World J Surg (2008) 32:2578–2585
DOI 10.1007/s00268-007-9454-z
Breast Cancer Issues in Developing Countries: An Overview of the
Breast Health Global Initiative
Benjamin O. Anderson Æ Raimund Jakesz
Published online: 19 February 2008

Société Internationale de Chirurgie 2008
Abstract
Background Of the 411,000 breast cancer deaths around
the world in 2002, 221,000 (54%) occurred in low- and
middle-income countries (LMCs). Guidelines for breast
health care (early detection, diagnosis, and treatment) that
were developed in high-resource countries cannot be
directly applied in LMCs, because these guidelines do not
consider real world resource constraints, nor do they pri-
oritize which resources are most critically needed in
specific countries for care to be most effectively provided.
Methods Established in 2002, the Breast Health Global
Initiative (BHGI) created an international health alliance to
develop evidence-based guidelines for LMCs to improve
breast health outcomes. The BHGI held two Global Sum-
mits in October 2002 (Seattle) and January 2005
(Bethesda) and using an expert consensus, evidence-based
approach developed resource-sensitive guidelines that
define comprehensive pathways for step-by-step quality
improvement in health care delivery.
Results The BHGI guidelines, now published in English
and Spanish, stratify resources into four levels (basic,
limited, enhanced, and maximal), making the guidelines
simultaneously applicable to countries of differing
B. O. Anderson
Breast Health Global Initiative, Fred Hutchinson Cancer
Research Center, Seattle, WA, USA
B. O. Anderson (&)
Department of Surgery, University of Washington, 1959 NE
Pacific St, Box 356410, Seattle, WA 98195, USA
e-mail: banderso@u.washington.edu
R. Jakesz
Division of General Surgery, Vienna Medical School,
Waehringer Guertel 18-20, Vienna A-1090, Austria
123
economic capacities. The BHGI guidelines provide a hub
for linkage among clinicians and alliance among govern-
mental agencies and advocacy groups to translate
guidelines into policy and practice.
Conclusions The breast cancer problem in LMCs can be
improved through practical interventions that are realistic
and cost-effective. Early breast cancer detection and
comprehensive cancer treatment play synergistic roles in
facilitating improved breast cancer outcomes. The most
fundamental interventions in early detection, diagnosis,
surgery, radiation therapy, and drug therapy can be inte-
grated and organized within existing health care schemes in
LMCs. Future research will study what implementation
strategies can most effectively guide health care system
reorganization to assist countries that are motivated to
improve breast cancer outcome in their populations.
Introduction
Breast cancer is the most common cancer of women,
comprising 23% of all female cancers around the globe,
with an estimated 1.15 million cases diagnosed in 2002 [1].
There is marked geographical variation in incidence rates,
being highest in the developed world and lowest in the
developing countries in Asia and Africa. The age-stan-
dardized incidence in North America is the highest, at 99.4
per 100,000, while the lowest is in central Africa where it is
16.5 per 100,000 [2]. However, in most low- and middle-
income countries (LMCs), incidence rates are increasing at
a more rapidly than in areas where incidence rates are
already high. Global breast cancer incidence rates have
increased by about 0.5% annually since 1990, but cancer
registries in China are recording annual increases in
World J Surg (2008) 32:2578–2585
incidence of 3-4% [1]. In the urban areas of India, cervical
cancer had the highest incidence of cancers 15 years ago
but has been overtaken by breast cancer as the most
commonly diagnosed cancer among women [3].
Prognosis from breast cancer is rather good, although
globally it still ranks as the leading cause of cancer mor-
tality among women. Very favorable breast cancer survival
rates in the United States and other developed countries
have been attributed to early detection by screening, and by
timely and effective treatment [4]. For example, women
diagnosed with breast cancer between 1990 and 1992 and
reported in the population-based case series from the Sur-
veillance, Epidemiogy, and End Results (SEER) program
(13,172 women) had an 89% 5-year survival rate [5]. By
contrast, age-adjusted survival rates for breast cancer in
developing regions average 57% and are as low as 46% in
India and 32% in sub-Saharan Africa [1].
Poorer survival in LMCs is largely due to late presen-
tation of the disease which, when coupled with limited
resources for diagnosis and treatment, leads to particularly
poor outcome [6]. Of the over 75,000 new cases that
present for treatment each year in India, between 50% and
70% have locally advanced breast cancer at diagnosis [7].
Compounding the problem of late diagnosis, breast cancer
case fatality rates are high because LMCs typically lack
major components of health-care infrastructure and
resources necessary to implement improved methods for
early detection, diagnosis, and treatment of breast cancer
[8, 9]. Although low-resource countries have not identified
cancer as a priority health-care issue because infectious
diseases are a predominant public health problem, never-
theless, as the control of communicable diseases improves
and life expectancy rises, cancer care will become an
increasingly important health problem [10].
Evidence-based guidelines outlining optimal approaches
to breast cancer detection, diagnosis, and treatment have
been well-developed and disseminated in several high-
resource countries [11, 12]. Even in some developing
countries, there have been attempts to develop clinical
practice guidelines for the treatment of breast cancer based
on the resources available [13]. Most guidelines define
optimal practice, which have limited utility in developing
countries where resources are poor. Optimal practice
guidelines may be inappropriate to apply in LMCs for
numerous reasons, including poverty, infrastructure con-
straints, drugs, and cultural barriers. Hence, there is a need
to develop clinical practice guidelines oriented toward
countries with limited financial resources [14]. For these
reasons, the Breast Health Global Initiative (BHGI) was
established in 2002. Cosponsored by the Fred Hutchinson
Cancer Research Center in Seattle, Washington, and the
Susan G. Komen For The Cure in Dallas, Texas, the BHGI
