Download BOLETíN MÉDICO del HOSPITAL INFANTIL de MÉXICO

Boletín Médico del
ISSN-1665-1146
Boletín Médico del
Hospital Infantil de México
PUBLICACIÓN BIMESTRAL
Vol. 69 Noviembre-Diciembre, 2012 No. 6
CONTENTS
In memóriam Gustavo Gordillo Paniagua
Felipe Mota Hernández, Luis Velásquez Jones
EDITORIAL
513
Food insecurity and abdominal obesity in adolescents
Samuel Flores Huerta
REVIEW ARTICLE
516
Current role of—and new evidence for—continuous positive airway pressure in respiratory distress syndrome
Lorenzo Osorno-Covarrubias
RESEARCH ARTICLES
524
534
541
553
Obesity, eating behavior, and food insecurity among adolescents in Mexico City
Luis Ortiz-Hernández, Magdalena Rodríguez-Magallanes, Hugo Melgar-Quiñónez
Niches of opportunity for improving health care of children covered by “Medical Insurance for a New
Generation”
Luis Jasso-Gutiérrez, Luis Durán-Arenas, Samuel Flores-Huerta, Gabriel Cortés-Gallo, Onofre Muñoz-Hernández
Global neurodevelopmental screening tests for children <5 years of age in the United States and Latin
America: a systematic review and comparative analysis
Beatriz Romo-Pardo, Silvia Liendo-Vallejos, Guillermo Vargas-López, Antonio Rizzoli-Córdoba, Guillermo Buenrostro-Márquez
Risk factors and consequences of cyberbullying in teenagers: association with bullying
Gerardo García-Maldonado, Gerardo Jesús Martínez-Salazar, Atenógenes Saldívar-González, Rafael Sánchez-Nuncio, Gerardo
Manuel Martínez-Perales, María del Carmen Barrientos-Gómez
CLINICAL CASES
564
570
Acrodermatitis enteropathica
Marco A. Toxtle-Román, Ana Elena Hernández-Arroyo
Erratic migration of Ascaris lumbricoides to the scrotum
Rubén Martín Álvarez-Solís, Marcela Vargas-Vallejo, Griselda Orozco-Barrientos, Armando Quero-Hernández, Gabriel GarcíaHernández, David Bulnes-Mendizábal
CLINICOPATHOLOGICAL CASE
575
Acute respiratory failure secondary to Bordetella pertussis infection in a 4-month-old infant
Sarbelio Moreno Espinosa, Bárbara Inés Morales Mérida, Carlos Alberto Serrano Bello, Orlando Domínguez Pacheco, Olga
Camaño Andrade, Rubí Rojas Padilla, Ernesto Calderón Jaimes
PEDIATRIC THEME
589
Renal tubular acidosis
Luis Velázquez Jones
VITAL STATISTICS
595
Mortality due to exposure to smoke, fire and flames in children under 15 years of age during the period 19982010
Sonia B. Fernández-Cantón, Ana Ma. Hernández-Martínez, Ricardo Viguri Uribe
Boletín Médico del Hospital Infantil de México
Indexado en/Indexed in
Scopus, Elsevier
Embase/Excerpta Medica
Current Awareness in Biological Sciences (CABS)
Index Medicus Latinoamericano (IMLA)
Literatura Latinoamericana en Ciencias de la Salud (LILACS)
Scientific Electronic Library Online (SciELO)
Biblioteca Virtual en Salud (BVS)Periódica-Índice de Revistas Latinoamericanas en Ciencias, UNAM
Latindex
EBSCO/MedicLatina
Artemisa
Versión completa (español e inglés):
www.himfg.edu.mx
www.nietoeditores.com.mx
La revista Boletín Médico del Hospital Infantil de México es una publicación del Hospital Infantil de México Federico Gómez. Revista bimestral.
Editor responsable Gonzalo Gutiérrez. Reserva de Título de la Dirección General del derecho de Autor (SEP): 04-1985-000000000361-102.
Certificado de Licitud de Título 11924 y Certificado de Licitud de Contenido de la Comisión Calificadora de Publicaciones y Revistas Periódicas (SeGob) 8328. Publicación realizada por Edición y Farmacia SA de CV. José Martí 55, colonia Escandón, 11800 Ciudad de México.
El contenido de los artículos firmados es responsabilidad de sus autores. Todos los Derechos Reservados.
Boletín Médico del
Hospital Infantil de México
La revista pediátrica con mayor difusión en México
Más de 65 años de publicación ininterrumpida. Seis números al año con más de
70 artículos de investigadores nacionales y extranjeros con los temas
más actuales en Pediatría.
Suscripciones 2012
En México: $500 pesos
En el extranjero: $60 USD
Departamento de Ediciones Médicas
Edificio Mundet, tercer piso
Dr. Márquez 162, Col. Doctores
06720 Cuauhtémoc, Ciudad de México
Formas de pago
Condiciones
Efectivo
Directo en la caja del
Hospital Infantil de México Federico Gómez
Trámite en el
Departamento de Ediciones Médicas
Edificio Mundet, tercer piso
Dr. Márquez 162, Col. Doctores
06720 Cuauhtémoc, Ciudad de México
Horario: Lun a Vie de 8 am a 3 pm
Se entregará o se remitirá nota de venta a todos
nuestros suscriptores. Los ejemplares se entregarán directamente o se enviarán vía postal; en el
segundo caso se requerirán los siguientes datos:
nombre y domicilio completos, teléfono
y correo electrónico.
Depósito bancario
Cuenta Banorte: 0102801543
Enviar copia de depósito por fax:
(55) 57 61 89 28
Tel./Fax: (55) 57 61 89 28
Email: [email protected]
Transferencia bancaria
Banorte
CLABE interbancaria: 072180001028015432
“Fondo de Ediciones Médicas”
Cheque
Remitir vía postal a:
Hospital Infantil de México Federico Gómez
Dudas, aclaraciones, informes
o sugerencias
Boletín Médico del
Hospital Infantil de México
Federico Gómez Santos †
Fundador
José Alberto García Aranda
Director General
Onofre Muñoz Hernández
Director Asociado
Gonzalo Gutiérrez
Editor
María G. Campos Lara
Editora Ejecutiva
Ricardo Viguri Uribe
Editor Asociado y Administrativo
Sharon Morey
Editora Asociada
Julia Segura Uribe
Editora Adjunta
COMITÉ EDITORIAL
BIOMÉDICO
Jesús Kumate Rodríguez1
Pedro Valencia Mayoral2
SALUD PÚBLICA
Sonia Fernández Cantón5
Hortensia Reyes Morales4
TEMAS PEDIÁTRICOS
Luis Jasso Gutiérrez2
Luis Velásquez Jones2
EDUCACIÓN EN SALUD Y ÉTICA CLÍNICA
Jaime Nieto Zermeño2
Juan José Luis Sienra Monge2
CLÍNICO
Blanca Estela del Río Navarro2
Fortino Solórzano Santos3
EPIDEMIOLOGÍA CLÍNICA
Juan Garduño Espinosa2
Miguel Ángel Villasis3
CASOS CLÍNICOS
Salvador Villalpando Carrión2
CASOS CLÍNICO PATOLÓGICOS
Stanislaw Sadowinski Pine2
1
Fundación IMSS
Hospital Infantil de México Federico Gómez
3
Hospital de Pediatría, Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social
4
Instituto Nacional de Salud Pública, Secretaría de Salud
5
Dirección de Información Epidemiológica, Dirección General de Epidemiología, Secretaría de Salud
2
Boletín Médico del
Hospital Infantil de México
CONSEJO EDITORIAL
José Luis Arredondo GarcíaInstituto Nacional de PediatríaMéxico D.F., México
Manuel Baeza BacabCentro Médico de las AméricasMérida, Yucatán, México
Eduardo Bancaleri
Holtz Children´s HospitalMiami, Florida, EUA
Alessandra Carnevale CantoniInstituto Nacional de Medicina GenómicaMéxico D.F., México
Aldo CastañedaUnidad de Cirugía Cardiovascular de Guatemala
Guatemala, Guatemala
Leticia CastilloChildren´s Medical Center, Dallas, Texas, EUA
University of Texas Southwestern
Francisco CigarroaUniversity Hospital
San Antonio, Texas, EUA
Alejandro Cravioto QuintanaOrespes S.A. de C.V.México D.F., México
Blanca Estela Del Río Navarro
Hospital Infantil de México Federico GómezMéxico D.F., México
Alfonso Delgado Rubio
Hospital Universitario Madrid SanchinarroMadrid, España
Arturo Fajardo GutiérrezCentro Médico Nacional S. XXI, IMSSMéxico D.F., México
Samuel Flores Huerta
Hospital Infantil de México Federico GómezMéxico D.F., México
Carlos Franco ParedesEmory University HospitalAtlanta, Georgia, EUA
Sara Huerta Yepez
Hospital Infantil de México Federico GómezMéxico D.F., México
Fima LifshitzCottage Children´s Hospital
Sta. Barbara, California, EUA
Gabriel ManjarrezCentro Médico Nacional S. XXI, IMSSMéxico D.F., México
Homero Martínez Salgado
Hospital Infantil de México Federico GómezMéxico D.F., México
Mara Medeiros
Hospital Infantil de México Federico GómezMéxico D.F., México
Juan Pablo Méndez BlancoInstituto Nacional de Ciencias Médicas y NutriciónMéxico D.F., México
Salvador Zubirán
Guadalupe Miranda NovalesCentro Médico Nacional S. XXI, IMSSMéxico D.F., México
Verónica Morán Barroso
Hospital Infantil de México Federico GómezMéxico D.F., México
Ángel Nogales Espert
Hospital Universitario Reina SofíaCórdoba, España
Samuel NurkoChildren’s Hospital BostonBoston, Massachusetts, EUA
Miguel O’ryanUniversidad de Chile Santiago de Chile, Chile
Alberto PeñaCincinnati Children´s HospitalCincinnati, Ohio, EUA
Francisco J. Puga MuñuzuriMayo ClinicRochester, Minnesota, EUA
Guillermo Ramón
Hospital Infantil de México Federico GómezMéxico D.F., México
Vesta Richardson López ColladaCentro Nacional de Salud para la Infancia yMéxico D.F., México
la Adolescencia
Fabio Salamanca GómezCentro Médico Nacional S. XXI, IMSSMéxico D.F., México
Eduardo Salazar LindoDS-CONSULT S.A.C.Lima, Perú
Norberto Sotelo CruzEscuela de Medicina, Universidad de Sonora
Hermosillo, Sonora, México
Alejandro Sweet Cordero
Stanford University School of Medicine
Stanford, California, EUA
Gustavo Varela Fascinetto
Hospital Infantil de México Federico GómezMéxico D.F., México
Arturo Vargas Origel
Facultad de Medicina, Universidad de GuanajuatoLeón, Guanajuato, México
Edgar Vásquez GaribayInstituto de Nutrición Humana
Guadalajara, Jalisco, México
Federico Raúl VelázquezCentro Médico Nacional S. XXI, IMSSMéxico D.F., México
Alberto Villaseñor SierraCentro de Investigaciones Biomédicas de Occidente
Guadalajara, Jalisco, México
In memóriam
Dr. Gustavo Gordillo Paniagua (1923-2012)
(Died on September 12, 2012)
P
rofessor Gustavo Gordillo was born in Comitán,
Chiapas on May 20, 1923. He completed his professional studies at the Military Medical School
(1941-1946), postgraduate studies at the Hospital Infantil
de México (HIM) (1948-1950) and the Division of Metabolism of the Children’s Medical Center in Boston, MA
(1952-1954).
Upon completion of graduate school he was named
“Full-time Investigator” of the Department of Hematology
and Nephrology at Children’s Hospital
of Mexico by Dr. Rafael Soto Allende.
In 1961 he founded and was the first
director of the Research Department of
Nephrology, newly created in the same
hospital institution. Professor Gordillo
was a pioneer in both national and international professional circles. He continued
in that position, carrying out prolific
activities both in research and teaching
until his retirement in 1990. In 1990 he
was commissioned by La Salle University
to create and direct the Graduate Division
of the Medical School (1990-2000) and
remained a member of the Academic
Council of the Faculty of Medicine until 2005.
The first line of research developed by Professor Gordillo in the Hospital Infantil de México Federico Gómez
(HIMFG) was in relation to electrolyte disturbances in
the malnourished child with acute diarrhea. This area of
research led to the decline of the lethality of this condition,
which was mainly due to inadequate correction of these
changes and are simply part of the same characteristics of
chronic malnutrition. Along this line of research, studies
in severely malnourished children allowed the definition
of a new problem: severe kaliopenic nephropathy due to
severe potassium deficiency.
Another line of research was the histopathological
study of childhood kidney diseases using percutaneous
renal biopsy, a procedure introduced in the Department
of Nephrology at the HIMFG in 1967. With this resource
it was possible to contribute to the prognosis of glomerulonephritis and to some tubulointerstitial nephropathies
by performing renal immunohistopathological studies
at disease onset and to establish clinicopathological
correlations in children with nephritic syndrome, acute
nephritic syndrome and nephropathies
due to analgesics, among others. These
patients were able to be maintained under surveillance on an outpatient basis
for several years.
These pioneering studies at the international level led to the invitation of the
Nephrology Department of HIMFG to
participate in the International Study of
Kidney Disease in Children. Professor
Gordillo had an impressive and outstanding role in this study.
The development of the Department
of Nephrology in its first 20 years culminated in the publication of five books:
• Pediatric Nephrology
• Epidemiology and Prevention of Renal Disease
• Acute Dehydration in Children
• Diagnostic and Therapeutic Procedures in Kidney
Diseases of Children
• Electrolytes in Pediatrics: Physiology and Clinical
These publications marked a milestone in the knowledge of nephrology during his career and had a great impact
on the pediatric community and pediatric nephrology in
Mexico and Latin America. These publications were the
product of more than 150 investigations conducted and
published by Professor Gordillo and colleagues: 17 publi-
cations in international journals, 126 in national journals,
nine collaborations in international books and 15 national
book collaborations. Likewise, during this time, the first
kidney transplant in children in Mexico was done.
In addition to founding the first pediatric nephrology
service worldwide and certainly with this endorsement,
Professor Gordillo was able to organize and “chair” the
First International Symposium of Pediatric Nephrology in
Guadalajara, Jalisco in December 1968, which launched
the presence of Mexico into the international arena. The
foundation of the International Pediatric Nephrology
Association and the Latin American Association of Pediatric Nephrology were derived from these activities, and
Professor Gordillo was president of these associations. He
was also president and founder of the Mexican Society of
Nephrology, the Mexican Institute of Nephrology Research
and an honorary member of 40 research partnerships, both
national and international.
To commemorate his 30 years of professional activities,
Professor Gordillo was honored with the publication of a
book “Select Topics in Nephrology” written by several of
the “academic heavyweights” of the international arena
of pediatric nephrology 36 years ago. It was a universal
tribute to his work, which is still valid, in which 60 distinguished pediatric nephrologists of various countries of
the American continent and Europe participated. Professor
Gordillo received other major awards, among which are
the following:
• Member of the National Academy of Medicine of
Mexico
• “Federico Gomez” Award from the Physicians Association of HIM
• Medical Excellence Award granted by the Ministry
of Health of Mexico
•
“Golden Kidney” medal of the European Society of
Pediatric Nephrology
• “Ira Greifer” Recognition Award (the highest award
of the International Pediatric Nephrology, New
York, July 2010)
We are convinced that the most important and permanent recognition that Professor Gustavo Gordillo has
received (and will receive) is that which is given with admiration and respect from his students and from pediatric
nephrologists trained under his tutelage from all areas of
the country and from many countries of Latin America and
the Caribbean. Many of his students were, in turn, pioneers
in their countries of origin in the creation and development
of pediatric nephrology services. These professionals keep
alive and in force his thought and his tireless struggle in
the development of pediatric nephrology for the benefit
of thousands of children who in the Americas suffer from
illnesses that affect renal structure and function and, above
all, his willingness to always be present to teach, educate
and guide along the correct pathways by his example. His
decisive influence paved the way of life for his students.
Our highest tribute to his memory will be to keep the
tradition of a high level of medical care alive in the field
of kidney disease, and to conduct an ongoing search for
answers to many questions already posed and those that
continue to be posed in pediatric nephrology.
Dr. Felipe Mota Hernández
Ex-Jefe, Departamento de Nefrología y Decano
Hospital Dr. Luis Velásquez Jones
Jefe del Departamento de Nefrología
Hospital Infantil de México Federico Gómez
Mexico, D.F., Mexico
E-mail:
Bol Med Hosp Infant Mex 2012;69(6):513-515
Editorial
Food insecurity and abdominal obesity in adolescents
Samuel Flores Huerta
W
ith regard to the worldwide overweight and
obesity epidemic and given the serious consequences on the health of the population due to
the strong relationship with metabolic and cardiovascular
diseases, there is interest in understanding the mechanisms
conducive to obesity as well as the mechanisms that triggers its consequences. Genetic and environmental factors
deserve the most attention. With respect to genetic factors,
>400 genes associated with this problem have been described in both adults and children.1 In certain populations,
some of these factors partially explain this problem, but
not necessarily in other populations. However, the genetic
factor has remained stable since the advent of mankind
and does not explain the emergence of the problem of
overweight and obesity dating back to the last three or
four decades.
Regarding environmental factors, the focus is on changing lifestyles that are increasing becoming "civilized
ways of living." Technological changes and economic
interests have left behind thousands of years in which a
large investment in energy was required for both obtaining
Departamento de Investigación en Salud Comunitaria, Hospital
Infantil de México Federico Gómez, México, D.F., México
Correspondence:
Dr. Samuel Flores Huerta
Departamento de Investigación en Salud Comunitaria
Hospital Infantil de México Federico Gómez
México, D.F., México
E-mail: [email protected]
Received for publication: 11-5-12
Accepted for publication: 11-5-12
Vol. 69, November-December 2012
food and for the occupational way of life. Specifically, the
availability of food followed the seasonal cycles, balancing the periods of abundance and scarcity. Not long ago,
more natural and fresh foods were consumed than those
currently commercialized. However, in recent decades
there has been a reversal in the ratio of its consumption.2 To
consume a higher proportion of processed foods equals the
consumption of foods that are densely energetic, high in
sodium and high in saturated fat. Meanwhile, high-caloric
commercial beverages that use fructose as a sweetener
have displaced plain water.3 This means that humans consume nutrients that cannot be metabolized appropriately.4
Commercialized foods and drinks have been made available to all populations even in remote areas, competing in
price with natural healthy foods. The imbalance between
consumption/energy expenditure has been associated with
the occurrence of changes in nutritional status and health
that start with obesity. Recently, as part of the complexity
of the overweight and obesity problem, the paradox has
emerged that involves not only the abundance of food as
a factor for developing obesity but also its shortage. This
issue is addressed by Ortiz Hernandez et al. in this issue
of Boletín Médico del Hospital Infantil de México. This
article explores the role of food insecurity as a factor in
the development of obesity and particularly abdominal
obesity in adolescents in Mexico City schools.5 Whatever
the limitations of the study—whether related to the set of
instruments used to gather information about the presence
of food insecurity, not having questioned in homes those
persons connected with the processes for food access, failing to investigate food consumption on weekends, using
skin folds to establish a criterion of obesity6—the issue is
513
Samuel Flores Huerta
relevant for the growing number of persons living in food
poverty, a situation not exclusive to rural areas.
Food insecurity is an indicator with which the Food and
Agriculture Organization (FAO) systematically monitors
world hunger, for which it continually updates its instruments. To date, the main interest of the FAO is to monitor
chronic hunger (acute or cyclical) to avoid or reduce forms
of malnutrition related to lack of or food insufficiency.7,8
The agency assumes that under conditions of food safety,
proper food availability should be available to 100% of
the members of a family or community. However, in virtually all populations, there are periods when nutritionally
appropriate foods may not be available, initiating the first
link in the chain of food insecurity. If, due to the lack or
insufficiency of food for socioeconomic reasons, one adds
the fact of not having access to purchase food, the gap further widens. In order to compensate for food shortages that
are not culturally accepted, acceptability and consumption
are further limited. Additionally, the availability of foods
and access to their consumption are not a guarantee of
good nutritional status because food bioavailability is
affected by many other factors. Thus, it is advisable to
determine the concepts of security/food insecurity and
food poverty. Food security is when all people have, at all
times, physical and economic access to satisfy their need
for food and their preferences with regard to food in order
to have an active and healthy life. On the other hand, food
insecurity is when there is a limited or uncertain capability
of acquiring nutritionally appropriately and adequate foods
in a socially acceptable manner.7,8
The National Council for Evaluation of the Policy of
Social Development in Mexico (CONEVAL) establishes
that food poverty is the inability to obtain a basic food
basket, even when use is made of all available family
economic resources for its purchase.9 In this publication,
CONEVAL shows the co-existence in the same home of
problems of malnutrition, overweight and obesity, but
not stipulated as proposed by Ortíz-Hernández et al., that
food insecurity also plays a role in the development of the
problem of overweight and obesity. It has recently been
reported that in a North American population of children
of Mexican descent who live on the U.S. border with
Mexico and are subjected to conditions of very low food
security, foods more densely energetic are consumed than
by children who do not find themselves in the same condition, being positively associated with a greater prevalence
514
of obesity.10 Food insecurity and its association with the
consumption of unhealthy foods that carry a cardiovascular
risk have also been mentioned in reviews about this topic.11
When one lives with food insecurity, the first alteration
observed is the change in eating habits. When there are
food shortages, households with limited economic resources increase their reliance on processed foods, which are
less expensive than fresh natural foods but at the same time
are more energy dense. Moreover, chronic dissatisfaction
or prolonged fasting predisposes to food gorging when it
is available, a phenomenon different from what was proposed by Ortiz-Hernandez et al. According to the definition
proposed by Hernandez et al., eating without inhibition
is associated with eating without being hungry, caused by
emotional factors or stress.5 In adults, it was found that
skipping breakfast is associated with obesity. 11 Recent
studies found that the proportion of school children, in a
manner similar to their parents, who do not eat breakfast
reached 23.5% (20% in eutrophic children vs. 26% in
obese children).12 When the child has access to food, he/
she does so greedily. The metabolic response between a
child who ate breakfast and another child who did not
is different, although both consume the same amount of
energy. Abdominal fat is higher in those who regularly skip
breakfast vs. those who have breakfast.13 Eating breakfast,
therefore, appears to be a healthy habit for school-age
children, whether they do so at home or as part of school
programs to address food insecurity. These programs have
shown that children, who participate in breakfast, increase
their school performance and reduce malnutrition without
evidence of increasing obesity. Conversely, breakfast
would be a way to reduce this problem.14
Moreover, faced with the problem of obesity (particularly of abdominal obesity), it is relevant that the
formation of healthy habits such as eating breakfast daily
is promoted by both the home and the schools. On the
other hand, we must pay attention to the work of OrtizHernandez et al., whose results suggest the possibility
that food insecurity participates in increasing this health
problem in children.5,15
REFERENCES
1.
Snyder EE, Walts B, Pérusse L, Chagnon YC, Weisnagel SJ,
Rankinen T, Bouchard C. The human obesity gene map: the
2003 update. Obesity Res 2004;12:369-439.
Bol Med Hosp Infant Mex
Food insecurity and abdominal obesity in adolescents
2.
3.
4.
5.
6.
7.
8.
9.
Rivera JA, Barquera S, Campirano F, Campos I, Safdie M,
Tovar V. Epidemiological and nutritional transition in Mexico:
rapid increase of non-communicable chronic diseases and
obesity. Public Health Nutr 2002;5(1A):113-122.
Barquera S, Campirano F, Bonvecchio A, Hernández-Barrera
L, Rivera JA, Popkin BM: Caloric beverage consumption patterns in Mexican children. Nutrition J 2010;9:47.
Bremer AA, Mietus-Snyder M, Lustig RH. Toward a unifying
hypothesis of metabolic syndrome. Pediatrics 2012;129:557570.
Ortiz-Hernández L, Magallanes MR, Melgar-Quiñónez H.
Obesidad, conducta alimentaria e inseguridad alimentaria en
adolescentes de la ciudad de México. Bol Med Hosp Infant
Mex 2012 (include pages on final proofs)
WHO Expert Committee (Ed.). Physical status: the use and
interpretation of anthropometry. Geneva; 1995.
FAO. El estado de la inseguridad alimentaria en el mundo.
Rome: FAO; 2012.
FAO and UN. Handbook for defining and setting up a food
security information and early warning systema (FSIEWS).
Rome: FAO; 2000.
Consejo Nacional de Evaluación de la Política de Desarrollo
Social: Dimensiones de la seguridad alimentaria: evaluación
estratégica de nutrición y abasto. México: CONEVAL; 2010.
Vol. 69, November-December 2012
10. Sharkey JR, Nalty C, Johnson CM, Dean WR: Children's very
low food security is associated with increased dietary intakes
in energy, fat, and added sugar among Mexican-origin children
(6-11 y) in Texas border colonias. BMC Pediatr 2012, 12:16.
11. Ma Y, Bertone ER, Stanek EJ III, Reed GW, Hebert JR, Cohen
NL, et al. Association between eating patterns and obesity in a
free-living US adult population. Am J Epidemiol 2003;158:385392.
12. Vilchis-Gil J, Galván-Portillo M, Klünder-Klünder M, Cruz M,
Flores-Huerta S. Healthy eating, increased exercise and less
sedentary are protective factors against obesity in school age
children, despite high caloric intake. 2012 (in press).
13. Alexander KE, Ventura EE, Spruijt-Metz D, Weigensberg MJ,
Goran MI, Davis JN: Association of breakfast skipping with
visceral fat and insulin indices in overweight Latino Youth.
Obesity 2009;17:1528-1533
14. Ramírez-López E, Grijalva-Haro MI, Valencia ME, Ponce JA,
Artalejo E: Impacto de un programa de desayunos escolares en
la prevalencia de obesidad y factores de riesgo cardiovascular
en niños sonorenses. Salud Publica Mex 2005;47:126-133.
15. Ortíz-Hernández L, Acosta-Gutiérrez MN, Núñez-Pérez AE,
Peralta-Fonseca N, Ruiz-Gómez Y. En escolares de la ciudad
de México la inseguridad alimentaria se asoció positivamente
con el sobrepeso. Rev Invest Clín 2007;59:32-41.
515
Bol Med Hosp Infant Mex 2012;69(6):516-523
Review article
Current role of—and new evidence for—continuous positive airway
pressure in respiratory distress syndrome
Lorenzo Osorno Covarrubias
ABSTRACT
Mechanical ventilation and early or prophylactic surfactant has been the standard of care for many years in neonates with respiratory
distress syndrome (RDS). Evidence for this practice is supported in meta-analyses of well-controlled clinical trials. Observational studies
shown at the end of the 1980s in perinatal centers that used continuous positive airway pressure (CPAP) as the primary method of ventilatory support had a lower rate of bronchopulmonary dysplasia and used less ventilation for their neonates. Lack of more solid evidence has
been one of the reasons for which this method of care of RDS has remained restricted to a few perinatal centers worldwide.
Randomized multicenter clinical trials carried out during the last decade in very low birth weight neonates, which compare prophylactic or
early nasal CPAP vs. mechanical ventilation with prophylactic or selective surfactant with early or programmed extubation, were reviewed.
Recent clinical trials enable us to assert that early nasal CPAP is an alternative to intubation, and surfactant in the delivery room, decreases
the need for mechanical ventilation, use of surfactant and steroids for bronchopulmonary dysplasia. A low threshold for surfactant in neonates supported early with CPAP diminishes the need for mechanical ventilation.
Key words: continuous positive airway pressure, respiratory distress syndrome, surfactant.
INTRODUCTION
In this study we review the evidence of the efficacy and
safety of nasal continuous positive airway pressure (CPAP)
in infants with respiratory distress syndrome (RDS) from
initial clinical trials in the 1970s to the present. We reviewed all clinical trials written in English that appear
in PubMed, 1995 to date, with the following keywords:
continuous positive airway pressure, newborn infant, respiratory distress syndrome. We analyzed the reasons why
this method fell into disuse and the subsequent renewed
interest in this treatment.
In light of the studies published in the last decade, the
author attempts to answer several clinical dilemmas: What
Pediatra Neonatólogo, Hospital Star Médica Mérida, Mérida, Yucatán, México
Correspondence to:
Dr. Lorenzo Osorno Covarrubias
Pediatra Neonatólogo, Hospital Star Médica Mérida
Mérida, Yucatán, México
E-mail: [email protected]
Received for publication: 5-17-12
Accepted for publication: 10-5-12
516
to choose—initial nasal CPAP support or intubation and
surfactant? When to use surfactant in infants assisted early
with CPAP? When to start CPAP? Are there advantages to
early extubation vs. conventional post surfactant?
At the end of the text the information presented regarding the use of nasal CPAP in preterm infants with RDS
is summarized.
Evidence of the Efficacy and Safety of Nasal CPAP in
the 1970s
The application of continuous distending pressure in the
airway in neonates with RDS in the 1970s from the work
of Gregory et al.1 had a huge impact on neonatal morbidity
and mortality, with a 50% decrease in overall mortality
from RDS [relative risk, RR 0.52 (95% CI 0.32-0.87)]
and 76% in infants with birth weight >1500 g [RR 0.24
(95% CI 0.07-0.84)], with a 40% decrease in the need for
mechanical ventilation (MV).2 This effect is comparable
to that obtained 20 years later with the use of the alveolar
surfactant.
This simple therapeutic method has spread rapidly
worldwide. However, its use declined thereafter for several
reasons, among which are the availability of mechanical
ventilators specifically designed for infants, the high
Bol Med Hosp Infant Mex
Current role of—and new evidence for—continuous positive airway pressure in respiratory distress syndrome
rate of failure in infants <1500 g, and increased risk of
pneumothorax.2 Other factors that had a later influence
were 1) availability of exogenous surfactant and 2) staff
perceptions that infants on CPAP require more medical
and nursing care.
Impact of Exogenous Surfactant Therapy on Morbidity
and Mortality from RDS
Use of exogenous surfactant in the treatment of RDS
has been a breakthrough in the treatment of RDS. It
was quickly established as the standard of care. Seger
and Soll, in a meta-analysis, reported a 32% decrease in
neonatal morbidity and mortality, 53% decrease of air
leaks, 17% decrease in the risk of bronchopulmonary
dysplasia (BPD) or death at 28 days.3 The benefits are
greater for early (within 2 h) vs. late (RDS established)
application: lower mortality [RR 0.87 (0.77, 0.99)]; less
pneumothorax [RR 0.70 (0.59, 0.82)], and less BPD [RR
0.70 (0.55, 0.88)].4 Furthermore, in neonates <32 weeks
gestational age, prophylactic use (in the first 15-30 min)
has more benefits than rescue treatment (after 2 h), lower
mortality [RR 0.61 (0.48, 0.77)], less pneumothorax
[RR 0.62 (0.42, 0.89)], and less BPD or death [RR 0.85
(0.76, 0.95)].5
Reasons for CPAP Resurgence of CPAP from the Late
1980s to Date
In the late 1980s there was a resurgence of interest in CPAP
beginning with the work of Avery et al.6 who compared the
rate of BPD in eight perinatal centers in the U.S. The center
with the lowest rate of BPD was at Columbia University
Hospital in New York that used nasal CPAP (NCPAP) as
the primary method of care in preterm infants with RDS
and had a lower proportion of infants assisted with MV,
with a similar rate of mortality.
The beneficial effect of NCPAP in preventing BPD
has been supported by other observational studies. In
a multivariate logistic regression analysis it was found
that onset of MV (vs. NCPAP) explains the difference
between the prevalence of BPD in two hospitals (Babies
and Children’s Hospital in New York, 4% and Children’s
Hospital in Boston 22%).7
The association between MV and BPD and the protective role of CPAP in this disease has been fairly consistent
in several observational studies with historical controls,
before and after implementing the CPAP as the primary
Vol. 69, November-December 2012
method of ventilation.8-15 However, until now, there was a
lack of clinical trials to support those observations.
Role of MV in the Generation of BPD
Various experiments in preterm animals have demonstrated
an association of MV with BPD. Brief MV with high tidal
volume initiated pulmonary damage in preterm lambs.16
Preterm lambs assisted with CPAP had lower levels of
inflammatory markers compared with those that had been
subjected to MV.17 Preterm baboons managed early with
surfactant and CPAP compared with those who received
only surfactant and gentle MV at 28 postnatal days had
higher respiratory efficiency (greater a/A ratio of O2, less
ventilatory resistance, increased dynamic compliance,
normal volume pressure curve), favoring the formation
of pulmonary alveoli and preventing changes compatible
with BPD.18
Bohrer et al. demonstrated that even a short period of
MV induces elevation of proinflammatory cytokine levels
up to 10 times the baseline level in late preterm and term
neonates.19
The mechanisms of lung damage induced by MV include high pressure in the airway (barotrauma), excessive
lung volume (volutrauma), alveolar collapse and alveolar
re-expansion (atelectotrauma) and exaggerated inflammation (biotrauma).20
BPD Pathogenesis Is Complex and Multifactorial
Pulmonary inflammation plays a central role in the
complex multifactorial pathogenesis of BPD. The most
susceptible population is that representing low gestational
age, low birth weight, male gender, Caucasian, genetic
factors, intrauterine growth retardation, among others.
Also, pre- and postnatal factors such as chorioamnionitis,
oxygen toxicity, MV, patent ductus arteriosus and postnatal infections can induce and perpetuate a harmful and
complex inflammatory response in the airways, epithelium
and pulmonary endothelium of very immature neonates.21
The protective effect of CPAP may be obscured by the
multiplicity of involved factors.22
CPAP or MV and Surfactant: Clash of Cultures
For many years, use of CPAP as the primary method of
ventilatory support in infants with RDS has been restricted to a few perinatal centers in Scandinavia and to the
Columbia University Hospital in New York. The reasons
517
Lorenzo Osorno Covarrubias
are basically two: 1) lack of evidence of safety and efficacy of NCPAP in controlled clinical trials in extremely
preterm neonates, 2) difficulty in CPAP implementation
because of the characteristics of the system as well as to
the acceptance of the health care personnel.
This has led to an apparent dilemma—whether to intubate a neonate for prophylactic application of a surfactant
(but with increased risk of BPD due to being subjected to
MV) or temporarily assist the neonate with NCPAP and
early administration of rescue surfactant, with greater risk
of morbidity and mortality on deferring administration of
the surfactant.23
In Scandinavian countries, since the 1980s, a combination of strategies has been used: early NCPAP, surfactant,
brief MV, NCPAP postextubation NCPAP called INSURE
(intubation, surfactant, extubation) or ISX (intubation,
surfactant, extubation) that seems to have overcome the
dilemma.13,24,25
In the past decade, results of multicenter controlled
clinical trials have been published that allow us to answer
several questions regarding the efficacy and safety of
CPAP. These studies have added to the publications on
perinatal experiences of several centers in the implementation of CPAP.
Recent Evidence on Efficacy and Safety of CPAP in Mild
to Moderate RDS in Preterm Infants Weighing <1500 g
This new evidence from several multicenter clinical trials
answered several questions about the role of CPAP in the
management of RDS.
Initial CPAP support or intubation and surfactant?
The SUPPORT study group showed that early CPAP (in
the delivery room) + rescue surfactant (FiO2 >50%) is an
alternative to intubation and surfactant in the delivery room
in neonates of 24-27 weeks.26 There was no difference in
oxygen requirement or death at 36 weeks 47.8%. vs. 51.0%
[RR 0.95, 95% CI (0.85-1.05)]. Infants in the CPAP group
required fewer days of MV 24.8 vs 27.1 (p = 0.03), less
steroids for BPD 7.2% vs. 13.1% (p = 0.001) and less use
of surfactant 67.1% vs. 98.9% (p <0.001).
The results are similar to those obtained in the study
group COIN (Cpap Or INtubation) with the same initial
management scheme, although the following criteria
(surfactant application, mechanical ventilation, and extubation) were not controlled and were left to the judgment of
518
the participating institutions.27 There were no differences
observed between BPD or death at 36 weeks adjusted age:
CPAP 33.9% vs. intubation 38% [RR 0.80 (0.58-1.12)].
There was a lower risk of death or oxygen requirement
at 28 days in the CPAP group [RR 0.63 (0.16 to 0.88)],
less use of surfactant CPAP 38% vs. 77% (p <0.001), and
higher incidence of pneumothorax in the CPAP group 9%
vs. 3% (p = 0.001). It should be noted that in this protocol
a CPAP pressure of 8 cm H2O or greater was used.
Prophylactic application of surfactant vs. the selective
method has advantages in reducing morbidity and mortality as previously discussed.5 The recent review (March
2012) of the meta-analysis, in light of new published clinical trials, shows that infants in whom NCPAP was used
early there was no advantage in the use of prophylactic
surfactant in mortality [RR 1.24 (0.97, 1.58)], in BPD
or death [RR 1.12 (0.96, 1.31)]. In fact, the data show a
trend of less morbidity and mortality in favor of selective
use of surfactant in neonates assisted early with NCPAP.28
When should surfactant be used in infants assisted early
with CPAP?
Verder et al. demonstrated that using a low threshold for
early surfactant therapy (a/A PaO2 ratio 0.35-0.22) vs. (a/A
PaO2 ratio 0.21-0.15) with immediate extubation (10 min)
reduces the need of MV (63-21% p <0.05) in neonates of
25-29 weeks.25
The previous findings were confirmed in a stratified
meta-analysis, where a low threshold (FiO2 <45%) for
treatment with surfactant and extubation to NCPAP
resulted in fewer air leak syndromes (RR 0.52, 95% CI
0.28-0.96) and BPD (RR 0.51, 95% CI 0.26-0.99).29
The CURPAP study group showed that prophylactic
surfactant (INSURE prophylactic) was not superior to
INSURE early surfactant (FiO2> 40%) in infants of 25-28
weeks gestational age with early assisted NCPAP.30 There
was no significant difference in mortality or morbidity or
in the need for MV [31.4 vs. 33.0%, RR 0.95 (95% CI
0.64-1.41)]. With this strategy, 50% of infants needed
only NCPAP, 48% required intubation and surfactant and
about a third of the infants required MV during the first
5 days of life.
The recently published study developed by the Vermont
Oxford Neonatal Network supports the findings identified
in the previous paragraphs.31 It compared three strategies
of assistance to infants 26-29 weeks gestational age and
Bol Med Hosp Infant Mex
Current role of—and new evidence for—continuous positive airway pressure in respiratory distress syndrome
showed that early NCPAP with early rescue surfactant or
prophylactic surfactant with rapid extubation to NCPAP
has similar results to those treated with prophylactic
surfactant followed by MV. Early CPAP may obviate the
need for MV and/or surfactant.
When to initiate CPAP?
Some meta-analyses of clinical trials developed in the
1970s demonstrate the advantage of early initiation of
CPAP (FiO2 requirements <60%): lower mortality [RR
0.68 (0.34-1.38)] and lower need for MV [RR 0.55
(0.32-0.96)].32 Currently, the word “early” CPAP means
at birth or upon presentation of any signs of respiratory
distress.
The European consensus guidelines for management
of RDS recommend initiating CPAP from birth in all
infants at risk for RDS, such as those <30 weeks who do
not require MV until their status is evaluated.33
International consensus on neonatal resuscitation in
its 2010 update of the Neonatal Resuscitation Program
included CPAP as an option for initial management in
infants who had spontaneous respirations with heart rate
>100/min with respiratory difficulty.34
The evidence that supported this recommendation is
based on the results of the following studies: SUPPORT,26
COIN,27 CURPAP,30 and that of Dunn et al.31—commented
upon previously—that showed that infants managed early
with CPAP have the same mortality rate as infants managed
with prophylactic surfactant and MV, with the benefits of
reducing the use of surfactant, time on MV, and use of
steroids for BPD.
Levesque et al. observed that the sooner the application
of NCPAP (from birth) the more likely the success.15 The
median NCPAP startup time, when successful, was 4.3
min (range 3-19 min) vs. 29 min (range 13-33 min) those
in which NCPAP failed (p = 0.007) in an infant cohort of
26-32 weeks gestational age.
Use of prophylactic NCPAP (regardless of respiratory
condition) in more mature infants than shown in previous
studies (28-31 weeks) does not decrease the need for MV
or surfactant or the incidence of air leaks. The percentages
were as follows: the need for surfactant 22.6% vs. 21.7%
(p >0.05), the need for MV 2.12 vs. 12.2% (p >0.05),
pulmonary air leaks 2.6 vs. 2.6% (p >0.05). More than
80% of subjects received antenatal steroids.35
Vol. 69, November-December 2012
Are there advantages for early extubation vs conventional
post surfactant?
Dani et al. demonstrated that immediate extubation
(<5 min) vs. the conventional method has advantages
in neonates <30 weeks gestational age, less hours of
NCPAP therapy (3.2 vs. 6.2 days, p = 0.009), shorter
duration of MV (2.0 vs. 5.6, p <0.001), and less need
for a second dose of surfactant (0 vs. 50%, p = 0.06).36
Immediate reinstitution of NCPAP after surfactant administration is safe and effective. Bohlin et al. found
improved oxygenation as measured by a/A oxygen ratio
in infants extubated immediately vs. those maintained
on MV. This difference is evident within minutes and
lasts for >48 h. 37
The most optimal clinical and blood gases results of
NCPAP vs. MV appear to be related to a lower amount
of alveolar protein, inactivation of alveolar surfactant,
inflammation indicators, gas exchange and pulmonary
mechanics observed with NCPAP.17,19,38
What pressure to use with NCPAP?
There is consensus among Scandinavian39 and American40
authors about using minimum pressure of 5 cm. There is
still no consensus on whether to raise the pressure to 6, 7
or 8 cm H2O or to remain at only 5 cm H2O and increase
the FiO2 only if necessary. No clinical trials have compared
these strategies.
The use of 5 cm H2O or more of NCPAP postextubation
is supported not only by the opinion of experts, but in the
meta-analysis by Davis and Henderson-Smart41 where
morbidity decreases postextubation [RR 0.40 (95% CI
0.37-0.66)]. There was no difference when using <5 cm
H2O [RR 1.00 (95% CI 0.60-1.73)].
Progressive decrease in pressure or only of FiO2 while there
is improvement in respiratory distress?
Evidence in favor of maintaining pressure at 5 cm H2O
and only decreasing the FiO2 is strong and is based on
a previously discussed meta-analysis.41 Experts suggest
decreasing FiO2 up to 21% and removing NCAP if there
is no respiratory distress and apnea and blood gases are
aceptable.15 In extremely low-birth-weight infants who
required MV at birth for >7 days, it is recommended to
use NCPAP for longer periods, up to 32 weeks postconceptional age.
519
Lorenzo Osorno Covarrubias
Does the use of early CPAP improve pulmonary function
tests in the mid term vs. MV?
A subgroup of infants included in the COIN study was
studied at 8 weeks post-term. CPAP group had lower
respiratory rates (41 vs. 48/min; p = 0.007), lower minute ventilation (223 vs. 265 ml/min/kg; p = 0.009), better
pulmonary distention (0.99 vs. 0.82 ml/cm H2O/kg; p =
0.008) and better lung elasticity (p = 0.004).42
Does the surfactant used influence on the rate of success
of the INSURE strategy?
