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Breast cancer in Mexico: A growing challenge to

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 Review

Breast cancer in Mexico: a growing challenge to health and

the health system
Yanin Chávarri-Guerra, Cynthia Villarreal-Garza, Pedro E R Liedke, Felicia Knaul, Alejandro Mohar, Dianne M Finkelstein, Paul E Goss

Breast cancer is a major public health issue in low-income and middle-income countries. In Mexico, incidence and Lancet Oncol 2012; 13: e335–43
mortality of breast cancer have risen in the past few decades. Changes in health-care policies in Mexico have Avon International Breast
incorporated programmes for access to early diagnosis and treatment of this disease. This Review outlines the status Cancer Research Program,
Massachusetts General
of breast cancer in Mexico, regarding demographics, access to care, and strategies to improve clinical outcomes. We
Hospital, Boston, MA, USA
identify factors that contribute to the existing disease burden, such as low mammography coverage, poor quality (Y Chávarri-Guerra MD,
control, limited access to diagnosis and treatment, and insufficient physical and human resources for clinical care. P E R Liedke MD,
Prof D M Finkelstein PhD,
Prof P E Goss MD); Hematology-
Introduction breast-cancer care not only in Mexico, but also in other
Oncology Department,
Cancer accounted for 7·6 million deaths in 2008, nearly middle-income countries. Instituto Nacional de Ciencias
13% of all deaths worldwide.1 The ratio of mortality to Médicas y Nutrición, Salvador
incidence is substantially higher in low-income and Basic statistics for breast cancer in Mexico Zubirán, Mexico City, Mexico
(Y Chávarri-Guerra); Breast
middle-income countries (64–75%) than in high-income We obtained official data and statistics from academic Cancer Department, Instituto
countries (46%),2 which shows the great disparity in the publications and online resources from the Mexican public Nacional de Cancerología,
probability of survival within countries and across health system, National Institute of Statistics, Geography Mexico City, Mexico
socioeconomic groups.3 and Informatics (INEGI), GLOBOCAN, and WHO. Total (C Villarreal-Garza MD); Harvard
Medical School, Boston, MA,
Breast cancer is the most common cancer in women numbers of breast-cancer deaths from 1988 to 2009 were USA (Y Chávarri-Guerra,
worldwide, with about 1·38 million diagnoses made from the database generated by the National Epi- P E R Liedke, F Knaul PhD,
annually.1 460 000 deaths were reported in 2008, of which demiological Surveillance System (SINAVE).12 We Prof P E Goss); Harvard Global
269 000 (58%) were in low-income and middle-income calculated age-adjusted rates of breast-cancer mortality for Equity Initiative, Boston, MA,
USA (F Knaul); Mexican Health
populations and countries, and 68 000 (15%) were in the general population using total number of deaths in Foundation, Mexico City,
people aged 15–49 years in low-income countries.4,5 each age group during a specified time divided by the total Mexico (F Knaul); Tómatelo a
Global trends from 1980, to 2010, show that both population of each age group in the same time. We Pecho, Mexico City, Mexico
incidence and mortality have increased; however, rates obtained national population estimates from the 5 year (F Knaul); Unidad de
Investigación Biomédica en
have risen fastest in low-income and middle-income and 10 year census from databases generated by INEGI.13,14 Cáncer, Universidad Nacional
countries, thus worsening the burden of avoidable We calculated estimated mortality trends with probabilistic Autónoma de México, Mexico
disease, disability, and death in poor individuals.5 Breast models, adjusting by age with the Joinpoint Regression City, Mexico (Prof A Mohar MD);
cancer needs to be detected and treated as early and as Program (version 3.5.1).15 and Instituto Nacional de
Cancerología, Mexico City,
best as possible. Gathering of epidemiological data in Mexico is com- Mexico (Prof A Mohar)
Mexico has 31 states and one federal district plex and information is obtained through various Correspondence to:
with substantial socioeconomic and ethnic differences sources. SINAVE, supported by the General Directorate Prof Paul E Goss, Massachusetts
between these regions. Generally, the northern and of Epidemiology of the Ministry of Health, gathers General Hospital Cancer Center,
central states are wealthy, whereas the southern states epidemiological information directly from (mainly Boston, MA 02114, USA
pgoss@partners.org
are poor and include most indigenous populations.6,7 public sector) health-care facilities.16 SINAVE focuses on
Socioeconomic differences probably affect patterns of epidemiological surveillance of selected diseases,
breast-cancer incidence and mortality in the country.6 including breast cancer. Information is obtained
Similar to other middle-income countries, cancer through forms completed by health-care providers at
mortality has generally risen in Mexico, from 58 per the point of possible diagnosis and from death
100 000 inhabitants in 1998, to 67 per 100 000 in 2008. certificates; the information generated is analysed with
Since 2006, breast cancer has been the leading cause of the System for Epidemiologic Surveillance (also called
cancer mortality in Mexican women, accounting for 14% SUIVE) and has been published annually since 2003.16
of cancer-related deaths.8,9 GLOBOCAN’s prediction that SINAVE supports the Mexican histopathologic registry
by 2030, 24 386 women will be diagnosed and 9778 (40%) of malignant neoplasms, which gathers information
will die with breast cancer in Mexico, makes this disease directly from the pathology registry of selected hospitals.
