Composición corporal y condición física en niños

Transcription

Composición corporal y condición física en
niños y adolescentes con síndrome de Down;
efectos de un programa de acondicionamiento
físico combinado con saltos pliométricos
Body composition and physical fitness in children and
adolescents with Down syndrome; effects of a conditioning
program combined with plyometric jumps
ALEJANDRO GONZÁLEZ DE AGÜERO LAFUENTE
Composición corporal y condición física en niños y adolescentes con síndrome de Down;
efectos de un programa de acondicionamiento físico combinado con saltos pliométricos.
-2-
Tesis Doctoral Europea [European PhD Thesis]
2011
COMPOSICIÓN CORPORAL Y CONDICIÓN FÍSICA EN
NIÑOS Y ADOLESCENTES CON SÍNDROME DE DOWN;
EFECTOS DE UN PROGRAMA DE ACONDICIONAMIENTO
FÍSICO COMBINADO CON SALTOS PLIOMÉTRICOS.
BODY COMPOSITION AND PHYSICAL FITNESS IN CHILDREN AND ADOLESCENTS WITH DOWN
SYNDROME; EFFECTS OF A CONDITIONING PROGRAM COMBINED WITH PLYOMETRIC JUMPS.
ALEJANDRO GONZÁLEZ DE AGÜERO LAFUENTE
Departamento de Fisiatría y Enfermería
Facultad de Ciencias de la Salud y del Deporte
Universidad de Zaragoza
-4-
A mis padres, a Sara
-5-
-6-
“Las ideas no duran mucho. Hay que hacer algo con ellas.”
Santiago Ramón y Cajal, Premio Nobel de Medicina y “aragonés”
“Cuando llegué a casa, papá y mamá no sabían qué hacer conmigo.
Ahora no sabrían qué hacer sin mí.”
Pablo, un niño con síndrome de Down
-7-
-8-
Composición corporal y condición física en niños y
adolescentes con síndrome de Down; efectos de un programa
de acondicionamiento físico combinado con saltos pliométricos.
Body composition and physical fitness in children and adolescents with Down syndrome;
effects of a conditioning program combined with plyometric jumps.
DIRECTORES DE TESIS:
Dr. José A. Casajús Mallén
Dr. Germán Vicente Rodríguez
Dr. Ignacio Ara Royo
Facultad de Ciencias de la Salud y
Facultad de Ciencias de la Salud
Facultad de Ciencias del Deporte,
del Deporte
y del Deporte
Toledo
Universidad de Castilla-La Mancha
MD, PhD
PhD
PhD
MIEMBROS DEL TRIBUNAL:
Presidente
Secretario
Ricardo Mora Rodríguez
Gerardo Rodríguez Martínez
Departamento de Actividad Física y
Departamento de Pediatría y
Ciencias del Deporte
Radiología
PhD
MD, PhD
Vocal 1º
Vocal 2º
Vocal 3º
Fernando D. Pereira
Manuel J. Castillo Garzón
Antonio F. Laclériga Giménez
Faculdade de Motricidade Humana
Departamento de Fisiología
Médica
Facultad de Ciencias de la Salud
Universidad de Oporto
Universidad de Granada
Universidad San Jorge
PhD
MD, PhD
MD, PhD
-9-
-10-
Prof. Dr. José Antonio CASAJÚS MALLÉN
Prof. Titular de Universidad
----------Departamento de Fisiatría y Enfermería
JOSÉ ANTONIO CASAJÚS MALLÉN, PROFESOR TITULAR DE LA
UNIVERSIDAD DE ZARAGOZA, CERTIFICA:
Que la Tesis Doctoral titulada “Composición corporal y condición física en niños y
adolescentes con síndrome de Down; efectos de un programa de acondicionamiento
físico combinado con saltos pliométricos.” que presenta D. ALEJANDRO GONZÁLEZ
DE AGÜERO LAFUENTE al superior juicio del Tribunal que designe la Universidad
de Zaragoza, ha sido realizada bajo mi dirección durante los años 2008-2011, siendo
expresión de la capacidad técnica e interpretativa de su autor en condiciones tan
aventajadas que le hacen merecedor del Título de Doctor, siempre y cuando así lo
considere el citado Tribunal.