The INSURE strategy implies prompt extubation to continue with assistance with NCPAP, after the application
of a surfactant. The definition of prompt varies according
to different authors and may be from 5 min to 1 h. The
poractant has several advantages on the beractant, a more
rapid effect manifested with less requirements of FiO2,
increase in the a/A O2 ratio, and less time of MV. These
effects begin in a few minutes and persist for >48 h.43-45
The preceding would facilitate a more rapid extubation.
The 200 mg/kg dose of a poractant decreases the need for
reintubation and additional doses of surfactant.45 However,
clinical implications of these differences have not yet been
fully elucidated.
Currently, there is only one clinical trial comparing the
percentage of infants extubated at 48 h of the poractant vs.
beractant in neonates of 24-27 weeks managed with MV.46
The extubation criteria was somewhat conservative for it
to be really INSURE (FiO2 <25%, PMVA <5 cm H2O).
The percentage of infants extubated at 48 h was higher
with poractant (52 vs. 22%, p = 0.027) and at 72 h (60 vs.
27%, p = 0.029).
What impact do antenatal steroids have in the effectiveness
of CPAP?
Antenatal steroids are an indispensable part in the management of infants at risk of preterm birth. The effects are
clearly beneficial with decreased mortality [RR 0.69 (0.58
to 0.81)], RDS [RR 0.66 (0.59 to 0.73)], severity of RDS
(moderate and severe) [RR 0.55 (0.43 to 0.71)], need for
MV [0.51 (0.26, 0.99)], duration of MV (days) [weighted
mean difference (WMD) -3.47 (-5.08 to -1.86)], and days
of supplemental oxygen [WMD -2.86 (-5.51 to -0.21)].47
The American Academy of Pediatrics (AAP) and American College of Obstetricians and Gynecologists (ACOG)
recommend the administration of a course of corticoste-
520
roids in all women at 24-34 weeks of pregnancy who are
at risk of preterm delivery in the following 7 days.48
What is the probability of success with CPAP at a lower
gestational age and weight? Is there a weight or gestational
age limit to provide the option of CPAP?
The probability of success in extremely preterm neonates
increases as gestational age and birth weight increase.
Ammari et al. observed that CPAP was successful in 76%
of neonates with weighing <1250 g and in 50% weighing
<750 g.49 Of the group of 26-28 weeks, 95% received initial
support with CPAP in the delivery room and in 78% of
these neonates CPAP was successful as sole ventilatory
support. Of the neonates with birth weight <700 g, 73%
received initial CPAP support, with a success rate of 33%.
In the group weighing 800-899 g, 91% began CPAP and it
was successful in 84%. The initial severity of respiratory
distress (alveolar gradient/arterial O2) is an adverse factor
in the success of CPAP. However, the authors noted that
several indicators of severity were poor predictors of
CPAP failure.
Does the experience of the health care personnel on the use
of CPAP have an influence on success rate?
Aly et al. observed from the time of CPAP implementation in their hospital as the primary method of respiratory
assistance that the greater the rate of CPAP utilization in
an extremely premature neonate cohort, the greater the
success rate.50 In the three time periods studied, the use of
nasal CPAP increased from 17.6-61.8 and 66.7%, respectively (p <0.001). Failure of CPAP on infants initiated early
with nasal CPAP and who were intubated decreased from
38.5-13.8 and 7.4%, respectively. The use of surfactant
decreased from 48% to 13.3 and 33.3%, the incidence of
BPD decreased from 46.2% to 25.9 and 11.1%. The authors
concluded that there is a learning curve for the staff.
What implementation strategies increase acceptance of
CPAP by health care personnel as the primary method of
care in preterm infants?
The use of nasal CPAP has been confined to a few centers
of perinatal care, largely because of staff resistance to
adopt the method. Over the last decade there have been
several successful experiences published in implementing
NCPAP that used similar strategies to improve the quality
of care. We can summarized these as follows: a) review
Bol Med Hosp Infant Mex
Current role of—and new evidence for—continuous positive airway pressure in respiratory distress syndrome
of the evidence for the use of early NCPAP, b) review of
“best care” practices in hospitals with the lowest neonatal
mortality and BPD rates, c) clear guidelines for indications
of CPAP, MV, surfactant, extubation, d) full and adequate
equipment to provide NCPAP (blender, humidifier with
heater, system of interface fixation, nasal prongs, pressure
generator), e) training for all medical and paramedical
staff on the use of CPAP, f) assessing staff adherence to
the new standards with a focus on technical aspects and
focus on changing attitudes of care providers, g) discussion
of clinical cases of infants managed using CPAP, and h)
evaluation of the results so as to improve over time.
Among the best care practices adopted in these studies
are the antenatal administration of steroids in pregnancies
at risk for preterm delivery, saturation goal of 88-92%,
alarm limits of saturation 85-96%, selective intubation ≤29
weeks, to not intubate if there is good respiratory automatism, heart rate, and positive response after ventilation with
bag and mask, reevaluation in the nursery for intubation,
introduction of CPAP in the delivery room (ventilation
with resuscitation with T piece, ventilation with positive
pressure at end expiration, application of CPAP with mask,
CPAP bubble for transfer), prolonged use of CPAP (avoid
oxygen without pressure), avoid endotracheal intubation
routinely in the delivery room without a careful assessment
of respiratory effort of the infant or response to facial
CPAP before intubation and avoid unnecessary intubations
while receiving NCPAP without proper assessment of the
patient and CPAP circuit.14,15
Nasal CPAP, MV and surfactant are integral to the
current management of RDS. Antenatal steroids play
a central role in the prevention of RDS in reducing its
severity and increasing the success rate of CPAP as the
primary method of ventilatory support.
In preterm infants with respiratory automatism and
cardiac frequency (CF) >100/min, early installation of
CPAP (in the delivery room or when breathing difficulties
begin) with selective application of surfactant (with low
threshold) is an alternative to intubation and prophylactic
application of surfactant because there is no difference in
morbidity and mortality.
The current trend is to use MV only when necessary
and for the shortest time possible to prevent complications.
Reviewed research confirms that early CPAP reduces the
need for mechanical ventilation and surfactant. Early
extubation (INSURE) after application of surfactant has
Vol. 69, November-December 2012
advantages (higher ventilation efficiency and reduced
exposure to oxygen). At least 5 cm H2O of CPAP should
be used to prevent extubation failure.
For additional information on the level of evidence and
grade of recommendation of the current role of CPAP in
the management of RDS, a review of the Management
Guidelines of RDS in preterm neonates from the European33 consensus and that published by Mexican authors
is recommended.51
REFERENCES
1.
Gregory GA, Kitterman JA, Phibbs RH, Tooley WH, Hamilton
WK. Treatment of the idiopathic respiratory-distress syndrome
with continuous positive airway pressure. N Engl J Med
1971;284:1333-1340.
2. Ho JJ, Subramaniam P, Henderson-Smart DJ, Davis PG.
Presión de distensión continua de las vías respiratorias
para el síndrome de dificultad respiratoria en recién nacidos
prematuros (Revisión Cochrane traducida). Available at:
http://www.update-software.com/BCP/BCPGetDocument.
asp?DocumentID=CD002271
3. Seger N, Soll R. Animal derived surfactant extract for treatment
of respiratory distress syndrome. Cochrane Database Syst Rev
2009;2:CD007836. doi: 10.1002/14651858.CD007836.pub2
4. Soll R. Early versus delayed selective surfactant treatment
for neonatal respiratory distress syndrome. Cochrane Database Syst Rev 2009;2:CD001456. doi: 10.1002/14651858.
CD001456.pub4
5. Soll R, Morley CJ. Prophylactic versus selective use of
surfactant in preventing morbidity and mortality in preterm
infants. Cochrane Database Syst Rev 2001;4:D000510. doi:
10.1002/14651858.CD000510.pub4
6. Avery ME, Tooley WH, Keller JB, Hurd SS, Bryan MH, Cotton
RB, et al. Is chronic lung disease in low birth weight infants preventable? A survey of eight centers. Pediatrics 1987;79:26-30.
7. Van Marter LJ, Allred EN, Pagano M, Sanocka U, Parad R,
Moore M, et al. Do clinical markers of barotrauma and oxygen
toxicity explain interhospital variation in rates of chronic lung
disease? The Neonatology Committee for Developmental
Network. Pediatrics 2000;105:1194-1201.
8. Lindner W, Vossbeck S, Hummler H, Pohlandt F. Delivery room
management of extremely low birth weight infants: spontaneous breathing or intubation? Pediatrics 1999;103:961-967.
9. Gittermann MK, Fusch C, Gittermann AR, Regazzoni BM,
Moessinger AC. Early nasal continuous positive airway pressure treatment reduces the need for intubation in very low birth
weight infants. Eur J Pediatr 1997;156:384-388.
10. Joris N, Sudre P, Moessinger A. Early application of CPAP in
newborns with gestational age below 34 weeks lowers intubation rate and shortens oxygen therapy without altering mortality
and morbidity. Schweiz Med Wochenschr 2000;130:1887-1893.
11. De Klerk AM, De Klerk RK. Nasal continuous positive airway
pressure and outcomes of preterm infants. J Paediatr Child
Health 2001;37:161-167.
521
Lorenzo Osorno Covarrubias
12. Aly HZ. Nasal prongs continuous positive airway pressure: a
simple yet powerful tool. Pediatrics 2001;108:759-761.
13. Jacobsen T, Gronvall J, Petersen S, Andersen GE. ‘‘Minitouch’’ treatment of very low-birth-weight infants. Acta Paediatr
1993;82:934-938.
14. Birebaum HJ, Dentry A, Cirelli J, Helou S, Pane MA, Starr K,
et al. Reduction in the incidence of chronic lung disease in
very low birth weight infants: results of quality improvement
process in a tertiary level neonatal intensive care unit. Pediatrics 2009;213:44-50.
15. Levesque BM, Kalish LA, LaPierre J, Welch M, Porter V. Impact
of implementing 5 potentially better respiratory practices on
neonatal outcomes and costs. Pediatrics 2011;128:e218-e226.
16. Hillman NH, Moss TJM, Kallapur SG, Bachurski CJ, Pillow JJ,
Polglase GR, et al. Brief, large tidal volume ventilation initiates
lung injury and a systemic response in fetal sheep. Am J Respir
Crit Care Med 2007;176:575-581.
17. Jobe AH, Kramer BW, Moss TJ, Newnham JP, Ikegami
M. Decreased indicators of lung injury with continuous
positive expiratory pressure in preterm lambs. Pediatr Res
2002;52:387-392.
18. Thomson MA, Yoder BA, Winter VT, Martin H, Catland D,
Siler-Khodr TM, et al. Treatment of immature baboons for 28
days with early nasal continuous positive airway pressure. Am
J Respir Crit Care Med 2004;169:1054-1062.
19. Bohrer B, Silveira RC, Neto EC, Procianoy RS. Mechanical
ventilation of newborns infant changes in plasma pro- and
anti-inflammatory cytokines. J Pediatr 2010;156:16-19.
20. Attar MA, Donn SM. Mechanisms of ventilator-induced lung
injury in premature infants. Semin Neonatol 2002;7:353-360.
21. Speer CP. Chorioamnionitis, postnatal factors and proinflammatory response in the pathogenetic sequence of bronchopulmonary dysplasia. Neonatology 2009;95:353-361.
22. Bancalari E, del Moral T. Bronchopulmonary dysplasia and
surfactant. Biol Neonate 2001;80(suppl 1):7-13.
23. Polin RA. Bubble CPAP: a clash of science, culture, and religion. J Pediatr 2009;154:633-634.
24. Verder H, Robertson B, Greisen G, Ebbesen F, Albertsen P,
Lundstrøm K, et al. Surfactant therapy and nasal continuous
positive airway pressure for newborns with respiratory distress
syndrome. Danish-Swedish Multicenter Study Group. N Engl
J Med 1994;331:1051-1055.
25. Verder H, Albertsen P, Ebbesen F, Greisen G, Robertson B,
Bertelsen A, et al. Nasal continuous positive airway pressure
and early surfactant therapy for respiratory distress syndrome in newborns less than 30 weeks’ gestation. Pediatrics
1999;103:e24.
26. SUPPORT Study Group of the Eunice Kennedy Shriver NICHD
Neonatal Research Network, Finer NN, Carlo WA, Walsh MC,
Rich W, Gantz MG, et al. Early CPAP versus surfactant in
extremely preterm infants. N Engl J Med 2010;362:1970-1979.
27. Morley CH, Davis PG, Doyle LW, Brion LP, Hascoet JM,
Carlin JV, for the COIN Trial Investigators. Nasal CPAP or
intubation at birth for very preterm infants. N Engl J Med
2008;358:700-708.
28. Rojas-Reyes MX, Morley CJ, Soll R. Prophylactic versus
selective use of surfactant in preventing morbidity and
mortality in preterm infants. Cochrane Database Syst Rev
2012;3:CD000510. doi: 10.1002/14651858.CD000510.pub2.
522
29. Stevens TP, Harrington EW, Blennow M, Soll RF. Administración temprana de surfactante con ventilación breve versus surfactante selectivo y ventilación mecánica continua para recién
nacidos prematuros con o en riesgo de síndrome de dificultad
respiratoria. Available at: http://www.update-software.com.
30. Sandri F, Plavka R, Ancora G, Simeoni U, Strank Z, Martinelli
S, et al; for the CURPAP Study Group. Prophylactic or early
selective surfactant combined with nCPAP in very preterm
infants. Pediatrics 2010;125:e1402-e1409.
31. Dunn MS, Kaempf J, de Klerk A, de Klerk R, Reilly M, Howard
D, et al; for the Vermont Oxford Network DRM Study Group.
Randomized trial comparing 3 approaches to the initial
respiratory management of preterm neonates. Pediatrics
2011;128:e1069-1076.
32. Ho JJ, Henderson-Smart DJ, Davis PG. Iniciación temprana
versus tardía de la presión de distensión continua para el síndrome de distrés respiratorio en niños prematuros. Available
at: http://www.update-software.com/BCP/BCPGetDocument.
asp?DocumentID=CD002975
33. Sweet DG, Carnielli V, Greisen G, Hallman M, Ozek E, Plavka
R, et al. European consensus guidelines on the management of neonatal respiratory distress syndrome in preterm
infants—2010 update. Neonatology 2010;97:402-417.
34. Perlman JM, Wyllie J, Kattwinkel J, Atkins DL, Chameides L,
Goldsmith JP, et al. Neonatal Resuscitation: 2010 International
Consensus on Cardiopulmonary Resuscitation and Emergency
Cardiovascular Care Science With Treatment Recommendations. Pediatrics 2010;126;e1319-e1344.
35. Sandri F, Ancora G, Lanzoni A, Tagliabue P, Colnaghi M, Ventura M, et al. Prophylactic nasal continuous positive airways
pressure in newborns of 28-31 weeks gestation: multicentre
randomized controlled clinical trial. Arch Dis Child Fetal Neonatal Ed 2004;89:F394-F398. doi:10.1136/adc.2003.030701.
36. Dani C, Bertini G, Pezzati M, Cecchi A, Caviglioli C, Rubaltelli F.
Early extubation and nasal continuous positive airway pressure
after surfactant treatment for respiratory distress syndrome
among preterm infants <30 weeks’ gestation. Pediatrics
2004;113:e560-e563.
37. Bohlin K, Gudmundsdottir T, Katz-Salamon M, Jonsson B,
Blennow M. Implementation of surfactant treatment during continuous positive airway pressure. J Perinatol 2007;27;422-427.
38. Thomson MA, Yoder BA, Winter VT, Giavedoni L, Chang LY,
Coalson JJ. Delayed extubation to nasal continuous positive
airway pressure in the immature baboon model of bronchopulmonary dysplasia: lung clinical and pathological findings.
Pediatrics 2006;118:2038-2050.
39. Verder H, Bohlin K , Kamper J, Lindwall R, Jonsson B. Nasal
CPAP and surfactant for treatment of respiratory distress
syndrome and prevention of bronchopulmonary dysplasia.
Acta Pædiatrica 2009;98:1400-1408.
40. Polin RA, Sahni R. Newer experience with CPAP. Semin
Neonatol 2002;7:379-389.
41. Davis PG, Henderson-Smart DJ. Presión positiva nasal continua en las vías respiratorias inmediatamente después de
la extubación para prevenir la morbilidad en recién nacidos.
Available at: http://www.update-software.com/bcp/bcpgetdocument.asp?documentid=cd000143
42. Roehr CC, Proquitté H, Hammer H, Wauer RR, Morley CJ,
Schmalisch G. Positive effects of early continuous positive
Bol Med Hosp Infant Mex
Current role of—and new evidence for—continuous positive airway pressure in respiratory distress syndrome
43.
44.
45.
46.
airway pressure on pulmonary function in extremely premature
infants: results of a subgroup analysis of the COIN trial. Arch
Dis Child Fetal Neonatal Ed 2011;96:F371-F373.
Baroutis G, Kaleyias J, Liarou T, Papathoma E, Hatzistamatiou
Z, Costalos C. Comparison of three treatment regimens of
natural surfactant preparations in neonatal respiratory distress
syndrome. Eur J Pediatr 2003;162:476-480.
Speer CP, Gefeller O, Groneck P, Laufkötter E, Roll C, Hanssler
L, et al. Randomised clinical trial of two treatment regimens of
natural surfactant preparations in neonatal respiratory distress
syndrome. Arch Dis Child Fetal Neonatal Ed 1995;72:F8-F13.
Ramanathan R, Rasmussen MR, Gerstmann D, Finer N,
Sekar K; North American Study Group. A randomized, multicenter masked comparison trial of poractant alfa (Curosurf)
versus beractant (Survanta) in the treatment of respiratory distress syndrome in preterm infants. Am J Perinatol
2004;21:109-119.
Fujii AM, Patel SM, Allen R, Doros G, Guo CY, Testa S. Poractant alfa and beractant treatment of very premature infants with
respiratory distress syndrome. J Perinatol 2010;30:665-670.
Vol. 69, November-December 2012
47. Roberts D, Dalziel S. Corticosteroides prenatales para la
aceleración de la maduración del pulmón fetal en mujeres
con riesgo de parto prematuro (revisión). Available at: http://
www.update-software.com.
48. Committee on Obstetric Practice. ACOG committee opinion.
Antenatal corticosteroid therapy for fetal maturation. American
College of Obstetricians and Gynecologists. Int J Gynaecol
Obstet 2002;78:95-97.
49. Ammari A, Suri M, Milisavljevic V, Sahni R, Bateman D, Sanocka
U, et al. Variables associated with the early failure of nasal CPAP
in very low birth weight infants. J Pediatr 2005;147:341-347.
50. Aly H, Milner JD, Patel K, El-Mohandes AA. Does the experience with the use of nasal continuous positive airway pressure improve over time in extremely low birth weight infants?
Pediatrics 2004;114:697-702.
51. Ballesteros del Olmo JC, Udaeta Mora E, Villegas Silva R,
Cardiel Marmolejo L, Fernández Carrocera LA, Flores Nava
G, et al. Guía de práctica clínica. Tratamiento del síndrome de
dificultad respiratoria neonatal. Rev Mex Pediatr 2011;78(suppl
1):S3-S25.
523
Bol Med Hosp Infant Mex 2012;69(6):524-533
Research article
Obesity, eating behavior, and food insecurity among adolescents in
Mexico City
Luis Ortiz-Hernández,1 Magdalena Rodríguez-Magallanes,2 Hugo Melgar-Quiñónez3
ABSTRACT
Background. Food insecurity is presented when there is a limited availability of nutritionally adequate food. Food disinhibition refers to
excessive eating in the absence of hunger. We analyzed the relationships among food insecurity, food disinhibition, food consumption and
obesity in Mexico City adolescents.
Methods. A cross-sectional survey was carried out with a convenience sample (n = 543) of adolescents in Mexico City. Food insecurity
was the independent variable and was assessed through the U.S. Household Food-Security/Hunger Survey Module. Food consumption,
food disinhibition (assessed through an ad hoc inventory), and nutritional status (overweight using body mass index, obesity through triceps
and subscapular skinfolds, and abdominal obesity using waist circumference) were the dependent variables. Logistic regression models
were estimated to assess the existence of associations.
Results. Adolescents who experienced food insecurity had a higher probability of reporting an indicator of food disinhibition (hunger in the
presence of stimuli), higher intake of animal-origin food and higher rate of abdominal obesity. According to the logistic regression models
it was observed that the higher probability of abdominal obesity among adolescents with food insecurity without hunger was partially due
to another indicator of dietary disinhibition (eating rapidly).
Conclusions. In this sample of adolescents, food insecurity was related to higher probability of abdominal obesity. More studies are necessary to explore this problem in depth and to confirm the possible mediating role of dietary disinhibition.
Key words: food insecurity, hunger, obesity, overweight, food consumption, disinhibition.
INTRODUCTION
Obesity is a public health problem in Mexico with a rapidly
increasing prevalence. From the National Health Survey
of 2000 it was estimated that among adolescents aged
10-17 years, according to the criteria of the U.S. Centers
for Disease Control and Prevention (CDC), the prevalence
of overweight was 24.7% nationally and 28.5% in the
metropolitan area of Mexico City.1 By 2006, according
1
2
3
Departamento de Atención a la Salud,
Licenciatura en Nutrición Humana, Universidad Autónoma
Metropolitana Xochimilco, México, D.F., México
Departamento de Nutrición Humana, Ohio State University,
Columbus, Ohio
Correspondence: Dr. Luis Ortiz-Hernández
Departamento de Atención a la Salud
Universidad Autónoma Metropolitana Xochimilco
México, D.F., México
E-mail: [email protected]
Received for publication: 4-24-12
Accepted for publication: 9-20-12
524
to the National Health and Nutrition Survey2 it was found
that in males aged 12–19 years the prevalence of being
overweight and obese (evaluated using the tables from The
International Obesity Task Force) was 31.2%, whereas
for females it was 32.6%. Between 1999 and 2006 there
was an increase in both overweight (21.6% –23.3%) and
obesity (6.9%–9.2%) in females of that age.
Food insecurity occurs when an individual experiences
limited or uncertain availability of nutritionally adequate
and safe foods or limited ability to access food in socially acceptable ways.3 Since the 1990s, studies have
been carried out that have postulated that food insecurity
can increase the risk of obesity.4 Most studies that have
scrutinized the relationship between food insecurity and
obesity have been conducted in countries with a high socioeconomic status.5,6 It has mainly been in the U.S. where
such links have been explored in adult women7-13 and in
children.14-20 However, there are few studies that have been
carried out in school-age children21-23 or adults24,25 of low
or medium socioeconomic status. Studies have not been
identified that have been carried out in adolescents in
Bol Med Hosp Infant Mex
Obesity, eating behavior, and food insecurity among adolescents in Mexico City
these countries. In these countries, this relationship with
food may be more relevant because of the rapid increase
in the prevalence of obesity. In these societies a greater
proportion of the population lives in poverty.
Three mechanisms have been proposed to explain the
relationship between food insecurity and increased risk
of obesity, which are as follows. First, in households that
experienced this phenomenon, consumption of purchased
foods are related to low-cost energy-dense foods with a
greater capacity to generate satiety.15,22 Second, subjects
who experience food insecurity have cycles of loss (at
times when they do not have access to food) and weight
gain (when there is access), which causes changes in their
body composition and metabolism, making it more efficient for accumulation of body fat.4,12 Third, subjects who
frequently suffer food insecurity experience a cognitive
restriction, which causes them to focus their attention
on food. This is expressed in binge eating when food is
available.4,12,13 However, there is little empirical evidence
to support the latter two explanations.26
The term “food disinhibition” is used to refer to overeating in the absence of hunger and when certain stimuli
are present such as emotional stress or situations of social
interaction.27,28
Only one study has been identified that explored the
relationship between food insecurity and changes in eating
behavior.29 Considering the above, the main objective of
our study was to analyze the relationship between food
insecurity, food disinhibition, food intake and obesity in
adolescents in Mexico City.
SUBJECTS AND METHODS
An analytical, cross-sectional study was done. Sample
size was estimated with the EPIDAT program.30 Using a
previous study as a basis21 along with the results of the
ENSANUT,2 the sample size was estimated according to
two scenarios: (1) the prevalence of being overweight—
defined as +1 standard deviation of the body mass index
(BMI) for age, of at least 35% less in the group studied,
with a prevalence ratio of 1.70 and accuracy of 25%, and
(2) the prevalence of obesity—defined as >90 percentile
of skinfold or waist circumference, <13% in the group
studied, with a prevalence ratio of 1.70 and an accuracy of
40%. Sample size, obtained with a 95% level of confidence
and proportion of those not studied of 1.5, were 515 and
Vol. 69, November-December 2012
545, respectively. Inclusion criteria were subjects 11–16
years of age, without endocrinological disease, and without
any extremity with a cast. Written informed consent obtained from students and their guardian was required for
study participation. The ethical aspects of the study were
approved by the Research Committee of the Division of
Biological Sciences and Health, Metropolitan Autonomous
University–Xochimilco campus.
In order to obtain a heterogeneous sample in terms of
socioeconomic status, we chose five secondary public
schools located in different areas of Mexico City. Three
were located in delegations or municipalities with a
low socioeconomic status (Xochimilco, Iztapalapa and
Ecatepec), whereas two other schools were located in a
delegation with higher socioeconomic conditions (Miguel Hidalgo). All students were invited to participate
(taking into consideration that in the five schools there
were 1205 students), but informed consent and data were
obtained from only 534 adolescents, implying a response
rate of 44.3%. Fieldwork was conducted during October
and November 2006 in the following schools: Secondary
School No. 56 Juan Rodríguez Puebla (n = 124), Secondary
School No. 291 Javier Barros Sierra (n = 185), Secondary
School Constitution 1857 (n = 43), Secondary School No.
30 Don Benito Juarez (n = 107) and Secondary School
Xochimilco No. 107 (n = 84).
Areas of study interest were included in a questionnaire. The socioeconomic status was evaluated using the
number of assets in the child’s home. Questions included
if the household has six assets (refrigerator, washer, water
heater, telephone line, automobile or pick-up truck, and
computer). According to the General Census of Population and Housing 2010, those are the assets available in
few households. The number of assets was totaled and
the children were classified accordingly in three levels
of socioeconomic status: high (6 assets), medium (5 or
4) and low (≤3).
To determine the existence of food insecurity the
six-question version of the U.S. Household Survey
Food-Security/Hunger Module was used.3 Questions and
answers adapted for Mexico were used.31 Initially it was
planned to apply the 18-question version of the scale.
However, upon application of the pilot questionnaire it was
observed that for adolescents the questions were repetitive
and, therefore, it was decided to use the short version. It
has been shown that the six-question scale is reasonably
525
Luis Ortiz-Hernández, Magdalena Rodríguez-Magallanes, Hugo Melgar-Quiñónez
sensitive and specific when compared to the 18-question
scale.3 In order to score the questions of scale 3 (Table 1),
the procedures suggested by Bickel were followed.3 The
answers to questions 1 and 2 were dichotomized to give
them values of zero (options “never” and “do not know”) or
one (option “sometimes” and “very often”). For questions
3, 4 and 5, response options were “no” (zero) and “yes”
(one). Question 4 refers to the frequency of the occurrence
of the situation described in the previous item. Responses
were also dichotomized into “almost every month of the
year” and “a few months, but not all” (one) and “only one
or two months” or omitted responses (zero).
To determine the internal validity of the food insecurity
scale, the procedure described by Melgar-Quiñonez et al.
was followed, recommending the use of the scaling analysis based on the Rasch model.32 Attributed to this model is
the underlying premise that the phenomenon of interest is
one-dimensional and that it varies according to the degree
of severity with which it is present. In the case of the food
insecurity scale, the questions in the scale were designed
to explore the different intensity levels of insecurity; therefore, it was expected that as the questions inquire about
the most severe situations, they will be answered by fewer
subjects. This analysis yields two summary statistics: (1) a
severity score for each question, which is an expression of
the probability that a question is answered affirmatively,
and (2) a statistical model fit (infit-internal adjustment),
which provides information on the relationship between
the item and the underlying construct. Low values of the
statistics indicate that the relationship is stronger. The infit
statistical values of 0.80–1.20 are considered acceptable.
Table 1 presents the results of the analysis of the validity
of the scale of food insecurity. The infit values (0.85–1.13)
are within the satisfactory range. However, one noticed
problem was that question 4 had the highest severity
score in addition to having had the lowest percentage of
affirmative responses (3.1%) when conceptually it should
have a lower severity to questions 5 and 6. Because of this,
and because it was a question related to the frequency of
occurrence of the condition established in the previous
question and not of a condition by itself, it was decided to
eliminate it. With this, the fit of the model was maintained
(infit statistics of 0.81–1.11). Only questions that referred
to underlying conditions of the construct were included.
Questions that reflected a situation of more intense insecurity have higher severity values than those with milder
underlying conditions of food insecurity.
Answers to the questions in the scale of insecurity
(excluding question 4) were added to the results of the
scaling analysis. The authors of the scale of insecurity
suggested that food insecurity be identified with two or
more positive responses.3 It was decided to lower the cutoff point to a positive response because of the question
that was eliminated. This procedure has been proposed
by authors who have implemented this type of scale in
other Latin American countries.33, 34 Thus, the groups that
were formed are food security (zero positive responses),
insecurity without hunger or with moderate hunger (one or
two positive responses) and insecurity with severe hunger
(three to five positive responses).
Considering that obese subjects tend to eat faster than
those who are thin,35 adolescents were asked about the
Table 1. Analysis of the internal validity of the scale of food insecurity
Questions
%*
Including question 4
Severity
Infit
Excluding question 4
Severity
Infit
1. Foods that your family bought met the needs and there was no money to
buy additional food?
25.6
-2.12
1.07
-1.83
1.06
2. You did not eat a varied diet because your family had no more money?
3. Food portions were small or you did not eat because there was no more
money?
19.7
11.0
-1.43
0.40
1.13
0.85
-1.14
0.70
1.11
0.90
4. How frequent did this situation occur?
5. You ate less at home because there was no more money to buy food?
3.1
9.2
1.50
0.72
1.01
0.85
1.03
0.81
6. You were hungry but you did not eat because there was not enough food
in your house?
8.1
0.93
1.10
1.25
0.81
Infit, internal adjustment.
*Positive responses, n = 543. Omitted responses or “I do not know” were considered as missing.
526
Bol Med Hosp Infant Mex
Obesity, eating behavior, and food insecurity among adolescents in Mexico City
time they took for eating. This variable was used as an
indicator of food disinhibition. Also, on a scale of 13
items, the presence of food disinhibition was evaluated
(Table 2). The items consisted of phrases that described
situations in which one eats without being hungry or in
the presence of external stimuli. After all phrases were
read, the adolescents had to respond with what happened
to them in the mentioned situations for which they had
three options: no, sometimes, and yes. The responses were
dichotomized for the analysis (“sometimes” and “yes” = 1
and “no” = 0). Table 2 shows the results of the exploratory
factor analysis with varimax rotation that was carried out
with the items on the scale of food disinhibition. From
this analysis, five food disinhibition scales were formed
corresponding to the five factors identified in the factorial
analysis. To consider that an item was part of a factor, the
criteria used was that it had a weight of at least 0.40. In
the first subscale seven items were included (explaining
18% of the variance) and this was called “hunger in the
presence of stimulus.” From this, two groups were formed, with (4–7 positive items) and without disinhibition
(0 or 3 positive items). In subscale 4 (called “emotional
eating”) and 5 (eating without being hungry), 2 items were
included in each (explaining ~8% of the variance). It was
defined that there was disinhibition when the adolescents
responded positively to the two phrases. The factors 2
(“eats fast”) and 3 (“eats foods they like”) were each
comprised of a question.
To evaluate food consumption, a questionnaire of the
frequency of consumption was designed, which inquired
about the number of days of the last week in which the
adolescents had eaten 25 foods. The questionnaire was
developed to identify differences in the diversity of the
adolescent’s diet. For this reason, serving size was not
included in the questionnaire. Also, a week was defined
as a period of reference to reduce the memory effect. Considering the manner in which it has been suggested that
dietary diversity be measured,36 data were dichotomized as
follows: if each food had been eaten (1) or not (0) during
the prior week. Foods were classified into five groups:
fruits (apple, mandarin, papaya, melon, orange, banana
and guava), vegetables (spinach, swiss chard or purslane;
cucumber or lettuce; corn; pumpkin and cactus), high
energy-dense foods (bakery sweet bread or packaged pastries, chips, tamales, quesadillas or tacos, candy, lollipops
or chocolates, and sodas), animal products or foods high
Table 2. Factorial analysis of the scale regarding food disinhibition
Eigen value
% variance
Hunger with stimulus
1. If you are at a party, are you hungrier than usual or do you crave more food?
3. When you have money, do you buy foods that you like?
6. You are hungry almost every day?
8. You are very hungry between meals?
9. Do you consider that you eat a lot of food?
12. If you are happy, are you hungrier than usual or do you crave more food?
13. If you are with your friends, are you hungrier than usual or do you crave more food?
Eating rapidly
5. Do you think you eat quickly?
Eating foods that you like
4. If someone invites you to eat foods that you like, do you eat a lot of these foods?
Emotional eating
10. If you see tasty food advertised on TV, do you crave them and want to eat?
11. If you are sad, are you hungrier than usual or do you crave more food?
Eating without being hungry
2. You're eating and you feel full and yet you still eat?
7. Sometimes when you finish eating, you feel very full?
F1
F2
F3
F4
F5
2.35
18.19
1.25
9.63
1.22
9.36
1.11
8.56
1.03
7.93
0.55
0.42
0.56
0.62
0.45
0.52
0.56
-0.20
-0.26
0.28
0.00
0.33
0.04
-0.13
0.15
0.34
-0.13
0.08
-0.13
-0.06
-0.04
-0.38
0.38
0.13
-0.08
-0.30
-0.13
-0.11
-0.13
-0.19
-0.07
-0.01
-0.20
-0.30
0.19
0.10
0.59
0.57
-0.12
0.03
0.25
-0.49
-0.50
-0.20
0.05
0.33
0.28
-0.39
0.23
0.40
-0.36
0.52
0.48
-0.01
0.19
0.37
0.13
0.33
-0.18
-0.28
0.32
0.33
-0.33
0.44
0.76
Questions recoded: no = 0; yes = 1 and sometimes = 1. Numbers of the items corresponded to the order of the questions in the questionnaire.
Vol. 69, November-December 2012
527
Luis Ortiz-Hernández, Magdalena Rodríguez-Magallanes, Hugo Melgar-Quiñónez
in protein [beans, chicken wings (or chicken breast, thigh
or leg), ham or sausage, and milk] and cereals (breads,
tortilla and noodle soup). For each group the number of
foods consumed for each food group was added.
Following standardized measurement techniques,37,38
four observers performed the following measurements on
the adolescents: weight, height, waist circumference, and
triceps or subscapular folds.
Before beginning the fieldwork, observers were trained
according to the procedures described by Habicht.39 Using
tables of the WHO,40 the Z score for the BMI was estimated
for age and two groups were formed: with (Z score ≥1.0)
and without (≤0.99) overweight. From tables published
by a group of WHO experts,41 adolescents were diagnosed
with obesity when they were placed in a ≥90 percentile
of triceps and subscapular skinfolds. Abdominal obesity
was assessed by waist circumference using the reference
tables published by Fernandez et al.37 Two categories
were formed with (≥90 percentile) and without abdominal
obesity (<90 percentile).
Statistical analysis was done with the program SPSS
v.10. First, a descriptive analysis of each variable was
obtained (simple and relative frequency). Food disinhibition was then compared, food consumption and nutritional
status by gender, socioeconomic status (Table 3) and food
insecurity (Table 4). Also analyzed were differences in
food consumption and nutritional status according to food
disinhibition (Table 5). For comparing averages, Student
t-test was used for independent samples (comparisons
according to gender and food disinhibition) or analysis
of variance (to compare according to the socioeconomic
level and food insecurity). χ2 test was used for comparison of ratios. Using logistic regression analysis (Table
6), effect of possible confounders was adjusted (gender
and socioeconomic status) in regard to the relationship
between food insecurity and nutritional status. To assess
the impact of food disinhibition in the association of food
insecurity with nutritional status, we estimated models that
incorporated indicators for food insecurity.42
RESULTS
Table 3 shows the characteristics of the study population.
The percentage of females was higher than for males. The
majority of adolescents were 13 years of age and 50% were
classified as middle class. Nearly 4/10 teens experienced
528
food insecurity. The frequency of food disinhibition ranged between 16% and 56%, according to the indicator
used. The frequency of overweight was 30%, whereas the
frequency of obesity did not exceed 15%. Students in the
lower socioeconomic status experienced food insecurity
more often and ate faster but had lower rates of obesity.
Regarding gender, it was more common in males to eat
foods they liked, but emotional eating was less frequent,
unlike for females. Also, it was more likely for males to
present obesity.
Compared with adolescents with food security, those
with food insecurity ate in less time (p = 0.025) and the
frequency of hunger due to stimuli was higher (<0.000)
(Table 4). In males, the same difference was observed for
hunger due to stimuli (p = 0.003). Hunger due to stimuli
(p = 0.020) and consumption of animal foods (p = 0.013)
were more common in female students who had food
insecurity than for those with food security.
Adolescents who were hungry due to stimuli more frequently consumed energy-dense foods, foods from animal
products and cereals, but they had lower rates of obesity
and abdominal obesity (Table 5). Children who ate fast
had a lower consumption of fruits and foods from animal
products, but higher prevalence of overweight, obesity
and abdominal obesity. Those who ate foods they more
frequently liked energy-dense foods, foods from animal
products and cereals. Those who experienced emotional
eating more frequently consumed high-energy dense foods
and cereals, but had a lower rate of obesity. The consumption of high energy-dense foods was higher in those who
reported eating without being hungry.
After adjusting for gender and socioeconomic status,
food insecurity was not associated with overweight and
obesity (Table 5). With regard to adolescents presenting
food security, those with food insecurity without hunger
had a higher risk of abdominal obesity (OR = 1.76, p =
0.056). The difference became clear when adjusting for
gender and socioeconomic status (OR = 1.80, p = 0.049).
The relationship was attenuated by incorporating into the
food disinhibition model the indicator of eating rapidly
(OR = 1.72, p = 0.073).
DISCUSSION
In the Mexico City adolescents we studied, it was observed that in relation to those who had food insecurity,
Bol Med Hosp Infant Mex
Obesity, eating behavior, and food insecurity among adolescents in Mexico City
Table 3. Descriptive characteristics of the adolescents
Total
Socioeconomic status
Middle
High
%
%
n
%
Low
%
225
318
41
59
45
55
40
60
41
59
0.572
172
190
181
32
35
33
32
43
25
30
32
38
34
33
33
0.090
135
267
141
25
49
26
p
Male
%
Gender
Female
%
29
36
35
34
34
32
0.502
27
47
26
23
51
26
0.572
p
Gender
Male
Female
Age (years)
11–12
13
14–16
Socioeconomic level
Low
Middle
High
Insecurity food
Security
Insecurity without hunger
Insecurity with hunger
Food disinhibition
Hungry in the presence of stimulus
Eating rapdly
Eating food that you like
Emotional eating
Eating without hunger
300
203
40
55
37
7
48
38
14
54
40
6
65
31
4
0.001
54
37
9
56
38
6
0.334
196
304
283
89
123
26
56
52
16
23
36
62
53
18
21
36
55
52
15
23
56
53
52
17
23
0.983
0.294
0.948
0.803
0.828
39
56
60
9
20
34
56
47
21
25
0.218
0.995
0.004
0.000
0.147
Time to eat (h)
M
0.7
D.E.
0.4
M
0.6
M
0.7
M
0.7
0.053
M
0.7
M
0.7
0.267
Consumtion of foods (#of foods)
Fruits
Vegetables
High energy-dense
Animal origin
Cereals
All
4.3
2.4
3.7
3.7
2.5
16.6
1.9
1.5
1.1
1.1
0.7
4.2
4.3
2.3
3.7
3.7
2.5
16.4
4.3
2.4
3.7
3.8
2.5
16.7
4.1
2.4
3.8
3.7
2.4
16.4
0.588
0.844
0.559
0.280
0.851
0.700
4.5
2.3
3.8
3.8
2.5
17.0
4.1
2.4
3.7
3.7
2.4
16.3
0.006
0.448
0.105
0.137
0.136
0.041
Nutritional status
Overweight
Obesity (subscapular skinfold)
Obesity (tríceps skinfold)
Abdominal obesity (WC)
N
214
75
35
56
%
39
14
6
10
%
41
15
6
10
%
36
13
5
10
%
45
15
11
11
0.146
0.774
0.053
0.878
37
23
11
11
41
8
4
10
0.405
0.000
0.001
0.820
M, medium; SD, standard deviation; WC, waist circumference.
those who experienced insecurity without hunger had the
greater risk of presenting abdominal obesity; the difference was independent of the socioeconomic status and
gender. This finding is similar to that observed in other
Mexican pediatric populations21 and in countries with
Vol. 69, November-December 2012
high socioeconomic status.19,22 For example, according to
data from the U.S. Continuing Survey of Food Intakes by
Individuals (CSFII), it was found that in subjects 0–17
years of age, the prevalence of overweight was higher
in subjects from low-income households and there was
529
Luis Ortiz-Hernández, Magdalena Rodríguez-Magallanes, Hugo Melgar-Quiñónez
Table 4. Association of food insecurity, food consumption, and indicators of obesity
Total population
IWOH ISWH
%
%
S
%
Food dishinibition
Hunger due to stimulus
Eating rapidly
Eating foods that you like
Emotional eating
Eating without hunger
Time for eating (h)
Food consumption (# of foods)
Fruits
Vegetables
High energy-dense
Animal origin
Cereals
All
Nutricitional status
Overweight
Obesity (subscapular skinfold)
Obesity (tricep skinfold)
Abdominal obesity (WC)
p
S
%
Males
ISWOH ISWH
%
%
p
S
%
Female
ISWOH ISWH
%
%
p
29
52
52
14
21
42
60
52
17
25
60
65
53
28
28
0.000
0.134
0.998
0.098
0.435
31
53
61
6
17
45
59
60
12
24
67
62
48
19
14
0.003
0.582
0.500
0.088
0.400
28
52
46
20
23
40
60
47
21
25
53
68
58
37
42
0.020
0.206
0.603
0.235
0.183
M
0.7
M
0.6
M
0.6
0.015
M
0.7
M
0.6
M
0.6
0.025
M
0.7
M
0.6
M
0.7
0.302
4.2
2.4
3.7
3.7
2.5
16.4
%
38
13
6
8
4.2
2.3
3.8
3.8
2.5
16.6
%
42
14
6
13
4.8
2.6
3.7
4.0
2.5
17.6
%
35
20
10
13
4.5
2.3
3.8
3.8
2.5
16.8
%
36
21
11
8
4.5
2.4
3.8
3.9
2.6
17.2
%
36
23
8
12
5.0
2.3
4.0
3.7
2.4
17.3
%
48
33
19
19
4.1
2.5
3.6
3.6
2.4
16.2
%
40
8
3
8
3.9
2.3
3.7
3.8
2.4
16.1
%
46
8
4
14
4.6
3.0
3.4
4.3
2.7
18.0
%
21
5
0
5
0.146
0.469
0.653
0.074
0.853
0.228
0.611
0.484
0.625
0.142
0.550
0.831
0.737
0.639
0.490
0.753
0.592
0.440
0.371
0.294
0.297
0.082
0.475
0.013
0.232
0.136
0.110
0.922
0.648
0.156
S, security; ISWOH, insecurity without hunger; ISWH, insecurity with hunger; M, medium; WC, waist circumference.