a substantial challenge for the health-care system.4 The last report was published in 2006, and the registry
This Review provides a detailed overview of breast is being restructured with a plan to reopen in 2012.17 The
cancer in Mexico, regarding demographics, access to National Health Information System (also called
prevention, diagnosis, treatment and palliative care, and SINAIS) gets epidemiological information from
strategies to improve clinical outcomes. Country and hospitals to generate data for morbidity and mortality.12
regional initiatives are needed to address care of patients This information includes, but is not restricted to,
with breast cancer worldwide.10,11 We aim to focus on diseases under formal epidemiological surveillance.
areas of weaknesses and future avenues to improve INEGI publishes statistics for breast-cancer mortality

www.thelancet.com/oncology Vol 13 August 2012 e335

 Review
with information obtained directly from death
certificates and SINAVE.14
Breast-cancer incidence has risen in Mexico in the past
few decades, from an annual risk of 2% in 1980, to 5% in
2010; however, true trends should be interpreted with
care because of possible reporting bias and absence of a
national cancer registry.5 According to SUIVE, in 2009,
8428 cases of breast cancer were noted, with a national
incidence of 15 per 100 000 women. The highest
incidences of breast cancer are in the northern and
central states, such as Coahuila (18 cases per
100 000 women), Federal District (17 per 100 000), and
Nuevo Leon (14 per 100 000), whereas the lowest rates are
in the southern states, such as Chiapas (1·15 per 100 000)
and Quintana Roo (1·45 per 100 000).16
Of 4908 deaths from breast cancer in 2009, mortality
rates were 16 per 100 000 in women aged 25 years and
older, 52 per 100 000 in those older than 75 years, 31 per
100 000 in 50–69-year-olds, and nine per 100 000 in
30–49-year-olds.9,13
Absolute crude rates of breast-cancer death show a
general increase in the country overall; however, this
increase has progressively declined, especially since 1995,
falling from 10% in the late 1980s, to 4% since 2000.
Additionally, trends in death rates have plateaued for
most age groups, except for women older than 75 years
for whom it has increased at 1% annually since the late
1980s.18 Time series data for age-adjusted mortality rates
show a continual rise from the 1950s, to the mid-1990s,
with rates more than tripling then plateauing until 2008.
This pattern contrasts greatly with that for cervical cancer,
for which death rates have declined continuously and
sharply since the mid-1980s, falling to less than those for
breast cancer for the first time in 20063,9 (figure).
