FOR YOUNGER WOMEN
REVIEW of the
Breast Surgeon, Clinical Director,
Senior Lecturer, Waikato Academic Division, Auckland School of Medicine
Correspondence to: Mr I D Campbell
Dept of Surgery, Health Waikato PB 3200, Hamilton
MAMMOGRAPHY FOR YOUNGER WOMEN
- A DIFFERENT LOOK AT THE EVIDENCE -
The Ministry of Health, epidemiologists, clinicians and the vast majority of women's organisations in
New Zealand are uniformly in agreement that screening mammography is very much
indicated for women over 50 years of age.
The Ministry of Health Policy on Mammography for Younger Women has to
date been opposed to screening of 40-49 year old women. 1
The issue of screening for younger women 40-49 years of age has been a
highly controversial subject world wide and not the least in New Zealand, as
evidenced by the multiple letters to the New Zealand Medical Journal on this
are polarised between two extremes ;
(1) the view that screening
mammography in this age group has no justification (2) the view
that the current evidence provides very strong justification for nation-wide
annual screening mammography of 40-49 year olds.
The issue is especially important in New Zealand where we have the
dubious distinction of the highest death rate in the world from breast cancer
in women under 50 years of age.12
A recently published meta-analysis of the results of the randomised
trials of screening mammography for younger women has shown a statistically
significant 23% reduction in deaths from breast cancer by offering screening
and resolves much of the controversy for many epidemiologists and clinicians.13
Eight randomised controlled trials ( RCT's) of routine mammographic
screening for breast cancer have been performed. The meta-analysis13 combines the data from these
trials with periods ranging from 7-18 years of follow up.
Over 170,000 women 40-49 years are included and the data represent over
1,800,000 women - years of follow
up. The data for each of the
individual studies is summarised in Table 1.
The data has been analysed both with and without inclusion of the
Canadian National Breast Screening Study14(CNBSS-1) as with
previous meta-analyses. 15,16
Excluding CNBSS-1 data yields a relative risk of death from breast cancer of 0.77 for the group
offered screening versus the control group not offered screening (95%
confidence intervals 0.62 - 0.95
) - a statistically significant 23% reduction in mortality. Inclusion of
CNBSS-1 yields a relative risk of death from breast cancer of 0.84 (95%
confidence intervals 0.69 - 1.02 ), a
non significant 16% reduction in mortality by offering screening.
These are remarkable results given the numerous deficiencies(by modern
screening programme standards) in design and execution of every one of these
Of the seven RCT's excluding CNBSS-1, the results are fairly consistent.
Five of the seven studies show a trend towards a mortality reduction
for screening. Of the two that
show no trend, Ostergotland had a disproportionally high number of deaths in
women who were randomised to screening but refused or had cancers found prior to undergoing mammography.
Without these deaths the Ostergotland Study shows a relative risk for
breast cancer death of 0.81 in favour of regular screening.18
The Stockholm study, the second study to show no trend, screened the
control group after only two screening rounds and had the longest screen
interval at 28 months between mammograms.
The results therefore represent a 3 - 5 year difference in offering
screening between the intervention and control group and it is not
surprising that little difference has emerged.
Both the Malmo and Edinburgh Trials began screening at age 45 so it
could be argued that the RCT evidence remains less certain for 40-44 year old
women. Unfortunately there are
barely enough women in the RCT's for the whole group to have the statistical
power to demonstrate an effect19 and certainly not enough women or
events (breast cancer deaths) in the 40-44 year old age group to enable
meaningful analysis of this subgroup alone. Indeed if the women with cancer in
the control group experience an 80% 5 year survival, it has been estimated20
that more than 250,000 women would be needed in each arm of a RCT to prove a
benefit for younger women at an earlier follow-up than the current RCT's. It
is doubtful these numbers will ever be achieved in a further screening
with the Canadian Studies14, 21
There are a number of reasons for excluding the CNBSS-1 data.
CNBSS-1 utilised clinical breast examination prior to randomisation
into study and control groups, and the control group received ongoing
screening by physical examination.
The study therefore compares mammographic screening with regular
clinical examination. In the
other RCT's the control groups are not offered any form of screening.
The study recruited volunteers rather than utilising a defined
The randomisation process in CNBSS-1 was non blinded and somehow a
significantly greater number of women20 with advanced breast
cancers at the outset of the study were "randomised" to the
mammographic screening group compared to the control group.
