ORIGINAL ARTICLE

Breast Cancer Screening

Recommendations Inclusive of All
Women at Average Risk: Update from
the ACR and Society of Breast Imaging
Debra L. Monticciolo, MD a , Sharp F. Malak, MD, MPH b, Sarah M. Friedewald, MD c,
Peter R. Eby, MD d, Mary S. Newell, MD e, Linda Moy, MD f, Stamatia Destounis, MD g,
Jessica W. T. Leung, MD h, R. Edward Hendrick, PhD i, Dana Smetherman, MD j

Abstract

Breast cancer remains the most common nonskin cancer, the second leading cause of cancer deaths, and the leading cause of
premature death in US women. Mammography screening has been proven effective in reducing breast cancer deaths in women age
40 years and older. A mortality reduction of 40% is possible with regular screening. Treatment advances cannot overcome the
disadvantage of being diagnosed with an advanced-stage tumor. The ACR and Society of Breast Imaging recommend annual
mammography screening beginning at age 40, which provides the greatest mortality reduction, diagnosis at earlier stage, better
surgical options, and more effective chemotherapy. Annual screening results in more screening-detected tumors, tumors of smaller
sizes, and fewer interval cancers than longer screening intervals. Screened women in their 40s are more likely to have early-stage
disease, negative lymph nodes, and smaller tumors than unscreened women. Delaying screening until age 45 or 50 will result in
an unnecessary loss of life to breast cancer and adversely affects minority women in particular. Screening should continue past age 74
years, without an upper age limit unless severe comorbidities limit life expectancy. Benefits of screening should be considered along
with the possibilities of recall for additional imaging and benign biopsy and the less tangible risks of anxiety and overdiagnosis.
Although recall and biopsy recommendations are higher with more frequent screening, so are life-years gained and breast cancer
deaths averted. Women who wish to maximize benefit will choose annual screening starting at age 40 years and will not stop
screening prematurely.
Key Words: Breast cancer, breast cancer screening, early detection, mammography, mammography screening

J Am Coll Radiol 2021;-:---. Copyright ª 2021 American College of Radiology

a i
Vice-chair for Research, Department of Radiology, and Section Chief, Department of Radiology, University of Colorado School of Medicine,
Breast Imaging, Texas A&M University Health Sciences, Baylor Scott & Aurora, Colorado.
j
White Healthcare—Central Texas, Temple, Texas. Department Chair and Associate Medical Director of the Medical Spe-
b
St. Bernards Healthcare, Jonesboro, Arkansas. cialties, Department of Radiology, Ochsner Medical Center, New Orleans,
c
Chief of Breast and Women’s Imaging; Vice Chair of Operations, Louisiana.
Department of Radiology; Medical Director, Lynn Sage Comprehensive Corresponding author and reprints: Debra L. Monticciolo, MD, Baylor
Breast Center, Northwestern Memorial Hospital, Northwestern University Scott & White Healthcare, Department of Radiology, 2401 South 31st
Feinberg School of Medicine, Chicago, Illinois. Street, MS-01-W256, Temple, TX 76508; e-mail: debra.monticciolo@
d
Chief of Breast Imaging, Radiology Representative to the Cancer Com- bswhealth.org.
mittee, Virginia Mason Medical Center, Seattle, Washington. Dr Friedewald reports Hologic consultant and Google research grant; Dr
e
Associate Division Director; Associate Director of Breast Center, Depart- Leung reports advisory board Subtle Medical; speaker at educational events
ment of Radiology and Imaging Sciences, Emory University, Atlanta, supported by Fujfilm, GE Healthcare, and Hologic; Dr Hendrick reports
Georgia. consultant, GE Healthcare; Dr Moy reports iCAD advisory board, insti-
f
Laura and Isaac Perlutter Cancer Center, NYU School of Medicine, New tutional grants Siemens, stock unit. The other authors state that they have
York City, New York. no conflict of interest related to the material discussed in this article. Dr
g
Chair of Clinical Research and Medical Outcomes Department, Elizabeth Monticciolo, Dr Malak, Dr Friedewald, Dr Eby, Dr Newell, Dr Moy, Dr
Wende Breast Care, Rochester, New York. Leung, and Dr Smetherman are nonpartner, non–partnership track em-
h
Deputy Chair of Department of Breast Imaging, The University of Texas ployees. Dr Hendrick is retired. Dr Destounis is Partner; Owner and
MD Anderson Cancer Center, Houston, Texas. Managing Partner at Elizabeth Wende Breast Care, Rochester, New York.

