Professional Documents
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clinical practice
A 44-year-old woman who is a new patient has no known current health problems
and no family history of breast or ovarian cancer. Eighteen months ago, she had a nor-
mal screening mammogram. She recently read that mammograms may not help to
prevent death from breast cancer and that “the patient should decide.” But she does
not think she knows enough. She worries that there is a breast-cancer epidemic. What
should her physician advise?
considering other methodologic aspects, such as tween 65 and 74 years of age led to a 55 percent de-
the age of participants (one of the trials included crease in mortality from breast cancer (relative risk
only women in their 40s); the number, type, and of death from breast cancer, 0.45 [95 percent con-
quality of screenings and the intervals between fidence interval, 0.20 to 1.02]).25
them; compliance with the assigned strategy; and
contamination (the degree to which women in risks associated with mammography
control groups underwent screening mammogra- False Positive Mammograms
phy).14,15,17,18 Finally, they included a study that Because most women do not have breast cancer at
compared two methods of screening19 and had no the time of screening, there is potential to do harm
unscreened control group. with false positive results that necessitate further in-
In summary, criticisms of all but one of the trials vestigation before a woman can be declared to be
excluded from the meta-analysis have been an- free of disease. Nationally, an average of 11 percent
swered. In-depth independent reviews of the criti- of screening mammograms are read as abnormal
cisms concluded that they do not negate the effec- and necessitate further diagnostic evaluation26;
tiveness of mammography, especially for women breast cancer is found in about 3 percent of women
older than 50 years of age.3,18,20 with an abnormal mammogram (representing 0.3
percent of all mammograms). Therefore, on aver-
women in their 40s age, a woman has about a 10.7 percent chance of a
For many years, there has been controversy over false positive result with each mammogram. Be-
the use of screening mammography for women in cause women are screened repeatedly, a woman’s
their 40s.21 In general, the effect of screening risk of having a false positive mammogram increas-
younger women has been slower to appear and es over time. One study estimated that after 10 mam-
less dramatic than the effect among women older mograms, about half of women (49 percent [95 per-
than 50 years of age. These differences may result cent confidence interval, 40 to 64]) will have had a
from mammographically denser breasts in younger false positive result, which will have led to a needle
women (leading to reduced sensitivity of mammog- biopsy or an open biopsy in 19 percent (95 percent
raphy), faster spread of some cancers in younger confidence interval, 10 to 41).27
women, or both. Meta-analyses show that screen- False positive mammograms increase patients’
ing in this age group decreased 15-year mortality anxiety; the degree of anxiety is related to the in-
from breast cancer by about 20 percent.3,22 tensity of the additional diagnostic procedures and
Because trial results are presented according to the recency of the screening mammogram.20 One
women’s ages at the time of entry into the studies, study found that in the 12 months after a false pos-
some women who entered in their late 40s received itive mammogram, women initiated more health
a diagnosis of breast cancer in their 50s; there- care visits for both breast-related and non–breast-
fore, some of the benefit ascribed to the screening related problems.28 However, false positive mam-
of women in their 40s would have occurred if the mograms increase women’s adherence to further
women had waited until 50 years of age to be screening.29-31
screened.23,24 Also, although analyses are usually The risk of a false positive mammogram varies
presented according to the decade of life, it is likely according to characteristics of the woman and ra-
that a gradual change occurs as a woman ages. The diologic factors: a younger age, an increasing num-
latest analysis of the four Swedish trials — the first ber of breast biopsies, a positive family history of
to examine screening effects according to five-year breast cancer, estrogen use, an increasing interval
age increments — found that screening was most between screenings, the lack of comparison with
effective after 55 years of age.16 previous mammograms, and a tendency by the ra-
diologist to consider mammograms abnormal (as
mammography in women older determined by the percentage of mammograms
than 70 years of age read as abnormal) were independent risk factors
Too few women older than 70 years of age partici- for a false positive result in one study.32 Having
pated in randomized trials to permit conclusions mammographically dense breasts also increases the
to be drawn about the effects of mammographic risk of false positive (or false negative) mammo-
screening in this age group. One case–control study grams.33-35 Many characteristics of patients are im-
in the Netherlands found that screening women be- mutable, but obtaining mammograms during the
luteal phase of the menstrual cycle may decrease icy and Research recommends that the false positive
mammographic breast density.36 Also, a prelimi- rate be no more than 10 percent.38 The malpractice
nary investigation found that stopping hormone- climate in this country may work against the lower-
replacement therapy 10 to 30 days before a repeated ing of the threshold, since failure to diagnose breast
mammogram eliminated or reduced mammo- cancer is the leading reason for malpractice suits.39
graphic abnormalities.37 Comparison of current and previous mammograms
Lowering the recall rate (the percentage of mam- decreases the false positive rate, as does the use of
mograms that result in recommendations for fur- screening intervals of 18 months or less.
