual MAM screening or annual MRI screening should be given and the starting age should be earlier than the average-risk group ( Table 4 ; Fig. 5 ) .

The screening recommendations in high-risk women in eligible guidelines.

Abbreviations: ACR: American College of Radiology; BRCA: Breast cancer gene; BSE: Breast Self-Examination; CBE: Clinical Breast Examination; CBR: Brazilian College of Radiology and Diagnostic Imaging; CEWG: Cancer Expert Working Group; DBT: Digital Breast Tomosynthesis; DM: Digital Mammography; ESMO: European Society for Medical Oncology; EUSOMA: European Society of Breast Cancer Specialists; FEBRASGO: Brazilian Federation of Gynecological and Obstetrical Associations; MAM: mammography; MOH: Ministry of Health; MRI: Magnetic Resonance Imaging; NCC: National Cancer Centre; NCCN: National Comprehensive Cancer Network; NR: No Recommendation; SBI: Society of Breast Imaging; SBM: Brazilian Society for Breast Disease; US: Ultrasound.

The main screening recommendations in high-risk women in the eligible guidelines.

( Abbreviations: BSE: Breast Self Examination; CBE: Clinical Breast Examination; MAM: Mammography; MRI: Magnetic Resonance Imaging; NR: No Recommendation; US: Ultrasound)

3.5.1. Women with the personal history of pre-cancerous lesions and/or breast cancer

For women with biopsy-proven Lobular Carcinoma in Situ (LCIS), Atypical Ductal Hyperplasia (ADH), Ductal Carcinoma in Situ (DCIS), or invasive breast cancer or ovarian cancer, annual MAM or annual MRI was mainly recommended after diagnosis onward [ 18 , 20 , 22 , 31 , 33 , 35 ] . Especially for patients with unilateral invasive breast cancer, close monitoring of the contralateral breast was recommended. NCCN [ 18 ] also recommended breast awareness and clinical encounter every 6–12 months for this group of women. NCC of China [ 32 ] recommended MAM and US as screening methods for women at higher risk of breast cancer.

3.5.2. Women with the family history of breast cancer

For women with a family history suspicious of the inherited predisposition of breast cancer, two guidelines recommended that an annual MAM or annual MRI began 10 years before the age of diagnosis of the youngest-affected relative but not before the age of 30 [ 18 , 33 ]. NCCN [ 18 ] also recommended regular clinical visits every 6–12 months once the women were identified as begin at increased risk of breast cancer.

3.5.3. Women with the known genetic predisposition of breast cancer

Women with breast cancer susceptibility gene 1 (BRCA1) or breast cancer susceptibility gene 2 (BRCA2) mutations, or untested but have first-degree relatives (mothers, sisters, or daughters) who are proven to have BRCA mutations, have a higher risk for breast cancer. Two guidelines recommended that women with gene mutations should start to undertake annual MAM or annual MRI at 25–30 years [ 22 , 30 ]. European Society of Breast Cancer Specialists (EUSOMA) [ 26 ] recommended that annual MRI screening was performed for women carrying BRAC at 25–29 years, and those carrying TP53 at 20 years. MOH of Malaysia [ 31 ] provided age-specific recommendations for women carrying gene mutations, specifically, annual MRI for 30–49 years, annual MAM for 40–69 years, and biennial MAM for 70 years and above. For other recommended screening methods, ACR [ 19 ] recommended MRI as an adjunct to MAM or DBT and recommended US when the patient cannot tolerate MRI. MOH of Singapore [ 30 ] also recommended monthly BSE and 6 monthly CBE.

3.5.4. Women with the history of mantle or chest radiation therapy

For women with a history of mantle or chest radiation therapy that occurred before the age of 30 years or had a cumulative dose of 10 Gy radiation, most guidelines recommended starting regular screening 8 or 10 years after radiation therapy [ [18] , [19] , [20] , 35 ]. Recommended screening strategies included annual MAM (not before age 30), annual MRI (not before age 25), or annual digital mammography (DM) (with or without digital breast tomosynthesis (DBT)). NCCN [ 18 ] also recommended increasing breast awareness or clinical encounters every 6–12 months.

3.5.5. Women with dense breasts

For women with dense breasts, ACR [ 20 ] recommended MRI should be performed annually. NCC of China [ 32 ] recommended screening with MAM and US annually. US (as adjunctive screening tools) was recommended for high-risk women who may be suitable for MRI but can not be accepted for any reason [ 20 ]. Two guidelines [ [22] , [35] ] also recommended US as an adjunctive examination to MAM in asymptomatic women with dense breasts.

4. Discussion

To the best of our knowledge, this study is the largest and most comprehensive systematic review, which identified and compared the latest international breast screening guidelines and recommendations. A total of 23 guidelines issued between 2010 and 2021 in 11 countries or regions were included in this study. The content and quality varied between the guidelines. The average AGREE Ⅱ scores ranged from 33.3% to 87.5%, which is consistent with that reported by Li J et al. [ 12 ]. We found discrepancies between guidelines concerning screening age, methods, and intervals. In general, the majority of guidelines agreed upon annual or biennial MAM for average-risk women aged 40 to 74. Annual MAM or annual MRI should be given and start earlier for women at high risk for breast cancer.

Our study showed that many low- and middle-income countries (LMICs) lacked published clinical practice guidelines for breast cancer screening. Most included guidelines in our study were issued by developed countries, mainly in the United States (9/23) and Europe (4/23). One possible explanation is that high-income countries have accumulated more high-quality evidence for developing guidelines by implementing breast cancer screening programs and related research for a long time [ [4] , [5] , [6] ]. However, although LMICs have a severe breast cancer burden, few tailored guidelines have been issued due to lacking sufficient national evidence about breast cancer screening and the front-line impact of sparse resources to develop guidelines in these areas [ 36 , 37 ]. Additionally, some LMICs guidelines might be published in local languages and were not picked up in our search. We also found that some guidelines issued by LMICs are often based on evidence from high-income countries. The extent to which these guidelines can be applied to the clinical practice of routine screening in LMICs is unknown.

High-quality guidelines are vital to facilitate clinical decision making and to improve health outcomes and health service efficiency. Our findings showed nearly half of the included guidelines were rated as high quality. Most of the guidelines provided a clear description of "scope and purpose" as screening for populations with different breast cancer risks, and screening recommendations were described clearly. For these reasons, the domains "scope and purpose" and "clarity of presentation" received high scores. In contrast, the majority of the guidelines received low scores in the domains of "rigour of development" and "applicability". According to prior studies [ [38] , [39] ], the domain "rigour of development" was the most relevant to the overall quality of the guideline. The main reason was that this domain reflects the evidence collection and synthesis process, as well as the formation and follow-up update of recommendations, which can provide enough information to evaluate whether the guidelines followed the best methodology and developed evidence-based recommendations. Meanwhile, the development process of guidelines is also one of the key reasons causing the variations between the recommendations from different guidance documents. In our study, 17 of 23 guidelines reported using eight different grading systems to evaluate the quality of evidence and strength of recommendations, which somewhat impeded the implementation of the guidelines and caused confusion in clinical practice. The most important purpose of guidelines is to promote their application to real-world medicine practice. Therefore, guideline developers should clearly describe the promotion conditions and hindrance factors in the implementation of recommendations and their improvement strategies, as well as consider the likely resource implications involved. At the same time, the quality of the "applicability" domain also plays a critical role in whether they can be extended to LMICs that might lack indigenous guidelines. Our study showed that the scores of different guidelines varied greatly in the domain "applicability". For example, the guideline issued by MOH of Malaysia [ 31 ] contained a separate section called "implementing the guidelines", which described the types of facilitators and barriers in detail, as well as put forward suggestions to ensure the implementation of the guideline. In contrast, the "ACR Appropriateness Criteria® Breast Cancer Screening" [ 19 ] did not mention facilitators and barriers to its application. Based on the above considerations, we considered the guideline developed by MOH of Malaysia with high "applicability" rather than ACR.