Table 5. Association of food inhibition with food consumption and indicators of obesity
Hunger with
estimulus
Total
Food consumption
(# of foods)
No
M
Fruits
4.2
Vegetables
2.3
High energy-dense
3.5
Animal origin
3.7
Cereals
2.4
All
16.1
Nutritional status
%
Overweight
42
Obesity (subscapular 16
skinfold)
Obesity (triceps skinfold)
Abdominal obesity (WC)
8
13
Yes
M
4.3
2.5
4.0
3.9
2.6
17.3
%
35
9
3
6
Eating rapidly
p
No
M
0.829 4.4
0.196 2.5
0.000 3.7
0.004 3.9
0.000 2.5
0.001 17.0
%
0.132 34
0.019 10
0.016
0.016
3
6
Yes
M
4.1
2.3
3.8
3.7
2.4
16.6
%
44
17
9
14
p
Eating foods
that you like
No
M
0.049 4.2
0.190 2.3
0.345 3.6
0.010 3.6
0.124 2.4
0.045 16.1
%
0.012 39
0.024 14
0.009
0.002
7
12
Yes
M
4.3
2.4
3.8
3.9
2.6
17.0
%
40
14
6
9
Emotional
eating
p
No
M
0.260 4.3
0.354 2.4
0.008 3.7
0.011 3.7
0.003 2.4
0.007 16.5
%
0.664 40
0.820 15
0.664
0.368
7
11
Yes
M
4.0
2.5
3.8
3.8
2.6
16.8
%
38
7
5
9
Eating without
being hungry
p
No
M
0.116 4.3
0.531 2.4
0.074 3.6
0.569 3.7
0.037 2.5
0.630 16.5
%
0.799 40
0.034 13
0.412
0.653
7
11
Yes
M
p
4.1
2.3
4.0
3.8
2.5
16.7
%
37
15
0.412
0.493
0.006
0.717
0.505
0.742
6
7
0.698
0.214
0.604
0.550
M, medium.
530
Bol Med Hosp Infant Mex
Obesity, eating behavior, and food insecurity among adolescents in Mexico City
food insufficiency (i.e., not having an adequate amount of
food) (46.7%) compared with children from high-income
households with sufficient food (31.5%).15 However, other
studies have found inconsistent patterns in the relationship
between obesity and food insecurity. Some authors have
reported that this association is negative in certain age
groups, but in other groups the relationship is positive.14,43
In school-age children in Bogota, Colombia, there were
no differences in the prevalence of overweight according
to the level of food insecurity.23
In studies on food insecurity and obesity, gender
differences have been observed such that initially a
positive relationship was reported in females, whereas
in males no such association was observed or even that
the relationship was negative.14,43 Nevertheless, in more
recent studies the association was also observed among
adult males, although less than in females.44 In the case of
Mexico City adolescents, upon stratifying the relationship
of food insecurity with the nutritional status according
to gender, no differences were seen between males and
females (Table 4). Similarly, when adjusting for gender in
the regression models, the relationship between insecurity
and overweight was maintained (Table 6).
A possible explanation for why food insecurity can
increase the risk of obesity is that in homes where it is experienced, there is a greater availability of inexpensive, high
energy-dense foods that are perceived as more satisfying such
as refined cereals, fatty meats, etc.15,22 At the same time, in
homes with food insecurity there is less access to healthier
but more costly foods such as fruits, vegetables, whole cereals
and lean meats. In our study, partial support was found for
this explanation as the students with food insecurity had a
higher consumption of animal products. It should be pointed
out that in Mexico, in recent years, meats have become less
expensive.45 Persons in the lower socioeconomic strata have
increased their expenditure for these products, especially for
inexpensive, high-fat meats.46 However, in some studies in the
pediatric population, it has been reported that food insecurity
is accompanied by a reduction of calorie consumption20,47,48
and foods such as meats.19,20,23
Table 6. Logistic regression models using obesity as the dependent variable and food insecurity and food disinhibition as independent
variables
Overweight1
Overweight2
Obesity (subscapular skinfold)1
Obesity (subscapular skinfold)2
Obesity (triceps skinfold)1
Obesity (triceps skinfold)2
Abdominal obesity (WC) 1
Abdominal obesity (WC) 2
Abdominal obesity (WC) 3
Abdominal obesity (WC) 4
Abdominal obesity (WC) 5
Abdominal obesity (WC) 6
Abdominal obesity (WC) 7
Abdominal obesity (WC) 8
OR
ISWOH
95% CI
p
OR
ISWH
95% CI
p
1.16
1.20
1.07
1.08
0.93
1.00
1.76
1.80
2.03
1.72
1.81
1.81
1.84
1.77
0.81-1.67
0.83-1.73
0.64-1.80
0.63-1.85
0.44-1.96
0.46-2.13
0.99-3.16
1.00-3.24
1.12-3.68
0.95-3.10
1.00-3.24
1.00-3.25
1.02-3.31
0.98-3.20
0.426
0.336
0.797
0.779
0.847
0.989
0.056
0.049
0.020
0.073
0.048
0.047
0.042
0.057
0.87
0.90
1.67
1.50
1.64
1.74
1.64
1.69
2.29
1.55
1.69
1.74
1.76
1.67
0.43-1.73
0.44-1.81
0.72-3.89
0.62-3.62
0.53-5.10
0.54-5.66
0.59-4.58
0.60-4.81
0.78-6.74
0.54-4.44
0.59-4.82
0.61-4.98
0.62-5.02
0.59-1.72
0.683
0.759
0.232
0.365
0.390
0.355
0.343
0.324
0.133
0.416
0.326
0.299
0.292
0.334
Reference group: food security; WC, waist circumference.
1
Crude estimates.
2
Adjusted estimates according to gender and socioeconomic status.
3
Adjusted estimates according to gender, socioeconomic status and indicator of food disinhibition in the presence of stimulus.
4
Adjusted estimates according to gender, socioeconomic status and indicator of food disinhibition of eating rapidly.
5
Adjusted estimates according to gender, socioeconomic status and indicator of food disinhibition of eating foods that are liked.
6
Adjusted estimates according to gender, socioeconomic status and indicator of food disinhibition of emotional eating.
7
Adjusted estimates according to gender, socioeconomic status and indicator of food inhibition of eating without being hungry.
8
Adjusted estimates according to gender, socioeconomic status and indicator of food disinhibition of time for eating.
Vol. 69, November-December 2012
531
Luis Ortiz-Hernández, Magdalena Rodríguez-Magallanes, Hugo Melgar-Quiñónez
It has also been postulated that persons who experience
chronic food insecurity develop food disinhibition, i.e.,
they learn to ignore the signs of hunger and satiety and
guide their consumption in terms of food availability.12,26
One study documented that females with food insecurity
have more problems with feeding habits such as having
food binges.29 In Mexican adolescents, food insecurity
was related to a greater probability of having two forms
of food disinhibition: hunger in the presence of stimulus
and eating in a shorter time. Although two other indicators
were more frequent between students with food insecurity (eating fast and eating due to emotional state), the
differences were not statistically significant (p >0.050).
Moreover, the greatest risk of abdominal obesity among
adolescents with insecurity without hunger was due in part
to the disinhibition indicator of eating fast.
A limitation of the study is its cross-sectional design in
addition to the fact that the rate of response was relatively
low, which prevents making categorical conclusions. Until
recently, the majority of studies that explored the relationship between insecurity and obesity were cross-sectional
in design. Recently analyses with longitudinal data have
been carried out confirming the relationship between food
insecurity and weight gain.44
Another limitation of our study is that we did not use
a representative sample of adolescents, which reduces
the possibility of extrapolating the results. The concept
of food disinhibition is just beginning to be used, and for
the Mexican population there is no valid tool available for
its measurement. Therefore, a scale that allowed a primary
approximation of the phenomenon had to be developed.
Measurement of food disinhibition can be performed
through controlled procedures under laboratory conditions; however, its use is not possible in epidemiological
research.
A further limitation of the study is that there is selection
bias: having conducted the study in educational institutions implied that those adolescents not enrolled in any
educational institution would not be included, and they
have the greatest risk of having food insecurity.
In conclusion, in our sample of adolescents, food insecurity was related with a greater risk of accumulation
of excessive abdominal fat, which can be attributed in
part to eating behaviors related to the loss of capacity
of regulating food consumption. However, more studies
are needed to strengthen and confirm the mediating role
532
of food disinhibition. A more consistent finding is that
persons who experience food insecurity tend to eat inexpensive and high-caloric foods.
REFERENCES
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
Del Río-Navarro BE, Velázquez-Monroy O, Sánchez-Castillo
CP, Lara-Esqueda A, Berber A, Fanghänel G, et al. The high
prevalence of overweight and obesity in Mexican children.
Obes Res 2004;12:215-223.
Olaiz-Fernández G, Rivera-Dommarco J, Shamah-Levy T,
Rojas R, Villalpando-Hernández S, Hernández-Ávila M, et al.
Encuesta Nacional de Salud y Nutrición 2006. Cuernavaca,
México: Instituto Nacional de Salud Pública; 2006.
Bickel G, Nord M, Price C, Hamilton W, Cook J. Guide to
Measuring Household Food Security, Revised 2000. Alexandria, VA: U.S. Department of Agriculture, Food and Nutrition
Service; 2000. Available at: http://www.fns.usda.gov/fsec/
files/fsguide.pdf
Dietz WH. Does hunger cause obesity? Pediatrics 1995;95:766767.
Dubois L, Farmer A, Girard M, Porcherie M. Family food insufficiency is related to overweight among preschoolers. Soc
Sci Med 2006;63:1503-1516.
Sarlio-Lahteenkorva S, Lahelma E. Food insecurity is associated with past and present economic disadvantage and body
mass index. J Nutr 2001;131:2880-2884.
Adams EJ, Grummer-Strawn L, Chavez G. Food insecurity is
associated with increased risk of obesity in California women.
J Nutr 2003;133:1070-1074.
Gibson D. Food stamp program participation is positively
related to obesity in low income women. J Nutr 2003;133:22252231.
Jones SJ, Frongillo EA. The modifying effects of Food
Stamp Program participation on the relation between
food insecurity and weight change in women. J Nutr
2006;136:1091-1094.
Kaiser LL, Townsend MS, Melgar-Quiñonez HR, Fujii ML,
Crawford PB. Choice of instrument influences relations between food insecurity and obesity in Latino women. Am J Clin
Nutr 2004;80:1372-1378.
Laraia BA, Siega-Riz AM, Evenson KR. Self-reported
overweight and obesity are not associated with concern about
enough food among adults in New York and Louisiana. Prev
Med 2004;38:175-181.
Olson CM. Nutrition and health outcomes associated with food
insecurity and hunger. J Nutr 1999;129(suppl 2):521S-524S.
Townsend MS, Peerson J, Love B, Achterberg C, Murphy SP.
Food insecurity is positively related to overweight in women.
J Nutr 2001;131:1738-1745.
Alaimo K, Olson CM, Frongillo EA Jr. Low family income and
food insufficiency in relation to overweight in US children: is
there a paradox? Arch Pediatr Adolesc Med 2001;155:11611167.
Casey PH, Szeto K, Lensing S, Bogle M, Weber J. Children in
food-insufficient, low-income families: prevalence, health, and
nutrition status. Arch Pediatr Adolesc Med 2001;155:508-514.
Bol Med Hosp Infant Mex
Obesity, eating behavior, and food insecurity among adolescents in Mexico City
16. Casey PH, Simpson PM, Gossett JM, Bogle ML, Champagne
CM, Connell C et al. The association of child and household
food insecurity with childhood overweight status. Pediatrics
2006;118:e1406-e1413.
17. Gibson D. Long-term food stamp program participation is
differentially related to overweight in young girls and boys. J
Nutr 2004;134:372-379.
18. Jyoti DF, Frongillo EA, Jones SJ. Food insecurity affects school
children’s academic performance, weight gain, and social skills.
J Nutr 2005;135:2831-2839.
19. Kaiser LL, Melgar-Quiñonez HR, Lamp CL, Johns MC, Sutherlin JM, Harwood JO. Food security and nutritional outcomes of
preschool-age Mexican-American children. J Am Diet Assoc
2002;102:924-929.
20. Matheson DM, Varady J, Varady A, Killen JD. Household food
security and nutritional status of Hispanic children in the fifth
grade. Am J Clin Nutr 2002;76:210-217.
21. Ortiz-Hernández L, Acosta-Gutiérrez MN, Núñez-Pérez AE,
Peralta-Fonseca N, Ruiz-Gómez Y. En escolares de la Ciudad
de México la inseguridad alimentaria se asoció positivamente
con el sobrepeso. Rev Invest Clin 2007;59:32-41.
22. Oh SY, Hong MJ. Food insecurity is associated with dietary
intake and body size of Korean children from low-income
families in urban areas. Eur J Clin Nutr 2003;57:1598-1604.
23. Isanaka S, Mora-Plazas M, Lopez-Arana S, Baylin A, Villamor
E. Food insecurity is highly prevalent and predicts underweight
but not overweight in adults and school children from Bogotá,
Colombia. J Nutr 2007;137:2747-2755.
24. Gulliford MC, Mahabir D, Rocke B. Food insecurity, food
choices, and body mass index in adults: nutrition transition in
Trinidad and Tobago. Int J Epidemiol 2003;32:508-516.
25. Shariff ZM, Khor GL. Obesity and household food insecurity:
evidence from a sample of rural households in Malaysia. Eur
J Clin Nutr 2005;59:1049-1058.
26. Dinour LM, Bergen D, Yeh MC. The food insecurity-obesity
paradox: a review of the literature and the role food stamps
may play. J Am Diet Assoc 2007;107:1952-1961.
27. Stunkard AJ, Messick S. The three-factor eating questionnaire
to measure dietary restraint, disinhibition and hunger. J Psychosom Res 1985;29:71-83.
28. Bond MJ, McDowell AJ, Wilkinson JY. The measurement of
dietary restraint, disinhibition and hunger: an examination of
the factor structure of the Three Factor Eating Questionnaire
(TFEQ). Int J Obes Relat Metab Disord 2001;25:900-906.
29. Kendall A, Olson CM, Frongillo EA Jr. Relationship of hunger
and food insecurity to food availability and consumption. J Am
Diet Assoc 1996;96:1019-1024.
30. Dirección General de Saúde Pública, Consellería de Sanidad,
Xunta de Galicia; Área de Análisis de Salud y Sistemas de
Información Sanitaria, Organización Panamericana de la
Salud. EPIDAT. Programa para análisis epidemiológico de
datos tabulados. Version 3.1, 2006.
31. Melgar-Quiñonez H, Zubieta AC, Valdez E, Whitelaw B,
Kaiser L. Validation of an instrument to monitor food insecurity in Sierra de Manantlán, Jalisco. Salud Publica Mex
2005;47:413-422.
32. Melgar-Quiñonez HR, Nord M, Pérez-Escamilla R, Segall-Correa AM. Psychometric properties of a modified US-household
Vol. 69, November-December 2012
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
food security survey module in Campinas, Brazil. Eur J Clin
Nutr 2008;62:665-673.
Pérez-Escamilla R, Segall-Correa AM, Kurdian ML, Sampaio
MDA, Marín-León L, Panigassi G. An adapted version of the
U.S. Department of Agriculture Food Insecurity module is a
valid tool for assessing household food insecurity in Campinas,
Brazil. J Nutr 2004;134:1923-1928.
Alvarez MC, Estrada E, Montoya EC, Melgar-Quiñonez H.
Validation of a household food security scale in Antioquia,
Colombia. Salud Publica Mex 2006;48:474-481.
Birch LL, Fisher JO. Development of eating behaviors among
children and adolescents. Pediatrics 1998;101:539-549.
Ruel MT. Operationalizing dietary diversity: a review of measurement issues and research priorities. J Nutr 2003;133:3911S3926S.
Fernández JR, Redden DT, Pietrobelli A, Allison DB. Waist
circumference percentiles in nationally representative samples
of African-American, European-American, and Mexican-American children and adolescents. J Pediatr 2004;145:439-444.
Lohman TG, Roche A, Martorell R. Anthropometric Standardization Reference Manual. Champaign, IL: Human Kinetics; 1988.
Habicht JP. Standardization of quantitative epidemiological
methods in the field. Bol Oficina Sanit Panam 1974;76:375384.
De Onis M, Onyango AW, Borghi E, Siyam A, Nishida C,
Siekmann J. Development of a WHO growth reference
for school-aged children and adolescents. Bulletin WHO
2007;85:660-667. Available at: http://www.who.int/bulletin/
volumes/85/9/07-043497/en/index.html
World Health Organization Expert Committee. Physical status:
the use and interpretation of anthropometry. Geneva: World
Health Organization; 1995.
Baron RM, Kenny DA. The moderator-mediator variable
distinction in social psychological-research: conceptual,
strategic, and statistical considerations. J Pers Soc Psychol
1986;51:1173-1182.
Jones SJ, Jahns L, Laraia BA, Haughton B. Lower risk of
overweight in school-aged food insecure girls who participate
in food assistance: results from the panel study of income
dynamics child development supplement. Arch Pediatr Adolesc
Med 2003;157:780-784.
Wilde PE, Peterman JN. Individual weight change is associated
with household food security status. J Nutr 2006;136:13951400.
Ortiz-Hernández L. Price evolution of foods and nutriments in
Mexico from 1973 to 2004. Arch Latinoam Nutr 2006;56:201215.
Ortiz-Hernández L, Delgado G, Hernández A. Desigualdad
social, alimentación y obesidad en México. In: Bertan M, Arroyo
P, eds. Antropología y Nutrición. México: FUNSALUD, UAM
Xochimilco; 2006. pp. 237-256.
Mazur RE, Marquis GS, Jensen HH. Diet and food insufficiency
among Hispanic youths: acculturation and socioeconomic
factors in the third National Health and Nutrition Examination
Survey. Am J Clin Nutr 2003;78:1120-1127.
Rose D, Oliveira V. Nutrient intakes of individuals from foodinsufficient households in the United States. Am J Public Health
1997;87:1956-1961.
533
Bol Med Hosp Infant Mex 2012;69(6):534-540
Research article
Niches of opportunity for improving health care of children covered by
“Medical Insurance for a New Generation”
Luis Jasso-Gutiérrez,1 Luis Duran-Arenas,2 Samuel Flores-Huerta,3 Gabriel Cortes-Gallo,4
Onofre Muñoz-Hernández5
ABSTRACT
Background.The focus of the program “Medical Insurance for a New Generation” (SMNG) is to offer social and economic protection and
to eliminate costs for those families who lack medical insurance coverage. The objective of this study was to identify niches of opportunity
in the program to improve health care for children funded by the SMNG.
Methods. With information provided by the SMNG, nine “performance indicators” were calculated and described in the rules of operation of
the SMNG and a “documentary review” was carried out in accordance with the National Council of Social Development Policy Evaluation.
Results. Three of the “performance indicators” were poor. The “documentary review” revealed some faults in the quality of completing the
database of 6,440 children and 128 accredited hospitals. Of these, only 51.9% were admitted during the first 24 h of birth. Overall mortality
was 4.43%, with differences according to federal entities from 0.0% to 18.8%. There was a predominance of intrauterine hypoxia, necrotizing enterocolitis and diaphragmatic hernia. From 108 diseases, 41 represented 90.9% of all children admitted.
Conclusions. It is necessary to improve the efficiency of three of the “performance indicators.” In regard to the “documentary review” it
will be required to expand information and the quality of the clinical information contained in the database, promote more timely admission
of children to the hospital, and analyze mortality differences among the federal entities.
Key words: performance indicators, documentary review, Medical Insurance for a New Generation, newborn morbidity, newborn mortality.
INTRODUCTION
With the goal of continuing to decrease neonatal and infant
mortality in Mexico, as of December 2006 the Federal
government implemented the program Medical Insurance
for a New Generation (SMNG) with well-defined rules of
operation.1,2 The focus of this program is to provide costfree social and financial protection to those families who
1
2
3
4
5
Departamento de Evaluación y Análisis de Medicamentos,
Centro de Estudios Económicos y Sociales en Salud,
Departamento de Investigación en Salud Comunitaria,
Dirección del Seguro Médico para una Nueva Generación,
Dirección de Investigación, Hospital Infantil de México Federico
Gómez, México, D.F., México
Correspondence: Dr. Luis Jasso-Gutiérrez
Departamento de Evaluación y Análisis de Medicamentos
Hospital Infantil de México Federico Gómez
México, D.F., México
E-mail: [email protected]
Received for publication: 4-25-12
Accepted for publication: 10-15-12
534
lack a system of medical insurance and whose newborn
children require generally high-cost medical care.
SMNG included for the year 2008 a total of 108 diseases
which, in general, present themselves during the neonatal
age and require hospital care. The listing is recorded in
the rules of operation of the SMNG itself.1 With the goal
of reducing the variability in clinical practice and to improve as much as possible the quality of medical care,3 a
Medical Care Protocol was developed for each disease.
These protocols describe the basic elements of the etiology,
diagnosis and treatment, which also serve as a guideline
for the National Commission of Social Health Protection
as an orientation for estimating the costs of care of each
illness. SMNG also finances other specific neonatal diseases (e.g., prematurity, respiratory insufficiency and certain
types of congenital malformations that will be discussed
in this study) at a much higher cost and that tax medical
care in the newborn intensive care unit (NICU) through the
program called Fund for Protection Against Catastrophic
Costs (FPCGC).4,5
Social programs of the federal government, such as
the SMNG, need to periodically evaluated after beginBol Med Hosp Infant Mex
Niches of opportunity for improving health care of children covered by “Medical Insurance for a New Generation”
ning their operations, by external organizations that are
not part of their management directors, for which reason
the Hospital Infantil de México (HIMFG) was chosen to
perform this evaluation. The evaluation must adhere to the
guidelines that are described and set forth in the regulations
issued by the National Council for Evaluation of Social
Development Policy(CONEVAL)6 in which is indicated
to verify the degree of compliance with the “performance
indicators” that were previously designed in the Rules of
Operation of the SMNG1,2—in which aspects of financial
coverage for the population are determined and the “document review”, which consists of analyzing achievements
and deficiencies present in the document review that justifies medical care for those neonates covered under the
SMNG. Therefore, the goal of this study was to verify the
level of compliance with the performance indicators of the
program and document review. Based on the results, there
were niches of opportunity for improvement identified to
upgrade the processes of care of infants treated in 2008.
MATERIALS AND METHODS
Pursuant to the terms and conditions outlined in the Rules
of Operation of the SMNG1 and in accordance with regulations issued by the CONEVAL,6 two components were
evaluated. The first corresponding to the nine performance
indicators whose numerators and denominators were already preset in the above operating rules and where the
ideal result of the calculation of each indicators should
be 100% or greater. Calculations and their analysis were
carried out with the information that was provided by the
General Directorate of the SMNG (GD-SMNG) to the
HIMFG. The second component, corresponding to the
document review, is supported according to the guidelines, revising and analyzing the corresponding document
information which, in this case was included on the basis
of data of children hospitalized in 2008. On this basis along
with what is indicated in the Protocols for Medical Care
for each disease, degree of compliance was verified. The
database was provided by the GD-SMNG and included a
total of 128 medical centers that were accredited by the
Department of Health to provide medical care to children
of the 108 diseases authorized by the SMNG. The process
of accreditation of the medical centers was carried out
by health authorities of each federal entity, supported by
the Manual of Accreditation published for this purpose.7
Vol. 69, November-December 2012
The database contained the following information:
name of the child’s parents, date of report, state, hospital
name, membership number, child’s name, date of birth,
gender, age in days, months or years, medical record
number, date of confirmation of diagnosis, treatment start
date, reason for discharge (improvement, death or transfer
to another hospital), principal diagnosis with its corresponding International Classification of Disease (ICD-10)
code, type of treatment (medical or surgical), authorized
cost of care for each condition and number of the report
with which the information that was sent to the appropriate
federal entity to the GD-SMNG. With this database provided in Excel (Microsoft, Redmond, WA), diverse runs
were done that would allow for different components to
be analyzed such as behaviors of federal entities, medical
centers, number of patients, diseases, age at birth, age at
admission to the hospital, gender, discharge condition,
cause of death, among other variables. The protocol was
approved by the HIMFG Research and Ethics Committee.
When necessary, simple linear correlations were used as
statistical method.
RESULTS
Performance Indicators
The indicators identified with performance numbers 1,
2, 5, 7, 8 and 9 were 100% efficient or higher, whereas
those related to numbers 3, 4, and 6 showed percentages
of 1.8, 5.5 and 64%, respectively, and were classified as
poor (Table 1).
Document Review
The first type of data verified was which medical centers were accredited in 2008. It was identified that the
accreditation process began in that year and was done
progressively by states. Therefore, in the first 7 months
there were medical centers accredited in 14 states, by
October there were 14 more and between November and
December another three, with the last state being Nayarit.
The only federal entity without an accredited medical
center in 2008 was Baja California Sur. Accreditation
is an indispensable condition for receiving funds for the
care of children protected by SMNG.7 The total number of
medical centers accredited was 28, the majority of which
were concentrated in the Federal District, Guanajuato,
Jalisco, Morelos and Veracruz. The states of Sinaloa,
535
Luis Jasso-Gutiérrez, Luis Duran-Arenas, Samuel Flores-Huerta, Gabriel Cortes-Gallo, Onofre Muñoz-Hernández
Table 1. Percentage of results of indicators of performance corresponding to SMNG in 2008
Indicator
1. % of children with access to
the system of social protection
in health under the SMNG
2. % of children affiliated with
SMNG vs. the previous year*
Method of calculation
Data
N° of children affiliated with SMNG
1,852,891
Children born from December 1,
2006 without health insurance
1,748,000
No. of children affiliated in
2008 with SMNG
1,033,481
No. of children affiliated in
2007 with SMNG
3. Care of children by SMNG as Cases treated of children by SMNG
a percentage of those incorpoChildren affiliated with SMNG
rated with the SMNG
Cases treated of children affiliated
with SMNG paid with FPCGC with
4. % follow-up of cases of
follow-up appointment
children treated*
Cases treated of children incorporated into SMNG paid from the
FPCGC
Budgetary exercise of SMNG in
MDP
5. Percentage of budgetary
exercise of SMNG
Modified budget of SMNG in MDP
6. Efficiency of budgetary exercise of SMNG*
7. Advance in transfer of
capital*
8. Advances in the transfer of
reimbursements*
Observations
106
The denominator was estimated
according to CONAPO projections,
assuming that 54% of children were
born unprotected by any social
security system
126
819,410
18,505*
1,033,507
1.8
Reported by hospital care*
5.5
Most of the interventions in the NICU
in medical care are resolved without
the need for follow-up
646
11,739
1,697.8
100
1,697.8
Budgetary exercise of SMNG in
MDP
1,697.8
Budget of SMNG authorized in MDP
2,641.2
Funds transferred per capita in MDP
67.8
Total funds budgeted per capita
MDP
67.8
Funds transferred for reimbursement
in MDP
154.5
Total budgetary resources reimbursed in MDP
154.5
Funds transferred for vaccines in
9.Advances in funds transfer for
MDP
vaccines*
Total budgetary resources for vaccines in MDP
Value (%)
64
Returned to TESOFE 943.4 MDP for
budgetary savings
100
100
1,428.7
1,428.7
100
Financing of pneumococcal and heptavalent vaccines (2008 and 2009)
*The first rules of operation of the health program, Seguro Médico para una Nueva Generación, were published 3/31/08. Indicators refer
to the 2008 exercise.
SMNG, Seguro Médico para una Nueva Generación (Medical Insurance for a New Generation); FPCGC, Fondo de Protección Contra
Gastos Catastróficos (Fund for the Protection Against Catastrophic Expenses); NICU, neonatal intensive care unit; MDP, millions of pesos; CONAPO, Consejo Nacional de Población (National Population Council); TESOFE, Tesorería de la Federación (Federal Treasury).
Chiapas, Chihuahua, Mexico, Nuevo Leon, and Aguascalientes, despite having numerous accredited medical
centers, had a proportionately less demand for medical
care for children. It can be noted that the total financing
of the 6440 children treated was $201,644,884 (Mexican
pesos). This represented an average cost per patient of
536
$31,311.31. The greatest numbers of patients treated
and financed by the federal entities were in the states
of Guanajuato, Federal District, Jalisco, Tamaulipas,
Veracruz and Puebla, and the lowest number of patients
was in Yucatán, Campeche and Michoacán (Table 2). No
significant linear correlation was found depending on the
Bol Med Hosp Infant Mex
Niches of opportunity for improving health care of children covered by “Medical Insurance for a New Generation”
Table 2. Number of patients, financing, number of deaths and
percentage of mortality according to federal entity of children protected by SMNG
Federal
entity
Aguascalientes
Baja California
Baja California Sur
Campeche
Chiapas
Chihuahua
Coahuila
Colima
México Distrito Federal
Durango
Guerrero
Guanajuato
Hidalgo
Jalisco
México
Michoacán
Morelos
Nayarit
Nuevo leon
Oaxaca
Puebla
Quintana Roo
Querétaro
Sinaloa
San Luis Potosi
Sonora
Tabasco
Tampico
Tlaxcala
Veracruz
Yucatán
Zacatecas
Total
Patients
Financing
Death Mortality
(n)
($)
(n)
(%)
89
135
SD
11
119
81
31
132
614
130
220
1307
152
485
244
7
274
37
159
322
298
63
117
116
248
187
105
365
103
341
6
166
6440
3,408,312
3.946.606
SD
415,800
3,834,312
2,480,978
943,597
4,650,973
21,692,756
2,956,923
7,281,595
42,193,132
4,948,310
16,725,638
8,473,358
271,779
6,679,646
927,351
5,027,565
9,138,640
9,556,795
1,747,750
2,749,535
3,311,827
7,779,485
5,375,986
3,428,151
8,730,118
4,992,032
11,186,079
210,232
3,934,541
201,644,884
2
1
SD
2
5
3
0
13
25
2
17
86
11
23
4
0
4
3
3
7
21
4
0
8
9
5
4
7
6
12
0
6
290
2.25
0.74
SD
18.18
4.20
3.70
0.00
9.85
4.07
1.54
7.73
6.58
7.24
4.74
1.64
0.00
1.46
8.11
1.89
2.17
7.05
6.35
0.00
6.90
3.63
2.67
3.81
1.92
5.83
3.52
0.00
3.61
4.43
ND, no data; SMNG, Seguro Médico para una Nueva Generación (Medical Insurance for a New Generation).
number of months in which medical centers were added
to the number of patients seen. There were a total of 290
deaths, representing a mortality rate of 4.43%. Linear
correlation coefficient showed no statistical significance(r
= 0.038) between the number of cases managed by state
and percentage of mortality, so that the reasons for the
Vol. 69, November-December 2012
variations from 18.8% in Campeche to 0% in the states
of Coahuila, Querétaro and Yucatán could not be identified with the information contained in the database. Of
the 108 authorized diseases in the Operating Rules, 41
accounted for 90.9% of the children cared for.
There are 12 diseases listed that accounted for 57.32%
of the total 6440 admissions which, in turn, represented
67.7% of the total budget provided by the SMNG. Moreover, of the total revenue, 51.94% of children were
admitted within 24 h of postnatal age, 28.9% between 2
and 28 days and 24.8% after 28 days (Table 3).
Several children who were admitted after 24 h of
postnatal age had the following diagnoses: child of a
hypertensive mother, intrauterine malnutrition, acute
renal failure, neonatal intracranial hemorrhage, necrotizing enterocolitis, seizures and congenital diaphragmatic
hernia. In contrast, there were diagnoses of children with
bilateral hearing loss, congenital lacrimal duct stenosis,
polydactyly, syndactyly, hydrocele, and spermatocele
and who exceeded their hospital stay for 100, 55, 55 and
45 days, respectively. It should be noted that a statistical
linear correlation was not identified between the increase
in the length of stay and the amount in pesos disbursed
by GD-SMNG.
In the analysis of the database there were several
omissions found on the health status at discharge, type
of treatment (medical or surgical) and identification of
the principal disease diagnosis and secondary diagnosis
including ICD-10 coding, as well as data capture of
errors and inconsistencies. For example, some children,
in addition to receiving medical treatment, required a
surgical resolution as with cases of pyogenic arthritis
or intestinal obstruction, but it was not mentioned in
the database if they had undergone surgery or may have
been referred to another hospital. In contrast, children
who should have undergone medical treatment such as
in the case of bronchopulmonary dysplasia or lactose
intolerance and who were classified as cases requiring
surgical intervention only.
It can be appreciated that the five principal causes
of death in the population examined were intrauterine
hypoxia (14.9%), necrotizing enterocolitis (10.1%), congenital diaphragmatic hernia (6.4%), hypovolemic shock
(6.1%) and atraumatic intracranial hemorrhage (5.4%)
(Table 4).
537
Luis Jasso-Gutiérrez, Luis Duran-Arenas, Samuel Flores-Huerta, Gabriel Cortes-Gallo, Onofre Muñoz-Hernández
Table 3. Selection by number of patients and total cost or both of the top 12 diseases of the total for children cared for in medical units
funded by SMNG in the year 2008
Age at admission
Discharge
condition
Treatment
Code
ICD-10
Description
No. of
cases
Total cost
≤24
h
2-28
days
>28
days
Imp
(n)
P20,
P21
P05
Intrauterine hypoxia
1206
34,610,707
893
236
77
1155
3.8
1202
4
Delayed fetal development and
fetal malnutrition
Necrotizing enterocolitis
Hemolytic disease of fetus and NB,
other excessive hemolysis
548
27,534,649
378
150
20
532
1.4
548
0
302
562
21,895,912
13,863,740
101
257
132
272
69
33
269
556
2.6
0.5
273
554
29
2
256
13,094,416
68
60
128
241
1.3
256
0
150
151
4,616,113
4,118,414
8
57
27
57
115
37
144
137
0.4
1.2
47
149
103
2
69
3,698,534
14
33
22
53
1.4
61
8
52
67
3,323,783
3,297,438
21
12
19
4
12
51
33
66
1.6
0.0
6
8
46
59
88
59
3,295,738
3,277,187
8
6
8
20
72
33
69
55
1.5
0.2
87
9
1
50
3510
6440
136,626,632
201,644,844
1823
1018
671
3315
5.5
3200
304
P77
P55,
P58
P00.0
Q79.0
Q69;
Q70
R57.1
Q43
Fetus and NB affected by maternal
hypertension
Other intestinal obstruct-ions
Convulsions of NB
Cerebral depression
Hypoxic ischemic encephalopathy
Nontraumatic intracranial hemorrhage of the NB
CDH
Polydactyly
Syndactyly
Hypovolemic shock
Other intestinal mal-formations
Subtotal
Total
K56.4
P90,X;
P91.4;
P91.6
P52
Death Medical Surgical
(%)
(n)
(n)
NB, newborn; CDH, congenital diaphragmatic hernia; SMNG, Seguro Médico para una Nueva Generación (Medical Insurance for a New
Generation); Imp, improved.
DISCUSSION
Performance Evaluation of Indicators
Indicator 1, related to access to SMNG-funded public
health services, presented a percentage of 106%, which
was considered satisfactory based on the number of members as of December 1, 2006, which was slightly higher
than the number of births. With this result there are no
recommendations for improvement opportunity for the
program. Regarding indicator 2 that refers to the number
of SMNG members compared to the previous year, this
was 126%, exceeding the proposed target of 100%, which
was shown to have been met and exceeded the policy of
the Popular Insurance of a progressive expansion of the
coverage.
538
Indicator 3, which assesses the number of children
served by the SMNG as a percentage of program affiliates,
had a poor performance (1.8%) because the GD-SMNG
only had available statistics of hospitalized children, but
not for children seen as outpatients. This result represents
a niche of opportunity that must be addressed and, in the
following evaluation, must be corrected, and include
outpatients in the database.
Regarding indicator 4, which refers to follow-up of
children, this showed an efficiency of 5.5% because the GDSMNG database did not have that information for 2008. For
this reason, the time to do it did not run in parallel with the
time that the Operating Rules were issued in March 2008.
In addition, the GD-SMNG considered these children to be
discharged, and generally there was no follow-up required.
Bol Med Hosp Infant Mex
Niches of opportunity for improving health care of children covered by “Medical Insurance for a New Generation”
Table 4. Most relevant causes of mortality of 290 patient deaths
presented by children protected by SMNG
Disease
Mortality (%)
Intrauterine hypoxia
NEC
CDH
Hypovolemic shock
Newborn nontraumatic IC
Developmental delay and intrauterine malnutrition
Newbornwith maternal hypertension
Superficial scalp trauma
Convulsions and ischemic hypoxic encephalopathy
DIC
ARI
Pneumothorax, aspiration of meconium, pulmonary hemorrhage
Cardiac insufficiency
Alterations of Na and K equilibrium of newborn
14.9
10.1
6.4
6.1
5.4
5.4
5.1
4.7
4.7
Bronchopulmonarydyplasia
2.0
Hemolytic disease of the newborn and other
hemolysis
Pneumothorax, pleural effusion
Intestinal obstruction
2.0
4.1
3.7
2.7
2.4
2.0
1.7
1.7
NEC, necrotizing enterocolitis; CDH, congenital diaphragmatic hernia; IC, intracranial hemorrhage; DIC, disseminated intravascular
coagulopathy; ARI, acute renal insufficiency.
Despite the above, this is an area of opportunity
for improvement in that, necessarily, there should be a
follow-up program to ensure the complete recovery of the
children and minimize the risks posed by the precarious
socioeconomic conditions of their families. Follow-up
should be incorporated not only for neonates who require
hospitalization but also those who, having been born
healthy, need to be examined periodically in the outpatient
primary care clinic to check the progress of their growth
and development, administer vaccines, offer dietary guidelines, and treat intercurrent infections, among others. This
will certainly result in a decrease in childhood morbidity
and mortality.
An issue of great concern in the management of the
budget in the public sector is to assure that the programmed budget is equal to that spent, which was not the
case in 2008 as demonstrated in indicator 6 (64%). The
explanation for this was that the GD-SMNG, because of a
requirement from theFederal Treasury, had to return part of
the budget. Another area for improvement is ensuring that
Vol. 69, November-December 2012
from 2009 its complete cost is guaranteed. With respect to
progress indicators, the transfer of capital (indicator 7), the
progress in the transfer of funds (indicator 8), the progress
in the transfer of funds for vaccines (indicator 9), which
reached 100%, these were considered as accomplished
targets with efficient results.
Document Evaluation
We identified deficiencies in completing the database,
producing variations in the results. This situation occurred
with the number of deaths by state, with the emission of
different diagnoses for the same disease or prolonged
duration of hospital days based on the child’s condition.
For these examples and many others, opportunities for
improvement reside in making adjustments to the contents
of the existing database in the following order: first and last
name of the child, complete address of the insured, date
of report, federal entity and name of the hospital where
the child was born, name of the accredited hospital and
federal entity to which the child was referred, affiliation
number, date of birth, gender, age in days, months and
year on admission, date of confirmation of diagnosis, date
of start of treatment, cause for discharge (improvement,
death, transfer to another hospital, or voluntary discharge),
principal diagnosis and two secondary diagnoses (when
they exist), precise coding of death based on the ICD-10,
type of treatment used (medical, surgical, or both), cost
authorized for financing of the principal illness, number
of the report with which the information was sent to the
GD-SMNG, date of release, days of hospital stay and date
of confirmation of the diagnosis.
The existence of different diagnoses for the same disease within the same medical center and among other centers
required that training be carried out for those responsible
for management in the SMNG of each state. Once trained,
there should be no errors in completing the data bases until
they have been corrected by the physicians responsible for
the care of each infant. Special emphasis should be placed
on making the diagnosis according to the strict adherence
to the description of the disease and its respective ICD-10
code. All this must be done in accordance with the existing
medical protocols issued by the GD-SMNG.3
It is shown that the ideal time to hospitalize an infant
with a condition requiring hospitalization is within the first
24 h of postnatal age. However, this occurred in only 55%
of the children evaluated. Therefore, another area of oppor-
539
Luis Jasso-Gutiérrez, Luis Duran-Arenas, Samuel Flores-Huerta, Gabriel Cortes-Gallo, Onofre Muñoz-Hernández
tunity recommended is that if the mother is affiliated with
Seguro Popular during pregnancy and before or during
labor and the child is born with any of the conditions listed,
the child will be timely transferred to an accredited hospital
in the care of diseases covered by the SMNG in case the
center where the child was born does not have the capacity to treat the child. The mortality rate of 4.43% shown
when analysis is carried out by federal entity showed a
great variability, which did not permit a precise analysis
to be carried out of the results based only on the information present in the database. This is relevant because the
primordial objective, in addition to social protection and
decrease in costs to the family, is the decrease in neonatal
mortality. To place these findings in context, it is important to note that in the year 2008 there were 8,795,000
children <5 years of age who died worldwide. Of these,
45% (3,575,000) were neonates whose principal causes
of death were prematurity in 12% (1,033,000), asphyxia
9% (814,000), septicemia 6% (521,000) and pneumonia
4% (366,000).8 With the exception of the latter, this is
similar to what occurs in Mexico and other countries.9,10
However, the results found in the present evaluation indicate that intrauterine hypoxia was the principal cause
of death followed by necrotizing enterocolitis, congenital
diaphragmatic hernia and atraumatic intracranial hemorrhage. These results do not coincide in that order with the
statistics from Mexico.9 This is noteworthy, which makes
it indispensable that the database be reviewed in depth by
those responsible for the 128 medical centers evaluated.
Having found a low mortality rate (4.43%) and taking into
account the diseases identified, it is possible that it may
be due to a deficiency in completing the database. This is
inferred by the large differences found between the different states ranging from 0% to18.8%. In practice, this does
not correspond to reality, even though respiratory failure,
prematurity, sepsis and congenital cardiac malformations
were not included among the 108 diseases evaluated that
are covered by the FPCGC.
Taking into consideration that the international goal
No. 4 of Millenium of the WHO has as its goal to reduce
mortality by two thirds between the years 1990 and 2015
in children <5 years of age and because neonatal mortality represents 50% of deaths, it is indispensable that
540
the SMNG continues to improve and develop different
quality strategies at the federal level to achieve reduction
in mortality in the years after 2008.8,11
REFERENCES
1.
ACUERDO por el que se emiten las Reglas de Operación del
Programa Seguro Médico para una Nueva Generación, para
el ejercicio fiscal 2008. México; 2008. Available at: http://www.
ropsa.net/ropsa/
2. Secretaría de Salud. Seguro Popular. México. Seguro Médico
para una Nueva Generación. Available at: http://www.seguropopular.salud.gob.mx/index.php?option=com_content&view=
article&id=280&Itemid=295
3. Secretaría de Salud. Seguro Popular. México. Protocolos de
Atención Médica. Available at: http://www.seguro-popular.
gob.mx/images/contenidos/SeguroNuevaGeneración/protocolos_smng.pdf
4. Jasso-Gutiérrez L, Duran-Arenas L, Flores-Huerta S, CortésGallo G. Recommendations to improve health care of neonates
with respiratory insufficiency beneficiaries of Seguro Popular.
Salud Pub Mex 2012;54(suppl 1):S57-S65.
