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903
Benefits versus Risks from Mammography
A Critical Reasessment
Fred A. Mettler, M.D., M.P.H.
Arthur C. Upton, M.D.
Charles A. Kelsey, Ph.D.
Robert N. Ashby, M.D.
Robert D. Rosenberg, M.D.
Michael N. Linver, M.D.
Department of Radiology, University of New
Mexico, Health Sciences Center, Albuquerque,
New Mexico.
BACKGROUND. The use of mammography has increased rapidly over the last decade. The justification for mammographic examinations is the potential benefit
they provide in detecting breast cancer at an early stage and reducing mortality.
However, this benefit must be balanced against the associated potential risk of
radiation carcinogenesis, economic costs, and a number of other factors. Most
publications to date have used radiation risk factors and data from studies that
were published over a decade ago, which now have been superseded by the results
of more recent epidemiological studies.
METHODS. This report examines the current literature regarding the benefits of
cancer detection and the risk of radiation carcinogenesis, and calculates the ratio
of benefit and risk for women who begin annual mammography screening at
different ages. We have used current data to calculate the expected individual
benefits and radiation risks associated with annual mammographic screening.
RESULTS. It now appears that there is little risk of breast cancer associated with
radiation exposure from annual mammography in women over the age of 35,
although there is some indication that exposure of younger women may pose a
risk for those women in a genetically sensitive subgroup.
CONCLUSIONS. New data document that for a woman beginning annual mammographic screening at age 50 and continuing until age 75, the benefit exceeds the
radiation risk by a factor of almost 100. Even for a woman who begins annual
screening at age 35 and continues until age 75, the benefit of reduced mortality
is projected to exceed the radiation risk by a factor of more than 25. Cancer 1996;
77:903-9. 0 1996 American Cancer Society.
KEYWORDS mammography, breast cancer, radiation risk, radiation dosage.
A
Address for reprints: Fred A. Mettler, M.D.,
M.P.H., University of New Mexico, Health Sciences Center, Department of Radiology, Albuquerque, NM 87131-5336.
Received April 20, 1995; revision received July
27, 1995; accepted July 27, 1995.
0 1996 American Cancer Society
n increased incidence of breast cancer following exposure to ionizing
radiation has been recognized since the 1960s.’ Over the last decade,
the literature on radiation carcinogenesis in the breast has come to include new findings, and a number of combined analyses have clarified
the benefits of mammography screening. The most common question
women ask about mammography screening is “What are the benefits and
risks to me?” rather than “What are the results of large population studies?” Published data now allow each woman to evaluate her radiation risk
and her benefit in order to decide whether or not to have a mammogram.
Recent updates of epidemiologic studies have delineated the risks of
radiation-induced breast cancer for women of different ages at exposure.
National accreditation with dosimetric evaluation of mammographic facilities over the last three years has provided reliable data concerning the average mammographic dose in the United States. Meta-analysis of a number
of mammographic screening studies has also provided new data on the
magnitude of the reduced mortality from screening mammography at
CANCER March 1,1996 / Volume 77 / Number 5
904
I
25
30
35
40
45
50
55
80
85
70
75
80
85
Attained Age (years)
FIGURE 1. Estimated excess relative risk per Sv. by interval of attained
age (25-34 years, 35-44 years, 55-64 years, 65-74 years, and 2 7 5
DI exp (/&A) where D is equivalent
years) with fitted model ERR (D;A) = C
dose in Sv (neutron RBE = 10) and A is attained age. Estimates and 90%
confidence limits stratified on city, age at the time of the bombings,
attained age, and period. Total number of cases appears above the upper
confidence limit for each interval of attained age. Sv: Sievert; CI: confidence
interval. (Reprinted with permission from Tokunaga M, Land C, Tukapka
S, Nishimori I, Soda M, Akiba S. incidence of female breast cancer in
atomic bomb survivors, 1950-1985. Radiat Res 1994;138:209-23.)
different ages. With these studies, it has been possible to
quantify the cancer mortality risk-benefit ratio.