Similar to incidence, mortality was higher in the
northern and central states, and lower in the southern
states. Palacio-Mejia and colleagues6 noted that nationally,
in 2006, risk of death from breast cancer was two times
higher in urban than rural areas (relative risk [RR] 1·88
[95% CI 1·76–2·00]). The highest risk of death for urban
versus rural areas was within the Federal District (1·44
[1·32–1·56]), followed by the northern (1·14 [1·07–1·21],
central (0·94 [0·89–0·99]), and southern regions (0·74
[0·68–0·80]). The same happening was noted when the
investigators adjusted mortality rates for marginal
socioeconomic status: the highest level of margination
has the lowest risk of death from breast cancer, which is
the opposite of findings for cervical cancer.6 Although
absolute rates are lower in the south than in the north, a
rise in mortality can be noted within both poor and
wealthier states since the late 1970s, from when data are
available.3
Screening
Routine mammography screening for selected women
reduces mortality from breast cancer by 7–23%.19 Inter-
national recommendations for breast-cancer screening
e336
are controversial, for both recommended starting age
(>40 years vs 50 years) and frequency (annually vs every
2 years) on the basis of existing data, and especially for
potential benefits and harms associated with screening
mammography.20,21 Mexico’s Ministry of Health first
published the official standard for breast-cancer
prevention, diagnosis, treatment and epidemiological
surveillance in 1994, which was updated in 2003, and
2011. Although the standards committee’s position
regarding the controversy is unclear in the 2011 document,
the 2011 committee supported their recommendations
with a balanced international and national literature
review.22 The Mexican official standard recommends
annual clinical breast examination for women older than
25 years, and mammography every 2 years for those aged
40–69 years. Furthermore, the official standard
recommends starting of screening 5–10 years before the
age at which the youngest member in the family was
diagnosed with breast cancer, but not before age 25 years,
in specific cases: family history of breast cancer in two or
more first degree relatives, bilateral breast cancer, male
breast cancer, ovarian and breast cancer in any family
member, more than one ovarian cancer case in a family,
BRCA mutation, or Ashkenazi ancestry.22
In Mexico, mammographic equipment is scarce, as
are trained personnel to adequately address screening
needs. In 2000, there were 63 mammography machines
in public health centres; this amount increased to
413 machines by 2006.23,24 According to WHO, in 2010,
there were 314 mammography machines in the public
sector of Mexico and 366 in the private sector, with a
density per population of 37 per 1 000 000 women aged
40 years or older, compared, for example with 72 per
1 000 000 in Canada.25
A national survey in 2006, showed that 16% of Mexican
women had received a mammogram in the previous year.
Although this proportion represents an increase from the
2000 national survey, which reported 10% mammography
coverage, the rates are still low. Furthermore, disparities
exist between the 2000 survey, which asked about clinical
examination, including mammograms, and the
2006 survey, which asked specifically about
mammography.26 In 2007, a survey was done in rural
Mexican households that included information about
mammography and cervical Pap smear. Of 13 614 women
interviewed, 1141 (12%) of 9513 aged 20–49 years had had
a mammogram in the past 12 months, and 163 (7%) of
2337 aged 65 years and younger had had mammogram
within the past 3 years. 35 (71%) of the 20–49-year-olds,
and two (33%) of those aged 65 years and older with
abnormal results had subsequent access to health care.
Results for women aged 50–64 years were not reported.27
By comparison, in the USA in 2008, 83% of women aged
40 years and older had had a mammogram in the previous
2 years.28 WHO states that for a screening programme to
be effective, population coverage needs to be at least
70%.10 In 2010, coverage of mammographic screening in
www.thelancet.com/oncology Vol 13 August 2012

18 Breast cancer
Cervical cancer
16
14
12
Mortality per 100 000 women
10
0
60
70
80
55
65
75
19
19
19
19
19
19
Year
Figure: Age-adjusted mortality from breast and cervical cancer in Mexico, 1955–2008
Reproduced with permission from references 3 and 9.
Mexico was 19·2% of women aged 40–69 years, with
1·5 million mammograms done during that year; an
increase of 3·2% from 2006.29
For cost-effectiveness, one analysis30 showed that
screening programmes could be done at a cost per life-
year saved of less than two times the gross national
product per capita, and was therefore deemed cost
effective. Another study31 showed that cost per life-year
saved was greatly reduced with early detection.
Shortage of trained health personnel is a well-known
barrier to early detection of breast cancer.24 A survey32
done in Mexican medical students and residents, aimed
at identifying the level of knowledge of cancer screening,
showed suboptimum results with an average knowledge
score for the entire group of 64 of 100 (60 for under-
graduate and 70 for postgraduate students).
