Childhood acute leukemias are frequent in Mexico City: Descriptive epidemiology

Abstract

Worldwide, acute leukemia is the most common type of childhood cancer. It is particularly common in the Hispanic populations residing in the United States, Costa Rica, and Mexico City. The objective of this study was to determine the incidence of acute leukemia in children who were diagnosed and treated in public hospitals in Mexico City.
Included in this study were those children, under 15 years of age and residents of Mexico City, who were diagnosed in 2006 and 2007 with leukemia, as determined by using the International Classification of Childhood Cancer. The average annual incidence rates (AAIR), and the standardized average annual incidence rates (SAAIR) per million children were calculated. We calculated crude, age- and sex-specific incidence rates and adjusted for age by the direct method with the world population as standard. We determined if there were a correlation between the incidence of acute leukemias in the various boroughs of Mexico City and either the number of agricultural hectares, the average number of persons per household, or the municipal human development index for Mexico (used as a reference of socio-economic level).
Although a total of 610 new cases of leukemia were registered during 2006-2007, only 228 fit the criteria for inclusion in this study. The overall SAAIR was 57.6 per million children (95% CI, 46.9-68.3); acute lymphoblastic leukemia (ALL) was the most frequent type of leukemia, constituting 85.1% of the cases (SAAIR: 49.5 per million), followed by acute myeloblastic leukemia at 12.3% (SAAIR: 6.9 per million), and chronic myeloid leukemia at 1.7% (SAAIR: 0.9 per million). The 1-4 years age group had the highest SAAIR for ALL (77.7 per million). For cases of ALL, 73.2% had precursor B-cell immunophenotype (SAAIR: 35.8 per million) and 12.4% had T-cell immunophenotype (SAAIR 6.3 per million). The peak ages for ALL were 2-6 years and 8-10 years. More than half the children (58.8%) were classified as high risk. There was a positive correlation between the average number of persons per household and the incidence of the pre-B immunophenotype (Pearson's r, 0.789; P = 0.02).
The frequency of ALL in Mexico City is among the highest in the world, similar to those found for Hispanics in the United States and in Costa Rica.

Full text

RESEARCH ARTICLE Open Access
Childhood acute leukemias are frequent in
Mexico City: descriptive epidemiology
María Luisa Pérez-Saldivar
1
, Arturo Fajardo-Gutiérrez
1
, Roberto Bernáldez-Ríos
2
, Armando Martínez-Avalos
3
,
Aurora Medina-Sanson
4
, Laura Espinosa-Hernández
5
, José de Diego Flores-Chapa
6
, Raquel Amador-Sánchez
7
,
José Gabriel Peñaloza-González
8
, Francisco Javier Álvarez-Rodríguez
9
, Victoria Bolea-Murga
10
, Janet Flores-Lujano
1
,
María del Carmen Rodríguez-Zepeda
2
, Roberto Rivera-Luna
11
, Elisa María Dorantes-Acosta
4
,
Elva Jiménez-Hernández
5
, Martha Alvarado-Ibarra
6
, Martha Margarita Velázquez-Aviña
8
, José Refugio Torres-Nava
9
,
David Aldebarán Duarte-Rodríguez
1
, Rogelio Paredes-Aguilera
12
, María de los Ángeles del Campo-Martínez
5
,
Rocío Cárdenas-Cardos
3
, Paola Hillary Alamilla-Galicia
1
, Vilma Carolina Bekker-Méndez
13
,
Manuel Carlos Ortega-Alvarez
14
and Juan Manuel Mejia-Arangure
1*
Abstract
Background: Worldwide, acute leukemia is the most common type of childhood cancer. It is particularly common
in the Hispanic populations residing in the United States, Costa Rica, and Mexico City. The objective of this study
was to determine the incidence of acute leukemia in children who were diagnosed and treated in public hospitals
in Mexico City.
Methods: Included in this study were those children, under 15 years of age and residents of Mexico City, who
were diagnosed in 2006 and 2007 with leukemia, as determined by using the International Classification of
Childhood Cancer. The average annual incidence rates (AAIR), and the standardized average annual incidence rates
(SAAIR) per million children were calculated. We calculated crude, age- and sex-specific incidence rates and
adjusted for age by the direct method with the world population as standard. We determined if there were a
correlation between the incidence of acute leukemias in the various boroughs of Mexico City and either the
number of agricultural hectares, the average number of persons per household, or the municipal human
development index for Mexico (used as a reference of socio-economic level).
Results: Although a total of 610 new cases of leukemia were registered during 2006-2007, only 228 fit the criteria
for inclusion in this study. The overall SAAIR was 57.6 per million children (95% CI, 46.9-68.3); acute lymphoblastic
leukemia (ALL) was the most frequent type of leukemia, constituting 85.1% of the cases (SAAIR: 49.5 per million),
followed by acute myeloblastic leukemia at 12.3% (SAAIR: 6.9 per million), and chronic myeloid leukemia at 1.7%
(SAAIR: 0.9 per million). The 1-4 years age group had the highest SAAIR for ALL (77.7 per million). For cases of ALL,
73.2% had precursor B-cell immunophenotype (SAAIR: 35.8 per million) and 12.4% had T-cell immunophenotype
(SAAIR 6.3 per million). The peak ages for ALL were 2-6 years and 8-10 years. More than half the children (58.8%)
were classified as high risk. There was a positive correlation between the average number of persons per
household and the incidence of the pre-B immunophenotype (Pearson’s r, 0.789; P = 0.02).
