The Breast 20 (2011) S54eS59

Contents lists available at ScienceDirect

The Breast
journal homepage: www.elsevier.com/brst

The role of health system factors in delaying nal diagnosis and treatment
of breast cancer in Mexico City, Mexico
Kristin Bright a, *, Maya Barghash b, Martin Donach a, Marcos Gutirrez de la Barrera c,
Robert J. Schneider a, Silvia C. Formenti a
a
New York University School of Medicine, New York, NY, USA
b
Mount Sinai School of Medicine, New York, NY, USA
c
Hospital de Oncologa del Centro Mdico, Mexico City, Mexico

a b s t r a c t
Keywords: In Mexico, breast cancer is the leading cancer-related death among women and most cases are diagnosed
Breast cancer at advanced stages (50e60%). We hypothesized health system factors could be partly responsible for this
Delayed diagnosis
delay and performed a prospective review of 166 new breast cases at a major public hospital in Mexico
Mexico
Structural factors
City. Our analysis conrmed the prevalence of locally advanced and metastatic disease (47% of patients).
A subset analysis of 32 women with conrmed stage IeIIIC breast cancer found an average time interval
of 1.8 months from symptom onset to rst primary care consultation (PCC), with an additional 6.6
months from rst PCC to conrmed diagnosis, and 0.6 months from diagnosis to treatment initiation.
Patients underwent an average of 7.9 clinic visits before conrmed diagnosis. Findings suggest that
protracted referral time from primary to specialty care accounts for the bulk of delay, with earlier stage
patients experiencing longer delays. These ndings reveal a critical need for further study and explo-
ration of interventions.
2011 Elsevier Ltd. All rights reserved.

Introduction A number of studies have focused on psychosocial and cognitive

Steady rises in breast cancer incidence in Mexico have been
observed in the past decade.1 While cervical and uterine cancers
are more commonly diagnosed, breast cancer is the leading cause
of cancer-related death among women and also accounts for a large
burden of premature death since 60% of women who die of breast
cancer are aged 30e59 years.2 Despite a greater overall incidence of
breast cancer in high income countries, breast cancer deaths are
higher in low and middle income countries like Mexico.3 An esti-
mated 50e60% of all cases of breast cancer in Mexico are detected
at advanced stages and only 22% of women report having
a mammogram in the past year.4 This is likely due to a range of
factors including a dearth of public knowledge and awareness,
social and cultural barriers, and inadequate medical resources.5
Biological factors such as a higher prevalence of negative prog-
nostic indicators (e.g., tumors that are aneuploid or higher grade)
may also play a role in increased risk for breast cancer-related
mortality among Latinas as compared with Caucasian women.6
* Corresponding author. Department of Sociology and Anthropology, B742 Loeb
Building, 1125 Colonel By Drive, Carleton University, Ottawa, Ontario, Canada K1S
5B6.
E-mail address: kristin_bright@carleton.ca (K. Bright).
factors impacting patient delay7 including older age, low socio-
economic status, limited knowledge regarding benets of early
detection, expressed fatalistic perspectives about breast cancer,
benign attribution of symptoms, and lack of education about
perceived seriousness of breast symptoms.8e10 Comparably fewer
studies have examined provider delay. One study performed at
Instituto Nacional de Cancerologa, a cancer hospital in Mexico City,
examined patient and provider delay in the Popular Health Insur-
ance system (Seguro Popular), a Ministry of Health supported
program for the uninsured.11 Delays to diagnosis were examined
through in-depth qualitative interviews with women diagnosed
with breast cancer. While patient fear was found to be both
a facilitator and inhibitor for care-seeking behavior, other factors
(e.g., competing needs, perceptions that breast cancer is incurable,
and the use of rationalization as a defense mechanism) were
identied as barriers to care seeking. Health system delay was
examined and broken down into medical error at the level of
primary care providers and gynecologists, and problems with
access to quality care and affordability. This case study provided
examples of diagnostic delays of up to 9 months from symptom
onset to treatment initiation.
While health policy research in Mexico has led to expansion of
coverage for the uninsured and development of public awareness