The majority of guidelines recommended mammographic screening for average-risk women aged 40–74 years. 50–69 years were regarded as the optimal age group for screening due to the steep increase of breast cancer beginning around age 50. In 2019, almost 82% of breast cancer was diagnosed among women aged ≥ 50 years in the United States [ 40 ]. Most randomized controlled trials (RCTs) from developed countries also showed that mammographic screening between 50 and 69 years had the greatest benefit in reducing mortality [ [41] , [42] ]. However, due to the disease burden of breast cancer and the allocation of public health resources vary in different countries, a one-size-fits-all approach to screening is considered inapplicable. In several Asian countries, such as Japan and South Korea, the peak age of breast cancer incidence in women mainly ranges from 45 to 69 years old which is more than 10 years earlier than that in Europe and the United States [ 43 , 44 ]. Although some Asian guidelines agreed on beginning screening from the age of 40 or 45 years [ 9 , 30 , 32 ], high-quality evidence from large population-based RCTs is insufficient. In addition, based on several RCTs conducted in Canada, the UK, and Sweden, ECIBC and CTFPHC did not recommend regular screening begin at 40–44 years since the lower absolute benefit and higher overdiagnosis and false positives rate with related biopsies of this age group [ 2 , 25 , 27 , [45] , [46] , [47] ]. Furthermore, nine of 23 guidelines did not recommend an upper age limit. However, some guidelines recommended against regular screening for women older than age 70 or 75 years, as the harm potentially exceeds the benefits if screening is continued after these age groups [ 48 ]. The risk of breast cancer increases with age. Consequently, the decision to stop screening should be individually based on life expectancy or comorbid conditions.

Currently, MAM is widely accepted in developed countries with sufficient evidence to decrease breast cancer mortality among women aged 50–74 years and is recommended as a primary screening method in most screening guidelines [ 49 ]. Due to relatively high cost and the demand for high-quality radiologists, the application of MAM in low resource areas is limited [ 50 ]. Additionally, because higher mammographic density is associated with the masking of breast cancer on a mammogram, the sensitivity of MAM for women with dense breasts is lower than that for women with mainly fatty breasts [ 51 ]. Mammographic density among Asian women is higher than among Western women [ 52 ]. Several Asian studies have shown that US can improve the detection rate of breast cancer for women with dense breasts [ 53 , 54 ]. However, there is limited evidence for US in breast cancer screening to reduce mortality. Accordingly, the guidelines from European and American countries did not recommend US as the primary technique for breast cancer screening in average-risk population, but mainly as a supplemental method to MAM. Among the included guidelines of the present study, only Chinese guidelines recommended US as the primary screening tool. China has carried out a national breast cancer screening program since 2009. The screening tool of the program was changed from CBE to US in 2012, which provided preliminary evidence for the application of US in breast cancer screening in other Asian countries [ 55 , 56 ].

With greater emphasis on more accurate risk management based on patients and more personalized recommendations for diagnosis, treatment, and follow-up, age-oriented screening suggestions have been shifted to risk-based screening recommendations. By accurately identifying women who are above-average risk in the general population, we can provide timely and effective early diagnosis measures. High-risk women identified in the guidelines fell within many categories. The related recommendations for every category of high-risk women were different, which brought some difficulties to the implementation of breast cancer screening for high-risk women in the low resource areas. Thereby, identifying the risk factors of breast cancer by establishing a risk assessment model may be an effective way to prevent breast cancer. Currently, various risk prediction models were developed, such as the Gail model and BOADICEA model, whose application values in different countries are still under evaluation [ 57 , 58 ]. It is reported that China applies risk models as supplementary tools for screening in urban areas [ 59 ].

Few guidelines provided explicit recommendations for the management of women with positive findings except for NCCN [ 18 ] and NCC China [ 32 ]. Improper management of abnormal screening results may compromise the effectiveness of breast cancer screening programs. Doubeni et al. performed the PROSPR multi-model microsimulation study, which showed that the relative risk for the late-stage disease was higher when the time for diagnostic testing was delayed after an abnormal mammogram [ 60 ]. A previous study observed that low-income women and women of ethnic minority (African-American and Asian women) were less likely to have adequate follow-up abnormal breast cancer screening mammograms [ 61 ]. For these reasons, it is necessary to explore different referral and recall standards according to different initial screening results, to make a balance between the anxiety caused by false-positive breast cancer and the benefit of follow-up.

The strengths of this systematic review include its originality and the most comprehensive search strategy. This study was the largest and comprehensive systematic review to map the recommendations of the latest international breast screening guidelines. Furthermore, we systemically summarized the screening recommendations for both average-risk women and high-risk women.

Our study has some limitations. Even though we performed a comprehensive systematic search, we could not find all relevant guidelines. And we also did not include the breast screening program protocols in some countries. Another limitation was that non-English guidelines were not included in this review due to translation restrictions.

5. Conclusions

In summary, this study reviewed and compared the latest international breast screening guidelines for women both at average risk and at higher risk. The majority of guidelines were issued by developed countries, containing roughly the same but not identical recommendations for breast cancer on screening age, methods, and intervals. Most guidelines recommended annual or biennial mammographic screening for average-risk populations aged between 40 and 74 years and early annual MAM or annual MRI for high-risk populations. Current guidelines varied in methodological quality and increased efforts are needed to develop high-quality guidelines to provide more powerful supporting evidence for guidelines users. LMICs lacked published tailored clinical practice guideline. Therefore, we encourage policymakers and clinicians to use the evidence-based guidelines with higher AGREE Ⅱ scores considering local adaption.

Funding source

This work was supported by International Agency for Research on Cancer, France; World Health Organization, Switzerland [grant numbers CRA/SCR/2019/1].

Declaration of competing interest

All authors declare that they have no conflict of interest.

Acknowledgments

We gratefully acknowledge Ms. Huijiao Yan for her linguistic assistance during the revision of this manuscript.

☆ Present address: Department of Cancer Epidemiology, National Cancer Centre/National Clinical Research Centre for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, 17 South Pan Jia Yuan Lane, Beijing 100,021, China.

Appendix A. Electronic search strategies

A) medline (via pubmed).

