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AJR.17.18730

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Wo m e n ’s I m a g i n g • R ev i ew
Destounis and Santacroce
Age to Begin and Intervals for Cancer Screening
FOCUS ON:
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Women’s Imaging
Review
Stamatia Destounis1
Amanda Santacroce
Destounis S, Santacroce A
Age to Begin and Intervals for
Breast Cancer Screening: Balancing
Benefits and Harms
OBJECTIVE. Screening mammography has been widely used for breast cancer detection
and has been found to decrease mortality, but debate continues. The purpose of this article
is to review screening recommendations and the benefits and perceived harms of earlier and
more frequent screening.
CONCLUSION. Annual mammography beginning at age 40 decreases mortality. Clinicians should educate women and preserve recommendations for early and annual screening.
he number of breast cancer cases
was estimated to reach 252,710 in
2017 with an estimated 40,610
deaths, according to American
Cancer Society (ACS) surveillance research
[1]. Screening for breast cancer with mammography has been widely used and has been
found to decrease mortality in all age groups
[2]. For years, most medical associations recommended annual breast cancer screening
beginning at the age of 40 years. Major controversy began in 2009, when the U.S. Preventive Services Task Force (USPSTF) revised its recommendations. The previous
recommendation included screening mammography every 1–2 years for all women older than 40 years. This was changed to biennial
screening for women 50–74 years old with the
guidance that the decision to screen before
age 50 be an individual one [3]. The debate
over when to begin breast cancer screening
and its interval thereafter has continued.
The goals of this article are to review relevant literature on the benefits and harms
of screening mammography and to discuss
prominent medical organization guidelines
to assist the medical community in making
sound and educated breast cancer screening
recommendations to women. Discussion includes guidelines for patients, whether they
are at average risk of breast cancer (no risk
factors, that is, no personal history, no known
or suspected BRCA mutation, no radiotherapy to the chest, < 15% lifetime risk, and nondense breasts), intermediate risk (risk factors
present, such as personal history of breast
cancer, lobular neoplasia, atypical ductal hy-
T
Keywords: breast cancer, cancer detection,
­screening mammography
doi.org/10.2214/AJR.17.18730
Received July 6, 2017; accepted after revision
August 19, 2017.
S. Destounis has received a research grant from and is
on the board of Hologic, Inc.
1
Both authors: Elizabeth Wende Breast Care,
170 Sawgrass Dr, Rochester, NY 14620. Rochester, NY.
Address correspondence to S. Destounis
(sdestounis@ewbc.com).
AJR 2018; 210:1–6
0361–803X/18/2102–1
© American Roentgen Ray Society
perplasia, or 15–20% lifetime risk of breast
cancer), or high risk (BRCA mutation or
first-degree relative with known or suspected BRCA mutation, radiotherapy to the chest,
and > 20% lifetime risk).
Studies of Early Breast
Cancer Screening
An early study in Sweden [4] showed an
overall 30% mortality reduction after mass
screening of women 40–74 years old. A 1995
report of the Swedish trial [2] analyzed mortality reduction in various age groups and
showed a 34% mortality reduction among
women 50–74 years old and a 13% reduction among women 40–49 years old. These
study results suggested that the smaller reduction in mortality in the 40- to 49-year-old
group was due to rapid tumor progression in
these younger women and to the lower sensitivity of mammography in this age group
due to the increased prevalence of mammographically dense breast tissue. The authors
determined that an estimated 19% reduction in mortality would be observed if annual screening were conducted for in the 40to 49-year-old age group, because the study
group underwent screening at 24-month intervals. The most recent results [5] of this
longest running screening trial showed that
mortality rates remained stable over 3 decades of follow-up. The authors of the Swedish studies pointed out that these results were
achieved with single-view mammography
and with 24- to 33-month intervals between
screenings. They stated that their results
would have improved further had shorter
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Destounis and Santacroce
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intervals of annual screening and two-view
mammography been the standard of care, as
is the case in the United States.
Benefits of Early Screening
The benefit of screening of women in the
40- to 49-year age group cannot be ignored.
