Disparities in breast cancer mortality trends between 30
European countries: retrospective trend analysis of WHO
Philippe Autier, group head and research director,1,2Mathieu Boniol, biostatistician and senior researcher,1,2
Carlo LaVecchia, professor,3Lars Vatten, professor,4Anna Gavin, director of Northern Ireland Cancer
Registry,5Clarisse He ´ry, researcher,1Mary Heanue, senior researcher1
Design Retrospective trend analysis.
1989 to 2006
Main outcome measures Changes in breast cancer
≥70 years) calculated from linear regressions of log
was used to identify the year when trends in all age
mortality began to change.
in breast cancer mortality of 19%, ranging from a 45%
cancer mortality decreased by ≥20% in 15 countries, and
and Scotland had the second, third, and fourth largest
Finland, and Sweden, mortality decreased by 11%, 12%,
and 16%, respectively. In central European countries
mortality did not decline or even increased during the
period. Downward mortality trends usually started
between 1988 and 1996, and the persistent reduction
from 1999 to 2006 indicates that these trends may
continue. The median changes in the age groups were
−37% (range −76% to −14%) in women aged <50, −21%
(−40% to 14%) in 50-69 year olds, and −2% (−42% to
80%) in ≥70 year olds.
Conclusions Changes in breast cancer mortality after
1988 varied widely between European countries, and the
UK is among the countries with the largest reductions.
mortality, also in countries where screening at that age is
uncommon. The increasing mortality in some central
European countries reflects avoidable mortality.
Since the 1990s, profound changes have taken place in
the clinical presentation and management of breast
cancer due to mammography screening, implementa-
tion of effective hormone treatments and chemother-
apy, and progress in radiotherapy and surgery. These
improvements in breast cancer survival in Europe,12
but the contribution of each factor is unknown. The
ability of new treatments, and healthcare expenditures
vary greatly across Europe.3-7One consequence could
be that mortality decreases between countries will also
vary, and the highest decreases are likely to be
observed in countries characterised by early imple-
mentation and high attendance to breast screening
combined with rapid uptake of anticancer drugs.
In this study we analysed breast cancer mortality in
30 European countries from 1980 to 2006 and exam-
ined temporal trends in rates for all women, and for
women aged <50, 50-69, and ≥70 years to help deci-
pher the effect of the contributing factors.
Breast cancer deaths registered in the World Health
Organization mortality database at December 2009
were extracted for European countries.8The quality
of mortality data has been evaluated by the WHO.9
England and Wales, Scotland, and Northern Ireland
were considered as three separate countries. Cyprus
was excluded as data were available for only four
years (1999, 2000, 2004, and 2006). Malta was not
included because abrupt changes in trends occurred
in 1979 and 1995, which seem to coincide with classi-
fication changes from ICD-8 (international classifica-
tion of diseases, eighth revision) to ICD-9 and from
ICD-9 to ICD-10. For almost all other countries, data
up to 2006 were available, and for some countries,
mortality data for 2007 and 2008 were also available.
In addition to the WHO data, we obtained informa-
tion on mortality statistics for several countries, which
allowed enhancement of quality. For Switzerland, a
change in coding practice in 1994 resulted in an over-
estimation of cancer mortality before 1994, and, as
1International Agency for Research
on Cancer, Lyon, France
Research Institute (iPRI), Lyon,
3Mario Negri Institute and School
of Medicine of the University of
Milan, Milan, Italy
4Department of Public Health,
Norwegian University of Science
and Technology, Trondheim,
5Northern Ireland Cancer Registry,
Queen’s University, Belfast,
Correspondence to: P Autier,
International Prevention Research
69006 Lyon, France
Cite this as: BMJ 2010;341:c3620
BMJ | ONLINE FIRST | bmj.com page 1 of 7
recommended, we therefore applied a correction fac-
tor of 0.85 on rates before 1995.10For Belgium, coun-
try-specific mortality was recorded until 1997, but
thereafter mortality data were available for Flanders
(60% of the population) and for Brussels (10% of the
tion), mortality data were available only for 2004. For
Wallonia, we estimated mortality from 1998 to 2003
and for 2005 by using a linear interpolation calculated
the Brussels region. We subsequently estimated a
national mortality for Belgium using regional rates
weighted by population size.
In Italy for 2004 and 2005, and in Poland 1997 and
1998, we replaced missing data by interpolations
between previous and subsequent calendar years.
