Context Breast augmentation is not associated with an increased risk of breast
cancer; however, implants may interfere with the detection of breast cancer
thereby delaying cancer diagnosis in women with augmentation.
Objective To determine whether mammography accuracy and tumor characteristics
are different for women with and without augmentation.
Design, Setting, and Participants A prospective cohort of 137 women with augmentation and 685 women without
augmentation diagnosed with breast cancer between January 1, 1995, and October
15, 2002, matched (1:5) by age, race/ethnicity, previous mammography screening,
and mammography registry, and 10 533 women with augmentation and 974 915
women without augmentation and without breast cancer among 7 mammography registries
in Denver, Colo; Lebanon, NH; Albuquerque, NM; Chapel Hill, NC; San Francisco,
Calif; Seattle, Wash; and Burlington, Vt.
Main Outcome Measures Comparison between women with and without augmentation of mammography
performance measures and cancer characteristics, including invasive carcinoma
or ductal carcinoma in situ, tumor stage, nodal status, size, grade, and estrogen-receptor
status.
Results Among asymptomatic women, the sensitivity of screening mammography based
on the final assessment was lower in women with breast augmentation vs women
without (45.0% [95% confidence interval {CI}, 29.3%-61.5%] vs 66.8% [95% CI,
60.4%-72.8%]; P = .008), and specificity was slightly
higher in women with augmentation (97.7% [95% CI, 97.4%-98.0%] vs 96.7% [95%
CI, 96.6%-96.7%]; P<.001). Among symptomatic women,
both sensitivity and specificity were lower for women with augmentation compared
with women without but these differences were not significant. Tumors were
of similar stage, size, estrogen-receptor status, and nodal status but tended
to be lower grade (P = .052) for women with breast
augmentation vs without.
Conclusions Breast augmentation decreases the sensitivity of screening mammography
among asymptomatic women but does not increase the false-positive rate. Despite
the lower accuracy of mammography in women with augmentation, the prognostic
characteristics of tumors are not influenced by augmentation.
Breast augmentation is the third most common type of plastic surgery
performed for cosmetic reasons in the United States, with 268 888 procedures
in 2002.1 In 2 studies conducted in the late
1980s, between 3.3 and 8.1 per 1000 women reported ever having breast implants.2,3 Although breast implants have not been
found to be associated with an increased risk of breast cancer,4,5 implants
may interfere with routine mammography evaluation; therefore, women with breast
augmentation may be more likely to be diagnosed with advanced disease.6-16 Previous
studies of breast cancer following breast augmentation have typically had
small study samples and yield conflicting results as to whether breast implants
delay cancer diagnosis.4,7,8,16-25 In
addition, these studies include cancers diagnosed in the early 1980s when
routine screening mammography was uncommon26 and
radiologists did not use implantation displacement views, a technique that
improves visualization of breast tissue in women with implants.12
Two recent larger studies of breast cancer following augmentation mammoplasty
suggest breast cancer diagnosis may be delayed in women with augmentation.4,7 Brinton et al4 found
women with breast implants (N = 78) tended to have later-stage disease compared
with women without augmentation (35% vs 17% with regional or distant disease);
however, this difference was not statistically significant. Skinner et al7 found that mammography was less sensitive for women
with augmentation (N = 99) compared with women without augmentation (66.3%
vs 94.6%) and that women with augmentation were more likely to be diagnosed
with palpable tumors (83% vs 59%), invasive carcinoma (82% vs 72%), and to
have nodal involvement (48% vs 36%). Although both studies were relatively
large compared with earlier studies, they also included breast cancers diagnosed
in the early 1980s.
This study used recent prospective data from 7 US mammography registries
that participate in the Breast Cancer Surveillance Consortium (BCSC)27 to examine the effect of breast augmentation on mammography
accuracy and cancer characteristics. Because the majority of women in the
BCSC have undergone routine screening mammography during a time when displacement
views are standard of care for women with augmentation, this large cohort
can better answer the question of whether breast implants interfere with mammography
and thereby delay cancer detection among women with augmentation.