Copyright ª 2021 American College of Radiology

1546-1440/21/$36.00 n https://doi.org/10.1016/j.jacr.2021.04.021 1
 Visual Abstract

INTRODUCTION for diagnosis of tumors of smaller sizes with fewer nodal

Breast cancer remains the most common nonskin cancer, metastases and less histologic grade progression, making
the second leading cause of cancer death, and the leading treatment more effective [5-8]. The decline in advanced-
cause of premature death, measured by the average and total stage disease afforded by mammography screening is
years of life lost, for women in the United States [1]. Breast directly related to substantial declines in breast cancer
cancer currently accounts for 30% of all new invasive cancer mortality [5,9-12]. The ACR and SBI recommend annual
diagnoses in women. For 2021, 333,490 new invasive and mammography screening starting at age 40 to maximize
in situ cases and 44,130 breast cancer deaths are expected these benefits. Both benefits and risks of mammography
nationwide [2]. screening should be considered to assist women in making
Breast imaging experts from the ACR and Society of informed choices.
Breast Imaging (SBI) have reviewed extensive data from
randomized controlled trials (RCTs), observational trials,
and peer-reviewed literature on digital mammography, digital Benefits of Mammography Screening
breast tomosynthesis (DBT), ultrasound, and MRI. Our Mammography screening has been proven effective in
analysis incorporates the ACR Appropriateness Criteria, which reducing breast cancer death in women age 40 years and
use accepted robust strength-of-evidence methodology [3]. over [4,9,13-17].
Since our most recent guideline [4], new data are The 11 mammography RCTs have demonstrated a col-
available to evaluate the impact of screening using lective 22% reduction in breast cancer mortality [9,18], despite
advanced-stage and fatal breast cancers, to assess the utili- the limitations of RCT design. RCTs test only the invitation to
zation and benefits of DBT, and to evaluate disparities in screening, not actual screening. RCTs that achieved a 20% or
breast cancer screening and treatment among minority greater reduction in advanced-stage disease (a measure of trial
women. With this guideline, we offer recommendations efficacy) had average mortality reduction of 28% for invited
more inclusive of all women of average risk for breast cancer. women—corresponding to an approximately 40% mortality
reduction for women actually screened [9].
Numerous observational trials have demonstrated mor-
MAMMOGRAPHY SCREENING tality reductions of 40% or greater with organized screening
Mammography remains the principal modality of early [13,14,19-23]. The largest service screening trial to date
detection for women of average risk. Early detection allows screened 2.8 million women and achieved a 40%