is a program that strives to develop, implement, and study
2579
evidence-based, economically feasible, and culturally
appropriate guidelines that can be used in LMCs with the
aim of improving breast health outcomes. The first evi-
dence-based guidelines were developed at the 2002 BHGI
Global Summit, creating guidelines for (1) early detection,
(2) diagnosis, and (3) treatment. These guidelines, pub-
lished in 2003, are free and available on the internet
(http://www.fhcrc.org/science/phs/bhgi/). They outline
general principles for programmatic improvement in breast
health services as applied to LMCs [15–18].
BHGI Global Summit 2002
The first BHGI Global Summit adopted two axioms as
principles for guideline development [15]:
1. All women have the right to have access to health care,
although considerable challenges exist in implement-
ing breast health-care programs when resources are
limited, and
2. All women have the right to education about breast
cancer, but it must be culturally appropriate and
targeted and tailored to the specific population.
It was recognized that early detection should be empha-
sized in developing countries because breast cancer
presents in advanced stages in which survival is the
poorest. It was also recognized that each country is unique
and there is a need to build programs specific to its needs.
Poor data collection was identified as a barrier to
determining how best to apply resources and to measure
outcomes. These observations from the first global summit
served as a basis for the following summit in 2005.
BHGI Global Summit 2005
At the 2005 BHGI Global Summit, the guidelines were
updated and expanded into a flexible, fully comprehensive
framework for improving the quality of health-care deliv-
ery based upon outcomes, cost, cost-effectiveness, and use
of health-care services. Held January 12–15, 2005, and
hosted by the Office of International Affairs of the U.S.
National Cancer Institute in Bethesda, Maryland, the 2005
BHGI Global Summit convened 67 international experts
representing 33 countries and 5 continents to define spe-
cific ‘‘best practices with limited resources’’ and was
expanded to include medical ethics, international health,
medical economics, and sociology. Twelve national and
international groups (including Breast Surgery Interna-
tional, International Union Against Cancer, International
Atomic Energy Agency, International Society of Breast
Pathology, and World Society for Breast Health) joined the
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BHGI as collaborating organizations. In addition, the
BHGI established affiliations with three WHO programs:
The Cancer Control Programme, Health System Policies
and Operations, and the Alliance for Health Policy and
Systems Research. The 2005 guidelines addressed (1) early
detection and access to care [19], (2) diagnosis and
pathology [20], (3) cancer treatment and allocation of
resources [21], and (4) health-care systems and public
policy [22].
The stepwise systematic approach to health-care
improvement outlined by the 2005 BGHI panels involved a
tiered system of resource allotment defined using four
levels—basic, limited, enhanced, and maximal—based on
the contribution of each resource toward improving clinical
outcomes:
• Basic level—Core resources or fundamental services
absolutely necessary for any breast health-care system
to function. By definition, a health-care system lacking
any basic level resource would be unable to provide
breast cancer care to its patient population. Basic-level
services are typically applied in a single clinical
interaction.
• Limited level—Second-tier resources or services that
produce major improvements in outcome such as
increased survival, but which are attainable with
limited financial means and modest infrastructure.
Limited-level services may involve single or multiple
clinical interactions.
• Enhanced level—Third-tier resources or services that
are optional but important. Enhanced-level resources
may produce minor improvements in outcome but
increase the number and quality of therapeutic options
and patient choice.
• Maximal level—High-level resources or services that
may be used in some high-resource countries and/or
may be recommended by breast care guidelines that
assume unlimited resources but that should be consid-
ered a lower priority than those in the basic, limited, or
enhanced categories on the basis of extreme cost and/or
impracticality for broad use in a resource-limited
environment. In order to be useful, maximal-level
resources typically depend on the existence and func-
tionality of all lower-level resources.
Each panel created tables that prioritize resources to
facilitate programmatic improvement in breast cancer early
detection (Table 1), diagnosis and pathology (Table 2),
treatment (Tables 3–6), and health-care systems (Table 7),
each stratified for resource level of basic, limited,
enhanced, and maximal. This stratified matrix scheme
assumes incremental resource allocation and
implementation.
During the BHGI Summits, several key points were
identified or demonstrated [23]. First, early breast cancer
detection improves outcome in a cost-effective fashion
assuming treatment is available [24]. Second, the effective-
ness of early-detection programs requires public education to
foster active individual participation in diagnosis and treat-
ment [25]. Third, clinical breast examination combined with
diagnostic breast imaging (breast sonography with or with-
out diagnostic mammography) can facilitate cost-effective
tissue-sampling techniques for cytologic or histologic diag-
nosis [20]. Fourth, breast-conserving treatment (BCT) with
partial mastectomy and radiation requires more health-care
resources and infrastructure than mastectomy but can be
provided in a thoughtfully designed limited-resource setting
[26]. Fifth, the availability and administration of systemic
therapy are critical to improving the survival of breast cancer
patients. Sixth, estrogen-receptor testing allows patient
selection for hormonal treatments (tamoxifen, oophorec-
tomy), which is better for patient care and allows proper
distribution of services. Seventh, chemotherapy, which
requires substantial allocation of resources and infrastruc-
ture, is needed to treat locally advanced breast cancer, which
represents the most common clinical presentation of the
disease in low-resource countries. Furthermore, when che-
motherapy is unavailable, patients presenting with locally