The quality of the mammography in this study has been heavily
From the first two points above, it is clear that the design of the
CNBSS-1 is different from the other RCT's.
Most randomised studies blind the investigator and the patient to
the randomisation process
specifically to avoid any possibility of selection bias.
For the CNBSS's the investigators were not blinded and of women with
particularly poor prognosis breast cancers (four or more involved axillary
lymph nodes) 19 were assigned to the screening group and five to the control
group. Of the 19 assigned to the
screening group, 17 had palpable breast cancers.
The magnitude of this
difference suggests that it is unlikely
that this difference has arisen by chance and has raised the unproven doubt
that the pre-randomisation clinical examination has influenced the assignment
of women to the screening or control groups.
This suggestion has been supported by the fact that women with breast
cancer in the control group have an "
unprecedented survival of over 90% at five years "20
although contemporary data show women aged 40-49 years in Canada and the
USA have an average 5 year survival rate of less than 80%.
In fact for the CNBSS-1 to have shown a benefit for screening
mammography would have required virtually no breast cancer deaths among the
screened women. The randomisation
problem achieves particular importance when it is appreciated that the trend
towards an increased death rate in the screening population (38 deaths in this
group vs 28 deaths in the control group) is more than entirely accounted for
by the excess of advanced breast cancers assigned to the screening group at
the start of the study.
Problems with the way the CNBSS's were set up have impacted heavily on
the quality of mammography.
In many centres existing mammography equipment was used although in a
number of centres this was far from state of the art even at the time of
commencement of study in 1980. (1972 equipment used in one centre).22
External reviews of technical quality were carried out23, 24
and internal audit was carried out by a reference radiologist.25
Neither the radiographers who took the mammograms nor the radiologists
who interpreted the films had received special training.22
Mediolateral oblique projections were not used for the first 5 years of
the 8 year study. A considerable
area of breast tissue is not visualised on straight mediolateral views.
This process is in stark contrast with the Quality
Standards in each of these areas required of BreastScreen Aotoeroa and indeed
any good modern mammography screening programme.
Over 50% of the mammograms obtained during the first four years of the
trial, were technically inadequate and concern was expressed as to the
sharpness, contrast and overall quality of the mammograms.
As a result of the above factors, 42% of the cancers that were missed at
screening and became palpable in the interval between screenings were visible
on the previous mammogram and had been missed by the interpreting radiologist.
Of the cancers diagnosed in the screening programme, 25% could be
identified one year earlier having been missed by the interpreting
radiologist. The number of
cancers which have never shown on mammograms because of poor quality
mammography is not known.20
In the HIP Study, decreased breast cancer mortality among women aged
40-49 years on entry only became apparent seven years after entry.
Every subsequent randomised trial has confirmed that
a greater length of follow up is necessary for demonstration of benefit
for younger women than for women aged 50 years and over.26 The
RCT's also show diverging mortality curves with time for the screened vs
control populations, 27,28 in spite of the fact that screening was
either stopped after a period of years or the control group screened (after 3
- 6 years).
When first published, the
Canadian data have only seven years follow-up and a previous meta analysis of
all the RCT's at seven years follow up shows no benefit for mammography in
younger women at this time. 15
why the RCT's may underestimate benefit.
Compliance and Contamination :
To avoid selection bias randomised trials compare a study group of women
offered screening with a control group not offered screening.
The groups are analysed on an intention
to screen basis
ie; according to which group the women were randomised and not
according to whether screening
actually took place. Some 25%
(10-39%13) of women offered screening in the randomised studies
never had it. Some 25% of women
not offered screening had mammography at some stage during the course of these
studies. The exact percentages
vary from study to study. The
result of this contamination of the control group and dilution of the
screening group is that randomised trials underestimate the true effect of
actually screening women vs not screening women. What women (and clinicians and other concerned individuals)
want to know is :
" What is the benefit
to me if I actually have a mammogram ? "
Statistical methods have been developed to account for the problems of
compliance and contamination in randomised trials. Utilising these it has been estimated that the
true mortality benefit of having a mammogram is some 40-50% higher than
the randomised trials indicate.29
Improvement in mammography :
These studies represent the learning
curve in the development of
mammographic interpretation and technique and a period of time during which
there were major advances in equipment technology. Today (20-25 years
later) we have much better equipment and knowledge; Radiologists and
mammographers undergo detailed training on mammography interpretation and
technique, we utilise grid techniques, better film and film processors and
two-view mammography - all of which improve sensitivity for small cancers.30
It is quite unscientific to discount this improvement31
based on a lack of improvement in detection rate for small breast cancers from
1977 to 1982 compared with a period 10 years later from 1989-92 (data from the
two-counties study).32 Many
other factors besides quality of mammography may influence detection rates of
breast cancer over a ten year period. It
is exactly because of other potential biases that studies using historical
controls as evidence of effect are generally regarded as poor quality
evidence. It could just as well be argued that the improved small cancer
detection rates seen in the New Zealand Pilot Programme33 compared
with the RCT data, is proof of the advances in knowledge, equipment and
technique over the last 15 years. This
argument may be true but many other factors may also be playing a role.