0960-9776/$ e see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.breast.2011.02.012
 K. Bright et al. / The Breast 20 (2011) S54eS59
programs to increase education and screening, data on access and
utilization of breast cancer services are sparse.4 In low and middle
income countries the resources and infrastructure for routine
screening mammography are often unavailable and a majority of
breast cancer patients present with a self-identied symptom.12 A
study by Couture et al. suggests a correlation between increased
access to cancer care including breast cancer screening and higher
socioeconomic status, education and type of insurance.13 Psycho-
social and cultural factors have also been shown to impact care
seeking once a breast cancer sign or symptom is identied;
however these studies have tended to focus on perceptions and
experiences among Mexican immigrant women with breast cancer
or cervical cancer in the United States and along the United States-
Mexico border.14e16 It is likely that elevated rates of advanced
breast cancer in Mexico represent a complex interplay of biological,
socioeconomic, cultural, and health system factors including access
to screening, timely diagnosis, and initiation of treatment. In this
paper we report on an exploratory study to investigate the impact
of health system factors (e.g., physician referral, time between clinic
visits) on breast cancer diagnosis and initiation of treatment at
a large cancer hospital for publicly insured patients.
Methods
Study context
Setting
Hospital de Oncologia del Centro Medico Nacional Siglo XXI
(HOCM) is located in the center of Mexico City and one of only three
specialty cancer hospitals in Mexico City, and the only one
administered by Instituto Mexicano del Seguro Social (IMSS) or the
Mexican Social Security Administration, the largest public organi-
zation in Latin America. Funded through payroll contributions by
employers and employees, IMSS is responsible for the provision of
health care, pensions, and social security to Mexican workers in the
formal sector of the economy and their families, 40% of the coun-
trys population of 100 million. For IMSS patients, there are no co-
pays, deductibles or out-of-pocket costs; and for cancer patients,
surgery, radiotherapy and routine chemotherapy are fully covered.
The public structure of HOCM coupled with the high proportion of
advanced cancer cases seen there make HOCM a key site for the
exploration of health system factors affecting clinical presentation
and initiation of treatment among insured breast cancer patients in
a major urban setting.
Study period
The study was conducted over a two-month period from
February to April 2008. We used a mixed-method approach that
consisted of prospective chart review of all new breast cases seen at
the breast clinic during the study (N 166) and in-depth ethno-
graphic interviews with a subset of newly diagnosed breast cancer
patients (n 32).
Chart abstraction
In the absence of an ofcial national tumor registry, patient
charts were abstracted to determine demographics and breast
cancer disease characteristics, including staging, as well as dates of
prior visits for breast symptom consultation and/or testing.
Interview guide development
The guide was developed based on: (1) a review of the literature
regarding factors associated with diagnostic and treatment delay
and (2) ndings from a qualitative interview study with breast
cancer patients at HOCM (n 10) conducted by KB in 2007
[unpublished data]. The guide was translated from English to
S55
Spanish by the research team and crosschecked by an HOCM
research nurse uent in Spanish and English. It was further assessed
for feasibility based on pilot interviews with two breast cancer
patient volunteers at HOCM. Lastly, it was reviewed and approved
by ethics committees at IMSS and NYU School of Medicine.
Interview process and questions
Interviews were conducted in a private room at the hospital and
participants had the option of being accompanied by a family
member or being interviewed alone. Each interview was taped with
a digital voice recorder after verbal consent was obtained, and tapes
were subsequently transcribed and translated from Spanish to
English. In each interview, participants were asked to provide an
account of what took place between the discovery of a breast
symptom/sign and subsequent primary, secondary, and specialty
clinic visits. Through the use of ethnographic interview probes.17
(e.g., Which day of the week did you return to the clinic? What
else happened at your appointment?), we gathered information
regarding type of provider seen; information exchanged during clinic
visits; types of tests performed; referrals provided; and barriers
encountered in getting from one clinic visit to the next. Recall bias
was minimized by the fact that patients carried with them docu-
mentation (IMSS information cards) of clinic visits and test reports.
Symptom denitions
We dened a symptom or sign as a breast or axillary mass,
nipple discharge, and/or skin color or texture change that triggered
a womans decision to pursue medical care that ultimately led to
a denitive tissue diagnosis. For participants detected asymptom-
atically through screening mammography, the date of that
mammogram was used as a starting point to calculate the time
from which to discuss further workup and diagnosis.
Staging determination
Locally advanced breast cancer (LABC) was dened according to
the 2002 American Joint Committee on Cancer (AJCC) guidelines.18
Time delay denitions
Study timeline criteria were informed by denitions of diag-
nostic delay (patient, primary care, referral, secondary care delay)
used by Allgar and Neal,19 and in a study of maternal mortality in
West Africa by Thaddeus and Maine that dened treatment delay
according to: (1) delay in the decision to seek care; (2) delay in
arrival at a health facility; and (3) delay in the provision of adequate
treatment.20 While a number of studies have referred to patient
delay and provider delay to distinguish components of treat-
ment delay, we chose to use a more neutral categorization of Time
1, Time 2 and Time 3.
Time 1. Time 1 is dened as the interval between the participants
rst awareness of a sign/symptom and her initial consultation with
a medical provider for that sign/symptom.
Time 2. Time 2 is the interval between initial primary care consul-
tation (PCC), when an abnormal screening examination or rst eval-
uation with a provider was conducted, and the receipt of a conrmed
cancer diagnosis. An abnormal screening examination is dened as
the rst date when either a suspicious clinical breast examination
(CBE) or mammogram result of category four or ve was reported.
Time 3. Time 3 is the interval between receipt of conrmed diag-
nosis and initiation of treatment.
Total diagnostic delay. Total diagnostic delay is dened as the sum
of Times 1 and 2.
S56 K. Bright et al. / The Breast 20 (2011) S54eS59