Table 1 Early detection and

Level of Detection method(s) Evaluation goal
access to care (reproduced from
resources
[40] with permission)
Basic Breast health awareness (education ± self-examination) Baseline assessment and repeated
Clinical breast examination (clinician education) survey
Limited Targeted outreach/education encouraging CBE for at-risk Downstaging of symptomatic
groups disease
Diagnostic ultrasound ± diagnostic mammography
Enhanced Diagnostic mammography Opportunistic screening of
Opportunistic mammographic screening asymptomatic patients
Maximal Population-based mammographic screening Population-based screening of
BHA = breast health Other imaging technologies as appropriate: high-risk asymptomatic patients
awareness; CBE = clinical groups, unique imaging challenges
breast examination

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Table 2 Diagnosis and pathology (reproduced from [40] with permission)

Level of Clinical Pathology Imaging and lab tests
resources

Basic History Interpretation of biopsies

Physical examination
Clinical breast examination
Surgical biopsy Cytology and/or pathology report
Fine-needle aspiration biopsy describing tumor size, lymph node
status, histologic type, tumor grade
Limited Core needle biopsy Determination and reporting of ER and Diagnostic breast
PR status ultrasound ± diagnostic
mammography
Plain chest radiography
Image-guided sampling Determination and reporting of margin Liver ultrasound
(ultrasonographic ± mammographic) status Blood chemistry profile /
complete blood count (CBC)
Enhanced Preoperative needle localization under On-site cytopathologist Diagnostic mammography
mammographic or ultrasound guidance Bone scan
Maximal Stereotactic biopsy HER-2/neu status CT scanning, PET scan, MIBI
Sentinel node biopsy IHC staining of sentinel nodes for scan, breast MRI
cytokeratin to detect micrometastases
ER = estrogen receptors; PR = progesterone receptors; CBC = complete blood count; IHC = immunohistochemistry