5. Secretaría de Salud. Seguro Popular. México. Intervenciones
médicas cubiertas por el Programa Seguro Médico para
una Nueva Generación(SMNG). Available at: http://www.
seguro-popular.gob.mx/images/contenidos/FPGC/IntervencionesFPGC.pdf
6. CONEVAL. México. Lineamientos Generales para la Evaluación de los Programas Federales de la Administración Pública
Federal. Diario Oficial de la Federación. México. Viernes 30
de marzo de 2007. Available at: http//www.coneval.gob.mx/
contenido/eva_mon/361pdf
7. Secretaría de Salud. México. Sí Calidad. Manual para la
acreditación y garantía de calidad en establecimientos para
la prestación de servicios de salud. Available at: http://www.
calidad.salud.gob.mx/calidad/acred.html.
8. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, Bassani
DG, et al. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 2010;375:1969-1987.
doi:10.1016/S0140-6736(10)60549-1.
9. Jasso GL. Mortalidad perinatal y neonatal. In: Neonatología
Práctica. Mexico: Manual Moderno; 2008. pp.1-5.
10. Subspecialty Group of Neonatology, Pediatric Society, Chinese Medical Association. Epidemiologic survey for hospitalized neonates in China. Zhongguo Dang Dai ErKeZaZhi
2009;11:15-20.
11. Rajaratnam JK, Marcus JR, Flaxman AD, Wang H, LevinRector A, Dwyer L, et al. Neonatal, postneonatal, childhood,
and under-5 mortality for 187 countries, 1970–2010: a systematic analysis of progress towards Millennium Development
Goal 4. Lancet 2010;375:1998-2008. doi:10.1016/S01406736(10)60703-9.
Bol Med Hosp Infant Mex
Bol Med Hosp Infant Mex 2012;69(6):541-552
Research article
Global neurodevelopmental screening tests for children <5 years of age in
the United States and Latin America: a systematic review and comparative
analysis
Beatriz Romo-Pardo, Silvia Liendo-Vallejos, Guillermo Vargas-López, Antonio Rizzoli-Córdoba,
Guillermo Buenrostro-Márquez
ABSTRACT
Background. The American Academy of Pediatrics recommends the application of neurodevelopmental screening tests for early intervention of neurodevelopmental disorders. In order to refer these tests appropriately, it is important to have well-founded information in regard
to these tools.
Methods. A systematic literature search targeted on validation studies of neurodevelopmental screening tests in children <5 years of age
in the U.S. and Latin America from 1980 to 2012 was conducted.
Results. We found 19 validation studies of 13 screening tests. Battelle Developmental Screening Inventory (2nd edition) reported the best
sensitivity and specificity (0.93/0.88) and PRUNAPE, with predictive positive and negative values (0.94/0.97)
Conclusions. From 1980-2012 we found 13 neurodevelopmental screening tests in the U.S. and Latin America for children <5 years of
age. The best criterion and predictive validity was for the Battelle Developmental Inventory Screening and PRUNAPE, respectively. No
validation studies were found in Mexico; therefore, we consider it important to have a validated tool in our country.
Key words: neurodevelopment, screening tests, validation.
INTRODUCTION
Early detection of neurodevelopmental problems is critical to the welfare of children and their families because
it allows access to timely diagnosis and treatment.1 In
developing countries, a large number of children <5 years
of age are exposed to multiple risk factors such as poverty,
malnutrition, health problems and an environment with
poor stimulation, which affects their cognitive, motor and
socioemotional development.2 It has been observed that
children who receive early long-term intervention had improvement in IQ, better school performance, lower crime
Dirección de Investigación, Hospital Infantil de México Federico
Gómez, México, D.F., México
Correspondence: Dra. Beatriz Romo Pardo
Dirección de Investigación
Hospital Infantil de México Federico Gómez
México, D.F., México
E-mail: [email protected]
Received for publication: 10-3-12
Accepted for publication: 10-26-12
Vol. 69, November-December 2012
rate and, during adulthood, a greater chance of obtaining
employment and higher incomes compared to those who
did not receive early intervention.3
To identify alterations in neurodevelopment, the American Academy of Pediatrics (AAP) suggests continuous
surveillance and monitoring of development, taking into
account risk factors, both biological and environmental,
as well as the concerns of parents about their child’s development at each follow-up visit. Another recommendation
is the systematic application of screening tests in key
moments of development, i.e., at 9, 18 and 30 months of
age.1 Several studies have shown that the pediatrician’s
clinical judgment is not sufficient to identify neurodevelopmental delays. From this time, the importance of using
standardized screening tools to detect these patients was
emphasized.4,5
A screening test identifies individuals suspected to
be ill in an apparently healthy population, establishes
the risk or suspicion of a developmental problem but
does not define a diagnosis. It should be easy and quick
to implement, economically viable, reliable and valid
(sensitivity and specificity >0.70).4 The usefulness of a
541
Beatriz Romo-Pardo, Silvia Liendo-Vallejos, Guillermo Vargas-López, Antonio Rizzoli-Córdoba, Guillermo Buenrostro-Márquez
test must be preceded by a concurrent validation process,
which seeks to understand the extent to which the test
results coincide with diagnostic evaluations commonly
used (gold standard).6,7
Having solid evidence on the neurodevelopmental
screening tests is to facilitate understanding of their
advantages and disadvantages as an assessment tool. In
order to have a better knowledge about the effectiveness
and accuracy of screening tests in children as well as to
provide useful information about these tools based on wellfounded evidence, we conducted a systematic review of
the literature on the validation of the screening tests in the
U.S. and Latin America designed to detect developmental
problems in children <5 years of age.
SUBJECTS AND METHODS
For inclusion and exclusion criteria, we conducted a systematic search and review of the literature on validation
studies of screening tests of global neurodevelopment of
children <5 years of age in the U.S. and Latin America,
from 1980 until February 14, 2012, in English and Spanish.
Editorials and conference papers were excluded from the
review articles.
Studies were identified by a search of electronic databases and bibliographies of the articles retrieved. This
search was conducted in MEDLINE/PubMed, LILACS
and Artemisa. The search was limited to studies in English
or Spanish that were conducted in humans, in children <5
years of age, in the U.S. and Latin America, and classified
according to the category of validation studies.
The following sets of terms were combined in the
search:
1. For illness: developmental delay
2. For study types: screening
3. For outcome: psychometric properties, sensitivity,
specificity
4. For personnel administering screening in primary
care: general practitioner.
Below are examples of the search strategies of the
different combinations of terms in PubMed/MEDLINE:
• Strategy 1: 184 articles
("diagnosis"[Subheading] OR "diagnosis"[All
Fields] OR "screening"[All Fields] OR "mass
screening"[MeSH Terms] OR ("mass"[All Fields] AND
"screening"[All Fields]) OR "mass screening"[All
542
Fields] OR "screening"[All Fields] AND ("sensitivity
and specificity"[MeSH Terms] OR ("sensitivity"[All
Fields] AND "specificity"[All Fields]) OR "sensitivity
and specificity"[All Fields] OR "sensitivity"[All Fields])
AND (developmental[All Fields] AND delay[All Fields])
• Strategy 2: 154 items, 143 items + 11 included in
strategy 1
("diagnosis"[Subheading] OR "diagnosis"[All
Fields] OR "screening"[All Fields] OR "mass
screening"[MeSH Terms] OR ("mass"[All Fields] AND
"screening"[All Fields]) OR "mass screening"[All
Fields] OR "screening"[All Fields] AND ("sensitivity
and specificity"[MeSH Terms] OR ("sensitivity"[All
Fields] AND "specificity"[All Fields]) OR "sensitivity
and specificity"[All Fields] OR "sensitivity"[All Fields])
AND (developmental[All Fields] AND delay[All Fields])
• Strategy 3: 74 articles; 53 articles + 21 included in
strategies 1 and 2
("diagnosis"[Subheading] OR "diagnosis"[All Fields]
OR "screening"[All Fields] OR "mass screening"[MeSH
Terms] OR ("mass"[All Fields] AND "screening"[All
Fields]) OR "mass screening"[All Fields] OR
"screening"[All Fields] AND ("primary health care"[MeSH
Terms] OR ("primary"[All Fields] AND "health"[All
Fields] AND "care"[All Fields]) OR "primary health
care"[All Fields] OR ("primary"[All Fields] AND
"care"[All Fields]) OR "primary care"[All Fields]) AND
(developmental[All Fields] AND delay[All Fields])
• Strategy 4: 47 articles; 36 articles + 11 included
in strategies 1, 2 and 3 ("diagnosis"[Subheading] OR
"diagnosis"[All Fields] OR "screening"[All Fields]
OR "mass screening"[MeSH Terms] OR ("mass"[All
Fields] AND "screening"[All Fields]) OR "mass
screening"[All Fields] OR "screening"[All Fields] AND
("psychometrics"[MeSH Terms] OR "psychometrics"[All
Fields] OR "psychometric"[All Fields]) AND
(developmental[All Fields] AND delay[All Fields]) AND
((English[lang] OR Spanish[lang]) AND ("infant"[MeSH
Terms] OR "child, preschool"[MeSH Terms]))
• Strategy 5: 12 articles; 9 articles + 3 included in strategy
3 ("diagnosis"[Subheading] OR "diagnosis"[All Fields] OR
"screening"[All Fields] OR "mass screening"[MeSH Terms]
Bol Med Hosp Infant Mex
Global neurodevelopmental screening tests for children <5 years of age in the United States and Latin America:
a systematic review and comparative analysis
OR ("mass"[All Fields] AND "screening"[All Fields])
OR "mass screening"[All Fields] OR "screening"[All
Fields] AND ("general practitioners"[MeSH Terms] OR
("general"[All Fields] AND "practitioners"[All Fields])
OR "general practitioners"[All Fields] OR ("general"[All
Fields] AND "physician"[All Fields]) OR "general
physician"[All Fields]) AND (developmental) [All Fields]
AND delay[All Fields]).
Evaluation of the choice of included articles was
done openly and independently by two reviewers. Disagreements were resolved by consensus. We developed a
data uptake sheet based on data extraction template user
group communication and Cochrane reviews. Evidence of
global neurodevelopmental screening was based on those
articles that assessed multiple domains of development
(e.g., motor, cognitive, adaptive, communication, etc.).
We excluded those tests that focused on a single area of
development or those directed at the diagnosis of a disease
or to evaluate academic areas. Information obtained from
each test was as follows: 1) test characteristics (name,
country of origin, authors, mode of evaluation, domain
of development, age range in which it is applied, rating
system, criteria of normality and abnormality and evaluation time), 2) diagnostic test used for its validation, and
3) validation of results.
RESULTS
With regard to the results of the systematic review in
the different search strategies we found a total of 454
articles; 19 articles were included that described 13
neurodevelopmental screening tests (Figure 1). These
19 articles selected were diverse studies (validation as
well as systematic reviews) of the neurodevelopment
screening tests published on the American continent.
We used those written in English or Spanish. Of the
13 tests found, those that had the greatest number of
publications were Ages and Stages Questionnaires (five
articles) and CAT/CLAMS (three articles). The oldest
study included was from 1986 of the screening test CAT/
CLAMS. A total of 9217 children <8 years of age were
included in the different validation test studies carried
out in Argentina, Canada, Chile, Costa Rica, Cuba and
the U.S. It is interesting to mention that in the systematic
review only one article was found on the psychometric
Vol. 69, November-December 2012
characteristics of a screening test in a Mexican population. This was a standardization study of the Denver I
test in 288 children from 2–54 weeks of age where the
motor scale of the Bayley test was also used. The Denver
I scale failed to identify as suspicious 16/17 children
identified by the Bayley test. The study was considered
to be unsatisfactory and in practice the results were not
used as Mexican standards. At present we use the second
Denver version, so it was decided to not include this
article in the systematic review.
According to their method of administration, the selected screening tests can be categorized into two major
groups: direct observation or evaluation (done by the physician to the child) and parent questionnaires (which can be
applied by any members of the health care team). There are
tests that utilize both resources in which questions are asked of the parents and the child is also observed. The items
that evaluate each test are distributed in different areas of
development. Although there is considerable homogeneity
in the grouping of motor or language milestones, in the
domains of adaptive and social behavior they are distributed differently in the various tests. The different screening
tests found are described, with mention of their authors,
country of origin, mode of administration, domains of
development for evaluation, time of administration and
available languages (Table 1).
Rating systems vary among the different tests. The total
score is generally obtained from the individual scores of
the items. These, in turn, are derived from the parental
responses to the survey questions (i.e., Ages & Stages
Questionnaires) or the score given by the physician to the
child’s performance (Battelle Developmental Inventory).
In general, screening tests qualify the child as normal—or
as suspicious for—or at risk for developing problems.
Table 2 shows the rating method and criteria of normality
and abnormality for each test.
The efficiency of detection measurements are reported
in the validation studies. The concept of validity refers
to how well a tool measures what it purports to measure.
For concurrent validation of the screening tests, different diagnostic tools have been used such as the Battelle
Developmental Inventory, Bayley Scales of Infant Development, preschool and primary Wechsler Scale (Wechsler
Preschool and Primary Scale or Intelligence), among
others. We examined both the criterion and predictive
validity.
543
Beatriz Romo-Pardo, Silvia Liendo-Vallejos, Guillermo Vargas-López, Antonio Rizzoli-Córdoba, Guillermo Buenrostro-Márquez
Citations found in the
search of
PubMED/Medline
Citations found in the
search of LILACS
Citations found in the
Artemisa search
n=425
n=19
n=0
Citations found in the
bibliographic search of
citations of PubMED/Medline
and LILACS
n=10
Total de Artículos
n=454
Articles excluded during the
title/abstract stage
n=435
Specific pathology
Specific group
Review
Specific area of development
Prognostic
No validation
Other type of study
Experimental
Epidemiological
Other type of study
Animal model
Clinical guidelines
Case report
167
50
48
39
33
31
23
14
13
8
6
2
1
Articles revised in extenso included
n=19
Figure 1. Flow chart of the results of the systematic review
Criterion Validity
Criterion validity is a type of concurrent validity that
establishes the validity of a measuring instrument by
comparing it with some external criterion. The sensitivity
shows how well a test correctly identifies children with
delays, whereas specificity indicates the degree to which
a test detects those without delay. Some tests resulted to
be a poor screening tool for identifying children with neurodevelopmental delay because they showed a sensitivity
of 0.50, such as the test of Child Development Inventory
(CDI) or were unable to differentiate those with normal
neurodevelopment compared with those that are abnormal,
with a specificity of 0.43 to 0.80, such as the Denver test. In
contrast, other studies proved to be useful tools in assessing
neurodevelopment after maintaining a high sensitivity and
specificity such as the Battelle Developmental Inventory
544
Screening (2nd edition) with a sensitivity of 0.93 and
specificity of 0.88.
Predictive Validity
Predictive validity is a type of concurrent validity referring
to the ability of a test to predict or correlate with another
of the same construct. We found eight predictive validity
studies. The predictive value was poorer for Ages & Stages
Questionnaires with positive predictive value 0.34 (PPV)
and negative predictive value (NPV) 0.71, whereas the
best predictive validity test was PRUNAPE with PPV of
0.94 and NPV of 0.97 (Table 3). Each neurodevelopmental
screening test selected for this review has advantages and
disadvantages in terms of method and time of application,
materials and features of the validation study. We have
summarized the strengths and weaknesses of each of the
Bol Med Hosp Infant Mex
Global neurodevelopmental screening tests for children <5 years of age in the United States and Latin America:
a systematic review and comparative analysis
Table 1. General description of the screening tests according to the method of administration, age range, time of administration and
available languages
Test name
Country of origin
Authors
Age range
(months)
Time
Language
Ages & Stages Questionnaires Parent questionnaires Communication, fine and
3th ed.
gross motor skills, pro(EUA)
blem resolution, language,
Squires, et al, 19958
personal- social
Squires, et al, 20099
4-60
10-15 min
English, Spanish, French and
Korean
Battelle Developmental Inventory (BDI) Screening Test
2nd ed.
(EUA)
Newborg J, 200512
0-95
10-30 min
English and
Spanish
Method of evaluation
Developmental areas
evaluated
Direct observation of Personal-social, adaptive,
the child and parent motor, communication and
questionnaires
cognition
Bayley Scales of Infant and
Toddler Development (BSID)
Neurodevelopment
Screening Test
3rd ed.
(EUA)
Aylward G, 201013
Direct observation of
the child
Cognition, language and
motor
1-42
15-25 min
English
Brigance Early Childhood
Screen
(EUA)
Glascoe F, 200214
CAT/CLAMS Clinical Adaptative Test/Clinical Linguistic and
Auditory Milestone Scale
(EUA)
Capute, et al, 198615
Direct observation of
the child and parent
questionnaires
Cognition, language, motor, adaptive and socioemotional
0-35
36-60
10-15 min
English and
Spanish
Direct observation of
child
Language, problem resolution and motor skills
1-36
10-15 min
English and
Spanish
Child Development Inventory
(EUA)
Doig, et al, 199916
Direct observation of
child
Social, language, motor,
adaptive, reading and
arithmetic skills
15-72
30-50 min
English
Denver Development Screening Test
(EUA)
Glascoe, et al, 199217
Direct evaluation
of child and parent
questionnaires
Gross and fine motor
skills, language, adaptive,
personal-social
0-72
10-20 min
English and
Spanish
Escala de Evaluación del
Direct evaluation of
Desarrollo Psicomotor (EEDP) child
(Chile)
Schapira, 200718
Bedregal, 200819
Vericat Ay Orden, 201020
Social, language, coordination and motor skills
0-24
20 min
Spanish
Escala de Desarrollo Integral
del Niño (EDIN)
(Costa Rica)
Schapira, 200718
Vericat Orden, 201020
Neurodesarrollo Pediátrico
(NPED)
(Cuba)
Guadarrama-Celaya, et al,
201121
Direct evaluation of
child
Fine and gross motor
skills, reflexes, socioemotional and cognition
0-72
NR
Spanish
Direct evaluation of
the child
Language/communication,
psychomotor and sensory
maturation (hearing/
vision)
1-60
15 min
Spanish
Vol. 69, November-December 2012
545
Beatriz Romo-Pardo, Silvia Liendo-Vallejos, Guillermo Vargas-López, Antonio Rizzoli-Córdoba, Guillermo Buenrostro-Márquez
Table 1. General description of the screening tests according to the method of administration, age range, time of administration and
available languages
Test name
Country of origin
Authors
Method of evaluation
Developmental areas
evaluated
Age range
(months)
Time
Language
PEDS Parents Evaluation of
Developmental Status
(EUA)
Glascoe, 1998
Parent questionnaires that ask about
concerns
Global development/cognitive, expressive language, receptive language,
behavior, socioemotional,
schooling, self-help, fine
and gross motor skills
and others (sensory and
medical concerns)
0-96
2-5 min
English and
Spanish
PRUNAPE
(Argentina)
Pascucci, et al, 200222; 200623
Direct evaluation of
the child and some
questions for the
parents
Fine and gross motor
skills, personal-social and
language
0-60
10-15 min
Spanish
Test de desarrollo Psicomotor
TEPSI
(Chile)
Haeussler, Marchant, 1980
Direct evaluation of
the child
Coordination, motor skills
and language
24-60
15-20 min
Spanish
tests as well as offering some comments on the validation
process (Table 4).
DISCUSSION
Recommendations on the systematic application of neurodevelopmental screening tests suggested by the AAP
have led to an increasing demand for tests with solid
evidence, reliability, usefulness, validity, specificity
and sensitivity. Awareness of the available evidence on
these tools leads to well-founded decision-making by
physicians. It is useful to know how an investigation on
a research instrument was carried out and if it has the
ability to support its use. Although some tests have a large
number of investigations, it does not necessarily mean
that these are optimal or more stringent for detecting
developmental delays.
No evidence was found to justify using one application
method over another (direct observation, parental questionnaire or mixed) because what matters in a screening
test is its scientific basis and methodology of the validation
study. For example, in the study of Rydz et al., it was found
that the Child Development Inventory has a low sensitivity
compared to other studies. Only 5/31 children failed the
Battelle Developmental Inventory (comparison) and it
would be necessary to analyze a larger sample.
546
Regarding the rating scales, there are quantitative scoring systems (with a scoring system per item) or qualitative
scoring systems (with a categorical classification as failed/
passed, present/absent, yes/no, etc.). No tendency was
found for increased reliability with respect to a scoring
method in different screening tests included in this study
because, for example, PRUNAPE and the Battelle have
different rating systems. However, they were the two tests
found with better sensitivity and specificity.
With regard to studies included in this review, it
was found that very few meet the optimal conditions to
support its reliability, validity and usefulness because
some are limited in terms of design. Few studies use a
quasi-experimental design or randomized assignment,
resulting in being one of the main problems for its reliability. Furthermore, accuracy in the administration of the
test is crucial, although there are limitations in both test
knowledge and experience of the person who administers
it, as well as the time and place where it is administered. This causes a variability in the results as important
as having a sensitivity of 0.67–0.90 and specificity of
0.39–0.95, as in the case of Ages & Stages Questionnaires studies where, in some cases, the questionnaire was
administered to parents in the waiting room, with a time
of 15 min, and others were sent home, allowing time for
greater trust in the results.
Bol Med Hosp Infant Mex
Global neurodevelopmental screening tests for children <5 years of age in the United States and Latin America:
a systematic review and comparative analysis
Table 2. Qualification method and criteria of normality and abnormality of the screening tests included in the systematic review
Screening test
Qualification system
Criteria of normality and abnormality
Ages & Stages
Questionnaires
(EUA)
Questions for parents with option of responses:
yes, sometimes, or no
Giving a score of 0 for no, 5 for sometimes and 10
for yes
Evaluating the concerns of parents with yes or no
answers
Divided into three categories (higher than cut-off
point, close to cut-off point and below the cut-off point)
Battelle
Developmental Inventory
Screening 2nd ed
(EUA)
There are 100 items (20 of each area of develop- Abnormality:
ment: motor, communication, cognition, adaptive
and social behavior). Scores of 0, 1 and 2 in each < -1 SD and > -1.5 SD: borderline. Refer child for
one reflect the level of acquisition of skills
further evaluation with BDI-2
Cut-off point is between 1.5 and 2 SD
With this, determination of the possibility of a subsequent value
< -1.5 SD and > -2.0 SD: clear indication for referral. Administer BDI-2 to determine specific areas of
deficiency
< -2.0 SD: clear indication of serious developmental
problems. Administer BDI-2 and determine the origin
and extent of deficit
Bayley Scale of Infant and
Toddler Development Screening Test
(EUA)
Qualification of four areas (basic/intact neuroTwo cut-off points divided into three risk categories:
logical function, receptive functions, expressive
mild, moderate and severe
functions and cognitive process) with qualification
options 1 (optimal) and 2 (not optimal)
No total development score, only for each of the four
areas evaluated
Brigance Screens-II
(EUA)
Results based on the criteria of the examiner
Without established criteria for classification
CAT/CLAMS
(EUA)
Two domains: communication and problem
resolution
Items organized according to age group with
scores (0.3-1.5)
Total score according to area tested and general
test score
Establishes baseline age, ceiling equivalent age and
developmental quotient
Child Development Inventory
(EUA)
Eight areas quantified by parents with options of
yes or no for response
Classification according to three groups:
Normal limits, borderline <1.5 SD and with developmental delay <2 SD
DENVER-II
(EUA)
Items administered to child or according to information obtained by parents in accordance with
age line
Each item was quantified using success, failure or
rejection
Normal: skills appropriate for age (1 failure by area)
Suspicion: failure to perform skills carried out by 7590% of children their age (>2 failures in two areas
Delay: failure to carry out activities compared to >90%
of children their age
EEDP Escala de Evaluación Items administered to child.
del Desarrollo Psicomotor
Score 0 = failure, 1 or 2 = passing
(Chile)
NPED Neurodesarrollo
Pediátrico (Cuba)
Cut-off point, development quotient <70: developmental delay
Sum and cut-off point. Establishment of categories:
normal, risk, delay
Computerized evaluation instrument for nurses to Reported as: normal, overall failure or by areas
answer
Parents Evaluation of Deve- The parent responds: yes, no and somewhat
lopmental Status
Answer questions in regard to concerns about
(EUA)
overall development, expressive and receptive
language, fine and gross motor skills, behavior
and social interests
Vol. 69, November-December 2012
Classification according to three risk categories of
developmental delay: slight, moderate and severe
547
Beatriz Romo-Pardo, Silvia Liendo-Vallejos, Guillermo Vargas-López, Antonio Rizzoli-Córdoba, Guillermo Buenrostro-Márquez
Table 2. Qualification method and criteria of normality and abnormality of the screening tests included in the systematic review
Screening test
Screening test
Criteria of normality and abnormality
PRUNAPE
(Argentina)
Guidelines are given to the child and questions to
parents are ​​according to child’s age line. Each
pattern is described as pass (if criteria are met) or
failure (if not met)
Type A patterns are completely to the left of the
age. Type B patterns cross the age line at the 7590% percentile
Passes the test if meets all type A patterns and fails
when not meeting one type B pattern
The child is described as suspect or at risk with failure
on one type A pattern or two type B patterns
TEPSI Test de evaluación
del desarrollo psicomotriz
Evaluation of the child with items that can be quali- Sum and cut-off point. Establish categories: normal,
fied with scores 0, 1 and 2
risk, delay
Table 3. Comparison of screening tests designed and validated according to the results of the systematic literature review
Diagnostic test used for comparison
Validation results
Ages & Stages Questionnaires (EUA)
Squires & Bricker, 1997
BSID
SBIS
MSCA
S=0.70-0.90
Sp=0.76-0.91
PPV=0.45
Ages & Stages Questionnaires (EUA)
BSID
WPPSI-III
VABS
PLS-IV
S = 0.82
Sp = 0.78
PPV = 0.30 (>1 domain) and 0.48
(>2 domains)
NPV = 0.97 (>1 domain) and 0.94
(>2 domains)
BDI-2
S=0.67
Sp=0.39
PPV=0.34
NPV=0.71
BDI Battelle Developmental Inventory
Screening 2nd edition (EUA)
Newborg J, 2005
BDI-2
S=0.72-0.93
Sp=0.79-0.88
BSID Bayley Infant Neurodevelopmental
Screen (EUA)
Aylward GP, 2005
BSID
S=0.61-0.80
Sp=0.81-0.90
Multidisciplinary panel of specialists:
pediatricians, nurses, teachers and
developmental psychologists
Parental report
BSID
S=0.76-0.77
Sp=0.85-0.86
Validation test
Limbos MM, Joyce DP; 2011
Ages & Stages Questionnaires (Canada)
Rydz, 2006
Brigance Screens-II
Glascoe FP, 2002
CAT/CLAMS
Capute, 1986
CDI Child Development Inventory (EUA)
Doig, et al, 1999
CDI Child Development Inventory
Rydz, et al, 2006
548
CAT/CLAMS and BSID
BDI
S=0.21- 0.66
Sp=0.79-0.95
PPV=0.80
NPV=0.65
S=0.70-0.80
Sp=0.70-0.80
S=0.50
Sp=0.86
Bol Med Hosp Infant Mex
Global neurodevelopmental screening tests for children <5 years of age in the United States and Latin America:
a systematic review and comparative analysis
Table 3. Comparison of screening tests designed and validated according to the results of the systematic literature review
Validation test
DENVER-II
(EUA)
Glascoe, et al, 1992
EDIN Integral Child Evaluation Scale
(Costa Rica)
Schapira, 2007
Vericat, 2010
EEDP Evaluation Scale of Psychomotor
Development (Chile)
Schapira, 2007
Bedregal, 2008
Vericat A, 2010
NPED Pediatric Neurodevelopment
(Cuba)
Guadarrama-Celaya et al., 2011
PEDS Parents Evaluation of Developmental Status (EUA)
Glascoe, et al, 2003
Glascoe , 2001
PEDS Parents Evaluation of Development Status (EUA)
Limbos MM, 2011
PRUNAPE (Argentina)
Pascucci MC, 2002 and 2004
TEPSI Psychomotor Development Test
(Chile)
Schapira, 2007
Bedregal P, 2008
Vericat A, 2010
Diagnostic test used for comparison
Validation results
BSID
KABC
SBIS
VABS
No validation data available
S=0.56-0.83
Sp=0.43- 0.80
PPV=0.37
Low S and Sp in children of 4 months
PPV in children >4 months: 97-100%
No validation data found
No detailed validation data found
S=0.95
Sp=0.86
Development of the child was measured
using a standard test package by psychology
graduate psychologists blindly, either with
regard to the concerns of the parents or to
their relevance
S=0.74-0.79
Sp=0.70-0.80
BSID
WPPSI-III
VABS
PLS-IV
S = 0.74
Sp = 0.64
PPV = 0.19 (>1 concern) and 0.30
(>2 concerns)
NPV = 0.96 (>1 concern) and 0.93
(>2 concerns)
BSID
WISC
Terman
VABS
Gardner test
EN
Psychiatric clinical evaluation
EA
Tonal audiometry
BAEP
S=0.80
Sp=0.93
PPV=0.94
NPV=0.97
No published validation studies found
BSID, Bayley Scales of Infant Development; SBIS, Stanford Binet Intelligence Scales; MSCA, McCarthy Scales of Children’s Abilities; BDI-2,
Battelle Development Inventory-2; WPPSI-III, Wechsler Preschool and Primary Scale of Intelligence; KABC, Kaufman Assessment Battery
for Children; VABS, Vineland Adaptive Behavior Scale; PLS-IV, Preschool Language Scale–Fourth Edition; WISC, Wechsler Intelligence
Scale for Children; OE, otoacoustic emissions; BAEP, brainstem auditory-evoked potentials; NE, neurological examination; S, sensitivity;
Sp, specificity; PPV, positive predictive value; NPV, negative predictive value.
Vol. 69, November-December 2012
549
Beatriz Romo-Pardo, Silvia Liendo-Vallejos, Guillermo Vargas-López, Antonio Rizzoli-Córdoba, Guillermo Buenrostro-Márquez
Table 4. Advantages and disadvantages of screening tests according to the literature
Screening test
Advantages
Ages & Stages
Questionnaires
(USA)
Squires & Bricker, 1997
Limbos MM, 2011
Rydz, 2006
Can be resolved by the parents No direct observation of the
at home or in the waiting room child by experienced health
(recommended to be sent home) personnel
Application is short and quickly
quantified Material support for
parents
Battelle
Developmental Inventory
Screening 2nd ed.
(EUA)
Newborg J, 2005
Requires minimal training
Low sensitivity (0.64-0.67) Three cut-off points used with a wide
Training materials
and specificity (0.74- 0.76) for sample of children
High sensitivity and specificity for motor skills
the area of communication
Can be modified for children with
disabilities
Bayley Scale of Infant and Helpful materials
Toddler Development Scree- Is short term
ning Test
(EUA)
Aylward GP, 2005
Disadvantages
Observations
Sensitivity and specificity show much
variation between one study and
another. Sensitivity is from 0.67-0.82
and a specificity as low as 0.39.
Personnel required who can Validation study was carried out with
evaluate muscle tone and basic a significant sample of 600 cases,
neurological functions
correcting the age and with three
cut-off points
Brigance Screens-II
Glascoe FP, 2005
Short term
Cannot account for material In the study, cut-off points cannot be
Can be answered by parents, help
explained
by direct observation or by both
methods
In waiting rooms or schools
CAT/CLAMS
Capute, 1986
Short duration
Good material help
Is quantitative, establishes
developmental age
Child Development Inventory
(EUA)
Doig, et al, 1999
Rydz, et al, 2006
Short time of application
No helpful materials
Sensitivity and specificity are not Total of 300 questions and can
changed depending on the so- last 30 min
cioeconomic level of the parents
Validation study carried out for open
and at-risk population
Is the unique study evaluating 36 patients comparing them with the “gold
standard” (Battelle)
DENVER-II
Glascoe, et al, 1992
Ease of application
Low sensitivity and specificity
Does not require intensive training Evaluation time of 30 min
The study sample was subject to only
104 children, of whom very few were
<24 months of age
Despite re-standardization and using
different combinations of scoring
methods, lacks adequate sensitivity
and specificity
Integral Developmental Child Adequate psychometric properties
Scale (Costa Rica)
Observations at different socioecoVericat A, 2010
nomic levels
EEDP Escala de Evaluación Ease of application
del Desarrollo Psicomotor
Can be carried out by
(Chile)
nonspecialized personnel
Bedregal P, 2008
Vericat A, 2010
550
Considers only two developmental areas (communication
and problem resolution)
No published validation data found
for this test
Does not encompass all areas Validation studies not available in the
of development
literature
Bol Med Hosp Infant Mex
Global neurodevelopmental screening tests for children <5 years of age in the United States and Latin America:
a systematic review and comparative analysis
Table 4. Advantages and disadvantages of screening tests according to the literature
Screening test
Advantages
Disadvantages
Pediatric Neuroevelopment
(Cuba)
Guadarrama-Celaya, 2011
High sensitivity and specificity
Can be carried out by nurses
without requirement of extensive
complicated training
Short duration
Necessary to have a computer No reports of psychometric characteand training may be necessary ristics of the test
to manage software with difficult application
Parents Evaluation of Developmental Status
(EUA)
Glascoe, et al, 2003
Glascoe, 2001
Limbos MM, Joyce DP; 2011
Based on discussions with parents Requires an experienced evaabout their concerns of child de- luator to obtain adequate invelopment
formation
With an experienced evaluator,
highly valid information can be
obtained
Requires short time of administration
In the study by Limbos MM and Joyce
DP, it was determined that very low
specificity leads to over-referrals (1/3
children did not require evaluation)
PRUNAPE (Argentina)
Pascucci MC, 2002 y 2004
Design similar to Denver that
allows quick organization of the
evaluator about guidelines to be
administered
Helpful materials
Brief time of administration
Test is validated with 78 guidelines
The “father/mother-specific
pattern was incorporated after
the validation process
For validation, the study is significant
with 839 children
Uses diagnostic tests for validation,
and evaluations by hearing and vision
specialists
Test de desarrollo Psicomotor
(Chile)
Bedregal P, 2008
Vericat A, 2010
Well-designed
Can be used by pre-school
teachers
Has a version for the blind
Does not evaluate all develop- No published validation data available
mental areas
Sample size in some studies is not sufficient. It is particularly problematic when calculating the specificity and
sensitivity of the test because the number of patients with
a developmental alteration may be limited. In other cases,
the problem is that it does not include a similar number
of patients by age group, as in the Denver case where, in
addition to a small sample (104 subjects), very few were
<24 months of age.
It is critical to determine suitable cut-off points to calibrate the tool in order to obtain accurate results. Those tests
that have low specificity produce large numbers of false
positives that may result in diagnostic over-reporting. The
opposite problem leads to not refer and to not detect those
children with a developmental problem and, therefore,
to not intervene early. On the basis of the results observed, it is concluded that between the period of 1980 and
2012, which includes the systematic review, we found 13
neurodevelopmental screening tests in the U.S. and Latin
America for use in children <5 years of age.
Battelle Development Inventory Screening and PRUNAPE were the two screening tests that had the greatest
sensitivity and specificity in the validity criteria. It should
be noted that the evidence of its validation offered by the
Vol. 69, November-December 2012
Observations
publications is of high methodological quality, which
confirms that they are reliable tools for detection of neurodevelopmental alterations.
Although there are different methods of administration,
scoring and criteria of normality and abnormality, there
was no scientific evidence to support either of the test
systems because what matters is the scientific basis on
which the validation test is performed.
Of the screening tests included, we found no validation
study in Mexico. Therefore, we believe it to be of utmost
importance to have a valid tool, preferable for our own
country, in order to be applied to our own population
and to use it to implement early interventions in a directed, systematic manner with a scientific foundation.
This is in order to achieve the maximum potential of
developing—and avoiding—the causal factors of intergenerational poverty.
REFERENCES
1.
Council on Children With Disabilities; Section on Developmental Behavioral Pediatrics; Bright Futures Steering Committee;
Medical Home Initiatives for Children With Special Needs
551
Beatriz Romo-Pardo, Silvia Liendo-Vallejos, Guillermo Vargas-López, Antonio Rizzoli-Córdoba, Guillermo Buenrostro-Márquez
Project Advisory Committee. Identifying infants and young
children with developmental disorders in the medical home:
an algorithm for developmental surveillance and screening.
Pediatrics 2006;118:405-420.
2. Grantham-McGregor S, Cheung YB, Cueto S, Glewwe P,
Ritcher L, Strupp B, et al. Developmental potential in the
first 5 years for children in developing countries. Lancet
2007;369:60-70.
3. Hamilton S. Screening for developmental delay: reliable, easyto-use tools. J Fam Pract 2006;55:415-422.
4. Rydz D, Srour M, Oskoui M, Marget N, Shiller M, Birnbaum
R, et al. Screening for developmental delay in the setting of a
community pediatric clinic: a prospective assessment of parent-report questionnaires. Pediatrics 2006;118:e1178-e1186.
5. Mackrides PS, Ryherd SJ. Screening for developmental delay.
Am Fam Physician 2011;84:544-5499.
6. Rydz D, Shevell MI, Majnemer A, Oskoui M. Developmental
screening. J Child Neurol 2005;20:4-21.
7. Glen P Aylward, T. S. Measurement and psychometric considerations. In: Wolraich ML, Drotar DD, Dworkin PH, Perrin
EC, eds. Developmental-Behavioral Pediatrics: Evidence and
Practice. Philladelphia: Mosby Elsevier; 2008. pp. 123-201.
8. Squires J, Bricker D, Potter L. Revision of a parent-completed
developmental screening tool: Ages and Stages Questionnaires. J Pediatr Psychol 1997;22:313-328.
9. Squires J, Twombly E, Bricker D, Potter L. ASQ-3™ User’s
Guide. Baltimore, MD: Paul H. Brookes Publishing Co.; 2009.
10. Schonhaut BL, Salinas AP, Armijo RI, Schönstedt GM, Álvarez
LJ, Manríquez OM. Validación de un cuestionario autoadministrado para la evaluación del desarrollo psicomotor. Rev Chil
Pediatr 2009;80:513-519.
11. Limbos MM, Joyce DP. Comparison of the ASQ and PEDS in
screening for developmental delay in children presenting for
primary care. J Dev Behav Pediatr 2011;32:499-511.
12. Newborg J. Development and standardization. In: Newborg
J, ed. Battelle Developmental Inventory. Itaska, IL: Riverside
Publishing; 2004. pp. 95-148.
552
13. Aylward GP. The Bayley Infant Neurodevelopmental Screener (BINS): different test and different purpose. In: Weiss
LG, Oakland T, Aylward G, eds. Bayley III Clinical Use and
Interpretation. New York: Academic Press; 2010. pp. 201-233.
14. Glascoe FP. The Brigance Infant and Toddler Screen: standardization and validation. J Dev Behav Pediatr 2002;23:145-150.
15. Capute AJ, Shapiro BK, Watchel RC, Gunther VA, Palmer FB.
The Clinical Linguistic and Auditory Milestone Scale (CLAMS).
Identification of cognitive defects in motor-delayed children.
Am J Dis Child 1986;140:694-698.
16. Doig KB, Macias MM, Saylor CF, Craver JR, Ingram PE.
The Child Development Inventory: a developmental outcome measure for follow-up of the high-risk infant. J Pediatr
1999;135:358-362.
17. Glascoe FP, Byrne KE, Ashford LG, Johnson KL, Chang B,
Strickland B. Accuracy of the Denver-II in developmental
screening. Pediatrics 1992;89:1221-1225.
18. Schapira IT. Comentarios y aportes sobre desarrollo e inteligencia sensorio-motriz en lactantes. Análisis de herramientas
de evaluación de uso frecuente. Actualización bibliográfica.
Rev Hosp Mat Infant Ramón Sardá 2007;26:21-27.
19. Bedregal P. Instrumentos de medición del desarrollo en Chile.
Rev Chil Pediatr 2008;79(suppl 1):32-36.
20. Vericat A, Orden AB. Herramientas de screening del desarrollo
psicomotor en América. Rev Chil Pediatr 2010;81:391-401.
21. Guadarrama-Celaya F, Otero-Ojeda GA, Pliego-Rivero B,
Porcayo-Mercado MR, Garcell JR, Pérez-Ábalo MC. Screening
of neurodevelopmental delays in four communities of Mexico
and Cuba. Public Health Nurs 2012;29:105-115.
22. Pascucci MC, Lejarraga H, Kelmansky D, Álvarez M, Boullón
M, Breiter P, et al. Validación de la prueba nacional de pesquisa
de trastornos de desarrollo psicomotor en niños menores de
6 años. Arch Argen Pediatr 2002;100:374-384.
23. Pascucci MC, Lejarraga H, Kelmansky D, Álvarez M, Boullón
M, Breiter P, et al. Validación de la prueba nacional de pesquisa
de trastornos de desarrollo psicomotor en niños menores de
6 años. Arch Pediatr Urug 2004;75:79-90.
Bol Med Hosp Infant Mex
Bol Med Hosp Infant Mex 2012;69(6):553-563
Research article
Risk factors and consequences of cyberbullying in teenagers: association
with bullying
Gerardo García-Maldonado,1,2 Gerardo Jesús Martínez-Salazar,2 Atenógenes H. Saldívar-González,2
Rafael Sánchez-Nuncio,2 Gerardo Manuel Martínez-Perales,1 María del Carmen Barrientos-Gómez2
ABSTRACT
Background. Cyberbullying (CB) uses electronic tools to intimidate. We undertook this study to determine the prevalence of CB and to
identify its characteristics. We explored the association with bullying and analyzed consequences and risk factors.
Methods. Junior-high-school students were included. CB was used as exposure and outcome variable. Nonparametric statistics and
logistic regression were applied.
Results. Six hundred three students with a mean age of 13.4 years (±0.98 years) were included. Cybervictims were more prevalent. The
cell phone was the most common tool used to intimidate. The most important risk factor for cybervictims was “feeling unsafe at school” (c2
= 6.485, p = 0.011, OR = 4.1, 95% CI 1.30-11.2); for cyberaggressors it was “to use the computer hidden from parents and late at night” (c2
= 14.584, p <0.05, OR = 4.2, 95% CI 2.10-16.30); for cybervictims–cyberaggressors it was “to be female” (c2 = 2.891, p >0.05, OR = 3.50,
95% CI 1.70-16.80). The strongest association with bullying was shown for males and between traditional victim–aggressor and cyberaggressor roles (c2 = 28.821, p <0.05, OR = 7.37, 95% CI 3.78-14.3). When CB was considered as the exposure variable, the most relevant
outcome measure was “to have headaches” for cyberaggressors (c2 = 15.125, p <0.05, OR = 7.91, 95% CI 2.28-29.6).
Conclusions. The prevalence of CB was less than demonstrated in other studies, but the risk factors and consequences are relevant.
Key words: cyberbullying, risk factors, consequences, bullying.