EFFECT OF RADIATION ON THE INCIDENCE OF
BREAST CANCER
Women in a number of study populations have shown
dose-dependent increases in the frequency of breast cancer after irradiation. The largest such population is comprised of women exposed to atomic bomb radiation at
Hiroshima and Nagasaki, in whom 295 cases of breast
cancer occurred between 1950 and 1987, versus the 200
cases expected in the 510,000 person-years of follow-up
study.' The excess relative risk appears to have increased
in proportion with the dose, averaging about 1.7 at a
dose of 1 sievert (100 rem). It also appears to have varied
inversely with age at the time of irradiation (Fig. 11,
prompting speculation that the level of hormonal stimulation in women who were exposed at older ages was too
low to promote the full expression of carcinogenic effects
on their b r e a ~ t sAnother
.~
possibility is that proliferating
cells in the breasts of young women retain damage or are
more susceptible to carcinogens. The Japanese data also
showed that in women exposed younger than age 20 who
developed cancer before the age of 35, the excess was
more than 6 times greater than in those women whose
cancers occurred at later ages, implying that women with
early disease may represent a genetically susceptible subpopulation.4
Other study populations in whom similar dose-dependent excesses of breast cancer have been reported
include women treated with radiation for various medical
conditions in adult life, i.e., acute postpartum mastitis,s
other benign breast disease^,^" and ankylosing spondylitis'; women treated with radiation for various medical
conditions in childhood, i.e., hemangioma of the skin,'
tinea capitis," enlargement of the thymus gland at infancy,' ' Hodgkin's disease," and other childhood malignanciesI3;women who received multiple fluoroscopic examinations of the chest in the treatment of pulmonary
tuberculosis'4~15;
women who received repeated X-ray examinations in the treatment of scoliosis"'; and early radium dial painters.".'*
In contrast to the aforementioned populations,
women exposed to low levels of radiation, such as those
exposed to elevated environmental concentrations of radioactive weapons fallout,'"20those residing in the vicinity of nuclear power plants," those employed as radiation
workers (other than radium dial painter^),".^" and those
injected with diagnostic doses of radioactive iodine,24
have shown no consistent or significant increases in
breast cancer rates.
Risk of Causing Breast Cancer by Mammography
Dose From Mammography
The American College of Radiology has been accrediting
mammography practices for several years. As part of this
practice, dosimetry has been carried out, and at a May
1994 conference of the College, the average dose at accredited mammography facilities in the United States was
reported to be 1.38 mGy per view, or typically double this
dose (2.8 mGy) per examination, because 2 views of each
breast are typically obtained (Pamela Wilcock, ACR, personal communication). These values are within the range
reported in a number of other countries, for which the
mean glandular dose ranged from 0.6-4.8 mGy.25
Dose-Incidence Relationship
The mathematical relationship between incidence and
dose, and the question of whether there is a practical
threshold at low doses for radiation-induced breast cancer, has been evaluated by a number of investigators,
including Land et al., who inferred that the best statistical
fit to the available data was a dose-response curve of
approximate linearity.26 The epidemiologic studies of
breast cancer incidence after low-LET irradiation that are
sufficient to enable risk estimates to be derived are summarized in Table 1."
Although there may be some element of curvilinearity in the dose-incidence relationship, it appears from the
available data that the error in risk estimates based on
the assumption of linearity is likely to be small; however,
in fitting potentially linear curves to the available data,
Benefits vs. Risks in Mammography/Mettler et al.
TABLE 1
Risk Factors for Female Breast Cancer Incidence from Various
Epidemiologic Studies"
Study
Average excess
absolute risk (I04PSY,,l~'
Atomic Bomb survivors
Postpartum mastitis
Fluoroscopy (Massachusetts)
Ankylosing spondylitis
Swedish breast irradiation
Thymic irradiation
Skin hemangioma
Scoliosis patients
Cervical cancer
Hodgkin's disease
6.8 (4.9-8.7)
9.1 (6.0-13)
8.0 (3.6-13)
9.0 (2.0-18)
2.7 (2.2-3.3)
4.9 (2.4-8.1)
4.1 (1.8-6.9)
17.8 (2.4-431
-0.3 (<0-0.2)
0.04 (0.03-0.07)
Numbers in parentheses indicate 90% confidence intervals.
