Document 4008

parkin
Original
Global
Breast
and
Article
fernández
Cancer
Statistics
Blackwell
Malden,
The
TBJ
1075-122X
January/February
12
12006
suppl
Breast
Blackwell
USA
Publishing
Journal
Publishing
2006
Inc
ORIGINAL ARTICLE: GLOBAL EPIDEMIOLOGIC METHODS
Use of Statistics to Assess the Global Burden of
Breast Cancer
D. Maxwell Parkin, MD, MFCM, MRCP* and Leticia M. G. Fernández, MD, PhD†
*Clinical Trials Service Unit and Epidemiological Studies Unit, University of Oxford, Oxford, United
Kingdom; and †National Institute of Oncology, Havana, Cuba
■ Abstract: A variety of statistics are used to quantify the burden (occurrence and outcome) of cancer generally and of breast cancer
specifically. When undertaking any cancer control program, understanding these statistics, their source, and their quality is important
for assessing the current situation, allocating resources to different control strategies, and evaluating progress. Two core statistics are
the cancer incidence rate and the cancer mortality rate, which provide estimates of the average risk of acquiring and of dying from
the disease, respectively. About 16% of the world’s population is covered by registration systems that produce cancer incidence statistics, while mortality data are available for about 29%. Breast cancer incidence and mortality vary considerably by world region. In
general, the incidence is high (greater than 80 per 100,000) in developed regions of the world and low (less than 30 per 100,000),
though increasing, in developing regions; the range of mortality rates is much less (approximately 6–23 per 100,000) because
of the more favorable survival of breast cancer in (high-incidence) developed regions. The incidence of breast cancer is increasing
almost everywhere. This unfavorable trend is due in part to increases in risk factors (decreased childbearing and breast-feeding,
increased exogenous hormone exposure, and detrimental dietary and lifestyle changes, including obesity and less physical activity). On
the other hand, mortality is now decreasing in many high-risk countries due to a combination of intensified early detection efforts and the
introduction of mammographic screening, resulting in the diagnosis of more small, early stage tumors, and advances in treatment. Key Words: breast cancer, burden of illness, health care evaluation mechanisms, health planning, outcomes assessment,
program evaluation, registries, resource allocation, statistics
S
everal statistics are used to quantify the burden
(occurrence and outcome) of cancer generally and of
breast cancer specifically. Understanding these statistics,
their source, and their quality is important for the planning
and evaluation of cancer control programs. In this article
we review the core statistics commonly used for planning
and assessing the effectiveness of a cancer control program,
the strengths and limitations of selected statistics, and the
key sources of global cancer statistics. In addition, we
discuss regional differences and temporal trends in
breast cancer incidence and mortality, as well as possible
explanations for the observed patterns.
CORE STATISTICS FOR ESTIMATING CANCER
BURDEN
Although the general idea of the burden of a disease
such as cancer to a community seems fairly straightforward,
there are multiple dimensions in which it may be
expressed.
Incidence
Cancer incidence is the number of new cancer cases
occurring in a specific population during a period of time.
It can be expressed as an absolute number of cases per year
(the volume of new patients presenting for treatment) or
as a rate per 100,000 persons per year. The latter provides
an approximation of the average risk of developing a
cancer. Because the risk of cancer is strongly related to
age, comparison of the risk of cancer among populations
(e.g., countries, ethnic groups, or populations at different
time periods within a country) may use age-standardized
incidence rates to allow for the effect of differences in their
age structure (1). When evaluating the impact of primary
prevention strategies, a reduction in incidence (occurrence
of new cases) is the appropriate statistic to use.
Mortality
Address correspondence and reprint requests to: D. Maxwell Parkin, MD,
MFCM, MRCP, Visiting Consultant, Clinical Trials Service Unit and
Epidemiological Studies Unit, University of Oxford, Oxford OX3 7LF, United
Kingdom, or e-mail: [email protected]
©2006, The Fred Hutchinson Cancer Research Center, 1075-122X/06
The Breast Journal, Volume 12 Suppl. 1, 2006 S70– S80
Cancer mortality is the number of deaths occurring due
to cancer, and the cancer mortality rate is the number of
deaths due to cancer per 100,000 persons per year in a
defined population. The number of deaths provides one
measure (and a rather unambiguous one) of the outcome
Global Breast Cancer Statistics • S71
or impact of cancer. It is the product of the incidence and
the fatality of a given cancer. Fatality, the inverse of
survival, is the proportion of cancer patients that die. The
cancer mortality rate therefore measures the average risk
to the population of dying from a specific cancer, while
fatality (1 − survival) represents the probability that an
individual with cancer will die from it. Mortality rates are
frequently used as a convenient proxy measure of the risk
of acquiring the disease (the incidence rate) when comparing different populations or groups because they may be
more generally available (as described below). However,
such use introduces an assumption of equal survival/
fatality in the populations being compared. This may be
reasonable for cancers with poor survival rates (liver,
lung, esophagus), but for breast cancer, for example, there
are quite large variations in survival between countries
and over time. It is safer therefore to use mortality as a
measure of outcome rather than occurrence.
Prevalence
Prevalence refers to the proportion (or percentage) of
the population that has the disease in question at a given
point in time. For cancer, this sometimes refers to individuals who have developed a cancer at some time in their life
(1). However, this definition includes as cancer cases those
who are cured of the disease, and it is not particularly useful for health care planning purposes. Partial prevalence,
which limits the number of patients to those in whom
cancer was diagnosed during a fixed time in the past, is
therefore a more practical measure of cancer burden (2).
The prevalence of cases diagnosed within 1, 3, and 5 years
is likely to be of relevance to the different stages of cancer
therapy, namely, initial treatment (1 year), clinical followup (3 years), and cure (5 years). Patients who are still alive
5 years after diagnosis are usually considered cured, since
for most cancers, the death rates of such patients are similar
to those of the general population. Breast cancer is a notable
exception, however, as the risk of death remains higher
than that of the general population for many more years.
These involve a further weighting (between 0 and 1) of
the years of life lived between diagnosis and death, reflecting the quality of these life-years (where 0 = dead and
1 = perfect health). Such estimates require a lot of data on
incidence and duration of disease, as well as a lot of guesswork
about quality of life in different circumstances and cultures.
Survival
The survival time of a patient with cancer is defined as
the time that elapses between diagnosis and death. The
most basic measure of patient survival is the observed
survival. The 5-year observed survival is the probability
for an individual of survival at 5 years from the date of
diagnosis. Not all deaths among cancer patients will, however, be due to the primary cancer in question. Deaths from
other causes reduce the observed survival and preclude
comparison between groups for which probabilities of
death in the general population vary. This problem is
avoided by the use of relative survival—the observed survival in a patient group divided by the expected survival
of a comparable group in the general population with
respect to age, sex, and calendar period of investigation.
INTERNATIONAL CANCER STATISTICS
Sources
The sources of information on international cancer
incidence, mortality, and survival have been summarized
by Parkin and Bray (3). Incidence data derive from
population-based cancer registries. Registries cover about
16% of the world population, although the distribution is
very uneven by region (Table 1). Cancer incidence data from
Table 1. Percentage of the Population Covered by
Incidence and Mortality Registration Systems in
Various World Regions
Incidence (% covered)
Life-Years Lost
Several other more complex statistics have been used
to measure the impact of cancer, particularly in health
economics. Person-years of life lost (PYLL) quantifies the
years of normal life span that are lost due to deaths from
cancer, and the years of life lost (YLL) may be weighted
according to age, so that, for example, a year saved at age
20 is valued more highly than one at age 60. A further
refinement is to calculate disability-adjusted life-years
(DALYs) or quality-adjusted life-years (QALYs) lost.
Region
Africa
North America
Latin America and
Caribbean
Japan
Asia (other)
Europe
Oceania
World total
Based on registries
in CI5 vol. VIII
Based on
all registries
Mortality
(% covered)
1
32
3
8
99
10.5
0.1
99
50
12.7
4.7
26.2
82
8.1
19.6
7
36.5
86
16.3
100
8.6
98.3
84
28.7
CI5 vol. VIII, Cancer Incidence in Five Continents, vol. VIII (4).
S72 • parkin and fernández
registries meeting stringent quality criteria (of completeness
and validity) are included in the series Cancer Incidence
in Five Continents (4). Cancer registries also produce survival statistics, and population-based figures have been
published from many developed countries; for example,
the Surveillance, Epidemiology, and End Results (SEER)
program comprising 14 cancer registries covering 26% of
the U.S. population (5) and the EUROCARE-3 project
covering 12 countries of Europe (6). Survival data from
populations in China, the Philippines, Thailand, India, and
Cuba have been published by Sankaranarayanan et al. (7).
Statistics on cancer mortality are derived from the information on death certificates, which are collected by civil registration systems that record vital events (births, marriages,
deaths). National-level mortality statistics are collated and
made available online by the World Health Organization
(WHO) (http://www3.who.int/whosis); this source also
provides tables of estimated coverage and completeness of
the data from the different countries. Mortality data are
available for about 29% of the world’s population (Table 1).
Estimation
Cancer incidence and mortality data are available for
only a small number of the world’s countries, and estimation procedures are required to obtain a comprehensive
global picture of the cancer profile and its evolution
over time. In its GLOBOCAN estimates, the International
Agency for Research on Cancer prepares national estimates
of incidence, mortality, and prevalence of cancer that
uses all available sources of information from the different
countries. The level of accuracy depends on the extent
and quality of locally available data. The most recent
country-level estimates have been provided for 24 different
cancers and 5 broad age-groups in GLOBOCAN 2002.
These estimates are available on CD-ROM (8) and, in a
format allowing rather less flexibility for analysis and
presentation, on the Internet (http://www.dep.iarc.fr/
globocan/globocan.html).
REGIONAL VARIATIONS IN BREAST CANCER
INCIDENCE AND MORTALITY
Breast cancer is by far the most common cancer of
women, comprising 23% of all female cancers, and there
were an estimated 1.15 million new cases in 2002 (9). It
ranks second overall when both sexes are considered.
More than half of all cases occur in industrialized countries—
about 361,000 in Europe (27.3% of cancers in women)
and 230,000 in North America (31.3%). Incidence rates
are high in most of the developed areas of the world
(except for Japan, where breast cancer is third after
colorectal cancer and stomach cancer), with the highest
age-standardized incidence in North America (99.4 per
100,000) (Fig. 1). Within the United States, certain populations, such as white women in California and Hawaiian
women, have age-adjusted rates of 100 per 100,000 or
higher (4). In part, the high incidence in the more affluent
world areas is likely due to the presence of screening programs that detect early invasive cancers, some of which
would otherwise have been diagnosed later or not at all
(10). The incidence is more modest in eastern Europe,
South America, southern Africa, and western Asia, but
breast cancer is still the most common cancer of women
in these regions. In contrast, low rates (less than 30 per
Figure 1. Breast cancer incidence rates
worldwide according to GLOBOCAN 2002
(18). Rates are age-standardized (world
standard) rates (per 100,000).
Global Breast Cancer Statistics • S73
100,000) are found in most African and Asian populations,
although they are increasing; in some Asian populations,
they are already the same as in southern Europe, and in
others (e.g., the Philippines), they are even higher. The
incidence in the Jewish population of Israel is especially
high (87.1 per 100,000). The lowest incidence internationally is in central Africa, where the age-standardized
rate is 16.5 per 100,000.
The prognosis of breast cancer is generally rather good,
so that this cancer ranks as the fifth cause of death from
cancer overall, although it is still the leading cause of
cancer mortality in women (the 411,000 annual deaths
worldwide represent 14% of female cancer deaths). The
very favorable survival of breast cancer cases in western
countries—for example, 89% at 5 years in cases registered
by the U.S. SEER program in 1995–2000 (5)—is also in
part a consequence of the presence of screening programs.
Because of the very favorable survival of breast cancer
in the more affluent developed countries and the poor survival in some of the least affluent developing countries,
differences in mortality rates worldwide are much less
marked than differences in incidence rates (Fig. 2). The
estimated mortality rates in Africa and the Pacific
Figure 2. Breast cancer incidence and
mortality rates per 100,000 by region or country.
Reprinted with permission from Parkin et al. (21).
Copyright 2002, Lippincott, Williams and
Wilkins.
(Micronesia and Polynesia), for example, are not greatly
inferior to those in Europe.
The combination of its high incidence and relatively
good prognosis make breast cancer the most prevalent
cancer in the world today; there are an estimated 4.4 million women alive in whom breast cancer was diagnosed
within the last 5 years (compared with just 1.4 million survivors—male and female—from lung cancer). It has been
estimated that 1.5% of the U.S. female population are
survivors of breast cancer (11).
EXPLAINING REGIONAL VARIATIONS IN BREAST
CANCER INCIDENCE
Genetic factors, including the major susceptibility
genes (BRCA-1, BRCA-2), may account for up to 10% of
breast cancer cases in developed countries (12), but their
prevalence in the population is too low to explain much
of the international or interethnic variation in risk. Most
must therefore be a consequence of different environmental exposures. This is clear from studies of migrants,
which show quite clearly that incidence changes following
migration; for example, an increase in the risk of breast
S74 • parkin and fernández
cancer in populations from European countries at relatively low risk (Italy, Poland) occurs after migration to
Australia, particularly if they migrate as children (13,14).
Furthermore, studies comparing the risks in migrants and
their offspring (particularly among Asians migrating to
the United States) demonstrate that there are major increases
in risk between first, second, and third generations (15).
The major influences on breast cancer risk appear to be
certain reproductive factors (low parity, late age at first
pregnancy), larger body size/obesity, and less certainly,
diet (16). There have, however, been few attempts to
quantify the magnitude of risk differentials between
populations that might be explained by such factors.
Internationally there is some association between national
incidence (or mortality) rates of breast cancer and population averages for various variables related to fertility
(17) or body weight (18). However, such models can explain
only a minor component of the variation in incidence. In
the United States, Brinton et al. (19) calculated that the
difference in incidence between whites and blacks, at
least among women age 40–54 years (20%), was entirely
explicable in terms of the different prevalences of certain
reproductive and lifestyle variables.
REGIONAL TRENDS IN BREAST CANCER
INCIDENCE AND MORTALITY
The changing profile of breast cancer incidence and
mortality among populations in each world region, and
within populations over time, has been recently reviewed
by Bray et al. (20).
Europe
In countries where national screening programs started
in the mid- to late 1980s (the Nordic countries, England,
Wales, and The Netherlands), incidence rates were increasing at an annual rate of 1–3% before organized screening
activity began (Fig. 3) (21). In several countries, such as
England and Wales (22) and Sweden (23), a screeningrelated increase—a short-duration “bump” in the incidence
curve—can be seen in the age groups being screened as a
result of the detection of prevalent cancers during the first
screening round. Quite substantial increases in incidence
(greater than 2% per year) up to the mid-1990s were also
seen in several countries where there was no national program, or where screening was very limited (e.g., Spain and
Slovakia) (Fig. 3). Annual increases of 2–4% per year have
been reported for the incidence of breast cancer in the
former Soviet Union between 1971 and 1987 (24).
The most recent data indicate some signs of a slowdown or leveling off of the increase in incidence in several
countries since the mid-1990s, particularly in The
Netherlands, Sweden, and England and Wales (21). This
may be a result of a cohort-specific peak in incidence (25),
although the observations are also consistent with what
would be expected after the initial breast screening round:
a decline after the postscreening increase to a level slightly
higher than that before screening (26).
Figure 3. Breast cancer incidence rate in
selected European and Scandinavian countries.
ASR, age-standardized rate (world standard)
(per 100,000). CI5, Cancer Incidence in Five
Continents.
Global Breast Cancer Statistics • S75
Mortality in most countries has increased from the
1950s until at least the 1980s, particularly in countries of
eastern and southern Europe. A leveling off and subsequent decline in breast cancer mortality from the early
1990s is now evident in several other European countries
(21), although the declines are often confined to women
younger than 50 years of age (Fig. 4).
Some recent decreases in mortality are also evident in
several countries that do not have national screening
programs, although these tend to be confined mainly to
younger age groups. Mortality is still increasing in several
eastern European or former Soviet countries, where rates
were relatively low in the past (Russian Federation, Estonia,
Romania, and Hungary).
North America
The pattern observed in the United States and Canada
is broadly similar to that in Europe, with increases in incidence among both white and black women (Fig. 5) (27).
Most of this increase occurred in the period between 1980
and 1987 (5) and is related to increases in mammographically detected incident cases as a result of the intensification
of breast screening at this time (28). The overall rate of
increase has slowed to 0.6% per year since the late 1980s
(29).
The leveling off in mortality and subsequent decline
noted in several northern European countries in the 1980s
was also observed in both the United States (30) and
Figure 4. Percentage change in breast cancer mortality in selected countries. (For China, the earlier period is 1988 – 1990; for Argentina, the later
period is 1994 –1996.) Countries are sorted in descending order of the magnitude of the change. Source of data: http://www.dep.iarc.fr/. Reprinted
with permission from Bray et al. (32). Copyright 2004, BioMed Central Ltd.
S76 • parkin and fernández
Figure 5. Breast cancer incidence rates in
Canada, the United States, Japan, and Australia.
SEER, Surveillance, Epidemiology, and End
Results; ASR, age-standardized rate (world
standard) (per 100,000); CI5, Cancer Incidence
in Five Continents.
Canada (31), and the extent of the decrease in both
younger and older women is shown in Figure 4. Since the
mid-1980s, the trends in U.S. whites and blacks have
diverged, with white women experiencing a leveling off
and subsequent decline in mortality from the early 1990s,
but black women experiencing a slight increase in mortality
throughout the same period (27).
Australia and New Zealand
The incidence of breast cancer in New South Wales
(representing about one-third of Australian women)
increased steadily from the early to mid-1980s (Fig. 5),
and by 1995 was nearly 50% higher than in 1983. The
greatest increase was in the target age group for mammography screening (50–69 years), which became available
in 1984 on a limited basis and in 1992 was nationwide and
accessible to all women at least 40 years of age (32). In
New Zealand, there were steady increases in incidence
rates among both Maori and non-Maori women from
1978 to 1992 (33).