Conclusions: The frequency of ALL in Mexico City is among the highest in the world, similar to those found for
Hispanics in the United States and in Costa Rica.
* Correspondence: juan.mejiaa@imss.gob.mx
1
Unidad de Investigación en Epidemiología Clínica, Unidad Médica de Alta
Especialidad UMAE Hospital de Pediatría, Centro Médico Nacional (CMN)
Siglo XXI, Instituto Mexicano de Seguridad Social (IMSS), México D.F., México
Full list of author information is available at the end of the article
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© 2011 Pérez-Saldivar et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.

Background
Acute leukemias (AL), especially acute lymphoblastic
leukemias (ALL), have been reported with a very ele-
vated incidence within the Hispanic pediatric population
in the United States (USA) [1-3]. For children under the
age of 15 years, the incidences of ALL worldwide varies
between 20-35 cases per million [4], whereas the inci-
dence of ALL for Costa Rica and in Mexico City (also
known as the Distrito Federal)andfortheHispanic
populations that live in the USA are greater than 40
cases per million [1-6].
The incidence rates of leukemias that have been
reported for Mexico City correspond fundamentally to
that portion of the population, i.e., private-sector
employees and their families, entitled to the services
provided by the Instituto Mexicano del Seguro Social
(IMSS), which comprises approximately 40% of the
entire population [6,7]. In those studies, the overall inci-
dence of leukemia was found to be between 55.4 and
58.4 per million [6,7]. The incidences for various leuke-
mias are the following: ALL, between 43.2 and 44.9 per
million; acute myeloid leukemias (AML), between 9.8
and 10.6 per million [6,7]; chronic myeloid leukemias
(CML), 2.5 per million; and unspecified leukemias (UL),
0.5 per million [6]. The proportion of T-lineage ALL
has been reported at 23.6% [8], a frequency relatively
higher than that reported for the White population of
the United States of America (USA) or for Asiatic popu-
lations [8]. For our population, the proportion of chil-
dren with ALL at high risk vs. standard risk is 1:1, a
proportion higher than that reported by other institu-
tions in the USA [9].
Nevertheless, in Mexico City, there exist other popula-
tion groups that have not been represented in these stu-
dies, because they do not fall under the aegis of IMSS.
For government workers (which include such groups as
public school teachers, civil service workers, and public
servants) and their families, social security and medical
care are provided by a separate agency, the Instituto de
Seguridad Social al Servicio de los Trabajadores del
Estado (ISSSTE) [10,11]. The unemployed in Mexico
City receive medical attention at the hospitals of the
Secretaría de Salud (SSa) and at the hospitals under the
aegis of the Distrito Federal. Therefore, included in this
studywereallthepublichospitals (i.e., dependent on
the government) that provide medical care for children
with leukemia in Mexico City. It has been shown that
these public hospitals treat 97.5% of all the cases of leu-
kemia occurring in Mexico City [12]. At present, there
is no population-based registry of childhood leukemias
which encompasses the population either of Mexico
City or of the whole of Mexico, nor is there one con-
cerning childhood cancers in general [7]. For this rea-
son, the participation of all the hematological and
oncological medical personnel of the public hospitals in
Mexico City was necessary in order to be able to iden-
tify actively all the new cases of AL diagnosed within
the study period.
In Mexico, few studies have dealt with the question of
whether socio-economic level has an influence on the
incidence of leukemias [13]. From the foregoing, the
objectives of the present study were 1) to determine the
incidence of acute leukemias in children from Mexico
City; 2) to determine the frequency of the T phenotype
and the ratio of high risk to standard risk for the chil-
dren with leukemia who reside in Mexico City; and 3)
to determine the correlation between the incidence of
ALL, T-cell ALL, Pre-B ALL, and AML with municipal
human development index (MDHI), number of agricul-
tural hectares, and average number of persons per
household.
Methods
Design
Population-based, descriptive study.
Population studied
For a case to be included in this study, the patient had
to meet the following criteria:
•Be a child under 15 years of age;
•Reside in Mexico City;
•Be newly diagnosed with leukemia during the years
2006-2007, with the diagnosis confirmed by
histopathology;
•Be diagnosed and treated in a public hospital in
the Distrito Federal. (See next section, Hospitals).
All such cases from 2006 to 2007 were analyzed.
Hospitals
Although medical attention for children with AL is pro-
vided by different health institutions, both public and
private, the public sector has been estimated to treat
97.5% of the cases of AL that occur in Mexico City [10].