Fdo. José A. Casajús Mallén
En Zaragoza a 8 de agosto de 2011
-11-
-12-
Prof. Dr. Germán VICENTE RODRÍGUEZ
----------Departamento de Fisiatría y Enfermería
GERMÁN
VICENTE
RODRÍGUEZ,
PROFESOR
TITULAR
DE
LA
UNIVERSIDAD DE ZARAGOZA, CERTIFICA:
físico combinado con saltos pliométricos.” que presenta D. ALEJANDRO
GONZÁLEZ DE AGÜERO LAFUENTE al superior juicio del Tribunal que designe la
Universidad de Zaragoza, ha sido realizada bajo mi dirección durante los años 20082011, siendo expresión de la capacidad técnica e interpretativa de su autor en condiciones
tan aventajadas que le hacen merecedor del Título de Doctor, siempre y cuando así lo
Fdo. Germán Vicente Rodríguez
-13-
-14-
Prof. Dr. Ignacio ARA ROYO
----------Departamento de Actividad Física y Ciencias del Deporte
Facultad de Ciencias del Deporte, Toledo
IGNACIO ARA ROYO, PROFESOR TITULAR DE LA UNIVERSIDAD DE
CASTILLA-LA MANCHA, CERTIFICA:
físico combinado con saltos pliométricos.” que presenta D. ALEJANDRO GONZÁLEZ
DE AGÜERO LAFUENTE al superior juicio del Tribunal que designe la Universidad
de Zaragoza, ha sido realizada bajo mi dirección durante los años 2008-2011, siendo
expresión de la capacidad técnica e interpretativa de su autor en condiciones tan
aventajadas que le hacen merecedor del Título de Doctor, siempre y cuando así lo
Fdo. Ignacio Ara Royo
-15-
-16-
Lista de publicaciones [List of publications]
La presente Tesis Doctoral es un compendio de trabajos científicos previamente
publicados, aceptados para publicación o sometidos a revisión. Las referencias de cada
uno de los artículos que componen este documento se detallan a continuación:
I.
González-Agüero A, Vicente-Rodriguez G, Moreno LA, Guerra-Balic M, Ara I,
Casajus JA. Health-related physical fitness in children and adolescents with Down
syndrome and response to training. Scand J Med Sci Sports. 2010 Oct;20(5):71624.
II.
González-Agüero A, Vicente-Rodriguez G, Moreno LA, Casajus JA. Bone mass
in male and female children and adolescents with Down syndrome. Osteoporos
Int. 2011 Jul;22(7):2151-7.
III.
González-Agüero A, Ara I, Moreno LA, Vicente-Rodriguez G, Casajús JA. Fat
and lean masses in youths with Down syndrome: gender differences. Res Dev
Disabil. 2011 Sep-Oct;32(5):1685-93.
IV.
González-Agüero A, Vicente-Rodriguez G, Moreno LA, Casajús JA. Dimorfismo
sexual en grasa corporal en adolescentes con síndrome de Down. Rev Esp
Obesidad. 2010 Jan-Feb;8(1):28-33.
V.
González-Agüero A, Villarroya MA, Vicente-Rodriguez G, Casajús JA. Masa
muscular, fuerza isométrica y dinámica en las extremidades inferiores de niños y
adolescentes con síndrome de Down. Biomecánica. 2009;17(2):46-51.
VI.
González-Agüero A, Vicente-Rodriguez G, Ara I, Moreno LA, Casajús JA.
Accuracy of prediction equations to assess percentage of body fat in children and
adolescents with Down syndrome compared to air displacement plethysmography.
Res Dev Disabil. 2011 Sep-Oct;32(5):1764-9.
VII. González-Agüero A, Vicente-Rodriguez G, Gómez-Cabello A, Ara I, Moreno
LA, Casajús JA. A combined training intervention programme increases lean mass
in youths with Down syndrome. Res Dev Disabil. 2011 Nov;32(6):2383-8.
VIII. González-Agüero A, Vicente-Rodriguez G, Ara I, Moreno LA, Casajús JA.
Conditioning including plyometric jumps training improves cardiovascular fitness
in youths with Down syndrome. Adapt Phys Activ Q. submitted.
IX.
González-Agüero A, Vicente-Rodriguez G, Gómez-Cabello A, Ara I, Moreno
LA, Casajús JA. A 21-week bone deposition promoting exercise programme
increases bone mass in youths with Down syndrome. Dev Med Child Neurol.
submitted.