Risk factors, risk assessment, and prevention
In Mexico, reproductive factors—eg, age of menarche
and menopause, parity, and age at first full-term
pregnancy—are associated with risk of breast cancer.33–36
Other Mexican studies37–40 have shown a reduction in
the odds of breast cancer related to a healthy lifestyle
in women pre- and post-menopause (odds ratio [OR]
0·50, 95% CI 0·29–0·84 vs 0·20, 0·11–0·37), and an
increase in risk with high-calorie and high-carbohydrate
diets. 7–20% of Mexican patients have a strong family
history of breast cancer, which is similar to reports for
other countries.36,41 For breast-cancer risk factors, the
2011 official Norm for breast-cancer prevention,
diagnosis, treatment and epidemiological surveillance
www.thelancet.com/oncology Vol 13 August 2012
Review
90
00
85
95
05
20
19
20
19
19
includes a section for primary prevention that promotes
healthy lifestyle, including diet enriched with fruit and
vegetables, low content of lipids, folic acid, and
30–60 min of daily exercise. Furthermore, this norm
encourages breastfeeding and avoidance of other known
risk factors, such as tobacco and alcohol consumption
greater than 15 g per day.22
Prevalence of predisposing germline mutations in
BCRA1 and BRCA2 genes is unknown in Mexico.42
A small exploratory analysis noted 9% of BRCA1 and
BRCA2 mutations in patients aged 35 years and
younger at diagnosis of early-onset breast cancer, which
is consistent with international rates. The types of
mutations identified in this study were similar to those
from other countries.43 Three studies of mutations in
Mexican women who live in the USA have been done,
and have noted inconsistent rates, with 4% in northern
California, 4% in Los Angeles, and 18% in Texas.42
A study44 of Mexican women showed an association of
breast-cancer risk in women with European genetic
ancestry (OR 1·3, 95% CI 0·96–1·91) that was directly
related to the proportion of specific nucleotide
polymorphisms of European origin.
Information is scarce about risk assessment and pre-
vention in Mexico. A retrospective study45 analysed
1000 women according to the Gail Risk Assessment
model. Results showed a mean calculated 5-year risk of
invasive breast cancer of 1·2% (range 0–5·7) for all
women, with 26% having a risk higher than 1·66%. This
rate is less than that of 58% reported in the USA, which
could be explained by the younger mean age of the
e337
 Review
female population in Mexico (27 years) compared with
those in the USA and other developed countries
(≥38 years).46 Although no woman had received
chemoprevention with tamoxifen, which is an option
recommended by international guidelines and by the
Mexican consensus statement, only 4% of women at risk
in the US have taken this drug for prevention.47,48
Clinical diagnosis
As in other low-income and middle-income countries,
breast cancer in Mexico is detected at a more advanced
stage than in high-income countries.49 A cross-sectional
study50 done in three public hospitals in Mexico’s
Federal District reported that 90% of breast cancers
were diagnosed through a self-detected breast lump.
10% of patients had stage I disease, and 56% had locally
advanced or metastatic disease. In 2007, the National
Cancer Institute of Mexico (INCAN) issued a report of
patients covered by the Mexican health insurance, so-
called Seguro Popular. 744 patients had newly diagnosed
breast cancer during that year: 8% presented with
stage I disease and more than 80% with locally advanced
or metastatic disease.51 This finding is in sharp contrast
to that in the USA,52 where 60% of newly diagnosed
breast cancers are mammographically detected at an
early stage.
Social and cultural barriers, ie, fear that the male
partner might leave at the first sign of breast cancer,
poor awareness of the population and of primary health-
care providers, and deficient mammographic screening
programmes, can lead to late diagnosis.9,53 A small study54
from a major public hospital in Mexico confirmed a
delay of 1·8 months between first breast symptom and
first primary-care consultation, followed by 6·6 months
from primary-care consultation to diagnosis, and
0·6 months from diagnosis to treatment, with an
average total delay of 10 months. Information is
restricted about the reasons for such delays. A study50
that included 40 women with reported delays of more
than 3 months showed that patients were responsible in
35% of cases and providers in 53%. A preliminary
report55 from INCAN showed that the most important
factors that account for differences in appropriate
medical care of breast cancer are women’s sociocultural
characteristics, especially poverty; social networks; social
support; accessibility to health services; and medical
errors in primary and secondary levels of care.
Mean age at diagnosis of breast cancer in Mexico is
50 years (SD 50·5),41,51,56 which is on average at least a
decade earlier than in European and North American
women.53 The age distribution of breast cancer in foreign-
born and US-born Hispanic women is younger than that
of white American women and similar to that of patients
in Mexico.57 Furthermore, of Mexican patients with breast
cancer, 40–50% are postmenopausal, 74% have had fewer
than two previous livebirths, and more than 70% have
never used oral contraception.41,58
e338
Accurate diagnosis and assessment of tumour bio-
markers is crucial to guide breast-cancer investigation
and treatment recommendations. The most common
diagnostic methods in the morphological diagnosis of
breast lesions are fine-needle aspiration and core-needle
biopsy. Because each method has advantages and
disadvantages, centre resources and experience, and
clinical characteristics determine which one is chosen.59
In Mexico, information is scarce about quality of breast-
cancer specimens and diagnostic accuracy of biopsies.