Of the 13 hospitals that are equipped to treat children
with AL in Mexico City, four were not included in this
study because it had been determined in previous stu-
dies that these four hospitals (two hospitals of Petróleos
Mexicanos,aHospital Militar de México,andtheHos-
pital Regional No. 25 of IMSS) had not treated cases of
children from Mexico City. The nine hospitals that were
included represent various governmental agencies:
IMSS, SSa, ISSSTE, and the Secretaría de Salud del Dis-
trito Federal (SSDF). These hospitals, in descending
order of the proportion of cases each contributed to this
study, were the following: Instituto Nacional de Pedia-
tría (SSa), 27.6%; Hospital Infantil de México “Federico
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Gómez”(SSa), 20.2%; Hospital de Pediatría del Centro
Médico Nacional “Siglo XXI”(IMSS), 19.3%; Hospital
General “Gaudencio González Garza”of the Centro
Médico Nacional “La Raza”(IMSS), 18.0%; Centro Méd-
ico Nacional “20 de Noviembre”(ISSSTE), 6.6%; Hospital
Regional “Carlos McGregor Sánchez Navarro”(IMSS),
3.5%; Hospital Juárez de México (SSa), 2.6%; Hospital
Pediátrico de Moctezuma (SSDF), 1.8%; and Hospital
General de México (SSa), 0.4%.
Sources of patient data
In each participating hospital, we had a trained nurse or
medical assistant for identifying cases of suspected acute
leukemia. For each such case, after having signed a con-
sent form, the parents were interviewed to determine
demographic variables, and the patient’s record was
reviewed to obtain the clinical variables and the diagno-
sis. To ensure the quality of our data, the information
was collected independently of the only existing Mexi-
can Registry of Childhood Cancer (MRCC), which is
maintained by IMSS and which contains data only for
those served by IMSS [7]. The concordance between the
data in our register for patients served by IMSS and the
data in the MRCC was 100%.
Diagnosis
Once diagnosed with presumed leukemia, a child was
referred to one of the hospitals where trained staff
(hematologists and onco-hematologists) did a compre-
hensive follow-up of the case to either confirm or dis-
card the diagnosis of leukemia. Bone marrow smear was
used to confirm each diagnosis; histochemical tests
(myeloperoxidase, Sudan black B reaction, esterases,
periodic acid Schiff (PAS) reaction, and acid phospha-
tase) were performed to differentiate the types of
leukemia.
Morphological classification was used to divide the leu-
kemias into five groups, according to the International
Classification of Childhood Cancer (International Classi-
fication of Disease for Oncology) [14]. Only four of the
five types were found in this study: a) ALL (9820-9827,
9850); b) AML (9840, 9841, 9861, 9864, 9866, 9867,
9891, 9894, 9910); c) CML (9863, 9868); and d) UL
(9800-9804). The files were reviewed to corroborate that
there were no duplicate records or inconsistent data. A
database was generated to record age, sex, residency, year
of diagnosis, and clinical manifestations of the patients.
Immunophenotyping was performed by flow cytome-
try. Cases of ALL were classified according to one of the
following immunophenotypes: precursor-B cell, mature-
B cell, T lineage, or “not otherwise specified”,ifthe
registered information did not allow proper classifica-
tion. For the cases of ALL, the immunophenotypes
registered were the following: for precursor B-cell ALL,
CD19+, HLADR+, cyCD22+, CD10+ or CD10, TdT+,
CD20+, cyCD79a+, and CD34+; for T lineage ALL,
CD19, CD22, CD79a, CD7+, CD5+, cyCD3+, clgm, and
sIg; and for mature B cells, immunoglobulin (kappa or
lambda light chain as surface markers).
Risk Criteria
Only two risk categories were used for this study: 1)
children, aged 1-9 years, with a white blood cell count
less than 50,000/μL were classified as being at standard
risk; 2) children either who were in the 10-14 age group
or who were younger and had a white blood cell count
greater than 50,000/μL were designated as being at high
risk [15].
Populations
Because the size of the base population, estimated from
the data for Mexico City from the Instituto Nacional de
Estadística, Geografía e Informática (INEGI) [16], was
known, it was feasible to obtain the incidence rate for
the population under 15 years of age (Additional file 1
Table S1). The denominator was calculated by using
data from the intermediate census of 2005. In 2005, the
Distrito Federal had a population of 8.72 million inhabi-
tants, 2.04 million of whom were children under the age
of 15 years [16]. With no census having been carried
out in 2006 or 2007, there is no official count for those
years; therefore, as estimation for those two years, the
2005 value for the population under 15 years of age was
multiplied by two. (The population of Mexico City has
remained quite stable from 1990 to date, with changes
of only 0.04% per year [16].)
Analysis
AAIR were calculated in total, by kind of leukemia, by
age group (< 1 year, 1-4 years, 5-9 years, or 10-14
years), and by sex. The standardized average annual
incidence rates (SAAIR) were standardized by age by
using the direct method with the world standard popu-
lation [17], reported per million.
To determine whether the SAAIR of leukemias varied
by some characteristic in the boroughs of Mexico City,
the correlation, as calculated by using Pearson’sr,
between the incidence of ALL and that of AML and the
MHDI [18] for Mexico was determined. The value of P
was reported, with P = 0.05 used as the cutoff value for
statistical significance. The MHDI is a measurement of
how well cities and their subdivisions are doing. The
values of this index range between 0 and 1, with values
closer to 1 signifying a greater degree of well-being.