-17-
-18-
Tabladecontenidos
Proyecto de investigación .................................................................................... 23 Listado de abreviaturas ........................................................................................ 25 Resumen general .................................................................................................... 27 1. Introducción ........................................................................................................ 31 1.1 1.2 El síndrome de Down ................................................................................... 31 Condición física en niños y adolescentes con síndrome de Down ................. 34 1.2.1 Composición Corporal ............................................................................................................. 34 1.2.2 Condición Aeróbica ................................................................................................................. 36 1.2.3 Fuerza Muscular ...................................................................................................................... 38 1.3 Efectos del entrenamiento físico en niños y adolescentes con síndrome de Down 41 1.3.1 Entrenamiento cardiovascular .............................................................................................. 41 1.3.2 Entrenamiento de fuerza ........................................................................................................ 42 1.3.3 Entrenamiento combinado cardiovascular y de fuerza ..................................................... 42 2. Hipótesis .............................................................................................................. 47 3. Objetivos .............................................................................................................. 49 4. Material y métodos ........................................................................................... 53 4.1 Comité de ética ................................................................................................. 53 4.2 Muestra y diseño del estudio ............................................................................ 53 4.3 Pruebas de composición corporal ...................................................................... 55 4.4 Pruebas de condición física ............................................................................... 56 4.5 Otros datos ....................................................................................................... 59 4.6 Programa de entrenamiento ............................................................................. 59 4.7 Análisis estadísticos ........................................................................................... 61 5. Referencias .......................................................................................................... 63 6. Resultados y discusión ...................................................................................... 71 7. Aportaciones principales de la Tesis Doctoral ........................................... 175 8. Conclusiones ..................................................................................................... 179 Apéndice ................................................................................................................ 183 Agradecimientos .................................................................................................. 185 -19-
-20-
Table of contents
Research Project ..................................................................................................... 23 List of abbreviations [part in Spanish] ............................................................... 25 General abstract ..................................................................................................... 29 1. Introduction [part in Spanish] ......................................................................... 31 1.1 1.2 The Down syndrome .................................................................................... 31 Physical fitness in children and adolescents with Down syndrome .............. 34 1.2.1 Body Composition ................................................................................................................... 34 1.2.2 Cardiovascular Fitness ............................................................................................................ 36 1.2.3 Muscular Strength ................................................................................................................... 38 1.3 Effects of training in children and adolescents with Down syndrome .......... 41 1.3.1 Cardiovascular training .......................................................................................................... 41 1.3.2 Strength training ..................................................................................................................... 42 1.3.3 combined cardiovascular and strength training ................................................................. 42 2. Hypothesis ........................................................................................................... 47 3. Objectives ............................................................................................................ 51 4. Material and methods [part in Spanish] ....................................................... 53 4.1 Etics comitee ..................................................................................................... 53 4.2 Sample and study design ................................................................................... 53 4.3 Body composition test ....................................................................................... 55 4.4 Physical fitness test ........................................................................................... 56 4.5 Other data ......................................................................................................... 59 4.6 Training program ............................................................................................... 59 4.7 Statistical analyses ............................................................................................ 61 5. References ........................................................................................................... 63 6. Results and discussion ...................................................................................... 71 7. Contributions of the Doctoral Thesis ........................................................... 177 8. Conclusions ....................................................................................................... 181 Appendix ................................................................................................................ 183 Acknowledgments ................................................................................................ 185 -21-
-22-
Proyectodeinvestigación
La Tesis Doctoral que se presenta a continuación, así como los artículos que la
conforman, se enmarcan dentro del siguiente proyecto de investigación:
“Determinantes fisiológicos y genéticos de la composición corporal en adolescentes con
síndrome de Down. Respuestas y adaptaciones al ejercicio de fuerza.”
Proyecto autonómico de 3 años de duración financiado por el Gobierno de Aragón
(Proyecto PM 17/2007) y desarrollado en colaboración con agrupaciones relacionadas
con el ámbito: Fundación Down Zaragoza y Special Olympics Aragón.
Investigador principal: José A. Casajús Mallén.
Researchproject
The present Doctoral Thesis, as well as the manuscripts that are part of it, are within the
frame of the following research project:
“Physiological and genetic determinants of the body composition in children and
adolescents with Down syndrome. Response and adaptations to the strength training.”
Autonomic Project of 3 years of length granted by the Aragon’s Government (Proyecto
PM 17/2007) and developed in collaboration with associations with long experience in
the field: Fundación Down Zaragoza y Special Olympics Aragón.
Principal investigator: José A. Casajús Mallén.
-23-
-24-
Listadodeabreviaturas[Listofabbreviations*]
SD
Síndrome de Down
DI
Discapacidad intelectual
CMO
Contenido mineral óseo
DMO
Densidad mineral ósea
AF
Actividad física
IMC
Índice de masa corporal
V̇ O2max
Consumo máximo de oxígeno
FCmax
Frecuencia cardíaca máxima
CRmax
Cociente respiratorio máximo
VEmax
Ventilación respiratoria máxima
DXA
Absorciometría dual de rayos-X
1RM
Una repetición máxima
* Abbreviations in English language are shown in each manuscript included in this
document.