Table 3 Treatment and allocation of resources: Stage I breast cancer (reproduced from [40] with permission)
Level of Local-regional treatment Systemic treatment (adjuvant)
resources
Surgery Radiation therapy Chemotherapy Endocrine therapy

Basic Modified radical Ovarian ablation

mastectomy Tamoxifen
Limited Breast-conserving Breast-conserving whole-breast irradiation Classical CMFb
therapya as part of breast-conserving therapy
Postmastectomy irradiation of chest wall and AC, EC, or FACb
regional nodes for high-risk cases
Enhanced Taxanes Aromatase inhibitors
LH-RH agonists
Maximal Sentinel node biopsy Growth factors
Reconstructive surgery Dose-dense chemotherapy
CMF = cyclophosphamide, methotrexate, and 5-fluorouracil; AC = doxorubicin and cyclophosphamide; EC = epirubicin and cyclophospha-
mide; FAC = 5-fluorouracil, doxorubicin, and cyclophosphamide; LH-RH = luteinizing hormone–releasing hormone
a
Breast-conserving therapy requires mammography and reporting of margin status
b
Requires blood chemistry profile and complete blood count (CBC) testing

advanced, hormone receptor–negative cancers can receive
only palliative therapy [21].
Breast cancer in LMCs: Early diagnosis and access to
care
There is solid evidence supporting the value of diagnosing
cancer early, and guidelines on early detection are
available [27, 28]. The only screening method that has been
demonstrated to reduce mortality from breast cancer is
mammographic screening [29–32]. However, mammogra-
phy is expensive and requires manpower and technical
expertise that is not affordable in most LMCs. As a result,
BHGI guidelines recommend that breast health awareness
(BHA) should be promoted to all women at the basic level.
In addition to this basic facility, further development will
require training of relevant staff to perform clinical

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Table 4 Treatment and allocation of resources: Stage II breast cancer (reproduced from [40] with permission)
Level of Local-regional treatment Systemic treatment (adjuvant)
resources
Surgery Radiation therapy Chemotherapy Endocrine therapy

Basic Modified radical —a Classical CMFc Ovarian ablation

mastectomy AC, EC, or FACc Tamoxifen
Limited Breast-conserving Breast-conserving whole-breast
therapyb irradiation as part of breast-conserving
therapy
Postmastectomy irradiation of chest wall
and regional nodes for high-risk cases
Enhanced Taxanes Aromatase inhibitors
LH-RH agonists
Maximal Sentinel node biopsy Growth factors
Reconstructive surgery Dose-dense chemotherapy
CMF = cyclophosphamide, methotrexate, and 5-fluorouracil; AC = doxorubicin and cyclophosphamide; EC = epirubicin and cyclophospha-
mide; FAC = 5-fluorouracil, doxorubicin, and cyclophosphamide; LH-RH = luteinizing hormone–releasing hormone
a
Chest wall and regional lymph node irradiation substantially decreases the risk of postmastectomy local recurrence. If available, it should be
used as a basic-level resource
b
Breast-conserving therapy requires mammography and reporting of margin status
c
Requires blood chemistry profile and complete blood count (CBC) testing

Table 5 Treatment and allocation of resources: Locally advanced breast cancer (reproduced from [40] with permission)
Level of Local-regional treatment Systemic treatment
resources
Surgery Radiation therapy Chemotherapy Endocrine therapy