Three indicators are used to construct this index:
•Long and healthy life (measured by life expectancy
at birth);
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•Educational level (measured by the adult literacy
rate and the combined raw rates of matriculation in
primary, secondary, and higher education, as well as
the length of compulsory education); and
•Standard of living (measured by the gross domestic
product (GDP) per capita purchasing power parity
(PPP) in dollars).
Information concerning this index was available only
for the year 2005 [16]. Each borough of Mexico City
was analyzed both according to the hectares used for
agriculture contained within its boundaries and accord-
ing to the average number of persons per household,
information that also was available only for the year
2005, [16] (data not shown).
This study was approved by the Ethics Board of the
National Commission of Scientific Investigation (Regis-
try No. 2008-785-063).
Results
During the period of the study, the number of new cases
of childhood leukemias diagnosed in public hospitals in
Mexico City was 303 in 2006 and 307 in 2007. Of these
610, only 228 children were residents of the Distrito
Federal (37.4%). Of the 228 patients, 194 (85.1%) had
ALL; 28 (12.3%), AML; four (1.7%), CML; and two
(0.9%) UL (Table 1).
General incidence of leukemias in children in the Distrito
Federal
The overall SAAIR was 57.6 per million (95% CI, 46.9-
68.3), with the SAAIR for ALL being 49.5 per million;
for AML, 6.8 per million; and for CML, 0.9 per million.
The male:female ratio was 1.0 for leukemias in general,
1.1 for ALL, 0.9 for AML, and 1.0 for CML.
Incidence of leukemia by age group
The AAIR for ALL was highest (77.7 per million) for the
1-4 year age group. In this age group, the AAIR for ALL
for males was higher than that for females (87.1 and 67.8
per million, respectively), whereas for the 5-9 year age
group, the AAIR for ALL was higher for females (Table 1).
Incidence of leukemia by immunophenotype
The immunophenotypes were determined for 96.4% of
the ALL cases: 73.2% of the total ALL cases were classi-
fied as precursor B-cell; 12.4% as T cell; 8.2% as B cell;
and 2.1% as dual phenotype, with 0.5% as undetermin-
able. The SAAIR of the pre-B ALL was 35.8 per million
and that of the T-cell ALL was 6.3 per million (Table 2).
Ratio of high risk to standard risk for ALL
Of the ALL patients, 58.8% were classified as being high
risk; when only those cases of ALL having precursor B-
cell immunophenotype were considered, 53.5% were
high risk.
Morphological subtypes of AML
Of the cases of AML, the most frequent classifications
were M2 with seven cases; M4, with six; and M1 and
M5, with five cases each. M3 represented only 10.7% of
the cases.
Age peak for leukemias
As determined from the graph (Figure 1) the peak age
for AL was found to be between 2-6 years of age for
Table 1 Number of cases, average incidence rates, and standardized average annual incidence rates for children from
Mexico City by kind of leukemia, sex, and age group (in years), 2006-2007
Age Group (Years)
Childhood Sex < 1 y 1-4 y 5-9 y 10-14y Total SAAIR*
Leukemia n AAIR n AAIR n AAIR n AAIR n AAIR
ALL M 4 31.9 48 87.1 26 38.1 22 30.8 100 48.2
F 2 16.5 36 67.8 36 54.6 20 28.7 94 46.8
Total 6 24.3 84 77.7 62 46.2 42 29.8 194 47.5 49.5
AML M 1 8.0 3 5.4 3 4.4 6 8.4 13 6.3
F 0 0 5 9.4 4 6.1 6 8.6 15 7.5
Total 1 4.1 8 7.4 7 5.2 12 8.5 28 6.9 6.8
CML M 0 0 1 1.8 0 0 1 1.4 2 1.0
F 0 0 0 0 0 0 2 2.9 2 1.0
Total 0 0 1 0.9 0 0 3 2.1 4 1.0 0.9
UL M 0 0 0 0 0 0 1 1.4 1 0.5
F 0 0 1 1.9 0 0 0 0 1 0.5
Total 0 0 1 0.9 0 0 1 0.7 2 0.5 0.5
AAIR: average annual incidence rate; SAAIR: standardized AAIR; ALL: acute lymphoid leukemia; AML: acute myeloid leukemia; CML: chronic myeloid leukemia; UL:
unspecified leukemia; M: male; F: female; *Expressed per million children.
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ALL, with another noteworthy peak at 8-10 years of age.
These age peaks corresponded to those for precursor B-
cell ALL. For T-cell ALL, a small peak was seen
between 1-4 years of age. The AML showed a peak at
one year and between 10-11 years (Figure 1).
Incidence of leukemias by borough and correlation with
MDHI, number of cultivated hectares, and average
number of persons per household
The SAAIRs for the boroughs of Mexico City ranged
from 23.0 to 87.7 per million, with Cuauhtémoc, a rela-
tively affluent borough, having the highest SAAIR
(Table 3).