-25-
-26-
Resumengeneral
Las personas con síndrome de Down tienen una composición corporal y una condición
física poco saludables comparados con sus homólogos sin discapacidad. Debido al
incremento en su esperanza de vida, ciertas enfermedades asociadas con la edad adulta
que anteriormente no habían sido detectadas en personas con síndrome de Down
comienzan a aparecer, y a edades incluso más tempranas. El entrenamiento físico mejora
composición corporal y condición física en adolescentes sin discapacidad. Sin embargo,
no existen muchas referencias a este respecto en jóvenes con síndrome de Down.
Por tanto, el principal objetivo de esta Tesis Doctoral fue ampliar el conocimiento
científico respecto a composición corporal y condición física en jóvenes con síndrome de
Down y, por otro lado, determinar los efectos de un programa de 21 semanas de
acondicionamiento físico combinado con saltos pliométricos sobre dichas variables.
Un grupo de 32 jóvenes con síndrome de Down y otro grupo de 35 jóvenes sin
discapacidad participaron en el estudio. Se evaluó su composición corporal usando
absorciometría dual de rayos X, pletismografía por desplazamiento de aire y
antropometría; y su condición física con pruebas de esfuerzo y test de fuerza isométricos
y dinámicos. 16 participantes con síndrome de Down realizaron un entrenamiento de
acondicionamiento físico combinado con saltos pliométricos durante 21 semanas, el resto
actuaron como grupo control (con y sin síndrome de Down).
Al término del programa de entrenamiento, el grupo de intervención mostró mejoras
significativas en resistencia cardiorrespiratoria, masa muscular y masa ósea, indicando
que este tipo de ejercicio puede ser beneficioso para niños y adolescentes con síndrome
de Down.
-27-
-28-
Generalabstract
Children and adolescents with Down syndrome have a worse body composition and
physical fitness than their counterparts without disabilities. Due to the increment in their
lifespan, diseases more common to happen in the adulthood, which previously have not
been detected in persons with Down syndrome, are now starting to appear and even at an
earlier age. It is well known that physical training improves physical fitness and body
composition in children and adolescents without disabilities. However, not much is
known about body composition, physical fitness or the effect of training in these variables
in youths with Down syndrome.
Therefore, the main objective of this Doctoral Thesis was to increase the scientific
knowledge in body composition and physical fitness of youths with Down syndrome, and
to observe the effects of 21 weeks of conditioning combined with plyometric jumps over
those variables.
A group of 32 youths with Down syndrome and another group of 35 youths without
disabilities took part in the study. Body composition was evaluated using dual energy Xray absorptiometry, air displacement plethysmography and anthropometry; and physical
fitness towards effort test in a treadmill, and also towards isometric and dynamic strength
tests. A group of 16 participants with Down syndrome performed a training of
conditioning combined with plyometric jumps during 21 weeks; the remaining youths
were the control group (with and without Down syndrome).
At the end of the training program, the intervention group showed improvements in
cardiovascular fitness, lean mass and bone mass, indicating that this kind of training
could be beneficial for children and adolescents with Down syndrome.
-29-
-30-
1.Introducción[Introduction]
1.1 ElsíndromedeDown
El síndrome de Down (SD) fue descrito pormenorizadamente por primera vez por
John Langdon H. Down en 1866, mientras trabajaba en el Asilo para Retrasados
Mentales de Earlswood (Inglaterra). En su informe detalló las características de un grupo
de pacientes que presentaban muchas similitudes tanto físicas como cognitivas y
emocionales.(1) Décadas después, el SD ha sido ya profundamente estudiado y se sabe con
exactitud que se trata de una condición genética caracterizada por discapacidad intelectual
(DI) de diferentes grados, y que está causado por anomalías en el cromosoma 21.(2)
Dentro de esas anomalías la más común es la triplicación del cromosoma, pero también
están descritas la no disyunción y la translocación.(3) La estimación del SD es alrededor
de 1/700 a 1/1000 nacidos vivos en la actualidad.(2,
4)
Se han descrito más de 80
características clínicas en individuos con SD, incluidos problemas cardiacos congénitos,
presentes aproximadamente en el 40% de los individuos con SD.(3) El problema cardíaco
congénito más común es el prolapso de la válvula mitral, aproximadamente presente en el
80% de las ecocardiografías anómalas efectuadas a estos sujetos.(5) La leucemia es otra
enfermedad que aparece con mayor frecuencia en niños con SD que en niños sin SD; sin
embargo las personas con SD tienen menor riesgo de desarrollar otro tipo de tumores
sólidos en todos los grupos de edad.(6)
La esperanza de vida de las personas con SD se está viendo aumentada gracias
principalmente a los avances de la ciencia, y en especial de la medicina. Durante las
últimas décadas, las personas con SD, han pasado de una esperanza de vida media de 9
años en 1929,(7) a más de 55 años hoy en día.(4 ,8) Debido a este aumento en su esperanza
de vida, ciertas enfermedades con tendencia a aparecer con la edad adulta y la vejez como
-31-
la osteoporosis, la osteopenia o el síndrome metabólico, que anteriormente no habían sido
detectadas en esta población, comienzan a aparecer, y a edades más tempranas que en
población sin SD, agravando así sobremanera los problemas propios de esta población.