The difference in the quality of mammograms taken today compared with
the mammograms of 15 years ago is very obvious even to a surgeon such as
Better evidence is available from a number of sources.34
Indeed the two-counties study32 provides other evidence
supporting improved sensitivity of modern equipment and techniques - a lower
rate of interval cancers (cancers
arising in the interval between screening rounds and not detected at the
previous screen) in the more recent series and a higher detection rate of
For the Edinburgh Trial35 both improved cancer detection
rates and decreased interval cancer rates were noted in later rounds
concomitant with a significant improvement in mammographic technique and
attributed by the investigators to improved
Even the CNBSS'S have demonstrated this trend.
Baines et al23 showed that 51%
of mammograms performed in 1980-82 were acceptable rising steadily to 85%
acceptable for 1985-87. Coincident
with this improvement, interval cancer rates dropped progressively over years
1-4 from 60% to 20% and the non
palpable cancer detection rate doubled for women aged 40-49.36
Even with modern day equipment small improvements such as use of higher
density film37 may improve the detection rate of small cancers by
as much as 50%.
Quality improvements such as single versus two-view mammography and
double reading of films can and have been rigorously tested. Two-view
mammography increases the sensitivity of mammography for detection of
cancer by 3-11%38-41 and
this improvement is especially of value for women with dense breasts (more
common in younger women) and for detection of small cancers - the ones we need
to detect to save lives. Single
view mammography only
was used in over half the RCT's rather than two-view. (Table
reading by two
independent radiologists has also been studied and improves the sensitivity of mammography42
by up to 15%.43 This
is now standard practice in BSA, but was not routine in the original
Screen Intervals :
The interval between
screens was up to 2½ years in a number of the RCT’s.
1) As the
growth rate for breast cancers in younger women is considerably faster on
average than that for older women18,44
screening at a one year interval for younger women may improve the
mortality benefits by 50-100%18.
Further support for a better screening interval is apparent from the
RCT's. The 2 studies with the
greatest trend towards a benefit ( Malmo and Gothenberg) are also the two
studies (apart from CNBSS-1 for reasons above and HIP because this was
conducted in the 1960’s) with
the shortest screening interval13.
Screening period :
The control group in four of the five Swedish studies were all offered
screening some 4 to 6 years after the study commenced.
The results for these studies therefore represent an approximate 5 year
period of offering screening vs not offering screening28.
Had the control group not been offered screening we would expect that
with time any differences between the control and study groups would have been
considerably more dramatic.
Age group analysis :
The full effects of screening by age remain far from completely sorted
out. The data have thus far been
arbitrarily analysed in the age brackets 40-49 years and over 50 years.
breasts do not suddenly change at 50 years of age Although they do
gradually become less dense with age only 26% of women 40-49 years of age have
mammographically dense glandular tissue32.
We should be looking especially closely at the 45-49 year old age group
because these women have a breast cancer incidence very similar to the
50-54 group45, and the latest NSW, reveal more actual cancers
registered for 45-49 year old women than for the 50-54 age group (Prof J
Forbes - personal communication). Furthermore,
saving the life of a woman between 45 and 49 years of age contributes an
average 10 extra women-years of life compared with saving the life of a woman
between 50 -64 years of age.
The Ministry of Health have previously attempted to dismiss the
potential benefits of screening younger women by pointing out that only a
minority of breast cancer deaths occur in women under 50 years of age.
This is a gross misuse of statistics.
It ignores the point that in order to save the lives of many women who
die of breast cancer in their 50’s and 60’s these breast cancers need to
be diagnosed many years earlier while these women are in their 40’s.
At this time these breast cancers are at a much earlier stage or even
at a precancerous stage such as ductal carcinoma in situ (DCIS).