Breast cancer mortality in Australia rose steadily from
the early 1970s to the late 1980s (34). Between 1985 and
1989 and 1990–1994, breast cancer mortality fell by
3.2% among women 50–69 years of age and by 4.2%
among women 25–49 years of age, with little change
(−0.2%) among older women (34). The proportion of
women screened in all age groups increased substantially
between 1988 and 1994, and by 1994 nearly 65% of women
in the target age group had had at least one mammogram
(34).
Japan
Although breast cancer remains relatively rare in
Japan, the incidence (Fig. 5) and mortality (Fig. 4) have
been increasing quite rapidly, which is consistent with
increasing risk in successive generations of women (35).
The overall incidence has been increasing since the
mid-1970s (35,36), although the increase has been much
larger than that for mortality, demonstrating improving
prognosis over time (35).
Developing Countries
There are few data from developing countries, but
where they are available, increases in breast cancer incidence and mortality are seen, an observation often more
apparent within recent birth cohorts (37), and a probable
consequence of the adoption of western lifestyles (38).
Latin America. Most Latin American countries have
intermediate rates of breast cancer occurrence. Incidence
Global Breast Cancer Statistics • S77
and mortality rates have been observed to be increasing in
most countries (38); incidence has at least doubled, for
instance, in Cali, Colombia (Fig. 6), and in Puerto Rico
between the early 1970s and the mid-1990s. In Uruguay,
Argentina, and Chile, women are at high or intermediate
risk, and mortality rates in younger women have been
reported to be more or less constant over time (37).
Asia. The age-adjusted incidence is low in most Asian
countries, although world-standardized rates are greater
than 50 per 100,000 in Manila, Philippines, and in
Karachi, Pakistan. Rates in Singapore, particularly
among the Chinese population, are also relatively high for
the region. Rising incidence has been observed in India
(39) and also in Singapore (40) (Fig. 6). In China, breast
cancer mortality increased during the period 1987–1999
in both rural and urban areas, with a more marked rise
among rural women, although the rates have remained
lower than those among urban women (41). Substantial
increases are reported also in Taiwan between the 1960s
and 1990s (42), and in Hong Kong (43).
Africa. In Africa as a whole, breast cancer is less common
than cervical cancer (8); however, it is the most common
malignancy in North Africa and in urban populations in
Figure 6. Breast cancer incidence rates in
selected developing countries in Latin America
and Asia. ASR, age-standardized rate (world
standard) (per 100,000); CI5, Cancer Incidence
in Five Continents.
sub-Saharan Africa (44). Few datasets are available for the
study of time trends in Africa, but some increases in incidence are apparent, for example, in Ibadan, Nigeria (44),
and in Kampala, Uganda (45), between the 1960s and the
late 1990s. Steady increases in breast cancer mortality
rates of the same order of magnitude have also been noted
from the early 1960s in Mauritius (44).
EXPLAINING REGIONAL TRENDS IN BREAST
CANCER INCIDENCE AND MORTALITY
In general, the largest increases in breast cancer risk
have been seen in populations of women historically at
lowest risk, often within developing countries, whereas
relatively recent departures from the long-term upward
trend have been observed in several, mainly western
countries. In contrast, as described above, there have been
declines in mortality rates from breast cancer in several
developed countries in Europe, North America, and
Australia and New Zealand, dating from around 1990
(Fig. 7). A variety of factors are contributing to these trends.
Changes in Risk Factors
Changing patterns of childbearing and breast-feeding,
of exogenous hormonal exposure, and of lifestyle factors
S78 • parkin and fernández
Figure 7. Breast cancer mortality rate in six
countries, 1960–2002. Rates are agestandardized rates (world standard) per
100,000 at ages 45 – 74 years. UK, United
Kingdom.
including obesity, alcohol consumption, and reduced physical activity have certainly contributed to trends in incidence
and mortality. Earlier menarche and later menopause
associated with better nutrition and greater body weight,
resulting in an increasing lifetime length of exposure to
endogenous estrogen, are consistent with upward trends
in the incidence of breast cancer, particularly in developed
countries.
Early Detection and Mammographic Screening
Mammographic screening for women age 50–69 years
is effective in reducing breast cancer mortality, and reductions in mortality have been observed where screening
has been introduced (46,47). Evidence that at least part of
this decline can be attributed to screening comes from the
expected increase in incidence of early stage and in situ
breast cancers, followed by a decline in the incidence of
advanced cancers and in subsequent mortality in the
United Kingdom, northern Europe, and Australia (48–
51). It has been estimated that about one-third of the overall 21% reduction in breast cancer mortality in the United
Kingdom by 1998 (10 years after screening began) was
due directly to screening (52), although the time lag before
any benefits from screening can be expected (53), together
with the reduction in mortality resulting from notable
advances in treatment (discussed below), makes quantification of the contribution of each of these factors
problematic. Part of the beneficial effect of screening is
probably due to a shift toward earlier diagnosis of breast
cancer as a consequence of better awareness of the disease
following the extensive publicity surrounding the breast
cancer and its prevention.
Improved Treatment and Management
Reductions in mortality before the introduction of
screening, and in those countries without screening,
suggest that improvements in disease treatment and
management might be responsible for observed declines
in mortality (53,54). In the United Kingdom (55) and
Finland (49), the rapid decline in mortality rates was
probably due in part to an increased use of tamoxifen
among postmenopausal women with node-positive disease.
The Early Breast Cancer Trialists’ Collaborative Group (56)
reported in a meta-analysis of 55 randomized adjuvant trials that tamoxifen reduced the incidence of contralateral
breast cancers by 47% at 5 years. It is likely that the
increasing use of this antiestrogen has contributed to
decreases in mortality from breast cancer in women with
estrogen receptor-positive tumors in developed countries
during the 1990s (57). However, it has been suggested
that the absolute benefit is more modest (58), because
most trials reported on women with estrogen receptorpositive tumors who had early disease, whereas about
one-third of women have tumors that are negative for this
Global Breast Cancer Statistics • S79
receptor, and many women with breast cancer do not
present with early disease.
Additional factors that have likely contributed to the
decline in mortality, as noted in the United Kingdom, have
been the establishment of treatment protocols, improvement in chemotherapeutic options, and development of
better therapeutic guidelines (52). Specific structural
changes that have embraced the specialization of breast
cancer care (such as centralized treatment, adjustments in
clinician workload, and use of multidisciplinary teams)
have been shown to improve outcome (59).
CONCLUSION
Existing data confirm the magnitude of the problem of
breast cancer—the number one cancer of women worldwide. Although the introduction of screening programs
has perturbed the preexisting trends in incidence (by
bringing forward the date of diagnosis), they do not disguise the steady increase in risk of breast cancer almost
everywhere. Combating this will be difficult: primary
prevention strategies require changes in lifestyles that
run counter to the aspirations of the majority of women
worldwide. Fortunately many countries with a high risk of
breast cancer have achieved something of a triumph as far
as improved outcome (better survival and decreased
mortality) is concerned. The data on stage of disease at
diagnosis, survival, and mortality suggest that this is the
consequence of earlier diagnosis of clinically detectable
cancers, detection of nonpalpable lesions by mammography, and improved treatment with hormonal therapy and
chemotherapy. How much more improvement is possible
with this combination in these countries is unclear, but it
clearly offers room to reduce the mortality and morbidity
in countries in which the epidemic of breast cancer is
still emerging. The intelligence derived from statistical
information systems is an important component of breast
cancer control programs everywhere.
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groot
Original
Cost-Effectiveness
et al.
Article
of 2006
Breast
Blackwell
Malden,
The
TBJ
1075-122X
January/February
12
12006
suppl
Breast
Blackwell
USA
Publishing
Journal
Publishing
Inc Cancer Interventions
ORIGINAL ARTICLE: GLOBAL EPIDEMIOLOGIC METHODS
Costs and Health Effects of Breast Cancer Interventions in
Epidemiologically Different Regions of Africa, North
America, and Asia
Martijn T. Groot, MSc,* Rob Baltussen, PhD,* Carin A. Uyl-de Groot, PhD,*
Benjamin O. Anderson, MD,† and Gabriel N. Hortobágyi, MD‡
*Institute for Medical Technology Assessment, Erasmus Medical Center Rotterdam, Rotterdam, The
Netherlands; †Department of Surgery, University of Washington, Seattle, Washington; and ‡Department of
Breast Medical Oncology, University of Texas M. D. Anderson Cancer Center, Houston, Texas
Abstract: We estimated the costs and health effects of treating stage I, II, III, and IV breast cancer individually, of treating all
stages, and of introducing an extensive cancer control program (treating all stages plus early stage diagnosis) in three epidemiologically different world regions—Africa, North America, and Asia. We developed a mathematical simulation model of breast cancer
using the stage distribution and case fatality rates in the presence and absence of treatment as predictors of survival. Outcome
measures were life-years adjusted for disability (DALYs), costs (in 2000 U.S. dollars) of treatment and follow-up, and cost-effectiveness
ratios (CERs; in dollars per DALY averted). Sensitivity analyses were performed to determine the robustness of the results. Treating
patients with stage I breast cancer resulted in 23.41, 12.25, and 19.25 DALYs averted per patient in Africa, North America, and
Asia, respectively. The corresponding average CERs compared with no intervention were $78, $1960, and $62 per DALY averted.
The number of DALYs averted per patient decreased with stage; the value was lowest for stage IV treatment (0.18–0.19), with
average CERs of $4986 in Africa, $70,380 in North America, and $3510 per DALY averted in Asia. An extensive breast cancer
program resulted in 16.14, 12.91, and 12.58 DALYs averted per patient and average CERs of $75, $915, and $75 per DALY averted.
Outcomes were most sensitive to case fatality rates for untreated patients, but varying model assumptions did not change the
conclusions. These findings suggest that treating stage I disease and introducing an extensive breast cancer program are the
most cost-effective breast cancer interventions. Key Words: breast cancer, cost-effectiveness, costs, developing countries, economic evaluation, modeling
ach year, breast cancer is newly diagnosed in more
than 1 million women worldwide and more than
400,000 women die from it (1,2). Breast cancer as a public
health problem is growing throughout the world, but
especially in developing regions, where the incidence has
increased as much as 5% per year (1,3). The mortality:
incidence ratio is much higher in developing countries
than in developed countries: only half of global breast
cancers are diagnosed in the developing world, but they
account for three-fourths of total deaths from the disease
(1). The increasing burden of breast cancer is also acknowledged in the resolution on cancer prevention and control,
as adopted by the 58th World Health Assembly in May
2005 (4). Therein, member states are urged to develop and
E
Address correspondence and reprint requests to: M. T. Groot, Institute for
Medical Technology Assessment, Erasmus Medical Center, P.O. Box 1738, 3000
DR Rotterdam, or e-mail: [email protected]
© 2006 The Fred Hutchinson Cancer Research Center, 1075-122X/06
The Breast Journal, Volume 12 Suppl. 1, 2006 S81–S90
reinforce comprehensive cancer control programs to reduce
cancer mortality and improve quality of life for patients
and their families.
Cost-effectiveness analyses (CEAs) can provide useful
information for planning and developing a breast cancer
control policy. CEAs can be used to guide budget development, justify allocation of scarce resources to national
breast cancer control programs, and identify the most efficient ways of delivering diagnostic and treatment services.
Nearly all studies of the costs and health effects of breast
cancer control interventions have been performed in
developed countries (5), so data to guide resource allocation
decisions in developing countries are scarce. Moreover,
studies to date have focused on individual interventions,
and interactions among interventions have been largely
ignored. In addition, existing studies have focused on
interventions specific to breast cancer control in situations
where breast cancer care was already in place. This
limitation precludes comparisons with interventions in
settings where care systems have not been established or
S82 •
GROOT ET AL.
with interventions that might be more relevant to other
regions of the world.
Our intention was to broadly assess the cost-effectiveness
of breast cancer control that covers various interventions
in different settings and to enable comparisons with recent
CEAs of other health care interventions that follow the
same analytic approach (6–9).
METHODS
Study Design
We used a simplified breast cancer model to simulate
the impact of six basic interventions on the course of
breast cancer in three regions of the world (10). Each intervention was compared with no intervention (i.e., no active
case finding or breast cancer treatment). All interventions
were introduced starting in the year 2000 for a period of
10 years, after which no breast cancer interventions were
available, and the maximum follow-up was 100 years, which
is in line with the World Health Organization (WHO) guidelines on CEA (10). Following this standardized approach,
we assumed that interventions were performed optimally.
The outcomes of our analysis were life-years adjusted for
disability (DALYs) and the total costs of breast cancer
treatment and follow-up for each of the six interventions.
We adopted a societal perspective (11) and included all
costs and effects in our model. Future costs and effects
were discounted at a rate of 3% per year (11). The average
cost-effectiveness ratio (CER) compared to the do-nothing
scenario was calculated for each intervention by dividing
the total intervention costs (the costs are zero in the
do-nothing scenario) by the total DALYs averted (i.e.,
the DALYs lost when no intervention is applied minus the
DALYs lost when an intervention is applied for 10 years).
The interventions were also compared to arrive at the
incremental CER, which we defined as the additional costs
of a more effective intervention divided by the size of this
additional effect in terms of DALYs averted. To calculate
the incremental CERs, the interventions were ordered by
increasing effectiveness and the ratio of a scenario with its
adjacent, less effective scenario was determined.
Model Assumptions
Interventions In recent years, many developments in
diagnosing and treating breast cancer have occurred, and
we could analyze a large number of interventions in our
model. However, we confined the model to a small set of
basic interventions to allow comparability among the
regions. We assessed the following six basic interventions:
• Stage I treatment: Lumpectomy with axillary dissection
supplemented with external radiotherapy to the breast.
Eligible patients also receive endocrine therapy.
• Stage II treatment: Lumpectomy with axillary dissection
supplemented with external radiotherapy to the breast.
Eligible patients also receive endocrine therapy.
• Stage III treatment: Neoadjuvant chemotherapy followed
by mastectomy with axillary dissection supplemented
with adjuvant chemotherapy. External radiotherapy to
the breast is also administered and eligible patients
receive endocrine therapy.
• Stage IV treatment: Systemic chemotherapy, supplemented
with endocrine therapy for eligible patients. In this
group of patients, these therapies are palliative.
• Treatment all stages: Treatment of all stages as described
above.
• Extensive program: Treatment of all stages as described
above, plus a breast awareness program and early case
finding through biannual mammographic screening in
women age 50–70 years.
Model Structure Six mutually exclusive health states were
included (Fig. 1): healthy (no breast cancer); American
Joint Committee on Cancer (12) stages I, II, III, and
Study Population and Analyzed Regions
The breast health of adolescent and adult women age
15 years and older was simulated in an open cohort. The
costs, effects, and cost-effectiveness of each of the interventions were evaluated for three epidemiologic regions of
Africa, North America (including Cuba), and Asia, defined
by mortality strata (Appendix A) (10).
Figure 1. Graphical representation of the model showing the
relationships between the six different health states through the
incidence rates of breast cancer (Rx1–Rx4) and the different mortality
rates for the different breast cancer stages (Fx1– 4) and the background
mortality (M).
Cost-Effectiveness of Breast Cancer Interventions • S83
Table 1. Input Data for the Disease Model by Breast Cancer Stage and WHO Region (10)
Model element
North America
Africa and Asia
Stage distribution of prevalent cases, 2000 (%)
Stage I
49.00
9.40
Stage II
37.40
14.20
Stage III
8.60
58.00
Stage IV
5.00
18.40
Stage distribution of incident cases in absence of an extensive program, 2000 –2010 and the whole population thereafter (%)
Stage I
9.40
9.40
Stage II
14.20
14.20
Stage III
58.00
58.00
Stage IV
18.40
18.40
Stage distribution of incident cases in presence of an extensive program, 2000 –2010 (%)
Stage I
49.00
49.00
Stage II
37.40
37.40
Stage III
8.60
8.60
Stage IV
5.00
5.00
Case fatality rate of untreated patients, 2000 –2100
Stage I
0.020
0.020
Stage II
0.063
0.063
Stage III
0.150
0.150
Stage IV
0.300
0.300
Case fatality rate of treated patients, 2000 –2100a
Stage I
0.006
0.006
Stage II
0.042
0.042
Stage III
0.093
0.093
Stage IV
0.275
0.275
b
Quality of life
Stage I
0.9325
0.9325
Stage II
0.9301
0.9301
Stage III
0.9284
0.9284
Stage IV untreated
0.9097
0.9097
Stage IV treated
0.9275
0.9275
References
15,16
15,16
15,16
15,16
16
16
16
16
15
15
15
15
16
16
16
16
15
15
15
15
17–20
17–20
17–20
17–20
17–20
a
Includes the 100% of prevalent cases in North America, 10% in Africa, and 25% in Asia that were treated in 2000 (13).
On a scale from 0 (dead) to 1 (perfect health).
b
IV breast cancer; and death from breast cancer. Regional
age-adjusted population estimates of breast cancer incidence, breast cancer prevalence, percentage of prevalent
cases treated, and background mortality rates were based
on the WHO Burden of Disease study estimates for 2000
(13).
Following the WHO guidelines (10), the interventions
were aimed at initial disease treatment only, but patients
could experience a relapse or progression after initial
diagnosis; therefore we filtered out the effect of treating
patients whose disease progressed. It was assumed that
patients could have a progression only to stage IV breast
cancer and that cancer progressed at a constant rate (14).
Stage Distribution and Case Fatality Rates The key
elements of the model were the stage distribution of both
prevalent and incident cases, and the case fatality rate for
untreated and treated patients (Table 1). We distinguished
between the stage distribution in the developed region
(North America) and the two developing regions (Africa
and Asia) to reflect the difference in levels of breast cancer
care.
Stage distributions for prevalent cases were derived
from registry data (Table 1). The stage distribution of
prevalent cases in North America was based on the U.S.
National Cancer Data Base (NCDB) (15). The stage distribution of prevalent cases in Africa and Asia was based
on registry data from Southeast Asia (16).
In the no-intervention scenario, the stage distribution
of incident cases and stage-specific case fatality rates were
based on registry data from Southeast Asia (16) and applied
to all regions. The case fatality rates for treated patients
were derived from the NCDB (15). In the extensive breast
cancer program scenario, the stage distribution of incident
cases and stage-specific case fatality rates were based on
data from the NCDB (15) for all regions.
Quality of Life The quality of life of patients with breast
cancer (Table 1) was based on the WHO Global Burden
of Disease study (17). Using NCDB data on stage distribution (15) and quality of life data from several sources
(18–20), we arrived at stage-specific quality of life estimates.