The MHDI of the boroughs of Mexico City (Figure
2A, B) showed a negative correlation both with the
incidence of ALL (Pearson’s r, -0.138; P = 0.30) and
with the incidence of precursor B-cell ALL (Pearson’sr,
-0.185; P = 0.49); in both instances, there was little pre-
cision in the estimation. No correlation was found
between the number of cultivated hectares and the inci-
dence of either AML, ALL, or precursor B-cell immuno-
phenotype. However, there was a statistically significant,
positive correlation between the average number of per-
sons per household and the incidence of the pre-B
immunophenotype (Pearson’s r, 0.789, P = 0.02).
Discussion
The incidence rates of AL differ in the various countries
of the world, depending in great measure on the socio-
economic level of the populations [19]: the higher the
Table 2 Age-group average incidence rates of two immunophenotypes in acute lymphoid leukemia in children from
Mexico City (2006-2007)
Age Group (years)
Immuno-phenotype < 1 y 1-4 y 5-9 y 10-14 y Total
in ALL n AAIR* n AAIR* n AAIR* n AAIR* n AAIR* SAAIR*
T-Cell 0 0 13 12.0 8 6.0 3 2.1 24 5.9 6.3
Pre B 3 12.2 58 53.6 46 34.2 35 24.8 142 34.8 35.8
AAIR: average annual incidence rate; SAAIR: standardized AAIR; ALL: acute lymphoid leukemia; Pre B: Precursor B cell. *Expressed per million children.
Figure 1 Comparison of age-specific incidence rates of childhood leukemia in Mexico City (2006-2007). The age-specific incidence rates
of acute lymphoid leukemia (ALL), of acute myeloid leukemia (AML), and of ALL immunophenotypes (precursor B-cell, T cell, and B cell) for
Mexico City children (2006-2007) were compared.
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Table 3 Average annual age-standardized incidence by kind of leukemia and immunophenotype in boroughs of
Mexico City (2006-2007)
Boroughs of Mexico City Leukemia type Immunophenotype
ALL AML T-Cell Pre-B Cell
MHDI†(n) SAAIR* (n) SAAIR* (n) SAAIR* (n) SAAIR*
Alvaro Obregón 0.8719 8 23.0 2 5.0 1 2.5 6 17.1
Azcapotzalco 0.8915 5 29.4 3 16.5 3 17.4 2 12.0
Benito Juarez 0.9509 5 48.3 0 0 0 0 4 38.9
Coyoacan 0.9169 14 59.6 2 8.7 1 4.8 12 50.0
Cuajimalpa de Morelos 0.8994 3 30.1 0 0 0 0 3 30.1
Cuauhtémoc 0.8921 16 87.7 1 5.0 2 11.6 8 44.0
Gustavo A. Madero 0.8700 34 62.7 2 3.0 6 11.0 24 43.8
Iztacalco 0.8765 8 48.6 0 0 1 6.7 5 28.4
Iztapalapa 0.8463 45 47.0 10 10.9 4 4.6 33 33.7
La Magdalena Contreras 0.8558 6 54.3 0 0 0 0 6 54.3
Miguel Hidalgo 0.9188 6 43.7 2 14.1 1 6.6 5 37.1
Milpa Alta 0.7983 4 61.5 1 16.5 0 0 4 61.5
Tláhuac 0.8473 10 54.8 0 0 2 11.8 6 31.8
Tlalpan 0.8791 9 31.2 2 5.9 0 0 9 31.2
Venustiano Carranza 0.8740 12 63.7 3 14.7 1 6.2 8 41.4
Xochimilco 0.8481 9 48.4 0 0 2 9.4 7 39.1
194 49.47 28 6.76 24 6.26 142 35.80
SAAIR: standardized average annual incidence rate; ALL: acute lymphoid leukemia; AML: acute myeloid leukemia; CML: chronic myeloid leukemia; UL: unspecified
leukemia; Pre B: Precursor B cell. *Expressed per million children.
†
MHDI: Municipal Human Development Index for Mexico 2005 [18].
S
AAIR
PRE B
C
ELL ALL
ALL
MHDI
Figure 2 Correlations between municipal human development indices of boroughs of Mexico City and incidences of ALL and of
precursor B-cell immunophenotype. Panel A: Incidence of ALL; Panel B: Incidence of precursor B-cell immunophenotype. SAAIR: standardized
average annual incidence rate by million of children below under 15 years of age; MHDI: municipal human development index; Boroughs of
Mexico City: 1) Álvaro Obregón; 2) Azcapotzalco; 3) Benito Juárez; 4) Coyoacán; 5) Cuajimalpa de Morelos; 6) Cuauhtémoc; 7) Gustavo A. Madero;
8) Iztacalco; 9) Iztapalapa; 10) La Magdalena Contreras; 11) Miguel Hidalgo; 12) Milpa Alta; 13) Tláhuac; and 14) Tlalpan; 15) Venustiano Carranza;
and 16) Xochimilco. Source: Municipal Human Development Index (MHDI) for Mexico 2005 [18]. *Expressed per million children.
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socio-economic level, the higher the incidence of AL
[20]. However, the incidences among Hispanics are dis-
tinct, as Hispanic populations have the highest incidence
rates of AL. The population of Mexico City exemplifies
this situation [6,7].