2 Journal of the American College of Radiology

Volume - n Number - n Month 2021
mortality reduction in every province in Canada in every age
Table 1. Overdiagnosis rates as a function of age and
group, including those 40 to 49 years [14]. assuming an average lead time of 24 months
Cancer Intervention and Surveillance Modeling
Network (CISNET) models have been used to evaluate US Age (y) DCIS Invasive All Cancer
screening. The US Preventive Service Task Force has 40 0.5 0.3 0.3
commissioned CISNET to examine outcomes of particular
interest to them [24-26]. For example, 2016 CISNET 50 1.2 0.7 0.8
models considered screening only to age 74, even though 60 2.8 1.8 2.1
data exist beyond that age, so that recommendations by
70 8.4 6.0 6.5
organizations other than the US Preventive Service Task
Force could not be evaluated [26,27]. Regardless, 80 19.6 13.9 14.8
independent researchers studying CISNET models have
confirmed that annual screening starting at age 40 would Rates of overdiagnosis for all breast cancers are less than
1% for women under 60 years old. DCIS ¼ ductal carcinoma in situ.
result in a 40% reduction in breast cancer mortality
[24,27], consistent with observational studies worldwide.
There is risk in not screening. Treatment advances are after a screening examination for women of all ages ranged
important but cannot overcome the disadvantage of being from 9.6% to 11.6% [34-37]. Most abnormal screening
diagnosed with an advanced-stage tumor. Using the inci- examinations are resolved by imaging alone. Recommendations
dence rates of fatal breast cancers, Tabar et al have shown for biopsy, most performed with minimally invasive
that, with equivalent state-of-the-art treatment, screened percutaneous techniques, occur in fewer than 2% of screened
women had 60% lower breast cancer mortality at 10-year women [38].
follow-up and 47% lower mortality at 20-year follow-up A woman screened annually starting at age 40 could
than unscreened women over a 58-year study period [6]. expect recall for benign diagnostic workup once every 13
Using similar methodologies, Duffy et al found that years and to undergo a benign biopsy once every 187 years,
among 559,091 women who participated in screening, based on CISNET modeling [27]. Modeling the risks of
there was a statistically significant 41% reduction in breast screening based on different screening regimens
cancer deaths within 10 years of diagnosis and a 25% demonstrates more risks (primarily recalls) with annual
reduction in the rate of advanced cancers, compared with screening beginning at age 40 compared with other
unscreened women, independent of treatment regimen strategies, but often these risks are overstated [26,27].
[5]. Participation in screening saved lives that would Although recall and biopsy recommendations are higher
otherwise be lost with current therapies. with more frequent screening, so are life-years gained and
Mammography-detected tumors are more effectively deaths averted [27]. Comparing biopsy risk to benefit shows
treated [28-33]. Women in their 40s [29] and women 75 that a woman screened annually starting at age 40 could
and older [30] with mammographically detected cancers expect 1 life-year gained for every benign biopsy [27].
have lower-stage disease, less treatment, lower recurrence Efforts to reduce risks have been made through im-
rates, and better disease-specific survival. The method of provements in mammographic technology. Specifically,
detection is an independent prognostic factor for breast DBT decreases false-positive mammograms while simulta-
cancer mortality [28,31]. neously increasing cancer detection. In the largest study to
date, involving 454,850 patients, Friedewald et al showed
the recall rate decreased from 10.7% to 9.1% (relative
Risks of Mammography Screening decrease 15%) using DBT, with a concomitant increase in
The primary, quantifiable risks of screening mammography cancer detection rate (CDR) from 4.2 in 1,000 to 5.4 in
are recall for additional imaging and, after diagnostic eval- 1,000 (relative increase 29%) [39].
uation, recommendation for biopsy that yields benign These improvements are sustainable. The digital
results. Recall occurs when an abnormality identified at mammography recall rate decreased from 10.4% to 8.8%
screening requires further evaluation; if the ultimate result after the prevalent screen with DBT. After 5 years of DBT
is not malignant, this is referred to by some as a false- screening, the recall rate decreased to 6.1% while main-
positive mammogram. Lee et al reviewed 5,680,743 taining the improvement in CDR [40].
screening examinations in the National Mammography Anxiety has been given as a reason to delay the onset and
Database, the largest mammography registry in the United decrease the frequency of screening mammography [18,41].
States. On average, 9.6% of screened women had to return This fails to account for the highly variable experience of
for additional imaging [34]. In other studies, risk of recall anxiety among women who attend screening [42-45] and