A mortality reduction benefit from screening has been found across multiple studies.
One such study was the Pan-Canadian Study
of Mammography Screening and Mortality
from Breast Cancer [6], in which data were
collected on screening participants and nonparticipants to judge the mortality benefit of
mammographic screening. The results of that
study, the results of which were published in
2014, showed a 40% mortality reduction benefit among the screening participants, a benefit that was also seen for the 40- to 49-year
age group. Overall, there was not a large difference in mortality reduction benefit among
the various age groups.
The USPSTF [3, 7] acknowledges that a
15% reduction in deaths accompanies regular screening of younger women but considers the reduction not pertinent enough to the
population at average risk of breast cancer
to justify exposure to the associated screening risks [3]. The mortality rate quoted by
the task force is a highly conservative number. According to Hendrick and Helvie [8], beginning screening of women in their 40s and
continuing annually beyond that would save
99,829 more lives than USPSTF recommendations of only biennial screening of women
50–74 years old. Hendrick and Helvie also
stated that with a current 65% rate of adherence to annual mammography, 64,889 more
lives would be saved. In addition to this and
the pan-Canadian study, the randomized controlled trials in Malmö [9] and Gothenburg
[10] in Sweden showed mortality reductions
of 45% (Malmö) and 36% (Gothenburg). In
the Swedish screening study [11], the mortality reduction was estimated the to be 26–29%.
In addition to the reduction in mortality,
when screening is begun at age 40, tumors
can be detected when they are smaller, have
less nodal metastasis, and are at an earlier
stage than when the tumor becomes palpable
[12]. This is important because the stage of a
tumor at diagnosis is still one of the most important factors in survival [13]. Along with
finding the tumor at an earlier stage, which
increases chances of survival, the patient is
less likely to need chemotherapy, radiation,
and other extreme treatments [14]. Newer
screening technologies, such as digital breast
2
tomosynthesis (DBT), have proven value in
breast cancer screening. Many studies have
proved the added benefit of screening with
DBT; use of the technology has been associated with an increase in breast cancer detection rates and a reduction in recall rates [15–
18]. These benefits have been seen in various
subgroups, including women with mammographically dense breasts and women 40–49
years old [19–21]. Because one of the cited
harms of screening mammography is falsepositive results leading to recall from screening, DBT is a welcome imaging modality for
use in screening.
The USPSTF indicates that mammography
should be used for women in their 40s who
have known high risk factors, such as a firstdegree relative with cancer or a BRCA1/2 gene
mutation [3]. Solely recommending screening
to such patients at high risk has revealed that
66% of malignancies could be missed [22].
Results of several studies on the topic [22–24]
agree that most women younger than 50 years
with cancers detected by screening would be
considered at average risk, and a risk-based
screening program would detrimentally leave
these women out. Our center’s experience
with women 40–49 years old with and without a family history of breast cancer showed
that 61% of the cancers diagnosed were in
women without a family history and 39%
in women with a family history. The study
showed no difference in the rates of invasive
versus noninvasive breast cancer, reemphasizing that all women in their 40s benefit from
screening regardless of risk factors [25]. Despite the discordant recommendations, many
women are still choosing to start screening at
an early age. Two studies following trends in
mammographic screenings resulting from the
changes in the USPSTF guidelines [26, 27]
showed that mammographic screening was
used for over one-half of women in the 40- to
49-year age bracket with a continual increase
over the years. As of 2012, screening initiation in this age group was at the highest point
seen in the years before and after the guideline change [27].
Despite the aforementioned changes in
guidelines of the USPSTF, most physicians
continue to recommend beginning screening at the age of 40 years [28–31], for reasons including many of the benefits already
discussed. In a national survey concerning
breast cancer screening recommendations
[29], responses were collected from 2000
primary care physicians, including internal
medicine physicians, family medicine and
general practice physicians, and gynecologists. In that study, known as the Breast Cancer Social Network Study, it was found that
81% of respondents continued to recommend
mammography to women 40–49 years old.