PYSv: person year sieveri
one should bear in mind that the confidence intervals
(CI) from the Japanese mortality study encompass zero
for doses of less than 0.5 Gy, although the corresponding
incidence data demonstrate a statistically significant increase in the frequency of breast cancer at dose levels
down to approximately 0.3 Gy for women of all ages.
Although a large number of studies, which include natural
background exposure and occupational exposure, do not
demonstrate a statistically significant increase in breast
cancer, this may be due to the relatively low doses and
therefore low expected yields of tumors relative to the
spontaneous incidence in such studies. Therefore, for
purposes of an estimate of the potential detriment from
mammography, it would appear that utilization of a linear extrapolation is not unreasonable, although it may
provide a conservative scenario.
Influence of Dose Rate
A question that arises in risk estimation is the possible
effect of dose rate on the induction of breast cancers by
irradiation, and the applicability of various epidemiologic
observations to mammography. In women exposed repeatedly to small doses of X-rays for months or years
through fluoroscopic examinations of the chest for pulmonary tuberculosis, the relative risk of breast cancer per
unit dose, adjusted for age at the time of exposure and
duration of follow-up, is not significantly different from
the risk in women exposed instantaneously to atomic
bomb radiation and the risk in women exposed in one or
more daily radiotherapy treatments for acute postpartum
mastitis or ankylosing ~ p o n d y l i t i s . ~ As
' - ~ a~ result of the
generally good agreement among studies (Table 11, the
age specific excess risk factors derived from the atomic
bomb survivors can probably be used justifiably without
905
a dose or dose-rate correction factor in estimating" the
risks attributable to mammography.
Influence of Age at the Time of Exposure
Age at exposure appears to be the most significant modifying factor affecting the risks of screening mammography. Early reports in the literature indicate that radiation
exposure during infancy may result in breast cancer in
young women. In most studies of childhood and adult
exposure, breast cancer risk decreases markedly with increasing age at exposure. In fact, the Life Span Study of
atomic bomb survivors and studies of multiple fluoroscopies in Canadian tuberculosis patients show little, if
any, detectable risk in women exposed older than the age
of 40. The Japanese data indicate a three- to tenfold
higher excess relative risk at 1 Gy for women exposed
before age 20 than in those exposed after age 40. The
data also indicate that survivors exposed before age 20
have a 13-fold excess relative risk at 1 Sievert (100 rem)
for cancers occurring before the age of 35 compared with
a twofold excess relative risk for cancers occurring after
age 35.3
Because of the marked dependence of risk on age at
exposure (Fig. l),utilization of a generalized risk estimate
for all women in the population would significantly overestimate the frequency of potential cancer deaths in
women exposed only after age 40.
Efficacy of Screening
The potential benefits of screening mammography have
been the topic of numerous scientific studies over the
last three decades. A number of these studies have recently been examined in detail, leading to the conclusion
that screening of women over the age of 50 results in a
25-30% decrease in mortality.'"
The value of screening in the 40-49 year age group
has been a matter of debate, with some authors stating
that it affords a benefit but that previous studies had not
examined this age group specifically.3' This question has
been addressed in a meta-analysis of 13 studies by Kerlikowske et al. who concluded that breast cancer mortality
was reduced by 26% as a result of screening mammography in women aged 50-74 years (95% CI, 17-34%), but
by only 7% in women aged 40-49 years (95% CI, -1324%)."l The latter does not represent a statistically significant benefit, but there is no reason to assume that the
benefit from mammography suddenly begins at age 40 or
50. Another meta-analysis directed specifically at women
40-49 years of age estimated a 14% benefit from screening, which was not statistically significant at the 95% C1,
but the same analysis, excluding the Canadian National
Breast Screening (CNBS) Study, found a 24% benefit,
which was statistically significant at the 95% CI.33 The
Canadian National Breast Screening Study has been
906
CANCER March 1,1996 I Volume 77 I Number 5
judged as flawed on the basis of several factors, including
selection bias, poor image quality, inadequate reader
training, and a significant randomization e r r ~ r . ~ ~ - ~ '
TABLE 2
Breast Cancer BenefitlRisk Ratio for a Woman Having Annual
Mammography Beginning at Age 35
Annual baseline
breast cancer
incidence per
METHODS
Individual Risk and Benefit
We have compiled tables to show the benefit of screening
and the potential radiation risk of mammography for
women who begin screening programs at different ages.