If DCIS can be removed, invasive cancer may be prevented which
otherwise might take many years before leading to death from cancer if left
undiagnosed and untreated.
It has also been argued that because it takes a longer time for the
benefits of mammography to emerge for younger women than for women 50 and
over, the benefits may be due to younger women turning 50 during the course of
the trials and benefiting once they reach this age. In fact, of the breast cancers diagnosed by screening younger
women in the randomised trials, 75% were diagnosed in women under 50 years of
age (personal communication – Stephen Duffy, Principle Statistician for the
Two Counties Study and Swedish Screening Trials).
If the benefit was solely due to screening women in their 50’s (ie
there was no benefit from detecting the 75% of cancers found while women were
in their 40’s) we therefore might expect the screening trials for younger
women to be only 25% as effective as for older women.
Actually the benefits seen are very similar in magnitude to those for
women in their 50’s and 60’s. Other
factors must explain the difference in time to benefit.
Two possible explanations are: that
women in their 40’s have the best outcome, when
matched for stage, of any age group.
It therefore takes longer for screening to produce a benefit, because
nonscreened women of this age group who get breast cancer live longer on
average than older women. Another
possible explanation is that a higher proportion of breast cancers are
diagnosed at the DCIS stage. DCIS,
if it progresses to invasive cancer and death, takes on average more years to
do so than a cancer that is already invasive .
The RCT's examine only the mortality issue and ignore morbidity.
While mortality benefits are the ultimate goal, morbidity from breast
cancer treatment is also an important goal.
There is no doubt that the average size of cancer detected by screening
mammography is smaller in all age groups32.
Small breast cancers are much easier to treat by breast conserving
surgery with a good cosmetic result and, pending the result of current trials,
are also likely to be amenable to sentinel node based management of the
axilla. This technique removes
the need for axillary dissection with it’s attendant risk of arm lymphoedema
for many women with small breast cancers.
The technique is not appropriate for women with larger breast cancers.
Many women will also not require treatment with chemotherapy if
diagnosed at an earlier stage. These
factors represent very significant advantages to these women.
Adverse effects of Screening Mammography
The adverse effects can be summarised as: the cost; the psychological
impact; the discomfort and inconvenience of the procedure; the recall of
normal women; breast biopsies of some women with benign problems; possible
risks from radiation, and; the false reassurance of a false negative result.
Cost: The cost
of screening 40-49 year old women has been estimated at $AUS14,65646
- $US26,20047 per year of life saved - very much in the mid range
of health care costs for current routine health care interventions
( eg; costs per year of life saved for drug treatment of moderate to
severe hypertension: $US11 -73,00048; coronary artery bypass
surgery: $US7,000; haemodialysis for chronic renal failure: $US35,00049.
These estimates of cost benefit may overestimate the cost compared with the
marginal increase in cost of extending the age group of an existing programme
for 50 - 64 year old women. In
this situation much of the capital outlay for equipment and infrastructure has
already been spent and extending the age range primarily increases the costs
of consumables and staff with a much lesser impact on requirement for
additional equipment, buildings etc.
The psychological impact of
breast cancer screening has yet to be determined. However studies have shown that women are less anxious about
their risk of death from breast cancer having gone through the screening
process than women who have never been invited to screening mammography50.
Certainly the process of screening and of recall and biopsy for some women may
be stressful and highlights the need for any screening service to be properly
run with rapid assessment, information and support for women concerned so that
such stresses can be minimised.
discomfort have been assessed in the Waikato Pilot Programme A randomised survey of
almost 1,000 screening participants ( unpublished
data ) has shown that some 6%
of women 50-64 years of age find mammography painful and a further 10% find it very uncomfortable.
Similar results have been shown in a British study where most women
rated mammography similar to having their blood pressure taken and less
uncomfortable than a venepuncture51. These are the results of
dedicated mammography units and staff and again highlight the need for such
units, along with public education to counter the widespread misconception
that most women find mammography painful.
of normal women: Some six normal women will be recalled for more detailed assessment
including further mammographic workup ± ultrasound ± needle biopsy for each
100 women screened, and 1-2 benign biopsies (most of these needle biopsies
rather than open surgical procedures) will be performed for each cancer
other words, while the number of cancers detected per thousand younger women
screened is lower at 3-4/1,000, the recall rate and the positive predictive
value for surgical intervention are well within established guidelines for
older women53. These
are results from modern quality
breast clinics in the Australian and U.K. settings and are considerably more
specific than figures quoted from the North American environment54.