Mortality values were adjusted by the age distribution
of the European standard population11to obtain Eur-
opean standardised rates. Because of small popula-
tions, rates in Luxembourg (450000 inhabitants) and
Mortality (age adjusted rate
per 100 000 women)
Mortality (age adjusted rate
per 100 000 women)
Mortality (age adjusted rate
per 100 000 women)
Mortality (age adjusted rate
per 100 000 women)
UK (England and Wales)
Fig 1 | Temporal trends in breast cancer mortality in European countries. Countries have been grouped in graphs according to
percentage change in mortality from 1989 to 2006. (Five-year smoothing was applied on Iceland and Luxembourg rates to
avoid unstable trends because of small population size)
page 2 of 7
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Iceland (320000 inhabitants) were unstable, with
We were most interested in recent trends in mortal-
ity because efficient treatments and breast screening
spread in many European countries in the 1990s.
After logarithmic transformation of rates, we fitted a
linear regression from 1989 until 2006 and from 1999
until 2006. Because of missing data for the later years,
and between 1989 and 2004 for Portugal. From the
slope of each country, we derived the annual percen-
tage change in breast cancer mortality for the periods
1989-2006 and 1999-2006, and the overall percentage
change from 1989 to 2006. We performed these ana-
lyses for women of all ages, and for women aged <50,
50-69, and ≥70.
A systematic analysis of temporal trends in women
of all ages was done by joinpoint regression using the
Joinpoint Regression Program version 3.4.2 from the
Surveillance Research Program of the US National
Cancer Institute.12Joinpoint regression identifies peri-
ods when distinct linear or log-linear trends are sepa-
joinpoint regression on data from 1960 onwards (or
from the earliest available data after 1960) until the
last year of available data.
Table 1 |Changes in breast cancer mortality between 1989 and 2006 in European countries ranked according to overall decline in mortality
Mortality change for all ages (%) Mortality change 1989-2006 by age group (%)
Annual changeOverall change
1987-92004-6† Annual Overall<5050-69
England and Wales41.9 28.1
Northern Ireland 37.0 28.1
Spain 23.7 18.9
Denmark 40.5 32.0
Czech Republic 30.626.4
1994 0.5 8.6Medium
Sweden 25.6 22.0
None0.8 14.6 Low
20001.1 20.5 High
Bulgaria 21.322.2 0.0
Estonia20.9 23.6 0.59.6 NR
Latvia22.525.1 0.611.4 NR0.0
Romania19.923.1 0.916.6 NR 0.0
Maximum41.932.0 0.916.6 NR 1.1
0.8 3.514.380.2 NR
NA= not available; NR=not relevant.
*Age adjusted (European standard) rate per 100000 women.
†Data for 2004-5 for Spain, Hungary, Slovakia, and Estonia; data for 2004 for Belgium; data for 2006 for Italy; 2003 was the last year of data for Portugal.
‡By joinpoint analysis, year of statistical significance at P<0.05 (two sided).
§Quality of information on cause of death according to WHO (from Mathers et al9).
¶Mortality values before 1996 were decreased by 15% (as recommended by Lutz et al10).
BMJ | ONLINE FIRST | bmj.com page 3 of 7
Overall changes in breast cancer mortality
Figure 1 and the table show the changes in breast can-
cer mortality in 30 European countries from 1989 to
2006. Over the 18 years, mortality declined by a med-
ian of 19%, with individual values ranging from a 45%
reduction in Iceland to a 17% increase in Romania.
The decrease was >30% in three countries, 20%-30%
in 12 countries, and in four countries breast cancer
mortality continued to increase.
In the 15 countries where mortality declined overall
by ≥20% the decrease started before 1996, except in
Germany, where the decline started in 1999. In Swe-
cancer mortality since 1972, without a further join-
When the 18 year mortality changes were plotted
against the mean breast cancer mortality in 1987-9
(fig 2), countries with high mortality in 1987-9 tended
to have greater reductions in mortality. However, the
ity >35 per 100000 in 1987-9, decreases ranged from
20% in Belgium to 35% in England and Wales. In sev-
eral countries with mortality in the range of 23-40 per
100000 in 1987-9, there were also substantial reduc-
tions in breast cancer mortality—such as 27% in
tions in Finland, France, and Sweden were 12%, 11%,
and 16%, respectively.
decline tended to slow during the last eight years of
observation. In most other countries, declines after
1998 tended to be more pronounced than for the
erate mortality reductions, however, declines between
1999 and 2006 were less pronounced or even absent,
notably in Sweden and Poland. In several central Eur-
decline after 1998.
With time, breast cancer mortality values for differ-
ent countries seemed to converge. In 1987-9 mortality
(per 100000) ranged from 19.9 in Romania to 41.9 in
6 mortality ranged from 18.9 in Spain to 32.0 in Den-
mark (difference 13.1).