In another survey—the National Cancer Institute–funded Population-Based Research
Optimizing Screening through Personalized
Regimens program—the reasoning behind
practitioners’ recommendation of screening despite some of the published guidelines
(such as those of USPSTF) was assessed.
Physicians cited their own disagreement
with the guidelines, concerns expressed by
patients about the guidelines, the use of conflicting performance measurement metrics,
and concerns about liability [28]. In an online survey [32], the physicians surveyed reported their recommendations for screening
were influenced by institutional policy and
interest in earlier detection for their patients.
Debate Over Screening Interval
Another topic of debate among organizations is the interval at which to continue
breast screening. The argument for biennial screening versus annual screening is that
a woman has a decreased chance of experiencing the reported harms associated with
screening mammography. The Agency for
Healthcare Research and Quality found that
biennial versus annual screening can reduce
a woman’s chance of a false-positive result
by 19% and reduces the risk of unnecessary
biopsy by 1–4% [33] while maintaining up
to 81% of the benefits of annual screening,
according to a Cancer Intervention and Surveillance Modeling Network study conducted in 2009 [34]. The 19% decrease in benefits from annual screening predominantly
affects younger women attending screening, because disease in this cohort of women tends to be diagnosed as more aggressive,
fast-growing cancers with less favorable outcomes [35]. The mean lead time for women
younger than 50 years is less than 2 years
[36]. According to this lead time, if a biennial screening schedule is adopted, approximately two-thirds of these aggressive cancers would become clinically apparent
before the subsequent screening appointment
[37]. Larger tumors are more likely to be at
an advanced stage when detected, which requires more extensive treatment and has a
poorer prognosis [38]. Detection of smaller
tumors at an earlier stage, with less nodal involvement, is a key factor in the overall mortality outcome for the patient [22]. Biennial
AJR:210, February 2018
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Age to Begin and Intervals for Cancer Screening
screening could cost life years for women
with these more advanced tumors.
A retrospective study that included 1421
women with breast cancer diagnoses [38]
showed that an annual screening schedule
before breast cancer is diagnosed proved to
be a positive predictor of increased chance of
survival. The study showed that each missed
year of mammography was associated with a
decline in overall survival, that is, a 2.3-fold
increased chance of death compared with
findings in the study group who had undergone yearly mammography. A failure analysis performed at two major medical centers in
Boston showed that interval cancers detected
within a 2-year window from the last mammogram caused 34% of deaths in the study.
This percentage increased to 47% of deaths
of women in the age group 40–49 years. The
study authors concluded that these findings
support a recommendation for increased frequency of screening of younger women [35].
Harms of Screening
Though mammography has advanced in
many ways since its inception, it is not without its faults. Over the years, harms from
screening have been identified, such as falsepositive results, overdiagnosis, and accumulation of radiation dose. Many organizations
take these possible side effects into consideration but believe that yearly and early screening is still the best route to save lives and life
quality. Others, such as the USPSTF, believe
that the harms are too detrimental to a woman’s life to justify yearly screening as early
as age 40. In a response to the statement by
the USPSTF, Hendrick and Helvie [8] stated that for a woman in her 40s, the potential
harms of a screening examination consist of
the risk of recall for diagnostic workup every 12 years, negative biopsy results every
149 years, missed breast cancer every 1000
years, and a fatal radiation-induced breast
cancer every 76,000–97,000 years. Despite
these numbers and the evidence given to support them, the USPSTF claims that the riskto-benefit ratio of screening of women in
their 40s is not skewed enough in favor of the
benefits of yearly screening.
False-Positive Findings
One harm of mammography frequently cited is the psychologic stress and anxiety that
can come from a false-positive test result [3],
which is widespread among women who have
been recalled. Surveys of women’s moods
immediately after undergoing mammogra-
phy have shown that anxiety can be markedly higher in women who are notified they are
being asked to return for additional evaluation. This anxiety, however, was noted to be
short term, decreasing once the negative result was confirmed, and sharply decreasing
by the 6-month follow-up point [39]. Anxiety
has been found to resurface concerning future
appointments but has not been found to deter
women from attending their routine screening
mammography appointments [40]. Instead,
these women felt more convinced to continue regular screenings because of a heightened
awareness of breast cancer [41]. Though receiving a false-positive result is an anxietyproducing event, women seem to find it an
acceptable event for saving lives. According
to a telephone survey of 500 U.S. adults, 98%
of respondents who had received a false-positive result were still glad they had the initial
testing done, though many reported the situation to be “very scary” or “the scariest time of
their life” at the time [42]. The anxiety associated with false-positive results could be mitigated preemptively by honest conversations
between physicians and their patients.