Total treatment delay. Total treatment delay is dened as the sum of patients for whom pathological staging was available (Table 1),
Times 1, 2 and 3. 70.15% had advanced stage breast cancer (IIBeIV).

Patient selection
A consecutive sampling method was used to identify and invite
32 breast cancer patients to participate in the semi-structured
interview conducted in Spanish with the assistance of a local
research assistant. Patients were invited to participate if they
received a conrmed diagnosis based upon core biopsy results for
clinical cancer stage I to IIIC. Patients with benign breast disease;
patients who had already received any treatment for their breast
cancer; and patients with recurrent or second primary breast
cancers were not included.
Data on clinic visits (dates, providers, tests)
Dates of visits and procedures were obtained through self-
report and cross-referenced with participants information cards
and procedural reports.
Data collection and entry
Dates were recorded in Excel for the following: initial symptom,
initial PCC visit, subsequent visits with providers specic to breast
condition, rst specialty care consultation (SCC), rst visit at HOCM,
date of core biopsy, date of receipt of biopsy results, and treatment
initiation. Data were also collected regarding the type of provider
and health care sector corresponding with each visit.
Data analysis
Data were subsequently analyzed via descriptive statistics in
Excel to calculate each of the corresponding time intervals.
Informed consent
Study procedures were reviewed and approved by institutional
review boards at IMSS and NYU School of Medicine, and informed
consent was obtained from all interview participants.
Interview study: 32 patients
Demographics
Age. The average age of interviewed women was 54 years (range
26e88 years); women with early stage disease, 57 years (range
47e70 years), women with late stage disease, 53 years (range 26e88
years).
Children, marital status. Approximately 81% (26 women) had chil-
dren; and 22% (7 women) had never been married.
Education and employment. 81% (26 women) had completed either
primary school or high school; over half (53%) of women were
employed and 100% had medical insurance coverage through the
IMSS health care plan. Over 70% of women had an estimated annual
household income of less than 108,000 pesos (wUS $8557) and
none of the interview participants earned more than 270,000 pesos
(wUS $21,392).
Stage of disease. Breast cancer stage was conrmed through chart
review (Table 2). Approximately 66% of women had locally
advanced (IIB e IIIC) disease. Approximately 78% of women pre-
sented with a self-identied sign or symptom, with the remaining
participants referred due to an abnormal screening mammography
(approximately 16%) or CBE (approximately 6%).
Number of visits. Women had an average of 7.9 visits (range 3e16)
with medical providers prior to receiving a conrmed diagnosis of
breast cancer; for women with early stage disease the average was
8.6 (range 4e16), and for late stage disease, the average number of
visits was 7.5 (range 3e11).