General incidence of leukemias
For Mexico City, the frequency of leukemia is higher
than those for other cities. For cities in Canada, the
USA, or the UK, the SAAIRs are 50.8, 46.9, and 40.8
per million, respectively [21], whereas the SAAIR for
Mexico City was 57.6 per million children, as deter-
mined in this study. There are several factors that could
affect the results: 1) Length of study period. Due to
funding constraints, we were able to carry out our study
only over a two-year period; therefore, the representa-
tiveness of the sampling could be questioned. However,
the SAAIR is similar to those published by IMSS for the
years 1996-2000 [6] and 1996-2002 [7] (58.4 and 55.4
per million children, respectively). 2) Value used in the
denominator. Although we used 2005 data (then the
most current official information) for the denominator
in the calculations for 2006 and 2007, we are confident
that little error was introduced, because over the last 20
years, the population of Mexico City has remained
stable [16]. 3) Scope of sampling. This report does not
contain information about the children treated in private
institutions. However, because in Mexico City, nearly
97.5% of children with leukemia receive medical care in
public institutions [12], the exclusion of this small per-
centage of patients in private institutions should not
affect the main conclusions of the current study. In fact,
inclusion of said cases would result in a larger numera-
tor, thus leading to an even higher incidence rate. For
these reasons, we think that the above-mentioned con-
siderations did not affect the results. We had the oppor-
tunity to corroborate only the concordance between the
cases of IMSS patients, which were registered in this
study, and the data from the MRCC. For the data
obtained from the other hospitals, there was no other
registry with which to corroborate that the information
was complete. Nevertheless, for this study, the register-
ing of cases was done actively, in that a nurse visited
the participating hospitals daily in order to identify any
child diagnosed with suspected leukemia. Once so diag-
nosed, the patient was followed until the diagnosis was
confirmed. The information in this study was compared
to the admissions lists of the hospitals in order to verify
that no patient, who had been admitted with the diag-
nosis of leukemia, had been overlooked by the nurses
that performed the data collection. Another factor that
gives us confidence in the numerator obtained in this
study is that the SAAIR of leukemias (57.6 per million)
is similar to those reported in studies by the IMSS (55.4
and 58.4 per million [6,7]). The especially high inci-
dences, reported for children from Mexico City [6] and
Costa Rica [5]; for Hispanic children in Florida [22], Los
Angeles [23], and Texas [24] in the USA; and for Hispa-
nic children in general as reported by the SEER and the
CDC (Table 4) [1-3,25,26], are due to the incidences of
lymphoid leukemia in these populations. This finding is
very interesting because, according to data from El
Table 4 Comparison of standardized average annual incidence rates of lymphoid leukemias per million children from
cancer registries
Study Parameters
Area Source of data Population Age range years
ye
Period SAAIR
a
Mexico City Present Study Mexicans 0-14 2006-2007 49.5
USA SEER
b
[25] All races 0-14 2007 35.0
CDC
c
(NPCR) [26] All races 0-14 2003-2007 37.0
Hispanics 0-19 2003-2007 46.0
ACSSR
d
[2] Hispanics 0-14 2002-2006 46.7
Texas TCR
e
[24] All races 0-14 1999-2008 41.4
California Wilkinson et al. [1] Hispanic 0-14 1988-1998 51.1
non-Hispanic White 0-14 1988-1998 40.8
Florida Wilkinson et al. [1] Hispanic 0-14 1988-1998 49.2
non-Hispanic White 0-14 1988-1998 37.1
Costa Rica Monge et al. [5] Costa Rican 0-14 1981-1996 43.1
El Salvador Mejía-Aranguré et al. [6] Salvadoran 0-11 1996-2000 34.2
Brazil (Sao Paulo) de Camargo B et al. [28] Brazilian 0-19 1998-2002 47.5
a
SAAIR: standardized average annual incidence rates;
b
SEER: Surveillance, Epidemiology and End Results Program in United States of America (nine areas:
Atlanta, Detroit, San Francisco, Seattle, Connecticut, Hawaii, Iowa, New Mexico and Utah);
c
CDC (NPCR): Center for Disease Control, Division of Cancer Prevention
and Control, National Program of Cancer Registries in USA;
d
ACSSR: American Cancer Society, Surveillance Research (13 SEER cancer registry areas: Atlanta,
Detroit, Los Angeles, San Francisco, San Jose Monterey, Seattle, Alaska Native Tumor Registry, Connecticut, Georgia, Hawaii, Iowa, New Mexico, and Utah);
e
TCR:
Texas Cancer Registry, Texas Department of State Health Services, Cancer Epidemiology and Surveillance Branch.
Pérez-Saldivar et al.BMC Cancer 2011, 11:355
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Salvador [6], Argentina [27], and Brazil [28] and accord-
ing to the International Report of Cancer in Children,
populations in other regions of Latin America do not
have higher incidences of lymphoid leukemia than do
populations of Caucasian origin [21].