INTRODUCTION
Cyberbullying (CB)1-3 is defined as continuous intimidation or harassment used by one person (cyberaggressor)
against another (cybervictim) through electronic means
(internet or text messages via cell phone).4 Some cases
have been documented where subjects can simultaneously
1
2
Departamento de Enseñanza e Investigación, Hospital Psiquiátrico de Tampico, Secretaría de Salud, Tampico, Tamaulipas,
Mexico
Departamento de Investigación, Facultad de Medicina de
Tampico Dr. Alberto Romo Caballero, Universidad Autónoma
de Tamaulipas, Tampico, Tamaulipas, Mexico
Correspondence: Dr. Gerardo García Maldonado
Departamento de Enseñanza e Investigación
Hospital Psiquiátrico de Tampico
Secretaría de Salud
Tampico, Tamaulipas, Mexico
E-mail: [email protected]
Received for publication: 6-26-12
Accepted for publication: 10-23-12
Vol. 69, November-December 2012
be cybervictims and cyberaggressors or be concurrently
engaged in traditional bullying.5,6
Unlike the latter, CB invades the privacy of the home of
abused subjects at any time of day or night.6,7 Although it
is more common for high school students to be involved in
this practice,8,9 various reports have shown the participation
of students from other grade levels.9-12
For children at high risk of being cyberintimidated, the
factors involved are using computers for prolonged periods,13-15 having a profile on a social electronic network,16
and being in the age range of 14 to 17 years.13,16,17 Fear of
CB6,13,18 as well as low self-esteem,19-23 depression14,16,17
and loneliness13 are risk factors.
For cyberbullies, the fact that they are frustrated, angry and anxious,24 that their parents underestimate their
aggressive behavior,9.25 or use of the computer for long
periods17,26,27 are important elements.
Gender also appears to have a direct and significant
effect. It has been noted that there is a greater prevalence of females who are cyberbullied and males who are
cyberaggressors.13,14,16 The literature points out some
553
Gerardo García-Maldonado, Gerardo Jesús Martínez-Salazar, Atenógenes H. Saldívar-González, Rafael Sánchez-Nuncio,
Gerardo Manuel Martínez-Perales, María del Carmen Barrientos-Gómez
consequences surrounding this phenomenon: in the case
of cybervictims the presence of low self-esteem, insomnia, enuresis, anxiety, headache and abdominal pain,21,22
emotional alterations (unhappiness and loss of self confidence)28 and academic difficulties have been noted. In the
case of cyberaggressors, behavior disorders and, in extreme cases, criminal behavior are notable,29,30 although the
presence of insomnia, headache, anxiety, lack of empathy,
absenteeism and school suspension are also present.21,22
Another problem at present is the association between
CB and traditional bullying, such that in some countries
this co-occurrence has been studied.29,31-33 Regarding the
use of alcohol and tobacco among those involved in CB,
there are reports that victims of CB do not consume more
alcohol than cyberaggressors.30 As far as tobacco, the unlikelihood that cybervictims smoke as a consequence of
the event has been documented.32,34,35 With regard to CB
and ADHD disorder, there are no studies at this time where
the latter has been analyzed as a risk factor.
The objectives of this study were as follows: 1) to describe the prevalence of CB and traditional bullying in our
study sample; 2) to identify the methods and tools most frequently used for CB and to clarify if there are differences in
terms of gender, document if there are differences between
males and females who are cyberaggressors related to the
gender they preferentially cyberintimidate and also if there
were differences among the victims (males and females)
regarding gender identification of their aggressors, and
finally to establish the presence or absence of fear of cyberintimidation, 3) to explore if in those involved in CB there
is the presence of psychopathological or psychosomatic
manifestations, sleep difficulties and use of alcohol and
tobacco; 4) to explore the relationship of each of the roles
in the CB phenomenon with different variables, adding
traditional bullying which, according to the literature, are
likely associated circumstances and to explore also if CB
is a risk variable for development of some of these; and
5) to determine the index or magnitude of risk.
SUBJECTS AND METHODS
Study Sample
We included students from a morning shift of a high school
located in the town of Tampico, Tamaulipas, Mexico,
enrolled in the school year 2010-2011 and with an age
range of 11-15 years.
554
The total official campus population during that period
was 625 students but because some students were absent
during the study period, the sample was comprised of only
603 adolescents. Included in this study were all students
present during the day of the field work. With regard to
gender, the distribution was 53.4% males and 46.6% females; with respect to school grade 35.7% were in the first
year of high school, 31.3% in the second year and 33% in
the third year. The campus has six groups for each school
year. The project was reviewed and approved by the Ethics
Committee of the institutions that were headquarters for
the researchers after certifying that the facility complied
with the guidelines of the General Health Law regarding
human research for human health in Mexico and with the
principles as published in the Declaration of Helsinki. All
students voluntarily signed an informed consent and their
participation was kept confidential.
Instruments
CB measurement and other variables
At the time of study development, there was no identification of a specific instrument designed and validated in
Mexico for evaluation of CB. In a consensus it was decided that two direct and concrete questions be posed in a
manner similar to those formulated by Sourander et al. in
their study on CB27 where a similar questionnaire was used.
The goal was to establish the presence or absence of each
of the three roles that may be present in CB (cybervictimcyberaggressor, cybervictim, and cyberaggressor). Each
of the questions posed with this purposed constituted an
individual variable that required an individual and specific
response.33
Participating students were asked that they consider
their responses within their personal context, ranging
from 6 months prior to the time of study in the school.
CB was defined as a situation where someone repeatedly
intimidates another through e-mail or telephone text messages and/or disseminates private information of others or
embarrasses someone via the internet.36
The questions to establish CB were:
1) During the last 6 months, how often have you been
assaulted or intimidated by others through the internet or cell phone text messages?
2) During the last 6 months, how often have you attacked or bullied others via the internet or cell phone
text messages?
Bol Med Hosp Infant Mex
Risk factors and consequences of cyberbullying in teenagers: association with bullying
Response options for these questions were: a) never
b) once a week c) more than once a week; d) almost
every day. Choices b, c and d are considered together as
“sometimes.” Thus, the response was dichotomized for
operational purposes as “never” or “sometimes” in the two
items. Based on the two questions, the sample was divided
into four groups also for operational purposes: 1) never cybervictim or cyberaggressor, 2) only cybervíctim (at least
“sometimes” cybervictim, but “never” cyberaggressor), 3)
only cyberaggressor (at least “sometimes” cyberaggressor,
but never “cybervictim”), 4) cybervictim–cyberaggressor
(at least “sometimes” and cybervictim and cyberaggressor
simultaneously).
The questions listed below, including those of traditional bullying, were raised in consensus and were also
incorporated and considered to be individual variables
under the same premise as the previous two:
3) How often have you been assaulted or intimidated
via the internet or cell phone text messages in the
form of 1) being ignored, 2) offended by profanity,
3) nicknames, 4) who speak ill of you (rumors), 5)
threats; 6) criticisms or 7) made fun of?
For each of these seven options, the participant had the
following response alternatives: a) never b) once a week
c) more than once a week; d) almost every day.
4) In what ways are you intimidated or attacked?
5) In what ways do you intimidate or bully?
Response options were the same for these two questions: 1) cell phone messaging, 2) IM, 3) e-mail, 4) social
networking page. For each of these options, the participant
had the following alternatives: a) never b) once a week c)
more than once a week; d) almost every day.
In questions 4 and 5, the students were able to select
more than half if that was the case.
6) By whom have you been intimidated or attacked
through internet or mobile messaging?
7) Who do you assault or bully via internet or mobile
messaging?
The options for these questions were as follows: 1) girls,
2) boys, 3) boys and girls at the same time, 4) indifferent
to gender.
The response alternatives for each of these four options
as for the previous questions were these: a) never b) once
a week c) more than once a week; d) almost every day.
8) Have you felt fear from the intimidation or aggression to which you were subjected through the interVol. 69, November-December 2012
net or text messages? The response alternatives were
a) never, b) once a week, c) more than once a week,
d) almost every day.
Responses b, c and d of questions 3–8 were considered
together as “sometimes” for operational purposes, in the
same manner as questions 1 and 2, which allowed for
dichotomize the responses.
We collected sociodemographic information (age,
gender, education and parent with whom the child lives)
with a format (yes/present-no/absent) and screened for the
presence or absence of psychopathology, psychosomatic
manifestations, sleep problems, alcohol use, smoking and
traditional bullying, as variables of interest.
Psychopathological manifestations
For evaluation and measurement of psychopathological
problems, we used the strengths and weaknesses questionnaire (SDQ) in its self-reporting version for children and
adolescents 11–16 years of age.37,38 This questionnaire is
comprised of 25 items divided into five scales [hyperactivity-inattention, emotional symptoms (unhappiness, loss
of confidence and fear), behavior problems (oppositional
defiant), peer problems and prosocial behavior]. For the first
two scales, a score >7 was considered positive; positivity
with the instrument in the case of behavior problems and
with peers was >5. Three response options are available
on a Likert-type scale that are answered directly by the
participant and coded as 0 (not true), 1 (sometimes true)
or 2 (absolutely true), except for 5 “inverse” items that
are rated in the opposite direction. Translation and validation of the self-reporting version used in this study was
carried out to add more reliability to the results obtained.
To ensure greater equivalency of the translation, WHO
guidelines were followed.39 For study purposes we only
used the hypersensitivity–inattention scale and emotional
symptoms (unhappiness, loss of self-confidence and fear)
of the SDQ questionnaire. We conducted an analysis of
internal consistency of these two scales to determine its
internal consistency and coherence of the items in their
intercorrelation with each other, for which the Cronbach’s
alpha statistic was applied. For the scale of hyperactivity–
inattention, emotional symptoms, and the questionnaire as
a whole, Cronbach’s alpha was 0.78, 0.78 and 0.76, respectively, which are acceptable values according to Nunnally.40
For exploring the variables of psychosomatic manifestations, sleep problems, use of alcohol, tobacco and
555
Gerardo García-Maldonado, Gerardo Jesús Martínez-Salazar, Atenógenes H. Saldívar-González, Rafael Sánchez-Nuncio,
Gerardo Manuel Martínez-Perales, María del Carmen Barrientos-Gómez
school environment, questions were raised in consensus
and formulated as direct and concrete questions, also
similar to those formulated by Sourander et al.27 Each of
the questions constituted individual variables that required
individual and specific responses.33
Psychosomatic manifestations
There were basically two common and known symptoms
explored: headache and abdominal pain. The first was
addressed with the question “During the last 6 months,
have you experienced headaches that distract you from
what you are doing at the time?”, with the following
response options: a) at least once a week b) at least once
a month, c) never.
Abdominal pain was approached with the question
“During the last 6 months have you experienced recurrent
abdominal pain?” Response options were as follows: a)
at least once a week, b) at least once a month, c) never.
For operational purposes, responses “a” and “b” were
considered together as “yes/present” for both manifestations.
Sleep problems
This situation was addressed with two questions. The first
was “During the last 6 months, have you experienced
trouble falling asleep at night?” Response options were as
follows: a) at least once a week, b) <1 time per month, c)
never. The other question was “During the last 6 months,
have you experienced waking up during the night and
then having difficulty going back to sleep?” Response
options were these: a) almost every night; b) one or two
times a week, c) never. Similarly, for operational purposes
the responses and b were considered yes/present for both
questions.
Alcohol Use
Drinking alcohol to the point of intoxication was documented with the following question: “When you drink
alcohol, do you become drunk?” Response options were
as follows: a) never b) once a month; c) once a week; d)
daily. Responses b, c, and d were considered together as
“yes/present.”
Tobacco use
The use of tobacco was explored with the question: “Do
you smoke?” Response options were as follows: a) never,
556
b) rarely, c) some weekdays, d) daily. Responses b, c, and
d were considered together as “yes/present.”
School environment
To this end, two assertions were raised expressed in the
first person: 1) I feel insecure in my school or 2) the
teachers at my school care about me. Response options
were as follows: a) never b) sometimes c) frequently d)
forever. Responses b, c, and d were considered together
as “yes/present.”
Determination of traditional bullying
There were four questions raised, following the same
principles and considerations as those adopted for the CB.
The conceptual definition was used by Olweus.41
1) How often have you been bullied or harassed in your
school during the past 6 months?
2) How often have you been bullied or harassed outside
your school during the past 6 months?
3) How often have you bullied or harassed others in
your school during the past 6 months?
4) How often have you bullied or harassed others outside your school during the past 6 months?
According to the literature, the bullying phenomenon
can occur within or outside a school campus.42,43 To prevent participants from considering this problem exclusive
within the campus, it was decided to ask the question
including adverbs “within” and “outside.” The response
was considered positive with any of the four questions, or
with all, if that was the case. Response options for these
four questions were as follows: a) never b) once a week
c) more than once a week; d) almost every day.
Responses b, c and d are considered together as “at
least sometimes.” For operational purposes the sample
was categorized into four groups: 1) never aggressor or
victim, 2) only victims (at least sometimes victim, but
never aggressor), 3) only aggressors (at least sometimes
aggressor. but never victim), 4) victim–aggressor (sometimes both victim and aggressor).
Procedures
An informational meeting was conducted days before
with the school authorities. All information was handled
confidentially. Staff members who administered the questionnaires presented directly to the classrooms with the
students to explain the goal of the study. Teacher support
Bol Med Hosp Infant Mex
Risk factors and consequences of cyberbullying in teenagers: association with bullying
was available at all times. The participating students answered the questionnaires in a voluntary and anonymous
manner with an average time of 50 min.
Statistical Analysis
This was a cross-sectional, open, observational and
analytical study composed of two groups of participants:
one group was involved in the CB phenomenon and
another group was not involved. Those involved comprised the group of cybervictims, cyberaggressors and
cybervictims–cyberaggressors. These three groups were
analyzed separately from the group not involved. The
decision to use the uninvolved group as a control group
allowed representation of the population that had not
experienced CB. It was felt that this group corresponded
to the subpopulation of individuals at risk of developing
this and, if it should present itself, they would be included in the population involved. The same strategy was
applied to traditional bullying, which allowed integration
of the groups of victims, perpetrators and victims–aggressors involved in this phenomenon. Once selected,
the presence or absence of significant associations of this
phenomenon with the variables of interest was explored
(including traditional bullying), and the relative exposure
of each role in the CB with each of these variables was
compared, which were formed as independent variables.
According to the literature, these have relevance as risk
factors for CB.
In the analysis that specifically included variables of
psychosomatic manifestations, sleep problems and alcohol
and tobacco use, analyses were performed on the same
principles, but CB was integrated as an exposure factor
for the development of these variables.
For data analysis, descriptive statistics and Pearson
2
χ test for correlation of categorical qualitative variables
was done. To test the hypotheses regarding risk factors
and the correlation among the groups involved in CB,
logistic regression analysis calculating the odds ratio (OR)
was carried out.
To accurately quantify the association, calculation
of the 95% confidence interval was done; α ≤0.05 was
considered statistically significant. For the analysis, the
three groups involved in the CB with values (0-1) were
dichotomized as were all study variables.
Vol. 69, November-December 2012
RESULTS
Sociodemographic Variables
Among the participating students, the average age was
13.4 years (±0.98). According to high-school year, it was
12.5 years (±0.50) for first year, 13.4 years (±0.53) for
the second year and 14.4 (SD 0.54) for the third year.
According to gender, the figures were 13.4 years (±1.01)
for boys and 13.3 years (±0.96) for girls.
Prevalence of CB in 6 Months
Of the total sample, 3.5% of students were cybervictims,
2.8% cyberaggressors and 1.3% cybervictims–cyberaggressors. Although more females participated in the mixed
role, in general males predominate in this phenomenon.
Prevalence of Traditional Bullying in 6 Months
Regarding bullying, it was reported that 19.2% of the
sample corresponds to the aggressors, 24.4% to victims
and 32.9% to victims–aggressors.
Methods and Tools in CB
The manner in which victims are stalked and electronic
media through which participants cyberintimidate or are
cyberintimidated are listed in Table 1. A distinction based
on gender is also made. False rumors and criticisms as
a way of CB were the most commonly used. These and
cell phones as tools of harassment had higher significant
differences between males and females (p <0.05).
Who Has Cyberintimidated You? Who Do You Cyberintimidate?
The largest proportion of females are predominantly cyberintimidated by persons of the same gender (p <0.05).
In the case of cyberaggressors, it shows that males abuse
persons of their own gender with greater frequency (p
>0.05) (Table 1).
Fear of CB
Thirteen percent of the cybervictims stated they have been
afraid of the CB to which they are subjected, corresponding to 4.3% of males and 8.7% female. One youngster
expressed fear that at some point he could be a victim of
CB. It is noteworthy in this context that >80% of children
557
Gerardo García-Maldonado, Gerardo Jesús Martínez-Salazar, Atenógenes H. Saldívar-González, Rafael Sánchez-Nuncio,
Gerardo Manuel Martínez-Perales, María del Carmen Barrientos-Gómez
Table 1. Factors inherent to cyberbullying
Males
Table 2. Distribution of the study variables according to gender
Females
(p)
Methods and tools used in cyberbullying
How often and in what manner have you been cyberintimidated?
- Being ignored
21%
21%
0.24
- Offended
37%
19%
0.15
- Name calling
43%
24%
0.17
- False rumors
34%
58%
<0.05
- Embarrassment
20%
10%
0.36
- Criticism
40%
60%
<0.05
- Teasing
28%
19%
0.68
What method has been used to cyberbully you?
- Cell phone messages
5%
6%
<0.05
- Text messages
35%
34%
0.64
- E-mail
10%
6%
0.58
- Social network page
28%
34%
0.11
What methods have you used to cyberbully?
- Cell phone messages
2%
- Text messages
18%
- E-mail
4%
- Social network page
21%
By whom have you been cyberbullied?
- Girls
14%
- Boys
42%
- Girls and Boys at the same
6%
time
- Gender unknow
26%
Who have you cyberintimidated?
- Girls
8%
- Boys
22%
- Girls and boys at the same
6%
time
4%
22%
0%
25%
0.23
0.37
0.31
0.13
46%
21%
16%
<0.05
0.13
<0.05
29%
0.08
20%
10%
5%
<0.05
0.33
0.58
Variables
Psychopathological manifestations
Emotional symptoms
Hyperactivity-inattention
Psychosomatic manifestations
Recurrent headaches
Recurrent abdominal pain
Problems sleeping
Beginning
Afterwards
Tobacco and alcohol use
Tobacco
Alcohol
Gender
Male Female
Total
1.0%
4.6%
2.3%
3.2%
3.3%
7.8%
14.9%
12.3%
20.4% 35.3%
13.2% 25.5%
20.6%
9.5%
21.4% 42.0%
7.9% 17.4%
3.5%
8.0%
0.8%
2.0%
4.3%
10.0%
computer hidden from parents and use of the computer late
at night is a more representative risk [c2 = 14,584, p <0.05,
OR = 4.2, 95% CI (2.10-16.30)] (Table 3).
Finally, for development of the cyberaggressor–cybervictim role, being female is a salient factor for developing
this condition [c2 = 2891, p >0.05, OR = 3.5, 95% CI
(1.70-16.80)].
Traditional Bullying As a Risk Factor for CB
spend much time at the computer, not necessarily for
homework, and many of them do this even late at night,
unknown by their parents.
It is notable that for males there is a much greater risk
association between traditional victim–aggressor and
cyberaggressor [c2 = 28.821, p <0.05, OR = 7.3, 95% CI
(3.7-14.3)]. In females, the cybervictim–cyberaggressor
condition and traditional victim–aggressor [c2 = 5.603, p
<0.05, OR = 7.3, 95% CI (1.7-21.3)], p <0.05 OR = 7.3
95% CI (1.7-21.3)] showed the most significant association (Table 4).
Presence and Distribution of the Study Variables
CB As a Risk Factor
The results of the following variables—psychopathological, psychosomatic, sleep problems manifestations and use
of alcohol and tobacco—with regard to gender are shown
in Table 2. Interestingly, a significant proportion of sleep
problems are noted.
Risk Factors Associated with CB
Fear of CB and, therefore, feeling unsafe at school has
a significant risk of impacting on the condition of the
cybervictim [c2 = 6.485, p = 0.011, OR = 4.1, 95% CI
(1.30-11.2)]. For the role of cyberaggressor, the use of the
558
It is noteworthy that the condition of cyberaggressor had a
major impact on all variables considered, with headaches
being the most prominent [c2 = 15.125, p <0.05, OR = 7.9,
95% CI (2.2-29.6)] (Table 5).
DISCUSSION
To our knowledge, this study is the first to explore the
theme of CB, some consequences, characteristics and
various risk factors associated with traditional bullying,
including a group of teenagers in Tampico, Tamaulipas,
Bol Med Hosp Infant Mex
Risk factors and consequences of cyberbullying in teenagers: association with bullying
Table 3. Risk factors for cyberbullying
Cybervíctim
(n=23)
Risk factors
Age
Older than 13 years
Younger than 13 years
Gender
Male
Female
SDQ scale
Hyperactivity
Emotional problems
High school year
First year
Second year
Third year
Live with one parent
Yes
No
Time spent using the computer
Less than an hour
More than an hour
Use computer hidden from
parents or at late night hours
Yes
No
Fear of cyberintimidation
No
Yes
(*) p ≤0.05
Cyberaggressor
(n=16)
Cybervíctim-Cyberaggressor
(n=10)
X2
CI
OR
(p)
95%
OR
CI
95%
X2
(p)
OR
CI
95%
0.020 (0.887)
0.020 (0.887)
1.9
1
1.3-24.6
1.4-12.8
0.654 (0.419)
0.654 (0.419)
1.8
0.5
0.4-7.8
0.1-2.3
0.695 (0.405)
0.695 (0.405)
2.3
0.4
1.2-18.2
0.0-3.3
0.094 (0.760)
0.094 (0.760)
1
2.9
0.7-1.5
1.5-14.9
3.556 (0.04)*
1.556 (0.212)
2.2
0.6
2.9-13.2 2.891 (0.089)
0.3-1.3 2.891 (0.089)
3.4
3.5
1.7-16.3
1.7-16.8
3.064 (0.080)
0.4
0.1-1.1
2.2
1.1-14.9
0.079 (0.778)
2.7
1.1-15.3
9.355
(0.031)*
0.564 (0.453)
0
0.280 (0.594)
0.674 (0.412)
0.71 (0.790)
2.7
1.4
0.8
1.3-19.3
0.6-3.3
0.3-2.1
0.813 (0.367)
1.176 (0.278)
0.023 (0.880)
0.939 (0.333)
0.939 (0.333)
1.4
0.9
0.7-2.9
0.7-1.1
0.158
(0.691)
0.158
(0.691)
1.1
0.5-2.6
3.9
2.7-11.2
1.634 (0.201)
1.8
0.7-4.6
1.634 (0.201)
0.9
4.586 (0.112)
6.485
(0.011)*
0.8
4.1
X2
(p)
3.1
1.3-14.3
0
14.675
(0.000)*
8.826 (0.003)*
2.1
1.2-16.2
0.5
1.7
0.9
0.1-1.8
0.6-4.7
0.3-2.6
0.142 (0.707)
0.354 (0.552)
0.041 (0.839)
0.7
1.4
2.8
0.1-3.1
0.4-5.2
1.2-33.6
0.001 (0.971)
0.001 (0.971)
1
0.9
0.3-2.8
0.7-1.2
0.910 (0.340)
0.910 (0.340)
1.6
0.8
0.6-4.3
0.5-1.2
0.401
(0.527)
0.401
(0.527)
0.6
0.1-2.4
0.494 (0.482)
0.5
0.8-3.4
1
1.8-13.7 0.494 (0.482)
1.1
0.8-1.3
4.2
2.1-16.3 1.244 (0.265)
2.9
1.5-7.4
0.7-1.1
14.584
(0.000)*
1.789 (0.321)
0.6
0.4-1.0
1.244 (0.265)
0.8
0.6-1.2
0.7-1.0
1.3-11.2
0.372 (0.542)
0.372 (0.542)
0.9
1.8
0.8-1.1 0.368 (0.544)
0.2-12.8
0
1.03
0
1.2-3.5
0
OR: Odds Ratio; IC: confidence interval.
Mexico. We believe that this is relevant if we consider that
bullying43 and CB44 currently constitute forms of violence
with their own characteristics.
Although CB is less prevalent than traditional bullying,
this does not make its presence any less alarming, especially in children. The prevalence of this phenomenon in
our study was lower than that reported by Smith et al.6 and
Sourander et al.27 However, it is important to consider that
the sample in this study was comparatively lower. However, this phenomenon was able to be identified.
Vol. 69, November-December 2012
We note that false rumors and criticism as forms of CB
are more often used by females, whereas in males the use
of name calling was most often used. This was similar
to that reported in other studies.45 We were also able to
document that females participate less frequently in CB,
and this was in agreement with several other reports.15,17
However, it is important to point out that there are other
reports that note the opposite results.22,45 The differences
may be explained by the sociocultural heterogeneity of the
participants and the discrepancy in sample sizes.
559
Gerardo García-Maldonado, Gerardo Jesús Martínez-Salazar, Atenógenes H. Saldívar-González, Rafael Sánchez-Nuncio,
Gerardo Manuel Martínez-Perales, María del Carmen Barrientos-Gómez
Table 4. Traditional bullying as a risk factor for cyberbullying
Cybervíctim
(n=23)
Bullying groups
Cyberaggressor
(n=16)
X2
(p)
OR
CI
95%
Victim
Aggressor
Victim-Aggressor
16.005 (0.000)*
0.030 (0.861)
0.029 (0.866)
4.6
1.1
0.8
2.3-9.04
0.17-8.1
0.12-5.7
Victim
Aggressor
Victim-Aggressor
7.589 (0.006)*
0.358 (0.550)
2.603 (0.107)
3.6
1.8
3.01
1.5-8.2
0.26-12.3
0.80-11.2
X2
(p)
Boys
1.479 (0.224)
16.637 (0.000)*
28.821 (0.000)*
Girls
0.701 (0.403)
1.940 (0.164)
8.326 (0.004)*
Cybervíctim-Cyberaggressor
(n=10)
OR
CI
95%
X2
(p)
OR
CI
95%
0
6.6
7.3
0
2.6-16.4
3.7-14.3
1.065 (0.302)
0.572 (0.449)
16.823 (0.000)*
0
0
6.2
0
0
2.8-13.8
0
3.6
6.1
0
0.59-22.7
1.9-19.6
0.277 (0.598)
0.122 (0.727)
5.603 (0.018)*
0
0
7.3
0
0
1.7-21.3
*p ≤0.05; X2: Ji cudadrada; OR: Odds Ratio; CI: Confidence interval.
Table 5. Cyberbullying as a risk factor
Headaches
(n=23)
X2
(p)
OR
CI
95%
Recurrent abdominal
pains
(n=16)
X2
CI
(p)
OR 95%
Sleep problems
Alcohol use
(n=10)
X2
(p)
OR
Tobacco use
(n=16)
CI
95%
X2
(p)
OR
(n=10)
CI
95%
X2
(p)
OR
CI
95%
Cybervictim
0.256 0.79 0.33-1.9 0.439 1.3 0.55-3.2 0.008 1.06 0.33-3.3 0.838 0.41 0.05-2.9 0.000 1.01 0.14-7.1
(0.613)
(0.507)
(0.927)
(0.360)
(0.993)
Cyberaggressor 15.125 7.9 2.2-29.6 7.997 3.7 1.40-9.7 4.299 4.4 0.94-20.8 13.923 5.4 2.04-14.4 8.304 5.1 1.55-16.8
(0.000)*
(0.005)*
(0.038)*
(0.000)*
(0.004)*
Cybervíctim- 0.950 1.8 0.53-6.2 1.080 1.9 0.55-6.7 0.627 2.5 0.23-27.5 1.146 2.2 0.49-10.4 0.797 2.4 0.32-18.7
Cyberaggressor (0.330)
(0.299)
(0.429)
(0.284)
(0.372)
* p≤0.05;
X2: Ji cudadrada; OR: Odds Ratio;
CI: confidence interval.
As for the tools used for harassment, as established by
other researchers,5,16 it was found that a high proportion of
participants used cell phones as a primary means of CB.
The cell phone, a universal communication tool that is versatile and affordable (in many cases given to the child by
his/her parents) becomes an important tool of harassment.
As in other studies,42,43 we were able to establish that the
persons who were cyberintimidated were able to identify
that those who intimidated them were of the same gender
and, on the other hand, cyberaggressors also preferred to
intimidate subjects of the same gender. In this sense, there
are no studies identifying the reasons for this behavior.
Because of the anonymity, which is characteristic of CB,
we initially thought that the attackers would choose males
and females alike to carry out the harassment. However,
according to our observed results, this dynamic is not ne-
560
cessarily what is done. Future studies will be worthwhile
to explore this situation further.
As reported by other experts,29 only 13% of the identified cybervictims expressed fear from the harassment they
encounter. This is probably because the cyberaggressions,
at least in this study sample, did not show serious repercussions. We must not forget, however, that fear of aggression
by itself promotes problems of adjustment, academic
achievement, dropouts and, of course, psychopathology.
It was possible to identify that >80% of youngsters
spend much time at the computer. This is relevant if
we consider that it has been reported that the longer
students surf the net, most face the likelihood of being
targeted for anonymous intimidation. We may also note
that excessive internet use can foster the intention of
harassing others.10,16
Bol Med Hosp Infant Mex
Risk factors and consequences of cyberbullying in teenagers: association with bullying
The posture that the parents take with regard to how
much time their children spend in front of a computer as an
entertainment tool is concerning. It was relevant to observe
that more than half of the children stated that their parents
do not comment about the excessive use of this tool. Either
way, it would be important to explore the opinion of the
parents directly, above all if we take into account that the
involvement in CB most frequently begins in the computer
at the home and that the observations made by the parents
to the children may not be taken as a disciplinary measure.
It is fundamental, nevertheless, that children be constantly
supervised and informed of the risks implied in the excessive and inappropriate use of the internet.
In this study we addressed the previously unreported
risk variables for the development of CB as in the case of
emotional symptoms (unhappiness, loss of confidence and
fear) and of hyperactivity–inattention. This was all documented by the SDQ scale. Validation of this instrument
that was done in the study sample allowed more certainty
in regard to the results.
For the role of cybervictim–cyberaggressor, hyperactivity is a significant risk factor and, for the role of
cybervictims, emotional problems constituted an important
risk factor. However, in both cases, confidence intervals
showed a very wide and, hence, imprecise range, which
may be due to lack of power of the study for these particular variables. It will be appropriate in future studies
with a larger sample of participants, to once again review
these elements, which obviously play an important role.
The other factors considered (age, school grade and living
with a single parent) should not be minimized because, as
we know, these have multifactorial implications for CB.
Another objective of this study was to determine
whether there was an association between CB and bullying,
and the implication of the latter as a risk factor. The results
were positive, depending on the role played in these problems. These findings should compel teachers and parents
to provide solutions not only to traditional bullying but also
to the possible presence of CB, which can go unnoticed
and result in severe implications for adolescents.
It has been hypothesized that victims of traditional
bullying will eventually become aggressors using the internet, apparently within a context of personal revenge.5,6,26
Based on the results of this study, it would be precipitious
to take this circumstance into consideration—first, because
the study design is not focused on approaching causality
Vol. 69, November-December 2012
and because the number of participants was not larger. In
a future study it would be pertinent to increase the sample
size through the collaboration of several campuses and to
further explore this particular relationship.
Any of the CB roles can lead to the presence of psychosomatic manifestations, sleep problems and tobacco and
alcohol use. Our results were consistent with the findings
from other authors.30,31 The repercussions generated by
this phenomenon, in varying degrees, are undeniable.
Therefore, it is important to consider these eventualities,
especially considering that they may become the reason
for consultation in child psychiatry services.
The results observed in this sample of high school
students showed the prevalence of CB and the significant
presence of various factors involved. If it is true that the
results are not able to be generalized or are conclusive, they
demonstrate, in this preliminary study, a complicated and
risky reality, which unfortunately is becoming increasingly
common in school populations. Early identification of CB
and structuring of programs aimed at the eradication of
the cases already present should be an urgent priority for
parents and school authorities.
Within the limitations of this study, we can cite, of
course, that the sample size was not sufficient so that the
results may have a higher statistical power. In fact, we
observed that virtually all confidence intervals were very
wide. But we reiterate that this is a preliminary study. Also,
an element that may lend itself to discussion is not having
had a self-administered and standardized CB instrument.
However, its approach was serious, reliable, structured
and similar to other previous studies.27
Due to the cross-sectional design of this study, it was
not feasible to address causality. However, the results obtained are relevant and may be a guide to structure other
methodological designs. We should also note that it is
likely that use of the same sample to check for risk factors
and consequences may have overstated the associations
observed. Finally, it is always advisable to document
information through other sources.
Although it was not the subject of this paper, risks
and consequences of CB generated by adults on minors
should not be ignored. This phenomenon is unfortunately
becoming more frequent and alarming. The research is
still in early stages and, although there are difficulties
in its approach, efforts need to be redirected to provide
scientific, not only anecdotal, information.
561
Gerardo García-Maldonado, Gerardo Jesús Martínez-Salazar, Atenógenes H. Saldívar-González, Rafael Sánchez-Nuncio,
Gerardo Manuel Martínez-Perales, María del Carmen Barrientos-Gómez
On behalf of our team, the next project will be to expand
the study to other basic secondary schools, both private
and public, in the southern suburbs of Tamaulipas in order
to generalize the results.
REFERENCES
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
562
Aricak T, Siyahhan S, Uzunhasanoglu A, Saribeyoglu S, Ciplak
S, Yilmaz N, et al. Cyberbullying among Turkish adolescents.
Cyberpsychol Behav 2008;11:253-261.
David-Ferdon C, Hertz MF. Electronic media, violence, and
adolescents: an emerging public health problem. J Adolesc
Health 2007;41(6 suppl 1):S1-S5.
Swartz MK. Cyberbullying: an extension of the schoolyard. J
Pediatr Health Care 2009;23:281-282.
Vandebosch H, Van Cleemput K. Defining cyberbullying: a
qualitative research into the perceptions of youngsters. Cyberpsychol Behav 2008;11:499-503.
Juvonen J, Gross EF. Extending the school grounds? Bullying
experiences in cyberspace. J Sch Health 2008;78:496-505.
Smith PK, Mahdavi J, Carvalho M, Fisher S, Russell S, Tippett
N. Cyberbullying: its nature and impact in secondary school
pupils. J Child Psychol Psychiatry 2008;49:376-385.
Kowalski RM, Limber SP, Agatston PW. Cyberbullying: Bullying
in the Digital Age. Malden, MA: Blackwell Publishing; 2008.
Available at: http://www.cyberbullyhelp.com.
Joffre-Velázquez VM, García-Maldonado G, Saldívar-González AH, Martínez-Perales G, Lin-Ochoa D, Quintanar-Martínez
S, et al. Bullying en alumnos de secundaria. Características
generales y factores asociados al riesgo. Bol Med Hosp Infant
Mex 2011;68:193-202.
Li Q. Cyberbullying in schools: a research of gender differences. School Psychol Int 2006;27:157-170.
Ortega R, Calmaestra J, Mora-Merchán JA. Cyberbullying. Int
J Psych Psychol Ther 2008;8:183-192.
Ybarra M, Mitchell KJ, Wolak J, Finkelhor D. Examining
characteristics and associated distress related to internet
harassment: findings from the Second Youth Internet Safety
Survey. Pediatrics 2006;118:e1169-e1177.
Slonje R, Smith PK. Cyberbullying: another main type of bullying? Scand J Psychol 2008;49:147-154.
Mesch GS. Parental mediation, online activities, and cyberbullying. Cyberpsychol Behav 2009;12:387-393.
Williams KR, Guerra NG. Prevalence and predictors of internet
bullying. J Adolesc Health 2007;41(6 suppl 1):S14-S21.
Ang RP, Goh DH. Cyberbullying among adolescents: the role of
affective and cognitive empathy, and gender. Child Psychiatry
Hum Dev 2010;41:387-397.
Ybarra ML. Linkages between depressive symptomatology
and internet harassment among young regular internet users.
Cyberpsychol Behav 2004;7:247-257.
Kaltiala-Heino R, Fröjd S, Marttunen M. Involvement in bullying
and depression in 2-year follow-up in middle adolescence. Eur
Child Adolesc Psychiatry 2010;19:45-55.
Frisén A, Jonsson AK, Persson C. Adolescents’ perception of
bullying: who is the victim? Who is the bully? What can be done
to stop bullying? Adolescence 2007;42:749-761.
19. Jankauskiene R, Kardelis K, Sukys S, Kardeliene L. Associations between school bullying and psychosocial factors. Soc
Behav Personal 2008;36:145-162.
20. Cava MJ, Musitu G, Murgui S. Individual and social risk factors
related to overt victimization in a sample of Spanish adolescents. Psychol Rep 2007;101:275-290.
21. Patchin J, Hinduja S. Traditional and nontraditional bullying
among youth: a test of General Strain Theory. Youth Society;
2010. Available at: www.cyberbullying.us
22. Dehue F, Bolman C, Völlink T. Cyberbullying: youngsters’
experiences and parental perception. Cyberpsychol Behav
2008;11:217-223.
23. Ybarra ML, Mitchell KJ. Online aggressor/targets, aggressors,
and targets: a comparison of associated youth characteristics.
J Child Psychol Psychiatry 2004;45:1308-1316.
24. Topçu C, Erdur-Baker O, Capa-Aydin Y. Examination of cyberbullying experiences among Turkish students from different
school types. Cyberpsychol Behav 2008;11:643-648.
25. Garaigordobil M. Prevalencia y consecuencias del cyberbullying: una revisión. Int J Psychol Psychol Ther 2011;11:233254.
26. Hinduja S, Patchin JW. Offline consequences of online victimization, school violence and delinquency. J School Viol
2007;6:89-112.
27. Sourander A, Brunstein Klomek AB, Ikonen M, Lindroos J,
Luntamo T, Koskelainen M, et al. Psychosocial risk factors associated with cyberbullying among adolescents, a populationbased study. Arch Gen Psychiatry 2010;67:720-728.
28. Comisión Nacional de Derechos Humanos en México (CNDH).
Comunicado 121. Acciones para proteger a los menores.
México; 2011. Available at: http://www.cndh.org.mx/node/37.
29. Gradinger P, Strohmeier D, Spiel C. Traditional bullying and
cyberbullying: identification of risk groups for adjustment problems. J Psychol 2009;217:205-213.
30. Vieno A, Gini G, Santinello M. Different forms of bullying and
their association to smoking and drinking behavior in Italian
adolescents. J School Health 2011;81:393-399.
31. Forero R, McLellan L, Rissel C, Bauman A. Bullying behavior
and psychosocial health among school students in New South
Wales, Australia: cross sectional survey. BMJ 1999;319:344348.
32. Garcia X, Pérez A, Nebot M. Factores relacionados con el
acoso escolar (bullying) en los adolescentes de Barcelona.
Gac Sanit 2010;24:103-108.
33. Asociación Psiquiátrica Mexicana. Programa de Actualización Continua en Psiquiatría. México: Evaluación Clínica en
Psiquiatría; 2003.
34. Hinduja S, Patchin JW. Bullying Beyond the Schoolyard. Preventing and Responding to Cyberbullying. Thousand Oaks,
CA: Corwin Press, A Sage Company; 2009.
35. Hinduja S, Patchin JW. Bullying, cyberbullying, and suicide.
Arch Suicide Res 2010;14:206-221.
36. Patchin JW, Hinduja S. Bullies move beyond the schoolyard.
A preliminary look at cyberbullying. Youth Viol Juv Justice
2006;4:148-169.
37. Woerner W, Fleitlich-Bilyk B, Martinussen R, Fletcher J,
Cucchiaro G, Dalgalarrondo P, et al. The Strengths and Difficulties Questionnaire overseas: evaluations and applications
of the SDQ beyond Europe. Eur Child Adolesc Psychiatry
2004;13(suppl 2):ii47-ii54.
Bol Med Hosp Infant Mex
Risk factors and consequences of cyberbullying in teenagers: association with bullying
38. Marzocchi GM, Capron C, Di-Pietro M, Duran Tauleria E, Duyme M, Frigerio A, et al. The use of the Strengths and Difficulties
Questionnaire (SDQ) in Southern European countries. Eur
Child Adolesc Psychiatry 2004;13(suppl 2):ii40-ii46.
39. Sartorius N, Janca A. Psychiatric assessment instruments
developed by the World Health Organization. Soc Psychiatry
Psychiatr Epidemiol 1996;31:55-69.
40. Nunnally JC. La Teoría Psicométrica. Nueva York: McGrawHill; 1978.
41. Olweus D. Bullying at School. Malden, MA: Blackwell Publishers; 1993.
Vol. 69, November-December 2012
42. Raskauskas J, Stoltz AD. Involvement in traditional and electronic bullying among adolescents. Dev Psychol 2007;43:564575.
43. Vanderbilt D, Augustyn M. The effects of bullying. Pediatr Child
Health 2010;20:315-320.
44. Spears B, Slee P, Owens L, Johnson B. Behind the scenes
and screens: insights into the human dimension of covert and
cyberbullying. J Psychol 2009;217:189-196.
45. Wang J, Iannotti RJ, Nansel TR. School bullying among adolescents in the United States: physical, verbal, relational, and
cyber. J Adolesc Health 2009;45:368-375.
563
Bol Med Hosp Infant Mex 2012;69(6):564-569
Clinical case
Acrodermatitis enteropathica
Marco Antonio Toxtle Román,1 Ana Elena Hernández Arroyo2
ABSTRACT
Background. Acrodermatitis enteropathica is a rare but easy to manage condition but with great clinical relevance. The condition must be
diagnosed properly and timely. We present an infant with the following clinical triad: acral dermatitis, diarrhea and alopecia. Zinc treatment
should be initiated, even from a primary care level. Clinical response is immediate and without sequelae.
Case report. We present the case of an infant with chronic malnutrition, short stature, psychomotor retardation and large symmetrical
scaly skin lesions with disseminated alopecia totalis. The patient was admitted to the Hospital Regional de la Huasteca, Huejutla, Hidalgo.
Acrodermatitis enteropathica was suspected in the clinic and serum zinc and skin biopsy were carried out. Clinical improvement was
obtained after the first 2 weeks of treatment.
Conclusions. Treatment initiation with zinc sulfate at a dose of 2-5 mg/kg/day has immediate clinical implications with complete symptom
remission.
Key words: acrodermatitis enteropathica, zinc.
“What is not considered is not diagnosed and what is not known is not thought about.”
INTRODUCTION
Acrodermatitis enteropathica (AE) is a rare autosomal recessive disease caused by an impairment of zinc absorption
at the level of the duodenum and jejunum. It responds quickly to adequate dietary zinc supplementation.1 The genetic
defect has been mapped to human chromosome 8q24.3
locus in the Slc39a4 gene identified as that encoding the
zinc transporter (zip4).1-4 Diagnosis is accomplished clinically together with histopathology and laboratory studies.3
Its presentation is characterized by the clinical triad: acral
dermatitis, alopecia and diarrhea (Figure 1).5
1
2
Servicio de Pediatría, Hospital Regional de la Huasteca, Secretaria de Salud, Huejutla, Hidalgo, Mexico
Residente de Pediatría, Hospital General de Pachuca, Hidalgo,
México
Correspondencia: Dr. Marco A. Toxtle Román
Servicio de Pediatría
Hospital Regional de la Huasteca
Secretaria de Salud
Huejutla, Hidalgo, Mexico
E-mail: [email protected]
Received for publication: 2-17-12
Accepted for publication: 6-18-12
564
In this paper we present the case of an older infant, an
AE carrier who presented a characteristic clinical picture
and with favorable progress and prognosis.
CLINICAL CASE
We present the case of an older male infant who at the
time of admission was 2 years and 10 months of age. The
patient was from a low socioeconomic background. He was
the third child of a 39-year-old mother who admitted to an
unwanted pregnancy. The mother received regular prenatal
care and there was no report of intake of iron and folic acid.