ther tests) is likely to reduce the risk of false positive
mammograms. Because of the trade-off between Possible Overdiagnosis — Ductal Carcinoma in Situ
sensitivity and specificity, it is important not to low- Ductal carcinoma in situ was a relatively rare diag-
er the radiographic threshold for recall so much that nosis before the introduction of mammography. In
cancers are missed. The Agency for Health Care Pol- 1973, the incidence in the United States was 2.4
Table 2. North American Recommendations for Routine Mammographic Screening in Women at Average Risk
Who Are 40 Years of Age or Older.*
* Adapted from the U.S. Preventive Services Task Force.3 A “no” recommendation may be a statement that there is insuf-
ficient evidence for a positive recommendation.
† Recommendations are for mammography with or without clinical breast examination.
‡ There is an explicit recommendation to screen women older than 70 years of age.
§ Recommendations note that women should be counseled about the risks and benefits of mammography.
¶ Recommendations note that women at high risk should be screened beginning at 40 years of age.
guidelines
cases per 100,000 women; by 1998, it was 30.7 per Recommendations from several leading groups re-
100,000 women, accounting for approximately 14 garding mammographic screening are summarized
percent of all breast cancers diagnosed.1 With treat- in Table 2.3 After the analysis by Gotzsche and
ment, the prognosis is excellent. In one study, wom- Olsen, some, but not all, reconsidered and changed
en given a diagnosis of ductal carcinoma in situ had their recommendations. For example, the editorial
a 9-year survival rate that was the same as or better board of the Physician Data Query data base of the
than that in the general population,40 and in anoth- National Cancer Institute (which does not issue rec-
er study, the risk of death from breast cancer within ommendations, as such) backed away from con-
10 years after the diagnosis of ductal carcinoma in cluding that mammography is effective; instead, the
situ was 1.9 percent.41 board now concludes that mammography “may”
Such an excellent prognosis could be attribut- decrease mortality.23 The U.S. Preventive Services
able to the detection of lesions before they become Task Force moved in the opposite direction and ex-
invasive cancers, which could save lives. However, tended its recommendations for the use of screen-
if ductal carcinoma in situ were the usual precursor ing to include women ranging from 40 years of age
to early invasive cancer, the incidence of early-stage to more than 70 years of age.3
invasive breast cancer should decrease as the inci- Recommendations from expert groups with re-
dence of in situ cancer increases, but the opposite gard to screening women in their 40s have long var-
is happening. Also, autopsy studies in women who ied, but over time, more groups have moved toward
died from causes unrelated to breast cancer have endorsing the same approach for this age group as
shown a substantial “reservoir” of ductal carcino- for older women. Most groups have not issued ex-
ma in situ in such women.42 Therefore, detection plicit recommendations for women older than 70
of ductal carcinoma in situ may be an example of years and merely recommend that screening begin
at a certain age. More groups have begun calling for relative risks (occurring over meaningful periods),
shared decision making about breast-cancer screen- and through comparisons with other risks.54
ing, but the information to be shared has not been
specified. specific recommendations
All women, regardless of age, should be asked
whether they have a family history of breast cancer,
conclusions and
recommendations ovarian cancer, or both (Table 3).55,56 For women
without strong family histories, discussions about
general conclusions breast-cancer screening should begin at 40 years of
Breast cancer is common, but when viewed over a age and continue until life expectancy is less than
10-year period, the risk for the average woman is 10 years. Evidence supporting the usefulness of
relatively small. During the past few years, scientific mammographic screening is strongest for women
controversy about the benefits of screening mam- between 50 and 69 years of age, and screening
mography has increased. As with most screening should be routinely recommended for women in
tests, there are hazards — primarily, risks of false this age group. For women 40 to 49 years of age
positive mammograms, with associated anxiety and (such as the patient described in the vignette),
unnecessary biopsies, and perhaps a risk of overdi- shared decision making is especially important,
agnosis. because the absolute benefit of screening is smaller
When the benefits of medical interventions are and the risks associated with it are greater. Screen-
controversial and when hazards exist, shared deci- ing should be routinely discussed, and the patient
sion making is needed, with the clinician providing and clinician should decide together according to
facts and the patient assessing her situation from the woman’s values.