Time to diagnosis T1 and T2.

Results
Prospective study: chart review N 166
During the two-month study period, chart review was per-
formed for every new patient seen at HOCM breast clinic for a total
of 166 cases. Of these cases, 27.1% (n 45) were proven to be benign
after pathological assessment, and the remaining 72.9% (n 121)
were biopsy-conrmed breast cancer cases. The average age of
newly diagnosed patients was 56 (range 25e93 years) and
approximately 33% of patients had entered HOCM after having
already received some treatment for breast cancer (e.g., neo-adju-
vant therapy, surgery) at an outside facility. Among the 121 cancer
cases, pathological staging was not available for 38 patients and an
additional 16 were evaluated only as BIRADS 4/5. Among the
Delay to diagnosis. The average total diagnostic delay (time from
symptom onset to conrmation of diagnosis) was 7.8 months: 10.9
months for early stage disease, and 6.1 months for late stage
disease. The average Time 1 (symptom onset to rst medical
consultation) was 1.8 months: 1.2 months for early stage disease
and 2.1 months for late stage disease. The average Time 2 (time
from rst medical consultation to receipt of a conrmed diagnosis)
was 6.6 months: 9.7 months for early stage disease and 4.7 for late
stage disease. See Table 3 for median and ranges.
Delay from diagnosis to treatment. The average Time 3 (time from
receipt of conrmed diagnosis to treatment initiation) was 0.6
Table 2
Characteristics of Participants Based on Chart Review (N 32).

Clinical Characteristics n %
Table 1
New Breast Cancer Cases by Stage at HOCM (N 67). Clinical Breast Cancer Stage
DCIS 3 9.38
Conrmed diagnosis of suspicious lesion n % Stage I 3 9.38
DCIS 2 2.98 Stage IIA 5 15.63
Stage I 6 8.96 Stage IIB 13 40.63
Stage IIA 12 17.91 Stage IIIA 4 12.50
Stage IIB 18 26.86 Stage IIIB and Inammatory Carcinoma 4 12.50
Stage IIIA 7 10.45 Stage IIIC 0 0.00
Stage IIIB and Inammatory Carcinoma 12 17.91 Method of Detection
Stage IIIC 4 5.97 Self-identied Symptom (Breast lump) 25 78.13
Stage IV 6 8.96 Mammography (Screening) 5 15.63
Clinical Breast Examination (CBE) 2 6.25
Total 67 100
Abbreviation: DCIS, ductal carcinoma in situ.
 K. Bright et al. / The Breast 20 (2011) S54eS59 S57

Table 3 Discussion
Time to Breast Cancer Diagnosis and Time to Treatment, by Clinical Stage.