The quality of life of the susceptible population was also
included (17).
S84 •
GROOT ET AL.
Table 2. Patient-Level Resource Use Patterns for Breast Cancer Interventions
Resourcea
Diagnosis
No. of
outpatient visits
Length of
hospitalization (days)
1
NA
1
NA
1
2
1
2
1
2
1
2
2
NA
1
NA
1
NA
Bilateral mammography
Complete blood count
Total bilirubin assay
Alkaline phosphatase assay
Fine needle aspiration or core needle biopsy
Liver function tests
ECG in 50%
Bone scan in 25%
Ultrasonography of the liver in 25%
Non-breast cancer examinationb
Bilateral mammography
Ultrasonography of the liver in 28%
Fine needle aspiration or core needle biopsy in 0.27%
Stage I treatment
Lumpectomy with axillary dissection
Radiotherapyc
Endocrine therapy in 50%d
Stage II treatment
Lumpectomy with axillary dissection
Radiotherapyc
Endocrine therapy in 50%d
Stage III treatment
(Neo)adjuvant chemotherapye
Mastectomy with axillary dissection
Radiotherapyc
Endocrine therapy in 50%d
Stage IV treatment
(Neo)adjuvant chemotherapye
Endocrine therapy in 50%d
Follow-up year 1–5 (per year)
2 Bilateral mammographies
Pelvic examination in 50%
Follow-up year 6 –10 (per year)
Bilateral mammography
Pelvic examination in 50%
Screening
Bilateral mammography
Ultrasonography of the liver in 28%b
Fine needle aspiration or core needle biopsy in 0.27%b
a
Based on clinical practice guidelines (21,22).
Includes resource use of initial evaluation of women without breast cancer who were initially suspected of having breast cancer (23).
Radiotherapy includes a standard dose of 50 Gy given in 25 fractions of 2 Gy on an outpatient basis in all stages of breast cancer (33).
d
Endocrine therapy consists of 20 mg tamoxifen per day for 5 years (21,22).
e
The (neo)adjuvant chemotherapy combination regimen consists of four, 21-day cycles of doxorubicin (60 mg/m2) and cyclophosphamide (830 mg/m2) supplemented with 4 mg dexamethasone,
given on an outpatient basis (21,22).
ECG, electrocardiography; NA, not applicable.
b
c
Costs All costs were calculated and are presented in 2000
U.S. dollars. Two types of costs for health services were
distinguished: patient-level costs, which were those incurred
for individual patients, and program-level costs, which
were those incurred at a level above that of the patient (10).
Patient-Level Costs In all regions patient-level patterns of
resource use (i.e., initial evaluation, local treatment, and
follow-up) were based on clinical practice guidelines
(21,22) (Table 2). These costs included evaluation of
women without breast cancer; it was assumed that breast
cancer was diagnosed in only 6% of all presenting women
(23).
Screening in the extensive cancer program included
costs of mammographic screening in women age 50–70
years and further diagnostic tests on referral (Table 2).
Detailed lists of all tests and procedures, including housing, personnel, and medical devices, were retrieved from
a South African database (24) and were validated for
western countries by a team of oncologists.
Unit costs were retrieved from the WHO-CHOICE
database on prices of traded and nontraded goods (http://
www.who.int/choice). Unit costs of health center visits
and hospital inpatient days were based on a report by
Adam et al. (25). We combined unit costs with resource
Cost-Effectiveness of Breast Cancer Interventions • S85
use patterns to estimate the total costs per patient treated.
All unit costs are presented for the regions of Africa, North
America, and Asia in Appendix B.
Program-Level Costs We based estimated quantities of
resources required to start up and maintain each intervention for 10 years (e.g., personnel, materials and supplies, media, transport, maintenance, utilities, and capital)
at national, provincial, and district levels on a series of
evaluations made by regional costing teams in the different WHO regions and validated against the literature
(26). We obtained unit cost estimates of program-level
resources (e.g., the salaries of central administrators, capital costs of vehicles, storage, offices, and furniture) from a
review of the literature, which was supplemented by primary data from several countries (the full list of unit cost
estimates is available at http://www.who.int/choice). The
process and methodology for estimating program costs
are described in detail elsewhere (26,27).
Sensitivity Analyses
To address uncertainty and determine the robustness of
the model, we conducted both univariate and multivariate
sensitivity analyses on key parameters. Specifically we
assessed the effects of varying the stage distribution of
prevalent cases, the stage distribution of incident cases,
and the case fatality rate of treated patients, individually
and then collectively.
RESULTS
Intervention Effectiveness
In Africa, the smallest group treated in the 10-year
period was women who had stage I breast cancer (Table
3); of these 37,277 cases, 9604 were previously untreated
prevalent cases and 27,673 were new cases of breast cancer.
Most of the treated women were those with stage III breast
cancer (228,914; 58,978 prevalent and 169,936 incident
cases). In North America and Asia, the trends were the
same, although the absolute numbers of treated patients
were higher. The female population in North America
was four times smaller than the female population in Asia,
but the number of treated breast cancer patients was
one-third higher in North America. The population sizes
in North America and Africa were similar, but the
number of treated patients was four times larger in North
America.
Because of these differences between regions, the number
of DALYs averted for the total population or per treated
patient in the 10-year period also varied considerably
(Table 3). For example, in Africa, treatment of stage I
patients resulted in a total of 873,000 DALYs averted for
the total population and 23.41 DALYs averted per treated
patient. Despite the greater number of treated patients
with stage II, III, or IV breast cancer, the total number of
DALYs averted was considerably less for each of these
stages. When all diagnosed cases were treated, 1,490,000
DALYs were averted for the total population (3.77 per
treated patient). When an extensive breast cancer program
was assumed to exist in Africa, 6,374,000 DALYs were
averted for the total population (16.14 per treated patient).
Costs and Cost-Effectiveness
The range in total costs per intervention over the 10year period was considerable. For example, the total costs
for introducing stage I treatment was $68 million in Africa,
$3879 million in North America, and $143 million in
Asia (Table 3).
The costs of diagnosis were a fixed component in all
intervention scenarios because cases must be diagnosed
correctly before treatment can be initiated. This category
also accounted for the exclusion of women presenting
without breast cancer. As a result, costs per treated patient
were lowest when all diagnosed cases were treated (Table
3). In all three regions, the diagnostic costs for patients
with stage I breast cancer constituted 62–68% of the total
costs, whereas the diagnostic costs for all patients made up
17–20% of the total costs.
The costs per treated patient with stage I disease were
$1829 in Africa, $24,008 in North America, and $1188
in Asia (Table 3). The costs of treatment represented
16–27% of the total costs in each region.
In the extensive program, different cost items accounted
for widely varying proportions of the total costs (Table 3).
In Africa, the patient-level costs of screening and associated diagnostic examination of false-positive screens
($180 million) were 38% of the total costs; in North
America, these costs ($5299 million) constituted only
26% of the total costs; and in Asia, these costs ($703 million) made up 58% of the total costs.
In each of the six intervention scenarios, the total program costs accounted for 8–24% of the total costs in
Africa and Asia, but only 1–4% of the total costs in North
America (Table 3).
When we compared the intervention scenarios with the
no-intervention scenario, treatment of stage I patients and
the extensive breast cancer program were the most
cost-effective interventions, with average CERs for stage
I treatment and extensive programs, respectively, of $78
and $75 per DALY averted in Africa, $1960 and $915 per
873
231
399
14
1490
6374
1979
542
1587
56
4282
22,098
2325
663
1205
42
4155
16,086
37,277
55,955
228,914
72,738
394,884
394,884
161,558
242,507
992,107
315,214
1,711,414
1,711,414
120,738
181,235
741,439
235,593
1,279,005
1,279,005
Total DALYs
averted
(in thousands)
11
11
11
11
11
11
500
500
500
500
500
500
27
27
27
27
27
27
12.25
2.24
1.60
0.18
2.50
12.91
19.25
3.66
1.63
0.18
3.25
12.58
Diagnosis
23.41
4.13
1.74
0.19
3.77
16.14
DALYs
averted
per patient
64
64
64
64
64
38
2171
2171
2171
2171
2171
1626
31
31
31
31
31
20
Non–breast
cancer
examination
23
34
178
29
264
251
1040
1562
7136
1074
10,812
10,874
13
19
93
14
138
134
Treatment
5
7
23
4
38
42
108
147
526
110
892
1057
2
3
9
2
15
17
Follow-up
703
5299
180
Screening
120
133
292
125
393
1061
3820
4380
10,334
3857
14,375
19,356
56
63
143
58
195
362
Total per
patient
24
24
24
24
62
145
59
59
59
59
223
856
12
12
12
12
42
115
Total per
program
143
156
316
149
455
1206
3879
4439
10,392
3915
14,598
20,213
68
75
155
70
238
477
Total
overall
1188
863
426
630
356
943
24,008
18,304
10,475
12,421
8530
11,811
1829
1342
679
959
602
1208
Costs
per treated
patient 2000
U.S.$
62
236
262
3510
110
75
1960
8187
6549
70,380
3409
915
78
324
389
4986
159
75
Averagea
62
NA
NA
NA
NA
77
NA
NA
NA
NA
NA
915
NA
NA
NA
NA
NA
75
Incrementalb
CER (2000 U.S.$ per
DALY averted)
Incremental CER versus less effective alternative. To calculate the incremental CER, the interventions were ordered by increasing effectiveness and the ratio of a scenario with its adjacent, less effective scenario was determined.
b
Average CER compared to the do-nothing scenario. In the do-nothing scenario costs were zero.
CER, cost-effectiveness ratio; DALY, disability-adjusted life-year; WHO, World Health Organization; NA, not applicable, because the intervention is less cost-effective than others.
a
Africa
Stage I treatment
Stage II treatment
Stage III treatment
Stage IV treatment
Treatment all stages
Extensive program
North America
Stage I treatment
Stage II treatment
Stage III treatment
Stage IV treatment
Treatment all stages
Extensive program
Asia
Stage I treatment
Stage II treatment
Stage III treatment
Stage IV treatment
Treatment all stages
Extensive program
Region and
intervention
No. of
patients
treated
Population-level costs (millions of 2000 U.S.$)
Table 3. Number of Patients Treated, DALYs Averted, Costs, and CERs at an 80% Coverage Level, Over a 10-Year Period (2000–2010) by
WHO Region
S86 •
GROOT ET AL.
Cost-Effectiveness of Breast Cancer Interventions • S87
DALY averted in North America, and $62 and $75 per
DALY averted in Asia (Table 3). The least cost-effective
option was stage IV treatment (average CERs of $4986,
$70,380, and $3510 per DALY averted in Africa, North
America, and Asia, respectively).
Incremental CERs revealed that in Africa and North
America, the optimal breast cancer program was the most
cost-effective intervention scenario ($75 and $915 per
DALY averted, respectively) (Table 3). In Asia, the most
cost-effective options were stage I treatment ($62 per DALY
averted) and then the optimal breast cancer program ($77
per DALY averted).
The order in which interventions should be introduced
according to the cost-effectiveness results (i.e., the “expansion
path;” for more details on expansion paths, see Tan-Torres
Edejer et al. (10)) is illustrated for Asia in Figure 2. Stage
I treatment would be introduced first. With more resources,
an optimal breast cancer program would be established.
Sensitivity Analyses
In the first two univariate sensitivity analyses, it was
assumed that cancers were diagnosed earlier compared
with the base case analysis (i.e., more stage I and II cancers
and fewer stage III and IV cancers). This assumption produces a more favorable distribution, with the sole exception of the prevalent cases in North America, where the
distribution becomes less favorable. Applying these alternative stage distributions for prevalent and incident breast
cancer cases resulted in lower average CERs for stage I
treatment and for treatment of all stages in Africa, North
America, and Asia because more stage I patients received
treatment, which was associated with lower case fatality
rates (Table 4 shows results for Asia as an example). For
Figure 2. Expansion path for the Asian region.
stage III and IV treatment, the average CERs increased
because fewer cases were diagnosed at these stages. Because
the shift in distribution of incident cases of stage II breast
cancer decreased the overall mortality in the no-intervention
scenario, the average CERs for stage II treatment and the
extensive program also increased.
In a third univariate analysis, the assumption of a 50%
reduction in treatment effect on case fatality rates (i.e.,
higher case fatality rates of treated cases than those used
in the base case analysis) increased the average CERs of
each of the six interventions in Africa, North America,
and Asia (Table 4 shows results for Asia as an example).
Combining all three univariate sensitivity analyses in a
multivariate analysis resulted in a further increase in the
average CERs for stage II, III, and IV treatment and the
extensive program (Table 4). The average CERs for stage
I treatment and treatment of all stages were between the
CERs calculated in the individual sensitivity analyses.
Table 4. Results of Univariate and Multivariate Sensitivity Analyses for Asiaa
Univariate analyses
Alternative stage distribution
of prevalent casesb
Intervention
Stage I treatment
Stage II treatment
Stage III treatment
Stage IV treatment
Treatment all stages
Extensive program
a
Average
Incrementalf
45
224
283
4103
79
73
45
NA
NA
NA
NA
82
Alternative stage distribution
of incident casesb,c
Average
48
261
390
4888
84
127
Alternative case
fatality ratesd
Incrementalf
Average
Incrementalf
Average
Incrementalf
48
NA
NA
NA
NA
182
162
609
642
5175
255
113
NA
NA
NA
NA
NA
113
107
618
1186
8875
178
216
107
NA
NA
NA
NA
274
Data are presented as cost-effectiveness ratios, calculated as cost (in 2000 U.S.$) per DALY (disability-adjusted life-year) averted.
Stage distribution: stage I, 29%; stage II, 26%; stage III, 33%; and stage IV, 12%.
In the absence of an extensive breast cancer program.
d
Case fatality rates of treated patients: stage I, 0.013; stage II, 0.053; stage III, 0.122; and stage IV, 0.288.
e
All adjustments in the three univariate sensitivity analyses were implemented simultaneously.
f
Incremental cost-effectiveness ratio versus lesser effective alternative.
NA, not applicable, because the intervention is less cost-effective than others.
b
c
Multivariate analysise
S88 •
GROOT ET AL.
DISCUSSION
Our analyses showed that treating early stage breast
cancer is more cost-effective than treating late-stage
disease. In Africa and Asia, treatment of stage I, II, or III
disease costs less than $390 per DALY averted, whereas
treatment of stage IV disease costs more than $3500 per
DALY averted; in North America, the respective values
were $6550 and $70,400. For comparison, we can use
benchmarks suggested by other researchers to assess
whether a health intervention is cost-effective: cost per
DALY averted or life-year gained equal to the per capita
income (28), twice per capita income (29), or three times
per capita income (30) (low-income countries are defined
as having per capita incomes of $765 or less per year, and
high-income countries are defined as having per capita
incomes of more than $9386 per year). According to these
benchmarks, all interventions except treatment of stage IV
disease were cost effective in all three regions.
The incremental CERs indicated that priorities in
national breast cancer control programs would be treatment of stage I disease or implementation of an extensive
cancer control program (including breast cancer awareness campaigns and active mammographic screening).
Although the extensive cancer control program reflects
the economic attractiveness of diagnosing breast cancer at
an earlier stage, many developing countries may not be
able to meet the total costs of such a program (including
the required infrastructure, logistics, and expertise). Given
the limited available resources, priorities are probably
best directed at treatment of early stage disease and at
developing a less expensive means of early diagnosis. We
did not evaluate clinical breast examination or breast selfexamination because currently there is no consensus on
their value alone or in addition to mammography. Nevertheless, together with other ways of raising awareness,
clinical breast examination and breast self-examination
could be a cost-effective means by which to diagnose
breast cancer earlier in resource-poor settings.
A number of our study limitations have to be addressed.
We used data on stage distribution and case fatality rates
from a sample of developing countries to reflect the
absence of breast cancer control interventions. For the
same variables, we used data from U.S. cancer registries to
reflect intervention effectiveness. Whether these data are
accurate can be assessed only when studies on the effectiveness of breast cancer interventions in developing
countries become available.
We did not include stage 0 disease (i.e., ductal carcinoma in situ) in our model because very little information
is available on this type of breast cancer in developing
regions. Furthermore, the WHO Global Burden of
Disease study provides information only on the prevalence
and incidence of palpable breast cancer. From the NCDB,
it is clear that through screening, the proportion of disease
diagnosed at stage 0 increased substantially in the United
States (15). Although not all stage 0 breast cancer will result
in breast cancer-related death if not treated, and overtreatment (with its associated costs) will likely be introduced,
including stage 0 disease in the model will probably reinforce our conclusion that treating earlier stages of breast
cancer is the most cost-effective intervention.
We estimated program costs for breast cancer interventions that are not yet in place on this scale in developing
countries and therefore cannot be validated. However, an
extensive cancer control program was estimated to cost
$50 million for 95% geographic coverage in The Netherlands; this value compares well with the costs of breast
cancer screening in that country, which were $49 million
in 2003 (31).
Our simplified cost-effectiveness model is appropriate
to use for broadly assessing the relative economic attractiveness of breast cancer interventions and for comparing
interventions among regions. Our analysis shows that
there is a broad variation in epidemiology between regions
and that there are large differences in cost structure as
well. In contrast to North America, where personnel is the
major cost component, the costs of personnel are only a
small part of the total costs in developing regions (Africa
and Asia). Therefore, while the pattern of most cost-effective
interventions is the same, there are substantial differences
between interventions across regions and likely within a
region. A more detailed country-level analysis, using local
cost and resource estimates and epidemiologic information,
could be useful for testing whether our model assumptions
hold and for obtaining more specific information on the
impact of interventions on budgets, especially when there
is competition for scarce resources with interventions that
are more intensive with respect to either personnel time or
resource use. We developed the cost-effectiveness model
in such a way that these country-specific adaptations can
be performed easily.
For reasons of comparability, we were unable to include
many of the elements of breast cancer care that are considered standard in developed countries. A few examples
are sentinel lymph node biopsy, breast reconstruction after
surgery, and variations in surgical treatment of breast
cancer within the same stage. Furthermore, we assumed
the use of only one type of chemotherapy and one type of
hormonal therapy. These issues can be addressed in a
Cost-Effectiveness of Breast Cancer Interventions • S89
more tailor-made country-level analysis using the model’s
framework.