Por tanto, no se trata únicamente de vivir más años, sino de vivirlos de una manera lo más
autónoma posible y sobre todo, con salud para poder disfrutar, mejorando así su calidad y
expectativas de vida.
Estudios científicos indican que algunas de las características físicas del SD están
relacionadas con el ejercicio: hipotonía, hipermovilidad de las articulaciones, hiperlaxitud
de los ligamentos, ligera a moderada obesidad, sistema respiratorio y cardiovascular poco
desarrollado, estatura más baja y extremidades cortas en relación al torso.(3,
9)
Además
también se ha descrito un equilibrio muy pobre y dificultades en la percepción
espacial.(10) Asociadas a la hipotonía y a la hipermovilidad encontramos lordosis, caderas
dislocadas, pies planos, cabeza adelantada e inestabilidad atlantoaxial.(10 ,11) Es de hecho,
esta inestabilidad atlantoaxial uno de los problemas más importantes que se relacionan
con la poca participación en actividades deportivas, ya que las actividades de contacto
brusco (p. ej., Judo, rugby, etc.) están contraindicadas en casos de personas con SD e
inestabilidad atlantoaxial.(11) En parte debido a estas características clínicas, las personas
con SD tienen niveles más bajos de condición física y una composición corporal menos
saludable que otras personas de su misma edad sin SD, con o sin DI.(12-14)
Como consecuencia de lo anteriormente mencionado, los jóvenes con SD tienden hacia
comportamientos más sedentarios y pasan más tiempo dentro de casa, que sus homólogos
sin SD.(15) Otra causa de este comportamiento sedentario podría ser la sobreprotección
que estos niños a menudo tienen por parte de sus familias.(16) Los bajos niveles de
condición física previamente comentados, unidos a la inactividad física, darán lugar a un
-32-
deterioro funcional reflejado en incrementos en la prevalencia del sobrepeso y la obesidad
y en una reducción del desarrollo de la masa ósea y muscular lo cual puede, finalmente,
resultar en un agravamiento de los problemas clínicos de esta población (Figura 1).
Figura 1. Asociación de complicaciones en personas con síndrome de Down.
Traducido de González-Agüero et al. 2010, Scand J Med Sci Sports©
Está ampliamente demostrado que la actividad física (AF) y la práctica deportiva
producen gran cantidad de beneficios relacionados con la salud a todas las edades, y aún
más si cabe en niños y adolescentes. La AF mejora la capacidad cardiovascular,(17)
contribuye a un estilo de vida más saludable y puede mejorar el sistema de defensa
antioxidante,(18) el cual retrasa el envejecimiento celular. En niños y adolescentes, la AF
regular y los niveles de condición física están íntimamente relacionados con una
adquisición de masa ósea superior,(19) con una reducción de masa grasa(20
,21)
y con un
-33-
desarrollo adiposo saludable.(22) Las intervenciones de AF también se han mostrado
beneficiosas en niños y niñas con leucemia.(23) El beneficio que se obtiene de la práctica
de AF no es únicamente físico, existen también otros factores sociales asociados a la
participación deportiva.(24) Por tanto, la AF podría ser un factor que potencialmente
ayudaría a jóvenes con SD a mejorar su calidad de vida, desde un punto de vista tanto
físico como social.
De acuerdo con el Colegio Americano de Medicina del Deporte (ACSM), las variables de
la condición física relacionadas con la salud son: composición corporal, condición
aeróbica, fuerza muscular y flexibilidad.(25) Estudiar la flexibilidad no es, sin embargo
una prioridad en personas con SD ya que, una gran flexibilidad es, precisamente, una de
sus características clínicas.(9)
Con el propósito de obtener una base sólida de conocimiento, a continuación se hará un
resumen con los datos encontrados en la literatura científica publicada, previa a esta Tesis
Doctoral, en lo referente a condición física, composición corporal y también los efectos
que el entrenamiento físico tiene en niños y adolescentes con SD.