Average Time Median Range The exact effect of diagnostic and treatment delay on mortality
(months) (months) (months) is difcult to assess due to a number of other potential confounders
All N 32 (i.e., biology of breast cancer, host factors and co-morbidities, type
Time 1 1.8 0.3 0e21.6 of treatment, and adherence to therapy). As the natural disease
Time 2 6.6 2.8 0.3e35.8
course and response to treatment of breast cancer is highly
Total Diagnostic Delay 7.8 4.6 0.2e36.7
Time 3 0.6 0.3 0e3.3 heterogeneous, there is no comprehensive or uniform model of
Total Treatment Delay 8.4 5.2 0.9e39.2 breast cancer program development, making it difcult to study the
Early Stage (0e2A), n 11 temporal effect of delay on mortality from breast cancer. For
Time 1 1.2 0.3 0e6.7 instance, some patients who present with shorter delays may have
Time 2 9.7 6.0 0.3e35.8
Total Diagnostic Delay 10.9 7.3 1.3e36.7
poorer outcomes due to a rapid evolution of symptoms, reecting
Time 3 0.8 0.2 0e3, 3 aggressive tumor biology.21 Consistently, a tendency to more
Total Treatment Delay 11.8 7.5 1.3e36.7 expeditiously evaluate women with high suspicion for malignancy,
Advanced Stage (2Be3B), n 21 termed suspicion bias, may articially increase the proportion of
Time 1 2.1 0.2 0e21.6
poor prognosis cancers diagnosed rapidly.22
Time 2 4.7 2.4 0.8e35.0
Total Diagnostic Delay 6.1 4.0 0.2e35.1 While we cannot rule out biological factors underlying the higher
Time 3 0.5 0.3 0e1.9 rates of advanced breast cancer in Mexico, the preliminary results
Total Treatment Delay 6.7 4.7 0.9e35.2 presented suggest that the current health care system might be
responsible for delaying diagnosis and initiation of treatment. The
women interviewed for this study experienced a total diagnostic
delay of 7.8 months and a total treatment delay of 8.4 months. The
months: 0.8 months for early stage disease and 0.5 months for late average delay from symptom onset to rst consultation was
stage disease. See Table 3 for median and ranges. comparably shorter (1.8 months), and participants attributed
a range of factors inuencing their behavior to seek care including
Total delay to treatment. The average overall time from symptom perceptions that symptoms were benign or not serious; a lack of
onset to treatment was 8.4 months; 8.6 months for early stage availability of appointments with a primary care physician; a desire
disease and 7.5 months for late stage disease. See Table 3 for median to save money to cover the cost of a mammogram in a private facility
and ranges. For individual patient data, see Fig. 1. (a strategy used by patients to reduce waiting time in the IMSS

Fig. 1. Time to breast cancer diagnosis and treatment.