Women were selected from 7 mammography registries that form the National
Cancer Institute–funded BCSC, which can be found at http://breastscreening.cancer.gov.27 The 7 registries were Carolina Mammography
Registry (CMR), Chapel Hill, NC; Colorado Mammography Project (CMAP), Denver;
Group Health Cooperative (GHC), Seattle, Wash; New Hampshire Mammography Network
(NHMN), Lebanon; New Mexico Mammography Project (NMMP), Albuquerque; San Francisco
Mammography Registry (SFMR), San Francisco, Calif; and Vermont Breast Cancer
Surveillance System (VBCSS), Burlington. These population-based mammography
registries include screening and diagnostic mammography examinations performed
in defined catchment areas. To determine cancer status and tumor characteristics,
each mammography registry links to a state cancer registry (CMAP, CMR, NHMN,
VBCSS) or regional Surveillance, Epidemiology, and End Results program (GHC,
NMMP, SFMR). Some registries additionally link to pathology databases (CMR,
GHC, NHMN, NMMP, VBCSS). Cancer ascertainment from these combined sources
is estimated to be more than 94.3% complete.28 Each
registry has approval from its institutional review board to collect these
data for analysis.
Women were included in analyses if they had a mammography examination
between January 1, 1995, and October 15, 2002, and were consistent about reporting
the presence or absence of breast augmentation. We excluded women with a personal
history of breast cancer (self-report or prior diagnosis in the cancer registry
or pathology database); self-report of prior mastectomy or breast reconstruction,
or augmentation for only 1 breast (total of 5%); or women with an inconsistent
reporting of breast augmentation once augmentation was first reported (eg,
augmentation reported at 1 examination and no augmentation reported at a future
examination, <1%). The most recent mammography examination in the study
period was designated the index examination.
Because women with breast augmentation were younger, more likely to
be white and non-Hispanic, and more likely to have had a mammogram before
the index examination, which may influence the sensitivity of mammography,
and we had a limited number of women with augmentation and breast cancer,
we matched each woman with augmentation and breast cancer to 5 women without
augmentation but with breast cancer by age (plus or minus 3 years), race/ethnicity
(white non-Hispanic, black non-Hispanic, Hispanic, Asian, other), whether
or not their index examination was within 2 years of diagnosis, whether the
index examination was a first or subsequent mammogram, and mammography registry.
Women with augmentation were also more likely to have dense breasts, have
a family history of breast cancer, and be premenopausal or taking hormone
therapy; however, we did not match by these variables as they were missing
for 13% to 24% of women. Instead, we did a sensitivity analysis by adjusting
for these variables to see if the results changed.
The sensitivity and specificity of mammography were based on a 1-year
follow-up. For calculation of sensitivity and specificity, we excluded mammograms
occurring after December 31, 2000, to allow sufficient time to detect cancers
in the year following a mammogram. To calculate sensitivity, we also excluded
mammograms occurring more than 1 year before cancer diagnosis.
Demographic information and a self-reported breast health history were
obtained at the time of each mammography examination that included birth date,
race, ethnicity, current symptoms, breast augmentation status, history of
mastectomy or breast reconstruction, family history of breast cancer, menopausal
status, current postmenopausal hormone therapy use, and time since last mammography
examination. Women were considered to have breast augmentation if augmentation
was either self-reported on the questionnaire or indicated on the radiologist's
report. Women who reported a breast lump or nipple discharge were considered
to be symptomatic. Women were considered to have a family history of breast
cancer if they reported having at least 1 female first-degree relative (mother,
sister, or daughter) with breast cancer. Women aged 55 years or older were
assumed to be perimenopausal/postmenopausal and those younger than 40 years
were assumed to be premenopausal. Women aged 40 to 54 years were considered
to be perimenopausal/postmenopausal if both ovaries had been removed, menstruation
had stopped permanently, or they were taking hormone therapy.