1.2 CondiciónfísicaenniñosyadolescentesconsíndromedeDown
Todos los estudios relacionados con la condición física y la salud en niños y adolescentes
con SD incluidos en este documento se encuentran resumidos en la Tabla 1.
1.2.1ComposiciónCorporal
El Índice de Masa Corporal (IMC) y los diferentes compartimentos corporales como masa
grasa, masa magra y masa ósea han sido estudiados en niños y adolescentes con SD.
Pese a que en un estudio describieron a los niños con SD como menos activos y más
tendentes a pasar más tiempo dentro de sus casas, no encontraron diferencias en el IMC,
-34-
comparados con sus hermanos sin DI.(15) No obstante, los trabajos científicos revisados
habitualmente encuentran valores más altos de IMC y porcentaje de grasa corporal en
personas con SD comparadas con personas sin SD prácticamente a cualquier edad.(26-28)
En estudios llevados a cabo solo con adultos, también se encontró un IMC y porcentaje
graso más alto en sujetos con SD comparados con sujetos con DI sin SD,(32 ,33) pero no se
hallaron diferencias en el IMC entre sujetos adultos activos o sedentarios con SD.(34) Luke
y col.(29) no encontraron diferencias en la masa libre de grasa (medida mediante dilución
de deuterio y otros métodos) entre niños con y sin SD. Sin embargo, mediante
absorciometría dual de rayos-X (DXA), Guijarro y col.(30) y Baptista y col.(28), estimaron
la masa muscular total siguiendo el protocolo establecido por Heymsfield y col.(31) y
encontraron niveles más bajos tanto en hombres como en mujeres adultos jóvenes con
SD, comparados con sus homólogos sin SD. Niños, adolescentes y adultos con SD
presentan de manera general, niveles bajos de contenido mineral óseo (CMO) y densidad
mineral ósea (DMO) comparados con personas sin SD de su misma edad. Estos niveles
bajos han sido detectados tanto a nivel de cuerpo completo, como en la espina vertebral
lumbar,(26 ,28 ,35 ,36) extremidades superiores e inferiores,(28) y en la cadera.(30) También la
DMO volumétrica ha sido estudiada, encontrando niveles más bajos en extremidades(28) y
espina lumbar(30) en personas con SD que en personas sin SD. De manera similar, un
estudio con ultrasonografía detectó una amplitud dependiente de la velocidad del sonido,
la cual depende de la DMO, más baja en niños con SD que en niños sin SD, con o sin DI.
Sin embargo, estas diferencias permanecían estables con el tiempo,(37) lo que sugirió baja
masa ósea pero desarrollo normal.
A pesar de que existe información sobre composición corporal en personas con SD, se
necesitan más estudios para describir con más detalle, no solo la composición corporal de
niños y adolescentes con SD sino también el efecto del ejercicio sobre la masa magra, la
-35-
masa grasa y la masa ósea en esta población. Así mismo, tampoco hasta la fecha ninguna
ecuación de predicción ha sido validada, o demostrada como más fiable para evaluar el
porcentaje de grasa corporal en este grupo de población concreto.
1.2.2CondiciónAeróbica
La capacidad aeróbica de niños y adolescentes con SD comparados con sujetos sin SD,
con o sin DI, ha sido descrita como muy baja en diversas ocasiones.(12 ,13 ,38 ,39)
Eberhard y col.(38) en 1988 encontraron un consumo máximo de oxígeno (V̇ O2max) más
bajo y menores tiempo y carga de trabajo en niños con SD comparados con sus
homólogos sin SD. En las últimas décadas, se han hecho considerables progresos en
cuanto a la evaluación de los niños y adolescentes con DI, y especialmente con SD.
Fernhall y col.(40) desarrollaron un test en tapiz rodante y lo validaron para adolescentes y
adultos con DI (incluidos algunos con SD). Los resultados de este estudio mostraron un
coeficiente de fiabilidad de 0.94 entre dos pruebas repetidas. En otro estudio, Fernhall y
col.(41) desarrollaron una ecuación de regresión para predecir el consumo de oxígeno pico
(V̇ O2pico) en niños y adolescentes con DI (incluidos algunos con SD) mediante pruebas de
campo (600-yard walk-run, 20m shuttle run, y un modificado 16m shuttle run), y en el
año 2000 validaron la ecuación de nuevo con el 20 m shuttle run.(42) Sin embargo, Guerra
y col.(43) encontraron que la fórmula de regresión para averiguar el V̇ O2pico en niños con
DI no era válida para la muestra de adolescentes con SD de su estudio, y atribuyó esto al
bajo número de participantes con SD en el estudio previo de Fernhall. Estaba claro que
las personas con SD, en términos de capacidad de ejercicio máxima, no se comportaban
como las personas con DI en general, se trataba pues de un grupo específico a estudiar.
