Clin Transl Oncol
DOI 10.1007/s12094-017-1666-6
RESEARCH ARTICLE
Breast self-exam and patient interval associate with advanced
breast cancer and treatment delay in Mexican women
E. Leon-Rodriguez1 • C. Molina-Calzada1 • M. M. Rivera-Franco1
A. Campos-Castro1
Received: 21 March 2017 / Accepted: 19 April 2017
Ó Federación de Sociedades Españolas de Oncologı́a (FESEO) 2017
Abstract
Purpose The objective of this study was to compare
treatment intervals in breast cancer patients according to
the detection method (breast self-exam vs screening).
Patients and methods We conducted a retrospective anal-
ysis including 291 breast cancer patients at a Mexican
tertiary referral hospital.
Results Breast cancer detection method was mostly breast
self-exam (60%). The median patient interval was
60.5 days, and was associated with marital status and
socioeconomic level. Differences between the two groups
were statistically significant for global interval, p = 0.002;
however, health system interval was not statistically
different.
Conclusion In our country, breast cancer screening is
opportunistic, with several weaknesses within its manage-
ment and quality systems. Our study showed that even in
specialized health care centers, breast cancer is detected by
self-exam in up to 2/3 of patients, which can explain the
advanced stages at diagnosis in our country. In developing
countries, the immediate health care access for breast
cancer patients should be prioritized as an initial step to
reduce the global treatment initiation interval in order to
reduce mortality.
Keywords Breast cancer
Breast self-exam

Mammogram
Mexico
& E. Leon-Rodriguez
eucarios@hotmail.com
1
Hematology and Oncology Department, Instituto Nacional de
Ciencias Medicas y Nutricion Salvador Zubiran, Vasco de
Quiroga 15 Belisario Dominguez Seccion XVI,
14080 Mexico City, Mexico
•
Introduction
Breast cancer is the second most common cancer in the world,
and the most frequent cancer in women with approximately
1.67 million new cases diagnosed in 2012, and half of these
cases occurring in less developed regions [1]. At the beginning
of 2006, breast cancer became the second most common cause
of death in women aged 30–54 years in Mexico. Breast cancer
affects young and older women, but in developing countries,
the affected population entails up to 50% of women younger
than 54 years [2].
It has been demonstrated, especially in developed coun-
tries, that breast cancer mortality at a population level can be
decreased. Since 1990, in the United States, breast cancer
mortality has been falling by nearly 2% every year as a result
of early detection by screening combined with timely and
effective treatments [3]. Low- and middle-income countries
(LMICs) report a high breast cancer mortality as a result of
late-stage diagnosis, which leads to poor outcomes when
combined with delayed therapy [4]. The few available data
suggest that only between 5 and 10% of breast cancer cases in
Mexico are detected at initial stages when compared to 50% in
the USA [5]. Prognosis in breast cancer depends on stage at
diagnosis, thus, survival correlates with the existence of early
detection programs and provided health services. Care delay
has been subdivided in patient delay (PD) and health system
(SD) delay [6]. According to Caplan [7], PD is a delay in
seeking medical attention after discovering a potential breast
cancer symptom, whereas SD is a delay within the health care
system. On the other hand, there are growing international
efforts to describe and measure patient journeys prior to a
cancer diagnosis. Accurate descriptions of these patient
journeys and valid measurements of diagnostic intervals are
essential to determine the effectiveness of interventions to
reduce them.
123

Currently, cancer care programs are gaining priority in
middle-resource countries; however, late stage at presen-
tation remains a substantial barrier to improving breast
cancer outcomes and underscores the importance of early
detection.
Breast self-examination (BSE) is the least expensive early
detection screening method because it does not require
advanced technology neither physician intervention.