It is true that a false-positive result is not
an entirely uncommon occurrence. Among
1000 women who undergo screening, a mean
of 100 women will be recalled for further
imaging. Of this 100, approximately 60 will
undergo additional imaging and have negative findings. Of the 100 patients recalled,
15 undergo needle biopsy, and two to five
of the 100 recalled have a confirmed cancer diagnosis [43]. Over the course of 10
years, among all women who undergo annual mammographic examinations, there is
a 57% chance of being called back for additional imaging or testing. Specifically, for
women in their 40s, this chance does increase slightly: the mean chance of a falsepositive result occurring over the course of
10 years for any woman 40–49 years old is
62.1%, which extends to 64.7% among black
women and 56.1% among Asian women [44].
This is not an unexpected phenomenon, because younger premenopausal women tend
to have denser breast tissue [45], and women
with dense breast tissue are almost 2 times
as likely as those without dense tissue to be
called back for further evaluation [46]. In addition to those with dense breast tissue, women who are just beginning to attend screening
do not have a baseline of images for the reading radiologist to use for comparison. Once
previous images are available for comparison, the recall rate decreases as much as 33%
[47]. Because many women start attending
screening in their 40s, this would be a cause
of higher recall rates in this age group.
Overdiagnosis
An additional harm stated by the USPSTF
is the finding and treatment of cancers that
would never become medically relevant to
a patient without screening. This is known
as overdiagnosis and can lead to unnecessary treatment, stress, and anxiety. Studies
have been performed to estimate the occurrence of overdiagnosis, but it is difficult to
standardize such a measurement and to accurately portray the results. Estimates of the
occurrence of overdiagnosis range from 0%
to over 30% [48]. The significant difference
in statistics could show bias in addition to
methodologic differences [49]. Because the
purpose of population-based screening is to
find breast cancer in the earliest, most treatable stages, it is not surprising that some of
the cancers found would not have been a concern for the woman in her lifetime. At this
point, science is unable to differentiate lesions found as ones that would remain indolent and ones that may progress to cause the
patient life-threatening harm.
Because of methodologic heterogeneity in
studies, the possible biases that exist within
each study, and inability to reach consensus
on how to calculate the rate of overdiagnosis, a true estimate cannot be made [50]. This
point should be communicated to patients in
counseling about when to begin breast cancer screening, so that they can understand
what overdiagnosis is and how it may affect
them. It is difficult to know how individual
women would react to the effects of overdiagnosis and the anxiety that could accompany it, because feelings about this topic are
difficult to gauge, and attempts at reporting
vary widely [51].
Multiple studies have been conducted
to monitor public opinion about overdiagnosis. These studies have shown the range
with which women respond to the information concerning this risk [51–53]. Many are
unaware of what overdiagnosis is and have a
challenging time grasping the concept. Once
the concept was understood, many women
thought it would not have an impact on future screenings, though this response varied
with the number quoted as the rate of overdiagnosis [51]. When given a range of 1–10%,
women quickly dismissed the statistic. When
the rate was quoted at 50%, however, more
women paused to consider how this would
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affect their future screening practices [51].
To assist patients in making informed decisions, careful conversations regarding this
risk must take place.
Radiation Dose
A deterrent of mammography for many
woman and referring physicians is the radiation received from yearly mammography. Radiation received from an x-ray is measured in
average glandular dose (AGD) in milligray.