Changes in breast cancer mortality by age group
Reductions in mortality were most marked in women
aged <50 years (median change −37% (range −76% to
−14%), and reductions of 14% or more were observed
in all 30 countries. Reductions in women aged 50-69
were similar to those observed in women of all ages
(−21% (−40% to 14%). The median change in women
aged ≥70 was −2% (−42% to 80%), with breast cancer
mortality continuing to increase in 17 countries. In
countries where a mortality reduction could be
observed among older women, these reductions were
related differences were particularly noticeable in cen-
tral and eastern European countries.
This study shows substantial differences between Eur-
opean countries in temporal trends of breast cancer
mortality, as well as differences in mortality changes
with age. The sustained decline observed in many
countries after 1999 seems to indicate that breast can-
cer mortality will continue to decrease beyond 2006.
The convergence of annual mortality rates among
countries over time was noticed in 20002and could
be due to diminishing marginal returns because the
countries with the highest mortality in the late 1980s
simply had more opportunity for relative change over
Strengths and limitations of study
The cause of death reported in national statistics may
be of limited reliability, and WHO quality indices dis-
played in the table indicate that, for all causes of death
combined, data from Greece, Poland, and Portugal
should be considered with caution. However, deaths
caused by breast cancer may be more reliable than
for several other cancers.1314It is possible that some
changes in breast cancer mortality trends could be
due to changes in coding practices. This problem was
aware of similar problems in other European coun-
tries, and therefore, we are confident that our results
do reflect real trends.
Comparison with other studies
study on survival of breast cancer.15The cancer policy
of the UK National Health Service has been under
scrutiny after the publication of the EUROCARE
reports.1617These reports showed that five year rela-
tive survival of cancer patients in the UK (mainly
Mean mortality in 1987-9 (age adjusted rate per 100 000 women)
AT=Austria; BE=Belgium; BG=Bulgaria; CH=Switzerland; CZ=Czech Republic;
DE=Germany; DK=Denmark; EL=Greece; EE=Estonia; ES=Spain;
EW=England and Wales; FI=Finland; FR=France; HU=Hungary; IC=Iceland;
IE=Republic of Ireland; IT=Italy; LT=Lithuania; LU=Luxemburg; LV=Latvia;
NI=Northern Ireland; NL=Netherlands; NO=Norway; PL=Poland; PT=Portugal;
RO=Romania; SC=Scotland; SE=Sweden; SI=Slovenia; SK=Slovakia
Percentage change in mortality 1989-2006
Fig 2 | Percentage changes in breast cancer mortality in
European countries during 1989-2006 according to the mean
breast cancer mortality in 1987-9
page 4 of 7
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melanoma) was lower than in neighbouring countries
that the lower survival of breast cancer patients in the
UK could be due to delay in licensing new drugs.618
While mortality and survival data have their limita-
tions, mortality statistics are indicative of long term
trends, whereas the survival statistics can be severely
biased by changing trends in the incidence of small
when screening is widespread. Between 1990 and
2002, breast cancer incidence increased by 20%-48%
in most countries where five year relative survival was
estimated to be ≥80%.151920In the UK and Scotland,
the increases in incidence were 16% and 13%,
Hence, survival differences mainly stem from the
higher incidence of breast cancer in countries with
higher survival.21The substantial increase in breast
cancer incidence observed after 1990 in many Eur-
opean countries was partly due to advances in diagno-
sis (lead time) and to increasing detection of non-
progressive or slowly progressing tumours with no or
weak life threatening potential (length time).22Lead
time and length time were to a large extent introduced
by screening activities that led to increasing incidence
of early stage breast cancers.23-25Lead time and length
time biases will spuriously modify survival even in the
absence of a change in mortality.21Differences in sur-
vival may therefore reflect differences in screening
intensity, and not reductions in mortality. Therefore,
the UK NHS cancer policy was successful in reducing
breastcancer mortality,and theratherbleakpicture of
UK cancer policy portrayed using breast cancer survi-
val is likely to be erroneous.