Two studies from two national referral centres showed
that fine-needle aspiration biopsy of palpable lesions had
a positive predictive value of 97–100% and a non-
diagnostic rate of 34–37% because of inadequate sam-
pling or non-conclusive diagnosis.60,61 Although the
findings for fine-needle aspiration are favourable and
similar to international performance results, they do not
indicate the status of the rest of the country.
In a biomarker study41 with 2074 patients, 57% had
hormone receptor-positive tumours, 20% had HER2-
positive tumours, and 23% had triple-negative disease.
The prevalence of triple-negative disease in this study
was higher than that reported in white patients (10–13%)
and similar to that shown in several studies of Hispanic
patients in whom the proportion of hormone receptor-
negative tumours is between 17 and 30%, whereas the
distribution of HER2-positive tumours was uniform.62,63
Despite the clinical importance of methods for hormone-
receptor and HER2 determination, their availability and
quality is not available for other centres that treat breast
cancer in Mexico. Other novel methods for genetic
profiling, such as Mammaprint or OncotypeDx, are
generally not commonly available for Mexican patients
with breast cancer, and are mainly available at private
hospitals. INCAN reported results for 96 patients,
showing that physicians changed their treatment
recommendations in 31 (32%) of 96 cases on the basis of
genetic profiling of tumours, with a decrease from 48%
to 34% in chemotherapy recommendation.64
Treatment
Financial protection and insurance
Mexico has three major types of public insurance: the
Mexican Institute of Social Security provides insurance
for private sector, salaried employees and their families,
and covers roughly 40% of the population; the Institute of
Security and Social Services for State Workers covers the
public sector, who make up roughly 7% of the population;
and the Seguro Popular, which began in 2004, and has
been steadily expanded, covers about 35–40% of families
with a focus on the poorest individuals.51,65
The Seguro Popular covers breast-cancer diagnosis
and treatment through a network of 42 affiliated hos-
pitals by designating specific resources for each newly
diagnosed patient.51 Funding for breast-cancer treatment
for women who are not insured by the Social Security
Institution or the Institute of Security and Social Services
www.thelancet.com/oncology Vol 13 August 2012

for State Workers is provided by the fund for protection
against catastrophic expenditure. Breast cancer was
included in this fund in February, 2007; from then, any
women diagnosed with the disease, regardless of
socioeconomic status, can access a fairly complete
package of services.3
Human and physical resources
Public universities offer training programmes for
medical oncology, surgical oncology, and radiation
oncology in 11 academic centres. About 60 fellows
complete their training after 3–4 years. Each hospital
designs its own training programme and mandatory
credits in basic sciences, epidemiology, clinics, and
research are often included. In 2008, the National
Autonomous University of Mexico and the INCAN
started a formal postgraduate training course in oncology
for nurses. The number of positions on the course
increased from eight in 2008, to 18 in 2011. The duration
of the course is 12 months, including clinical practices
and didactic lectures. INCAN has offered training
courses for more than 20 years.
At present, 62 public institutions have oncology
services; one of these institutions is INCAN, two are
federal hospitals, and 39 are state cancer centres. Available
resources vary in these institutions.51 As of 2010,
986 oncologists were practicing in Mexico: 59% were
oncological surgeons, 23% medical oncologists, 14%
paediatric oncologists, and 4% gynecological oncologists.