These are first screening round figures and drop for subsequent rounds.
radiation dose from two view mammography is approximately 0.25 rads.
There is no known risk for induction of breast cancer from this dose
but certainly much higher doses of 100 rads or more as in Hiroshima victims
and women undergoing multiple chest fluoroscopies in the 1920's and 30's for
TB have been shown to cause breast cancer after a latent period of 4-10 years.
Extrapolating risks from these much higher doses it has been predicted
that five breast cancer deaths may occur per million younger women receiving a
single screen26. If
these possible radiation induced cancers were detected by screening at an
early stage this theoretical death rate might be decreased by 20-40%.
On the other hand, a single screen for women in this age group would be
expected to save between 150 and 300 deaths per million women assuming
mortality reductions of 20-40%.
reassurance: For all the potential benefits of screening mammography in any age
group, mammography is an imperfect tool.
Some 4-10% of breast cancers in older women and maybe as many as 20% of
breast cancers in younger women will not show up on mammography.
This needs to be made very clear to women and their GP's to avoid the
false reassurance of a false negative result. It is therefore important that
women continue to practise regular breast awareness see their family
practitioners for any new breast symptom.
Breast self examination for those who practise regularly, does reduce
average size and stage of detection of breast cancer (Prof
R Blamey, personal communication of the Nottingham Trial Results).
Many countries, including Australia, parts of Sweden, Iceland and
Finland already have national screening programmes under way including 40-49
year old women. After careful consideration of the evidence, many other
reputable groups including that US National Cancer Institute and American
Cancer Society and the 2002 review by the United States Preventative Services
Task Force59, all recommend mammography screening for women in
To tell women 40-49 years of age that screening is no good but on
turning 50 years of age it should suddenly become highly effective is a
confusing message. Not only is
nothing being achieved for the younger women but the message may have a
negative impact on compliance for older women where we are all agreed, breast
cancer screening is highly worthwhile.
A broader age range provides a more consistent and easier to administer
This review has concentrated predominately on RCT evidence to avoid
controversies and biases over non-randomised studies. It should be noted however, that there is a large body of
indirect evidence that is also supportive for screening younger women.
There is no doubt screening mammography detects breast cancers at an
earlier stage in younger women, 32,56,57 and
that survival rates for earlier stage breast cancers and screen detected
breast cancers in younger women are just as good if not better than for older
women (these data are however subject to several possible biases: selection
bias, lead and length time bias).
If a National Programme for younger women gets under way, it is
essential that it is of the highest quality.
The CNBSS's14,21 are useful for one thing: these studies
clearly demonstrate that poor quality mammography will at best achieve
nothing, and at worst may cause potential harm.
If a National Programme does not embrace a wider age range than 50-64
years of age, private radiology clinics certainly will and are promoting
screening in this age range, and are currently not subject to any adequate
quality assurance for breast cancer screening. To provide high quality
population based screening requires a national quality controlled approach
together with adequate funding.
The controversy over screening mammography for younger women is now to a
considerable extent resolved. It is clear that from the metaanalyses of RCT's13,28
that offering a population screening mammography reduces the death rate from
breast cancer for all ages at least from 45-70 years and probably from 40-75
modern day screening equipment and knowledge, appropriate quality standards,
two view mammography, an appropriate screen interval and for those women who
attend, we will achieve a considerably greater reduction in breast cancer
mortality than the RCT's indicate. As
breast cancer is the most common cancer in women and breast cancers diagnosed
in this age range account for many of the years of suffering and life lost
from breast cancer it is imperative that the National Screening Programme in
New Zealand is made available to women 40-49 years of age.
TABLE 1: SUMMARY OF RANDOMISED CONTROLLED TRIAL RESULTS FOR WOMEN AGED
Screening Study (Dates)
years of F/U
Breast cancer deaths
2 V MM+CBE
Annually 4 rounds
1 or 2 V MM
18-24 mos, 5 rounds
1 V MM
24 mos, 4 rounds
1 V MM
24 mos, 4 rounds
1 or 2 V MM
24 mos, 4 rounds
1 V MM
28 mos, 2 rounds
2 V MM
18 mos, 4 rounds
2 V MM+CBE
12 mos, 5 rounds
(Adapted from Smart C R, Hendrick R E, Rutledge J H and Smith R A. Benefit of Mammography Screening in Women aged 40-49 years. Cancer 1995; 75; 1619-26.)
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