Finally, we are aware of the current debate surrounding
the relative effect of breast cancer screening on reducing
mortality rates. This debate focuses on the overtreatment
and overdiagnosis that are said to be underappreciated
harms of screening (32). In our analysis, we assumed that
the introduction of an extensive breast cancer program
would cause a shift in stage distribution that would result
in reduced mortality rates for all patients, and this assumption probably led to an overestimation of the impact of
such a program. Sensitivity analyses showed that varying
model assumptions did affect the cost-effectiveness of the
interventions, but not our principal study conclusion.
We conclude that both treatment of early stage breast
cancer and interventions for down-staging disease at diagnosis are among the most valuable interventions in breast
cancer control.
Acknowledgments
The authors gratefully acknowledge the advice of Dr.
Sharon Giordano and the editorial assistance of Elizabeth
L. Hess and Susan London. This study was supported in
part by a grant from the World Health Organization,
which had no involvement in the study, and was presented
in part at the second biennial Global Summit Consensus
Conference on International Breast Health Care, Bethesda,
MD, January 12–15, 2005.
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Appendix A. Epidemiologic Regions as Applied in WHO Generalized CEA (10)
WHO region
Mortality stratuma
WHO member states
Africa
E
North America
Asia
A
D
Botswana, Burundi, Central African Republic, Congo, Côte d’Ivoire, Democratic Republic Congo, Eritrea,
Ethiopia, Kenya, Lesotho, Malawi, Mozambique, Namibia, Rwanda, South Africa, Swaziland, Uganda,
United Republic of Tanzania, Zambia, Zimbabwe
Canada, Cuba, United States of America
Bangladesh, Bhutan, Democratic People's Republic of Korea, India, Maldives, Myanmar, Nepal
a
A, have very low rates of adult and child mortality; D, have high adult and child mortality; E, have very high adult and high child mortality.
WHO, World Health Organization; CEA, cost-effectiveness analysis.
Appendix B. Unit Costs and Total Costs per Patient (in 2000 U.S. Dollars) by WHO Regiona
Resource or intervention
Unit costs
Outpatient visit
Hospitalization
Lumpectomy
Mastectomy
Radiotherapy
(Neo)adjuvant chemotherapy
Endocrine therapy
Bilateral mammography
Fine needle aspiration biopsy
Chest radiograph
Bone scan
Electrocardiography
Pelvic examination
Ultrasonography of the liver
Complete blood count
Total bilirubin assay
Alkaline phosphatase assay
Total costs per patient
Diagnosis
Non-breast cancer examination
Stage I treatment
Stage II treatment
Stage III treatment
Stage IV treatment
Follow-up year 1–5
Follow-up year 6–10
Screening
a
All unit costs are derived from a South African database (24).
WHO, World Health Organization.
Africa
North America
Asia
0.82
4.65
34.00
34.56
323.43
75.96
0.01
3.57
8.22
3.05
15.96
1.58
1.22
3.61
2.68
2.23
4.70
24.05
203.35
414.72
417.01
6465.55
852.72
0.04
48.36
51.42
31.76
107.79
28.47
20.44
66.10
35.10
36.83
46.76
0.53
3.75
23.54
24.01
173.20
54.87
0.01
2.60
6.47
2.26
13.06
0.91
0.70
2.12
1.97
1.51
3.59
30.96
5.57
367.54
367.54
444.06
86.08
31.95
24.26
4.46
300.23
91.94
7311.01
7311.01
8166.03
1283.47
547.31
378.69
62.60
17.32
3.85
204.77
204.77
260.11
62.89
22.75
17.51
3.15
Tumor
Original
duffy
Size
etArticle
al
and
. Breast
Cancer
Detection
Blackwell
Malden,
The
TBJ
1075-122X
January/February
12
12006
suppl
Breast
Blackwell
USA
Publishing
Journal
Publishing
2006
Inc
ORIGINAL ARTICLE: LIMITED-RESOURCE INTERVENTIONS
Tumor Size and Breast Cancer Detection: What Might Be
the Effect of a Less Sensitive Screening Tool Than
Mammography?
Stephen W. Duffy, MSc, CStat,* Laszlo Tabar, MD,† Bedrich Vitak, MD,‡ and Jane
Warwick, PhD*
*Cancer Research UK Center for Epidemiology, Mathematics, and Statistics, Wolfson Institute of
Preventive Medicine, London, United Kingdom; †Mammography Department, Central Hospital, Falun,
Sweden; and ‡Department of Medical Radiology, University Hospital, Linköping, Sweden
Abstract: In some limited-resource areas, a state-of-the-art mammography program is not affordable. In such circumstances, one might consider a less resource-intensive, but also less sensitive screening tool such as clinical breast examination
(CBE). We used data from the Swedish Two-County Trial to estimate the shift in tumor size resulting from invitation to mammographic screening. By postulating a lesser benefit of a less sensitive screening tool (CBE), particularly in terms of detecting very
small tumors, we predicted its likely effect on tumor size distribution. In addition, using the observed association between tumor
size and nodal status, and between tumor size and fatality, we predicted the likely benefit in terms of reductions in node-positive
disease and in breast cancer mortality. An invitation to mammographic screening was associated with a 27% reduction in the number of node-positive tumors and a 31% reduction in the number of breast cancer deaths. We estimate that in the trial population,
screening with CBE alone would have led to an 11% reduction in node-positive tumors and an 11% reduction in breast cancer
deaths (approximately 42 deaths prevented per 1000 cases). Assuming instead a tumor size distribution typical of a limitedresource setting (70% of tumors are 30 mm at presentation), we estimate that screening with CBE alone would lead to a 13%
reduction in node-positive tumors and a 12% reduction in breast cancer deaths (approximately 72 deaths prevented per 1000
cases). Thus, although the relative benefit of CBE is only slightly greater in the limited-resource setting, the absolute reduction in
deaths per case is about 70% higher. Our findings suggest that a less sensitive tool might be expected to confer a breast cancer
mortality reduction about half of that observed with mammography. Key Words: breast cancer, clinical breast examination, early detection, mammography, mortality, screening, tumor size
R
andomized trials show that breast cancer mortality
reductions on the order of 20–30% are observed in
association with invitation to breast cancer screening with
mammography, and that greater reductions may be
expected in association with actually being screened (1,2).
More recent research on service screening programs suggests that participation in modern, organized service
screening may well reduce the risk of dying from breast
cancer by 40% or more (3).
Mammography is the only single screening modality
with a strong evidence base for its efficacy in reducing
Address correspondence and reprint requests to: Stephen W. Duffy,
Professor of Cancer Screening, Cancer Research UK Center for Epidemiology,
Mathematics, and Statistics, Wolfson Institute of Preventive Medicine,
Charterhouse Square, London EC1M 6BQ, United Kingdom, or e-mail:
[email protected]
© 2006 The Fred Hutchinson Cancer Research Center, 1075-122X/06
The Breast Journal, Volume 12 Suppl. 1, 2006 S91–S95
breast cancer mortality, and as such it is the first recommendation for advancing the diagnosis of breast cancer
and thus preventing death from the disease. In a developed
country with a high level of awareness about the importance of early detection, and thus prompt seeking of health
care services when new symptoms develop, stage at clinical
presentation is such that one could not reasonably expect
a substantial improvement in stage by any less sensitive
screening modality than mammography. There is, however,
interest in considering the use of less resource-intensive
methods for countries that cannot afford a mass mammography program. It should be noted, however, that in
countries with very limited resources, where there is not
even general access to surgical treatment for cancer, early
detection is not worth considering at this time, and the
main objective for such countries must be the delivery of
basic treatment.
Possible less sensitive and less resource-intensive methods
for earlier diagnosis of breast cancer include education in
S92 • duffy et al.
breast awareness, training in breast self-examination (BSE),
and regular clinical breast examination (CBE) by experienced personnel (4). Breast awareness is a difficult concept
to measure, but it is clear that increased awareness has
contributed to a downshift in stage at diagnosis in the
absence of, or in addition to, that contributed by formal
screening (5). Although it seems reasonable that physical
examination could be a pathway to earlier diagnosis in
limited-resource settings, at the moment, there are no randomized trial results establishing a mortality-reducing
benefit of BSE or CBE (6,7), so these approaches cannot
be recommended outside of the research/evaluation
setting. However, it would be useful to those planning
such research studies to have some prior idea of the likely
benefit of such less sensitive screening tools.
In this article we examine the effect of mammographic
screening, within a randomized controlled trial, on the
size distribution of tumors diagnosed and the consequences for risk of node-positive disease and subsequent
death from breast cancer. We postulate lesser effects on
the size distribution of CBE, a screening test of lower
sensitivity, and estimate the likely consequences of these
effects for node-positive disease and breast cancer mortality.
We provide estimates both for the trial population with its
observed tumor size distribution and for the same population after applying a tumor size distribution typical of a
limited-resource setting.
METHODS
Our data are from the Swedish Two-County Trial of
mammographic screening for breast cancer (1). In this
study, 77,080 women age 40–74 years were randomized
to regular invitation to mammographic screening (active
study population [ASP]) and 55,985 were randomized to
no invitation (passive study population [PSP]). In the ASP,
women age 40–49 years at randomization were invited
every 2 years, and women age 50–74 years were invited
every 33 months. After 7 years, the first mortality results
were published, showing a significant 30% reduction in
breast cancer mortality with an invitation to screening (8),
the control group was invited for screening, and the trial
was closed. During the trial, 2468 breast cancers were
diagnosed, of which 2299 were invasive. Of the invasive
cases, we had tumor size data on 2294 (99.8%) and nodal
status data on 2147 (93.4%). At the time of our most
recent publication of trial results, we had more than 20years maximum follow-up (1). Our analyses in this article
are based only on the invasive cases, as very few deaths
arise from ductal carcinoma in situ (DCIS) and because an
alternative screening tool such as CBE is unlikely to detect
large numbers of in situ cases.
We first tabulated the tumor size distributions in the
ASP and PSP. We then tabulated the proportions of nodepositive cases and the 20-year fatality rates from breast
cancer by tumor size. From these, we derived the shifts in
tumor size and the consequent changes in proportions of
node-positive cases and fatal cases resulting from the
mammographic screening. By applying hypothesized
lesser shifts in tumor size from a screening test of lesser
sensitivity (CBE), we predicted the likely reductions in
node-positive disease and breast cancer deaths from such
a test. The methodology is as described in our article on
detection of early stage invasive disease and DCIS (9), but
it is best explained by demonstration, as in the “Results”
section below. Finally, to predict possible reductions in
node-positive disease and breast cancer deaths in the
limited-resource setting with the use of a less sensitive test,
we repeated the calculations assuming that the majority
of cancers were of a late stage at presentation.
RESULTS
Table 1 shows the observed distribution of sizes of
invasive tumors in the ASP and PSP. Clearly there was a
considerable shift toward smaller tumors in the ASP.
More than 40% of tumors in the ASP were smaller than
15 mm, whereas less than 30% of PSP tumors were of this
size.
If we assume that any shift in tumor size as a result of
screening in the ASP is no greater than one size category,
we can derive the numbers and percentages shifted to and
from each category. For example, on the basis of the rate
of tumors of size 50 mm or more in the PSP, the number
of cancers one would expect in this category in the ASP is
E50 = 77,080 × 76/55,985 = 105.
Table 1. Size Distribution of Invasive Tumors by Trial
Arma
Size (mm)
1–9
10 –14
15 –19
20 –29
30 – 49
50+
Total
a
ASP, no. (%)
PSP, no. (%)
249 (19)
319 (24)
259 (20)
270 (21)
128 (10)
76 (6)
1301 (100)
105 (11)
179 (18)
202 (20)
264 (26)
167 (17)
76 (8)
993 (100)
The trial randomized 77,080 women to the ASP (active study population: invitation to
mammographic screening) and 55,985 women to the PSP (passive study population:
no invitation).
Tumor Size and Breast Cancer Detection • S93
Table 2. Estimated Downshifting of Tumor Size in
the ASPa
Size (mm)
Shifted to lower size category (%)
1–9
10–14
15–19
20–29
30 – 49
50+
—
69
87
62
57
28
Figure 1. Survival of 2294 invasive breast cancer cases by tumor size.
a
Percentages of tumors from each size category in the ASP (active study population: invitation
to mammographic screening) estimated to have been shifted to the immediate lower size
category, assuming shifts of two categories or more are impossible.
In fact, we observed 76 such tumors in the ASP, so we derive
a shift of 29 tumors (29/105 = 28%) from size 50 mm or
more to 30–49 mm. The same procedure gives the expected
number of tumors in the 30–49 mm category in the ASP
as 230. Removing the 29 tumors downshifted from the
50 mm or more group, we have 99 tumors observed in
this category in the ASP. Thus we calculated that 230 −
99 = 131 tumors have been shifted from size category
30–49 mm to 20–29 mm (131/230 = 57%). Carrying on
with this procedure gives the derived size-shifted percentages in Table 2. These percentages correspond to 798
tumors size-shifted in the ASP, which is 86% of the screendetected tumors. These shifts resulted in an observed
27% reduction in the number of node-positive tumors
and a 31% reduction in the number of breast cancer deaths
(Table 3).
Figure 1 shows the observed 21-year survival by tumor
size (regardless of trial arm). The corresponding observed
proportions of node-positive tumors and 20-year fatality
rates are shown in Table 4. Clearly there are very strong
gradients of increasing fatality and increasing node positivity with increasing tumor size. By applying these rates
to the actual number of invasive tumors by size and trial
arm, given in Table 1, one can derive the expected number
of node-positive cases in each trial arm (407 in the ASP
and 380 in the PSP)—note that greater numbers of cases
(and not a higher rate) are expected in the ASP because the
size of the ASP was 38% larger than that of the PSP. The
expected incidence of node-positive disease in the ASP and
PSP is therefore 5.28 and 6.78 per 1000 women, respectively. This represents an expected 22% reduction in the
incidence of node-positive disease with an invitation to
screening. The actual reduction achieved was 27% (Table
3). Similarly we would expect 419 breast cancer deaths in
the ASP and 383 in the PSP and respective fatality rates of
5.43 and 6.83 per 1000 women. The expected reduction
in fatality is therefore 21%, considerably less than the
actual reduction of 31% (Table 3). Thus this methodology
gives a conservative estimate of the mortality-reducing
benefit of screening.
The percent of cases shifted to a lower size category,
assuming a less sensitive screening tool such as CBE instead
of mammography, are given in Table 5. The assumed
relative benefit of CBE (when compared with mammography) is somewhat arbitrary, due to a lack of available
evidence, but we nevertheless believe the predicted
estimates to be reasonable. The hypothesized effect of
using this screening tool on the distribution of tumor size
(assuming for simplicity, equal-size study arms) is shown
in Table 6. The predicted number of cases in the size group
of 50 mm, for example, is
P50 = 76 × 0.72 = 55.
Table 3. Node Positivity and Breast Cancer Deaths
by Trial Arm
Node-positive tumors
No.
RR (95% CI)
Breast cancer deaths
No.
RR (95% CI)
a
ASP (n = 77,080)
PSP (n = 55,985)
366
0.73 (0.63 – 0.85)
365
1.00 (—)a
319
0.69 (0.59 – 0.81)
334
1.00 (—)a
Reference group.
ASP, active study population (invitation to mammographic screening); CI, confidence interval;
PSP, passive study population (no invitation); RR, relative risk.
Therefore, for the 30–49 mm category,
Table 4. Node Positivity and Fatality by Tumor Size
for the Trial Population Overall
Size (mm)
1– 9
10 –14
15 –19
20 –29
30 – 49
50+
Node-positive tumors (%)
20-year fatality rate (%)
5
19
29
42
65
82
13
16
29
43
62
85
S94 • duffy et al.
Table 5. Predicted Downshifting of Tumor Size in the
ASP with the Use of CBE, a Less Sensitive Tool Than
Mammographya
Size (mm)
1–9
10–14
15–19
20–29
30–49
50+
Shifted to a
lower size category:
screening with
mammography (%)
Assumed
relative benefit
of CBE as a
screening tool
Shifted to a lower
size category:
screening
with CBE (%)
—
69
87
62
57
28
—
0
0.4
0.6
0.8
1.0
—
0
35
37
46
28
Table 7. Hypothesized Distribution of Tumor Size
When Screening with CBE in a Limited-Resource
Country Where the Disease Typically Presents at a
Late Stage
Size (mm)
1–9
10 –14
15 –19
20 –29
30 – 49
50+
ASP, predicted no. (%)
PSP, observed no. (%)
42 (4)
99 (10)
91 (9)
286 (29)
340 (34)
135 (14)
42 (4)
71 (7)
81 (8)
105 (11)
477 (48)
217 (22)
ASP, active study population (invitation to mammographic screening); CBE, clinical breast
examination; PSP, passive study population (no invitation).
a
Percentages of tumors from each size category in the ASP estimated to have been shifted
to the immediate lower size category, assuming use of a less sensitive screening tool than
mammography and that shifts of two categories or more are impossible.
ASP, active study population (invitation to mammographic screening); CBE, clinical breast
examination.
P30 − 49 = 167 × 0.54 + (76 − 55) = 90 + 21 = 111
(i.e., the number of cases not expected to downshift to the
20–29 mm category plus the number of cases downshifted
from the 50 mm category). Again applying the observed
node-positive and fatality rates from Table 4 to the
hypothesized tumor size distribution (Table 6), we obtain
respective estimates of 11% for the predicted reduction in
node-positive tumors and 11% for the reduction in breast
cancer deaths. This corresponds to a total of 42 deaths
avoided in 993 cases. We carried out similar calculations
using the joint effects of tumor size and nodal status, and
found the predicted reductions in the number of nodepositive cases and breast cancer deaths to be the same.
Unlike the situation described above, which derives
from a northern European population, in many limitedresource countries, stage at presentation is typically more
advanced (10). Thus in order to obtain more pragmatic
estimates of the effects on nodal status and breast cancer
deaths, we reweighted our PSP numbers to ensure that
Table 6. Hypothesized Distribution of Tumor Size
When Screening with CBE, Equalized Over the
Study Arms
Size (mm)
1–9
10–14
15–19
20–29
30–49
50+
ASP, predicted no. (%)
PSP, observed no. (%)
105 (11)
250 (25)
229 (23)
243 (24)
111 (11)
55 (6)
105 (11)
179 (18)
202 (20)
264 (26)
167 (17)
76 (8)
ASP, active study population (invitation to mammographic screening); CBE, clinical breast
examination; PSP, passive study population (no invitation).