The American College of Radiology (ACR)
sets a limit of 3.0 mGy per breast view. In one
single-center study [54], it was found that the
total AGD for 2D mammography was 3.77
mGy; for 2D mammography with DBT, 7.97
mGy; and for DBT with synthesized 2D images, 4.88 mGy. Though these values are below the set limits, it is apparent how quickly the radiation dose can add up because of
the possibilities of additional breast imaging
needed and of unforeseen other radiographic
procedures in the patient’s life.
Current Recommendations in the
United States
The benefits and harms of mammography
have factored heavily into recommendations issued by medical organizations. Currently in the United States, screening guidelines, the age to initiate screening, and the
interval at which to screen vary depending
on the organization.
American College of Radiology
The ACR recently published breast cancer screening guidelines for women at average risk [55]. Based on literature review
and resultant data from clinical trials, the
screening recommendation for those at average risk is to begin screening at age 40 and
to continue screening annually. The goal is
to continue to maximize the benefits of annual screening, such as reduced mortality
rate, and to provide more choices for breast
cancer treatments that are associated with
annual screening and early diagnosis. The
ACR decision to continue to advise women to begin screening at age 40 lies with the
increased cancer occurrence among women 40–44 years old compared with women
35–39 years old. Annual screening thereafter
continues to be recommended to minimize
deaths, increase life years gained, and to increase treatment options for those with a diagnosis of breast cancer.
In 2016, the ACR published appropriateness criteria [56] outlining mammogra-
4
phy guidelines and supplemental screening
guidelines for women at average risk and
those at high risk. The authors (a multidisciplinary expert panel) used current literature
and a modified Delphi consensus system to
rate breast imaging procedures. A rating of
1, 2, or 3 is defined as usually not appropriate; 4, 5, or 6 as may be appropriate; and 7,
8, or 9 as usually appropriate. The resultant
guidelines are reviewed and updated every 2
years. The 2016 guidelines for women at average risk specify annual mammography beginning at age 40. For the population at high
risk, the ACR recommends yearly mammographic examinations beginning as early as
age 25 and supplemental testing, including
MRI or screening ultrasound, for patients
with a contraindication to MRI. The ACR
states that screening ultrasound is an acceptable choice for those at intermediate risk and
those with dense breasts. It points out, however, the high false-positive rates associated
with ultrasound screening and notes that this
should be discussed and considered by patients and referring physicians.
American College of Obstetricians
and Gynecologists
The American College of Obstetricians and
Gynecologics (ACOG) in 2017 updated its
breast cancer screening clinical management
guideline practice bulletin for obstetricians
and gynecologists regarding women at average risk [57]. These guidelines changed slightly from those published in 2014, which had remained unchanged since 2011. The 2011 and
2014 bulletins stated that breast cancer screening includes three methods: annual mammography beginning at age 40; clinical breast examination annually for women age 40 and
older (every 1–3 years for women ages 20–39);
and breast self-awareness for all, which can include patient breast self-examination [58]. The
objective of the 2017 bulletin is to provide a
source of information for practices, evidence
supporting the guidelines, and information on
the controversies regarding screening based
on levels of recommendations.
A level A ACOG recommendation is
based on good and consistent scientific evidence; level B, limited or inconsistent scientific evidence; and level C, consensus and expert opinion. The guidelines emphasize that a
shared decision-making conversation should
occur between clinicians and their patients.
The conversation should include all screening
options and a discussion of the benefits and
harms associated with the decision to screen
versus not to screen. The ACOG 2017 guidelines are clinical breast examination offered
every 1–3 years for women ages 25–39 and
annually for women older than 40 (level C);
offer to start mammographic screening at age
40 or between ages 40 and 49 after the shared
decision-making discussion; and mammography at age 50 if not already initiated (level A).
The screening frequency recommendation is
for either annual or biennial imaging with the
shared discussion of benefits (reduced mortality with annual screening) and harms (recalls
and overdiagnosis) (level A).
Breast self-examination is no longer recommended for women at average risk because of the harms of false-positive findings
and lack of evidence of benefit (level B). The
guidelines state, however, that breast awareness should be discussed and encouraged
[57]. For women considered to be at high risk
and those who have positive results of tests
for the BRCA genes, the recommendations
are for what ACOG refers to as enhanced
screening [58], which includes clinical breast
examination every 6 months, annual mammography, and breast MRI.