Oncologists represent less than 1% of the
215 810 physicians in Mexico and are located mainly in
the largest cities with 44% practicing in the federal district
and 9% each in Nuevo Leon and Jalisco.66
Local-regional treatment
Both mastectomy and breast-conserving surgery with
radiation are standard treatments for primary breast
cancers.67 Since the US National Institutes of Health
consensus statement in 1990, breast-conserving surgery
is more common in the USA and mastectomies are
done in only 37% of cases.68 By contrast, mastectomy is
more common in low-income and middle-income than
in high-income countries, partly because of more
advanced disease at presentation, but also because of a
scarcity of available radiation therapy. A report from
INCAN showed an 85% mastectomy rate at their
institution.51 The risk of recurrence of ipsilateral breast
cancer indicates the quality of locoregional treatment
and is a predictor of systemic recurrence.67 INCAN is
the only establishment that has reported rates of positive
margins (defined as ≤3 mm) as low as 0·3% in treated
patients, either by breast-conserving surgery or
mastectomy,41 which is regarded as acceptable by
international standards.69
For the past 20 years up-front surgical dissection of
axillary lymph nodes has been replaced by sentinel
lymph-node biopsy because of the reduction in
www.thelancet.com/oncology Vol 13 August 2012
Review
morbidity with biopsy.70 Two reports from Mexico have
shown accurate technique for the biopsy procedure,
with sensitivity of more than 90% and negative
predictive values of more than 95%.71,72 Sentinel lymph-
node biopsy is now the main procedure (98% of cases)
at INCAN for patients with clinically lymph node-
negative breast cancer, but this institution, as a national
referral centre, does not indicate practice in the rest of
Mexico.41
Furthermore, radiotherapy is crucial for the man-
agement of patients with breast cancer who have breast-
conserving surgery, and for those with locally advanced
disease. All 39 Mexican state cancer centres have
radiation units, 12 of which have linear accelerators and
ten of which have only cobalt machines. Of these units,
nine do not have planning systems and dosimeters and
13 units do not have simulators. Moreover, although
roughly 200–300 radiation-oncologists are needed in
Mexico because of the population covered by these
centres, presently there are only 58.51 Further information
about the quality, toxic effects, and clinical outcomes For more on INCAN training
related to radiotherapy treatment were not available for courses see http://www.incan.
edu.nx
our Review.
Systemic treatment
The estimated reduction in mortality from breast cancer
is 6–13% for adjuvant tamoxifen and 6–10% for adjuvant
chemotherapy. When combined with screening pro-
grammes, this reduction should result in a 25–38%
overall decrease in breast-cancer mortality.19 Only a For more on oncologists in
few small phase 2 and retrospectives studies exist of Mexico see http://www.cmo.
org.mx
outcomes to systemic treatments. In the Mexican
Institute of Social Security, the main chemotherapy
schemes used are fluourouracil, epirubicin, and
cyclophosphamide in 29% of patients, epirubicin plus
docetaxel in 18%, and cyclophosphamide, methotrexate,
and fluorouracil in 15%, usually given for four to eight
cycles. Weekly trastuzumab is used for 8 months in 12%
of HER2-positive cases, although no information is
available about the proportional number of HER2-
positive patients in the studied population with breast
cancer.31 Patients treated through the Seguro Popular
receive an international standard of four cycles of
fluouroracil, doxorubicin, and cyclophosphamide
chemotherapy followed by 12 doses of weekly paclitaxel.
Patients with HER2-positive tumours receive trasuzumab
for 1 year, and those with hormone receptor-positive
tumours receive tamoxifen for 5 years.41,58 Aromatase
inhibitors—the first choice of endocrine treatment—
have rarely been used in Mexico, possibly because of
cost. However, the availability of generic forms of the
drug might increase their use. In a retrospective single-
centre study of neoadjuvant chemotherapy given to
204 patients in Mexico with anthracycline and taxane-
based chemotherapy (42% for overexpressing HER2,
29% for triple-negative, and 9% for hormone receptor-
positive tumours), pathological complete response was
e339
 Review
Number of publications* Number of ongoing trials†
Mexico 35 66
Argentina 18 70
Brazil 55 98
Canada 264 338
Chile 11 33
Colombia 1 28
Peru 3 63
Uruguay 2 5
USA 400 2512
*Retrieved from PubMed (June 27, 2011) with medical subject heading “breast
neoplasms” and country. †Retrieved from ClinicalTrials.gov (Jan 25, 2012) with
search term “breast neoplasms” and country.
Table 1: Publications and ongoing trials of breast cancer, June 2010–11
33%, which is similar to that reported from high-income
countries.58 INCAN presented preliminary data for
women treated at their institution through the Seguro
Popular. Of 259 women with primary breast cancer
treated between 2007 and 2008, 204 (78%) had locally
advanced disease. At 30 months follow-up, 44% of
women were disease free and 80% were alive, which is
similar to survival reports from the international
literature.58
Palliative care
The need for pain control and palliative care is crucial.
Similar to other developing countries, Latin-American
countries have limited access to palliative-care services.