Although there is increasing literature available on BSE,
randomized trials have not shown improvement in breast
cancer mortality, suggesting that BSE should only be
encouraged as part of breast cancer awareness programs and
not be depended upon alone to decrease breast cancer mor-
tality [8]. Early detection of breast cancer by systematic
mammography screening can potentially find lesions for
which treatment is more effective and generally more favor-
able for quality of life; however, simply establishing public
policies for mammogram screening programs is unlikely to be
adequate. For this reason, the European Guidelines for
Quality Assurance in Breast Cancer Screening and Diagno-
sis were developed within the Europe against Cancer Pro-
gramme [9]. Nonetheless, despite international guidelines
providing an overview of the fundamental points and princi-
ples that should support any quality breast cancer screening or
diagnostic service this is not always applied in developing
countries. Active recruitment through awareness programs
needs to be linked to screening to garner participation. Further,
health system and patient barriers, for instance, beliefs in
alternative medicine, persist in middle-resource settings. In
this context, socioeconomic and cultural background of
patients can contribute directly to PD. Also, early detection
programs for breast cancer, when available, are often inade-
quate and poorly organized. In upper-middle-income coun-
tries, such as Mexico, screening methods, such as
mammograms, are not always affordable for a target popu-
lation of women at risk and the coverage of the screening
provided by state-led health systems is insufficient. In the
absence of regular breast cancer screening programs, mea-
suring the extent of patient and health system intervals and
exploring the underlying causes can help understand barriers
to early detection, and foster the implementation of appro-
priate measures in order to improve outcomes. The objective
of the present study was to compare treatment intervals in
patients whose breast cancer was detected either by screening
or by self-examination in a Mexican tertiary referral hospital.
Patients and methods
Hospital, patients, and data
We conducted a retrospective study of breast cancer
patients treated at the National Institute of Health
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Clin Transl Oncol
Sciences and Nutrition Salvador Zubiran. This is one of
the National Institutes of Health under the Ministry of
Health in Mexico. It is one of Mexico’s most prestigious
medical and scientific assistance institutions. Most of the
patients have chronic degenerative diseases such as
rheumatoid arthritis, diabetes, cancer, among others.
Most requested outpatient services are internal medicine,
gastroenterology, rheumatology, hematology, oncology,
and endocrinology. Among our oncology population,
breast cancer is one of the most common malignancies,
providing treatment to approximately 50–100 patients
each year at our Institution. Some breast cancer patients
are referred from first contact centers in Mexico City or
other states, or they have been previously treated at our
Institution for other diseases.
Patients are assigned a social work classification during
the first interview, according to which health care expenses
are subsidized in different percentages by the Institution,
ranging from 1 (patient pays 5% of the total cost) to 6
(payment of 100%, total cost), and 110% is charged for
level 7 (private insurances).
We identified approximately 800 patients with breast
cancer diagnosis between June 2000 and July 2016, at
our Institution. Patients receiving treatment at another
institution were excluded (n = 400). Also, patients with
incomplete or unknown treatment (chemotherapy or
surgery) dates, as well as patients whose tumors were
detected by clinical breast exam, were excluded
(n = 109). The final study cohort included 291 newly
diagnosed breast cancer patients, who received first-line
treatment at our Institution. Data analysis was performed
between August and November 2016. The dataset used
for this retrospective study derived from patients’ infor-
mation collected from the hospital medical records.
Electronic records and imaging reports were also revised.
Informed consent was obtained from all the patients
before undergoing treatment. The Institutional Review
Board approved the usage of patients’ information for
this study.
Time intervals and endpoints
The time interval definitions were as follows: (1) Global
interval was defined as the time from identification of
the problem (self-examination or mammogram) to the
beginning of cancer treatment, (2) patient interval is
defined as the time point when first symptoms or bodily
changes (self-examination) were noticed to the first
medical consultation (either at our Institution or else-
where), and (3) health care system interval was defined
as the time from the first medical consultation (either at
our Institution or elsewhere) to the beginning of cancer
treatment.