70% of the tumors were in the 30 mm or more categories,
thereafter distributing cases among the categories in the
same ratios as before. The numbers in each study arm and
size category, after this reallocation, are given in Table 7.
Applying the node positivity and fatality rates from Table
4 as before, we predict that screening for breast cancer
with CBE alone in a limited-resource country would lead
to a 13% reduction in node-positive cases and a 12%
reduction in breast cancer deaths. This corresponds to
the prevention of 72 deaths in 993 cases. Thus, although
the relative benefit is only slightly greater in an environment where late stage at presentation prevails, the absolute reduction in deaths per case is about 70% higher.
DISCUSSION
The use of a less sensitive screening tool than mammography would be expected to result in a lesser impact on
tumor size, lymph node status, and breast cancer mortality
than that observed with mammography. Our results,
based on plausible assumptions about the relative effect of
a less sensitive screening tool in terms of size shifting, suggest that the benefit might approach half of the benefit of
invitation to mammography observed in the trials, with an
11–13% reduction in node-positive disease and in breast
cancer deaths. Thomas et al. (6) found an 8% reduction
in node-positive cases and an 11% reduction in tumors of
stage T2 or worse in a trial of BSE in Shanghai. Our predicted percentage size shifts correspond to an absolute
number of size-shifted tumors that is about half of the
number estimated from mammography. This is consistent
with Alexander’s estimates of sensitivity of around 40%
for CBE and around 60–80% for mammography (11).
Our predictions are arguably conservative, as the
mortality reduction predicted from the observed shift in
tumor size distribution with invitation to mammography
Tumor Size and Breast Cancer Detection • S95
underestimated the observed mortality reduction by a factor of one-third. However, the Two-County Trial resulted
in a relatively high mortality-reducing benefit compared
with the other breast screening trials and had a very
high participation rate, 85% on average (12). In a limitedresource country, one would not expect such a high participation rate. However, the effects of the offer of such an
intervention would almost certainly include an increase in
awareness that would in turn ameliorate stage at presentation, so that the overall benefit might be greater than
estimated.
It is therefore unlikely that the benefit of a less sensitive
screening method such as CBE would confer a breast
cancer mortality reduction substantially greater than the
11–13% predicted here. One would clearly prefer to
achieve the substantial benefit of mammographic screening, and indeed mammography is becoming more widespread worldwide, including areas of Africa and eastern
Europe that would be considered limited-resource areas
(13,14). However, it is not an option for some limitedresource areas, and the lesser benefit might still be worth
pursuing, especially if one assumes that some additional
improvements could derive from a steady growth in
awareness and prompt seeking of health care when a
woman first notices a change in her breast. The following
caveats should be borne in mind, however:
• Early detection is of no use if treatment facilities are not
available. Any early detection or awareness program
should be accompanied by efforts to ensure timely
delivery of responsive, appropriate treatment of the
cases diagnosed.
• In some countries, attitudes are as much a barrier to early
detection as limited resources. For example, in a trial of
breast cancer screening by CBE in the Philippines, intervention was discontinued due to noncompliance of
women recalled for further assessment of suspicious
lumps (7). Thus the introduction of screening may also
need to be accompanied by behavioral interventions.
• Breast cancer incidence in limited-resource areas is
often considerably lower than that in the developed countries of Europe, North America, and Australia. This has
implications for cost-effectiveness, even of screening
methods requiring minimal resources. However, increas-
ing incidence in some of these settings, and lower
average age at onset due to cohort effects, with considerably more potential years of life lost, are also are
considerations.
Acknowledgments
This article was presented in part at the second biennial
Global Summit Consensus Conference on International
Breast Health Care, Bethesda, MD, January 12–15, 2005.
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bese
Original
Radiotherapy
et al
Article
. Journal
for Publishing
Breast
Cancer in Limited-Resource Countries
Blackwell
Malden,
The
TBJ
1075-122X
January/February
12
12006
suppl
Breast
Blackwell
USA
Publishing
2006
Inc
ORIGINAL ARTICLE: LIMITED-RESOURCE INTERVENTIONS
Radiotherapy for Breast Cancer in Countries with Limited
Resources: Program Implementation and Evidence-Based
Recommendations
Nuran Senel Bese, MD,* Krystyna Kiel, MD,† Brahim El-Khalil El-Gueddari, MD,‡
Oladapo Babatunde Campbell, MD,§ Baffour Awuah, MD,¶ and Bhadrasain Vikram,
MD,# for the International Atomic Energy Agency
*Cerrahpasa Medical School, Istanbul, Turkey; †Northwestern University, Chicago; ‡Institut National
d’Oncologie, Rabat, Morocco; §University College Hospital, Ibadan, Nigeria; ¶Komfo Anokye Teaching
Hospital, Kumasi, Ghana; and #International Atomic Energy Agency of the United Nations, Vienna, Austria
Abstract: Radiotherapy is an essential part of the multimodality treatment of breast cancer. Applying safe and effective treatment requires appropriate facilities, staff, and equipment, as well as support systems, initiation of treatment without undue delay,
geographic accessibility, and completion of radiotherapy without undue prolongation of the overall treatment time. Radiotherapy
can be delivered with a cobalt-60 unit or a linear accelerator (linac). In early stage breast cancer, radiotherapy is an integral part
of breast-conserving treatment. Standard treatment includes irradiation of the entire breast for several weeks, followed by a boost
to the tumor bed in women age 50 years or younger or those with close surgical margins. Mastectomy is an appropriate treatment
for many patients. Postmastectomy irradiation with proper techniques substantially decreases local recurrences and improves survival in patients with positive axillary lymph nodes. It is also considered for patients with negative nodes if they have multiple adverse
features such as a primary tumor larger than 2 cm, unsatisfactory surgical margins, and lymphovascular invasion. Many patients
present with locally advanced or inoperable breast cancer. Their initial treatment is by systemic therapy; after responding to systemic therapy, most will require a modified radical mastectomy followed by radiotherapy. For those patients in whom mastectomy
is still not possible after initial systemic therapy, breast and regional irradiation is given, followed whenever possible by mastectomy.
For patients with distant metastases, irradiation may provide relief of symptoms such as pain, bleeding, ulceration, and lymphedema.
A single fraction of irradiation can effectively relieve pain from bone metastases. Radiotherapy is also effective in the palliation of
symptoms secondary to metastases in the brain, lungs, and other sites. Radiotherapy is important in the treatment of women with
breast cancer of all stages. In developing countries, it is required for almost all women with the disease and should therefore be
available. Key Words: breast cancer, developing countries, health resources, radiation oncology, radiation therapy, radiotherapy
R
adiotherapy is an essential component of the treatment of breast cancer. Depending on the stage of disease, this therapy can reduce the risk of local recurrence,
improve survival, and provide palliation of symptoms.
Available data suggest that the incidence of breast cancer
is increasing in countries with limited resources (1), which
typically have restricted or no access to radiotherapy (2–
5). Therefore, implementing and expanding radiotherapy
programs will be imperative to ensure the best possible
outcomes for women with the disease.
Address correspondence and reprint requests to: Bhadrasain Vikram, MD,
Head, Section of Applied Radiation Biology and Radiotherapy, International
Atomic Energy Agency, P.O. Box 100, Wagramer Strasse 5, A-1400 Vienna,
Austria, or e-mail: [email protected]
© 2006 The Fred Hutchinson Cancer Research Center, 1075-122X/06
The Breast Journal, Volume 12 Suppl. 1, 2006 S96– S102
In this article we review the resource requirements for
implementing a radiotherapy program in the limitedresource setting, with special reference to treating breast
cancer, and we discuss possible strategies for overcoming
barriers to a radiotherapy program. In addition, we provide evidence-based recommendations for radiotherapy
for breast cancer in such settings.
REQUIREMENTS FOR SAFE AND EFFECTIVE
RADIOTHERAPY FOR BREAST CANCER
In delivering radiotherapy for breast cancer, as for
other cancers, a health care system must strive to meet at
least basic staff and equipment requirements, each of
which plays a role in ensuring that the therapy is both safe
and effective (Table 1) (6). A major thrust of the program
in human health of the International Atomic Energy
Radiotherapy for Breast Cancer in Limited-Resource Countries • S97
Table 1. Roles of Staff and Equipment Requirements in Safe and Effective Radiotherapy for Breast Cancer (6)
Requirement
Staff
Radiation oncologist
Medical physicist
RTT
Maintenance techniciana
Equipment
Megavoltage teletherapy unitb
Dosimetry equipment
Clinical QA equipmentc
Immobilization devices
Shielding devices
Treatment planning computer system
Role(s)
Clinical evaluation, therapeutic decision, target volume localization, treatment planning, simulation/verification of
treatment plan, treatment evaluation during treatment, follow-up examinations
Quality control, computerized treatment planning, complex calculations and quality checks
Simulation/verification of treatment plan, routine calculations and quality checks, treatment
Maintenance of equipment
Radiation source
Physical quality assurance
Clinical quality assurance
Accuracy of therapy
Protection of healthy tissues such as heart, lungs, and spinal cord
Calculation of radiation distribution
a
Required if a linear accelerator (linac) is being used.
A cobalt-60 unit or linac; choice will depend on the factors discussed in the text. Breast brachytherapy is investigational at this time.
Includes a simulator (fluoroscopic or computed tomography).
QA, quality assurance; RTT, radiotherapy technologist/radiographer.
b
c
Agency (IAEA) is addressing the need for radiotherapy in
countries with limited resources (7). The IAEA has a long
track record of providing essential equipment and training
staff to safely treat patients with cancer. It has delivered
more than $57 million in radiotherapy technology to
developing member states since 1981 through the Technical Cooperation program, under which assistance is
provided to such states for establishing or upgrading
facilities for cancer treatment.
Lack of well-trained staff results in underuse or
inappropriate use of even the existing scarce radiotherapy
facilities in many countries. Therefore the IAEA provides
initial education and training as well as continuing
professional development activities for professionals in
radiation oncology and allied fields (e.g., physicians,
technicians, nurses, maintenance engineers). Another
reason for the suboptimal use of existing facilities is the
lack of a quality culture in many institutions in developing
countries. Many IAEA activities therefore focus on establishing and strengthening quality assurance programs.
The central equipment requirement for radiotherapy
for breast cancer is a megavoltage teletherapy unit, either
a cobalt-60 unit or a linear accelerator (linac). At present,
although the developing world has as many patients with
breast cancer as the developed world, it has only about
half as many radiotherapy units, with dozens of countries
having no radiotherapy at all (8). Either a cobalt unit or a
linac can be used for radiotherapy for breast cancer, but
experience in countries with limited resources has shown
that the downtime of linacs is generally considerably
greater. Any interruption to treatment due to equipment
breakdown adversely affects patients’ outcomes. The longer
or more frequent the interruptions, the worse the impact.
There have been numerous instances where, even after an
institution acquired a linac, few patients could be treated
because the proper support arrangements were not made.
There are many technical differences between cobalt units
and linacs, including the build-up region, penumbra, depth
dose, dose rate, versatility, beam profile, ease of maintenance, and decommissioning. These are discussed in detail
elsewhere (6,9,10). In addition to the teletherapy equipment, high-quality treatment by radiotherapy requires
certain quality assurance tools such as an imaging device
(a fluoroscopic or computed tomography simulator),
immobilization devices, shielding devices, a treatment
planning computer system, and tools for dosimetry.
Delivery of safe and effective radiotherapy also requires
addressing certain logistical issues. Specifically, in addition to the staff and equipment requirements, the health
care system must be able to provide the physical facility for
radiotherapy, support systems that allow delivery of therapy over a period of weeks, initiation of treatment without
long delay, and geographic accessibility to patients.
Although the initial investment in establishing radiotherapy is significant, the long life of radiotherapy equipment (20–30 years) means that the cost per patient treated
can be surprisingly modest in an efficiently run facility.
Nonetheless, given that substantial initial investment, and
in light of the competing needs in countries with limited
resources, collaborative and innovative approaches are
called for. For example, technical cooperation programs
between nations, or with international organizations such
as the IAEA (11), can aid in the establishment of radiotherapy in countries with limited resources. Advances
in telecommunications may also enable cost-effective
approaches by linking radiotherapy facilities with
Postmastectomy radiotherapy
Patients with positive axillary lymph nodes: 50
Gy in 25 fractions over 5 weeks, administered five times
per week to the chest wall and supraclavicular area; the
axilla is included only if axillary dissection was inadequate
Patients with negative axillary lymph nodes who
have multiple adverse features (e.g., primary tumor larger
than 2 cm, unsatisfactory surgical margins, lymphovascular
invasion): 50 Gy in 25 fractions over 5 weeks, administered
five times per week to the chest wall
Patients who have a response to systemic therapy
and can undergo breast-conserving surgery: whole-breast
radiotherapy
Patients who have a response to systemic therapy
and require radical or modified radical mastectomy:
postmastectomy radiotherapy
Patients whose tumors remain unresectable after
two regimens of non-cross-resistant chemotherapy:
whole-breast radiotherapy (including regional lymph nodes)
followed, if possible, by mastectomy; if mastectomy is still
not possible, then a further boost to the gross tumor using
shrinking fields
Early stage (stage I or II) breast cancer is surgically
treated by either excision of the cancer (lumpectomy) with
negative margins or a mastectomy. Disease in the axilla is
assessed by either axillary dissection or a sentinel node
biopsy followed by axillary dissection if the sentinel node
is positive. Radiotherapy is delivered to the breast in the
case of breast-conserving surgery, or is delivered to the
chest wall after mastectomy if axillary lymph nodes are
Whole-breast radiotherapy
All patients: 50 Gy in 25 fractions over 5 weeks
or 42.5 Gy in 16 fractions over 22 days, administered five
times per week
Patients ≤50 years of age and patients with close
surgical margins: an additional 16 Gy boost to the
tumor bed
Whole-Breast Radiotherapy
Locally advanced breast cancer
Radiotherapy has an important role in the treatment of
breast cancer at every stage. In early stage disease, radiotherapy is an integral part of breast-conserving therapy.
For patients with more advanced cancers, adjuvant radiotherapy substantially decreases the risk of local recurrence, and also improves the survival among patients with
positive axillary lymph nodes (13 –16). In locally advanced
disease (often the most common presentation in the
limited-resource setting), after neoadjuvant systemic therapy,
patients require both radiotherapy and modified radical
mastectomy in an effort to achieve local control. In addition, radiotherapy is a valuable tool for the palliation of
distant metastasis such as bone and brain metastases, as
well as palliation for local recurrences.
Delivery of radiotherapy for breast cancer in the doses
needed and according to the schedules supported by
current evidence (discussed subsequently and summarized
in Table 2) is essential for its effectiveness, as well as its
safety. Ongoing studies are exploring the possibility of
using lower doses or shorter schedules, which would reduce
costs and workloads, but their use should be considered
investigational at this time.
Breast cancer requires multimodality treatment that, in
addition to radiotherapy, includes surgery and systemic
therapy (chemotherapy, hormonal therapy, or both).
Approaches for integrating these therapies for safe and
effective breast cancer treatment in the limited-resource
setting are given in an accompanying guideline (17). Here
we elaborate on delivery of radiotherapy in such settings
by discussing the evidence base, doses and schedules, and
issues such as sequencing with other therapies.
Table 2. Recommended Doses and Schedules for Radiotherapy for Breast Cancer
RECOMMENDATIONS FOR RADIOTHERAPY FOR
BREAST CANCER
Stage I or II breast cancer
Metastatic or recurrent breast cancer
differing levels of treatment capability and expertise by
digital networks or satellite (12). Continued exploration
of such strategies will be essential to meet the goal of
delivering radiotherapy to all women with breast cancer
who need it in limited-resource countries.
Patients with single symptomatic bone
metastases: local-field radiotherapy with a single
8 Gy fraction
Patients with multiple symptomatic bone
metastases: wide-field (e.g., hemibody) radiotherapy with
12 Gy in four fractions over 2 days, or—if preceded by
intravenous ondansetron and dexamethasone—6–8 Gy
in a single fraction
Patients with symptomatic brain metastases:
steroids and whole-brain radiotherapy (30 Gy in 10
fractions or 20 Gy in 5 fractions); highly selected patients
may benefit from craniotomy or radiosurgery
Patients with symptomatic soft tissue
metastases: irradiation of the metastases
Patients with locally recurrent breast cancer after
mastectomy: irradiation of the chest wall and regional
lymph nodes, with a further boost to the gross tumor using
shrinking fields
S98 • bese et al.
Radiotherapy for Breast Cancer in Limited-Resource Countries • S99
involved or certain other adverse features are present
(discussed in a later section).
Randomized trials have shown that there are no significant differences in disease-free or overall survival between
patients treated by mastectomy and those treated by
breast-conserving surgery and whole-breast radiotherapy
(18–21). The main benefit of breast-conserving surgery
and radiotherapy is preservation of body image and a better
quality of life. Randomized studies evaluating the use of
breast-conserving surgery plus adjuvant systemic treatment have demonstrated higher rates of local recurrence
than after breast-conserving surgery plus radiotherapy
and adjuvant systemic treatment, but major differences in
survival have not been observed (22,23). In view of the
higher rates of local recurrence, breast irradiation is
currently recommended for most patients who undergo
breast-conserving surgery. Breast-conserving surgery
requires 1) high-quality breast imaging (mammography
and ultrasound) and pathology services to ensure tumorfree margins of excision, 2) surgeons experienced in
achieving a good cosmetic result with negative pathologic
margins of excision, and 3) radiotherapy facilities.
Radiotherapy should be started without a long delay
after breast-conserving surgery because a prolonged postoperative interval may compromise local control (24,25).
When chemotherapy is indicated, radiotherapy may follow chemotherapy, but for patients with close surgical
margins, radiotherapy can be given first. In a prospective
randomized trial, there were no significant differences in
time to any event, distant metastasis, or death, whether
radiotherapy or chemotherapy was given first (26).
Concomitant chemoradiotherapy can reduce the overall
treatment time, but the concomitant administration of
anthracyclines should be avoided because of the risk of
increased skin and cardiac morbidity (27). Regimens such
as cyclophosphamide, methotrexate, fluorouracil (CMF)
are cost effective and can be given concomitantly with
irradiation (28,29). Radiation therapy should be completed without undue prolongation of the overall treatment time (30).