We have chosen variables that can be quantified with
some degree of confidence. Using these tables, a woman
considering whether or not to have a mammogram can
assess the expected benefit in comparison with the radiation risk. In constructing these tables, we have necessarily
been limited by a number of assumptions and constraints.
We have not included the cost of mammography as
a risk, but it should be considered in the decision-making
process. The cost of mammography varies widely from
a low of about $45 (through American Cancer Society
screening programs) to a high of about $250. There is no
evidence that the quality of the mammography examination is related to price. We also have not included any
benefit as a result of the psychologic value of a negative
mammogram, nor have we included any calculation of
the costs of false-positive or false-negative results. These
latter issues tend to be societal or postmammography
concerns that are really not included in the decisionmaking process of a woman when she is deciding whether
or not to get a mammogram.
Age specific radiation risk factors that we have used
are related to incidence (rather than mortality) and have
been based on excess relative risk factors for the Japanese
atomic bomb survivors (Fig. I ) , adjusted to account for
the differences in baseline incidence between the Japanese and the U.S. populations. An excess relative risk of
1 means that there is a 100% increase in the natural breast
cancer incidence.
Based upon 1973-1990 SEER data," we have assumed that about 40% of naturally occurring or radiationinduced breast cancer cases are fatal and that radiationinduced breast cancer has a minimum latent period of
ten years.z7Based upon American College of Radiology
mammography accreditation data, we assumed a dose
for screening mammography of 2.8 mGy per two-view
examination. We have conservatively assumed a 5% reduction in breast cancer mortality as a result of annual
mammographic screening in women who are screened
from ages 35-39 and 25% in those who are 40 or older
when screened."""0
RESULTS
The results for women who begin annual screening at
ages 35, 40, and 50 and continue until age 75 are shown
Age
100,000
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
ti2
63
64
65
66
ti7
68
69
70
71
72
73
74
75
66
66
66
66
66
129
129
129
129
129
187
187
187
187
187
220
220
220
220
220
268
268
268
268
268
339
339
339
339
339
391
391
391
391
391
421
421
42 I
421
421
42 1
Fatal radiationinduced cases
0
0
0
0
0
0
0
0
0
0
<0.1
10.1
0.2
0.2
0.3
0.3
0.4
0.4
0.4
0.4
0.6
0.6
0.6
0.7
0.7
0.9
0.9
0.9
1
1
1.2
1.2
1.2
1.3
1.3
1.4
1.4
1.5
1.5
1.5
1.5
Fatal cases
prevented by
mammography
1.3
1.3
1.3
1.3
1.3
12.9
12.9
12.9
12.9
12.9
18.7
18.7
18.7
18.7
18.7
22
22
22
22
22
26.08
26.8
26.8
26.8
26.8
33.9
33.9
33.9
33.9
33.9
39.1
39.1
39.1
39.1
39.1
42.1
42.1
42.1
42.1
42.1
42.1
Benefit/
risk ratio
>400
352
181
120
91
73
66
61
57
53
50
47
44
43
41
39
38
37
36
35
34
33
33
32
31
30
30
29
29
28
28
27
Tables assume reduction in mortality from breast cancer as a resulr of screening as follows: age 3539, 5 % 40-49. 15%: and 50-75. 25%.
in Tables 2 , 3, and 4, respectively. The age 75 cutoff was
chosen because this is close to the average female life
span. The value of 40% mortality chosen for breast cancer
has no effect on the calculated benefit/risk ratios because
it applies to both naturally occurring and radiation-induced breast cancers. The value chosen for reduction of
mortality for those women screened from ages 40-49
907
Benefits vs. Risks in Mammography/Mettler et al.