((Breast Neoplasms [MH] OR breast cancer* [tiab] OR breast neoplasm* [tiab] OR breast carcinoma* [tiab] OR breast tumor* [tiab] OR breast tumour* [tiab] OR mammary cancer* [tiab] OR mammary neoplasm* [tiab] OR mammary carcinoma* [tiab] OR mammary tumor* [tiab] OR mammary tumour* [tiab])

("Mass Screening" [Mesh] OR "Early Detection of Cancer" [Mesh] OR screening [tiab] OR early detect*[tiab])

(("Guideline" [Publication Type] OR "Practice Guideline" [Publication Type]) OR ("Guidelines as Topic" [Mesh] OR "Health Planning Guidelines" [Mesh] OR consensus [MeSH]) OR (guideline [Title] OR guidelines [Title] OR "practice guideline" [Title] OR "practice guidelines" [Title] OR "Health Planning Guidelines" [Title] OR Guidance [Title] OR consensus [Title] OR recommendations [Title] OR recommendation [Title] OR manual [Title] OR guidebook [Title] OR guidebooks [Title] OR guide [Title] OR guides [Title] OR handbook [Title] OR handbooks [Title])))

B) EMBASE via embase.com

('breast cancer'/exp OR 'breast tumor'/exp OR 'breast carcinoma*'/exp OR ('breast neoplasm*' OR 'breast tumor*' OR 'breast tumour*' OR 'mammary cancer*' OR 'mammary neoplasm*' OR 'mammary carcinoma*' OR 'mammary tumor*' OR 'mammary tumour*'):ab,ti

('Mass Screening'/exp OR 'early cancer diagnosis'/exp OR "screening":ab, ti OR early detect:ab,ti)

('Practice Guideline'/exp OR 'health care planning'/exp OR consensus/exp OR (guideline OR guidelines OR 'practice guideline' OR 'practice guidelines' OR 'Health Planning Guidelines' OR Guidance OR consensus OR recommendations OR recommendation OR manual OR guidebook OR guidebooks OR guide OR guides OR handbook OR handbooks):ti)

C) Web of Science

TI or AB=("breast cancer*" OR "breast neoplasm*" OR "breast carcinoma*" OR "breast tumor*" OR "breast tumour*" OR "mammary cancer*" OR "mammary neoplasm*" OR "mammary carcinoma*" OR "mammary tumor*" OR "mammary tumour*")

TI or AB=("Mass Screening" OR "Early Detection of Cancer" OR screening OR "early detect*")

TI=(guideline OR guidelines OR "Practice Guideline" OR "practice guidelines" OR consensus OR Guidance OR recommendation OR recommendations OR manual OR guide OR guides OR guidebook OR guidebooks OR handbook OR handbooks)

TITLE-ABS("breast cancer*" OR "breast neoplasm*" OR "breast carcinoma*" OR "breast tumor*" OR "breast tumour*" OR "mammary cancer*" OR "mammary neoplasm*" OR "mammary carcinoma*" OR "mammary tumor*" OR "mammary tumour*")

TITLE-ABS("Mass Screening" OR "Early Detection of Cancer" OR screening OR "early detect*")

TITLE (guideline OR "Practice Guideline" OR consensus OR Guidance OR recommendation OR manual OR guide OR guidebook OR handbook)

• Conclusions
• Article Information

Evidence reviews for the USPSTF use an analytic framework to visually display the key questions that the review will address in order to allow the USPSTF to evaluate the effectiveness and safety of a preventative service. The questions are depicted by linkages that relate interventions and outcomes. A dashed line indicates a health outcome that immediately follows an intermediate outcome. For additional details see the US Preventive Services Task Force Procedure Manual. 13

Reasons for exclusion: Design: Study did not use an included design. Outcomes: Study did not have relevant outcomes or had incomplete outcomes. Comparator: Study used an excluded comparator. Intervention: Study used an excluded intervention/screening approach. Population: Study was not conducted in an average-risk population. Timing: Study only reported first (prevalence) round screening follow-up. Publication type: Study was published in non–English-language or only available in an abstract. Quality: Study did not meet criteria for fair or good quality. Setting: Study was not conducted in a setting relevant to US practice. KQ indicates key question.

DBT indicates digital breast tomosynthesis; DM, digital mammography; and RR, relative risk.

a From random-effects restricted maximum likelihood model.

eMethods. Literature Search Strategies for Primary Literature

eTable 1. Inclusion and Exclusion Criteria

eTable 2. Quality Assessment Criteria

eTable 3. Included Studies and Their Ancillary Publications

eTable 4. Screen-Detected DCIS Diagnosed in Studies Comparing Digital Breast Tomosynthesis and Digital Mammography

eFigure 1. Pooled Analysis of Screen-Detected Invasive Cancers Diagnosed in Trials Comparing Digital Breast Tomosynthesis and Digital Mammography

eFigure 2. Pooled Analysis of Interval Cancers Diagnosed in Trials Comparing Digital Breast Tomosynthesis and Digital Mammography

eFigure 3. Cumulative Probability of False-Positive Biopsy in One NSRI Using BCSC Data Comparing Annual vs Biennial Screening with DBT or DM

eFigure 4. Cumulative Probability of False-Positive Recall in One NSRI Using BCSC Data Comparing Annual vs Biennial Screening with DBT or DM

eFigure 5. Cumulative Probability of False-Positive Recall or Biopsy in One NSRI Using BCSC Data Comparing Annual vs Biennial Screening with DBT or DM, among Women with Extremely Dense Breasts

• USPSTF Recommendation: Screening for Breast Cancer JAMA US Preventive Services Task Force June 11, 2024 This 2024 Recommendation Statement from the US Preventive Services Task Force recommends biennial screening mammography for women aged 40 to 74 years (B recommendation) and concludes that evidence is insufficient to assess the balance of benefits and harms of screening mammography in women 75 years or older (I statement) and of screening using ultrasonography or MRI in women with dense breasts on a negative mammogram (I statement). US Preventive Services Task Force; Wanda K. Nicholson, MD, MPH, MBA; Michael Silverstein, MD, MPH; John B. Wong, MD; Michael J. Barry, MD; David Chelmow, MD; Tumaini Rucker Coker, MD, MBA; Esa M. Davis, MD, MPH; Carlos Roberto Jaén, MD, PhD, MS; Marie Krousel-Wood, MD, MSPH; Sei Lee, MD, MAS; Li Li, MD, PhD, MPH; Carol M. Mangione, MD, MSPH; Goutham Rao, MD; John M. Ruiz, PhD; James J. Stevermer, MD, MSPH; Joel Tsevat, MD, MPH; Sandra Millon Underwood, PhD, RN; Sarah Wiehe, MD, MPH
• USPSTF Report: Collaborative Modeling to Compare Breast Cancer Screening Strategies JAMA US Preventive Services Task Force June 11, 2024 This modeling study uses Cancer Intervention and Surveillance Modeling Network models and national data on breast cancer incidence, mammography performance, treatment effects, and other-cause mortality in US women without previous cancer diagnoses to estimate outcomes of various mammography screening strategies. Amy Trentham-Dietz, PhD, MS; Christina Hunter Chapman, MD, MS; Jinani Jayasekera, PhD, MS; Kathryn P. Lowry, MD; Brandy M. Heckman-Stoddard, PhD, MPH; John M. Hampton, MS; Jennifer L. Caswell-Jin, MD; Ronald E. Gangnon, PhD; Ying Lu, PhD, MS; Hui Huang, MS; Sarah Stein, PhD; Liyang Sun, MS; Eugenio J. Gil Quessep, MS; Yuanliang Yang, MS; Yifan Lu, BASc; Juhee Song, PhD; Diego F. Muñoz, PhD; Yisheng Li, PhD, MS; Allison W. Kurian, MD, MSc; Karla Kerlikowske, MD; Ellen S. O’Meara, PhD; Brian L. Sprague, PhD; Anna N. A. Tosteson, ScD; Eric J. Feuer, PhD; Donald Berry, PhD; Sylvia K. Plevritis, PhD; Xuelin Huang, PhD; Harry J. de Koning, MD, PhD; Nicolien T. van Ravesteyn, PhD; Sandra J. Lee, ScD; Oguzhan Alagoz, PhD, MS; Clyde B. Schechter, MD, MA; Natasha K. Stout, PhD; Diana L. Miglioretti, PhD, ScM; Jeanne S. Mandelblatt, MD, MPH
• Toward More Equitable Breast Cancer Outcomes JAMA Editorial June 11, 2024 Joann G. Elmore, MD, MPH; Christoph I. Lee, MD, MS
• When Is It Best to Begin Mammograms, and How Often? JAMA Medical News & Perspectives June 11, 2024 This Medical News story discusses new USPSTF recommendations about the timing of screening mammograms. Rita Rubin, MA
• Screening for Breast Cancer JAMA JAMA Patient Page June 11, 2024 In this JAMA Patient Page, the US Preventive Services Task Force provides a guide to screening for breast cancer. US Preventive Services Task Force
• New Recommendations for Breast Cancer Screening—In Pursuit of Health Equity JAMA Network Open Editorial April 30, 2024 Lydia E. Pace, MD, MPH; Nancy L. Keating, MD, MPH
• USPSTF Breast Cancer Screening Guidelines Do Not Go Far Enough JAMA Oncology Editorial June 1, 2024 Wendie A. Berg, MD, PhD