The high incidence in some Hispanic groups may have
resulted from an artifact in the data, or have been due
to environmental or genetic factors. In previous reports,
there may have been an artifact in the IMSS data, which
resulted in an overestimation of the incidence. The fol-
lowing scenario might explain such a situation: unem-
ployed parents, on learning that their child had
leukemia, would seek employment that would provide
access to medical benefits from IMSS. The child would
then be included in the numerator, without being repre-
sented in the denominator, thereby leading to an overes-
timation of the incidence. (A similar situation could be
envisioned for the Hispanic population in the USA,
many of which are undocumented workers. Illegal aliens
may be forced out of hiding to seek medical attention
for their child, thereby increasing the numerator). It
should be noted that the high incidence demonstrated
in the current study agrees with those found in prior
reports based on IMSS data, implying that the prior
reports were not biased, despite having come from only
one institution.
Another possible explanation of the higher incidence
among some groups of Hispanics is that exposure to
carcinogenic agents is greater among Hispanics in the
USA than it is for other ethnic groups [29], as a signifi-
cant portion of Hispanic immigrants in the USA are
employed in high-risk occupations, such as agriculture
in which pesticides are used. This is especially true for
Florida, California, and Texas [29], the states in which
higher incidences of ALL among Hispanic children have
been reported [22-25]. We have previously reported
that, in Mexico City, both exposure to carcinogenic
agents in the workplace and agriculture-related occupa-
tions were risk factors for AL in children [30]. However,
in this study, for the boroughs of Mexico City, no corre-
lation was found between agricultural hectares and the
incidence of ALL. Another possibility is that genetic fac-
tors could explain why Costa Ricans, Mexicans, and His-
panics in the USA have the highest incidences of ALL
[23]. In contrast, the SAAIR of AML for the study
population was 6.8 per million, a value similar to data
from Canada, the USA, and the UK (SAAIRs of 6.3, 6.0,
6.3 per million, respectively) [21].
Incidence of leukemia by age group
First, it should be noted that, when the age groups for ALL
are compared across various groups, the incidence for chil-
dren 1-4 years of age were consistently greater than those
for 10-14 year olds: for the majority of Mexican states, two-
fold greater (a finding in agreement with the IMSS data);
for the state of Nuevo León, three-fold; and for developed
countries, more than three-fold, even though the rate of
ALL is not so high [7]. In the current study, the incidence
for 1-4 year olds was 2.6-fold that for the 10-14 year olds.
This relation has been associated with socio-economic level
and with the possibility that a hypothetical infectious agent
may be involved [13]. It is interesting that the frequency of
ALL for Nuevo León, a Mexican state that borders the USA,
is similar to that for the Caucasian population of the USA
[7], the fact that Nuevo León has the highest MHDI of Mex-
ico, suggests the possibility that, among Hispanic children
who enjoy a higher quality of life, the incidence of ALL
tends to follow that of developed countries. Further studies
are required to validate this hypothesis.
Immunophenotypes
In this work, the frequency of immunophenotyping was
96.4%, a value higher than those in other published data
from Mexico [8] but similar to those in reports from
developed countries [31]. The frequency of precursor B-
cell ALL was similar to those in other reports from
Mexico [8,32,33]; the frequency of T-cell ALL was lower
than that (23.6%) in a previous report from IMSS [30],
but similar to those in the latest reports from the Insti-
tuto Nacional de Pediatría [32,33].
Ratio of high risk to standard risk for ALL
The higher incidence of ALL among children over ten
years of age is important because all children of this age
are generally considered at high risk for relapse [31,34].
In Mexico City, the ratio of high-risk children to stan-
dard-risk children is 1:1, a value in sharp contrast with
those for populations attended in hospitals outside Mex-
ico, e.g., St. Jude Children’s Research Hospital (Mem-
phis, Tennessee, USA) where the ratio is 1:3. Thus, only
25% of the children at Saint Jude [35] are at high risk,
compared to 50% in Mexico City [36].
The importance of a high incidence of ALL at an early
age is that it is a predictor of a higher frequency of a
genetic rearrangement that has a good prognosis for
ALL patients [37]. In Mexico, genetic rearrangements
(such as ETV6/RUNX1) that have a good prognosis
have been found at a frequency below those of devel-
oped countries [38], whereas genetic rearrangements
with a bad prognosis have been reported at a higher fre-
quency [38]. Of note is the high frequency found for
MLL/AF4 in Mexico City, because this rearrangement,
which has a very bad prognosis, has been related with
different intrauterine exposures [39].
AML
For Hispanic populations, AML M3 has been proposed
as the predominate subtype [7,40]. This idea was not
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corroborated in the present work: AML M3, with a fre-
quency of only 10.7%, was not the predominant subtype
in the population studied.
Peak ages for leukemias
In a previous study in Mexico City, peaks of incidence
of ALL were at 2-3 and at 6-8 years of age [8]; here, as
showninFigure1,twopeakswerefound,butat1-6
years of age and at 9-10 years of age. In other Hispanic
populations in which the incidence of ALL is high [41],
a similar situation seems to exist, that of there being
two age peaks, one early, one late. A small peak for T-
cell ALL occurred at 1-4 years, similar to that published
by the IMSS from Mexico [8].