Journal of the American College of Radiology 3

Monticciolo et al n Breast Cancer Screening Recommendations Update
also the added anxiety and regret women may endure when cancer in screened women and 47% of breast cancer
diagnosed with advanced breast cancer that might have been deaths in women 40 to 49 years old [33]. Modeling by
detected earlier with screening. Women have repeatedly Wu et al shows that biennial screening misses the
indicated their willingness to undergo diagnostic diagnosis of breast cancer in preclinical stages in nearly 2
mammograms and false-positive results in exchange for of 3 women [71].
increased likelihood of early detection [46,47]. Efforts to Annual mammography before a breast cancer diagnosis
diminish anxiety, such as individual and public education is predictive of increased overall survival; women who
of patients, rapid delivery of results, and other strategies, had missed any of the previous five annual mammograms
are encouraged [48-52]. had a 2.3-fold increase in all-cause mortality compared
Overdiagnosis occurs when a cancer is detected that with those who had missed none [76]. Although annual
would not have otherwise become clinically apparent in a surveillance is thought to be more important in younger
woman’s lifetime [53,54]. Overdiagnosis cannot be measured women, Sanderson et al used the National Cancer
directly. Unless specificity and sensitivity are 100%, the Institute’s Surveillance, Epidemiology, and End Results
results of any test will either overdiagnose or underdiagnose (SEER) data to show that women 69 to 84 years of
disease. A meta-analysis by the EUROSCREEN group age screened annually had lower 10-year breast cancer
showed overdiagnosis ranged from 0% to 10% (including mortality than women screened biennially or sporadically
ductal carcinoma in situ) among adequately adjusted studies regardless of race [77]. CISNET models confirm that
[55]. The higher end of the range occurs in older women, annual screening affords the best mortality reduction for
who are more likely to die of other causes than younger all age groups [24,27].
women. Current benchmarks produce less than 1% Screening should begin at age 40. Screened women in
overdiagnosis for women in their 40s and less than 2% for their 40s are more likely to have early-stage disease, negative
women in their 50s (Table 1) [54,56,57]. lymph nodes, and smaller tumors than unscreened women
Delaying screening until age 45 or 50, or lengthening [78,79]. A 10-year review showed statistically significant
screening interval, will not decrease the already low levels of improvement in 5-year disease-free survival (94% versus
overdiagnosis [58]. Overdiagnosed tumors persist on imaging 71%) and overall survival (97% versus 78%) for screened
just as lethal tumors do and will be diagnosed at the next versus unscreened women ages 40 to 49 years with breast
screening, which, if delayed, could result in later-stage diag- cancer, all of whom had similar treatments [79]. For a single
nosis [58]. Delay in discovery of lethal tumors would result in cohort who turned 40 years old in 2000, annual screening
underdiagnosis, with concomitant increases in anxiety, cost, from 40 to 84 years would avert 29,369 breast cancer
treatment, morbidity, and mortality [24,33,59]. deaths, 71% more deaths averted than biennial screening
Based on limited existing data, the international scien- limited to ages 50 to 74 [27].
tific consensus recognizes a linear relationship between ra- Recommendations to delay screening until age 50
diation dose and risk of radiation-induced solid organ adversely affect minority women as one-third of all breast
cancers, including breast cancer, for doses above 100 mGy cancers in Black, Asian, and Hispanic women are diagnosed
[60,61]. The mean glandular dose from a screening under age 50 [80]. The SEER program describes the
mammogram is approximately 3 mGy, or the equivalent different ethnic groups as non-Hispanic White (NHW),
of 6 weeks of natural background radiation [62]. Based on non-Hispanic Black (NHB), Hispanic, American Indian or
models that consider the unverified possibility (there are Alaska Native, and Asian or Pacific Islander. Analysis of
no documented cases) of radiation-induced breast cancer SEER 21 data by Hendrick et al [81] shows that, among all
at doses of 3 mGy [63-65], lives saved by screening women with breast cancer, minority women are 72% more
mammography far outweigh the theoretical possibility of likely to be diagnosed with invasive breast cancer under age
lives lost from radiation exposure by a ratio of 50 to 75:1 50 years and 58% more likely to be diagnosed with
[62,66,67]. advanced-stage disease under age 50 years than NHW
women. Among women dying of breast cancer, minority
women are 127% more likely to die under age 50 years than
Interval and Age NHW women (personal communication, R.E. Hendrick).
Annual screening is recommended. This results in more Comparison of younger (15-44 years) and older (45-64
screening-detected tumors, tumors of smaller size, and fewer years) women using SEER 18 data found a greater pro-
interval cancers than biennial screening, the latter a key portion of younger women were diagnosed at late stages
determinant of survival [33,68-75]. Webb et al found that compared with older women (48.1% versus 38.7%, P <
interval cancers presenting in the second year after a .0001) and a significant 54.5% of younger NHB women
negative mammogram caused 34% of deaths from breast and 52.9% of younger Hispanic women were diagnosed