In Mexico, the availability of palliative-care services has
been increasing since 1970, when the first service was
established at INCAN. In 2007, an official norm for
palliative care was published, and in 2009, treatment
recommendations for breast cancer included guidelines
for pain control and palliative care based on international
guidelines.73
The availability of opiods is poor, which might be
explained by restrictive drug-prescription laws and
regulations in Mexico.74 Moreover, this field has few
specialists, which further contributes to insufficient
palliative care in Mexico.74
Research
To understand and reduce the public health burden from
breast cancer, clinical, epidemiological, health systems,
and translational research are necessary to identify and
address country-specific issues and to appropriately
incorporate advances in other countries. The World
Health Initiative reported that research is insufficient in
Latin-American countries because of scarcity of funding
and available time for researchers, as an indicator of poor
support from governments.75
In November 2011, Mexico had 72 clinical trials of breast
cancer registered at ClinicalTrials.gov. Of these trials, 92%
were sponsored by industry and 8% were sponsored by
e340
Incidence* Mortality* Ratio deaths/new cases
Barbados 74 29·2 0·394
Mexico 27·2 10·1 0·371
Brazil 42·3 12·3 0·290
Argentina 74 20·1 0·271
Uruguay 90·7 24·3 0·267
European Union 77·1 16·6 0·215
USA 76 4·7 0·193
Canada 83·2 15·6 0·187
Data are adapted from reference 4. *Age-standardised rates per 100 000 women.
Table 2: Incidence and mortality, of breast cancer
academic and other sources; 95% interventional, 36%
phase 1–2 and 60% phase 3–4 (table 1).76 For the period
June 2010–11, 35 papers of Mexican breast cancer were
listed in PubMed. 45% were descriptive and epidemiological
studies, 35% basic and translational studies, and 17%
clinical trials. This number contrasts with the
400 publications from the USA in the same period.
Nevertheless, Mexico has the third greatest number of
clinical trials in Latin-American countries after Brazil
and Argentina (table 1). INCAN, the National Institute of
Public Health, and the National Autonomous University
of Mexico are the three main centres contributing to
breast-cancer research.
Discussion
Increases in incidence and mortality related to cancer
in developing countries could be due to population
growth, ageing, lifestyle changes, and low health-care
expenditures, which are shown in screening strategies
and access to treatment.75 Latin-American countries
contribute to 10% of breast-cancer deaths worldwide.4
In Mexico, policy reforms and the addition of financial
protection for several cancers through Seguro Popular,
including breast cancer in 2007, seem to be catalysing
change, at least for increased access and adherence to
treatment.
Improving trends in mortality for breast cancer in
Mexico since the late 1990s are not yet well explained.
They could partly be due to improvements in access to
screening, diagnosis, and treatment. However, this trend
started before changes in health-care policies and should
be analysed and compared with other trends in health
factors, such as obesity, diabetes, and other chronic
diseases, and changes in women’s reproductive patterns
that are related to improvements in outcomes for breast
cancer. Despite these changes, breast cancer in Mexico is
still more lethal than it is in wealthier countries (table 2).
Efforts should focus on adapting treatment models that
are effective in other populations to the Mexican
population.
In low-income to middle-income countries, screening
programmes for breast cancer might start at a young
age because of the age of breast-cancer presentation.75
www.thelancet.com/oncology Vol 13 August 2012

Although the average age of breast-cancer diagnosis in
Mexican women is about 10 years younger than in
women in the USA, the age presentation might be
driven by the age distribution of the population rather
than by higher age-specific incidences of breast cancer
in younger women in Mexico, where there is a smaller
proportion of women older than 50 years (16% of the
total female population vs 32% in the USA). In Mexico,
official screening guidelines that recommend starting of
screening at age 40 years have been debated inter-
nationally because mammographic screening pro-
grammes could be less effective in reducing mortality in
younger (<50 years) than in older (>50 years) women.
Mexican health-care authorities need to consider several
factors: that the recommended guidelines will raise
health-care costs, that a successful screening
programme should include at least 70% of the
population, that the last report in Mexico indicated
coverage of only 16% of the population, and that the
uptake of a screening programme could likewise be low
in a young population. Furthermore, the Ministry of
Health should consider that in young women, fast-
growing tumours are more common than in older
women. Additionally, tumours in dense breast tissue
are commonly missed on screening mammograms and
are more common in young women than in older
women, which could attenuate the potential benefit of
screening younger women.
Most Mexican women are diagnosed with breast
cancer at a late stage and triple-negative disease is
highly prevalent. Differences in breast-cancer stage or
detection, presentation, and limited access to health
care, might explain the poor outcomes in Mexican
patients. Nevertheless, other factors might be specific to
the Mexican population, such as different patterns of
gene expression, tumour biology, and host factors
related to response to treatments. These factors should
be explored, especially in the improving context of
financial protection and access to treatment through
Seguro Popular.