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Henderson JT , Webber EM , Weyrich MS , Miller M , Melnikow J. Screening for Breast Cancer : Evidence Report and Systematic Review for the US Preventive Services Task Force . JAMA. 2024;331(22):1931–1946. doi:10.1001/jama.2023.25844

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Screening for Breast Cancer : Evidence Report and Systematic Review for the US Preventive Services Task Force

• 1 Kaiser Permanente Evidence-based Practice Center, Center for Health Research, Portland, Oregon
• 2 University of California Davis Center for Healthcare Policy and Research, Sacramento
• Editorial Toward More Equitable Breast Cancer Outcomes Joann G. Elmore, MD, MPH; Christoph I. Lee, MD, MS JAMA
• Editorial New Recommendations for Breast Cancer Screening—In Pursuit of Health Equity Lydia E. Pace, MD, MPH; Nancy L. Keating, MD, MPH JAMA Network Open
• Editorial USPSTF Breast Cancer Screening Guidelines Do Not Go Far Enough Wendie A. Berg, MD, PhD JAMA Oncology
• US Preventive Services Task Force USPSTF Recommendation: Screening for Breast Cancer US Preventive Services Task Force; Wanda K. Nicholson, MD, MPH, MBA; Michael Silverstein, MD, MPH; John B. Wong, MD; Michael J. Barry, MD; David Chelmow, MD; Tumaini Rucker Coker, MD, MBA; Esa M. Davis, MD, MPH; Carlos Roberto Jaén, MD, PhD, MS; Marie Krousel-Wood, MD, MSPH; Sei Lee, MD, MAS; Li Li, MD, PhD, MPH; Carol M. Mangione, MD, MSPH; Goutham Rao, MD; John M. Ruiz, PhD; James J. Stevermer, MD, MSPH; Joel Tsevat, MD, MPH; Sandra Millon Underwood, PhD, RN; Sarah Wiehe, MD, MPH JAMA
• US Preventive Services Task Force USPSTF Report: Collaborative Modeling to Compare Breast Cancer Screening Strategies Amy Trentham-Dietz, PhD, MS; Christina Hunter Chapman, MD, MS; Jinani Jayasekera, PhD, MS; Kathryn P. Lowry, MD; Brandy M. Heckman-Stoddard, PhD, MPH; John M. Hampton, MS; Jennifer L. Caswell-Jin, MD; Ronald E. Gangnon, PhD; Ying Lu, PhD, MS; Hui Huang, MS; Sarah Stein, PhD; Liyang Sun, MS; Eugenio J. Gil Quessep, MS; Yuanliang Yang, MS; Yifan Lu, BASc; Juhee Song, PhD; Diego F. Muñoz, PhD; Yisheng Li, PhD, MS; Allison W. Kurian, MD, MSc; Karla Kerlikowske, MD; Ellen S. O’Meara, PhD; Brian L. Sprague, PhD; Anna N. A. Tosteson, ScD; Eric J. Feuer, PhD; Donald Berry, PhD; Sylvia K. Plevritis, PhD; Xuelin Huang, PhD; Harry J. de Koning, MD, PhD; Nicolien T. van Ravesteyn, PhD; Sandra J. Lee, ScD; Oguzhan Alagoz, PhD, MS; Clyde B. Schechter, MD, MA; Natasha K. Stout, PhD; Diana L. Miglioretti, PhD, ScM; Jeanne S. Mandelblatt, MD, MPH JAMA
• Medical News & Perspectives When Is It Best to Begin Mammograms, and How Often? Rita Rubin, MA JAMA
• JAMA Patient Page Screening for Breast Cancer US Preventive Services Task Force JAMA

Importance   Breast cancer is a leading cause of cancer mortality for US women. Trials have established that screening mammography can reduce mortality risk, but optimal screening ages, intervals, and modalities for population screening guidelines remain unclear.

Objective   To review studies comparing different breast cancer screening strategies for the US Preventive Services Task Force.

Data Sources   MEDLINE, Cochrane Library through August 22, 2022; literature surveillance through March 2024.

Study Selection   English-language publications; randomized clinical trials and nonrandomized studies comparing screening strategies; expanded criteria for screening harms.

Data Extraction and Synthesis   Two reviewers independently assessed study eligibility and quality; data extracted from fair- and good-quality studies.

Main Outcomes and Measures   Mortality, morbidity, progression to advanced cancer, interval cancers, screening harms.

Results   Seven randomized clinical trials and 13 nonrandomized studies were included; 2 nonrandomized studies reported mortality outcomes. A nonrandomized trial emulation study estimated no mortality difference for screening beyond age 74 years (adjusted hazard ratio, 1.00 [95% CI, 0.83 to 1.19]). Advanced cancer detection did not differ following annual or biennial screening intervals in a nonrandomized study. Three trials compared digital breast tomosynthesis (DBT) mammography screening with digital mammography alone. With DBT, more invasive cancers were detected at the first screening round than with digital mammography, but there were no statistically significant differences in interval cancers (pooled relative risk, 0.87 [95% CI, 0.64-1.17]; 3 studies [n = 130 196]; I 2  = 0%). Risk of advanced cancer (stage II or higher) at the subsequent screening round was not statistically significant for DBT vs digital mammography in the individual trials. Limited evidence from trials and nonrandomized studies suggested lower recall rates with DBT. An RCT randomizing individuals with dense breasts to invitations for supplemental screening with magnetic resonance imaging reported reduced interval cancer risk (relative risk, 0.47 [95% CI, 0.29-0.77]) and additional false-positive recalls and biopsy results with the intervention; no longer-term advanced breast cancer incidence or morbidity and mortality outcomes were available. One RCT and 1 nonrandomized study of supplemental ultrasound screening reported additional false-positives and no differences in interval cancers.