Mammograms performed for routine screening in women with augmentation
were often indicated to be diagnostic examinations by radiologists because
implantation displacement views must be read in addition to standard compression
views; therefore, the radiologists' indication for examination cannot reliably
identify screening examinations in women with augmentation. To allow a similar
definition of screening mammography for women with or without augmentation,
we defined mammography examinations of asymptomatic women occurring more than
9 months after any prior mammogram as screening examinations.
Mammographic assessments were based on the American College of Radiology
Breast Imaging Reporting and Data System (BI-RADS) coding scheme.29 A mammogram was considered positive if it was given a final BI-RADS assessment code of 4 (suspicious abnormality),
5 (highly suggestive of malignancy), or 0 (need additional imaging evaluation)
at the end of the screening work-up. A mammogram was considered negative if it was given a 1 (negative), 2 (benign finding), or 3 (probably
benign finding) with a recommendation for short interval or routine follow-up.
The BI-RADS assessments of 3 (probably benign finding) with a recommendation
for immediate follow-up were recoded to a BI-RADS of 0. If a mammogram had
an initial BI-RADS assessment of 0 and a nonzero assessment within 90 days,
we used the first nonzero assessment as the final assessment.
Time since prior mammography was determined by using dates of prior
mammography examinations recorded in each mammography registry and self-reported
information. Mammograms were considered first examinations if the woman self-reported no history of prior mammography and there
was no evidence of prior mammography in any mammography registry, or the time
since prior mammography was 5 years or longer. Mammograms were considered
to be subsequent examinations if time since prior
mammography was less than 5 years.
Women were considered to have mammographically dense breasts when extremely
dense or heterogeneously dense was reported according to BI-RADS density categories29 or when classified as dense according to a 2-category
system of dense and nondense. Women with nondense breasts were those that
had BI-RADS categories of entirely fatty or scattered fibroglandular densities
reported or were indicated to have nondense breasts when a 2-category system
was used.
Breast cancer was defined as either invasive
carcinoma or ductal carcinoma in situ according to a cancer registry or pathology
database. All breast cancers were classified according to the American Joint
Committee on Cancer Staging system.30 Invasive
cancers were categorized by nodal status, tumor size, grade, and estrogen-receptor
status. Tumor characteristics were slightly less likely to be missing for
women with augmentation but in general the amount of missing data was similar
among women with or without augmentation: 8% and 10% for stage, 2% and 4%
for nodal status, 8% and 12% for tumor size, 16% and 18% for tumor grade,
and 32% and 35% for estrogen-receptor status.
Sensitivity and Specificity. A 1-year follow-up
period is the standard for calculating the accuracy of mammography.29,31 We define the sensitivity of mammography as the proportion of positive mammograms
among women diagnosed with breast cancer within 1-year of their examination. Specificity was defined as the proportion of negative mammograms
among women without cancer. Sensitivity and specificity were calculated separately
for screening mammograms and mammograms among symptomatic women.
Exact binomial 95% confidence intervals (CIs) were calculated for estimated
sensitivity and specificity and χ2 tests were used to compare
these estimates for women with and without augmentation. Logistic regression
was used to adjust sensitivity and specificity for age, breast density, whether
the index examination was a first or subsequent mammogram, and mammography
registry. Because specificity was calculated from the entire cohort of women
without cancer, the larger sample size allowed specificity to be additionally
adjusted for race/ethnicity, family history, menopausal status, and hormone
therapy use.
Tumor Characteristics. For women diagnosed
with breast cancer, the distributions of cancer characteristics were estimated
and compared for women with and without augmentation by using χ2 tests for categorical outcomes (stage, nodal status, grade, estrogen-receptor
status) and the Wilcoxon rank sum test for tumor size. We fit logistic regression
models adjusting for age, first vs subsequent mammography, and mammography
registry to compare cancer characteristics among women with and without breast
augmentation. We did not adjust for race/ethnicity because the numbers of
nonwhite women were too small to allow stable parameter estimation.