the vantage point of her personal values. In addi- For women who want more information, Table
tion, the climate in the United States with regard to 1, the Breast Cancer Risk Assessment Tool, or both
malpractice makes discussions between clinician can be used to estimate the individual risk of breast
and patient about breast-cancer screening essential
for all women beginning at 40 years of age. To save
time, information can be provided by handouts and
≥1 False positive
an office practice that is organized to address the mammogram
concerns of patients. 600 560
Women vary in terms of how much they want to
500 470
participate in decisions about screening. In one sur-
vey of women younger than 50 years of age, 49 per- 400
No. of Women
wanted to make the decision themselves, and 7 per- 300 ≥1 Needle or open
biopsy
cent wanted the physician to decide.5 However, 79
190 190 190
percent wanted information from the doctor. Be- 200
cause of varying individual values, and because Development
of breast cancer
women have a good deal of fear about breast can- 100
37
cer,53 physicians should be prepared for a decision 15 28
0
different from the one they would recommend. 40 50 60 40 50 60 40 50 60
A woman needs some knowledge of her risk of Years of Age at Beginning of the 10-Yr Period
breast cancer and the benefits and hazards of
screening — specifically, her risks of the develop- Figure 1. Chances of False Positive Mammograms, Need for Biopsies,
ment of and death from breast cancer and her and Development of Breast Cancer among 1000 Women Who Undergo
Annual Mammography for 10 Years.
chances of successful treatment with screening and
All numbers are rounded. The numbers for 10-year rates of false positive
without screening, of having a false positive mam-
mammograms and breast biopsies come from a single study in which, over-
mogram or an invasive breast procedure, and of hav- all, the rate of false positive mammograms was 6.5 percent,27 and the rate
ing ductal carcinoma in situ diagnosed. Numerical may be different in other settings. Data on the development of breast cancer
risks may be best explained with the use of pictures are broken down further in Figure 2.
or graphs, with discussion of absolute as well as
25 regardless
of screening
— a fact that many women do not understand.57,58
20 18 Diagnosis of ductal
carcinoma in situ Recently, survival rates have been improving, but
15 14 Life saved by
15 because of screening how much of this improvement is attributable to
mammography mammography
10 8
treatment itself and how much to earlier diagnosis
7 7
4
6 due to screening are difficult to determine. The
5 3 2 number of women “saved” is calculated according
0 to the estimates that screening of women in their
40 50 60 40 50 60 40 50 60 40 50 60
40s reduces mortality from breast cancer by about
Years of Age at Beginning of the 10-Yr Period
20 percent and screening of women in their 50s or
Figure 2. Chances of Breast-Cancer–Related Outcomes among 1000 Women 60s reduces it by about 30 percent. It should be em-
Who Undergo Annual Mammography for 10 Years. phasized that these numbers may vary, depending
All numbers are rounded. The numbers for the incidence of invasive breast on the efficacy of mammography in reducing mor-
cancer and ductal carcinoma in situ, as well as the number of women whose tality. Individual women will interpret these num-
lives are saved by treatment (those surviving at least 20 years after the first di- bers differently depending on their own values.
agnosis of breast cancer) regardless of screening, were calculated on the ba-
To decrease the risk of false positive results, pa-
sis of data from the Surveillance, Epidemiology, and End Results program.1,57
The numbers of women whose lives are saved because of screening (those tients should be referred to experienced mammog-
surviving at least 15 years after diagnosis) were calculated on the assumption raphers with recall rates of no more than 10 percent.
of a reduction of 20 percent in mortality from breast cancer among women 40 They should be encouraged to obtain previous
to 49 years of age and a reduction of 30 percent among women 50 to 69 years mammograms for comparison and should undergo
of age; these numbers are approximate.
screening more frequently than every 18 months.