4 Journal of the American College of Radiology

Volume - n Number - n Month 2021
with late-stage disease, compared with 46.0% for younger equitable treatment could reduce disparity in the breast
NHW women (P < .0001 for both) [82]. cancer mortality. Chen et al reported that screening
Screening should continue past age 74 without an mammography reduced the mortality disparity when Black
upper age limit, unless severe comorbidities limit life expec- and White women had equitable treatment of triple-
tancy or ability to accept treatment. One in five breast cancers negative breast cancer [96].
occurs in women 75 years or older [83]. Performance metrics Individuals who identify as lesbian, gay, bisexual,
among women ages 75 to 90 years are increasingly favorable transgender, or queer are less likely to present for cancer
with higher CDRs, sensitivity, and specificity and fewer false- screening than non–lesbian, gay, bisexual, transgender, or
positives compared with younger women [34]. Destounis queer persons [97]. Facilities must work to create a
et al found a substantial CDR of 8.4 in 1,000 in 18,497 respectful environment that welcomes all people [98]. For
women aged 75 or older, with most cancers invasive but average-risk transgender patients, recommendations
highly treatable [84]. CISNET confirms that screening depend on sex assigned at birth, use and duration of hor-
women after age 74 results in benefits in terms of breast mones, and surgical history and are based on limited data
cancer deaths averted and life-years gained with no upper and expert opinion. Annual screening at age 40 is recom-
age limit, although both metrics steadily decline with age mended for transfeminine (male-to-female) patients who
[85]. In addition, quality-adjust life-years remain positive for have used hormones for 5 years, as well as for trans-
screening up to age 90 [27,85]. masculine (female-to-male) patients who have not had
Mammography-detected invasive breast cancer in mastectomy [99].
women aged 75 and older is associated with significantly
better 5-year disease-specific survival (97% versus 87%, Risk Assessment
P < .001) [30]. Even with mild to moderate comorbidities, In 2018, the ACR issued new recommendations that all
the relative risk of death for mammography-detected tumors women be evaluated for breast cancer risk by age 30, so that
is 53% less for women aged 75 to 79 years and 48% less for those at higher risk can be identified and begin screening
women 80 years and older [83]. Using recent SEER data, before age 40 [100]. Similarly, the American College of
Hendrick et al showed that, among women over 40, Breast Surgeons advises all women over age 25 to undergo
women aged 70 to 79 years have had the steepest increase risk assessment. There are a variety of risk assessment
in distant-stage breast cancer rates and slowest mortality models available, and new methods, including deep-
declines [86], highlighting the need to continue screening learning-based systems, are being tested [100-102].
this cohort.