Analyses were performed by using SAS version 8.02 (SAS Institute, Cary,
NC) and P<.05 was considered statistically significant.
There were 141 women with augmentation and 20 738 women without
augmentation diagnosed with breast cancer between January 1, 1995, and October
15, 2002, and 10 849 women with augmentation and 1 016 684
women without augmentation and without breast cancer. The prevalence of augmentation
in this screening population of women without a history of breast cancer was
11 per 1000 women. Women with augmentation were younger with denser breasts,
more likely to be white and non-Hispanic, more likely to have had a prior
mammogram, and more likely to use hormone therapy if menopausal (Table 1).
Four women with augmentation and breast cancer could not be matched
to 5 women without augmentation because 2 were of unknown race, 1 was of mixed
race, and for 1 woman it was not known whether she had a prior mammogram.
The remaining 137 women with augmentation were matched to 685 women without
augmentation for comparison. Among women with a mammogram within 1 year of
cancer diagnosis, women with augmentation were more likely to present with
symptoms: 47% of women with augmentation and 35% of women without reported
the presence of a lump or nipple discharge (P = .03).
To calculate the sensitivity of mammography, we selected mammograms
occurring within 1 year before cancer diagnosis and before December 31, 2000
(86 augmented, 434 nonaugmented). To estimate the sensitivity of screening
mammography (as defined in the "Methods" section), we excluded mammograms
of women with self-reported symptoms (41 with augmentation and 145 without
augmentation). In addition, we excluded mammograms of women with missing symptom
information and mammograms occurring less than 10 months after a previous
mammogram, resulting in screening mammograms of 40 women with augmentation
and 238 women without for analysis. The distribution of BI-RADS assessments
differed for women with and without augmentation, with a lower proportion
of women with augmentation having a BI-RADS assessment of 0 (7.5% vs 17.2%)
and 5 (0% vs 11.8%), a similar proportion with an assessment of 4 (37.5% vs
37.8%), and a higher proportion with a 1, 2, or 3 (55.0% vs 33.2%). The raw
sensitivity of screening mammography was lower for women with augmentation
vs without (45.0% vs 66.8%; P = .008; Table 2). Sensitivity remained significantly lower after adjustment
for age, breast density, first vs subsequent mammogram, and mammography registry
(P = .02).
We also estimated the sensitivity of mammography among symptomatic women
by using data from 41 women with augmentation and 145 women without augmentation
with self-reported symptoms. The sensitivity of mammography was 8 percentage
points lower in women with augmenation (73.2% for women with augmentation
and 81.4% for women without augmentation, Table 2); however, this difference was not statistically significant
(P = .25). This difference remained nonsignificant
after adjustment for age, breast density, first vs subsequent mammogram, and
mammography registry (P = .69).
To estimate the specificity of screening mammography, we excluded mammograms
of women with self-reported symptoms (1006 women with augmentation and 62 625
women without augmentation). In addition, we excluded mammograms of women
with missing symptom information and mammograms occurring less than 10 months
after a previous mammogram, resulting in screening mammograms of 9067 women
with augmentation and 854 997 women without augmentation for analysis.
Those women with augmentation were more likely to have a BI-RADS assessment
of 1, 2, or 3 (97.7% vs 96.7%) and less likely to have an assessment of 0
(1.8% vs 2.4%) or 4 (0.4% vs 0.9%) compared with women without augmentation.
There were very few assessments of 5 in both groups (1 woman with augmentation
and 234 women without augmentation). The specificity of screening mammography
was 1 percentage point higher for women with augmentation vs women without
augmentation (Table 2, P<.001). This difference remained after adjusting for age, race/ethnicity,
first vs subsequent mammogram, breast density, family history, menopausal
status, current hormone therapy use, and mammography registry (P<.001). Among symptomatic women without breast cancer (1006 women
with augmentation and 62 625 women without), adjusted specificity tended
to be lower for women with augmentation compared with women without (Table 2, P = .06).