TABLE 4
Breast Cancer BenefitlRisk Ratio for a Woman Having Annual
Mammography Beginning at Age 50
TABLE 3
Breast Cancer BenefitlRisk Ratio for a Woman Having Annual
Mammography Beginning at Age 40
~
Annual baseline
incidence per
Age
100,oOO
40
41
42
'13
14
I
5
16
129
12!t
Fatal radiation
induced cases
per 1 ~ , 0 0 0
0
18.i
56
1H7
0
0
<O.l
2iO
210
220
2:!0
.rn.i
?fiH
2liH
0.2
0.2
0.3
0.3
0.3
0.4
0.5
0.5
0.5
0.5
0.6
18.7
18.7
22
22
22
22
22
26.8
26.8
26.8
26.8
26.8
57
187
220
0
47
18
49
50
51
52
53
54
55
56
70
71
?iH
258
26R
339
339
339
:!3Y
?39
39 1
29 1
391
391
19 I
,121
12 I
72
121
73
74
42 I
.12 I
75
421
60
fil
62
ti3
64
65
66
67
6a
69
Age
A
0
12rj
I?9
0
58
59
Benefit/
risk ratio
Annual
incidence
per
12.9
12.3
12.9
12.9
12.9
18.7
18.7
0
0
0
I23
I87
I87
1 87
r.I I
Fatal cases
prevented by
mammography
per 100,OOO
0
10.1
0.1
0 .I
0.i
0.i
0.7
0.7
0.8
0.9
0.9
0.9
0.9
1
50
51
52
>850
53
54
--
JJ
100,ooO
B
220
220
220
220
220
268
268
268
268
268
339
339
333
339
Fatal radiation
induced cases
per 100,000
C
0
0
0
0
0
0
0
0
0
Fatal rases
prevented by
mammography
per 100,000
D
22
22
22
22
22
26.8
26.8
26.8
26.8
26.8
33.9
33.9
33.9
33.9
33.9
33.9
39.1
Benefit/
risk ratio
E
,
' 1500
104
58
59
60
(i1
62
63
64
65
66
92
67
3YI
33.9
3Y.1
61
61
68
69
70
71
72
73
331
39 I
33.9
83
78
74
71
67
33.1
39.1
39.1
59
57
75
54
52
51
Explanation 01 Table 4. If a G:i-year-old ivomaii !who has liad ail amiual screening niaminographic.
examinationsince age ,501 wanted to know hhar the ribk and henelir of her aiinual manimograni i\ou!d
he lor this year, she ivorrld refer to lahle 1. Enrering the age colunin LA: and p i n g to age 63. she
would first note [hat the baseline ["spuntancou<') risk :incidence)of breast cancer in this year is 33%
100.000 (Column R], ,411 her mammograms up to age 62 would haw given her an ;idditional fatal breast
cancer risk of 0.07 cases\lUO,OW :Column Cl. One additional mmmographic examination rhis year
33.9
33.9
33.3
33.1
42. I
42.1
42.1
42.1
42.1
42.1
826
413
275
206
165
I38
118
49
17
46
41
43
only affects the benefitIrisk ratio for those specific years,
regardless of whether a 40% or 15% value is used, the
benefit/risk ratio remains in excess of SO.
The results show that for any rational annual mammography screening program, the benefits substantially
outweigh the risks. Even for the extreme example of a
woman beginning annual screening at age 35 and continuing until age 75, we calculate a benefit that is at least
25 times greater than the potential radiation risk. IJsing
a more common protocol of annual screening from age
SO to age 75, the benefit in terms of reduced mortality as
a result of screening should exceed the radiation risk by
a factor of about 100.
74
339
39 1
39 1
421
42 1
421
121
421
421
0
0.1
0.1
0. I
0.1
0.1
0.2
0.2
0.2
0.2
0.3
0.3
0.4
0.4
0.4
0.4
0.5
39.1
39.1
39.1
12.1
12.1
12.1
42.1
42.1
12.1
1.140
^,
(20
480
360
288
240
206
1RO
160
144
131
1'0
111
103
9G
90
woiild rai% her total radiation risk to 0.09i100.000. These borh caii be rounded to 0.1 i100,ooO!Co!umn
(:I. 'I he chances [hat the inammogram would prevenr a iatal canwr ivould he 33.'3~100.000;Column
D;.'The herielitirisk ratio ~ o u l dbe 360 :Column El. In other w d c . her niamniogram exaniination
rhis year w u l d provide 360 limes more benefit than the polenrialharm from 311 of lier nianimography
screening examinations combined.