Conclusions and Relevance   Evidence comparing the effectiveness of different breast cancer screening strategies is inconclusive because key studies have not yet been completed and few studies have reported the stage shift or mortality outcomes necessary to assess relative benefits.

Breast cancer is the second leading cause of cancer mortality for US women, despite a steady overall decline in breast-cancer mortality rates over the past 20 years. 1 The average age-adjusted rate for the years 2016-2020 was 19.6 per 100 000, with an estimated 43 170 deaths in 2023. 1 , 2 The majority of cases occur between the ages of 55 and 74 years, 1 and incidence is highest among women ages 70 to 74 (468.2 per 100 000). 3 Non-Hispanic White women have the highest breast cancer incidence, 4 but mortality is 40% higher for non-Hispanic Black women (27.6 per 100 000) compared with White women (19.7 per 100 000); non-Hispanic Black women experience lower 5-year survival regardless of the cancer subtype or stage at the time of detection. 1 , 5 - 7

Previous reviews of breast cancer screening effectiveness established the benefits and harms of mammography based primarily on large, long-term trials. 8 , 9 In 2016, the US Preventive Services Task Force (USPSTF) recommended screening for breast cancer in women starting at age 50 years every 2 years continuing through age 74 years (B recommendation) and that screening from ages 40 to 49 years should be based on clinical discussions of patient preferences and individual breast cancer risk (C recommendation). 10 This comparative effectiveness systematic review of breast cancer screening strategies was conducted concurrently with a separate decision modeling study. 11 Both informed the USPSTF updated breast cancer screening recommendations. 12

This review addressed 3 key questions (KQs) on the comparative effectiveness and harms of different screening strategies ( Figure 1 ). Methodological details including study selection, a list of excluded studies, detailed study-level results for all outcomes and for specific subpopulations, and contextual observations are available in the full evidence report. 14

Studies included in the 2016 USPSTF reviews 8 , 9 , 15 , 16 were evaluated for inclusion with eligibility criteria for the current review. In addition, database searches for relevant studies published between January 2014 and August 22, 2022, were conducted in MEDLINE, the Cochrane Central Register of Controlled Clinical Trials, and the Cochrane Database of Systematic Reviews (eMethods in the Supplement ). Reference lists of other systematic reviews were searched to identify additional relevant studies. ClinicalTrials.gov was searched for relevant ongoing trials. Ongoing surveillance to identify newly published studies was conducted through March 2024 to identify major studies published in the interim. Two new nonrandomized studies were identified 17 , 18 and are not further discussed, as they would not change interpretation of the review findings or conclusions.

Two independent reviewers screened titles, abstracts, and relevant full-text articles to ensure consistency with a priori inclusion and exclusion criteria (eTable 1 in the Supplement ). We included English-language studies of asymptomatic screening populations not at high risk for breast cancer. The eligible population for this review is adult females (sex assigned at birth). For consistency with the underlying evidence, the term “women” is used throughout this report; however, cancer registries and studies of breast cancer generally infer gender based on physiology and medical history rather than measuring self-reported gender. Included studies compared mammography screening modalities (mammography with or without digital breast tomosynthesis [DBT]), different screening strategies with respect to interval, age to start, age to stop, or supplemental screening strategies using ultrasound or magnetic resonance imaging (MRI) with mammography.

For KQ1, randomized clinical trials (RCTs) or nonrandomized studies of interventions with contemporaneous comparison groups that reported breast cancer morbidity, mortality, all-cause mortality, or quality of life were included. For KQ2, the primary outcome of interest was progression to advanced breast cancer, defined for this review as stage IIB or higher, which encompasses tumors with local lymph node involvement or distant metastases. 19 Study-defined advanced breast cancer outcomes were used when this outcome was not reported (eg, stage II or higher). Invasive breast cancer detection outcomes from multiple screening rounds can indicate whether a screening modality or strategy reduces the risk of advanced cancer by detecting early cancers that would otherwise have progressed (stage shift), thereby potentially reducing breast cancer morbidity and mortality. 20 - 23

For KQ3, RCTs and nonrandomized studies of interventions reporting adverse events, including psychological harms, radiation exposure, and interval invasive cancers (incident or missed due to false-negative screening) were included, regardless of the number of screening rounds reported. False-positive recall, false-positive biopsy recommendation, and false-positive biopsy rates (individuals who underwent a biopsy for a benign lesion) were obtained from included RCTs and from nonrandomized studies reporting cumulative rates of these potential harms of screening.

Two reviewers evaluated all articles that met inclusion criteria using prespecified quality criteria (eTable 2 in the Supplement ). Discordant quality ratings were resolved through discussion and input from a third reviewer. Risk-of-bias assessment was conducted using the USPSTF-specific criteria for randomized trials 13 and an adapted tool from the Risk of Bias in Non-Randomized Studies of Interventions (ROBINS-I). 24 Studies determined to be at high risk of bias were excluded. One reviewer extracted key elements of included studies into standardized evidence tables in DistillerSR (Evidence Partners) and a second reviewer checked the data for accuracy. Limited evidence on sub-KQs is available in the full report. 14 When available, reported relative risks were provided in the tables, but we calculated and reported crude effect estimates and confidence intervals when studies did not provide them. For KQ2 intermediate detection outcomes, the definition of advanced cancer reported in the studies was used for synthesis; commonly this was stage II or later. Comparisons of prognostic characteristics or markers (eg, grade, tumor size, nodal involvement, receptor status) were included for comparisons as data allowed.

All quantitative analyses were conducted in Stata version 16 (StataCorp). The presence of statistical heterogeneity was assessed among pooled studies using the I 2 statistic. Where effects were sufficiently consistent and clinical and statistical heterogeneity low, random-effects meta-analyses were conducted using the restricted maximum likelihood; all tests were 2-sided, with P  < .05 indicating statistical significance.

Aggregate strength of evidence (ie, high, moderate, or low) was assessed for each KQ and comparison using the approach described in the Methods Guide for the Effectiveness and Comparative Effectiveness Reviews, 25 based on consistency, precision, publication bias, and study quality.

Investigators reviewed 10 378 unique citations and 419 full-text articles for all KQs ( Figure 2 ). Twenty studies reported in 45 publications were included. 26 - 45 A full list of included studies by KQ is located in eTable 3 in the Supplement .

Key Question 1. What is the comparative effectiveness of different mammography-based breast cancer screening strategies (eg, by modality, interval, initiation and stopping age, use of supplemental imaging, or personalization based on risk factors) on breast cancer morbidity and mortality?