Table 3 shows the corresponding
distributions of tumor characteristics for the women with a mammogram before
January 1, 2001, and cancer diagnosis within 1 year of the mammogram. Among
asymptomatic women, there were no significant differences in tumor characteristics
in women with augmentation compared with women without despite the difference
in sensitivity; however, the median tumor size at detection for women with
augmentation was 3 mm larger. In contrast, among symptomatic women, women
with augmentation were more likely to be diagnosed with invasive cancer (P = .04), but those cancers were smaller (P = .02), lower grade (P = .004), and more
likely to be estrogen-receptor positive (P = .05).
Table 4 displays the distributions
of tumor characteristics for the entire matched sample. There were no significant
differences in the percentages of invasive cancer or distributions of tumor
stage, nodal status, tumor size, or estrogen-receptor status for women with
augmentation compared with women without augmentation (P>.10 in all cases); however, women with augmentation tended to have
lower grade tumors (P = .052). Among women with augmentation,
52.0% had grade II cancer and only 25.5% had grade III or IV compared with
40.1% grade II cancer and 37.3% grade III or IV among women without augmentation.
Results from the logistic regression models (Table 5) that adjusted for age, previous screening, and mammography
registry were similar to unadjusted results. There were no significant differences
in the odds of invasive cancer, stage II or higher cancer, nodal involvement,
tumors of more than 20 mm, or estrogen-receptor–negative status among
women with augmentation compared with women without augmentation; however,
women with augmentation were less likely to have grade III or IV cancer (odds
ratio [OR], 0.52; 95% CI, 0.31-0.85; P = .02). Results
were similar after additionally adjusting for menopausal status, current hormone
therapy use, family history, or breast density; however, the difference in
grade became nonsignificant after adjusting for menopausal/hormone therapy
status (OR, 0.60; 95% CI, 0.32-1.09) or breast density (OR, 0.65; 95% CI,
0.34-1.18).
Breast augmentation may interfere with the interpretation of mammography
examinations because implants are radio-opaque.6-15 To
improve the accuracy of mammography in women with breast augmentation, Eklund
et al10 proposed the use of breast implant
displacement views, which are performed while the breast tissue is pulled
forward and the breast implant is pushed back to improve visualization of
breast tissue. During a time when displacement views are the standard of care,
we found that screening mammography missed 55% of the cancers in asymptomatic
women with augmentation compared with 33% in similarly aged women without
augmentation.
We report relatively low sensitivity and high specificity of screening
mammography even among women without augmentation. This is because of 2 factors.
First, we defined a positive mammogram by using the final assessment, which
was based on a complete work-up (the results of all imaging performed following
the screening mammogram).31 Using the final
assessment lowers sensitivity and increases specificity, because some mammograms
that were initially given a positive BI-RADS assessment of 0 are resolved
to a negative assessment after receiving additional imaging. Second, our study
sample is relatively young because women with augmentation tend to be younger
than a general screening population and these women were age-matched with
women without augmentation. The sensitivity of mammography is lower in younger
women because they tend to have dense breast tissue that can obscure signs
of cancer32-34 and
may have more rapidly growing tumors.
Despite the lower sensitivity of mammography in women with augmentation,
these women were diagnosed with cancer of similar stage, size, nodal status,
and estrogen-receptor status and lower grade compared with women without augmentation.
As found in other studies19,23,25 among
symptomatic women, women with augmentation had tumors with better prognostic
characteristics, including smaller size, lower grade, and estrogen-receptor
positive status. This suggests it may be easier to palpate breast masses in
women with breast implants given their lower native breast volume7 or because breast implants provide a firm platform
to palpate against.12,19,35 In
addition, women with augmentation may be more breast aware or body conscious
and hence seek medical care more quickly for breast changes or symptoms.