Diversity Other Modalities

In addition to being diagnosed at younger ages, NHB Evidence continues to accumulate confirming the ability of
women have 40% higher breast cancer mortality than supplemental screening technologies, including MRI, whole
NHW women [87]. Contributing factors include higher breast ultrasound, contrast-enhanced mammography, and
incidence of BRCA1 and BRCA2 mutations [88,89] and molecular breast imaging, to detect incremental cancers after
twice the incidence of aggressive, triple-negative breast negative mammographic screening [103,104]. Most studies
cancers in NHB women [90-92]. Systems-based factors involve women at elevated risk. Kuhl et al showed that
contribute to the mortality disparity and could be targeted screening MR found incremental cancers in women at
to eliminate much of the mortality difference [93,94]. For average risk (Interval Cancer Detection Rate [ICDR] ¼
example, Black and NHW women had equal breast cancer 15.5 per 1,000), 40% of which occurred in women with
mortality rates in the 1980s but rates declined only for ACR category A or B breast density [105]. However, at
NHW women after widespread utilization of screening this time, there is insufficient evidence to support
mammography in the 1990s [94]. Other minority groups supplemental screening in average-risk women.
face worse breast cancer outcomes as well. Examining the
SEER-17 database, Banegas et al found that breast-cancer- Other Considerations
specific mortality for Hispanic Black, Hispanic White and The ACR Appropriateness Criteria are evidence-based rec-
NHB women was 10% to 50% higher than for NHW ommendations using a process that entails extensive assess-
women [95]. ment of the literature and follows well-established
Although the disadvantages of younger age at diagnosis methodologies to rate the appropriateness of imaging for
and tumor biology cannot be eliminated, providing all specific clinical scenarios. The ACR Appropriateness
women earlier risk assessment, equal access to high-quality Criteria for breast cancer screening in average-risk women
screening mammography beginning at age 40, and assigned the highest rating (“usually appropriate”) to annual

Journal of the American College of Radiology 5

Monticciolo et al n Breast Cancer Screening Recommendations Update
screening mammography or DBT beginning at age 40 with to ensure that they are not in a higher-risk category, for
no upper age limit [106]. which supplemental screening might be considered [100].
The ACR Practice Parameters are expert-authored policy
statements regarding the safe and effective use of imaging. TAKE-HOME POINTS
The goal of the parameters is to narrow variability among
n Mammography screening has been proven effective in
radiology practices and provide guidance to optimize qual-
ity. The ACR Practice Parameter for the Performance of reducing breast cancer deaths in women age 40 years
Screening and Diagnostic Mammography recommends and older, with a mortality reduction of 40% possible
annual screening mammography beginning at age 40 for with regular screening.
average-risk women with no specific upper age for cessation n Annual mammography screening starting at age 40
of screening [107]. provides the greatest breast cancer mortality reduction
The National Comprehensive Cancer Network by enabling diagnosis at smaller sizes and earlier
(NCCN) is a not-for-profit organization of 30 leading stages, better surgical options, and more effective
cancer centers with multidisciplinary clinical experts [108]. chemotherapy.
The NCCN states that the primary goal of screening is n Delaying screening until age 45 or 50 results in un-
reduction of mortality and treatment-related morbidity necessary loss of life to breast cancer, adversely
and, therefore, recommends annual screening mammog- affecting minority women in particular.
raphy starting at age 40 [109]. Per the NCCN, upper age of
n Breast cancer screening in women ages 75 years and
screening should be based on assessment of comorbid
conditions that affect life expectancy and the individual’s older has continued benefits in terms of deaths averted
treatment desires. These recommendations are of Category and life-years gained.
1 Evidence and Consensus [110]. n Annual screening results in more screening-detected
NCCN recognizes that all major organizations are in tumors, tumors of smaller sizes, and fewer interval
agreement that maximum mortality reduction is achieved cancers than longer screening intervals.
when screening begins at age 40, but differences occur n There is risk in not screening; treatment advances are
because of “subjective value judgments between the benefits important but cannot overcome the disadvantage of
versus the risks.” The ACR, SBI, and NCCN believe that being diagnosed with an advanced-stage tumor.
each woman should have the opportunity to choose the
regimen with the highest associated benefit and that there
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