Más tarde, Fernhall y col.(13) desarrollaron una ecuación para predecir la frecuencia
cardíaca máxima (FCmax) en individuos con DI (incluidos algunos niños y adolescentes
-36-
con SD). Fernhall y col.(40) encontraron también niveles más bajos de V̇ O2pico, volumen
ventilatorio máximo (VEmax), FCmax y cociente respiratorio máximo (CRmax) en niños y
adolescentes con SD comparados con otros sin SD, con o sin DI. Baynard y col.,(39) en un
estudio multicéntrico más reciente, dividieron a toda la muestra en grupos de edad y
encontraron niveles más bajos de V̇ O2pico (expresado en valores absolutos y relativos) en
todos los grupos de edad comparados con otros grupos sin SD, con y sin DI. Además,
alarmantemente observaron que el V̇ O2pico, en el grupo con SD, no cambiaba a partir de
los 16 años. Pitetti y Fernhall(44) demostraron además que la economía de carrera era peor
en individuos con SD comparados con otros sin SD, con o sin DI.
En estudios desarrollados sólo con adultos con SD también se han encontrado valores
más bajos de V̇ O2peak, VEpeak, HRpeak y RERpeak comparados con otros sin SD, con o sin
DI.(12 ,45) Climstein y col.(46) demostraron que la ecuación de predicción para calcular el
V̇ O2pico de adultos jóvenes con DI desarrollada por el ACSM tiende a sobreestimar dicho
valor cuando se aplica a población con SD, y por tanto, la prescripción de ejercicio
derivada debe basarse en medidas más reales.
Un nivel bajo de capacidad aeróbica se considera un factor de riesgo para problemas
cardiovasculares futuros, y puede tener como resultado una disminución de la esperanza
de vida también en personas con SD. Sin embargo, debido a la falta de estudios que en
relación a este tema, incluyan únicamente población pediátrica con SD, así como la
escasez de estudios longitudinales, no permite corroborar esta hipótesis, y por tanto, es
necesaria más investigación al respecto.
-37-
1.2.3FuerzaMuscular
Niveles adecuados de fuerza muscular se relacionan con la salud y ayudan a las personas
a ser más autónomas e independientes;(25) sin embargo, es difícil mantener esos niveles
especialmente durante la vejez.(47 ,48)
Como la esperanza de vida de las personas con SD está incrementándose, es importante
estudiar la evolución de los niveles de fuerza en esta población y, si fuera necesario,
desarrollar programas para su mejora. Únicamente se encontró un estudio en el que
valoraran la fuerza muscular en niños con SD. Mercer y Lewis(27) encontraron niveles
más bajos de fuerza en los músculos involucrados en la abducción de la cadera y la
extensión de la rodilla en niños con SD comparados con otros sin DI, siendo además el
peso corporal, la talla, el sexo y el IMC buenos predictores para el pico de fuerza en
población con SD.
En población adulta con SD, varios estudios han mostrado niveles más bajos de fuerza en
los músculos implicados en las articulaciones del codo(49) y de la rodilla,(45) así como
musculatura del cuádriceps y muslo,(50) espalda baja(34) y piernas(32) comparándolos con
otros sin SD, con o sin DI.
Los estudios desarrollados hasta el momento parecen indicar que las personas con SD
tienen niveles bajos de fuerza, lo cual podría estar asociado con algunos de los problemas
clínicos descritos previamente. Se necesita más investigación sobre el tema para clarificar
si hay unos niveles bajos de fuerza generalizados en niños y adolescentes con SD y si
estos pueden mejorar con el entrenamiento.
-38-
Participantes
19
7M, 12V
133
39
7
67
33M, 34V
13
6M, 7V
119
57M, 62V
89, 47 obesos
Estudio
Guerra y col. (2009)
Baynard y col. (2008)
Guijarro y col. (2008)
Halaba y col. (2006)
Baptista y col. (2005)
Baynard y col. (2004)
Pitetti y Fernhall
(2004)
Fernhall y col. (2003)
14.5
14.8±2.6
18.5±2.3
22.8 ± 5.9
23.3 ± 6.2
9.6 ± 1.8
26 ± 7
9 a 45
Edad
14.8 ± 3
Test individualizado en
tapiz hasta agotamiento
DXA
Ultrasonido en las falanges
de la mano.
DXA.
Recolección de datos de los
últimos 20 años, usando el
test validado de tapiz
rodante.