Clin Transl Oncol
Statistical analysis
Continuous variables were presented as median with a
range (minimum–maximum). Categorical variables were
reported as numbers and percentages. Variables with nor-
mal distribution were compared with independent t test or
one-way ANOVA. Categorical variables were compared
with the Chi-square or Fisher’s exact test. Patients were
dichotomized by detection method (SBE or screening) with
analyses performed accordingly. Kaplan–Meier curves
were estimated for the total interval. Log-rank was used to
compare the group detected by self-examination versus
screening. Statistical significance was set at p \ 0.05. All
analyses were carried out using IBM-SPSS-Statistics, ver-
sion 21 (IBM, Armonk, NY, USA).
Results
Two hundred and ninety-one patients were included. The
median age at diagnosis was 57 years (range 27–89).
Twenty-four percent had a bachelor degree as highest
educational attainment. Most of the patients (90%) lived in
urbanized areas. Half of the patients (n = 144) were mar-
ried, and 63% were unemployed. One hundred and thirty-
eight (47%) patients had a social work classification III,
and 154 patients (53%) were previously registered in our
Institution due to other pathologies; 55% of our patients
were registered in the Catastrophic Health Expenditure
Fund of the People’s Health Insurance (Seguro Popular)
provided by the Mexican government, which covers all
breast cancer expenses at our Institution since August
2011. The detection method of the tumor was mostly self-
examination (n = 174, 60%). The other 40% were detected
by screening mammogram. Clinical stages at diagnosis
were as following in the self-exam group: 2.8% in situ,
48.8% I–IIA, and 37.3% IIB–IIIC, in comparison with the
screening group, which showed 20.5, 68.3, and 5.1%,
respectively. Treatment differed according to the clinical
stage, but most commonly, patients underwent breast sur-
gery as first-line treatment (n = 179, 59%). For the local-
ized breast cancer patients receiving chemotherapy as first-
line treatment (25%), the most commonly used regimen
was sequential weekly paclitaxel (75 mg/m2) for 12 weeks,
followed by AC (doxorubicin 60 mg/m2 and cyclophos-
phamide 600 mg/m2) on day 1 every 3 weeks for
12 weeks. This combination was also used for patients
undergoing adjuvant chemotherapy.
In the self-breast exam group, most of the patients had
positive hormone receptors and HER2- tumors (n = 117,
67%), followed by triple-negative tumors (n = 24, 14%),
pure HER2 tumors (n = 20, 12%), and positive hormone
receptors and HER2? tumors (n = 13, 7%). For patients
diagnosed by mammogram, the most common tumor sub-
type was also positive hormone receptors and HER2-
(n = 96, 82%), followed by triple-negative tumors (n = 10,
9%), positive hormone receptors and HER2? tumors
(n = 5, 4%), and pure Her 2 tumors (n = 3, 5%).
Statistically significant differences in clinical charac-
teristics were observed between the two groups (SBE vs
mammogram): age (p = 0.005), tumor size (p \ 0.0001),
clinical stage (p \ 0.0001), menopausal status
(p = 0.001), and first-line treatment (p \ 0.0001), which
are shown in Table 1.
Time intervals are shown in Table 2. For patients detected
by self-examination, intervals were as follows: patient interval
60.5 days, health system interval 52.5 days, and global
interval 150 days. For patients detected by mammogram,
intervals were 42 and 58 days for health system interval and
global interval, respectively. Differences between the two
groups (self-examination and screening) were statistically
significant for global interval, p = 0.002. Health system
interval was not statistically different, p = 0.2. Patient inter-
val was statistically associated with marital status (shorter
interval in married women) p = 0.04, and with socioeco-
nomic level (longer interval in levels 1–3) p = 0.045. It was
not associated with age, occupation, or education attainment
(p = 0.74, p = 0.3, and p = 0.18, respectively).
There was a statistically significant association in the
BSE group between advanced clinical stages and delayed
patient interval, as well as in the global interval
(p = 0.008, and 0.005, respectively); no significance was
observed when associating clinical stages with health sys-
tem interval (p = 0.13). In the screening group, neither
health system nor global intervals were significant when
associated with clinical stages (p = 0.31, and 0.30,
respectively). Tumor size was not statistically associated
with intervals when dichotomizing according to detection
method (results not shown).