DISCUSSION
Screening for High Risk and Sensitive Subgroups
In general, radiation-induced breast tumors do not appear in women until they have reached the age when
spontaneous breast cancers usually occur. Thus, most
radiation-induced cancers are indistinguishable in terms
of age of appearance from spontaneously occurring
breast cancers. It is possible that the reason for this is agedependent variations in hormonal stimulation or other
factors. In atomic bomb survivors, there is apparently a
markedly higher excess relative risk for those with early
908
CANCER March 1,1996 I Volume 77 I Number 5
onset breast cancers than for those with cancers that occur later, as noted above. This difference has been postulated to be due to the existence of a genetic subgroup with
a high sensitivity to radiation-induced breast ~ a n c e rIn
.~
the same population, a lower age at first pregnancy has
been inferred to be protective not only against spontaneous breast cancer but also against radiation-induced
breast ~ancer.‘“~~*
The implication of this for mammography screening is not clear at the present time.
Other genetic issues have been raised, particularly
because an increased risk of breast cancer has been reported in families affected by ataxia-telangiectasia; Swift
et al. have reported that heterozygous women who had
been exposed to diagnostic fluoroscopic examination exhibited a fivefold increase in risk.43Although this observation would seem to be important, the diagnostic radiology
involved was almost always to the abdomen, which would
give only scattered radiation to the breast at very low
doses (less than the annual dose from natural background); also, the exposed and control groups were of
very different ages, and adjustment for this difference was
not p o ~ s i b l e . Given
~~,~~
the numerous and major problems with the study, it is doubtful that it should affect
risk estimates for screening mammography.
Recently, several other breast cancer susceptibility
genes, including BRCAl and BRCA2 in germ cell lines,
have been identified.46.47
These two genes are thought to
be responsible for most hereditary breast cancers (which
account for 5-10% of all breast cancers). Women with
the BRCAl mutations are estimated to have an 85% lifetime risk of breast cancer, and more than half of them
will develop breast cancer before the age of 50:* The
estimated incidence of each of these genes is 1 in 200
women.49The issue arises as to the potential impact of
these discoveries on clinical practice and, in particular,
on the indications for screening mammography. At present, there is little clinical impact as a result of genetic
screening, in part because these genes are very large and
many mutations have already been reported for the
BRCAl gene alone. In addition, accurate and accessible
tests far these mutations are not yet available.
However, even without tests for these mutations being available, there are clearly persons with a strong family history of breast cancer, and whether such persons
should have screening at an early age is of interest. The
answer to this question depends on whether such “high
risk” women, including those with BRCA mutations, are
also at higher than normal risk for radiation-induced
breast cancers. There is no reason to assume, however,
that the excess risk in such women would be higher for
radiation-induced cancers than for breast cancer in general and that the benefit/risk ratio would necessarily be
different. If in the “high risk” groups the risk of radiationinduced cancer was not elevated disproportionately, the
benefitlrisk ratio would shift in favor of the benefit. This
might be offset by the increased difficulty of locating
small cancers in the dense breast tissues of young
women.
CONCLUSION
The possible harm from ionizing radiation should not be
a significant factor in deciding whether annual mammographic screening should be performed. This is true even
when considering screening in women as young as 35
years of age.
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Thompson D, Mabuchi K, Ron E, Tokumaga M, Ochikubo
S, Sugimoto S, et al. Cancer incidence in atomic bomb survivors, Part 11, solid tumors 1958-1987. Radiat Res 1964;
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Tokunaga M, Land C, Tukapka S, Nishimori I, Soda M, Akiba
S. Incidence of female breast cancer in atomic bomb survi-
1969;43:803- 11.
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vors, 1950-1985. Radiut Res 1994;138:209-23.
Tokunaga M, Land C, Aoki Y, Yamamoto T, Asano M, Sat0
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