The infant was born after 40 weeks of gestation through
vaginal delivery in a primary care center. Birth weight
was 2500 g and length was 48 cm. Apgar is unknown.
Regarding psychomotor development, the infant presented head support (2 months), social smile (5 months),
sitting (8 months), standing (9 months), and walking (1
year 6 months) with assistance only. The patient had poor
language development (disyllabic). He was breastfed for
1 year. Weaning was accomplished on the basis of fruits
and vegetables from 4 months of age. The patient became
integrated to the family diet at 1 year of age. When breastfeeding was stopped at 1 year of age, the patient began
Bol Med Hosp Infant Mex
Acrodermatitis enteropática
to have angular cheilitis and erythematous, symmetrical,
well-defined lesions associated with erosions, crusts and
exudate on the face, neck, lower back and limbs (Figure
2) between 5 and 10 cm diameter and covering areas of
flexion (Figure 3). Paronychia and onychodystrophy were
also present (Figure 4). Subsequently, total alopecia of the
scalp, eyebrows and eyelashes appeared (Figure 1).
There were intermittent periods of diarrhea from 1½
years of age with clinical data of malnutrition and failure to
thrive. Neurologically, the patient alternated with episodes
of irritability and apathy. He received multiple treatments
at a primary care hospital with amoxicillin, hydrocortisone
and colloidal baths, without improvement. At the time of
his admission to the Hospital Regional de la Huasteca,
he was evaluated by the emergency department with the
following diagnoses: febrile syndrome of 1 week evolution
(38–39°C), generalized dermatosis, and acute diarrhea
manifested by five to six bowel movements diminished
in consistency and accompanied by non-bloody mucus.
The infant suffered from chronic malnutrition from 1
year of age.
An evaluation was requested by our Department of
Pediatrics due to suspicion of AE with the clinical triad of
alopecia, chronic diarrhea and periorificial acral dermatitis,
along with changes in mood, alternating with periods of
apathy and irritability.
younger than his chronological age. He was irritable and
frightened, seeking his mother’s protection. The skull
was without exostosis or depressions and there was total
alopecia including eyebrows and eyelashes. Eyes were
symmetrical with isochoric and normoreflexic pupils,
photophobia, conjunctivitis and blepharitis, well-set ears,
and choanal permeability. Oral cavity was normal with
intact palate. There were erythematous, symmetrical,
oozing, scaly lesions on the face, neck, periorbital and
perioral regions, and covering the cheeks. The patient had
characteristic angular cheilitis (perlèche). The patient’s lips
were dry and the mucous membranes were poorly hydrated
(Figure1). Chest demonstrated normal dimensions with
a large, ~12 cm erythematous and weeping lesion in the
lumbosacral region (Figure 2). The lesions covered the
diaper area and inguinal and gluteal regions as well as
hyperkeratotic zones in the areas of flexion of the lower
Physical Examination
Physical examination revealed weight 7500 g, height 80
cm, and head circumference 49 cm. The patient appeared
Figure 1. Alopecia of the scalp, eyebrows and eyelashes.
Vol. 69, November-December 2012
Figure 2. Large weeping lesions in the lumbosacral and gluteus
regions.
565
Marco Antonio Toxtle Román, Ana Elena Hernández Arroyo
Figure 3. Erythematous lesions in the genital and perineal regions.
Figure 5. Lesions on the face 5 days after treatment.
and upper extremities (Figure 3) along with paronychia
and onychodystrophy (Figure 4). There were impetiginous
lesions in the face and diaper area. No cardiovascular
alterations were reported. The abdomen was soft without
organomegaly or lesions. Extremeties were hypotrophic.
There were clinical data of third-degree malnutrition with
45% weight deficit.
Laboratory Analysis
Figure 4. Paronychia and onychodystrophy.
566
The following laboratory results were reported: hemoglobin 12.3 g/dl, hematocrit 38.5%, WBC 32,800, platelets
219,000; glucose 70.5 mg/dl; urea 18.2 mg/dl; creatinine
0.5 mg/dl.
There were 38-40 leucocytes/high power field (hpf),
bact+, erythrocytes 0/2 hpf, Na 134.7 mEq/L, K 5.6
mEq/L, and Cl 108 mEq/L, albumin 3.36 g/dl, total protein
5.55 g/dl, TGO 23 U, TGP 26 U, and ALP 348 U.
Bol Med Hosp Infant Mex
Acrodermatitis enteropática
to cover impetiginized lesions with marked improvement
(Figures 5 and 6). As for recovery of nutritional status, the
patient was managed with a high-protein and high-calorie
diet (800 kcal). Diet was supplemented with Pediasure
for 2 weeks and the patient was started on parenteral
trace elements. For urinary tract infection and diarrheal
syndrome, the patient was administered amikacin (21 mg/
kg/day) and metronidazole (30 mg/kg/day).
Skin lesions were managed with topical zinc sulfate in
the form of a poultice three times daily and sweet almond
oil. Around the diaper area, topical myconazole was added
empirically for clinical suspicion of likely cutaneous candidiasis. For correction of zinc deficiency, oral zinc sulfate
was initiated (5 mg/kg/day). Improvement was observed
from the first 2 weeks of treatment initiation (Figure 7).
Outpatient follow-up was continued monthly for 6
months with administration of zinc sulfate (5 mg/kg/day).
The patient showed hair growth and recovery from the
alopecia of the eyebrows and eyelashes 1½ months after
Figure 6. Skin lesions of the extremities 7 days after treatment.
Fecal cytology reported positive for sugar reducers;
gram stain, gram-positive cocci (+), gram negative bacilli
(+); PMN 69%, positive for fresh ameba and E. histolytica
cysts (+). Serum levels of zinc were 41 mg/dl (normal
values 50–120 mg/dl).
Skin Biopsy (Left Hip)
We observed loss of epidermal epithelial lining. The
baseline showed melanin deposits with substitution of
countless erythrocytes and polymorphonuclear leukocytes
infiltrating the wall. In the lamina propria there were
lymphocytic nodules and plasma cells. Severe chronic
nonspecific dermatosis was reported associated with melanin incontinence.
Treatment
For correction of the patient’s hydration status, a crystalloid bolus was administered at 20 ml/kg/dose and i.v.
fluids at 150 ml/kg/day were administered. Antibiotic
coverage was initiated with dicloxacillin (50 mg/kg/day)
Vol. 69, November-December 2012
Figure 7. Disappearance of the lesions of the head and lumbosacral
regions after 1½ months.
567
Marco Antonio Toxtle Román, Ana Elena Hernández Arroyo
treatment initiation (Figure 8). The patient had a significant
weight gain with a weight of 12,600 g (10th percentile) and
height of 85 cm (3rd percentile) recorded.
DISCUSSION
Primary AE is a rare autosomal recessive disorder due
to deficiency or absence of a zinc ligand at the intestinal
level.7,8 Its presentation is 1:500,000 cases in infants with
a 1:4 risk of transmission from parents to children without
predilection for race or gender.3,9 The most common age
of symptom onset is during the first months of life immediately after the replacement of breast milk by dairy
milk.6 Clinical presentation is striking with characteristic
skin lesions. Treatment is fairly simple and based on zinc
sulfate. Full recovery of skin lesions and nutritional status
is achieved (Figure 9).10
Because breast milk has a better zinc bioavailability
in relation to cow’s milk, breastfeeding has a protective
function, which justifies the clinical presentation after
its interruption.6,11,12 The functions of zinc have been
organized into three categories: catalytic, structural and
regulatory.
Zinc deficiency can cause growth retardation, immune
system dysfunction, male hypogonadism, skin lesions and
neurological disorders in humans.2,13
Figure 9. Complete recovery of the alopecia, of the skin lesions
and nutritional status 3 months after treatment.
Figure 8. Hair growth of the scalp and eyebrows after 1½ months
of treatment.
We must consider this disease each time we are presented with a patient with features of alopecia, diarrhea
and acral and periorificial dermatitis. Within the differential clinical diagnoses that must be considered are the
following: pellagra, seborrheic dermatitis, disseminated
candidiasis, hypovitaminosis, fatty acid deficiency and
isoleucine deficiency.
Histopathological examination of the skin can be useful
in ruling out pathologies such as contact dermatitis and
seborrheic dermatitis. However, the diagnosis is essentially
clinical.6
There may also be secondary or acquired zinc deficiency from various causes such as prematurity, parenteral
nutrition, kidney disease, pancreatic insufficiency, diuretic
use, infections, malabsorption syndromes, intestinal surgery, diets high in phytates and calcium, and neoplasms.6
The importance of clinical diagnosis, corroborated with
serum zinc and timely treatment, even from a primary care
level should be emphasized because serum zinc levels rapidly
568
Bol Med Hosp Infant Mex
Acrodermatitis enteropática
normalize once supplement are initiated. Treatment duration
is prolonged and frequently must continue for life.14,15
This case is notable because of the striking chronic skin
lesions presented by the patient, the time of evolution and the
age of the patient, which was even confused with immunodeficiencies or neoplastic process. The patient also presented
angular cheilitis and characteristic paronychias, which comprise early manifestations of primary AE, as well as lesions
in the extremity folds, which are not seen in acquired AE.6
Our patient evolved rapidly with a complete recovery
of nutritional status, skin lesions with hair growth and
clinical improvement in psychomotor development. It
coincides with the cases reported in the literature, which
note an evident clinical improvement immediately after
zinc supplementation is begun. However, there are a limited number of cases reported of older infants, such as
is the case in our patient, probably because the diagnosis
is not suspected or is delayed.
Finally, it should be mentioned that major diagnostic
and therapeutic resources are not required, only suspicion
of the existence of the disease and timely initiation of
management at any level of care.
2.
Acknowledgments
11.
We appreciate the collaboration of Drs. Jazibe Sahira
Moreno Castillo (Departamento de Enseñanza), Jorge Luis
Ortuño Miranda (Servicio de Cirugía) and Erasmo García
Juárez (Servicio de Laboratorio).
3.
4.
5.
6.
7.
8.
9.
10.
12.
13.
14.
REFERENCES
15.
1.
Wang K, Zhou B, Kuo YM, Zemansky J, Gitschier J. A novel
member of a zinc transporter family is defective in acrodermatitis enteropathica. Am J Hum Genet 2002;71:66-73.
Vol. 69, November-December 2012
Dufner-Beattie J, Weaver BP, Geiser J, Bilgen M, Larson M,
Xu W, et al. The mouse acrodermatitis enteropathica gene
Slc39a4 (Zip4) is essential for early development and heterozygosity causes hypersensitivity to zinc deficiency. Hum Mol
Genet 2007;16:1391-1399.
Maverakis E, Fung MA, Lynch PJ, Draznin M, Michael
DJ, Ruben B, et al. Acrodermatitis enteropathica and
an overview of zinc metabolism. J Am Acad Dermatol
2007;56:116-124.
Küry S, Dréno B, Bézieau S, Giraudet S, Kharfi M, Kamoun R,
et al. Identification of SLC39A4, a gene involved in acrodermatitis enteropathica. Nat Genet 2002;31:239-240.
Rubio I, Ascione I, Glaussiuss G, Salmentón M. Acrodermatitis
enteropática. Arch Pediatr Urug 2001;72:298-302.
Bressan G, Oliveira V, Parolin L, Taniguchi K, Giraldi S. Acrodermatitis enteropática: descripción de siete casos y revisión
de la literatura. Dermatol Pediatr Lat 2006;4:211-216.
Moynahan EJ. Letter: Acrodermatitis enteropathica: a lethal
inherited human zinc-deficiency disorder. Lancet 1974;2:399400.
Avellaneda CF, Cruz CM, Palacio CA. Acrodermatitis enteropática, un reto diagnóstico. Reporte de un caso y revisión de
la literatura. Rev Fac Med 2009;17:150-154.
Van Wouwe JP. Clinical and laboratory assessment of zinc
deficiency in Dutch children. A review. Biol Trace Elem Res
1995;49:211-225.
Sandström B, Cederblad A, Lindblad BS, Lönnerdal B.
Acrodermatitis enteropathica, zinc metabolism, copper
status, and immune function. Arch Pediatr Adolesc Med
1994;148:980-985.
Coelho S, Fernandes B, Rodrigues F, Reis JP, Moreno A, Figueiredo A. Transient zinc deficiency in a breast fed, premature
infant. Eur J Dermatol 2006;16:193-195.
Prasad AS. Zinc: an overview. Nutrition 1995;11(suppl 1):9399.
Prasad AS. Zinc deficiency. BMJ 2003;326:409-410.
Álvarez P, Pais ME, Hernández M, Soliani A, GarcíaDíaz R. Acrodermatitis enteropática. Arch Argent Pediatr
2007;105:536-538.
Radja N, Charles-Holmes R. Acrodermatitis enteropathica—
lifelong follow-up and zinc monitoring. Clin Exp Dermatol
2002;27:62-63.
569
Bol Med Hosp Infant Mex 2012;69(6):570-574
Clinical case
Erratic migration of Ascaris lumbricoides to the scrotum
Rubén Martín Álvarez-Solís,1 Marcela Vargas-Vallejo,1 Griselda Orozco-Barrientos,2 Armando QueroHernández,2 Gabriel García-Hernández,3 David Bulnes-Mendizábal4
ABSTRACT
Background. Ascaridiasis is one of the main parasitoses affecting children. The main objective is to demonstrate the case of a child with
erratic migration of Ascaris lumbricoides found next to the testis in the vaginalis tunic, secondary to a perforation of Meckel diverticulum.
Case report. We present the case of a school-age male patient who was treated at our clinic due to acute abdomen. Laparotomy was
carried out, revealing a perforation of Meckel diverticulum with Ascaris lumbricoides free in the abdominal cavity and with migration to
scrotum of female adult Ascaris lumbricoides by way of an inguinal hernia.
Conclusions. We discuss the epidemiology and clinical presentation of acute abdomen of Ascaridiasis and intraoperative study.
Key words: Ascaris lumbricoides, complications, erratic migration, Meckel diverticulum, acute scrotum.
INTRODUCTION
Acute abdomen (AA) in children is usually accompanied
by the triad of vomiting, abdominal distension, and lack
of bowel movements. Diagnosis is clinical and imaging
techniques are used to confirm and to locate the area of
the obstruction.1 The main cause of AA in children is acute
appendicitis.2 However, there are other conditions that can
produce symptoms and signs of AA such as intussusception, Meckel’s diverticulum or intestinal obstruction by
Ascaris lumbricoides (AL).3,4
Ascariasis may cause AA when there is an intestinal
obstruction due to inadequate management of AL. Sometimes it may be accompanied by bowel “volvulus.” Among
the most common surgical complications is infestation due
1
2
3
División de Cirugía Pediátrica,
Sevicio de Pediatría, 4Servicio de Patología, Hospital del Niño
Dr. Rodolfo Nieto Padrón, Villahermosa, Tabasco, Mexico
Servicio de Gineco-Obstetricia, Hospital de Alta Especialidad
de la Mujer, Tabasco, Mexico
Correspondence: Dr. Rubén Martín Álvarez Solís
División de Cirugía Pediátrica
Hospital del Niño Dr. Rodolfo Nieto Padrón
Villahermosa, Tabasco, Mexico
E-mail: [email protected]
Received for publication: 2-17-12
Accepted for publication: 2-14-12
570
to AL. The following have been described: partial bowel
obstruction, intestinal obstruction, volvulus,5,6 appendicitis7,8 and intestinal perforation.9 However, other less
reported complications are cases of erratic migration to
other organs and tissues, most notably to the gallbladder,10
pancreas,11 lacrimal sac12 and chest.13
The objective of this study was to present an unusual
case of a school-aged child with erratic migration of AL
revealed within the vaginalis tunica attached to the testis
in the scrotum, whose migration was facilitated by the
peritoneum vaginal ductus or indirect right-side inguinal
hernia secondary to AA from a perforated Meckel’s diverticulum caused by AL.
CLINICAL CASE
We present the case of a 6-year-old male native to Pichucalco, Chiapas who presented a clinical picture of 24 h
onset characterized by abdominal pain, fever, vomiting and
no bowel movements. During physical examination, the
patient appeared thin and with generalized pain. Cardiopulmonary exam was normal. The abdomen showed data
of AA characterized by the presence of diffuse abdominal
pain, positive rebound and abdominal irritation. McBurney, Rovsing and Blumberg signs were positive, and there
was mild abdominal distension and absence of peristalsis.
The patient presented with mild edema and erythema of
Bol Med Hosp Infant Mex
Erratic migration of Ascaris lumbricoides to the scrotum
the right scrotum (Figure 1). CBC reported mild anemia,
hemoglobin 9.5, leukocytosis 15,000, segments 80%
with 5% bands and 5% eosinophils. Simple abdominal
x-ray while standing was done, which revealed poor air
distribution, air-fluid levels, absence of air in the pelvic
cavity, and diffuse core opacity. There was no calcification, no antalgic column, or fecaliths (Figure 2). With this
data along with the data of AA, we decided to perform an
exploratory laparotomy with a preoperative diagnosis of
a probable complicated appendicitis vs. AA secondary to
incarcerated hernia. For this reason, a Rocky-Davis type,
transverse infra-umbilical incision was made on the right
side. The appendix was found to be “normal” with hyperemia. Subsequently, we looked at the terminal ileum and a
Meckel’s diverticulum was located 75 cm from the valve.
We found the tip to be perforated (Figure 3) with mild
peritonitis; therefore, resection and ileo-ileal enteroanastomosis were performed. When conducting a thorough saline
lavage of the abdominal cavity, surprisingly we found two
25-cm AL, free between bowel loops. For this reason, we
decided to perform “taxis” of the jejunal ileal intestinal
content (Ascaris skein) that had gone unnoticed into the
colon. We cleaned the cavity with an intense washing with
2 L of saline and, prior to closure of the abdominal wall,
we palpated and explored the right hemiscrotum. Due to
feeling swollen and crackly, we decided to explore the right
inguinal canal. We found a 25-cm adult female curled in
the vaginalis tunica of the right testicle (Figure 4). It was
extracted and the patient underwent inguinal hernia repair,
extensively washing the area. Intravenous antibiotics were
prescribed along with fasting for 7 days. Oral feeding was
begun on the seventh day. The patient had a satisfactory
outcome and was discharged without complications, with
regular follow-ups for 2 years postsurgery.
Figure 1. Abdomen and genitalia of the patient before surgery.
DISCUSSION
In the approach of AA in children, clinical history and physical examination are essential for the diagnosis of acute
appendicitis. Laboratory tests and medical imaging tests
such as abdominal x-ray usually confirm the diagnosis of
acute appendicitis. However, in some cases, ranging from
5 to 10%, the clinical picture can be modified when there
is prior use of painkillers or antibiotics; therefore, there
may be diagnostic doubt and, subsequently, the need for
differential diagnosis.14,15
Vol. 69, November-December 2012
Figure 2. Simple x-ray of the abdomen.
Intestinal invagination, one of the differential diagnoses
of AA, is presented most frequently in children <1 year
of age. The main symptoms are vomiting, intermittent
571
Rubén Martín Álvarez-Solís, Marcela Vargas-Vallejo, Griselda Orozco-Barrientos, Armando Quero-Hernández, Gabriel García-Hernández,
David Bulnes-Mendizábal
Figure 3. Perforated Meckel’s diverticulum.
Figure 4. Female Ascaris lumbricoides adjacent to the testicle
during hernioplasty.
“colic-like” pain and bowel movements characterized as
“currant jelly.”16
Another differential diagnosis is Meckel’s diverticulum,
which is the most common congenital malformation of the
small intestine. It is present in 2% of the population and
occurs as a result of incomplete obliteration of the vitelline
or omphalomesenteric duct, which can occur at any age,
but is most frequently reported at 2 years of age.3 Failure
of involution of this duct gives rise to various residual
structures. This solitary diverticulum is found on the
edge of the antimesenteric bowel, usually in the terminal
60 cm of the ileum before the ileocecal valve. It is a true
diverticulum because it has all three layers of the normal
572
intestinal wall. In half the cases, there were remains of
heterotopic gastric mucosa or pancreatic tissue.3,17 The
clinical presentation may be due to bleeding or intestinal
obstruction. In pediatrics, clinical presentation that occurs
most often is due to bleeding.3,17,18
Due to the characteristics of this patient, the clinical
picture of AA suggests, in the first place, complicated acute
appendicitis for being the most common abdominal emergency in children.8 However, the patient’s clinical picture
suggested differential diagnoses with other diseases such
as intestinal perforation caused by Salmonella, strangulated right inguinal hernia, volvulus or possible obstruction
by Meckel’s diverticulum, among others.3 Preoperatively,
there was no suspicion of any surgical complications due
to ascariasis because there was no history of expulsion of
Ascaris though the digestive duct and abdominal x-ray
did not show the classic “bread crumb” appearance of
ascariasis.5,6
AL is the second most commonly seen parasite in outpatient pediatric coproparasitoscopy at the Hospital del
Niño in Tabasco.8 It is always associated with different
clinical presentations ranging from chronic abdominal
pain and diarrhea to more serious scenarios requiring
hospitalization such as subocclusion Ascaris. On other
occasions, surgical intervention is required when there is
a small bowel volvulus or acute appendicitis.8
Ascariasis is a widely disseminated helminth worldwide
and it has been estimated that ~25% of the population suffers from it. In Mexico, intestinal parasites are endemic
with a high incidence in pediatric patients. It is found in
>50% of preschoolers in the suburban areas of Mexico City
and close to 100% in some of the states of the Mexican
Republic such as Tabasco, Veracruz and Yucatan.6,8 It is
estimated that 33% of the population suffers from it and
5% suffer from massive ascariasis.6
Ascariasis is an asymptomatic infestation. Most of the
complications are caused by the rapid reproduction in the
GI tract causing mechanical obstruction. Clinical presentation depends on the mechanism of the obstruction and
can be acute or subacute, requiring medical or surgical
treatment.5,6
Female AL parasites measure between 20 and 49 cm in
length and produce 200,000 eggs/day. The fertilized eggs
are excreted in the feces and must mature in the ground
for 10 to 14 days before the development of the first stage
larvae, which are infectious.19 The adult worms live in the
Bol Med Hosp Infant Mex
Erratic migration of Ascaris lumbricoides to the scrotum
jejunum and ileum. Mechanical obstruction occurs when
their population increases and reaches 100 to 200 worms,
forming a solid mass causing obstruction, inflammation,
ischemia, necrosis and even intestinal perforation.7 The
adult AL may have erratic migration, i.e., the parasite may
travel to other organs and ducts and is favored by many
factors such as fever, diarrhea, consumption of spicy foods,
prolonged fasting, anesthesia, stress and even pesticides.4,6
In the case described here, the clinical scenario of AA
was secondary to perforation of Meckel’s diverticulum
caused by AL.
In other cases, erratic migration can occur in the bile
duct, gallbladder, pancreas and mouth.6,10 Ascaris can pass
through the stomach and be expelled through vomiting,
or enter the bronchi and the lungs by the same motility.
Through the pharynx it may enter the eustachian tube,
nose, external ear by eardrum perforation, tear ducts and
trachea.12,13,20 The parasite can also enter the appendix and
cause acute appendicitis or transient pain that disappears
when the adult parasite leaves. It can also penetrate the
common bile duct and the duct of Wirsung.8 Through the
formation of abscesses or fistulas, the Ascarids can move to
the peritoneal cavity, pleura, lung, vagina, bladder, urethra
and superficial lymph nodes.21 Recently, Diago-Caballero
et al. published a case of the erratic migration to the heart
of a pregnant woman.22
In this particular case it is thought that the adult female
heartworms possibly migrated to the peritoneal cavity after
perforating the Meckel’s diverticulum, later finding the
peritoneovaginal duct or inguinal hernia that is indirectly
on the right, introducing itself and placing itself and ending
near the testicle in the scrotum. They also found AL in the
abdominal cavity, supporting the diagnosis of massive or
chronic untreated ascariasis.
Cases have been reported in which eggs are deposited
in the lamina appendiceal serosa of the uterine tube and the
mesosalpinx, causing tissue parasitism and inflammation
suggestive of chronicity.21 Migration to the biliary tract
is the most frequently reported. It is produced by the canalicular duct, blood or lymphatics, and possibly by the
peritoneal route.10,23,24 However, to date there are no case
reports of erratic migration of Ascaris into the scrotum
of children.
Patients affected by erratic ascariasis to the appendix and
female genitals may present with abdominal pain localized
in the right lower quadrant, with positive McBurney point,
Vol. 69, November-December 2012
Rovsing and Blumberg sign. If the inflammatory process
progresses, we may find defensive or abdominal rigidity,
which suggests AA as interpreted in the initial clinical scenario when the patient was referred to our facility.6,8
In literature, hematologic biometry of patients with
ascariasis observed eosinophilic leukocytosis. It is usually
noticeable during larval migration and erratic migration
of the adult heartworms but tends to decrease and, at
times, disappear during the chronic intestinal phase of
the infection.19
In this case, the patient was admitted to the emergency
department with abdominal pain and was diagnosed with
acute appendicitis, the reason for which he was taken to
surgery. Abnormal eosinophilic values were observed at
the time of the patient’s hospital admission, suggesting
geo-helminth infection. This may have originated, from
the beginning, as the diagnosis of intestinal parasites as a
cause of abdominal pain.5-7
The pathological findings of the patients with erratic
ascariasis are directly related with the inflammatory
process during the erratic migration. Macroscopically,
multiple yellow nodular masses were observed of welldefined fibrous tissue in the affected organs, as in other
granulomatous lesions, measuring between 0.1 and 3 cm.
They can be observed in the mesentery, in the visceral
peritoneum and in the parietal, resembling tuberculosis.20,21
Histopathological findings consist of a granulomatous
inflammatory process with fibroblastic reaction. Granulomas are composed of epithelioid cells, lymphocytes,
giant cells to foreign body that sometimes engulfs eggs,
abundant eosinophils and, occasionally, Charcot-Leyden
crystals.25 Macrophages recognize the presence of the
parasite and try to destroy it before giving a cellular
and humoral immunological response. Macrophages as
well as granulocytes generate reactive O2 intermediaries
that lead to the destruction of the parasite. Eosinophilic
response is triggered when the parasite is too large to be
phagocytized, although its phagocytosis capacity is lower
than by neutrophils.26-28
Ascaris was found in liver lesions during different stages of their life cycle.21 For patient diagnosis of Ascariasis,
the presence of the parasite, in any form, in tissue, fecal
matter or other samples is required.
In Mexico, Vargas et al. described the perforation of
Meckel’s diverticulum by AL as a rare complication and,
if not timely diagnosed, usually has fatal consequences.25
573
Rubén Martín Álvarez-Solís, Marcela Vargas-Vallejo, Griselda Orozco-Barrientos, Armando Quero-Hernández, Gabriel García-Hernández,
David Bulnes-Mendizábal
In the current case we described how we managed the
patient according to the findings and in a manner most
appropriate at that time. Although it would cause some
controversy to first explore the inguinal canal and then
perform exploratory laparotomy, which we are fully in
agreement with, we felt that the resolution of both situations were important: first, the AA of the patient and
second, the extraction of Ascaris in the scrotum, secondary
to indirect inguinal hernia.
A rare case of erratic migration of AL has been presented, characterized by the scenario of an AA secondary
to perforation of Meckel’s diverticulum by Ascaris and
migration of it towards the vaginalis tunica of the right
testicle through a permeable vaginal duct, peritoneum or
indirect inguinal hernia.
Although in our case the eosinophilia was not as significant, it is necessary to regard it as a cause of helminthiasis
in endemic areas. AL is a worm capable of migrating erratically to almost any organ and may have very different
symptoms, including migration to the peritoneum and
scrotum. The clinical scenario of AA in children living
in ascariasis endemic areas can be a complication when
considering the cause due to AL.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
REFERENCES
1.
2.
3.
4.
5.
6.
7.
8.
574
Rebollar GR, García AJ, Trejo TR. Apendicitis aguda: revisión
de la literatura. Rev Hosp Jua Mex 2009;76:210-216.
Barahona JL, Wildt RD. Apendicitis aguda ¿ser o no ser? Revisión bibliográfica pediátrica. Rev Med Hondur 2009;77:99-152.
Álvarez-Solís RM, Reyes-Magaña JG, Vargas-Vallejo MP,
Ulloa-Patiño P, Bulnes-Mendizábal D. Divertículo de Meckel.
Salud Tabasco 2002;8:51-57.
Erdener A, Ozok G, Herek O, Arikan A. Abdominal complications of Ascaris lumbricoides in children. J Pak Med Assoc
1992;42:73-74.
Rodríguez GA, Belmares TJ, Hernández SJ. Factores de
riesgo para oclusión y suboclusión intestinal por Áscaris
lumbricoides. Cir Ciruj 2004;72:37-40.
Álvarez-Solís RM, Gutiérrez-Lucatero S, Vargas-Vallejo MP,
Quero-Hernández A, Bulnes-Mendizábal D, Hernández SJ.
Diferencias clínicas entre oclusión y suboclusión intestinal por
Áscaris que puedan sugerir cirugía. Pediatr Mex 2010;12:1117.
Wani I, Maqbool M, Amin A, Shah F, Keema A, Singh J,
et al. Appendiceal ascariasis in children. Ann Saudi Med
2010;30:63-66.
Álvarez-Solís RM, Graham-Zapata LF, Montalvo-Marín A,
Ulloa-Patiño P, Vargas-Vallejo MP. Apendicitis aguda asociada a parásitos en el apéndice. Bol Med Hosp Infant Mex
1999;56:10-17.
21.
22.
23.
24.
25.
26.
27.
28.
Chawla A, Patwardhan V, Maheshwari M, Wasnik A. Primary
ascaridial perforation of the small intestine: sonographic diagnosis. J Clin Ultrasound 2003;31:211-213.
De la Fuente-Lira M, Molotla-Xolalpa C, Rocha-Guevara ER.
Biliary ascariasis. Case report and review of the literature. Cir
Cir 2006;74:195-198.
Kenamond CA, Warshauer DM, Grimm IS. Ascaris pancreatitis.
Radiographics 2006;26:1567-1570.
Kumar V. Parasitic invasion of the lacrimal sac. Vestn Oftalmol
2003;119:45-46.
Zamora-Almeida O. Localization of Ascaris lumbricoides in
the thoracic cavity. Report of a case. Rev Cubana Med Trop
1976;28:71-75.
Nadler EP, Reblock KK, Vaughan KG, Meza MP, Ford HR,
Gaines BA. Predictors of outcome for children with perforated
appendicitis initially treated with non-operative management.
Surg Infect (Larchmt) 2004;5:349-356.
Newman K, Ponsky T, Kittle K, Dyk L, Throop C, Geiseker K,
et al. Appendicitis 2000: variability in practice, outcomes, and
resource utilization at thirty pediatric hospitals. J Pediatr Surg
2003;38:372-379.
Ibrahim-Ibrahim A. Prolapsed ileocolic intussuception. Ann
Pediatr Surg 2011;7:76-78.
Vane DW, West KW, Grosfeld JL. Vitelline duct anomalies. Experience with 217 childhood cases. Arch Surg 1987;122:542547.
Park JJ, Wolff BG, Tollefson MK, Walsh EE, Larson DR. Meckel
diverticulum: the Mayo Clinic experience with 1476 patients
(1950-2002). Ann Surg 2005;241:529-533.
Holland CV. Predisposition to ascariasis: patterns, mechanisms
and implications. Parasitology 2009;136:1537-1547.
Goyal A, Vishwakarma SK, Kumar R. Abnormal migration
of ascaris to the middle ear. Indian J Pediatr 1998;65:147148.
Baeza HC, Godoy EA, Sánchez FL, García CL, Nájera GH. Coledocoascariasis. Bol Med Hosp Infant Mex 2002;59:786-791.
Diago-Caballero D, García-Valdés R, Salabarria-Fernández
M. Áscaris lumbricoides en el corazón de una gestante. Rev
Cubana Obstet Ginecol 2011;37:243-250.
Cáceres Z, Arredondo C, González I, Landaeta N, Moreno
E, López C, et al. Absceso hepático ascardiano en la migración errática de Áscaris lumbricoides en niños. Rev GEN
2007;61:262-265.
González AH, Regalado VC, Van den Ende. Non-invasive
management of Ascaris lumbricoides biliary tract migration: a
prospective study in 69 patients from Ecuador. Trop Med Int
Health 2001;6:146-150.
Vargas-González R, Camacho-González C, García-Galicia A.
Clinical images in gastroenterology. Perforation of Meckel’s
diverticulum by Ascaris lumbricoides. Rev Gastroenterol Mex
2005;70:324.
Hopkin J. Immune and genetic aspects of asthma, allergy and
parasitic worm infections: evolutionary links. Parasite Immunol
2009;31:267-273.
Keiser J, Utzinger J. Efficacy of current drugs against soiltransmitted helminth infections: systematic review and metaanalysis. JAMA 2008;299:1937-1948.
Llop-Hernández A, Valdéz-Dapena VM, Zuazo-Silva JL.
Ascaris. Microbiología y Parasitología Médicas. La Habana:
Editorial Ciencias Médicas; 2001.
Bol Med Hosp Infant Mex
Bol Med Hosp Infant Mex 2012;69(6):575-588
Clinicopathological case
Acute respiratory failure secondary to Bordetella pertussis infection in a
4-month-old infant
Sarbelio Moreno Espinosa,1 Bárbara Inés Morales Mérida,2 Carlos Alberto Serrano Bello,3 Orlando
Domínguez Pacheco,4 Olga Camaño Andrade,5 Rubí Rojas Padilla,5 Ernesto Calderón Jaimes6
SUMMARY OF THE CLINICAL HISTORY (A-11-10)
We report the case of a 4-month-old infant who presented
to the Emergency Service due to a clinical picture of cough
and rhinorrhea.
The patient was fed exclusively with maternal breast milk.
She followed eye movements from 1 month of age, social
smile was noted and she was able to hold her head up at
2 months of age. She received immunization with bacilli
Calmette-Guerin (BCG) and hepatitis B at birth but did
not receive the remainder of the vaccines.
Family History
The patient’s mother is a 32-year-old healthy, married housewife with a primary education. The father is a healthy,
32-year-old male with a primary education and works as
a driver. Four siblings aged 8 to 15 years were reported
as healthy. Both maternal and paternal grandparents have
diabetes mellitus.
Nonpathological History
The family has a low socioeconomic status. They are
originally from and reside in Iguala, Guerrero. They live
in their own home with four rooms to accommodate six
people. There is no potable water or drainage. There are
adequate hygiene facilities. The home is shared with a dog.
1
2
3
4
5
6
Departamento de Infectología,
Departamento de Terapia Intensiva,
Departamento de Imagenología,
Departamento de Patología,
Departamento de Pediatría,
Subdirección de Servicios Auxiliares de Diagnóstico, Hospital
Infantil de México Federico Gómez, México D.F., México
Correspondence: Dr. Sarbelio Moreno Espinosa
Departamento de Infectología
Hospital Infantil de México Federico Gómez
México, D.F., México
E-mail: [email protected]
Received for publication: 10-23-12
Accepted for publication: 10-30-12
Vol. 69, November-December 2012
Perinatal and Pathological History
The patient was the product of a fifth pregnancy. The
mother received prenatal care from the second month
of gestation with folic acid and iron intake and tetanus
toxoid was given. Two obstetrical ultrasounds were done
and reported as normal. Term delivery took place at the
hospital and the newborn had a birth weight of 3500 g. The
mother was discharged at 24 h without complications. The
mother denied any history of allergies, surgeries, trauma,
transfusions or exanthems.
Present Illness
The patient’s current condition began 27 days prior to her
hospital admission with sudden nonprogressive, watery
rhinorrhea along with sneezing. Seven days later she
presented with long bouts of coughing 20 days before
admission, which began suddenly, becoming progressive
and with respiratory pause at the end. No time schedule
was noted or cyanosis, dyspnea or hemoptysis.
February 12, 2011
The patient was seen at a second-level care hospital with
progressive cough, cyanosis, and without hemoptysis.
Blood test was performed and showed leukocytes of
40,000, increasing to 78,000 at 48 h. Chest x-ray was done
and showed bilateral perihilar infiltrate and air trapping.
Antibiotic treatment was administered with erythromycin
575
Sarbelio Moreno Espinosa, Bárbara Inés Morales Mérida, Carlos Alberto Serrano Bello, Orlando Domínguez Pacheco, Olga Camaño
Andrade, Rubí Rojas Padilla, Ernesto Calderón Jaimes
for 1 day as well as ambroxol and micronebulizations.
The patient was referred to Hospital Infantil de México
Federico Gómez (HIMFG) with the diagnosis of coqueluchoide syndrome. There were three similar cases reported
in the referral hospital during the same time period with
two deaths.
February 14, 2011
The patient was admitted to HIMFG.
Physical Examination
Physical examination demonstrated a well-hydrated female whose appearance matched her chronological age,
normocephalic without depressions or exostosis. Eyes
and pupils were reactive and symmetrical. Nostrils were
permeable and ears were properly placed with intact
tympanic membranes. Pharynx was hyperemic without
exudate, posterior discharge or lesions of the oral cavity.
Neck was cylindrical without adenopathy. Thorax was in
alignment, respiratory movements were preserved and with
thoracoabdominal dissociation. Lung fields demonstrated
fine crepitant basal rales. Wheezing was absent, expiration
was prolonged and lung fields were clear to percussion.
There was normodynamic precordium without murmurs
or added sounds. Abdomen was soft, depressible, and nontender with peristalsis. Liver was at 2-0-0 cm of the costal
border. Extremities were symmetrical with redundant
folds. There was preserved capillary refill and peripheral
pulses. The patient was alert and reactive without neurological deterioration (Table 1).
Laboratory Analysis
Table 2 shows the results of the laboratory analysis.
Chest X-ray
There was horizontalization of the costal arches in the
eighth intercostal space and bilateral perihilar infiltrate
with image of “hairy heart.”
Management
The patient was managed with fasting, base solutions (150
ml/kg/day), glucose (6 g/kg/min), sodium and potassium
(3 mEq/kg/day), calcium (100 mg/kg/day), magnesium (50
mg/kg/day), erythromycin (50 mg/kg/day), benzonatate (8
mg/kg/day), and oxygen with face mask (9 l/min).
576
February 15, 2011
The patient was evaluated by the Infectious Disease Service. Heart rate was 147/min. Respiratory frequency was
48/min. Blood pressure was 90/60 mmHg. Temperature
was 36.2°C. The patient was admitted with face mask at
9 l/min, epidemiology was notified and serology for B.
pertussis was requested. Patient continued with tachypnea, tachycardia, prolonged bouts of coughing, dyspnea,
cyanosis and hemoptysis, with thoracoabdominal dissociation and intercostal retraction. The same management
was continued with face mask at 10 l/min.
February 16, 2011
At 00:16 h the patient experienced prolonged coughing with
respiratory difficulty, perioral cyanosis, tachycardia (40/min)
and 20% O2 saturation. Cardiac rhythm was recovered with
basic resuscitation maneuvers. Rapid intubation was done on
the second attempt and there were abundant secretions and
edema of the vocal cords. Mechanical assisted ventilation
was begun with fentanyl and midazolam and the patient was
admitted to the intensive care unit. At 03:00 h, in the intensive
therapy unit, a central venous catheter was placed: PVC (1
cm H2O). Due to low output, the patient was managed with
crystalloids (20 mL/kg/dose) (2), PVC 7 H2O but without
clinical improvement. Dobutamine was given with discrete
improvement, adding norepinephrine and milrirone. The
antibiotic was changed to clarithromycin (Table 3).
Chest X-ray
Right basal opacity suggestive of consolidation was demonstrated on chest x-ray (Figure 1). At 1600 h the patient
was reported to be in critical condition. Department of Infectious Diseases suggested broadening empiric coverage
against S. pneumoniae, H. influenzae type B and S. aureus,
with cefotaxime (150 mg/kg/day) and dicloxacillin (100
mg/kg/day) (Figure 2).
February 17, 2011
At 1100 h the patient’s vital signs were blood pressure
(average 47 mmHg) with 4-sec capillary refill. The patient
had tachycardia, which did not improve with the administration of crystalloids and albumin. Dobutamine, milrinone
and norepinephrine were continued at the maximum dose
without improvement. Hydrocortisone, vasopressin at a
dose for physiological restitution with gradual increase up
Bol Med Hosp Infant Mex
Acute respiratory failure secondary to Bordetella pertussis infection in a 4-month-old infant
Table 1. Antropometry and vital signs
Weight
Length
CF
RF
SAP
Temperature
CP
Glasgow
5,500 g
55 cm
168/min
60/min
85/55 mmHg
37.4°C
39 cm
15
CF, cardiac frequency; RF, respiratory frequency; SAP, systemic arterial pressure; CP, cephalic perimeter.
Table 2. Laboratory results (2-14-11)
Hemoglobin
Hematocrit
Leukocytes
Lymphocytes
Bands
Neutrophils
Platelets
Monocytes
Eosinophils
11.2 g/dL
Sodium
33.3%
Potassium
86,900/mm3
Chloride
42%
Calcium
16%
Phosphorus
32%
Viral panel
563,000
Bun
6%
Creatinine
4%
Uric acid
136 mEq/L
4.6 mEq/L
104 mEq/L
9.1 mg/dL
5 mg/dL
Negativo
4 mg/dL
0.3 mg/dL
3.3 mg/dL
Table 3. Laboratory results (2-16-11)
Hemoglobin Hematocrit Leukocytes Lymphocytes
10.8 g/dL
IB
32.6%
TB
0.21 mg/dL 0.21 mg/dL
BUN
Sangre
Orina
Bands
Neutrophils Platelets
PT
107,900/mm3
ALT
48%
AST
14%
Albumin
32%
T protein
498,000
pH
14.8”
PaO2
33 U
Creat
36 U
Na
2 g/dL
K
3.7 g/dL
Cl
7.3
Ca
120
P
2 mg/dL
0.4 mg/dL
121 mg/dL 18.1 mg/dL
PTT
INR
Uric acid
DB
76.8” 1.15” 1.3 mg/dL 0.06 mg/dL
PaCO2 HCO3
LDH
48.8
23.7
1.7
127 mEq/L 4.1 mEq/L 99 mEq/L 9.3 mg/dL 3.9 mg/dL
69 mEq/L 33.1 mEq/L 74 mEq/L 61.8 mg/dL
DB, direct bilirubin; IB, indirect bilirubin; TB, total bilirubin; PT, prothrombin time; PTT, partial thromboplastin time; ALT, alanine aminotrans
ferase; AST, aspartate aminotransferase; LDH, lactate dehydrogenase; INR, international normalized ratio.
to 0.0012 U/kg/h and norepinephrine (2 U/kg/min) were
begun. There was positive fluid balance and urine output
decreased from 5.1 to 1.5 mL/kg/h during the previous
night. With hyponatremia and elevated sodium/urea, a
correction was made to delta 10. For hyperglycemia, glucose was reduced in the solutions. The patient presented
an increase in creatinine (from 0.4-0.7 mg/dL), oliguria
and metabolic acidosis and bicarbonate was administered.
Mechanical assisted ventilation was continued with high
parameters. Due to hemoglobin of 7 g/dL, the patient was
transfused with red blood cells at 10 ml/kg/dose (Figure 3).
February 18, 2011
At 1350 h, the patient had anuria during the previous 4
h without dialysis. At 1600 h, in intensive therapy department, the patient had bradycardia, hypotension and
sudden desaturation with a decrease in central and periVol. 69, November-December 2012
pheral pulses. Adrenalin was administered and PVC 1-5
cm H2O was continued due to probable right heart failure.