When comparing previously registered patients in our
institution and new patients, there were no differences
between the detection methods or time intervals.
Overall survival comparing clinical stages according to
breast cancer detection method is shown in Fig. 1. With a
median follow-up of 40 months, survival in patients
detected by self-exam versus mammogram, for stages IA-
IIA was 93 vs 97.5%, and regarding stages IIB-IIIA, sur-
vival was 65 vs 100%, respectively. Nonetheless, this was
not statistically significant (p = 0.2).
Discussion
In 1938 [10], two main types of delay that influenced
cancer treatment were first defined in the literature: patient
delay (a delay C3 months from symptom discovery by the
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 Clin Transl Oncol

Table 1 Patients’
Characteristics Self-examination, n (%) Screening, n (%) p
characteristics
Population 174 (60) 117 (40)
Age Median: 55 (27–88) Median: 59 (34–89) 0.005
Educational attainment
None 8 (5) 4 (3.5) 0.2
Elementary to high school 101 (58) 58 (49.5)
Bachelor or higher 58 (33) 48 (41)
Unknown 7 (4) 7 (6)
Marital status
Married 79 (45) 65 (56) 0.4
Other 95 (55) 52 (44)
Living area
Urban 155 (89) 108 (92) 0.7
Rural 19 (11) 9 (8)
Occupation
Employed 67 (38) 40 (34) 0.9
Unemployed 108 (62) 77 (66)
Social work level
I–II 53 (31) 29 (25) 0.5
III 84 (48) 54 (46)
IV–VII 37 (21) 34 (29)
Previous institutional patient
Yes 66 (38) 88 (75) \0.0001
No 108 (62) 29 (25)
Popular Health Care
Yes 101 (58) 60 (51) 0.3
No 73 (42) 57 (49)
Tumor size (mm) Median: 23 (2–80) Median: 13 (0.6–80) \0.0001
BIRADS
4A 3 (2) 9 (8) \0.0001
4B 11 (6) 19 (16)
4C 15 (9) 29 (25)
5 81 (46) 42 (36)
6 40 (23) 11 (9)
Unknown 24 (14) 7 (6)
Clinical stage
In situ 5 (3) 24 (21) \0.0001
IA, IB, IIA 85 (49) 80 (68)
IIB–IIIC 65 (37) 6 (5)
IV 12 (7) 2 (2)
Unknown 7 (4) 5 (4)
Menopausal status
Pre-menopausal 67 (38) 23 (20) 0.001
Post-menopausal 107 (61) 94 (80)
First-line treatment
Surgical 73 (42) 99 (85) \0.0001
Pharmacological 100 (57.4) 18 (15)
Radiotherapy 1 (0.6) 0 (0)

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Table 2 Patient, health system,
Time interval
and global intervals (days)
Patient interval (days)
Health system interval (days)
Global (days)
N/A not applicable
Fig. 1 Overall survival comparing self-exam versus screening
according to clinical stages (CS) p = 0.2
patient to first medical visit) and provider delay (a
delay [1 month from first medical visit to the initiation of
treatment). However, current approaches to ‘delay’ within
the patient interval can be inconsistent and often judg-
mental according to different authors [11]. Analysis of the
patient interval should be based on presenting symptom, as
opposed to pathology, to better reflect the context of the
help-seeking interval, and suggest how new definitional
boundaries could be developed. Currently, the term interval
is a preferable alternative.
The association between patient delay and socio-de-
mographic factors, cancer knowledge, family history, and
other factors has been widely studied. According to the
meta-analysis published by Ramirez et al. [12], the only
socio-demographic factors that seemed to be strongly
associated with patient delay up to 1999 were the patient’s
single marital status and advanced age. Our results showed
an association with marital status and low socioeconomic
level; however, age was not statistically significant. Sub-
sequent studies have continued to come up with contra-
dictory results. However, most of these studies are from the
high- and middle-income countries. On average, 20–35%
of breast cancer patients delay seeking care for a breast
Self-examination, median (range) Screening, median (range) p
60.5 (0–2243) N/A
52.5 (3–3831) 42 (0–1398) 0.2
150 (11–4068) 58 (2–1403) 0.002
symptom three or more months [13]. The association
between socioeconomic status and delay has not been
firmly demonstrated. Thus, this variable has been measured
in different ways which are not comparable between
studies, and it could be an important factor mostly in
developing countries where socioeconomic differences are
more noticeable.