Two nonrandomized studies reported on the association of different screening programs with breast cancer morbidity and mortality. One study was designed to compare different ages to stop screening 30 and another compared annual and triennial screening intervals. 41

A fair-quality observational study (n = 1 058 013) on age to stop screening used an emulated trial methodology to analyze a random sample of US Medicare A and B claims data for enrollees aged 70 to 84 years (1999 to 2008), eligible for breast cancer screening, and with at least a 10-year estimated life expectancy. The study estimated the effect of stopping screening at ages 70, 75, and 80 years compared with continued annual screening. 30 , 46 Continuation of screening between the ages of 70 and 74 years was associated with reduced mortality risk based on survival analysis (hazard ratio, 0.78 [95% CI, 0.63 to 0.95]), but the absolute difference in the risk of death for the age group was small and the confidence interval included null (1.0 fewer deaths per 1000 screened [95% CI, −2.3 to 0.1]). These results indicate a difference in the cumulative incidence curves that approached a difference in the mortality risk for the age group. Conversely, continued screening vs no screening from ages 75 to 84 years did not result in statistically significant differences in the absolute risk of breast cancer mortality (0.07 fewer deaths per 1000 [95% CI, –0.93 to 1.3]) or the cumulative mortality incidence (hazard ratio, 1.00 [95% CI, 0.83 to 1.19]).

A fair-quality nonrandomized clinical study (n = 14 765) conducted in Finland during the years 1985 to 1995 assigned participants aged 40 to 49 years to annual or triennial screening invitations by alternating birth year. 41 The study reported no difference in breast cancer mortality: 20.3 deaths per 100 000 person-years with annual screening invitations and 17.9 deaths per 100 000 person-years with triennial screening invitations (relative risk [RR], 1.14 [95% CI, 0.59-1.27]).

Key Question 2. What is the comparative effectiveness of different mammography-based breast cancer screening strategies (eg, by modality, interval, initiation and stopping age, use of supplemental imaging, or personalization based on risk factors) on the incidence of and progression to advanced breast cancer?

No eligible studies of age to start or stop screening, supplemental screening, or personalized screening were included, because no RCTs or nonrandomized studies reported more than a single round of screening comparing screening strategies. For screening interval, 1 RCT 26 and 1 nonrandomized study, 41 and for comparisons of different screening modalities (DBT vs digital mammography) 3 RCTs 27 , 33 , 42 and 2 nonrandomized studies, 34 , 44 met eligibility criteria.

Two fair-quality studies addressed the effect of screening interval on the characteristics of detected cancers. A fair-quality United Kingdom Co-ordinating Committee on Cancer Research (UKCCCR) RCT comparing screening intervals was conducted as part of the UK National Breast Screening Program. The study randomized participants aged 50 to 62 years to annual (n = 37 530) or triennial (n = 38 492) breast cancer screening during the years 1989 to 1996. 26 After 3 years of screening (1 incidence screen in the triennial screening group), a similar number of cancers (screen-detected and interval) had been diagnosed in the annual and triennial screening groups (6.26 and 5.40 per 1000 screened, respectively; RR, 1.16 [95% CI, 0.96 to 1.40]). No statistically significant differences were found in the cancer characteristics (tumor size, nodal status, histological grade) between groups over the course of the study.

A fair-quality nonrandomized study using Breast Cancer Surveillance Consortium (BCSC) registry data (1996 to 2012) 39 found the relative risk of being diagnosed with a breast cancer with less favorable prognostic characteristics (stage IIB or higher, tumor size >15 mm, or node-positive) was not statistically different for women screened biennially compared with those screened annually for any age category (40-49, 50-59, 60-69, 70-85 years).

Three fair-quality RCTs 27 , 33 , 42 reported cancer detection over 2 rounds of screening, comparing the effects of screening with DBT and digital mammography on the presence of advanced cancer at subsequent screening rounds ( Table 1 ). Participants were randomized to the DBT intervention group or the digital mammography control group at a first round of screening, followed in 2 trials by a second round of screening with digital mammography for all second-round participants (Proteus Donna, 27 RETomo 42 ) and in 1 trial with DBT for all second-round participants (To-Be 33 ). The trials used an identical screening modality for both study groups at the second round because using the same instrument is a stronger design for detection of stage shift.

The RCTs reported increased detection of invasive cancer with DBT at the first round of screening (pooled RR, 1.41 [95% CI, 1.20 to 1.64]; 3 RCTs [n = 129 492]; I 2  = 7.6%) and no statistical difference in invasive cancer at the subsequent screening (pooled RR, 0.87 [95% CI, 0.73 to 1.05]; 3 RCTs [n = 105 064]; I 2  = 0%) (eFigure 1 in the Supplement ). 27 , 33 , 42 There was no statistically significant difference in the incidence of advanced cancers at the subsequent screening round (progression of cancers not found at prior screening that would indicate stage shift) in the individual trials ( Figure 3 ). Results were inconsistent and thus not pooled for the advanced cancer, larger tumor (>20 mm), and node-positive cancer outcomes. The results for histologic grade 3 cancer at the second screening were consistent (pooled RR, 0.97 [95% CI, 0.61-1.55]; 3 RCTs [n = 105 244]; I 2  = 0%) ( Figure 3 ). Due to the small number of cases, it was not possible to assess differences in the detection of cancers lacking hormone or growth factor receptors (ie, triple-negative cancers) that have the worst prognosis among breast cancer subtypes.

Two fair-quality nonrandomized studies of interventions (NRSIs), including a US study using BCSC data, compared breast cancer detection outcomes from screening over multiple rounds (≥2) with either DBT-based mammography or digital mammography alone. 34 , 44 The findings were generally consistent with the trial results for cancer detection and stage shift.

Key Question 3. What are the comparative harms of different mammography-based breast cancer screening strategies (modality, interval, initiation age, use of supplemental imaging, or personalization based on risk factors)?

No eligible studies of age to start screening or personalized screening were identified. For age to stop screening, 1 fair-quality nonrandomized study met eligibility criteria. 30 For comparisons of potential harms associated with different screening intervals, a fair-quality RCT 26 and 2 fair-quality nonrandomized studies 39 , 41 were included. For comparisons of different screening modalities (DBT vs digital mammography), 4 RCTs (3 good- and 1 fair-quality) 27 , 31 , 33 , 42 and 7 fair-quality nonrandomized studies were included. 28 , 32 , 34 - 36 , 43 , 44

In the NRSI using an emulated trial methodology to evaluate the age to stop screening, 30 the 8-year cumulative proportion of participants with a breast cancer diagnosis was higher among those who continued annual screening from ages 70 to 84 years (5.5%) compared with those who discontinued screening (3.9%) at age 70 years. Because fewer cancers were diagnosed among those who discontinued screening, there was a lower risk of undergoing cancer treatment and experiencing related morbidity. Notably, for participants aged 75 to 84 years, screening (and treatment) were not associated with lower breast cancer mortality (see KQ1 results).