American Cancer Society
After 18 years of recommending yearly
or biennial mammography starting at age
40, in the fall of 2015 the ACS changed its
guidelines regarding breast cancer screening
for women at average risk [59, 60]. The 2015
changes added an assessment of the recommendations, which were labeled as strong or
qualified on the basis of the Grading of Recommendations Assessment, Development,
and Evaluation (GRADE) approach [61]. In
the GRADE approach, evidence-based information is converted into a recommendation.
The strength of the recommendation reflects
that the expected or desirable effects will
outweigh the undesirable effects, or as it relates to the subject matter in this article that
the benefits will outweigh the harms. The updated recommendation was to begin regular
screening at age 45 and was categorized as a
strong recommendation. A recommendation
for annual screening of women 45–54 years
old was considered a qualified recommendation, as was biennial screening of women age
55 and older with the opportunity to continue
annual screening. For women 40–44 years
old, the opportunity should be provided to
begin annual screening (qualified recommendation). Women should continue screening for as long as they are in good overall
health and have a life expectancy of 10 years
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Age to Begin and Intervals for Cancer Screening
or more (qualified recommendation). The
ACS does not recommend clinical breast examination of women at average risk at any
age (qualified recommendation).
The ACS guidelines were the result of an
interdisciplinary working group that voted
on each recommendation and strength, giving an assessment of strong or qualified. A
strong recommendation meant that the benefits of screening outweigh the harms. A qualified recommendation meant that there is clear
evidence of the benefits of screening but less
regarding the balance between benefits and
harms or about patient values and preferences.
Annual mammography and MRI beginning at age 30 are recommended for women at high risk. The ACS high-risk designation [62] includes women who have a lifetime
breast cancer risk of 20–25% or more (risk
assessment based on family history); women
with BRCA1/BRCA2 mutations; women with
a first-degree relative with BRCA1/BRCA2
mutation (untested themselves); women who
have undergone radiation therapy to the chest
between the ages of 10 and 30; and women
with Li-Fraumeni, Cowden, or Bannayan-Riley-Ruvalcaba syndrome or a first-degree relative with one of these syndromes.
The review and recommendations of the
USPSTF are based on the claims that the
benefits of screening were at least moderate
for women ages 50–74 years old; show the
greatest benefits for women 60–69 years old;
and are small for women 40–49 years old,
which led to the controversial recommendation against screening of women in their 40s
at average risk.
U.S. Preventive Services Task Force
In 2009, the USPSTF [7] published an evidence-based review on the effectiveness and
harms of breast cancer screening modalities and on new breast cancer screening recommendations. The task force included the
three following recommendations, which
remain in place. Routine mammography
should not be performed for women 40–49
years old, and biennial mammography for
women younger than 50 years should be an
individualized decision (grade C recommendation, against routinely providing the service, there being moderate or high certainty
that the net benefit is small). Biennial mammography should be performed for women
beginning at age 50 (B recommendation, service is recommended; there is high or moderate certainty that the net benefit is moderate
to substantial). Teaching breast self-examination is not recommended (D recommendation, against the service; there is moderate
or high certainty that the service has no net
benefit or that harms outweigh the benefits),
and there is inadequate evidence that clinical
breast examination provides any additional benefit over mammography (I statement,
current evidence is insufficient to assess the
balance of benefits and harms of the service).
Acknowledgment
We thank Andrea Arieno for assistance
with the preparation of this manuscript.
Conclusion
The controversy surrounding screening
guidelines is ongoing and continues to cause
confusion for both patients and physicians trying to choose a screening schedule to follow. It
is important that women be informed and understand both the benefits and reputed harms
of screening. However, accurate portrayal of
false-positive rates and the prevalence of overdiagnosis will show that the benefits outweigh
these theoretic harms. Screening mammography depicts cancer early, when treatment is
more effective. Numerous studies have shown
that screening mammography works. Compared with all other screening regimens, annual mammographic screening beginning at
age 40 has the largest mortality reduction benefit in terms of life years gained.
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