Most local relapses are observed in the vicinity of the
primary tumor bed, and for this reason, partial breast irradiation is currently under investigation. The target volume
is smaller; therefore the radiation can be accelerated and
completed in only 1 week. However, robust long-term
results and toxicity evaluations are not yet available. At
present, after breast-conserving surgery, the target volume
for irradiation should include the whole breast.
The most common schedule for irradiation used in clinical practice is 50 Gy in 25 fractions to the whole breast,
administered daily, five times per week. In a large randomized trial, however, a shorter fractionation schedule (42.5
Gy in 16 fractions over 22 days) proved to be just as safe
and effective (31). Other schedules (e.g., 40 Gy in 3 weeks)
are currently under investigation (32). The shorter schedules
permit more efficient use of resources, and thus more
women can be treated with the existing equipment and
personnel in countries with limited resources.
Evidence suggests that boost radiation to the lumpectomy site significantly improves the local control rate for
women 50 years of age or younger (33). Therefore a 16 Gy
additional radiation dose to the tumor bed is recommended
for younger women, as well as for women with close
surgical margins. The boost dose can be delivered by
photons, electrons, or brachytherapy (34).
Postmastectomy Radiotherapy
Early Stage Breast Cancer Total mastectomy remains an
appropriate treatment for many patients with breast
cancer in the developing world. Radiotherapy following
mastectomy substantially improves local control (35,36).
Local recurrence after mastectomy usually occurs within
the first 12–24 months, even after adjuvant systemic
therapy, most commonly in the chest wall, followed by the
supraclavicular fossa. The major risk factor is positive
axillary lymph nodes (37). Other risk factors are large
tumor size, positive margins of resection, and lymphovascular invasion (38).
Studies have demonstrated that the use of postmastectomy irradiation improves overall survival in women with
axillary lymph node-positive breast cancer (13–16). Postoperative radiotherapy to the chest wall and supraclavicular
area is therefore recommended for all patients with four
or more positive lymph nodes and should be considered
for patients with one to three positive lymph nodes. Axillary irradiation is given only to those patients who did not
undergo an adequate axillary dissection. Irradiation of the
axilla is, in general, not recommended (37,39). The axillary
and internal mammary regions are relatively uncommon
sites of local recurrence (in comparison with the chest
wall), while the morbidity from axillary irradiation (e.g.,
arm edema) or internal mammary irradiation (e.g., cardiac
toxicity) is of concern (40,41). If sophisticated techniques
of modern treatment planning and delivery are available,
internal mammary irradiation is recommended for patients
with clinically or pathologically positive internal mammary
lymph nodes, and is considered for patients if the primary
tumor is located at the inner quadrant with the other adverse
risk factors. On the basis of a recent retrospective review,
postoperative chest wall irradiation should also
S100 • bese et al.
considered for patients with negative axillary lymph nodes
who have multiple adverse features (e.g., a primary tumor
larger than 2 cm, unsatisfactory surgical margins, or
lymphovascular invasion) (38).
A regimen of 50 Gy in 5 weeks is widely used for postoperative irradiation, but more rapid fractionation regimens (e.g., 40 Gy in 3 weeks) are under investigation in
randomized trials, some already completed (32,42). Such
approaches, with appropriate quality control, may be particularly beneficial in countries with limited resources by
reducing the radiotherapy workload and costs.
Information on the impact of the sequencing of postmastectomy radiotherapy and systemic chemotherapy on
survival is limited. At present, radiotherapy is most commonly delivered after the completion of chemotherapy in
patients with node-positive disease.
Locally Advanced Breast Cancer In developing countries,
a considerable proportion of the patients present with
locally advanced breast cancer (LABC) that is inoperable
due to direct extension to the ribs, intercostal muscles, or
skin; edema (including peau d’orange) or ulceration of
the skin of the breast; satellite skin nodules confined to the
same breast; inflammatory carcinoma; metastases to the
ipsilateral internal mammary lymph nodes; or metastases
to the ipsilateral supraclavicular lymph nodes. Patients
with LABC have a high probability of distant metastasis
as well as a high probability of local recurrence. Initial
treatment of LABC is systemic therapy. Approximately
80% of inoperable tumors treated with chemotherapy
may regress sufficiently to become operable (43,44). Neoadjuvant hormonal therapy is beneficial in patients with
hormone receptor-positive tumors (45). Following systemic therapy, most patients require a radical or modified
radical mastectomy, followed by radiotherapy (selected
noninflammatory breast cancers exhibiting a complete or
partial clinical response to initial chemotherapy can be
considered for breast-conserving surgery followed by
radiotherapy). Unresectable tumors that remain unresectable even after two regimens of non– cross-resistant chemotherapy should be irradiated. This should be followed,
whenever feasible, by mastectomy. If mastectomy is still
not possible, then definitive radiotherapy can be applied,
with a further boost to the gross tumor using shrinking
fields.
long as possible. Patients with bone metastases comprise
the largest group receiving palliative radiotherapy. Radiotherapy can prevent pathologic fractures in patients with
lytic lesions in weight-bearing bones. Traditionally localfield radiotherapy has been used for patients with symptomatic bone metastases. Evidence suggests that significant
symptomatic relief can be obtained with a single 8 Gy
fraction, a very cost-effective strategy (46–49). Wide-field
radiotherapy (e.g., hemibody irradiation) can be used for
patients with multiple bone metastases. The IAEA conducted a multinational, prospective, randomized trial that
showed that hemibody radiation of 12 Gy in four fractions
delivered over 2 days was a suitable treatment regimen
(50). Others have suggested that hemibody irradiation of
6 – 8 Gy in a single dose is also safe and effective, if preceded
by intravenous ondansetron and dexamethasone (51).
Patients with brain metastases can survive for many
months after radiotherapy. Whole-brain irradiation and
steroids are recommended for alleviating symptoms from
brain metastases. Selected patients with no extracranial
disease who have one or few metastases and a good
performance status can be treated with craniotomy or
radiosurgery if available (52).
Palliative radiotherapy is also useful for patients with
soft tissue metastases causing pain, discharge, or bleeding.
Locally recurrent breast cancer after mastectomy can
occasionally be cured with radiotherapy to the chest
wall and regional nodes. The likelihood of tumor control
increases with a longer disease-free duration since the
initial therapy and resection of the recurrent disease, and
also depends on the number of sites involved.
CONCLUSION
Delivery of safe and effective radiotherapy for breast
cancer requires a substantial investment of resources.
However, this therapy is important in the treatment of
women with breast cancer of all stages. With appropriate
treatment, many women are cured of breast cancer, while
many others live longer with the disease and have a better
quality of life. Use of evidence-based doses and techniques
is essential for ensuring the best possible clinical outcomes
and avoiding complications. In developing countries,
radiotherapy is required for almost all women with breast
cancer and should therefore be available.
Palliative Radiotherapy
In patients with metastatic breast cancer, radiotherapy
is an effective tool for palliation of the symptoms. The goal
is to prevent or relieve symptoms or loss of function for as
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remennick
Original
Barriers
toArticle
Breast
Screening
Blackwell
Malden,
The
TBJ
1075-122X
January/February
12
12006
suppl
Breast
Blackwell
USA
Publishing
Journal
Publishing
2006
Inc in Multicultural Societies
ORIGINAL ARTICLE: SOCIOCULTURAL BARRIERS TO CARE
The Challenge of Early Breast Cancer Detection among
Immigrant and Minority Women in Multicultural Societies
Larissa Remennick, PhD
Bar-Ilan University, Ramat Gan, Israel
Abstract: A sociological view of the barriers experienced by women from traditional cultures, both in their native countries
and as immigrants and minorities in multicultural western societies, in preventive health care generally and in breast screening
specifically, is essential not only to understand patterns of late-stage diagnosis, but also to design successful interventions and
programs. Breast cancer is a unique disease, as its name ties together a multisymbolic organ of the female anatomy and a potentially fatal affliction, the treatment of which commonly is a body-mutilating procedure (mastectomy). Because of its special nature,
breast cancer is shrouded in fears, myths, and connotations reaching far beyond the objective clinical understanding of the disease.
Many women do not use available breast-screening services and present with advanced symptoms. To help women detect and
treat breast cancer early, health care providers and policymakers should try to understand their predicaments and the factors influencing their decisions. Structural barriers include such socioeconomic factors as poor health insurance, distance to medical facilities,
and inability to take time off from work, while organizational barriers include difficulty in navigating complex health care systems
and interacting with medical staff. Psychological and sociocultural barriers include poor health motivation, denial of personal risk,
fatalism, mistrust of cancer treatments, and the fear of becoming a burden on family members. These barriers can often preclude
proactive breast screening or rapid response to symptoms, even when breast cancer awareness is rather high. Moreover, in many
traditional societies, especially Muslim ones, women’s decisions and actions are controlled by men, and men may be unaware of
or disapprove of breast screening. This article discusses several approaches to lowering the described barriers, including specially
tailoring educational programs that dispel cancer myths, involving men in breast cancer detection efforts, implementing cultural
competence training for mainstream health care providers, and recruiting minority health care professionals to enable better outreach to their coethnics. Key Words: attitudes, barriers, beliefs, breast cancer, cancer fears, cultural diversity, customs, fatalism, gender roles, health
motivation, immigrant and minority women, screening
B
reast cancer is a unique disease, as its name ties
together a symbolic and erotically charged organ of
the female anatomy and a potentially fatal affliction, the
treatment of which is based on a body-mutilating procedure (mastectomy). Because of its special nature, breast
cancer is shrouded in fears, myths, and connotations reaching far beyond the objective clinical understanding of the
disease. A gap is often found between knowledge and
practice: many women who are aware of breast cancer
risk do not use available breast-screening services (1–4).
To help women detect and treat breast cancer early, health
care providers and policymakers must attempt to understand their predicaments and the factors influencing their
decisions about breast screening.
This article offers a sociological view of the barriers
experienced by women from traditional cultures (both in
their native countries and as immigrants and minorities in
multicultural western societies) in preventive health care
generally and in breast care specifically. The empirical
data for this overview derive from the literature, as well as
research among Russian women who have immigrated to
Israel—a multicultural society that includes Jews originating from more than 100 countries and Arabs (predominantly Muslims, but also Christians and Druze). The
research included a survey among a national sample of
women age 35 years and older as well a series of personal
in-depth interviews with these women about their perceptions of breast cancer. The methodological details of these
studies have been previously described (1,2). In addition,
this analysis draws on the Israeli and international literature on the social and behavioral aspects of breast cancer
(3–7).
Address correspondence and reprint requests to: Larissa Remennick, PhD,
Department of Sociology and Anthropology, Bar-Ilan University, 52900 Ramat
Gan, Israel, or e-mail: [email protected]
CONTEXT OF WOMEN’S LIVES
© 2006 The Fred Hutchinson Cancer Research Center, 1075-122X/06
The Breast Journal, Volume 12 Suppl. 1, 2006 S103–S110
It is impossible to understand women’s health decisions
and actions outside of the general context of their lives.
S104 • remennick
Many societies with low per capita income and limited
medical resources are at the same time male-dominated
societies in which women have lower social status and
fewer personal resources (8). Both globally and in every
country individually, women comprise a majority among
the poor, uneducated, and unemployed (8). Minority
women in western countries are often marginalized, isolated from the mainstream culture, and have limited command of the dominant language. Most of these women
both work for wages (usually in low-skilled and poorly
paying positions) and serve a second shift at home, where
they care for their husbands, children, and elderly parents.
As a result of these multiple roles, women’s personal agendas are overburdened and have little room left for health
concerns, especially preventive ones, which are perceived
as less pressing. Because of low health motivation generally and the traditional emphasis on curative care (i.e.,
seeking help when the problem is already acute and needs
treatment), such women give a low priority to preventive
activities such as breast self-examination (BSE), wellwoman checkups with clinical breast examination (CBE),
Papanicolaou tests, and mammography (9,10). This selfneglect does not necessarily reflect ignorance, as many
women are aware of breast cancer risk; rather it reflects
social and economic disadvantage augmented by negative
emotional reactions to cancer.
An example of differing behavioral patterns that likely
reflect the economic and psychosocial differentials between
specific groups of women is provided by Israeli data
collected in the mid-1990s on compliance with recommended biannual mammography (which is accessible for
all citizens of Israel) among women age 50–75 years. The
rate of actual screening varied from 60% for Israeli-born
Jewish women to 40% for Russian immigrant women to
20% for both Ethiopian immigrant and Israeli Arab
women (11). Of note, however, after a targeted intervention among Israeli Arab women that entailed both a media
campaign and deployment of mobile mammography units
in their communities, the rate of screening among those
younger than 60 years of age increased between the mid1990s and 2003–2004 from about 25% to 60%—a rate
now almost equal to that among Israeli-born Jewish
women (12). This marked improvement suggests that culturally tailored interventions can overcome barriers to
breast screening among minority groups. Similar cases of
a rapid increase in women’s participation in breast-screening
activities after culturally sensitive educational and clinical
interventions have been reported for several minority
groups in the United States, such as Cambodian immigrants
in the Midwest (13). To ensure the success of such pro-
Table 1. Barriers to Breast Cancer Screening among
Immigrant and Minority Women in Multicultural
Societies
Structural barriers
Lack of or limited health insurance
Long distance to a screening facility
Lack of transportation
Inability to take time off from work
Inability to pay for child care
Organizational barriers
Difficulty understanding and navigating the health care system
Language barriers between women and providers
Arrogance or brusqueness of medical staff
Lack of female providers
Psychological barriers
Fear of cancer
Denial of susceptibility
Fatalism, often stemming from religious beliefs
Fear of and lack of knowledge about cancer treatment
Belief that treatment is futile
Sociocultural barriers
Complete dependence of women on men in some cultures
Subservient status of women in the family and the household
Possibility of being abandoned after a diagnosis of breast cancer
grams, it is important to identify the factors shaping
help-seeking behavior among disadvantaged and minority
women (14).
BARRIERS TO EARLY DETECTION OF BREAST
CANCER
A variety of structural, organizational, psychological,
and sociocultural barriers preclude many women in
multicultural societies from using breast-screening services
(Table 1). Let us look at each of these more closely.
Structural Barriers
Structural refers to the social factors related to women’s
place in the social system, with the ensuing personal
resources and opportunities. To begin with, many women
in developing countries, as well as minority women in the
West, do not have health insurance that includes access to
preventive services. In the United States alone, more than
25 million women have no access to health care except for
emergency care; another 40 million have basic insurance
plans with prohibitive deductibles and copayments that de
facto preclude women from using preventive services.
Among those uninsured and underinsured, more than
two-thirds are members of racial and ethnic minorities
(15). When they do have formal access to preventive services, many poor women cannot use them because of long
travel distances and the lack of transportation, and an
Barriers to Breast Screening in Multicultural Societies • S105
inability to take time off from work or pay for child care
during their absence (14).
Organizational Barriers
The next tier of barriers, organizational barriers, reflect
difficulties that are built into the medical encounters
between minority women and the mainstream medical
institutions: understanding the complex referral system
and the nexus between diagnostics and treatment;
communicating in their inadequate English or other host
language; and facing arrogance and brusqueness from
physicians, nurses, and administrative staff. Gender-related
barriers are also at work: the need to expose one’s breasts
for examinations performed by often male physicians,
surgeons, or radiology technologists. The last factor makes
breast examinations especially difficult among religious
Muslim women, for example, because rules of Islam strictly
prohibit nudity and self-exposure in front of any man other
than one’s husband. For many such women, shame is worse
than disease and death, and they will not visit women’s
health clinics unless they are staffed by women (16,17).
Psychological Barriers
However salient the organizational issues are precluding women from using breast-screening services, the psychological barriers are even more common and pervasive.
They all ensue from a deeply entrenched fear of cancer,
which is perceived as a universally fatal disease, and hence
any thought of cancer triggers multiple psychological
defense mechanisms. One such mechanism is denial of
one’s own susceptibility, a belief that “this cannot happen
to me.” This denial is especially common among women
from societies that have a low or moderate risk of breast
cancer, who have no personal experience of having a
relative or a friend with this disease, but it is also found
among women in high-risk populations (1,2,16,18). The
extension of this outlook is avoiding any early testing or
other preventive activities before trouble strikes in full. In
the words of one of my immigrant informants in the Israeli
study (2): “I have no time for potential troubles, having
enough actual ones; I am also not going to see my body as
a foe and test it endlessly for signs of disease. This in itself
is morbid.” Another woman expressed a similar view: “If
I discover a lump, I will go to a doctor of course, but I am
not going to look for it on purpose.” Similar attitudes
toward one’s body and the breasts as potential foe have
also been found among women in North America in studies
trying to elucidate causes for low adherence to BSE (6,19).
Another typical mode of psychological defense is fatalism, that is, the belief that one’s destiny is determined by
some higher power and one has no control over disease,
life, and death. Specifically, a woman may believe that if
she is destined to get breast cancer, she will get it, and then
her survival or death is all a matter of luck, fate, or providence, whichever she believes in. This outlook is, of course,
common among devout women of any religion, for example,
being shared by both ultraorthodox Jews and Muslims in
Israel (16), but it also is not uncommon among secular
women. Moreover, in many traditional cultures, disease is
interpreted as punishment for sins (one’s own or those of
the family, clan, or others), and medical intervention in
the intentions of the deity makes it even more sinful (16).
The fatalist view of cancer is often augmented by the
frightening prospect of mutilation of the body (mastectomy) as its treatment; a woman without a breast or
breasts is a castrate, and her femininity and body selfimage are greatly diminished (16). In many low-resource
countries, breast-conserving therapy may not be available,
and in settings where it might be an option, less educated
women may know little about recent advances in the
surgical treatment of breast cancer that allow breast preservation, provided diagnosis is timely. In addition, some
religions prohibit amputation of any body parts because
a deceased person must be buried whole.
Because it is common that, in the majority of women
with breast cancer in low-resource settings, the diagnosis
is made relatively late, the prognosis is often poor regardless of the severity and length of treatment, fully supporting the conclusion of those around patients that medical
intervention is futile. Apart from the fear of mutilation,
many women are terrified by cancer treatments that are
perceived to cause endless and futile suffering. This fear is
more common among those who have observed others
close to them being treated by the fearsome trio of “slash,
burn, and poison” (surgery, radiation therapy, and chemotherapy), with ensuing serious adverse effects such as
edema, nausea, hair loss, weakness, and weight loss (20).