The UKCCCR trial included for KQ2 26 reported fewer interval cancers (false-negative and incident cancers) diagnosed in the annual invitation group compared with triennial screening (1.84 vs 2.70 per 1000 women screened, respectively; RR, 0.68 [95% CI, 0.50 to 0.92]). The nonrandomized clinical trial conducted in Finland included for KQ1 41 also reported interval cancers diagnosed with annual vs triennial screening and found no statistical difference in incidence ( P  = .22, data not reported). Data from 2 studies from the BCSC registry reported higher probabilities of false-positive recalls and biopsy recommendations with annual screening compared with biennial screening and no statistical difference in interval cancers in adjusted analyses. 32 , 39 , 44

Four RCTs (3 good-quality, 1 fair-quality) 27 , 31 , 33 , 42 and 7 fair-quality nonrandomized studies 28 , 32 , 34 - 36 , 43 , 44 reported outcomes related to potential screening harms associated with DBT-based screening compared with digital mammography–only screening, including interval cancer rates, round-specific and cumulative false-positive recalls and biopsies, and radiation exposure. Meta-analysis of 3 large trials did not show a statistically significant difference in rates of interval cancer after screening with DBT compared with digital mammography (pooled RR, 0.87 [95% CI, 0.64 to 1.17]; 3 RCTs [n = 130 196]; I 2  = 0%) (eFigure 2 in the Supplement ). 27 , 33 , 42

Data on interval cancers were also obtained from 7 nonrandomized studies. 28 , 32 , 34 - 36 , 43 , 44 The most recent BCSC analysis, reporting interval cancer rates across multiple screening rounds with either DBT or digital mammography, did not identify statistically significant differences in invasive or advanced interval cancers. 44

The effects of DBT screening on false-positive recall and false-positive biopsy rates varied across studies 27 , 33 , 42 and by screening round, with small or no statistical differences between study groups, not consistently favoring DBT-based mammography or digital mammography.

Evidence from 2 nonrandomized BCSC studies provided false-positive results across several screening rounds. 32 , 44 In 1 study, rates of false-positive recall and false-positive biopsy rates were lower with DBT in initial screening rounds, but differences were attenuated and not statistically significant compared with digital mammography only after additional rounds of screening ( Table 2 ). 44 The other study reported no statistical difference in 10-year cumulative false-positive biopsy recommendation rates between biennial DBT and digital mammography screening, but false-positive recall was slightly lower with DBT (eFigures 3 and 4 in the Supplement ); no differences by modality were identified for individuals with extremely dense breasts in stratified analyses (eFigure 5 in the Supplement ). 32

Four RCTs 27 , 31 , 33 , 42 and 1 NRSI 35 reported the mean, median, or relative radiation dose received in each study group at a single screening round. The 3 studies using DBT/digital mammography screening reported radiation exposure approximately 2 times higher in the intervention group compared with the digital mammography–only group. 27 , 35 , 42 Differences between study groups in radiation exposure were smaller in studies using DBT with synthetic digital mammography. 33 , 47

The Dense Tissue and Early Breast Neoplasm Screening (DENSE) trial, a good-quality RCT conducted in the Netherlands, randomized (1:4) participants aged 50 to 75 years with extremely dense breasts and negative mammography findings (2011-2015) (n = 40 373) to an invitation or no invitation for supplemental MRI screening. 45 (The RCT was not included for KQ2 because second round results in the control group were unavailable). Fifty-nine percent of those randomized to the invitation underwent an MRI examination (n = 4783). In intention-to-treat analysis, 2.2 per 1000 experienced interval breast cancer diagnoses in the supplemental screening invitation group, compared with 4.7 per 1000 screened in the digital mammography control group (RR, 0.47 [95% CI, 0.29 to 0.77]). Adverse events related to the supplemental MRI screening reported in the trial included 5 classified as serious adverse events (2 vasovagal reactions and 3 allergic reactions to the contrast agent) and 2 reports of extravasation (leaking) of the contrast agents and 1 shoulder subluxation. Twenty-seven participants (0.6% of the MRI group) reported a serious adverse event within 30 days of the MRI. Those who underwent supplemental MRI screening also experienced additional recalls (94.9 per 1000 screened), false-positive recalls (80.0 per 1000 screened), and false-positive biopsies (62.7 per 1000 screened).

A fair-quality nonrandomized study used claims data from commercially insured women (MarketScan database) aged 40 to 64 years who had received at least 1 bilateral screening breast MRI (n = 9208) or mammogram (n = 9208) between January 2017 and June 2018. 29 Following propensity score matching, those undergoing screening with MRI were more likely to have additional health care cascade events such as office visits and follow-up tests unrelated to breast conditions (adjusted difference between groups, 19.6 per 100 screened [95% CI, 8.6 to 30.7]) in the subsequent 6 months.

A fair-quality RCT, the Japan Strategic Anti-cancer Randomized Trial, randomly assigned asymptomatic women aged 40 to 49 years (2007-2011) to breast cancer screening with mammography plus handheld ultrasound (digital mammography/ultrasound) (n = 36 859) or mammography only (digital mammography) (n = 36 139). 40 The relative risk of invasive interval cancer was not statistically significantly different for digital mammography/ultrasound vs digital mammography only (RR, 0.58 [95% CI, 0.31 to 1.08]). This result differs from the statistically significant population-average effect reported in the study ( P  = .03), which included interval ductal carcinoma in situ (proportion difference, −0.05% [95% CI, −0.09 to 0]). Those undergoing ultrasound in addition to digital mammography experienced 48.0 per 1000 additional false-positive recall results compared with those assigned to digital mammography screening only.

A fair-quality nonrandomized study using data from 2 BCSC registry sites compared screening outcomes for participants receiving ultrasonography on the same day as a screening mammogram (digital mammography/ultrasound) (n = 3386, contributing 6081 screens) compared with those that received only a mammogram (digital mammography) (n = 15 176, contributing 30 062 screens). 37 However, 31% of participants had a first-degree family history of breast cancer or previous breast biopsy. There was no statistical difference in interval cancer risk (adjusted RR, 0.67 [95% CI, 0.33 to 1.37]), and rates of false-positive biopsy were twice as high for the mammography/ultrasound group (adjusted RR, 2.23 [95% CI, 1.03 to 2.58]).

Prior screening effectiveness reviews based on large trials initiated in previous decades established a statistically significant mortality benefit for mammography screening of women aged 50 to 69 years. 8 , 9 , 15 The current review considered comparative effectiveness questions on the relative benefits and harms of different screening start and stop ages, intervals, and modalities for women at average breast cancer risk. Findings are summarized in Table 3 .

The evidence was insufficient for addressing the age to start or end screening. No eligible studies comparing different ages to start screening were identified. Limited evidence from 1 nonrandomized study, using an emulated trial study design, suggested that screening beyond age 74 years may not reduce breast cancer mortality. 30

Evidence was also insufficient for evaluating the effect of screening intervals on breast cancer morbidity and mortality. Two nonrandomized studies found no difference in breast cancer outcomes. 26 , 39 Moderate evidence supported longer screening intervals (eg, biennial) to reduce the cumulative risk of false-positive recall and biopsy. The observational studies of different screening intervals compared individuals who self-selected or were referred for different screening intervals, contributing to risk of bias in the results.

Results from 3 RCTs 27 , 33 , 42 and 2 nonrandomized studies 34 , 44 provided moderate evidence that DBT-based mammography does not reduce the risk of invasive interval cancer or advanced cancer at subsequent screening rounds. Additional rounds of screening and longer follow-up are needed to fully evaluate whether DBT reduces breast cancer morbidity and mortality. Consistent with trial findings, a nonrandomized BCSC study did not find reduced risks of advanced or interval cancers with DBT. 44 Limited evidence from trials on harms of screening with DBT 27 , 33 , 42 indicated similar false-positive recall and biopsy rates. An observational BCSC study did not show differences in the 10-year cumulative false-positive biopsy rates 32 ; lower false-positive recall and biopsy with DBT screening were attenuated after several screening rounds. 44 Additional research is needed to ascertain whether DBT-based screening would reduce false-positives over a lifetime of screening.