In addition, patients affiliated with general health care
plans have better access to health services and, therefore,
greater chances of breast cancer diagnosis. However, we
did not observe significant differences in intervals whether
the patients previously attended at our institution or not.
There are two Mexican studies reporting on patient
delay. Bright et al. [14], reported a retrospective study
including 32 patients (22% detected by mammogram) from
one of the main Social Security Hospitals in Mexico, which
reported a patient delay, a health system delay, and a global
delay of 1.8, 0.6, and 8.4 months, respectively. Four years
later, a multi-centric study including 886 patients, from
which 75.6% detected through self-exam, showed a patient
delay of 10 days, a health system delay of 5 months, and a
global delay of approximately 7 months [15]. However, the
latter, did not specify the patient delay interval, most likely
they used the interval between mammogram and first
medical consult, which would be inaccurate, making it
ambiguous to interpret that result.
Piñeros et al. [16] performed a study among 1106
Colombian women with breast cancer, using census
approach. Their results showed that more than 80% of the
women (902) consulted due to symptoms; the majority had
advanced-stage disease. Patient delay was established in
20.3% ([3 months) and the main related factors were older
age and lack of social security.
Higher education in patients was associated with
reduced delays. Patient delay and related factors were
similar to those found in other studies.
Odongo et al. [17], reported that in Uganda, the overall
median delay to the first medical consultation was
13 months (1–127), similar to another study published in
2014, reporting 12 months [18]. This contrasts with the
findings in studies done in developed countries where
median delay to the first medical consultations was found
to be 9–61 days [19, 20]. Our study participants had a
median patient interval of 60 days similar to other LMICs
with median times of 2–3 months like Malaysia and Egypt
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[21, 22], and very different from the recently reported in
Moroccan women (6 months) [23].
A study of 256 Mexican women diagnosed with breast
cancer revealed that 90% identified the problem by them-
selves, and only 10% was diagnosed in stage I [24]. In 40%
of our patients, breast cancer was detected by screening,
showing a higher percentage when compared to the pre-
viously reported literature in our country, where there is
only 16–26% of coverage [25]. This could be explained
because 75% of the 117 patients detected by screening
were previously institutional patients. However, in 25% of
these patients, detection was through self-exam.
It is widely known that breast cancers revealed by SBE
are more aggressive compared to those found on mam-
mogram. Ma et al. [26], demonstrated that cancers detected
by SBE were larger tumors (2.4 vs. 1.3 cm), higher grade,
more frequently ER- (29 vs. 16%), triple negative (21 vs.
10%), and lymph node-positive (39 vs. 18%); all p B 0.01.
In both groups of our cohort, the most common tumors had
positive hormone receptors (HER2 negative), followed by
triple-negative tumors.
Early detection has to be emphasized and an important
action to achieve this could be increasing consciousness
and education among women, an effort which has to be
complemented with an adequate and sufficient healthcare
offered for most of the population, as possible. It is not
realistic to assume that developing countries can become
large-scale mammogram providers in a short or medium
period of time for all women requiring this intervention.
Therefore, self-examination remains the only other viable
large-scale screening method in these limited-resource
settings. The situation is complicated by the fact that there
is enough evidence showing that breast self-exam and even
clinical exam are not effective enough to reduce mortality
in populations where breast cancer is mostly detected in
early stages [27]. The Health Department in Mexico has
been working on the implementation of an organized breast
cancer screening program, through the performance of
mammograms, with a target population of women aged
40–69 years, receiving medical attention from this gov-
ernmental institution (6,821,069) [28]. Nonetheless, there
are no organized screenings among the 32 states. Accord-
ing to the National Nutrition Surveys in Mexico, only 12%
women aged 40–69 years have undergone a clinical exam
(including mammogram) in 2000, with the percentage in
2012 increasing only 3% (15%) among women aged
40–69 years, and 26% in women aged 50–69 years [24].