Levosimendan was begun. There was frank pulmonary
edema, increase in ventilatory parameters, high index of
oxygenation and decreased Kirby index, and episodes of
bronchospasm that improved with salbutamol. The patient
continued with anuria and metabolic acidosis and a catheter was placed for initiating peritoneal dialysis (Table 4).
At 1800 h, a rigid catheter was placed and abundant
clear fluid was obtained. Peritoneal dialysis was performed
with standard solution at 18.8 ml/kg/dose for 2 h in the
cavity, alternating with hypertonic solution for 1 h in the
cavity, with some neutral and negative balance.
February 19, 2011
At 2:45 h, the patient had cardiorespiratory arrest without
response to 15-min resuscitation maneuvers.
577
Sarbelio Moreno Espinosa, Bárbara Inés Morales Mérida, Carlos Alberto Serrano Bello, Orlando Domínguez Pacheco, Olga Camaño
Andrade, Rubí Rojas Padilla, Ernesto Calderón Jaimes
A
B
Figure 2. (A) Follow-up projections of the same day. There is an
increase in interstitial as well as reticulonodular infiltrate. (B) At
the right apical level there is a zone of condensation. There is a
decrease in intestinal gas.
Department of Radiology (Dr. Orlando Dominguez
Pacheco)
Figure 1. Thoraco-abdominal projection (2-6-11). Patchy, bilateral
diffuse interstitial infiltrate is observed. At the level of the abdomen,
abundant intestinal gas is observed.
Case Report
Coordinator (Dr. Sarbelio Moreno Espinosa)
We report the case of a patient from the state of Guerrero with a 4-day hospitalization at the HIMFG. During
this period the patient presented multiple complications
secondary to her basic condition, requiring evaluation
by several of our hospital services. This was a multidisciplinary case with a great deal to learn from the events
of her illness. At the same time, this case is reminiscent
of a condition that is sometimes forgotten but which has
become very timely.
578
Classic findings of Bordetella pertussis infection demonstrated on chest x-rays consist of diffuse bilateral reticular
opacities that can coalesce into ground-glass opacities with
air bronchogram, complicated by atelectasis.1
Radiographically, these findings are indistinguishable from those observed in patients with various viral
respiratory tract infections or other pathogens that cause
disease, primarily bronchial and peribronchial disease as
observed in mycoplasma infections, Chlamydia and viral
infections.2,3
Chief of the Department of Evaluation and Drug Analysis
(Dr. Luis Jasso Gutiérrez)
The patient’s clinical history mentioned the presence of
“hairy heart.” Our colleagues who recall whooping cough
are accustomed to seeing this image. In this patient, was
this image there?
Department of Radiology (Dr. Orlando Dominguez
Pacheco)
Reference is made to the ill-defined heart border due to
perihilar and peribronchial infiltrate.
Discussion (Dr. Barbara Ines Morales Merida)
The patient was a 4-month-old female whose condition
evolved during a 27-day period of her and 4 days of hosBol Med Hosp Infant Mex
Acute respiratory failure secondary to Bordetella pertussis infection in a 4-month-old infant
Figure 3. Thoraco-abdominal projections (2-17-11). Increased infiltrate effacing cardiac borers and hemidiaphragms. Minimal intestinal
gas. Increase in volume of soft tissue.
Table 4. Laboratory results (2/18/11)
Hemoglobin Hematocrit Leukocytes Lymphocytes
7.3 g/dL
Glucose
21.6%
BUN
103,300/mm3
Creatinine
25%
DB
170 mg/dL
DB
4 mg/dL
IB
0.7 mg/dl
TB
125 mEq/L
ALT
0.14 mg/dL 0.02 mg/dL 0.16 mg/dL
18 U
Bands
Neutrophils
Platelets
PT
PTT
INR
Fibrin
28%
IB
36%
TB
351,000
Mg
40.5”
>120”
3.42”
113 mg/dL
1.6 mg/dL
Cl
Mg
pH
PaO2
PaCO2
HCO3
2.5 g/dL
3.1 g/dL
7.04
227
45.1
11.7
3.5 mEq/L 97 mEq/L
Na
K
16 U
40 U
CPK, creatinine phosphokinase (see Table 3 for other abbreviations).
pitalization in this institution. The following syndromatic
diagnoses were integrated:
1. Coqueluchoide syndrome—characterized by sudden
onset of cough that was progressive, productive,
cyanotic, dyspneic and with hemoptysis. There were
long bouts of coughing with respiratory pause at the
end.
2. Respiratory distress syndrome (RDS)—characterized by tachypnea, thoracoabdominal dissociation,
fine basal rales and intercostal retractions.
3. Systemic inflammatory response (SIR) syndrome—
characterized by tachycardia, tachypnea and elevated leukocytes.
Based on these syndromatic diagnoses as well as the
findings and results evidenced during its evolution, the
following nosological diagnoses were integrated:
1. Pertussis— presence of coqueluchoide syndrome,
RDS, hyperleukocytosis, and x-rays with evidence of
Vol. 69, November-December 2012
air trapping, bilateral perihilar infiltrates and image of
“hairy heart” as well as a history of three similar cases
in the referral hospital with the death of two children.
2. Lobar pneumonia—respiratory distress without improvement after initial treatment, evolving to respiratory failure, in addition to the SIR and hypoperfusion and x-rays suggestive of consolidation.
3. Septic shock refractive to catecholamines—shown
by data of sepsis with cardiovascular dysfunction
and hypotension, without relief after i.v. fluid administration, vasoactive drugs, or steroids.
4. Multiple organ failure—based on the history of refractory septic shock and data of cardiovascular, hematological, renal and lung dysfunction.
Important Points in the Evolution and Treatment of the
Patient during Hospitalization
The patient had a history of living at home with her parents and siblings, some of whom were adolescents. The
579
Sarbelio Moreno Espinosa, Bárbara Inés Morales Mérida, Carlos Alberto Serrano Bello, Orlando Domínguez Pacheco, Olga Camaño
Andrade, Rubí Rojas Padilla, Ernesto Calderón Jaimes
latter are risk factors for disease transmission because
even though they may have had whooping cough or were
immunized during infancy, immunity is not conferred
for a lifetime, resulting in a risk of contagion to certain
age groups. Overcrowding was observed, lack of potable
water and no drainage, increasing the risk of transmission
of infectious diseases.
The vaccination scheme was incomplete as the patient
had only BCG and one dose of hepatitis B. At her age, this
patient should have had BCG, two doses of hepatitis B,
two doses of acellular pentavalent including diphtheria,
pertussis and tetanus (Tdap), polio (IPV) and H. influenzae type B (HiB), two doses of rotavirus and two doses
of conjugated pneumococcus. Furthermore, although the
patient was breastfed, this does not provide immunoprotection for pertussis.
Given this background and the patient’s clinical history,
notification should have been made to epidemiology and
serology for B. pertussis from the time of admission to
the emergency room. The patient’s clinical history noting
that 20 days prior to her admission she presented with a
7-day evolution of watery rhinorrhea should have been
taken into consideration from the time of admission to
the emergency room—which corresponds to the catarrhal
period described in whooping cough and later begins with
cough, the characteristics of which are previously described and are typical of this disease and that already have
an evolution of 20 days (corresponding to the paroxysmal
period). Also, the absence of fever during the course of
the illness is notable and is another important piece of
information that may lead one to think of this diagnosis
and to rule out other etiologies such as viral. Finally, I will
mention the findings of hyperleukocytosis with lymphocytosis that were seen in the disease due to the pertussis
toxin that increases sensitivity to histamine and promotes
leukocyte dysfunction, recruiting lymphocytes that remain
in the circulation; thus, the typical, previously described
radiological findings of air trapping, perihilar infiltrate
and image of “hairy heart.” However, it was evident that
upon the patient’s admission, she had fever, respiratory
difficulty and fine crepitant basal rales atypical of whooping cough. Also, younger patients may usually develop
complications such as pneumonia and cultures should be
taken. Empiric antibiotic treatment should be initiated for
the most common bacteria seen at the age of this patient.
Treatment should be initiated with nebulization to decrease
580
bronchospasm, air trapping and, as a consequence, the frequency of bouts of coughing, emesis and hypoxia. Above
all, consideration should have been given that the high
risk factors in this infection are that they be <6 months
(because it is in this age group that 90% of the fatalities
due to B. pertussis present themselves and is common
for complications to develop, such as pneumonia of viral
or bacterial origin, as pertussis generally does not affect
the lower respiratory tracts) and that leukocyte counts
are >50,000. Association between pneumonia due to B.
pertussis and magnitude of the leukocytosis is described,
which represents a poor prognosis.
Another consideration is that at no time was there a
pulse oximetry done to assess the peripheral saturation
despite the degree of respiratory distress, in spite of it
being a practical, accessible, inexpensive and noninvasive measure for adequate monitoring and to evaluate the
response to treatment with oxygen. Because the patient
was at high risk for the previously mentioned reasons,
in addition to respiratory distress that did not improve
with oxygen therapy and that among the most frequent
complications for admission to intensive care was pulmonary hypertension (which occurs due to leukostasis and
hypoxemia), she should have been admitted to intensive
care from that time for strict monitoring, assessment of
endotracheal intubation and blood transfusion or leukopheresis, as the number of white blood cells continued
to rise.
It is noteworthy that despite the increase in the flow of
O2, the patient continued with increased respiratory distress and no other intervention was performed. I believe
that an arterial blood gas should have been performed
to again evaluate respiratory function because there was
absence of clinical improvement or of PaO2. Whether or
not there was hemodynamic stability, a new intervention
should have been carried out which, in this case, would
have been through programmed orotracheal intubation
so as to limit tissue damage due to hypoxia and prevent
development of pulmonary hypertension. It is dangerous to
assume that the administration of supplemental oxygen is
sufficient to correct a picture of hypoxemia without taking
into consideration additional causes of hypoxia, as the
availability of O2 depends as much on the administration
of O2 as ventilation, of the O2 concentration, O2 saturation
and cardiac output. Each cause should be corrected at once,
but all need to be corrected.
Bol Med Hosp Infant Mex
Acute respiratory failure secondary to Bordetella pertussis infection in a 4-month-old infant
As is expected due to the natural history of the disease,
there was respiratory insufficiency precipitated by a picture
of coughing bouts, which led to severe desaturation and
bradycardia, and then led to laryngospasm or vagal stimuli,
making it necessary to perform an urgent intubation in an
untimely manner. Shock presented itself, which may have
been of septic origin or secondary to a cardiac lesion due
to hypoxia. Nevertheless, antibiotics should have been
administered because it has been shown that in cases of
septic shock there is a direct impact on the decrease in
mortality with the use of antibiotics during the first hour.
Once in intensive care, being intubated and in a state
of shock, it was decided to change the antibiotic from
erythromycin to clarithromycin, which is proven to be
effective in whooping cough. It is assumed that the change
was to go from oral antibiotics to i.v. because of the low
absorption of the mucosa during shock. However, one
must remember that the aim of early administration is to
decrease transmission. The infectious period is usually in
the catarrhal stage and the first 3 weeks when live bacteria
still exist; however, in our patient the administration was
delayed. Therefore, clinical improvement or decrease in
transmission was not expected. Initial blood gas analysis
showed mild respiratory acidosis with acidemia and a
Kirby index of 120, which is in relation to the amount
of pulmonary short circuits that do not permit adequate
oxygenation. This translates as acute respiratory distress
syndrome (ARDS), indicated from the outset that there
was a high degree of lung injury with a predisposing
factor for the development of pulmonary hypertension
and, therefore, a determining factor in the evolution
and outcome of the patient. In severe infections due to
B. pertussis, it is reported that patients presenting with
treatment-refractory pulmonary hypertension, especially
those with WBC counts >60,000, experience a severe disease course with a poor outcome. Echocardiogram should
have been requested to assist with diagnosis and to guide
disease management.
Hemodynamically, the patient showed little response to
bolus administration of crystalloid solutions and presented
data of heart failure due to elevation of preventricular contractions without clinical improvement. Vasoactive amines
were begun (inotropic and vasopressor) as described in
the guidelines for management of septic shock (2005),
with a slight recovery. However, the patient presented
with hypotension. This is an indication that the compenVol. 69, November-December 2012
satory mechanisms are exhausted and that the approach
to the shock was probably delayed, or that the patient has
pulmonary hypertension manifested by hypotension and
right heart failure. Because of the continued instability,
new fluid boluses were again administered, this time also
colloids, which is not indicated in a patient with data of
right heart failure because it increases risk of pulmonary
edema. However, response to the intervention was inadequate and the patient continued to deteriorate, requiring
maximal doses of amines and initiation of vasopressin at
physiological doses (as described in the study of Carcillo)
to counter the depletion of reserves of vasopressin and
improve vasomotor tone. Hydrocortisone was also initiated
as indicated in the guidelines for management of septic
shock, in order to improve the hemodynamic variables
and decrease the requirement for vasopressors as cortisol
levels improve.
Also, increase in serum creatinine, FENa of 1.22 and
BUN/creatinine index ratio of 5 was observed, which
points to acute renal injury probably due to shock. Strict
control of urinary output and fluid balance should have
been done. The patient then presented with oligoanuria,
metabolic acidosis, doubling of serum creatinine, positive fluid balance and data of acute pulmonary edema.
Consultation with the nephrology department should then
have been done to initiate renal replacement method. The
indication, in this case, was renal failure with oligoanuria
and hypervolemia plus cardiac failure. It has been observed
that early onset of renal replacement method in patients
with heart failure improves survival.
Hyponatremia with elevated urine sodium is notable and may have been related to the administration of
crystalloid boluses (probably physiological solution) and
fluid retention due to renal failure, which translates to
hypervolemic hyponatremia—in which case there is a fluid
overload, not a sodium deficit. For this reason, treatment
should be on the basis of fluid restriction. It is concluded
that the sodium correction done was not indicated. Finally, a peritoneal dialysis catheter was placed and large
amounts of clear liquid were obtained, probably because
of the fluid leak secondary to endothelial lesion due to
shock. At that time it was impossible to rule out the presence of a capillary leak toward virtual spaces such as the
pleura, pericardium or interstitium, which would worsen
the prognosis. The ideal method for this patient, because
of the hemodynamic instability, was to carry out hemo-
581
Sarbelio Moreno Espinosa, Bárbara Inés Morales Mérida, Carlos Alberto Serrano Bello, Orlando Domínguez Pacheco, Olga Camaño
Andrade, Rubí Rojas Padilla, Ernesto Calderón Jaimes
diafiltration. However, this was not available; therefore,
peritoneal dialysis was begun as a rescue measure because
the patient would not have tolerated the fluid exchanges
of hemodialysis. Peritoneal dialysis was started. However,
because the indication was hypervolemia, it should have
been done with a hypertonic solution and more frequent
exchanges to extract fluids and negate the balance with a
minimal volume of 20 ml/kg per exchange. Considering
the low cardiac output, poor pulmonary function and
hypoperfused peritoneum as demonstrated by this patient,
probability of worsening hemodynamic conditions and
causing greater ventilatory restriction (mechanical) was
very high and the probability of it being successful as a
dialysis measure was very low.
Final diagnoses were as follows:
• Eutrophic female infant
• Infection due to Bordetella pertussis
• Acute lobar pneumonia
• Acute respiratory distress syndrome
• Probable pulmonary hypertension
• Septic shock refractory to catecholamines
• Disseminated intravascular coagulation
• Multiple organ failure due to
• Acute respiratory infection
• Cardiovascular dysfunction
• Pulmonary dysfunction
• Hematological dysfunction
with pneumonia can develop hypervolemic hyponatremia
and, the more severe the pneumonia, the greater the risk
of developing this condition.
Department of Integrated Patient Care (Dr. Erick Rosales
Uribe)
Some important aspects that were not elaborated were the
risk factors. Children <4 months presenting with leukocytosis and/or thrombocytosis have a high probability of
death, close to 90%, or as expressed in another way, 90%
of children who die are <4 months old. Serology was not
the most appropriate method for detection of B. pertussis
in this patient. The possibility of requesting PCR should
have been planned for or, failing that, a culture—although
this is not the most suitable method. An important fact is
mentioned about prevention and the high level of success
of vaccination campaigns with coverage for the first dose
between 95% and 96% and up to the fourth dose of ~95%.
Because of this, we see B. pertussis less frequently in
children although we do see other types of Bordetella.
Coordinator (Dr. Sarbelio Moreno Espinosa)
Additional Information
Multiplex PCR results (Respifinder): sample from February 15, 2011
1) B. pertussis
2) Coronavirus OC43
Causes of death were as follows:
• Respiratory failure secondary to B. pertussis
infection
• Multiple organ failure
15 days later: serological test results (described as
serology by InDRE with unknown origin)
1) Bordetella pertussis
2) Enterovirus
Subdirector of Ambulatory Pediatrics (Dr. Edgar Bustos
Cordova)
We considered doing this in an open session due to the
obvious diagnosis, but for clinical practice and because
the etiology, outcome and prognosis were unknown, we
decided to leave this information to the end.
When referring to management of hyponatremia, the term
“dilution” is no longer used. Today we mention hypervolemic hyponatremia and, obviously, as mentioned, the
patient developed hyponatremia due to excess fluid administration. In addition, the studies were poorly evaluated.
Elevated urinary sodium represents a hypervolemic (not
hypovolemic) hypernatremia. We would be least interested in additional sodium intake. Usually, in these cases,
a high sodium intake worsens, rather than improving, the
condition as occurred in this patient. An additional factor
is that it is reported that up to 25% of cases of patients
582
Pathological Findings (Dr. Carlos Alberto Serrano Bello)
We describe a normally developed female weighing 5500
kg with a height of 58 cm who presented with a sutured,
infraumbilical wound (0.7 x 0.7 cm) without apparent
alterations and with generalized edema. Upon neck
dissection, the trachea and epiglottis showed significant
edema (Figure 4) which, together with the thickness of
the secretions, caused the characteristic cough of the desBol Med Hosp Infant Mex
Acute respiratory failure secondary to Bordetella pertussis infection in a 4-month-old infant
Figure 4. Edematous epiglottis.
cribed disease as well as congestion of the lower mucosa.
On histological cuts we observed minimal intraepithelial
inflammatory infiltrate apoptosis of some respiratory cells.
Bilateral pleural effusion (45 mL) was found in the thoracic
cavity. Lung parenchyma showed extensive reddish-brown
areas of consolidation and indistinct borders involving
both lungs, predominantly basal (Figure 5). Trachea and
main bronchi exhibited only congestion. In histological
sections, we observed that the majority of the alveolar
spaces were filled with an intense inflammatory infiltrate,
which consisted mainly of neutrophils with formation of
microabscesses, necrosis of pneumocytes, cellular debris
and intraalveolar edema (Figure 6).
To understand the damage to the respiratory epithelium
caused by microorganisms, we must remember the primary
defense mechanisms present in the respiratory system,
which can be synthesized for practical purposes into four
major factors:
1. The respiratory epithelium itself, due to its available
and histological nature, is arranged in a pseudostratified manner and with strong intercellular junctions
that function as a mechanical barrier against aggressive pathogens
2. Goblet cells, epithelial cells and mucus-secreting
glands project towards the lumen of the bronchial
Vol. 69, November-December 2012
Figure 5. Pulmonary parenchyma with multiple areas of consolidation.
Figure 6. Histological cut with alveolae occupied by inflammatory
infiltrate, cellular detritus and mucus.
tree mucosa, which added to cilia propulsion act as
an efficient means of sweeping, but also produce
~100 chemical substances with antimicrobial effect
such as defencins, lysozyme, lactoferrin, nitric oxide, IgA, etc.4,5
3. Toll-like receptors (or TLR2) that, without need of
opsonins, directly recognize the microorganisms
and, in turn, activate nuclear transcription factors
583
Sarbelio Moreno Espinosa, Bárbara Inés Morales Mérida, Carlos Alberto Serrano Bello, Orlando Domínguez Pacheco, Olga Camaño
Andrade, Rubí Rojas Padilla, Ernesto Calderón Jaimes
and interferon pathways that activate or regulate the
cellular immune response
4. Finally, there are the intracytoplasmic receptors such
as MDA5, which directly detect microorganisms including virus5 and these receptors can also activate
the interferon pathway (Figure 7)
Now, when infection exists, microorganisms and virus
have the capacity of altering the first immune response so
that certain viruses can increase mucus production and
cause it to be thicker, making ciliary movement difficult
and fostering stagnation of the mucus. This functions as
a growth medium for other bacteria, facilitating their adherence to the epithelium as well as hindering molecular
bactericidal activity. Other bacteria have the ability of
producing certain molecules such as STAT and IFR3 that
block the interferon pathway, which impedes regulation of
the immune response.5 These bacteria also have proteolytic
enzymes that degrade the intercellular junctions, thereby
causing loss of integrity of the epithelium and facilitating
invasion by microorganisms. Other microorganisms are
conducive to overexpression of receptors such as I-CAM
and C-CAM (Figure 8) that facilitate bacterial adhesion,
causing superinfection.5
Moreover, B. pertussis has characteristic enzymes that
aggravate the histopathological status of the respiratory
epithelium such as pertussis toxin, filamentous hemagglutinin (FH), and pertactin, which make it more conducive to
adhesion of bacteria to the respiratory epithelium. LPS and
toxins cause cell death, adenylate cyclase toxin interferes
with proper leukocyte activation, and tracheal cytotoxin
acts on the inhibition of the ciliary motility.6 Table 5
summarizes the mechanisms of action of these toxins.
In making a correlation, with alterations of the primary
immune response and the action of toxins and enzymes
that characterize B. pertussis, we can explain the observed
histological changes in the lung, i.e., alveoli are filled with
inflammatory cells. These are probably not fulfilling their
function by interference of the adenylate cyclase enzyme.
The presence of cellular debris, mucus and epithelial necrosis is favored by toxins such as dermonecrosis, LPS, and
the pertussis toxin itself, in addition to ciliostasis (probably
produced by the action of tracheal cytotoxin) and prevents
clearance of these same components. This inevitably leads
to poor gas exchange and, therefore, the state of complete
tissue hypoxia in the patient (Figure 9). The remainder of
the organs showed signs of shock secondary to a persistent
584
Figure 7. Primary defense mechanisms of respiratory epithelium.
Figure 8. Overexpression of receptors such as I-CAM and C-CAM
that facilitate bacterial adhesion, resulting in superinfection.
state of hypoxia and hypoperfusion to which the patient
was subjected (Table 6). In the myocardium, vacuolization
of cardiomyocytes with macronucleation was observed. In
the thymus there was calcification of Hassall’s corpuscles
and reduction of lymphoid tissue. In the digestive tract,
characteristic changes of hypoxic intestinal myopathy were
observed characterized by contraction bands that refer to
the alternating pattern of cytoplasmic staining between
muscle fibers with ischemia and others more viable or
better perfused. Macroscopically, the liver showed no
abnormalities. In histological sections, microvesicular
steatosis and dilated sinusoids were observed. In the spleen
there was a decrease in lymphoid tissue in the white pulp
and dilation with sinusoidal congestion. Pancreas and adrenals showed no gross or microscopic abnormalities. There
was medullary congestion in the kidneys and microscopy
showed acute tubular necrosis characterized by lysis and
detachment of the tubular epithelium. No morphological
Bol Med Hosp Infant Mex
Acute respiratory failure secondary to Bordetella pertussis infection in a 4-month-old infant
Table 5. Actions of virulence factors of Bordetella pertussis in the
respiratory epithelium
Virulence factor
Biological effects
Pertussis toxin
Protein fixation (interference with signal
transmission)
FHA
Media adherence to epithelial
LPS
Pertactin
Activity of endotoxin
Adherence to epithelial and
immunogenic cells
Contracción de musculo liso vascular
Alterations of chemotaxis and
leukocyte function
Ciliostasis
Changes in the synthesis of DNA
of cellular cilia
Dermonecrotic toxin
Adenylate cyclase toxin
Tracheal cytotoxin
LPS, lipopolysaccharide; FHA, Filamentous hemagglutinin.
alterations were observed in the central nervous system.
However, in histological cuts, changes were demonstrated such as clear pericellular and perivascular halos with
pyknosis of a variable number of neurons. Bone marrow
showed secondary myeloid hyperplasia or a response to
the acute inflammatory process experienced by the patient.
As an independent finding, there were multiple cystic
follicles in the ovaries. Results of postmortem culture
media were negative, although it must be kept in mind
that the B. pertussis bacteria grow on special media such
as Regan Lowe or Bordet Gengou.
As a principal disease, we can state that the patient had
bilateral multilobar pneumonia with multiple foci along
with the history of B. pertussis infection. As concomitant
alterations of the principal diagnosis, we may mention the
massive alveolar damage characterized by cytotoxicity and
secondary ischemia of the respiratory epithelium that led
to acute respiratory insufficiency due to a deficiency of the
respiratory epithelial system. The remaining organs were
noted to have changes due to a state of sustained hypoxia.
Subdirector of Medical Assistance (Dra. Mónica Villa
Guillén)
Were there data of pulmonary hypertension?
Dr. Carlos Alberto Serrano Bello
Histologically, no data of pulmonary hypertension or
pulmonary vascular disease were demonstrated.
Coordinator (Dr. Sarbelio Moreno Espinosa)
Figure 9. Cellular hypoxia. (A) Necrosis of pneumocytes. (B) Cellular
detritus, accumulation of mucus due to ciliostasis. (C) Inadequate
leukocyte function.
Table 6. Histological changes secondary to persistent hypoxia
Organ
Histology
Thymus
Fluid depletion, califications of hassal corpuscles
Liver
Kidneys
Digestive tract
CNS
DHS
ATN
Hyproxic myopathy
Grave hypoxic encephalopathy
DHS, diffuse hepatic steatosis; ATN, acute tubular necrosis; CNS,
central nervous system
Vol. 69, November-December 2012
As can be seen, a cascade of events occurred. B. pertussis
can cause changes, locally as well as distant, that may
explain these series of events.
Chief of Ambulatory Care and Emergency Department
(Dr. Victor Olivar Lopez)
I see the opposite situation. Here is a patient with B. pertussis complicated by pneumonia due to coronavirus. It
is difficult for me to think otherwise, especially because
there is a history of three patients with infection due to B.
pertussis in the referral hospital. In contrast, up to 25% of
patients with B. pertussis have some type of complication,
some with bacteria and other viruses. From the clinical
condition in which the patient arrived, I think there was
an added viral picture, which explains the bronchospasm
mentioned by Dr. Barbara Morales. With respect to the
585
Sarbelio Moreno Espinosa, Bárbara Inés Morales Mérida, Carlos Alberto Serrano Bello, Orlando Domínguez Pacheco, Olga Camaño
Andrade, Rubí Rojas Padilla, Ernesto Calderón Jaimes
approach, this case is very interesting because it exemplifies what we are seeing today, but also in a patient
whose age places her in a high-risk age group for dying.
The first thing we must evaluate, in terms of respiratory
distress and respiratory failure, is the approach to the
airway and oxygen. Obviously, as soon as there is suspicion, the patient should be placed under isolation. We had
the advantage of knowing the history. I also clarify that,
in the hospital, there is a basic monitoring system, which
has pulse oximetry. In fact, it is stated here that the patient
desaturated when this catastrophic event occurred. In this
type of patient with this serious condition, we refer to it
as chronic pertussis.7 The natural history of these patients
includes the expected symptoms of apnea, desaturation,
cyanosis and bradycardia. Fortunately, it occurs in only
1% of patients. It is my opinion that the patient was monitored. However, these events cannot be avoided, probably
due to the interaction of some pertussis strains that favor
the development of multiple organ failure, as previously
mentioned. Under the best of situations, even in patients
with extracorporeal oxygenation systems, 70% of patients
will die. Regarding oxygenation systems, it is initially
free flow and such systems are incorporated as required. I
postpone the CPAP because the respiratory pause from the
cough of the patient with B. pertussis is precisely an inspiratory pause, and the individual objective is to increase
the inspiratory, not expiratory, pressure. If this patient had
prolonged expiration and some stigmatas, in my opinion it
was because there was an added viral infection. The patient
should be admitted, a differential diagnosis made, and the
patient should be kept under strict isolation. Mandatory
reporting is made, as was done in this patient. The patient
is monitored for any complications that may arise and is
managed in the emergency room.
tional literature increasingly better clarifies this fact. It is
believed that up to 70% in this series of illnesses is caused
purely by infections due to B. pertussis, without relation
to a different superimposed bacteria.6 The term “coqueluchoide syndrome” encompasses signs and symptoms that
occur in whooping cough, which may be caused by other
agents such as adenovirus, Chlamydia, Mycoplasma and
others. Due to the lack of access to appropriate diagnostic
methods and the belief of the infallibility of the vaccine
that it confers lifelong immunity, we have taken refuge
in this term. With the introduction of molecular methods
and a better understanding of this agent and its epidemiological changes, it is increasingly more difficult for us to
confuse this disease. It can be proven that in the majority of
cases in which patients present convulsive or paroxysmal
coughing, with vomiting after coughing and stridor at the
end of the inspiration, we are dealing with a B. pertussis
infection because a clinical picture of whooping cough
can only be compared with another clinical picture of
whooping cough. For this reason, the term coqueluchoide
syndrome is becoming less effective.
Coordinator: (Dr. Sarbelio Moreno Espinosa)
Coordinator (Dr. Sarbelio Moreno Espinosa)
Typically, a viral infection is the pivot for establishment
of a bacterial infection. It has been seen that coronavirus
infections, which is not the coronavirus of SARS, but that
which causes the common cold, rhinovirus, parainfluenza
and others, cause ciliostasis favoring the introduction of a
bacterial infection. When there is pneumonia superimposed on a clinical picture of pertussis, we have a bacterial
infection. Although a clinical picture of pertussis may be
complicated by a superimposed bacterial pneumonia, B.
pertussis per se can cause pneumonia. In fact, the interna-
586
Commentary (Dr. Erick Rosales Uribe)
When we speak about coqueluchoide syndrome, we refer
to a clinical spectrum that includes, in addition to B. pertussis, viral agents such as adenovirus, parainfluenza and
respiratory syncytial virus. We also include Mycoplasma
pneumoniae and other Bordetella species such as parapertussis, bronchiseptica and holemsi. According to the
characteristic clinical picture, one could declare that we
are dealing with B. pertussis. Because there was access
to PCR it would be interesting to know which primer was
used to determine if it was B. pertussis or another species
of Bordetella.
On this occasion, in addition to the IS481 that identifies a
common element of insertion to other Bordetella species
and has the highest sensitivity, we used ptxS1 primer that
identifies the subunit 1 promoter of the pertussis toxin,
giving the specificity for B. pertussis.
Commentary (Dr. Ernesto Calderón Jaimes)
There are several aspects to consider in this case. From
the epidemiological point of view, the disease acquired
characteristics of severe illness. Situations of the pathogen
Bol Med Hosp Infant Mex
Acute respiratory failure secondary to Bordetella pertussis infection in a 4-month-old infant
and host are combined. B. pertussis has, in the filamentous
hemagglutinin (FHA) and in several of the fimbriae (FIM),
two of the most potent adhesins. The first is a protein
secreted at the surface and the second is a filamentous,
also superficial, structure. Both are highly immunogenic.
Pertussis toxin and pertactin are elements of pathogenicity
and virulence as well as LPS and other toxins.
There are receptors in the tracheobronchial mucosa,
specifically in the ciliated cells and in mucin-producing
cells. B. pertussis acts locally: it does not invade and it
adheres firmly in situ and, from there, releases its toxins. B.
pertussis has various phenotypes. During minor outbreaks,
a clone with a gene vir/Bvg dominates, which makes
products such as FHA, FIM, FRN, PT and LPS, function
as a superantigen, increases the capacity for adherence
and directly activates T lymphocytes. This results in an
intense, uncontrollable and aberrant cascade of different
water-soluble products that modulate the response, both
at the interstitial level as well as in the mucociliary apparatus. Exotoxins are responsible for a marker of severity
expressed in blood studies with leukemoid, leukocytosis
and lymphocytosis counts.
On the side of the host there are crucial aspects: 1)
age, 2) not having been vaccinated with pertussis toxoid
vaccine, and 3) being involved in an outbreak with virulent
clones where three of four children died.
The mucociliary apparatus suffers the assault. Its
response disrupts ciliary function, and the mucins are
now more abundant, thick and difficult to expectorate. The lung “obstructs” with interstitial edema and
occupied alveolar syndrome, dramatically altering the
gas exchange. Cyanosis is prevalent and pulmonary
hypertension leads to a cardiopulmonary component,
becoming irreversible on not stopping the inflammatory
cascade. Although pertussis is typically described as a
highly infectious disease, transmission requires intimate
contact and prolonged exposure.
Neither the disease nor the vaccination confers permanent immunity, explaining why the accumulation of
susceptibility allows an outbreak to occur every 2-5 years.
The only postvaccine change occurs in the population
exposed to disease risk. Prior to 1980, the most affected
population was young children, including children <1 year
of age, most of whom were unvaccinated. Vaccination now
changes the population of adolescents and adults who are
contracting the disease.
Vol. 69, November-December 2012
Undoubtedly, B. pertussis is internationally accepted
as well as cases of whooping cough in adolescents and
adults. Recognition of cases is based on patients who are
“coughers” with an evolution of >2 weeks.
Pediatric Commentary (Dra. Rubí Rojas Padilla)
Prior to the availability of the vaccine, B. pertussis was a
common cause of morbidity and mortality in children. After the introduction of the vaccine in the 1940s, incidence
of the disease began to decrease and reached an incidence
of one case/100,000 population between 1980 and 1990.
However, the incidence has been increasing since the
1980s. Between 2001 and 2003 the highest annual incidence was found in patients <1 year of age and, particularly,
in those <6 months (100 cases/100,000). In recent years,
the incidence has increased in adolescents and adults, a
reason why vaccination in these age groups has become
very important to prevent transmission to young children.
The acellular vaccine has inactivated components of B.
pertussi cells. It is combined with tetanus and diphtheria
toxoids and is used in children between 6 weeks and
6–7 years of age. Recommended doses are at 2 months,
4 months, 6 months, and between 15 and 18 months of
age. For adolescents and adults, the acellular vaccine is
combined with tetanus toxoid and a smaller quantity of
diphtheria toxoid, compared with the pediatric vaccines.
It is recommended in persons between 10 and 64 years
of age. In persons between 11 and 18 years of age who
completed the vaccination schedule against Bordetella
pertussis in childhood, the application of a single dose of
Tdap vaccine is recommended. Similarly, its application
is recommended in patients between 7 and 10 years of
age who did not receive a complete vaccination scheme
against B. pertussis and in adults 65 years of age or older
who are expected to have contact with a child <12 months
of age. All women of childbearing age should receive a
dose of Tdap. Women who did not receive the vaccine
should receive the dose in the immediate postpartum. Td
administration is recommended during pregnancy but,
under certain circumstances, Tdap can be administered,
especially if a B. pertussis outbreak is documented in the
community or in pregnant adolescents.
Health care workers who work in hospitals and have
direct patient contact should receive a single dose of Tdap
as soon as possible, especially personnel in contact with
patients <12 months of age.
587
Sarbelio Moreno Espinosa, Bárbara Inés Morales Mérida, Carlos Alberto Serrano Bello, Orlando Domínguez Pacheco, Olga Camaño
Andrade, Rubí Rojas Padilla, Ernesto Calderón Jaimes
The epidemiological justification for booster vaccination against whooping cough is based on the fact that the
individual effectiveness of the vaccine is between 70 and
80% with protection of limited duration. Because of this,
there has been a disease transition to older age groups,
who transmit it to vulnerable infants.
The new epidemiology of whooping cough has a close
relationship with the vaccine coverage. Where coverage is
low, there will be a high incidence in children. However,
in areas where the coverage is high, we see a low incidence in children with a gradual decrease in the immunity
of adolescents and adults who may have the disease and
transmit it to infants who are not vaccinated or have been
partially vaccinated. Also, it is important to take into
account that 75% of infant cases were infected by family
members, of which the mother was the most frequent
transmitter because she has the closest contact with this
vulnerable age group. Regarding the duration of the immune response, recent studies suggest that the acquired
immunity for infection could be as short as 3.5 years in
children, and the protection provided by the vaccine between 4 and 12 years. Also, the protective immunity after
a natural infection decreases after 7 to 20 years. For all
these reasons, the use of acellular vaccines and boosters is
a priority for protection of adolescents and adults as well
as for the protection of children who are not vaccinated
or who are only partially vaccinated.
Intensive Therapy Physician (Dr. Alberto Jarillo Quijada)
Mention needs to be made on the pathophysiological
aspect as to why the patient expired. We have focused
only on the refractory hypoxemia, and though Dr. Rosales
already mentioned the poor prognostic factors, which are
pneumonia, hypoxemia and secondary convulsive crisis in
children <2 years of age, we focused and made the serious
mistake of concentrating only on the resolution of the
hypoxemia, managing the patient from a ventilatory standpoint. Another important risk factor that causes death in
children is hyperleukocytosis. The patient had a leukocyte
count of 100,000. In these cases, saline pheresis was then
proposed, although with the technical complications due
to the fact of dealing with an infant <4 months who needs
to have an 8 Fr catheter placed. The other is leukopheresis
588
as seen here. There is significant alveolar lymphocytic
infiltrate as well as intravascular. This patient behaved
like a patient with DIC, with platelet consumption. What
is done is thrombotic microangiopathy with capillary flow
obstruction, both pulmonary and systemic. In this patient,
as with those patients who come in with leukemoid reaction in leukemia and refractory hypoxemia managed with
adequate ventilation parameters, leukopheresis is carried
out, blood viscosity is decreased, and leukocyte binding
to pulmonary capillary level and inflammatory response
are reduced. This possibility should have been taken into
consideration. Technical difficulties are very important in a
4-month-old infant. If we consider that pertussis is making
a “come back”, we should also be prepared in this regard.
Coordinador: (Dr. Sarbelio Moreno Espinosa)
This case brings to mind several pathophysiological aspects of childhood disease, not only from the infectious
viewpoint. It also allowed the interaction of various
services. We must be prepared to deal with such cases,
especially taking into account the reemergence of this
disease.
REFERENCES
1.
2.
3.
4.
5.
6.
7.
Kuhlman JE, Reyes BL, Hruban RH, Askin FB, Zerhouni EA,
Fishman EK, et al. Abnormal air-filled spaces in the lung.
Radiographics 1993;13:47-75.
Romano MJ, Weber MD, Weisse ME, Siu BL. Pertussis
pneumonia, hypoxemia, hyperleukocytosis, and pulmonary
hypertension: improvement in oxygenation after a double
volume exchange transfusion. Pediatrics 2004;114:e264-e266.
John SD, Ramanathan J, Swischuk LE. Spectrum of clinical
and radiographic findings in pediatric mycoplasma pneumonia.
Radiographics 2001;21:121-131.
Fahy JV, Dickey BF. Air mucus function and dysfunction. N
Engl J Med 2010;363:2233-2247.
Vareille M, Kieninger E, Edwards M, Regamy N. The airway
epithelium: soldier in fight against respiratory viruses. Clin
Microbiol Rev 2011;24:210-229.
Paddock CD, Sanden GN, Cherry JD, Gal AA, Langston C,
Tatti KM, et al. Pathology and pathogenesis of fatal Bordetella
pertussis infection in infants. Clin Infect Dis 2008;47:328-338.
Burr JS, Jenkins TL, Harrison R, Meert K, Anand KJS, Berger
JT, et al. The Collaborative Pediatric Critical Care Research
Network (CPCCRN) Critical Pertussis Study: collaborative
research in Pediatric Critical Care Medicine. Pediatr Crit Care
Med 2011;12:387-392.
Bol Med Hosp Infant Mex
Bol Med Hosp Infant Mex 2012;69(6):589-594
Pediatric theme
Renal tubular acidosis
Dr. Luis Velásquez Jones
ABSTRACT
Renal tubular acidosis (RTA) refers to a group of clinical entities in which hyperchloremic metabolic acidosis occurs with normal anion gap
as a result of defective transport of the proximal tubular reabsorption of bicarbonate (proximal RTA or type 2), distal secretion of hydrogen
ions (distal RTA or type 1), or hyperkalemic RTA (or type 4). These RTA types can be inherited or acquired.
Primary forms of proximal RTA are extremely rare, with the majority of cases in children found associated with Fanconi syndrome. Primary
distal RTA is the most common distal RTA found in children. Hyperkalemic RTA is found together with aldosterone deficiency or aldosterone
resistance, which causes hyperkalemia, low synthesis and low levels of urinary ammonium and salts and titratable acids.
RTA may manifest early in infancy with vomiting, polyuria and polydipsia, dehydration crisis, failure to thrive and growth retardation. Children
with distal RTA may present with nephrocalcinosis.
Long-term treatment with alkalizing solutions (citrate or bicarbonate of sodium and potassium) to maintain normal values of serum bicarbonate
concentration induces catch-up growth, corrects the electrolyte abnormalities of the different types of RTA (hypocitraturia, hypercalciuria)
and arrests progressive nephrocalcinosis in patients with distal RTA.
Key words: renal tubular acidosis, proximal or type 2, distal or type 1, hyperkalemic or type 4.
INTRODUCTION
Proximal RTA
Renal tubular acidosis (RTA) includes a group of clinical entities in which hyperchloremic metabolic acidosis
occurs, i.e., with normal serum anion gap. These are characterized by alterations in bicarbonate resorption in the
proximal tubule of the nephron [proximal RTA (pRTA) or
type 2] or defect of hydrogen ion secretion in the distal
tubules of the nephron [distal RTA (dRTA) or type 1] and
hyperkalemic RTA (or type 4). Previously, type 3 RTA was
used to define children with type 1dRTA who, as infants,
also presented proximal loss of bicarbonate in the urine;
however, because this loss is transitory, this category has
been eliminated.1,2
Causes
Head, Departamento de Nefrología, Hospital Infantil de México
Federico Gómez, México, D.F., México
Correspondence to:
Dr. Luis Velásquez Jones
Departamento de Nefrología
Hospital Infantil de México Federico Gómez
México, D.F., México
E-mail: [email protected]
Received for publication: 10-23-12
Accepted for publication: 10-30-12
Vol. 69, November-December 2012
Approximately 75-80% of the filtered bicarbonate is
resorbed normally and therefore “returned” to the blood
by the proximal tubule of the nephron. If the resorptive
capacity of this segment of the nephron is reduced (as
seen in primary pRTA and Fanconi syndrome), increased
release of bicarbonate would occur to the distal segments
of the nephron, which exceeds the possibilities of their
absorption, developing bicarbonaturia and metabolic acidosis. The contraction of the extracellular water volume
induces increased resorption of chlorine, resulting in the
development of hyperchloremic metabolic acidosis.