Basic Modified radical mastectomy Neoadjuvant AC, FAC, Ovarian ablation

or classical CMFb Tamoxifen
Limited Postmastectomy irradiation of the
chest wall and regional nodes
Enhanced Breast-conserving therapya Breast-conserving whole-breast Taxanes Aromatase inhibitors
irradiation LH-RH agonists
Maximal Reconstructive surgery Growth factors
Dose-dense chemotherapy
CMF = cyclophosphamide, methotrexate, and 5-fluorouracil; AC = doxorubicin and cyclophosphamide; EC = epirubicin and cyclophospha-
mide; FAC = 5-fluorouracil, doxorubicin, and cyclophosphamide; LH-RH = luteinizing hormone–releasing hormone
a
Breast-conserving therapy requires mammography and reporting of margin status
b
Requires blood chemistry profile and complete blood count (CBC) testing

evaluation, including taking a history and performing a
clinical breast examination (CBE) for both symptomatic
and asymptomatic women. Higher-level early-detection
programs may include opportunistic screening with CBE,
trials of organized screening using CBE and/or breast self-
examination (BSE), and finally feasibility studies of
mammography screening (Table 1). There are sociocul-
tural barriers to breast cancer detection that need to be
overcome among women from traditional cultures. In some
cultures, the woman’s decision and actions are controlled
by men who may be unaware of breast screening as an
effective, life-saving modality [25, 33].
Breast cancer in LMCs: Diagnosis and pathology
Histologic diagnosis of breast cancer is essential before
embarking on treatment, and the type of biopsy (fine-nee-
dle aspiration cytology, core needle biopsy, and excisional
biopsy) should depend on the available tools and expertise.
The basic level required for diagnosis includes a history,
clinical examination, tissue diagnosis, and record keeping.
Increasing resources require imaging facilities (mammo-
gram with or without ultrasound), staging investigations for
metastases, and hormone receptor testing (Table 2). With
opportunistic and population-based screening, further

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Table 6 Treatment and allocation of resources: Metastatic and recurrent breast cancer (reproduced from [40] with permission)
Level of Local-regional treatment Systemic treatment
resources
Surgery Radiation therapy Chemotherapy Endocrine Supportive and
therapy palliative therapy

Basic Total mastectomy for ipsilateral breast Ovarian Nonopioid and opioid
tumor recurrenceb ablation analgesics
Tamoxifen
Limited Palliative Classical CMFa
radiation Anthracycline monotherapy or
therapy in combinationa
Enhanced Taxanes Aromatase Bisphosphonates
Capecitabine inhibitors
Trastuzumab
Maximal Growth factors Fulvestrant
Vinorelbine
Gemcitabine
Carboplatin
CMF = cyclophosphamide, methotrexate, and 5-fluorouracil
a
Requires blood chemistry profile and complete blood count (CBC) testing
b
Required resources are the same as those for modified radical mastectomy

Table 7 Healthcare systems and public policy (reproduced from [40] with permission)
Level of resources Services Facilities Record-keeping

Basic Primary care services Health facility Individual medical records and
Pathology services Operating facility service-based patient registration
Surgical services Pathology laboratory
Oncology services Pharmacy
Nursing services Outpatient care facility
Palliative services
Limited Imaging services Imaging facility Facility-based medical records and
Radiation oncology services Radiation therapy centralized patient registration
Peer support services Clinical information systems
Early detection programs Health system network Local cancer registry
Enhanced Opportunistic screening programs Centralized referral cancer center(s) Facility based follow-up systems
Cancer follow-up
Rehabilitation services Population-based cancer registry Regional cancer registry
Group support
Maximal Population-based screening program Satellite (noncentralized or National cancer registry
Individual psychosocial care regional) cancer centers

expertise with image-guided biopsy and training individu-
als to perform and interpret biopsies are required [20].
Breast cancer in LMCs: Treatment and allocation of
resources
Breast cancer patients in limited-resource countries differ
from those in high-resource countries in that they present
with more advanced disease where therapeutic options are
limited and resource-intensive. This panel’s recommenda-
tions have to apply to all four levels of resources, from
basic to maximal, and at all stages of disease [21]. The
early and accurate diagnosis of breast cancer is important
for optimizing treatment.
With surgical treatment, since radiation therapy is not an
available basic facility, only mastectomy and axillary dis-
section are recommended at the basic level, while breast-