Women often are unaware of the difference be-
tween screening and diagnostic examinations to
cancer. Women should be reminded that the risk of evaluate a breast symptom or abnormal finding. In
breast cancer increases with age and that the one- one study, cancer was diagnosed in about 10 percent
in-eight risk is a lifetime risk for a newborn who of women older than 40 years of age who reported
lives for 90 years. a breast mass and in almost 5 percent of those with
The chances of being helped or harmed by any breast-related problem.59 Clinicians and wom-
screening mammography are summarized in Fig- en should not be falsely reassured by a previously
ures 1 and 2, which contain information that may normal screening mammogram in the case of a
be useful to patients. These figures show the chanc- new breast-related problem.
refer enc es
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Mammographic screening after the age of icy and Research, October 1994. (AHCPR 54. Edwards A, Elwyn G, Mulley A. Explain-
65 years: evidence for a reduction in breast publication no. 95-0632.) ing risks: turning numerical data into mean-
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31. Physician Insurers Association of America, 55. Statement of the American Society of
26. Brown ML, Houn F, Sickles EA, Kessler June 1995. Clinical Oncology: genetic testing for cancer
susceptibility, adopted on February 20, 1996. Md.: National Cancer Institute, 1997. (NIH Breast symptoms among women enrolled in
J Clin Oncol 1996;14:1730-6. publication no. 97-2789.) a health maintenance organization: fre-
56. BRCA1 genetic screening. Guideline 58. Silverman E, Woloshin S, Schwartz LM, quency, evaluation, and outcome. Ann In-
NGC-0461. Rockville, Md.: Kaiser Perma- Byram SJ, Welch HG, Fischhoff B. Women’s tern Med 1999;130:651-7.
nente, 1998. views on breast cancer risk and screening Copyright © 2003 Massachusetts Medical Society.
57. Ries LAG, Kosary CL, Hankey BF, Miller mammography: a qualitative interview study.
BA, Harras A, Edwards BK, eds. SEER can- Med Decis Making 2001;21:231-40.
cer statistics review, 1973-1994. Bethesda, 59. Barton MB, Elmore JG, Fletcher SW.
CORRECTION ever, the rate of death due to breast cancer, as a percentage of the
rate of death from any cause, is highest among women in their 40s.
Mammographic Screening for Breast Cancer A reduction in mortality of 20 percent among women in their 40s is
a low estimate. The Gothenberg Breast Cancer Screening Trial,1 the
To the Editor: I was troubled by the lack of a cost–benefit analysis in Malmö Mammographic Screening Program,2 and the Swedish trials3
the article by Fletcher and Elmore on the effectiveness of mammog- showed statistically significant reductions in mortality of 44 percent,
raphy for screening for breast cancer (April 24 issue).1 In fairness, 35 percent, and 29 percent, respectively, among women younger than
their recommendations are more fiscally conservative than those of 50 years of age. Furthermore, because of noncompliance and con-
the U.S. Preventive Services Task Force. Still, their omission of any tamination, the trials underestimate the benefit. Women need to be
discussion of relative costs and benefits gives the implicit message provided with all the data in order to make informed decisions. The
that cost does not matter. concerns raised by Gøtzsche and Olsen were either unwarranted or
of no consequence,4 and the trial data remain valid.
William A. Hensel, M.D.
Moses Cone Health System Daniel B. Kopans, M.D.
Greensboro, NC 27401 Harvard Medical School
bill.hensel@mosescone.com Boston, MA 02115
References References
death due to breast cancer calculated on the basis of a screened pop- cancer with mammography. Lancet 2001;358:1340-1342.
ulation rather than a control population, thus compounding the error.
They estimate that four lives are saved by screening 1000 women 50 2. Gøtzsche PC. Screening for breast cancer with mammography.
to 60 years of age for 10 years and that six lives are saved by similar Lancet 2001;358:2167-2168.
screening among women 60 to 70 years of age. In reality, the number
3. Gøtzsche PC. Update on effects of screening mammography.
needed to screen is 1224 to save 1 life over a 14-year period1 (ap-
Lancet 2002;360:338-338.
proximately 1713, over a 10-year period); in other words, 5.8 lives will
be saved per 10,000 women screened, not 4 or 6 per 1000 screened
4. Shapiro S. Discussion II. In: Selection, follow-up, and analysis in
— almost a case of the missing zero. Among women younger than 50
prospective studies: a workshop. National Cancer Institute mono-
years of age, the number needed to screen is approximately 2508 —
graph 67. Bethesda, Md.: National Cancer Institute, May 1985:75-
that is, over a 10-year period, 4 lives will be saved per 10,000 women
9. (NIH publication no. 85-2713.)
screened, not 20 per 10,000, as estimated by the authors.
Finally, we wish to point out an error in our article. The statement (be-
ginning on the last line of page 1674) that ``obtaining mammograms
during the luteal phase of the menstrual cycle may decrease mammo-
graphic density´´ should have read ``obtaining mammograms during
the luteal phase of the menstrual cycle may decrease mammographic
sensitivity.´´
References