In pRTA, also called type 2, the primary forms are
included and are hereditary and sporadic variants and
secondary forms. Primary forms are rare in children,
with the majority of cases seen as part of Fanconi syndrome (Table 1).1-3 Autosomal dominant and autosomal
recessive variants have been described in some families
of patients with pRTA. The autosomal dominant variant
has been described in only a limited number of affected
families.4 The recessive variant is associated with mental retardation and ocular problems and is caused by a
defect in the co-transporter Na+ + HCO3-(NBC1); this
589
Dr. Luis Velásquez Jones
Table 1. Causes of proximal RTA
1. Primary
a) Hereditary forms: autosomal dominant, autosomal recessive,
osteopetrosis, Leigh syndromes, metachromatic leukodystrophy
b) Sporadic: persistent idiopathic, transitory
2. Secondary
a) Component of Fanconi syndrome: cystinosis, glycogenesis
type I, tyrosinemia, hereditary fructose intolerance, galactosemia, Wilson’s disease
b) Other diseases: nephrotic syndrome, cyanogenic cardiopathy, CVA, paroxysmal nocturnal hemoglobinuria, postrenal transplant
c) Drugs: isophosphamide, heavy metals
d) Carbon anhydrase inhibition: acetazolamide, sulfanylamide,
mafenide, topiramate
RTA, renal tubular acidosis; CVA, cerebrovascular accident.
transporter allows output (resorption) of the bicarbonate
ion together with sodium ions from the tubular cell to the
peritubular renal blood circulation. The gene SLC4A4,
which encodes for NBC1, is located on chromosome 4.3,5,6
Affected children with this autosomal recessive variant
present, in addition to pRTA, short stature, glaucoma,
cataract, band keratopathy, psychomotor retardation,
calcification of the basal ganglia and hyperamylasemia.4
These alterations manifest because, in addition to its expression in the proximal renal tubule of the nephron, the
NBC1 cotransporter is also present in ocular structures,
brain and pancreas.4
Patients with osteopetrosis associated with carbonic
anhydrase II deficiency exhibit both pRTA and dRTA because carbonic anhydrase II is important for renal tubular
resorption of bicarbonate and hydrogen ion secretion. For
this reason, it has also been called “mixed” renal tubular
acidosis.6 In the proximal tubule of the nephron, cytosolic
carbonic anhydrase II provides intracellular hydrogen
ion secretion continuously into the tubular lumen and
bicarbonate ion for its extrusion through the basolateral
membrane into the circulation. Both ions are derived from
CO2 and water.7
The clinical picture of pRTA has also been described
in patients with Leigh syndrome and metachromic leukodystrophy.3
Sporadic variants, also called isolated variants, may
be either persistent or transitory. The transient variation
is usually manifested during breastfeeding age and is
predominant in males. Affected patients have low stature
590
and have repeated episodes of vomiting and dehydration.8 Indicated treatment is alkalizing solutions and the
alteration disappears after several years. It is speculated
that there is an immaturity of transporter NBC1 in these
children, which persists beyond the neonatal period, but
the alteration corrects itself spontaneously some years
later.4 Development of proximal RTA has been observed
in infants with cyanotic heart disease and renal vascular
accidents.1
Secondary causes of pRTA include Fanconi syndrome and its various etiologies, other diseases such as
nephrotic syndrome, post-renal transplant, drugs and
inhibition of carbonic anhydrase. Acetazolamide and
some anticonvulsant medications such as topiramate
induce the clinical picture of pRTA by inhibiting the
action of carbonic anhydrase IV. Carbonic anhydrase
IV is located in the apical or luminal and basolateral
membranes of the proximal tubule cells and thick ascending branch of the loop of Henle. In the basolateral
membrane, release of the bicarbonate ion from the
tubular cell is facilitated.7-9
Clinical Manifestations and Laboratory Findings
Proximal RTA is usually manifested during infancy mainly
with growth retardation and is commonly associated with
low dietary intake by the presence of marked hyperoxia,
nausea and persistent vomiting. Polyuria is frequently
present.1
Laboratory tests typically show metabolic acidosis:
arterial blood pH ≤7.30 and arterial blood bicarbonate <21
mEq/L. Hyperchloremia is also present, which conditions
the finding of anion gap to be within normal limits (8-16
mEq/L) and with mild hypokalemia. Total CO2 contents
can also be examined in venous blood (normal range 2130 mEq/L or mmol/L)10 to document the decline in blood
bicarbonate concentration. Urine pH can be <5.5. Typically
no changes are observed in the serum concentrations of
calcium, phosphate and vitamin D.
To determine the ability of the kidney to resorb filtered bicarbonate, fractional excretion of bicarbonate
(FE-HCO3-) should be performed. This test should be
performed after the serum bicarbonate concentration has
been normalized (22-25 mEq/L or mmol/L) after starting
treatment with alkalizing solutions. Normally, FE-HCO3values are <5%. In contrast, in patients with pRTA, this
value is usually between 12 and 15%.1
Bol Med Hosp Infant Mex
Renal tubular acidosis
Treatment
The main goal of treatment for patients with pRTA is to
maintain normal pH and serum bicarbonate concentration.
This can be achieved only with the administration of relatively high volumes of alkalizing solutions containing
bicarbonate or organic anion equivalent, such as citrate,
which consumes hydrogen ions during metabolism in the
liver.11 The typical dose ranges from 8-15 mEq/kg/day,
with even higher doses to normalize serum bicarbonate
concentration.1
The composition of the solutions usually indicated is
as follows:
a) Bicarbonate solution: 43 g sodium bicarbonate, potassium bicarbonate 53 g and 500 mL water
b) Citrate solution: citric acid (70 g), sodium citrate (98
g), potassium citrate (108 g), water and currant syrup
(1000 mL)
The solution provides 1 mEq sodium, 1 mEq potassium
and 2 mEq bicarbonate/mL, whereas the citrate solution
contains 1 mEq of sodium, 1 mEq potassium and 2 mEq
of citrate/mL. The daily dose should be divided into 6-h
doses.1 In situations that require increasing amounts in
an attempt to normalize serum bicarbonate concentration, it may be necessary to add a thiazide diuretic to the
treatment.6 The diuretic induces a chronic state of depletion
of the extracellular water volume, which decreases the
glomerular filtration rate and the filtered bicarbonate load.
Although the disease prognosis will vary according to
the causative factor, pRTA itself will not produce serious
consequences for the patient if the electrolytic and acidbase alteration is corrected. In children with the isolated
idiopathic form, normal growth for age is recovered. It has
been observed that, with this variant, the tubular defect of
bicarbonate resorption improves with age.11
Distal RTA
Distal RTA (dRTA) is also called classic or type 1. It is
characterized by the presence of hyperchloremic and
hypokalemic metabolic acidosis with inability to reduce
urinary pH to values <6.0. This is due to a defect in the
transporters involved in the elimination of hydrogen ions
in the urine and the associated bicarbonate regeneration.
In this regard, when the ability of the distal nephron
to reduce urinary pH is altered, various metabolic consequences are presented: a) the bicarbonate that escapes
resorption of the proximal tube is not resorbed, with bicarVol. 69, November-December 2012
bonaturia occurring despite the acidosis, b) tubular renal
secretion of ammonia and titratable acids is reduced, c)
hypokalemia occurs due to the presence of nonabsorbable
anion (bicarbonate, sulfate) in the distal nephron, which
promotes excessive potassium secretion and d) hyperchloremic metabolic acidosis occurs because the contraction
of the extracellular space induces greater renal tubular
resorption of chlorine.1
Causes
The causes of dRTA include both the persistent sporadic
forms as well as the genetic forms, those associated with
heredity, autoimmune factors and renal tubulointerstitial
diseases, and also diseases accompanied by hypercalcemia
and nephrocalcinosis and drugs and toxic effects (Table
2).1,2,12,13
The disease can be transmitted in an autosomal dominant or autosomal recessive manner. In the dominant
variant, a defect was observed in the SLC4A1 gene located
on chromosome 17, which encodes the action of Cl-/HCO3(AE1) exchanger located on the basolateral surface of the
alpha intercalated cells and erythrocytes and allows the
release (resorption) of the bicarbonate ion to the blood of
the peritubular capillaries in exchange with chlorine.3,14
SLC4A1 gene mutations also cause anemia and spheTable 2. Causes of distal RTA
1. Primary
a) Sporadic (persistent)
b) Genetic: autosomal dominant, autosomal recessive with or
without or deafness
2. Diseases associated with hypercalciuria and nephrocalcinosis,
primary hyperparathyroidism, medullary sponge kidney, idiopathic
hypercalciuria, vitamin D intoxication
3. Renal tubulointerstitial diseases: obstructive nephropathy,
chronic pyelonephritis, renal transplant rejection, hyperoxaluria
4. Autoimmune diseases: SLE, chronic active hepatitis, hyperglobulinemia purpura
5. Other diseases:
a) Ehlers-Danlos syndrome
b) Hematologic diseases: spherocytosis, ovalocytosis, hemolytic
anemia
c) Renal cystic diseases: nephrocytosis, cystic medullary disease
d) Glycogenesis type I
e) Familiar hypercalciuria
f) Congenital cyanogenic cardiopathy
6. Medications and toxins: amphotericin, lithium salts, cyclamates,
foscarnet, amiloride, toluene
RTA, renal tubular acidosis; SLE, systemic lupus erythematosus.
591
Dr. Luis Velásquez Jones
rocytosis and ovalocytosis hemolytic anemia, which are
hereditary autosomal dominant diseases.2,15
In the autosomal recessive variant of dRTA, two genes
have been implicated: ATP6V1B1 and ATP6V0A4. These
codify the β1- and α4-subunits of H+-ATPase located in
the apical membrane of the intercalated renal tubular cells,
which participate in the transference of hydrogen ions
to the urine. It has been observed that children with this
variant have a more severe clinical picture with severe
growth retardation, metabolic acidosis and accentuated
hypokalemia, along with a tendency to depletion of the
intravascular volume. There is also early development of
nephrocalcinosis with renal function compromise. Finally,
in most cases, progressive sensorineural hearing loss can
be observed.6,16
Clinical Manifestations
Clinical manifestations can be observed from infancy
with growth retardation, hyperoxia, nausea and vomiting and, in some cases, concomitantly with severe
metabolic acidosis and accentuated hypokalemia. 1,17
Rhabdomyolysis has been noted in children with dRTA
and severe hypokalemia. 18 Severe acidosis in young
children is due to the fact that, apart from the defect to
acidify the urine, during these ages, an additional loss
of bicarbonate with fractional excretion of bicarbonate
is seen, which can reach values of 5-15%. Chronic metabolic acidosis alters bone mineralization, leading to
the development of rickets in children and osteomalacia
in adults.
In a recently published study that included children
from 5 months to 9 years of age with a diagnosis of primary
RTA, there was a high frequency (up to 28%) of sensitivity
to various allergens such as cow’s milk, wheat and egg
whites.19 However, it will be necessary to confirm these
findings in future diagnostic studies with greater sensitivity
and specificity.19
Laboratory and Imaging Findings
Disruption of hydrogen ion secretion in the distal nephron
leads to reduced ammonia excretion and titratable acid
in the urine, with increased bicarbonate excretion, all of
which lead to metabolic acidosis. It has been mentioned
that the main feature of the classic dRTA or type 1 is the
inability of the kidney to reduce urine pH <6.0 in the
presence of systemic acidosis.
592
In these cases of metabolic acidosis with normal plasma anion gap, it is useful to calculate the urine anion gap
[(Na+/K+) - Cl-].17 Thus, the urine anion gap can be used
as an indirect estimation of ammonia excretion, which
usually is excreted as ammonium chloride. In patients with
metabolic acidosis caused by dRTA, the acidemia is mainly
due to inadequate excretion of hydrogen and ammonium
ions. In these cases, the urinary anion gap gives positive
values, i.e., the sum of sodium and potassium is greater
than the chlorine concentration.20
In dRTA, acidosis is also related to significant loss of
sodium at the renal level, which leads to increased secretion of renin and aldosterone and aggravates hypokalemia.
Renal loss of sodium and the tendency to hypovolemia are
more pronounced also in patients with nephrocalcinosis.1
Moreover, chronic acidosis is associated with increased citrate resorption at the level of the proximal
renal tubule so as to help cushion acidosis. This leads to
reduced availability of citrate at the distal tubular level,
and hypocitraturia induces increased urinary excretion
of calcium.8 Also, because bicarbonate buffer reserves
are used to compensate for chronic metabolic acidosis,
liberation of hydroxyapatite from bone takes place to
release calcium and hydroxyl ions and buffer metabolic
acidosis. This also causes hypercalciuria, which favors
the development of nephrocalcinosis and nephrolithiasis
in these patients.3,8 In some patients with dRTA, particularly genetic forms, hypercalciuria may not present itself
in the initial stages of the disease.21 Renal ultrasound
should be performed to rule out nephrocalcinosis. We recommend repeating this study each year during treatment
and follow-up of the patient.
Treatment
It has been mentioned that, in infants and toddlers, the
concomitant presence of renal loss of bicarbonate in
addition to the distal urinary acidification defect, higher
doses of alkalizing solutions may be required, on the order of 5-10 mEq/kg /daily, divided every 6 h. This allows
maintaining normal growth rate. In this respect, it has been
observed after the age of 5 to 6 years, the required amount
of alkalizing solutions per kilogram of weight decreases.
After these ages, it is noted that, unlike what occurs in
patients with pRTA, the quantity of bicarbonate or citrate
to administer in dRTA is less, with doses between 1 and
3 mEq/kg/day to correct the acidosis.1
Bol Med Hosp Infant Mex
Renal tubular acidosis
It is also noted that correction of acidosis improves
the increased losses of sodium and potassium in the urine
and particularly increases citrate production in the kidney
and corrects hypercalciuria. It should be emphasized that
treatment with alkalizing solutions in children with dRTA
should be directed not only to achieve pH normalization
and serum concentration of bicarbonate but also, and
primarily, to correct the hypercalciuria. This will prevent
the deposition of calcium in renal tissue. It must be remembered that if there is development of nephrocalcinosis,
usually with recurrent stone formation of calcium oxalate
or phosphate, it can influence the progressive destruction
of functional renal mass with progression to chronic end
stage renal disease. Therefore, in laboratory tests for children with dRTA, in addition to the pH determination in
serum and especially the concentration of bicarbonate and
electrolytes, determination of calcium excretion in urine
for a 24-h period (normal value ≤4 mg/kg/24 h) should also
be determined or the ratio of urinary calcium to creatinine
(normal value with the same units of measure, i.e., mg/dL
in both determinations, is <0.2).1
With proper treatment, recovery of growth velocity in
these children can be achieved. Moreover, early diagnosis
and treatment will prevent the development of nephrocalcinosis and renal stones. In children with autosomal
dominant or recessive dRTA and development of sensorineural deafness, it will be necessary to provide early
support with speech therapy. In severe and progressive
cases a cochlear implant may be required.1
Table 3. Causes of hyperkalemic RTA
1. Aldosteron deficiency
a) Addison´s disease
b) Congenital adrenal hyperplasia
c) Congenital lipod adrenal hyperplasia
d) Medications: ACE inhibitors, nonsteroidal antiinflammatories,
beta-blockers, heparin
e) Medications: ACE inhibitors, nonsteroidal antiinflammatories,
beta-blockers, heparin.
2. Resistence to aldosterone
a) Pseudohypoaldosteronism: autosomal dominant, autosomal
recessive
b) Renal tubulointerstitial disease: Kidney transplant rejection,
obstructive uropathy, nephrocalcinosis, nephropathy due to
analgesics, nephropathy due to sickle cell disease
c) Medications: spironolactone, triamterene, amiloride, cyclosporin, tacrolimus, heparin, trimethoprim, indomethacin,
captopril
RTA, renal tubular acidosis; SLE, systemic lupus erythematosus;
ACE, angiotensin-converting enzyme.
also decreases the intake of the ammonia ion from the
medullary interstitium towards the interior of the cells of
the medullary collector tubules through its defect in the
secretion of potassium ion through the Na+-K+/ATPase
located on the basolateral portion of the tubular cellular
membrane. The net effect of these actions is the decrease
in urinary excretion of ammonia ions and titratable acids
with development of metabolic acidosis.3
Clinical Manifestations
Clinical manifestations are directly related to the underlying condition causing the altered acid-base balance.
Hyperkalemic RTA
Hyperkalemic RTA or type 4 (or IV) is characterized by the
development of mild to moderate hyperchloremic metabolic acidosis associated with hyperkalemia. Kidney patients
affected retain the ability to reduce urinary pH <5.5.1
Causes
Hyperkalemic RTA type 4 is seen in diseases accompanied
by aldosterone deficiency or resistance to its action in
target organs (Table 3).1,3,22-24 In these cases the resultant
hyperkalemia induces a decrease of production of the ammonia ion in the proximal renal tubule due to the defect in
action of aldosterone. The potassium also competes with
the ammonia ion for the Na+/2Cl/K+ transporter in the
ascending branch of the loop of Henle, thereby reducing
the medullary gradient of the ammonia ion. Hyperkalemia
Vol. 69, November-December 2012
Laboratory Findings
It has been mentioned that the clinical picture of metabolic
acidosis is usually mild to moderate. A characteristic fact
is also the finding of hyperkalemia. Although in these
patients there is also reduction of urinary excretion of
ammonia and titratable acids, the urine can generally be
acidified, noting a pH <6.0.
It is proposed that the response of the cortical collecting
tubule of the nephron can be evaluated through determination of transtubular potassium gradient (TTKG) using
the following equation:1,2,23
TTKG = [K+ urine]/[K+ plasma]
Uosm/Posm
where the numerator indicates potassium concentrations in urine and plasma and the denominator indicates
593
Dr. Luis Velásquez Jones
urine and plasma osmolality. It is considered that a TTKG
value ≥8 indicates there are normal values of aldosterone
and that in patients with hyperkalemia the cortical tubule
is properly responding to increased plasma potassium
concentration. However, values <8 suggest aldosterone
deficiency or lack of renal tubular response to its action.1,6
Treatment
The treatment indicated is also based on the correction of
the precipitating cause. The intake of alkalizing solution
(bicarbonate solution or citrate without potassium) may
be necessary for correction of metabolic acidosis.
It has been observed that patients with aldosterone
deficiency will have an increase in the TTKG after
several days of initiating glucocorticoid treatment or
mineralocorticoid replacement. However, this response
is not observed in cases of insensitivity to the action of
aldosterone.
REFERENCES
1.
Velásquez JL. Alteraciones Hidroelectrolíticas en Pediatría.
México: Prado; 2010. p. 425.
2. Chan JC, Santos F, Hand M. Fluid, electrolyte, and acid-base
disorders in children. In: Taal MW, Chertow GM, Marsden PA,
Skorecki K, Yu ASL, Brenner BM, eds. Brenner & Rector’s The
Kidney. Philadelphia: Elsevier Saunders; 2012. pp. 2572-2621.
3. Foreman JW. Renal tubular acidosis. In: Kher KK, Schnaper
HW, Makker SB, eds. Clinical Pediatrics Nephrology. London:
Informa Healthcare; 2007. pp. 302-316.
4. Gross P, Meye C. Proximal RTA: are all the charts completed
yet? Nephrol Dial Transplant 2008;23:1101-1102.
5. Alper SL. Familial renal tubular acidosis. J Nephrol
2010;23(suppl 16):S57-S76.
6. Karet FE. Disorders of water and acid-base homeostasis.
Nephron Physiol 2011;118:28-34.
7. Hamm LL. Mecanismos de acidificación renal. In: Brenner BM,
ed. Brenner y Rector. El Riñón. Tratado de Nefrología. Madrid:
Elsevier; 2005. pp. 497-534.
8. Quigley R. Renal tubular acidosis. In: Avner ED, Harmon WE,
Niaudet P, Yoshikawa N, eds. Pediatric Nephrololgy. Berlin:
Springer; 2009. pp. 979-1003.
9. Schwartz GJ, Kittelberger AM, Barnhart DA, Vijayakumar S.
Carbonic anhydrase IV is expressed in H(+)-secreting cells of
rabbit kidney. Am J Physiol Renal Physiol 2000;278:F894-F904.
10. Kratz A, Ferraro M, Sluss PM, Lewandrowski KB. Normal reference laboratory values. N Engl J Med 2004;351:1548-1563.
594
11. DuBose TD, Alpern RJ. Renal tubular acidosis. In: Scriver
CR, Beaudet AL, Sly WS, Valle D, eds. The Metabolic and
Molecular Bases of Inherited Diseases. New York: McGrawHill; 2001. pp. 4983-5021.
12. Ambühi PM. Posttransplant metabolic acidosis: a neglected
factor in renal transplantation? Curr Opin Nephrol Hypertens
2007;16:379-387.
13. Keven K, Ozturk R, Sengul S, Kutlay S, Ergun I, Erturk S, et al.
Renal tubular acidosis after kidney transplantation—incidence,
risk factors and clinical implications. Nephrol Dial Transplant
2007;22:906-910.
14. Fry AC, Su Y, Yiu V, Cuthbert AW, Trachtman H, Karet Frankl
FE. Mutation conferring apical-targeting motif on AE1 exchanger causes autosomal dominant distal RTA. J Am Soc Nephrol
2012;23:1238-1249.
15. Fawaz NA, Beshlawi IO, Al Zadjali S, Al Ghaithi HK, Elnaggari
MA, Elnour I, et al. dRTA and hemolytic anemia: first detailed
description of SLC4A1 A858D mutation in homozygous state.
Eur J Haematol 2012;88:350-355.
16. Mohebbi N, Vargas-Poussou R, Hegemann S, Schuknecht
B, Kistler A, Wüthrich R, et al. Homozygous and compound
heterozygous mutations in the ATP6V1B1 gene in patients
with renal tubular acidosis and sensorineural hearing loss. Clin
Genet 2012. doi: 10.1111/j.1399-0004.2012.01891.x.
17. Mul D, Grote FK, Goudriaan JR, de Muinck Keizer-Schrama
SM, Wit JM, Oostdijk W. Should blood gas analysis be part
of the diagnostic workup of short children? Auxological data
and blood gas analysis in children with renal tubular acidosis.
Horm Res Paediatr 2010;74:351-357.
18. von Vigier RO, Ortisi MT, La Manna A, Bianchetti MG, Bettinelli
A. Hypokalemic rhabdomyolysis in congenital tubular disorders: a case series and a systematic review. Pediatr Nephrol
2010;25:861-866.
19. Bojórquez OA, Morfin MBM, García CR, Hernández T, Barbosa
C, Zaltzman GS. Prevalence of sensitization to inhaled and
food allergens in a group of children with primary renal tubular
acidosis. Rev Alerg Mex 2011;58:87-92.
20. Rose BD, Post TW. Rose & Post Trastornos de los Electrólitos y
del Equilibro Ácido-Base. Madrid: Marbán Libros; 2005. p. 590.
21. Tsai HY, Lin SH, Lin CC, Huang FY, Lee MD, Tsai JD. Why
is hypercalciuria absent at diagnosis in some children with
ATP6V1B1 mutation? Pediatr Nephrol 2011;26:1903-1907.
22. Nalcacioglu H, Genc G, Meydan BC, Ozkaya O. Hyperkalaemia in a female patient with systemic lupus erythematosus:
questions. Pediatr Nephrol 2012;27:1499-1500.
23. Nalcacioglu H, Genc G, Meydan BC, Ozkaya O. Hyperkalaemia in a female patient with systemic lupus erythematosus:
answers. Pediatr Nephrol 2012;27:1501-1503.
24. Riveiro-Barciela M, Campos-Varela I, Tovar JL, Vargas V,
Simón-Talero M, Ventura-Cots M, et al. Hyperkalemic distal
renal tubular acidosis caused by immunosuppressant treatment with tacrolimus in a liver transplant patient: case report.
Transplant Proc 2011;43:4016-4018.
Bol Med Hosp Infant Mex
Bol Med Hosp Infant Mex 2012;69(6):595-598
Vital statistics
Mortality due to exposure to smoke, fire and flames in children under 15
years of age during the period 1998-2010
Sonia B. Fernández Cantón,1 Ana Ma. Hernández Martínez,1 Ricardo Viguri Uribe2
INTRODUCTION
On previous occasions, mention has been made of one
of the biggest public health problems facing our country:
deaths due to accidents. These are the leading cause of
death among the population <15 years (except for those
<1 year of age). It is therefore important to analyze and
disseminate the behavior of the causes, which in a disaggregated manner make up this great sector of mortality.
In this manner, the present paper addresses the issue of
mortality due to exposure to smoke, fire and flames
This analysis was carried out using official data from
vital statistics (mortality) generated by the National
Institute of Geography and Informatics (INEGI) from
death certificates distributed by the Ministry of Health.
The codes considered for this paper are those between
the X00 and X09 of the International Classification of
Diseases (ICD) (10th revision) (ICD-10) (Table 1). Time
period comprises 1998–2010 to correspond to the year
1
2
Dirección de Información Epidemiológica, Secretaría de Salud,
Mexico, D.F., Mexico
Departamento de Ediciones Médicas, Hospital Infantil de México
Federico Gómez, México, D. F., México
Correspondence: Dra. Sonia B. Fernández Cantón
Dirección de Información Epidemiológica
Secretaría de Salud
Mexico, D.F., Mexico
E-mail: [email protected]; sonia_fernandez@
prodigy.net.mx
Received for publication: 8-7-12
Accepted for publication: 8-14-12
Vol. 69, November-December 2012
in which the ICD-10 began and the last year of data with
final figures, respectively.
Although deaths caused by exposure to smoke, fire and
flames represent a quantitatively smaller figure to other
causes that have been addressed in this space, the human
suffering provoked by the severity of the process that
leads to death and the impact of its consequences within
the family are reason enough to pursue the subject. In
the context of the general population, 1.8% of accidental
deaths had as the underlying cause exposure to smoke, fire
or flames (8453 deaths of a total of 475,923 from 19982010). Within the group of children under 15 years, this
percentage rose to 2.4%, i.e., 1543 deaths that occurred
in a 13 year period, from a total of 65,236 accidents in the
same period (Table 2). It is noteworthy that almost one in
five deaths from this cause (smoke, fire, flames) occurred
in the age group under 15 years of age (18.3%)
According to available information, between 1998 and
2010, on average, just under 120 deaths were recorded
annually, so that together, that age group accumulated over
the period a total of 1543 deaths, equivalent to a rate of
3.6 deaths per million population of that age group, that is
0.36 deaths per hundred thousand population <15 years of
age (Table 3). The trend analysis shows that, in general, a
decrease over the period, although with some fluctuations:
a rebound in 2005-2007 (rate of 0.25 to 0.37), followed
by a decrease (to 0.28) and a new increase in 2009 (to
a rate of 0.40), with the two extremes in the years 1999
with 182 deaths (and a rate of 0.54) against the lowest on
record in 2004 with 83 deaths (and with a rate of 0.25).
The year 2010, latest available figure, had 92 deaths (Table
4). Fig 1 shows, in detail, the behavior of the fluctuations
described above.
595
Sonia B. Fernández Cantón, Ana Ma. Hernández Martínez, Ricardo Viguri Uribe
Table 1. Deaths due to exposure to smoke, fire and flames in the population <15 years of age, 1998-2010
Deaths
3-digit ICD code
< 1
year
X00 Exposure to uncontrolled fire in an area of a bulding or other construction
X01 Exposure to uncontrolled fire not in an area of a building or other construction
X02 Exposure to controlled fire in an area of a building or other construction
X03 Exposure to controlled fire in an area that is not a building or other construction
X04 Exposure to highly inflammable ignitable material
X05 Exposure to ignition or fusion of sleepwear
X06 Exposure to ignition or fusion of other clothes and accessories
X08 Exposure to other specified smoke, fire or flames
X09 Exposure to unspecified smoke, fire or flames
Total
31
1
2
5-year age group
1-4
5-9
10 - 14
years
years
years
101
1
3
3
2
45
1
2
1
2
27
3
1
2
2
1
27
674
812
1
8
268
328
3
162
200
3
13
153
203
< 15
years
204
6
8
6
6
3
2
51
1,257
1,543
Source: SINAIS/SSA/INEGI/sistema de defunciones/Sistema Dinámico de Información (Cubes), ICD-10 cause: X00 to X09.
http://dgis.salud.gob.mx/cubos
Table 2. Relative weight of deaths due to smoke, fire and flames
exposure with respect to the total accidental deaths in children
<15 years of age, 1998 - 2010
Year
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
Total
Deaths in children <15 years of age
Exposure to smoke,
Accidental
Relative
fire and flames
deaths
weight (%)
154
182
160
139
109
85
83
106
106
116
88
123
92
1,543
5,848
6,022
5,590
5,667
5,646
5,186
5,053
4,762
4,846
4,483
4,156
4,161
3,816
65,236
2.63
3.02
2.86
2.45
1.93
1.64
1.64
2.23
2.19
2.59
2.12
2.96
2.41
2.37
Source: SINAIS/SSA/INEGI/sistema de defunciones/Sistema
Dinámico de Información (Cubes), ICD-10 cause: X00 to X09
http://dgis.salud.gob.mx/cubos
While over the period analyzed, the number of deaths
of children under 15 years caused by exposure to smoke,
fire and flames have fallen by 40%, going from 154 deaths
in 1998 to 92 in 2010 (figure higher than the decrease of
35% of accidental deaths as a whole), it is noteworthy
596
that the relative weight of the former out of the total has
remained virtually unchanged, and has remained around
2.4% (with values ranging from 1.64 in 2003–2004 and
3 in 1999) (Table 2).
It is important to point out that the decline in mortality
was observed in both males and females and in all age
groups, although with different intensities: the greatest
reduction occurred in the group <1 year of age (56%)
followed by the 1- to 4-yearold age group (43%), 5- to
9-year-old group (30%), and 10- to 14-year-old group,
which showed the lowest reduction (only 22%). In particular, there were differences in mortality rates according
to gender. In males there was a 49% decrease observed
and in females only a 28% reduction of deaths.
With respect to the distribution of deaths by age, this is
heterogeneous within groups. More than half of the deaths
(52%) occurred in the 1- to 4-year-old age group followed
by the 5- to 9-year-old age group, affecting >20%. The
remaining 26% is distributed equally among children <1
year and the 10- to 14-year-old age group (Figure 2).
Regarding gender distribution, this was similar to all
deaths that occurred due to external causes, whether or not
accidental. In deaths due to exposure to smoke, fire and
flames, there is a clear prevalence of male/female deaths:
880 and 663 deaths, respectively (Table 5); 57% of the
deaths occurred in males and 43% in females (Figure 3).
In other words, there is a mortality rate in males of 133
(per 100 female deaths). The most accepted explanation is
Bol Med Hosp Infant Mex
Year
reported
<1
year
1-4
years
5-9
years
10 - 14
years
< 15
years
Rate*
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
Total
25
23
22
24
11
14
13
18
10
12
10
10
11
203
84
98
71
73
59
49
48
54
56
64
47
61
48
812
27
34
43
23
31
15
12
21
24
25
20
34
19
328
18
27
24
19
8
7
10
13
16
15
11
18
14
200
154
182
160
139
109
85
83
106
106
116
88
123
92
1,543
0.46
0.54
0.48
0.41
0.33
0.26
0.25
0.33
0.33
0.37
0.28
0.40
0.30
0.36
Number of deaths
Table 3. Deaths and mortality rate due to smoke, fire and flames
exposure in children <15 years of age, 1998-2010
4
200
0.60
0.5
8
180 0.46
4
.
0
0.50
1
160
0
0.4
4
.
0
140
.37
0.40
3
3 3 0
0.3
120
0.3 0.3
8
.30
2
0
.
6 5
0
0.30
100
0.2 0.2
80
0.20
60
40
0.10
20
0.00
0
8 99 00 01 02 03 04 05 06 07 08 09 10
9
19 19 20 20 20 20 20 20 20 20 20 20 20
Deaths
Year
México 1998 -2010
Deaths
Rate
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
Total
154
182
160
139
109
85
83
106
106
116
88
123
92
1,543
0.46
0.54
0.48
0.41
0.33
0.26
0.25
0.33
0.33
0.37
0.28
0.40
0.30
0.36
Source: SINAIS/SSA/INEGI/sistema de defunciones/Sistema
Dinámico de Información en Sistemas de Salud (Cubes), ICD-10
cause: X00 to X09
http://dgis.salud.gob.mx/cubos
Vol. 69, November-December 2012
Rate
Figure 1. Mortality rate and deaths due to exposure to smoke,
fire and flames in children <15 years of age (Mexico 1998-2010).
Source: SINAIS/SSA/INEGI/Sistema de defunciones/Sistema
Dinámico de Información (Cubes), ICD-10 cause: X00 to X09.
http://dgis.salud.gob.mx/cubos
*Rate per 100,000 population of the group of children <15 years
of age
Table 4. Deaths and morality rate due to exposure to smoke,
fire and flames in children <15 years of age
Percentages
Mortality due to exposure to smoke, fire and flames in children under 15 years of age during the period 1998-2010
<1 year
13.2%
10-14 years
13.0%
1-4 years
52.6%
5-9 years
21.3%
Figure 2. Percentage distribution of deaths due to exposure to
smoke, fire and flames broken down according to age groups
(1998-2010).
linked to learned behaviors by males and females, which
accepts that males are often at greater risk as a result of
playing with fire and risk-taking behaviors. Similarly,
there are frequent injuries associated with group activities
where the boys use gasoline or other flammable products,
such as fireworks.
597
Sonia B. Fernández Cantón, Ana Ma. Hernández Martínez, Ricardo Viguri Uribe
Table 5. Deaths due to exposure to smoke, fire and flames in
children <15 years of age according to gender (1998-2010)
Year reported
Male
Female
Total
1998
1999*
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
Total
88
109
95
77
60
55
52
73
54
59
44
69
45
880
66
73
65
62
49
30
31
33
52
57
44
54
47
663
154
182
160
139
109
85
83
106
106
116
88
123
92
1,543
Fuente: SINAIS/SSA/INEGI/Sistema de defunciones/Sistema
Dinámico de Información (Cubos), Cause CIE: X00 a X09
http://dgis.salud.gob.mx/cubos
* includes a death of unespecified gender.
Moreover, despite the importance that knowing the
specific breakdown of the causes that led to the death by
exposure to smoke, fire and flames would have, Table 1
demonstrates the serious problems in registration and the
598
Males
57.0%
Females
43.0%
Figure 3. Percentage of deaths due to exposure to smoke, fire and
flames in children under 15 years of age (1998-2010).
Percentage of deaths due to exposure to smoke, fire and flames in
children under 15 years of age, 1998-2010
lack of precision in the medical certification. It is observed
that >80% of deaths appear as "causes related to smoke,
fire and flames unspecified." This represents a major limitation for prevention and control of risks.
Bol Med Hosp Infant Mex
Guidelines to authors
Boletín Médico del Hospital Infantil de México is the official
publication of the Hospital Infantil de México “Federico Gómez.”
The journal has been continuously published on a bi-monthly
basis since 1944 and publishes studies relating to pediatrics according to the following areas: biomedical, clinical, public health,
clinical epidemiology, health education and clinical ethics. The
following guidelines are in accordance with the “Uniform Requirements for Manuscripts Submitted to Biomedical Journals,”
published by the International Committee of Medical Journal
Editors (http://www.icmje.org).
Types of articles
Types of articles published are as follows: Review Articles, Clinical Case Reports, Clinicopathological Cases, Pediatric Themes
and Letters to the Editor. Published articles appear both in print
and on-line in Spanish and on-line in English.
Submissions should be sent via electronic mail to: bolmedhim@
yahoo.com.mx with the following requirements:
1. Letter addressed to Dr. Gonzalo Gutiérrez Trujillo, Editor,
Boletín Médico del Hospital Infantil de México, Departamento de Ediciones Médicas. The letter, signed by the corresponding author, should include the following information:
a) The enclosed article is being submitted for evaluation
for eventual publication in Boletín Médico del Hospital
Infantil de México.
b) The authors declare that the work has not been previously published, has not been previously accepted for
publication and has not been submitted simultaneously
to another publication.
c) Type of study should be indicated along with the corresponding pertinent area of pediatrics.
d) Confirm that the Guidelines to Authors have been reviewed and adhered to prior to submission.
e) If applicable, the authors should declare any conflict of
interest or submit a statement that no conflict of interest
exists. In the event of a conflict of interest, the authors
must disclose any external financial or economic interest.
f) All external funding sources should be clearly indicated.
g) All authors must affirm that they are in agreement with
the submission of the manuscript and that they have
reviewed and approved the work.
Please be reminded that without the appropriately signed author
letter, the initial editorial process will be delayed.
Manuscript preparation
All manuscripts should be prepared with standard programs
(Word 97 or higher) using the word processor function of your
computer. Double space all sections of the manuscript including
References, Tables and Figure Legends. Do not justify right margins and use one-inch margins all around. Keep formatting to a
minimum. Pages should be numbered consecutively beginning
with the first page and numbers should appear in the lower right
corner of the page.
Abbreviations
Complex terms used frequently in the manuscript may be abbreviated. Abbreviations are placed in parentheses at first use in
the abstract and again at first use in the text. Confirm that any
abbreviations used in Tables are appropriately spelled-out in the
Table legend underneath.
Organization of the manuscript
The first page should include the following:
a) Title of the manuscript (Spanish and English)
b) Type of manuscript: Original Article, Review Article,
Clinical Case Report, etc.
c) Name(s) of all authors in their order of appearance in
relation to the publication
d) Affiliation of each author (degrees and honors should
be omitted)
e) Name, E-mail address, postal address and telephone
number of the corresponding author to whom any correspondence can be directed during the review process
of the manuscript.
The second page should contain the Abstract. Note that the
Abstract is the most-often read part of the manuscript. For this
reason, it must be clear, concise and contain information relevant
to the article. Do not use references in the Abstract. In the case of
Original Articles and Clinical Case Reports, the Abstract should
be structured according to the following sections: Background,
Methods, Results, Conclusions, or Background, Clinical Case
and Conclusions. Abstracts for Review Articles and Pediatric
Themes should be unstructured and include only one paragraph.
The Abstract should be limited to 200 words and include only
relevant aspects of each of the principal sections of the body of
the manuscript. Authors should provide 3–6 keywords following
the Abstract and use Medical Subject Headings (MeSH) terms
as a guide. Visit: http://www.nlm.nih.gov/mesh/meshhome.html.
The manuscript should include the following sections:
1) Original articles: Introduction, Methods, Results, Discussion and References.
2) Clinical case reports: Introduction, Clinical case, Discussion and References.
3) Clinicopathological cases: Clinical case, Discussion and
References.
An Acknowledgment section may be included directly following
the Reference section. Granting institutions or other financial aid
may be listed under Acknowledgments. If there are persons, other
than the authors, who assisted with the study or preparation of the
manuscript (i.e., technicians, nurses, ancillary health personnel,
editorial assistance), they may be listed here.
References
References should be numbered consecutively, double spaced,
and listed in the order in which they appear in the text using arabic numbers (in the text, references are indicated by superscript
arabic numbers after any punctuation). The Reference section
should follow the last section of the manuscript. It is not necessary to begin the References on a separate page. The references
should be formatted according to the instructions from the U.S.
National Library of Medicine. Abbreviated journal names should
reflect the style of Index Medicus (visit http://www.nlm.nih.gov/
tsd/serials/lji.html) When a reference cites six or fewer authors,
names should be included for all authors. When there are seven or
more authors, use the first six names followed by et al. Authors
are responsible for the accuracy of references. Please use the
following examples for presentation of references:
Journals:
• Klimo P, Rao G, Brockmeyer D. Congenital anomalies of
the cervical spine. Neurosurg Clin North Am 2007;18:463478.
• Published book:
• Bell RM. Holy Anorexia. Chicago: University of Chicago
Press; 1985.
• Book chapter:
• Hudson JI, Hudson RA, Pope HG. Psychiatric comorbidity and eating disorders. In: Wonderlich S, Mitchell J, eds.
Eating Disorders Review. Part 1. Oxford: Radcliffe Publishing; 2005. pp. 43-58.
• Internet consult:
• McKusick VA. Klippel Feil syndrome. Online. Mendelian
inheritance in man (accessed: March 26, 2008). Available at: http://www.ncbi.nlm.nih.gov/entrez/dispomim.
cgi?id=148900.
Tables and Figures All tables and figures including schemes,
diagrams and table legends must be presented in an editable
form. Do not “copy and paste” material from external sources.
Tables
Tables should be numbered using arabic numbers in the order in
which they are cited in the text and include a short descriptive
title. Tables should not reiterate information presented in the
Results section. For preparation of Tables containing only data,
use the “Table Editor” function of your word processing program.
Do not insert any vertical lines. Use horizontal lines only for
clarity of information under table headings. Confirm that information provided below each table heading is properly aligned
and clearly identifiable. Tables containing schemes or diagrams
should be prepared in PowerPoint; graphics with shading, bars,
dispersions, etc. should be prepared using Excel. Each Table
should be prepared on a separate page, following the Reference
section. Table footnotes should include any abbreviations that
need to be explained and notes relating to the Table should be
presented alphabetically using superscript letters.
Figures
Authors should number figures in the order in which they appear in the text. Figures include graphs, charts, photographs,
and illustrations. Each figure should be accompanied by a selfexplanatory legend. Digital images should be legible and printed
with a resolution of not less than 300 dpi, using .jpg (jpeg) or
.bmp extension.
If photographs submitted correspond to actual patients, the
anonymity of the patients should be protected or written permission from the patient and/or family/legal guardian to publish
the photograph(s) should be submitted. Figure legends with
corresponding figure numbers should be typed consecutively
on a separate page following the last Table (or following the
Acknowledgments if there are no Tables).
Permission to use previously published Tables or
Figures
If the manuscript contains Tables or Figures that have been previously published, permission must be obtained from the original
Publisher in order to reproduce the material. This applies to Tables or Figures that have been modified, adapted or translated. A
sample “permission” letter is available from the Editorial Office
of Boletín Médico del Hospital Infantil de México. Appropriate
credit must be written per the following example:
Reprinted (or Adapted, Modified, Translated) from Castilloux J,
Noble AJ, Faure C. Risk factors for short- and long-term morbidity
in children with esophageal atresia. J Pediatr 2010;156:755-760.
With permission.
Ethical approval of studies and informed consent
In regard to possible ethical conflicts, the rights of patients of
privacy and confidentiality shall be maintained. For studies
involving human subjects, state the manner in which informed
consent was obtained from the study participants (i.e., oral or
written). All manuscripts reporting data from studies involving
humans or animals are subject to formal review and approval
by an appropriate institutional review board or ethics committee
and should be described at the end of the Methods section. For
investigators who do not have formal ethics review committees,
the principles outlined in the Declaration of Helsinki as well as in
the Guide for the Care and Use of Laboratory Animals (Institute
of Laboratory Animal Resources, Commission on Life Sciences,
National Research Council) should be followed.
Review process
The first review of the manuscript is performed by the Editor
to assure that the manuscript corresponds to the theme of the
journal and that all required information has been properly
submitted in accordance with the Guidelines to Authors. The
second review is carried out by two independent reviewers
who have been assigned to the manuscript on the basis of their
field of expertise. The identities of authors’ and reviewers’ are
kept confidential.
Copyright
All accepted manuscripts become the permanent property of the
Boletín Médico del Hospital Infantil de México and may not be
published elsewhere, in whole or in part, without prior written
permission from the Editor and appropriate credit to the authors
and to Boletín Médico del Hospital Infantil de México. Upon
acceptance of an article for publication in Boletín Médico del
Hospital Infantil de México, a letter signed by all authors shall
be submitted transferring copyright of the published article to
Boletín Médico del Hospital Infantil de México. If the author(s)
wishes to reprint any of the material already published in Boletín
Médico del Hospital Infantil de México, prior authorization is
required from the Editor.
Note: For periodic up-to-dates of "Guidelines to Authors",
please consult our internet page: www.himfg.edu.mx