Incidence of leukemias by borough and correlation with
MDHI, number of cultivated hectares, and average
number of persons per household
In this study, there was a strong correlation between the
incidence of precursor B-cell immunophenotype and the
average number of people per household in the bor-
oughs of the city. This finding supports the infectious
agent hypothesis, because a child living a crowded
household would have a higher risk of being in contact
with infectious agents [13]. In our report, the incidence
of AML was not correlated with the agriculture hec-
tares, average number of people per household, or
MHDI. The incidence in Mexico City is similar to that
of other cities in the region [21].
Conclusions
We conclude that the frequency of AL, especially of
ALL, in Mexico City is among the highest in the world,
similar to those of Hispanic children populations in the
USA or Costa Rica [1,3,5]. Our result showed that this
high frequency in Mexico City was not due to any bias
that could have existed in prior reports that were based
on data from only one institution. The early peak of
precursor B-cell ALL occurred at the same ages as those
found for developed countries; however, a second peak,
at nine years of age and older, was found for children in
Mexico City. The frequency of T-cell ALL was similar
to those in developed countries; however, here, a peak
at an early age was found. It is possible that an infec-
tious agent could be related with the high incidence of
ALL in Mexican children. We hypothesize that a lower
socio-economic level and infectious agents could be
related with the higher incidence of ALL among Hispa-
nic populations.
We think that the establishment of population-based
registries in other jurisdictions of Mexico would help
tracktheincidenceofthesedisease–information that
may be useful in determining possible causal agents in
the environment or other factors that play a role. Such
information is also useful to decision-makers in plan-
ning for the future needs of the health-care system.
Additional material
Additional file 1: Table S1. Childhood population in boroughs of
Mexico City by age group, according to the intermediate census of 2005.
Population by each borough and by age group.
Acknowledgements and funding
This work was partially funded by the Instituto Mexicano del Seguro Social
through its program, Apoyo Financiero para el Desarrollo de Protocolos de
Investigación en Salud en el IMSS (2005/1/I/078; FIS/IMSS/PROT/C2007/056;
FIS/IMSS/PROT/G10/846); by the Consejo Nacional de la Ciencia y la
Tecnología (CONACYT) through its program, Fondo Sectorial de Investigación
en Salud y Seguridad Social (SALUD 2007-1-71223/FIS/IMSS/PROT/592); and
by the Fondo Sectorial de Investigación para la Educación (CB-2007-1-83949/
FIS/IMSS/PROT/616). We thank Veronica Yakoleff for translating and editing
the manuscript and for helpful comments. We thank the Coordinación de
Investigación en Salud of the IMSS for covering the cost of the translation
and publication.
Author details
1
Unidad de Investigación en Epidemiología Clínica, Unidad Médica de Alta
Especialidad UMAE Hospital de Pediatría, Centro Médico Nacional (CMN)
Siglo XXI, Instituto Mexicano de Seguridad Social (IMSS), México D.F., México.
2
Servicio de Hematología, UMAE Hospital de Pediatría, CMN “Siglo XXI”,
IMSS, México D.F., México.
3
Servicio de Oncología Pediátrica, Instituto
Nacional de Pediatría (INP), Secretaría de Salud (SSa), México D.F., México.
4
Servicio de Onco-Hematología, Hospital Infantil de México Federico Gómez,
SSa, México D.F., México.
5
Servicio de Hematología Pediátrica, Hospital
General “Gaudencio González Garza”, CMN “La Raza”, IMSS, México D.F.,
México.
6
Servicio de Hematología Pediátrica, CMN “20 de Noviembre”,
Instituto de Seguridad Social al Servicio de los Trabajadores del Estado,
México D.F., México.
7
Hospital General Regional “Carlos McGregor Sánchez
Navarro”, IMSS, México D.F., México.
8
Servicio de Onco-Pediatría, Hospital
Juárez de México, SSa, México D.F., México.
9
Servicio de Oncología, Hospital
Pediátrico de Moctezuma, Secretaría de Salud del D.F., México D.F., México.
10
Hospital General de México, SSa, México D.F., México.
11
Subdirección de
Hemato/Oncología, INP, SSa, México D.F., México.
12
Servicio de Hematología
Pediátrica, INP, SSa, México D.F., México.
13
Unidad de Investigación Médica
en Inmunología e Infectología, Hospital de Infectología Daniel Méndez
Hernández, “La Raza”IMSS, México D.F., México.
14
Coordinación de Salud en
el Trabajo, CMN Siglo XXI, IMSS, México D.F., México.
Authors’contributions
JMMA and MLPS conceived and designed the study, analyzed the data, and
wrote the first draft of manuscript. AFG and RBR designed the study,
analyzed the data, and provided guidance to all aspects of this project. JFL,
DADR, RAS, MCRZ, RPA, AMA, RRL, LEH, MAdCM, EJH, AMS, EMDA, VBM,
JGPG, MMVA, FJAR, JRTN, JDFCH, RCC, PHAG, VCBM, MCOA, and MAI
registered, encoded, and analyzed the data. All authors read and approved
the final manuscript.
Competing interests
The authors declare that they have no competing interests.
Received: 17 March 2011 Accepted: 17 August 2011
Published: 17 August 2011
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Pérez-Saldivar et al.BMC Cancer 2011, 11:355
http://www.biomedcentral.com/1471-2407/11/355
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