Several previous studies found similar or more favorable breast cancer
characteristics in women with augmentation compared with women without augmentation8,18-24;
however, the majority of women in these studies were not undergoing regular
screening mammography and most presented with palpable lumps. Therefore, previous
results cannot be generalized to a screening population. Two somewhat larger
studies4,7 found evidence supporting
delayed diagnosis in women with augmentation. Brinton et al4 compared
breast cancer stage in 78 women with augmentation with 36 women without augmentation
who had undergone other types of plastic surgery and found women with breast
implants tended to have later stage disease (35% vs 17% with regional or distant
disease), although this difference was not statistically significant. The
study conducted by Skinner et al7 compared
99 women with cancer in augmented breasts to 2857 cases in women without augmentation.
They found that women with augmentation were more likely to be diagnosed with
palpable tumors (83% vs 59%), invasive carcinoma (82% vs 72%), and have nodal
involvement (48% vs 36%). Although women with augmentation in our study also
presented more often with symptoms (47% vs 35%), the difference was smaller
and the overall symptomatic cancer rate was lower. In addition, we found very
small and nonsignificant differences between the groups for invasive disease
(85% vs 82%), nodal involvement (32% vs 28%), and cancer stage (38% vs 31%
with the American Joint Committee on Cancer stage II or higher). Taken together,
these results suggest that women with and without augmentation are diagnosed
with tumors of similar prognosis. The findings in this study may differ from
earlier reports because of the fact that Brinton et al4 and
Skinner et al7 included women diagnosed with
cancer in the 1980s, before the introduction of displacement views and when
screening mammography was less widely practiced.26
We found asymptomatic women with augmentation have 5 fewer false-positive
examinations per 1000 women screened than women without augmentation (34 vs
39 per 1000 women). Some women with breast implants develop thin layers of
calcium in the peri-implant capsular tissue but these calcifications do not
appear to mimic cancer or increase the chances of having a false-positive
mammogram.36 It should be reassuring to women
with augmentation that their breast implants will not increase their probability
of being called back for additional imaging or breast biopsy.
Our study has several limitations. First, we do not have information
on implant type and placement6,7,11 and
capsular contracture,6 which could influence
mammography accuracy in women with augmentation. Silverstein et al11 found that 39% to 49% of breast tissue is concealed
in women with subglandular implants compared with only 9% to 28% of tissue
in women with subpectoral placement. In contrast, Skinner et al7 found
no difference in mammography sensitivity for women by breast implant placement
(sensitivity of 65.7% for submammary compared with 66.7% for subpectoral placement).
Second, we rely on self-reported information of breast augmentation status
combined with an indication of augmentation from the radiologist. A previous
study37 found self-report of augmentation to
be very accurate; therefore, our combined measure should be reliable. Lastly,
we were missing 13% to 24% of data for some possible confounding variables,
such as breast density and hormone therapy status, and up to 35% of data for
tumor characteristics. Breast density, family history, and hormone therapy
status are most often missing because some participating facilities do not
collect this information, and 1 state cancer registry did not collect estrogen-receptor
status before 1998, contributing to the high missing rate for that outcome.
We are not aware of any reporting bias related to breast augmentation status,
hormone therapy use, breast density, or family history. Because we are using
likelihood-based estimation, our estimates are unbiased if data are missing
at random (ie, if missing data depend only on covariates included in the models).
Despite these limitations, our study has the major advantage of using recent
data from the BCSC, which include a large population of women undergoing screening
mammography from multiple sites throughout the United States.
Although the sensitivity of screening mammography is lower in asymptomatic
women with breast augmentation, there is no evidence that this results in
more advanced disease at diagnosis compared with women without augmentation.
Women with breast augmentation should be encouraged to have routine screening
mammography at recommended intervals.
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