In many less developed countries, effective clinical management of the adverse effects of cancer therapies is precluded by inadequate facilities and staff training, a lack of
sufficient and effective medication, and a lack of cultural
emphasis on patients’ quality of life. As a result, the amount
of suffering corollary to cancer treatment is indeed overwhelming, for both patients and their caregivers. For some
women, this image of suffering is a strong additional disincentive for cancer screening (5).
Sociocultural Barriers
A major sociocultural barrier to breast screening in
many traditional societies, especially Muslim ones, is that
S106 • remennick
women’s decisions and actions are controlled by men, and
men may be unaware of or disapprove of screening.
Furthermore, in many male-dominated societies, women’s
social status is totally dependent on their roles as wives,
mothers, and housekeepers, as they have no independent
income or other sources of identity and self-esteem (16).
Women are perceived (and perceive themselves) as subservient to the needs of the family, and their self-worth rests
on their ability to provide services to men, children, and
elders in their households. Therefore serious disease such
as breast cancer completely jeopardizes women’s status in
the nuclear and extended family, as they can no longer
function in the household and bear children, and, on the
contrary, become dependent on others for help and care.
Men are often unwilling or unable to cope with this role
reversal, and sick wives are eventually sent away or divorced,
especially when other wives or lovers are available (e.g., in
societies practicing polygamy). Thus in such societies, the
diagnosis of breast cancer, with subsequent amputation of
the breast(s) and long-term disability, means a de facto social
death of a woman. It is no wonder that women will do anything in their power to delay and deny any signs of illness,
let alone try to purposely detect the disease by screening (16).
BREAST SCREENING AMONG OLDER WOMEN
Breast cancer screening in older women is a particularly
useful example of the interplay between the barriers listed
above and the late stage of breast cancer diagnosis. Many
studies of screening behavior in Israel and the United
States (among other countries) have shown that the group
least likely to use breast-screening services is women older
than 60 years of age (1,6,7,21). Low health motivation is
typical for older women in many cultures because of their
“relational” view of themselves as secondary and subservient to the needs of those close to them; that is, as givers
rather than receivers of care and attention (18). Furthermore, many older women believe that breast cancer strikes
younger women and that after menopause the disease is
no longer a health concern for them. This belief has been
reinforced over the years by the images of younger women
in advertisements and promotional campaigns related to
mammography and breast cancer treatments (1,6,20,21).
Finally, older women who also belong to marginalized or
disadvantaged social groups experience higher than usual
barriers to health care for all of the aforementioned
reasons (9,18). The resulting paradox is that while breast
cancer risk increases with increasing age in many countries,
the actual use of screening among postmenopausal women
declines as they get older.
In the context of immigration, older women may be
especially disadvantaged. Such women typically have little
(if any) income from public subsidies and depend on the
support of their grown children and grandchildren to get
around in the new society. As a result of their poor command of the new language and their isolation from the
mainstream, these women cannot use the available health
services. In our survey among Russian immigrant women
age 35 years and older in Israel (1), respondents older than
60 years of age had the lowest frequency of gynecologic
visits, CBEs, and mammograms. Low awareness of their
rights as patients and flawed communication with providers
were common in this group. At the same time, older
women often held fatalistic attitudes toward cancer, did
not believe that early diagnosis could save their lives, and
generally doubted that the whole “fuss” over cancer was
worthwhile (2).
An additional finding was that many older immigrant
women felt very uncomfortable visiting gynecologic
clinics ostensibly meant for women in their reproductive
years. In interviews with older Russian immigrant women
in Israel, we discovered a cluster of life cycle-related beliefs
that may explain these women’s lack of interest in cancer
screening (2). These beliefs pertained to the nature of
womanhood at different ages and led these older women
to believe that they were way past the life stage at which
they had to take care of their reproductive system. When
asked to specify the types of problems that cause women
to visit gynecologists, most informants mentioned menstrual cycle irregularities, fertility problems, prenatal care,
sexually transmitted diseases, cervical lesions, pelvic pains,
irregular vaginal discharge, and general periodic checkups.
None mentioned any cancer-related tests or procedures.
At the same time, many informants opined that the whole
range of gynecologic conditions, including reproductive
cancers, mainly occur in younger women. Hence these
older women no longer saw themselves as needing gynecologic care, and visiting obstetrics and gynecology clinics
was therefore perceived as irrelevant and even ridiculous.
To make matters worse, the need to talk with a Hebrewspeaking male gynecologist was an ordeal for many of
these women, and if they visited gynecologists at all, it was
only because of complaints and symptoms. When there
was no Russian-speaking or female gynecologist in their
town or neighborhood, and a female family member could
not accompany them to the clinic to help translate, they
just canceled visits.
In addition, some older women (especially those in
their 70s) felt that their health and illnesses were of minor
relevance or interest to anybody and that their advanced
Barriers to Breast Screening in Multicultural Societies • S107
age made any intensive medical care pointless (2). One
woman expressed the following: “There is no point in
looking for small tumors in my sagging breasts. Even if
they find something and I get my breast cut off, how much
time do I have left anyway? I prefer to finish my days with
both breasts intact—with or without cancer” (Zelda, age
73 years). These women understood their value as human
beings mainly in terms of their capacity to be helpful to
their children and grandchildren during the remainder of
their lives. In addition, they perceived a focus on self-care
(including seeking preventive health services) as excessive
and selfish. Another woman stated the following: “Thank
God, I am still able-bodied and can help my daughter with
her two kids, so that she can get herself established as a
specialist in Israel. What good would it make if I started
rushing between medical offices checking myself for this
and that? They would surely find some disease, as nobody
of my age is totally healthy. But it is a waste of time, since
you cannot live forever, and anyway, who treats old
people seriously? The time that I still have to live I want
to give to my grandchildren, not to myself” (Ludmila, age
74 years).
In sum, older immigrant women expressed a mixed set
of cultural beliefs and communication barriers that
merged to produce low health motivation and low use of
the available preventive services. Our findings in Israel
are in line with those of other studies among older
minority women in the United States and Europe
(6,9,18,21). Such women could definitely benefit from
a proactive and culturally sensitive outreach campaign,
one that includes health care workers and is designed to
improve their health motivation, reduce cancer-related
fears, and increase supportive care among health care
workers.
POSSIBLE SOLUTIONS AND POLICY
APPROACHES
As described above, in multicultural societies, several
types of barriers can preclude women from marginalized
and disadvantaged social groups from using breastscreening services. Some of these barriers reflect limited
access to preventive health services, whereas others stem
from a lack of understanding, interpersonal skills, sensitivity, and motivation among health care providers to
accommodate marginalized groups. Even when breastscreening services are accessible and women-friendly, they
fail to attract many women because of psychological and
sociocultural factors such as fear of a cancer diagnosis and
treatment, and subsequent disability and dependence on
family members. For other women, breast cancer is a far
more remote and unreal concern compared with other,
more immediate problems they might have, such as excess
weight, aging, musculoskeletal pains, and menopausal
symptoms. Women in their 60s and 70s, who may have
multiple age-related health problems such as hypertension, heart disease, and diabetes often believe that breast
cancer can no longer strike them because it occurs in
younger women. Within the system of women’s competing health concerns, breast cancer may have a rather low
position, especially in low- to moderate-risk population
groups (13,22), in which women seldom have first-hand
encounters with this disease in other women. A better
understanding of these women’s predicaments and beliefs
allows us to suggest some viable approaches to lowering
the existing barriers and achieving greater participation of
women from minority or other disadvantaged social
groups in early detection programs (Table 2).
Macrolevel Approaches
Policymakers and health care providers should consider several macrolevel approaches, which address the
problem at the level of the population and the health care
system. First, although there are common denominators,
no single breast cancer education and early detection program can meet the needs of all social and cultural groups
of women. Programs in different countries (and among
social groups within countries) should draw on a combination of general and global evidence-based guidelines
with careful assessment of the needs of specific communities (23,24). These community needs assessments should
collect information on the general roles and social statuses
of women vis-à-vis men (i.e., gender relations), the extent
of women’s economic independence and the resources
they have access to (including health insurance, transportation, and command of the dominant language), and the
common epidemiologic and health profiles (to determine
which issues predominate on women’s personal health
agendas). The most efficient and time-saving method of
community needs assessment is conducting focus group
discussions with local leaders (both formal and informal),
grassroots community and health care workers (e.g., nurses
and social workers), and women belonging to the social or
ethnic groups one wishes to reach (e.g., recent immigrants,
religious minorities, the unemployed) (23,25,26). These
discussions will provide more specific information on the
barriers to breast health care experienced by these defined
groups of women (14).
Second, it is important to ensure actual access to breastscreening services and provision of these services in an
S108 • remennick
Table 2. Approaches to Improving Use of Breast-Screening Services among Immigrant and Minority Women
in Multicultural Societies
Macrolevel approaches
Conduct community needs assessments
Ensure women’s access to breast-screening services
Motivate health care providers to perform screening and to ensure follow-up
Train providers in culturally competent care for immigrant and minority women
Include more immigrant and minority providers in screening activities
Train community outreach workers
Increase the involvement of men in breast cancer detection
Educate religious and cultural authorities about breast cancer and early detection
Involve alternative and traditional healers in breast cancer advocacy
Engage breast cancer survivors in educational and screening efforts
Microlevel approaches
Empower women and improve their self-efficacy and self-care
Educate women about navigating complex health systems
Dispel popular myths about cancer and breast cancer
Encourage a proactive approach in cancer detection
Educate women about contemporary cancer therapies
Elevate the ranking of breast health on the list of women’s health concerns
efficient and women-friendly way. Otherwise, nascent
interest in the screening services among women “pioneers”
will quickly wane and the negative message passed from
one woman to the next by the grapevine will quickly kill
the initiative. Unfortunately, in countries with limited
health care resources, many providers are reluctant to
undertake breast screening because an influx of asymptomatic women (often frightened and poorly informed) into
the clinics means a sharp increase in their workload, perhaps
with no extra remuneration, as the experience of several
east European countries suggests (Soldak T, Director of
Belarusian Breast Cancer Screening and Early Diagnosis
Project, personal communication). In addition, in countries
with scarce medical resources, generally the curative paradigm dominates over the preventive one, which is seen as
a luxury despite its proven cost-effectiveness; this agenda
needs to be gradually shifted in favor of prevention and
early detection. Hence organizational measures should be
taken to boost the motivation of health care providers to
talk with patients about early detection and to conduct
screening tests, and to ensure an efficient nexus (referral
system) connecting positive findings with subsequent
diagnostic and treatment services that will be easy for
women to navigate regardless of their education, their
language skills, and other potential barriers. Experience
shows that a useful approach to coordination between
various steps in breast cancer diagnosis and treatment
is appointing special staff members (usually nurses) as
linkage workers (i.e., “navigators”), whose job it is to be
in touch with both women and service providers (27).
Other macrolevel and organizational approaches to delivering an effective screening program include the following:
• Training mainstream health care providers (physicians,
nurses, other medical staff) in culturally competent care
for minority women with special needs by informing
them of the cultural barriers and other issues discussed
above.
• Including more health care workers with immigrant or
minority backgrounds in breast-screening activities, as
these individuals are the best outreach agents for their
coethnics, with whom they share a common language
and culture.
• Training community outreach workers—laywomen from
the same communities—who could spread the message
of breast screening and educate other women in its
basics. For example, the positive role of “lay helpers,”
in this case, women from the same cultural and social
network who receive special training in breast-screening
outreach, has been shown to boost mammography
participation among older black women in the United
States (28). Efforts involving lay outreach workers in
other health areas, such as AIDS and tuberculosis, have
similarly proved to be very successful, both in developing countries and among ethnic minorities in the United
States (29).
• Increasing involvement of men in breast cancer detection, because in some societies, without men’s approval,
encouragement, and support, their wives, sisters,
daughters, lovers, and other female associates will rarely
visit clinics. This is especially true in Muslim cultures,
in which men largely control women’s options and
decisions (30). In other traditional cultures, such as
in various Latino minority populations in the United
States, men are less controlling but may still exert strong
Barriers to Breast Screening in Multicultural Societies • S109
influence on their female partners’ behaviors. One study
has shown a considerable lack of knowledge about female
cancers and a lack of concern about early detection of
such cancers among Latino men, especially younger
ones (31). Special educational programs targeting men
can potentially be very effective in changing women’s
motivation.
• Educating relevant religious and cultural authorities
(whose advice women seek about different lifestyle and
moral matters) about breast cancer and the benefits
of early detection. These authority figures may include
rabbis for ultraorthodox Jewish women, sheiks for
Muslim women, and clergy for observant Catholic
women. A recent study has shown that a network of
church activists can act as facilitators and encourage
older women from the same parish in their use of breast
screening (32).
• Involving alternative and traditional healers in breast
cancer advocacy in societies where women routinely
consult these healers for various health problems (22).
• Engaging breast cancer survivor groups in educating
women and implementing screening programs, as these
women are the living examples of prevailing over cancer
and the best advocates for early detection and timely
treatment.
Microlevel Approaches
Hand in hand with the macrolevel measures, there are
several microlevel approaches, which address the problem
at the level of the individual woman, for targeting social
and psychological barriers to proactive screening behavior.
These approaches include the following:
• Empowering minority and other disadvantaged women
in their interactions vis-à-vis their male partners and
other relatives, and boosting their self-efficacy and selfcare in preventive health matters, including breast care.
• Educating women about navigating complex health
systems and getting the most out of the available services,
including giving practical tips about interacting with
doctors and health bureaucracies.
• Dispelling popular myths about cancer generally and
breast cancer specifically as incurable and fatal.
• Giving women a better sense of control over their bodies
and health, and encouraging them to take a proactive
approach in cancer detection.
• Educating women about contemporary cancer therapies, especially breast-conserving surgery, as well as
supportive therapies that improve a patient’s quality
of life.
• Elevating the place of breast health on the list of women’s
health concerns relative to other diseases and conditions
they might have and teaching them simple methods of
breast awareness and periodic self-examination.
CONCLUSION
Most of the suggested interventions (especially at the
organizational level) will require some additional resources
and efforts, but in the long run they are going to be more
cost effective than purchases of expensive equipment or
building new medical facilities. These should mainly be
directed at training professionals and lay advocates who
would together bring more at-risk women to participation
in breast screening. When health care resources are limited, the measures described should help to ensure the best
possible use of the existing resources for preventive care
and women’s health. Indeed, community needs assessment alone can be a money-saving strategy, as it will allow
mapping out the services and resources in relation to
women’s needs, with subsequent more effective allocation
of funds and medical personnel. In addition, educating
physicians and other providers of breast care about women’s
concerns, lifestyles, and barriers to cancer screening will
have multiple positive effects on provider-patient interactions and ameliorate mutual misunderstandings and
tensions in cancer care.
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errico
Original
Shared
Journey
and
Article
rowden
inPublishing
Breast
Cancer Advocacy
Blackwell
Malden,
The
TBJ
1075-122X
January/February
12
12006
suppl
Breast
Blackwell
USA
Publishing
Journal
2006
Inc
ORIGINAL ARTICLE: SOCIOCULTURAL BARRIERS TO CARE
Experiences of Breast Cancer Survivor-Advocates and
Advocates in Countries with Limited Resources:
A Shared Journey in Breast Cancer Advocacy
Kathleen M. Errico, PhD, ARNP,* and Diana Rowden, MA†
*University of Washington Breast Health Center and Seattle University, Seattle, Washington; and †Susan G.
Komen Breast Cancer Foundation, Dallas, Texas
Abstract: The last decade has been marked by rapid growth in the breast cancer advocacy movement around the world.
Today such movements are well established in North America and western Europe, and are emerging and gaining momentum
in regions of the world with limited resources—Africa, Asia, eastern Europe, and Latin America. Internationally breast cancer advocates have faced the challenges of dealing with many languages, cultures, countries, and health systems. Because of these differences, existing models of breast cancer advocacy are not always appropriate or reproducible across countries. At the second
biennial Global Summit Consensus Conference on International Breast Health Care, 12 breast cancer survivor-advocates and
advocates from around the world gave statements describing the experiences of women with breast cancer and with advocacy
in their countries, and attended a roundtable meeting to discuss breast cancer advocacy from a global perspective. We used the
“long table” method to analyze their comments and identify common experiences. Although participants came from diverse settings, the analysis revealed five common experiences that were consistent across cultures: 1) the experiences and fears of breast
cancer survivors, 2) beliefs and taboos about breast cancer that hinder awareness programs and treatment, 3) the need for public
education and breast cancer awareness programs in countries with limited resources, 4) difficulty in translating the concept and
ethos of advocacy into many languages, and 5) the experiences in establishing and maintaining advocacy groups to promote
breast cancer awareness and to inform public policy. These themes constitute an action agenda for breast cancer advocacy groups
in countries with limited resources. In addition, they provide invaluable insight for policymakers, program planners, and others
undertaking efforts to improve breast cancer outcomes in low-resource settings. Key Words: advocacy, breast cancer, international health problems, language, life change events, life experiences, politics, social
support, support groups, terminology
T
he women’s health advocacy movement began in many
countries during the second half of the 20th century.
However, organizations by and for patients with breast
cancer that provide support and information for patients
have been active since the 1950s. In 1952, the American
Cancer Society started the Reach to Recovery program.
This was a group of women helping women: survivors of
breast cancer helping women with newly diagnosed disease. Members of Reach to Recovery, all of whom had had
mastectomies, provided a support group for women who
had mastectomies. This organization continues today as
an international organization supporting women throughout the world (1).