These data underscore the need to optimize early breast
cancer detection programs in settings with limited resour-
ces, and could explain the increase in mortality as a result
of this type of cancer, diagnosis at late stages in 80–90%,
and up to 5000 annual deaths in women 25 and older [29].
Considering these issues, breast cancer screening in
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Mexico remains opportunistic, with several weaknesses
within its management system, health information system,
and infrastructure quality control, patient follow-up sys-
tem, and accountability, factors that have been previously
studied and might contribute to the low effectivity of this
strategy [30]. Our study showed that even in specialized
health care centers, like ours, breast cancer is detected by
self-exam in up to 2/3 of patients, which can explain the
advanced stages at diagnosis in our country. In our cohort,
coinciding with previously reported literature, there were
differences in the clinical stages at diagnosis according to
the detection method. Eighty-eight percent of patients had
in situ or I–IIA clinical stage, and only 6.5% presented with
locally advanced stages or metastatic breast cancer when
detected by screening, compared to 20.5 and 73.4%,
respectively, when detected by BSE. Survival was better in
clinical stages IA–IIA compared to IIB–IIIC when detected
by BSE, and although none of the patients in the screening
group with clinical stages IIB–IIIC died, there were only
seven patients, so this could explain this outcome, com-
pared to 97.5% of survival in IA–IIA patients.
It seems therefore understandable that the non-govern-
mental organizations and the Ministry of Health in Mexico
continue to emphasize the importance of breast self-ex-
amination as an integral part of the early breast cancer
detection strategy. Also, even if regularly performed, a
clinical exam does not necessarily include the generalized
examination of the breasts, and might not be solid from the
technical perspective. Further, mammogram is not acces-
sible as a result of inadequate amount of units and staff,
especially in rural areas [5, 25].
Health centers with a multidisciplinary approach,
including pathology laboratories, radiotherapy, and surgi-
cal support, help avoid fragmentation of care, and should
be part of all breast cancer control programs worldwide,
accessible to all women in the population. While available
in most developed countries, these centralized services and
specialists are less available in the public sector of low- and
middle-income countries. Existing centers of excellence
need to develop methodologies for outreach into the public
sector including surrounding rural areas. Public policies
involving training and quality assurance need to be incor-
porated into breast cancer control programs in developing
countries to decrease delays and consequently mortality.
As an example, the most recent European Guidelines for
Quality Assurance in Breast Cancer Screening and Diag-
nosis established an approximate 8-weeks global interval
[13].
The limitations of this study include its small, retro-
spective, and unicentric nature, along with a possible lim-
ited generalizability as our Institution is a tertiary hospital.
However, we conclude that to reduce SD, health services
must fit within the socioeconomic and cultural or ethnic
Clin Transl Oncol
background of patients. Furthermore, in Mexico, like any
other low- or middle-income country, the immediate health
care access for breast cancer patients should be prioritized
as an initial step to reduce the global treatment initiation
interval and consequently reduce mortality, since breast
cancer detection through screening mammogram, if opti-
mized, will not be useful until the access interval to spe-
cialized health centers is diminished.
Compliance with ethical standards
Conflict of interest None of the authors have any conflict of interests
to disclose.
Research involving human participants and/or animals This ret-
rospective protocol was approved by the Institutional Review Board
(Ethics and Human Research Committees) of Instituto Nacional de
Ciencias Medicas y Nutricion Salvador Zubiran, Mexico City, Mex-
ico, with the reference number 2120.
Informed consent Informed consent was obtained from all the
patients before undergoing treatment. But our Institutional Review
Board (Ethics and Human Research Committees) agreed that patients
were not requested to fill out an additional informed consent to par-
ticipate in this retrospective study since all their information was
protected and codified with numbers in our database and the manu-
script, and no intervention was given.
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