Although in past years reporting of epidemiological
data has improved, a high-quality population-based
cancer registry is still needed in Mexico. Most Mexican
breast-cancer centres do not report the accuracy of
diagnosis, quality of tumour biomarkers, or access to
treatment. Information is scarce about the quality of
treatments given to patients; however, these data are
essential to identify ways to improve outcomes. Our
international breast cancer research group is undertaking
a survey of physicians for patterns of care in patients
with breast cancer in Mexico.76
The incorporation of programmes for early detection
and diagnosis of breast cancer coupled with health
insurance for poor individuals has been a major advance.
Early results have so far been encouraging. Although
rates of mammographic screening in Mexico are far
lower than WHO’s recommendations, since imple-
www.thelancet.com/oncology Vol 13 August 2012
Review
Search strategy and selection criteria
We identified relevant breast-cancer studies written in English or Spanish through a
structured literature search of Medline (Jan 1, 1996, to Dec 16, 2011) and Scientific
Electronic Library Online (conceived for Latin American and Caribbean countries) using
the medical subject headings (MeSH) “breast neoplasm”, “breast cancer”, or “breast
tumors”, and “Mexico”, not New Mexico. We included 35 of 187 retrieved articles.
Exclusion criteria were studies not specific to breast cancer, case reports, and articles that
had not been updated or were unavailable. We did additional searches of “breast
neoplasm” (MeSH) and “Mexico”, plus one of the following terms: “and risk factors”,
“and surgery”, “and sentinel node”, “and radiotherapy”, “and chemotherapy”, “and
endocrine therapy”, or “and palliative care”. We selected studies through detailed reading
of online abstracts and identified further studies by reviewing the reference lists from
retrieved manuscripts.
mentation in 2000, screening has probably contributed
to the 4% decline in deaths from breast cancer.9,10 Still
needed is an increase in quality control along with the
growth of screening, and a national referral system to
confirm diagnosis in combination with prompt and
appropriate treatment; only then will screening and
treatment programmes optimally improve clinical out-
comes. Furthermore, programmes that promote healthy
lifestyle should be supported, with continuing education
of health-care personnel and strategies to avoid the
centralisation of oncologists.
Civil society organisations participate in various
activities, including advocacy, education, early detection,
and treatment of breast cancer.77 Civil society has become
increasingly active in breast-cancer issues, and, in 2009,
a group of non-governmental organisations participated
in updating the national norms for the care of breast
cancer, and in advocacy and evidence building.78,79
Although we could not identify all research done in
Mexico, and the timeframe of our search is short and
production could fluctuate in time, we have ascertained
that a major weakness in Mexico is the paucity of re-
search and concomitant publications. A Mexican breast-
cancer collaborative research group would encourage
research in studies of epidemiology, demographic
characteristics, quality of diagnosis and treatment, and
patterns of response and toxic effects to anticancer
treatment in Mexico. Moreover, collaboration with
international research groups and participation in
multinational trials will improve the value and effect-
iveness of health interventions for the country.
The main limitations of our Review were the absence
of information available and publication and
registration bias, which favoured manuscripts
published in indexed peer-reviewed literature.
Nevertheless, we have summarised information about
the challenge faced by Mexico with respect to breast
cancer, especially in patterns of the disease. This Review
is relevant not only for Mexican health-care providers,
but also for readers from other countries that face
similar challenges.
e341
 Review
Contributors
YC-G did the literature search and designed the figures and tables.
YC-G, CV-G, PERL, FK, DMF, and PEF planned the manuscript,
analysed the data, and, with AM, wrote the manuscript. FK analysed the
data.
Conflicts of interest
FK is the wife of Julio Frenk, former Secretary of Health of Mexico;
participated in the design and research of Seguro Popular; and is a
co-investigator in a study funded by GlaxoSmithKline. All other authors
declare that they have no conflicts of interest.
Acknowledgments
PEG, DMF, PERL, and YC-G thank the Avon Foundation New York.
We thank the National Council of Science and Technology (CONACYT)
for their finacial support to breast-cancer research (grant number 85055,
Sector Research Fund for Education), and Gustavo Nigenda and
Hector Arreola for reviewing the manuscript.
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