The evidence was not adequate to evaluate the benefits and harms of supplemental MRI screening for people with dense breasts. No eligible studies were identified that provide evidence on breast cancer morbidity or mortality outcomes with supplemental MRI screening compared with mammography alone among individuals with dense breasts. The DENSE trial 45 reported fewer interval cancers with 1 round of supplemental MRI screening, but results from a second screening round are not yet published. Evidence of higher advanced cancer incidence in the mammography-only group relative to the MRI group would be needed to anticipate effects on morbidity or mortality. Supplemental MRI led to additional false-positive recalls and biopsies, and uncommon but serious adverse events were observed. 45 Two recent systematic reviews of the test performance literature reported higher cancer detection with supplemental MRI screening along with substantially increased recall and biopsy rates among individuals without cancer. 48 , 49

Lack of a standardized and reliable assessment tool for measuring breast density and density variation across the lifespan pose challenges for research into the optimal screening strategy for persons with dense breasts. 16 Research is also needed to evaluate personalized risk-based screening, based on breast cancer risk factors and personal screening preferences. The ongoing WISDOM trial and My Personalized Breast Screening study (expected completion in 2025) may help to address these research gaps. 50 , 51

Breast cancer is an active area of research, yet few longitudinal RCTs comparing different screening strategies have been conducted following completion of the major trials that established the effectiveness of mammography for reducing breast cancer mortality for women aged 50 to 69 years. This review included 6 new randomized trials, 27 , 31 , 33 , 40 , 42 , 45 4 comparing DBT with digital mammography screening 27 , 31 , 33 , 42 and 2 on supplemental screening compared with mammography alone. 40 , 45 Three of these trials are ongoing 31 , 40 , 45 and have reported preliminary results only. Observational studies were also included, but few studies were available that followed up a screening population over time to compare the health outcomes associated with different screening approaches. These studies, while potentially more representative of a screening population, have higher risk of biased results due to confounding and selection.

Changes in population health, imaging technologies, and available treatments may limit the applicability of previous studies. Recent trials included in this review were conducted outside of the US and enrolled mostly White European populations. No studies evaluated screening outcomes for racial or ethnic groups in the US that experience health inequities and higher rates of breast cancer mortality. Black women are at highest risk of breast cancer mortality, 52 with lower 5-year survival than all other race and ethnicity groups. 7 Breast cancer mortality risk also increases at younger ages for Black women compared with White women. 53 This review did not address additional factors beyond screening that contribute to breast cancer mortality inequities. 54 Rigorous research is essential to understand and identify improvements needed along the pathway from screening to treatment 55 and to address inequities in follow-up time after a positive screening result, time to diagnosis, 56 - 60 and receipt of high-quality treatment and support services. 59 , 61 , 62

Evidence comparing outcomes for different screening intervals and ages to start and stop screening was limited or absent. Trials of personalized screening based on risk and patient preferences are in progress and may address evidence gaps related to optimal screening start ages and intervals. Research is needed to better characterize potential harms of screening, including patient perspectives on experiencing false-positive screening results. Women with false-positive screening results may be less likely to return for their next scheduled mammogram, as reported in a large US health system study. 55 , 63 Rigorous studies that enroll screening populations and report advanced cancer detection, morbidity, and mortality outcomes from multiple rounds of screening are needed to overcome persistent limitations in the evidence on breast cancer screening. Multiple screening rounds are essential to determine whether a screening modality or strategy reduces the risk of advanced cancer by detecting early cancers that would otherwise have progressed (stage shift), potentially reducing breast cancer morbidity and mortality. 20 - 23 , 64

The potential benefits of risk-stratified screening strategies, including the use of supplemental screening with ultrasound or MRI, have not been fully evaluated, although some harms are evident. Longer term follow-up on existing comparative effectiveness trials, complete results from ongoing RCTs of personalized screening programs, 65 , 66 and rigorous new studies are needed to further strengthen the evidence and optimize breast cancer screening strategies.

Evidence comparing the effectiveness of different breast cancer screening strategies is inconclusive because key studies have not yet been completed and few studies have reported the stage shift or mortality outcomes necessary to assess relative benefits.

Accepted for Publication: November 23, 2023.

Published Online: April 30, 2024. doi:10.1001/jama.2023.25844

Corresponding Author: Jillian T. Henderson, PhD, MPH, Kaiser Permanente Evidence-based Practice Center, Center for Health Research, Kaiser Permanente Northwest, 3800 N Interstate Ave, Portland, OR 97227 ( [email protected] ).

Author Contributions: Dr Henderson had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: All authors.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: All authors.

Critical review of the manuscript for important intellectual content: Henderson, Weyrich, Miller.

Statistical analysis: Henderson.

Administrative, technical, or material support: Webber, Melnikow.

Supervision: Henderson.

Conflict of Interest Disclosures: None reported.

Funding/Support: This research was funded under contract number 75Q80120D00004, Task Order 75Q80121F32004, from the Agency for Healthcare Research and Quality (AHRQ), US Department of Health and Human Services.

Role of the Funder/Sponsor: Investigators worked with USPSTF members and AHRQ staff to develop the scope, analytic framework, and key questions for this review. AHRQ had no role in study selection, quality assessment, or synthesis. AHRQ staff provided project oversight, reviewed the report to ensure that the analysis met methodological standards, and distributed the draft for peer review. Otherwise, AHRQ had no role in the conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript findings.

Disclaimer: The opinions expressed in this document are those of the authors and do not reflect the official position of AHRQ or the US Department of Health and Human Services.

Additional Contributions: The authors gratefully acknowledge the following individuals for their contributions to this project: Howard Tracer, MD (AHRQ); Heidi D. Nelson, MD, MPH, MACP (Kaiser Permanente Bernard J. Tyson School of Medicine); current and former members of the USPSTF who contributed to topic deliberations; and Evidence-based Practice Center staff members Melinda Davies, MA, Jill Pope, and Leslie A. Purdue, MPH, for technical and editorial assistance at the Kaiser Permanente Center for Health Research. USPSTF members, peer reviewers, and federal partner reviewers did not receive financial compensation for their contributions.

Additional Information: A draft version of this evidence report underwent external peer review from 5 content and methods experts (Nehmat Houssami, MBBS, MPH, Med, PhD [University of Sydney-Australia]; Patricia Ganz, MD [UCLA]; Gerald Gartlehner, MD, MPH [Cochrane Austria]; Karla Kerlikowske, MD [UC San Francisco]; Lisa Newman, MD, MPH [New York Presbyterian/Weill Cornell Medical Center]) and 4 scientific representatives from 3 federal partner organizations (Centers for Disease Control and Prevention; Office of Research on Women’s Health; National Institute on Minority Health and Health Disparities). Comments were presented to the USPSTF during its deliberation of the evidence and were considered in preparing the final evidence review.

Editorial Disclaimer: This evidence report is presented as a document in support of the accompanying USPSTF Recommendation Statement. It did not undergo additional peer review after submission to JAMA .

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