The politics of breast cancer accelerated in the United
States in the 1970s and 1980s, when well-known women
Address correspondence and reprint requests to: Kathleen M. Errico, PhD,
ARNP, University of Washington Breast Health Center, P.O. Box 1101, Langley,
WA 98260, USA, or e-mail: [email protected]
© 2006 The Fred Hutchinson Cancer Research Center, 1075-122X/06
The Breast Journal, Volume 12 Suppl. 1, 2006 S111–S116
such as Betty Ford, Nancy Reagan, Happy Rockefeller,
and Shirley Temple Black began to speak out about their
experiences with the disease (2,3). As survivor-advocates,
these American women helped raise public awareness
about breast cancer and the need for early detection programs. Women increasingly identified themselves publicly
as survivors. Breast cancer advocacy further developed as
dedicated breast cancer advocacy organizations such as YME, the Susan G. Komen Breast Cancer Foundation, the
National Alliance of Breast Cancer Organizations, and
the National Breast Cancer Coalition added a political
dimension to the provision of breast cancer information
and support (3). Today, breast cancer advocacy movements are generally well established in North America and
western Europe. The movement in the United States, one
of the most successful worldwide, provides a good example
of the development of a breast cancer advocacy movement
and its power to improve breast health care.
During the 1980s and 1990s, organizations that advocate
on behalf of breast cancer championed the Mammography
S112 • errico and rowden
Quality Standards Act, the establishment of a special fund
in the U.S. Department of the Army for breast cancer
research, the establishment and expansion of the Centers
for Disease Control and Prevention’s Breast and Cervical
Cancer Early Detection Program, and extensive increases
in federal funding for the National Cancer Institute. For
example, during the 1990s, federal government funding
for breast cancer research increased from $81 million to
more than $400 million (4,5).
Internationally breast cancer advocates have faced
the challenges of dealing with many languages, cultures,
countries, and health systems. In particular, in many
cultures it is difficult to transcend ethnic and religious differences to break the silence and profound stigma that still
surround breast cancer. Because of these many differences,
the model of breast cancer advocacy generally endorsed in
the United States is not always appropriate or reproducible
in other cultures, suggesting the need for alternative models.
In addition, the experiences of breast cancer survivoradvocates and advocates in countries with limited resources
differ significantly from those in developed countries.
Although there is an emerging sense of global breast cancer advocacy, the growth of the advocacy movement in
countries with limited resources is somewhat hindered by
the difficulty of translating the ethos of advocacy into many
languages and cultures. Furthermore, resource-constrained
countries have differing financial needs, resource limitations, social barriers, and competing illnesses that frame
how breast cancer advocacy can be implemented.
To identify commonalities and differences in the experiences of breast cancer and in the development of breast
cancer advocacy movements in limited-resource settings,
we undertook a qualitative analysis of statements and
comments provided by breast cancer survivor-advocates
and advocates at a recent international summit.
Each of four sessions of the summit began with a 15minute introductory statement by a breast cancer survivoradvocate or advocate from a country with limited resources
in which she described her own experience or that of
women from her country with breast cancer and advocacy. In addition, a 2-hour Advocates Roundtable Meeting provided an opportunity for survivor-advocates and
other breast cancer advocates from around the world to
discuss breast cancer advocacy from a global perspective.
The meeting was facilitated by a representative of the
Komen Foundation (D.R.) and was attended by 12 participants, each representing a different country (Belarus,
Brazil, Canada, Chile, China, Ghana, Greece, India, Italy,
Kenya, Malaysia, and the United States).
In an effort to understand the commonalities and differences in experiences of breast cancer survivor-advocates
and advocates from countries with limited resources, we
analyzed the introductory statements from the summit
sessions and the transcripts from the roundtable discussion
for themes. For analysis, we used a low-technology “long
table” technique suggested by Krueger (6), which permits
analysis of content to identify themes and categorize results.
RESULTS AND DISCUSSION
METHODS
The introductory statements of the breast cancer
survivor-advocates and advocates were a powerful
addition to the proceedings of the 2005 Global Summit. The
stories of these quietly eloquent women illuminated the
connectedness of breast cancer survivors and their advocacy
efforts around the world. Similarly, although participants
in the roundtable meeting noted some differences between
their countries in breast cancer experiences and advocacy
movements, the commonalities were striking.
Overall, five major themes emerged from the analysis
of the statements and the transcript that reflected common
experiences of breast cancer survivor-advocates and of
advocates worldwide:
The second biennial Global Summit Consensus Conference on International Breast Health Care (hereafter
referred to as the 2005 Global Summit), sponsored by the
Fred Hutchinson Cancer Research Center, cosponsored
by the Susan G. Komen Breast Cancer Foundation, and
hosted by the Office of International Affairs, National
Cancer Institute, provided a forum for the voice of breast
cancer survivor-advocates and advocates from countries
with limited resources. (For the purposes of this article,
survivor-advocates are defined as breast cancer survivors
who work in partnership with a community-based group
or organization of survivors.)
• Common experiences and fears of breast cancer survivors
• Beliefs and taboos about breast cancer that hinder
awareness programs and treatment
• The universal need for public education and breast cancer
awareness programs in countries with limited resources
• The shared problems with language and difficulty
translating the concept and ethos of advocacy into many
languages
• Common experiences in establishing and maintaining
advocacy groups to promote breast cancer awareness
and to inform public policy
Shared Journey in Breast Cancer Advocacy • S113
Experiences and Fears of Survivors
The experiences of breast cancer survivor-advocates
from countries with limited resources were reflected in the
statements and transcripts. Participants’ comments indicated that the commonality of the experience of breast
cancer survivors led to the development of support groups.
Specifically, survivor-advocates and advocates recognized
the need to provide emotional support and education for
breast cancer survivors and to provide testimony “to the
power of life.” Certain issues are universal for all women
with breast cancer, irrespective of age, ethnic group,
nationality, or stage of disease, and this universality of the
experience of breast cancer was reflected in the comments
of survivor-advocates.
I was thinking that breast cancer is the same disease for
every woman all over the world, we were survivors. Maybe
we felt the same way and we suffer the same, but one of the
things I’m taking back home is that we are also different—
each country, each culture has a different approach, even
when you speak about countries of limited resources.
Avoiding awareness programs and information on this
disease as a result of fear has worsened the plight of
breast cancer patients in developing countries.
Survivor-advocates and advocates also identified
common themes related to the changes in body image
associated with mastectomy. In addition, they noted how
women with breast cancer must assimilate into their lives
the physical scars of treatment, emotional distress, and
disruption in family relations. They identified the need for
information about prostheses and the need for emotional
support for breast cancer patients.
The loss of a breast is a terrifying jolt to one’s body image.
Breast cancer creates an identity crisis with the initial loss
of body image. Encouragement, hope, and emotional
support from loved ones, family, friends, someone with
a common experience, and health care professionals
can help prevent social isolation and social discrimination, which can be devastating.
Beliefs and Taboos about Breast Cancer
I’m a breast cancer survivor, five years now, and I am
also a breast health advocate. I’m with an organization
called the Kenya Breast Health Program. This is basically the only advocacy group for breast health in my
country, and I likely got involved with Kenya Breast
Health Program at its formation, basically as a result of
my experience with breast cancer.
Along with common concerns, experiences, and anxieties, each woman’s journey with breast cancer has a
unique set of circumstances. A frequent common experience and expression of survivor-advocates was that of
fear. They described the personal fear that a woman experiences after receiving a diagnosis of breast cancer, as well
as the societal fear manifested in the response by family
members and neighbors:
One of the greatest fears expressed by almost all newly
diagnosed breast cancer patients is … am I going to die?
Several survivor-advocates and advocates identified
traditional societal beliefs and cultural taboos that affected
women’s access to information, early detection, and treatment. They noted how these beliefs may result in social
isolation for women with breast cancer. In addition, their
comments suggested that cultural attitudes and taboos,
especially beliefs of fatalism, may deter breast cancer
advocacy efforts:
Traditional beliefs dominate the Asian lifestyle. Negative attitude of society toward cancer can be a greater
killer than the disease itself. The woman is made to feel
guilty that she has brought “bad genes” into the family.
She keeps her disease under wraps just to avoid social
rejection and social isolation. In some cases she is isolated from her family members, whereby her dining
utensils are separated, fearing that she will “spread the
disease to the rest of the family members.”
Overcoming fear when alone is not easy … one feels no
longer accepted.… The word cancer terrified me.
I will never give up to those who suggested that when
you get close to a disease or have something to do with
it, it will follow or it will affect your family.
A woman’s journey in breast cancer in a developing
country has a long way to go. For many years, people
in developing countries have perceived breast cancer as
a frightening disease surrounded by fear and myths.
Cancer, if you talk about cancer, it comes into your
house or if you go to the doctor to be examined for breast
cancer, you end up with breast cancer. If you don’t go,
you won’t get breast cancer.
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Need for Public Education and Awareness Programs
Breast cancer survivor-advocates and advocates identified the need for culturally appropriate breast health
awareness programs and problems with competing for
scarce resources in the face of the burden of communicable
diseases in countries with limited resources. Participants
from such countries had a heightened awareness of disparities in access to diagnostic and treatment facilities that
lead to late presentations of the disease:
Most women in developing countries know very little
about breast cancer and its warning signs, and as a
result go to hospital for treatment when it is rather too
late to get cured.
We have a problem with awareness, we have stigmatization, we have all those and end up leading to late presentations, and we have lack of diagnostic facilities, lack
of treatment facilities, financing constraints for the women,
competition for resources. HIV/AIDS is a major problem,
so you talk about breast cancer and say how many
people are dying, and they say HIV, they’re always quoting figures, 700 people per day, and they say, “Wow,
this is the problem. Breast cancer, that’s not a problem.
Difficulty in Translating the Concept of Advocacy
Advocacy in the English language is generally interpreted as the art of representing or promoting a cause or
purpose on behalf of oneself or others. This may include
increasing awareness, influencing policy, affecting legislation, and changing attitudes. Traditionally patient advocacy has involved pleading on behalf of patients’ needs.
Yet the word advocacy is not directly translatable in many
languages (3,4). This difficulty with translation was a
theme that emerged from the analysis of comments. Participants in the advocacy roundtable identified the need to
develop an international word or language for advocacy
that would reflect the broad range of activities and
approaches generally interpreted as breast cancer advocacy. In addition, participants noted that in developing
countries, women may not have open access to resources,
information, or education that empowers them to implement change and promote advocacy.
I’m trying to find the exact meaning, not the exact
word, but the exact meaning.
We still don’t have in Portuguese a word for advocacy,
and it’s a big problem because we cannot say “advogados”—or lawyers, it would mean—because we are not.
We must find a word for this, outside English word,
because we cannot say “advogados” or something like
that. I don’t know. We have to think as a group because
I’m sure in Spanish and Italian, Latin countries have
this problem of the word and we have to make it like
an international word.
We don’t have a word for advocacy, it’s exactly the
same as what you say it may mean, that you are a
lawyer or something like that, and you have to have
that qualification to be one. So the word we use is
networking and influencing.
There were not rules that could regulate volunteer
work, nobody was talking about social responsibility
or advocacy was just out of question. It was a bunch of
women that were shouting about something, just no
credit whatsoever.
Experiences in Establishing and Developing Advocacy
Groups
Although there was apparent difficulty with defining
advocacy, breast cancer survivor-advocates and advocates identified common bonds, challenges, and steps that
propelled their efforts forward. Their comments reflected
the incremental nature of breast cancer advocacy and
movement along a continuum from support and education, to developing social responsibility, and finally to
influencing change. The burdens and hurdles on the road
to breast cancer advocacy were reflected in their comments:
So we decided that we have to work towards some
other issues, not just giving support to the women
themselves, and from there we started doing a little bit
of advocacy work.
I must say that the word advocacy is absolutely new for
me.
We started with six people and this was ’93 and things
really moved fast, and we start after 2 years we became
official Brazilian kind of educational group, volunteer
educational group, at that time volunteer work was not
accepted in Brazil because we’re intruders in hospitals.
What I’m trying to do is find what the word advocacy
means exactly in Spanish. I know what it means, but
So we came up with the idea that we need some form
of guideline so that we make sure that everybody is
Shared Journey in Breast Cancer Advocacy • S115
trying to do something that is normal, or acceptable, so
eventually we lobbied the ministry to set up what they
call a breast cancer working group.
The message of breast cancer advocacy has been spreading throughout the world. In the early 1990s, EUROPA
DONNA, the European Breast Cancer Coalition, was
formed. The emergence of breast cancer advocacy throughout Europe can be traced through the development of
EUROPA DONNA, a coalition of affiliated groups for
countries across Europe (2). Similarly, Reach to Recovery
has grown into an international network of survivoradvocates that includes 84 groups in 50 countries. While
some are mature groups, the majority are new groups
from Africa, Asia, eastern Europe, and Latin America who
need help in establishing support services (1).
In the late 1990s, the Komen Foundation began to
develop international affiliates in countries that were
interested in implementing Komen activities, such as the
Race for the Cure. Today the Komen Foundation has
three international affiliates—in Germany, Italy, and
Puerto Rico—that fund grants and carry out breast cancer
education programs. In addition, the foundation has made
grants to nongovernmental organizations (NGOs) in
more than 30 countries to support a range of breast cancer
education, outreach, and support programs. Representatives from several of these organizations participated in
the advocacy roundtable discussion and shared their
experiences. They remarked that financial support from
foundations and NGOs had been helpful in furthering
their activities
So you need some luck in life, and my lucky occasion
came in 1998 when I had the privilege and fortune to
cross roads with the Komen Foundation, very, very
early when they were starting to become an international
organization or at least to start some international efforts.
And we have had really the fortune to look at a wonderful model that in the United States has created, really
a switch in the way breast cancer is addressed and see
how we could apply at least some part of this model in
Italy, through innovation and new strategies, trying not
to duplicate efforts that were already there, but creating new opportunities. And in 5 years, we have been
able to become self-sufficient, we generate money that
allows [us] to fund, we have supported 50 programs of
other breast cancer groups in Italy, in small possibly
groups that would have good ideas but not have access
to funding, so that at the local level, the community
level, this is helping women with breast cancer to have
something more to face this disease better.
CONCLUSIONS
The last decade has been marked by rapid growth in the
breast cancer advocacy movement around the world.
There has been a shift in the activities of survivor-advocates
and advocates as breast cancer advocacy campaigns have
increased in intensity in regions with limited resources
including Africa, Asia, eastern Europe, and Latin America.
The practice of breast cancer advocacy has increasingly
become international, with sustained, effective collaboration among groups. The goals and methods of these campaigns may vary with the social, economic, and cultural
circumstances of the countries and women involved.
Despite this diversity, survivor-advocates and advocates
at the 2005 Global Summit voiced a set of common themes
in international breast cancer advocacy that reflected their
shared journey with breast cancer.
By virtue of their personal life experiences, breast cancer survivor-advocates possess unique insights regarding
the complex sociocultural issues that may hinder the
implementation of breast health awareness and early
detection programs in countries with limited resources.
Survivor-advocates and advocates at the summit expressed
common themes pertaining to the experience of breast
cancer, including societal fear of the disease, cultural
taboos and myths, and a lack of adequate educational
resources. Their statements indicated that these factors
can be major barriers to breast health awareness and early
detection programs in countries with limited resources.
Their experiences are consistent with the findings of several studies that have documented that fear, perceptions,
and lack of knowledge are obstacles to breast cancer
screening (7–9). To successfully recruit women to breast
health awareness and early detection programs, such programs must take into consideration women’s perceptions
and cultural beliefs about breast cancer. Participants’
comments indicated that these perceptions and beliefs
vary among countries and population groups, necessitating a tailored approach to program design. The impact of
effective programs is potentially large, as participants’
comments expressed confidence that such programs could
contribute to improved survivorship for women with
breast cancer.
Although the word advocacy is not directly translatable
in many languages, the role of breast cancer survivoradvocates and advocates appears to be universal. Participants in the Advocacy Roundtable strongly believed that
S116 • errico and rowden
with the assistance of governmental and NGOs, breast
cancer advocacy groups can continue to create change. In
partnership with organizations such as Reach to Recovery
International, the Komen Foundation, and the medical
community, survivor-advocates and advocates may be
instrumental in establishing effective breast health awareness programs as well as breast cancer research programs
that cross social, economic, and cultural boundaries in
countries with limited resources (9).
Breast cancer advocacy can have a marked positive
influence on societal awareness of and attitudes toward
the disease, on breast health care services, and on funding
for research (3). However, establishing and expanding
advocacy groups in countries with limited resources may
be especially challenging. Resource-constrained countries
have limitations in financial support, social barriers, and
competing illnesses that frame how breast cancer advocacy can be implemented. Comments made by survivoradvocates and advocates at the summit indicated that they
have a deep understanding of the barriers to developing
breast cancer advocacy in such countries. These individuals
are nonetheless motivated to integrate their insights and
experiences to support and maintain advocacy groups.
Given the potential of advocacy movements to improve
breast health outcomes, the founding and growth of advocacy groups should be fostered in countries with limited
resources.
Taken together, the five themes we identified constitute
an action agenda for breast cancer advocacy groups in
countries with limited resources. In particular, the survivoradvocates’ and advocates’ comments revealed barriers
and challenges to breast health care and breast cancer
advocacy, but at the same time suggested potential strategies for overcoming them. The themes also provide
invaluable insight to policymakers, program planners,
and others undertaking efforts to improve breast cancer
outcomes in such settings.
Acknowledgments
We are indebted to the following individuals for
sharing their personal experiences in the statements and
the discussion that formed the basis of this report: Brother
Charles S. Anthony, Monastery Center for Disease
Prevention Panagia Philanthropini, Ormylia, Chalkidike,
Greece; Maira Caleffi, MD, PhD, Breast Center at Hospital
Moinhos de Vento em Porto Alegre, and Breast Institute
of Rio Grande do Sul, Porto Alegre, RS, Brazil; Margaret
Fitch, RN, PhD, Toronto Sunnybrook Regional Cancer
Center, and Supportive Care, Cancer Care Ontario, Toronto,
Ontario, Canada; Alicia Gimeno, Corporacion Yo Mujer,
Santiago, Chile; Ranjit Kaur, Reach to Recovery International, Petaling Jaya, Malaysia; Arun Kurkure, MD,
Indian Cancer Society, Lady Ratan Tata Medical and
Research Center, Mumbai, India; Riccardo Masetti, MD,
Catholic University of Rome, Rome, Italy; Mary Onyango,
MBA, Kenya Breast Health Programme, Nairobi, Kenya;
Augustine Quashigah, Breast Cancer Support Group,
Osu-Accra, Ghana; Tatiana Soldak, MD, CitiHope International and Belarusian Breast Cancer Screening and Early
Diagnosis Project, Andes, New York; and Cao Wei, Tianjin
Medical University Hospital, Tianjin, People’s Republic
of China.
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