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2584
conserving surgery appears in the limited level upward, and
breast reconstruction after mastectomy is offered at the
maximal level (Tables 3–6).
For adjuvant therapy in Stage I–III breast cancer, che-
motherapy becomes available at the limited level beginning
with anthracyclines in Stage II at the basic level and
moving on to taxanes in the enhanced level and dose-dense
chemotherapy with growth factors in the maximal level. At
the time the guidelines were written, the data on adjuvant
trastuzumab was not available, but with the positive results
obtained so far [34], adjuvant trastuzumab is likely to be
recommended for HER2-overexpressing breast cancers in
the enhanced-resource level at the next consensus.
With respect to hormone therapy, tamoxifen is recom-
mended at the basic and limited levels for estrogen receptor
(ER)-positive tumors, and aromatase inhibitors are rec-
ommended for postmenopausal ER-positive tumors at the
enhanced and maximal levels in both the adjuvant and the
metastatic setting.
In metastatic breast cancer, the basic requirement is
supportive care, and mastectomy is a palliative rather than
therapeutic procedure. Because metastatic breast cancer is
an incurable disease, it makes sense not to actively treat at
the basic level, hence more resources can be spent on the
other areas of breast care.
With stratification based on resource levels, the panels
hope for the establishment of a ‘‘minimum standard of
care’’ as a foundation on which to build an incremental
model for improving treatment of breast cancer in all
stages. This incremental allocation of resources should lead
to the development of a multidisciplinary breast cancer
treatment system that gives priority to the most effective
resource-sensitive treatment interventions.
Breast cancer in LMCs: Health-care systems and public
policy
The health-care systems in limited-resource countries lack
core infrastructure elements required to sustain a breast
care program. The three areas described above—early
detection, diagnosis, and treatment—are inextricably
linked. With programs to detect breast cancer early, diag-
nosis and treatment facilities need to be developed to cater
to the expected increase in the number of cases. All these
activities depend on the organizational as well as the
resource capacity of the health-care system.
There is no perfect health-care system because any
system must strike a balance between the many diverse
health needs of the population. Specifically, the health-care
system must achieve a balance among four primary health-
care system tradeoffs, including equity of access, scope of
services, quality of care, and cost containment [35, 36].
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World J Surg (2008) 32:2578–2585
Approaches to implementing a breast health program
can be vertical, i.e., runs parallel to but is separate from
other programs, or horizontal, i.e., integrated with the
existing system and programs. The problem with the ver-
tical approach is that the program ends up competing with
all the other disease-specific programs for the same
resources. Integrating the breast health program within
existing programs, e.g., integrating breast health education
with child and maternal health care services, would allow
optimization of resources at the same time that other
health-care needs are met [37, 38].
To determine the basic health-care systems available to
run a breast cancer program, the services required at the
basic-resource level are primary care, surgical, pathology,
oncology, nursing, and palliative care, with a health facility
offering operating, pathology, pharmacy, and outpatient
services and individual medical record-keeping (Table 7).
Program implementation
The BHGI guidelines are designed with sensitivity to the
existing diversity in the delivery of breast health care and
recognize the economic and cultural differences in LMCs.
A key characteristic of these guidelines is the concept of
stratification into four resource levels, making it applicable
to countries with differing resource levels. This approach is
more realistic and each country should make an effort to
improve its delivery of breast health care [39].
Improving breast health care in LMCs requires collab-
oration of multiple sectors, both public and private. A
strength of the BHGI guideline development process is its
collaborative nature, creating partnerships between various
organizations to improve health care in these countries. In
the end it will be political will that will be the final decisive
factor in whether these guidelines will succeed.
The 2005 BHGI guidelines can be used to commu-
nicate programmatic needs to hospital administrations,
government officials, and/or health-care ministries. The
thesis of the BHGI is that these guidelines create a
framework for change by defining practical pathways
through which breast cancer care can be improved in an
incremental and cost-effective fashion [23]. However,
guidelines do not in and of themselves improve out-
comes for women. Implementation is the critical step by
which the value of the guidelines can be measured. The
results of pilot research projects and demonstration pro-
jects need to be studied and reported to determine the
effectiveness of the guidelines and to create evidence
that will guide and facilitate guideline implementation in
other settings. The 3rd BHGI Global Summit, held in
Budapest, Hungary in October 2007, was directed at
defining the next steps for programmatic implementation
World J Surg (2008) 32:2578–2585
of BHGI guidelines in LMCs. New dissemination and
implementation research focused on LMCs should pro-
vide guidance on optimal guideline implementation
strategies. In this way, the BHGI endeavors to help
women cope with and survive the ravages of the most
common cancer and most common fatal cancer among
women.
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