Interpretation of results
At least four factors may explain the considerable var-
iations in breast cancer mortality between European
countries. Firstly, mortality levels at the end of the
1980s could have influenced some of the relative dif-
ferences in mortality reductions, but they cannot
account for a large part of variations between coun-
Secondly, the incidence of breast cancer has
increased in most European countries over the past
20 years,1920resulting in doctors mentioning breast
cancer more frequently as the cause of death. Also, in
populations with a substantial increase in cancer inci-
dence moreadvancedcancers may have occurred that
have probably attenuated the mortality decline. The
sharp increases in incidence observed after 1985 in
many white populations were mainly due to the com-
bined effects of changes in reproductive factors, over-
weight and obesity, screening mammography, and
hormone replacement therapy.26-28Most of these fac-
tors do not have the same impact on risk of breast can-
cer as on death from breast cancer.29For instance,
breast screening is deemed to reduce breast cancer
mortality, but it also increases the incidence of cancers
with low aggressive potential.2530-33Also, a closer look
at both incidenceand mortalitydata in a large number
of countries with national cancer registries shows that
there is only a weak association between changes in
incidence and changes in mortality.1920
Thirdly, breast screening is expected to decrease the
median size of breast cancers, resulting in steadily ear-
ever, unclear whether the reductions in median breast
cancer size observed since the 1980s result from a gen-
eral decrease in size, with concomitant decrease in the
incidence of advanced cancer, or rather from the
increasing incidence of small, early cancers that would
give the overall impression of downsizing.2336-38
Fourthly, adoption of efficient treatment regimens
and reorganisation of health services that encourages
a multidisciplinary approach and high volume specia-
lised breast cancer clinics may have benefited women
irrespective of whether their cancer was detected by
screening. Few European countries, however, have
published time trends in hormone therapy and che-
tion on breast cancer management.39-45Recently
published data comparing spending on new cancer
drugs and their uptake6do not assess treatment efforts
specific to breast cancer, including changes in non-
therapy management). Mortality reductions started
and hormone therapy.46Similar reductions in mortal-
ity were observed in women aged <50 years in coun-
tries where screening of young women has been rare
(Denmark, UK, Netherlands, Norway, Finland) and
where it is common (Sweden, France, Germany).3-48
Hence, the particularly larger reduction in mortality
in women <50 years old may reflect better targeting
of effective treatments and response to treatments.
cancer mortality seen in women ≥70 years old may be
due to lower awareness, more frequent diagnosis of
cancer at an advanced stage, and less intensive treat-
ment of cancer.4049-52
Conclusions and policy implications
The largest decreases in mortality were expected in
countries that combined high mortality in the late
ing early in the 1990s, rapid adoption and easy access
to new treatments, and restructuring of medical ser-
vices towards high volume specialised breast clinics
and multidisciplinary management. Data on all these
factors have been published for the UK, showing high
screening coverage of women aged 50-64 after 1995,53
and adjuvant chemotherapy by UK doctors,5455and
the reorganisation of breast cancer services on the
basis of the Calman-Hine and Campbell evaluation
At the other end of the spectrum, in central Eur-
opean countries the small decreases or the continued
increase in breast cancer mortality were correlated
with low, usually non-organised, screening activities,3
BMJ | ONLINE FIRST | bmj.com page 5 of 7
low numbers of mammography machines,7slow
uptake of anticancer drugs,6and health expenditures
below the European average.59These epidemiological
patterns may also be linked to rapid changes in breast
cancer risk factors that took place in these countries
after the collapse of the communist regimes in the
1990s, such as decreasing fertility and increasing age
at first birth.60
devoted to combating breast cancer. For instance, the
decline in breast cancer mortality in France has been
quite modest despite this country having one of the
highest number of mammography units per million
women,7having the highest spending on cancer
drugs per person in Europe,6being at the forefront in
use of new costly treatments,6and devoting much
effort to enhancing adherence to guidelines.61
In Sweden, the 16% decrease in mortality between
1989 and 2005 includes reductions obtained with
screening, treatments, and system efficiency, and this
decrease has remained stable since 1972. Observa-
tional studies that included about 60% of the Swedish
female population have shown that screening alone
by25%-30%in allwomen≥40 yearsold.6263Giventhe
these results and given that breast screening was also
vational studies, one would have expected a better
match between mortality statistics and the results
from these studies.
ing the strong variations in breast cancer mortality in
Europe. Efforts should be made to reduce the avoid-
Contributors:Study concept and design: PA. Data collection: PA, MH, MB.
Data analysis: PA, CH, MB. Data interpretation: all authors. Writing of
manuscript: PA, CLV, AG, LV. Editing of final version and approval for
submission: all authors. PA is the guarantor of the study.
Funding:Institutions in which authors work had no influence in the
conduct of the research or in the writing of the paper. The work of the
Northern Ireland Cancer Registry is funded by the Public Health Agency
for Northern Ireland
Competinginterests:All authors have completed the Unified Competing
Interest form and declare no financial or non-financial interests that may
be relevant to the submitted work.
Datasharing:The WHO mortality database is available at www.WHO.int.
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WHAT THIS STUDY ADDS
Themajordecreasesinbreastcancer mortalityobservedinthe UKweremore markedthanin
most European countries and were only partly linked to high mortality at the end of the
Mortality dataare a more realistic measure ofsuccessfulcancer control thancancer survival,
as the latter is influenced by changes in cancer incidence
Some countries, such as France and Sweden, have mobilised large resources on screening
and acquisition of cancer drugs but have shown little change in breast cancer mortality
Breast cancer mortality is still increasing in several central European countries, representing
avoidable cancer deaths
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Accepted: 21 May 2010
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