S58 K. Bright et al. / The Breast 20 (2011) S54eS59
system); and competing pressures and responsibilities at home and
work. However a pattern of impasse to commencing treatment was
consistently detected in the interviews.
Women experienced an average of 7.9 clinical visits before
receiving a conrmed breast cancer diagnosis for a self-identied
breast sign or symptom in the case of advanced stage breast cancer,
and an average of nine visits prior to reaching an early stage
diagnosis. This trend is similar to that reported in a study from
Canada that found that women with the largest tumor size and
those with a high suspicion of cancer were less likely to experience
delay compared with women who started with earlier stage
disease.23 This study suggested reducing the waiting time for breast
cancer diagnosis by integrating imaging and biopsy earlier on in the
investigation phase. Other studies have pointed to the need for
further training among gynecological providers in how to identify
breast cancer through the use of clinical breast examination.4
To our knowledge, this is the rst study in Mexico evaluating time
to diagnosis among breast cancer patients in the national social
security health care system (IMSS). All of the women interviewed
were covered by IMSS; yet, prior to their visit at HOCM, most had
consulted with a range of private and public clinics and specialties
(radiology, gynecology, oncology, primary care), resulting in a large
number of visits prior to conrmation of diagnosis. Our analysis of
interviews with providers and patients conrmed that primary care
physicians are expected to serve as gatekeepers in the IMSS system.
These physicians are the ones who most often decide whether
a patient should be referred for diagnostic workup. While some
patients may try to expedite the process (e.g., by paying out-of-
pocket at private mammography centers in order to obtain test
results), it is very difcult to skip any step in the referral system.
The preliminary nature of this report on a small sample at
a single institution warrants further research. Studies from other
countries demonstrate that treatment delays beyond three to six
months for symptomatic breast cancer24 and beyond ve months
for asymptomatic or screen-detected breast cancer22 are associated
with an increase in mortality and rates of recurrence of up to 10%. If
conrmed on a larger scale, an intervention to modify the current
practice could have a direct impact on breast cancer mortality in
Mexico. Implementing breast cancer diagnostic opportunity in
gynecological care settings, for example, could drastically reduce
the length of the diagnostic workup for most patients. Integration
of breast cancer awareness and CBE training within existing
reproductive health interventions is currently an initiative in
Mexico which may lead to increased opportunities for diagnosis
and more timely detection.25
Mexico, like many low income and middle income countries, is
undergoing a rapid rise in the incidence of chronic morbidities
including cardiovascular disease, diabetes, obesity, and cancer. This
increase, coupled with late diagnosis, suggests that the burden of
suffering and the mortality related to breast cancer will increase
dramatically in the years to come, with associated health system
costs inevitably likely to escalate.26 Data from Mexicos Ministry of
Health suggest that only 5e10% of breast cancer cases in Mexico are
detected in the earliest stages (i.e., stage IA and IB), making treat-
ment less successful and more costly.27 While signicant strides
have been made in terms of the universal access to cancer care
provided through government programs such as Seguro Popular
established in 2003, utilization of screening and early detection
initiatives also rely on a complex and participatory alliance of
organizations (governmental, educational, legal) as well as clinical
delivery factors (e.g., availability, accessibility, and integration of
breast health services).28
The research presented in this article underscores the need for
a coordinated response at the level of education, policy, and health
care delivery toward more timely initiation of treatment among
otherwise insured patients. Toward these ends, further study is
needed to understand the complex relationship between existing
structural, socio-cultural, and economic factors that impact health
care providers and affect how women seek care for breast cancer
signs and symptoms as well as how they arrive at diagnostic
resolution and the initiation of breast cancer treatment. Impor-
tantly, a more thorough assessment of primary to specialty referral
networks could be benecial toward the development of inter-
ventions aimed at reducing delays to treatment initiation and
increasing clinical vigilance toward the early detection of smaller
breast lesions and triage to diagnosis. In a country where advanced
breast cancer cases account for a high burden of new breast cancer
diagnoses, such interventions may help to better mobilize and
adapt existing resources toward the reduction of breast cancer
morbidity and mortality in Mexico.
Contributors statement
KB conceived and designed the study and was the lead manu-
script writer. MB contributed to study design, data collection,
statistical analysis and writing. SCF contributed to study design and
writing. MD contributed to statistical analysis. MGB and RJS
contributed to study design. All authors contributed to interpre-
tation of results and reviewed and approved the manuscript.
Conict of interest and funding statement
All authors reported no conict of interest. Source of grant
support: U.S. Department of Defense Breast Cancer Research
Program e Center of Excellence Award Number W81XWH-04-1-
0905, HRPO A-13034.0.
Acknowledgments
We would like to express our gratitude to the physicians and
staff of the Breast Clinic of the Hospital de Oncologa del Centro
Mdico for their assistance with identication and referral of
eligible research participants. We would also like to thank all of the
women who took part in the interviews for sharing their time and
experiences with us. This research would not have been possible
without the generous support of the U.S. Department of Defense
Breast Cancer Research Program (Center of Excellence Award
Number W81XWH-04-1-0905) and the NYU School of Medicine
International Health Program. We also extend our heartfelt thanks
to Sandra Ripley Distelhorst, Publications Editor at the Breast
Health Global Initiative (BHGI). This paper would not be what it is
without her editorial guidance.
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