84 con DI sin SD,
22 obesos
Test de tapiz rodante
Continúa…
- FCmax mas baja en grupo SD, sin diferencias entre obesosno obesos
- Controlando por FCmax, sin diferencias en capacidad
aeróbica entre obesos y no obesos con SD
- Sujetos con SD mostraron economía de carrera peor que
los sujetos in SD.
- La determinación del umbral ventilatorio es muy
complicado, niveles bajos de VO2pico, VEmax, FCmax y CRmax
- Menos masa muscular en el grupo de mujeres, porcentaje
graso e IMC más alto.
- CMO, DMO y DMO volumétrica más bajos en
extremidades superiores e inferiores y en espina en todo el
grupo.
- Velocidad del sonido dependiente de la amplitud más baja
en todas las edades y permanece estable con el tiempo.
- Masa magra total más baja en el grupo SD.
- DMO y área menores en cuerpo complete, espina lumbar y
cadera.
- DMO volumétrica más baja en la espina lumbar.
- V̇ O2pico absoluto y relativo más bajo en todos los grupos de
edad.
- V̇ O2pico no cambió a partir de los 16 años.
Metodología
Resultadosa
Test anaeróbico de Wingate - La fiabilidad del test fue cuestionable
- Los adolescentes con SD mostraron valores bajos de
WAnT comparado con valores publicados.
396 con DI sin SD Test de 20 m shuttle run
607 sin DI
17 con DI sin SD
67 sin DI
24 sin DI
78 sin DI
180 con DI sin
SD; 322 sin DI
Controles
No
Tabla 1. Estudios relativos a condición física y salud en niños y adolescentes con síndrome de Down.
-39-
-40-
10
3M, 7V
10
3M, 7V
Kao y col. (1992)
Eberhard y col. (1989)
14.8
10 a 16
8 sin DI
Valores de
referencia sin DI
30 sin DI
10 sin DI
17 sin SD
179 con DI sin
SD; 196 sin DI
Controles
No
Test de cicloergómetro.
DPX
Medidas antropométricas,
acelerómetros, cuestionarios.
Medidas antropométricas,
impedancia bioeléctrica,
dilución de deuterio.
Medidas antropométricas.
Dinamómetro.
Estudio multicéntrico con
tapiz rodante.
Metodología
Test de 20 m shuttle run y
test de tapiz rodante
- VO2max más bajo
- Rendimiento más bajo y menos carga máxima de trabajo.
- La presión sanguínea no cambia regularmente.
- DMO menor en la espina lumbar.
- Retraso en la distribución de la curva de DMO a través
de las edades.
- Sin diferencias en IMC.
- Menos activos, más tiempo dentro de casa.
- Sin diferencias en la masa libre de grasa.
- IMC y %GC más altos.
- Valores más bajos para picos de fuerza de abducción de
cadera y extensión de rodilla.
- Test-retest fiabilidad alta (.89 a .95)
- Peso, talla, sexo, IMC y nivel de actividad buenos
predictores para pico de fuerza en poblaciones con SD
- V̇ O2pico, VEmax, FCmax, and CRmax más bajos.
Resultados
- La formula de regresión para adolescentes con DI no es
válida para sus adolescentes con SD
Tabla1.(continúa)
: Todas las comparaciones son: grupo con SD frente a grupo sin SD (con o sin DI) si existe.
M = Mujer; V = Varón; SD = síndrome de Down; DI = discapacidad intelectual; DXA = absorciometría dual de rayos-X; DPX = densitometría dual de fotones;
IMC = índice de masa corporal; CMO = contenido mineral óseo; DMO = densidad mineral ósea; VO2 = consumo de oxigeno; VE = ventilación; FC =
frecuencia cardíaca; CR = cociente respiratorio.
a
30
Sharav y Bowman
(1992)
2 a 14
8.8 ± 2.5
10
6M, 4V
Luke y col. (1996)
21.8 ± 8.4
11.2 ± 2.4
97
Fernhall y col. (2001)
Edad
15.3±2.7
Mercer y Lewis (2001) 17
11M, 6V
Participantes
26
11M, 15V
Estudio
Guerra y col. (2003)
a
1.3 Efectosdelentrenamientofísicoenniñosyadolescentescon
síndromedeDown
Como hemos podido comprobar, los niños y adolescentes con SD muestran niveles
inferiores de fuerza muscular, condición aeróbica, masa muscular y masa ósea, unidos a
niveles superiores de masa grasa, comparados con sus homólogos con o sin DI. Dado que
la AF es un predictor significativo de la fuerza muscular, comprobar si intervenciones de
ejercicio supervisado pueden ayudar a incrementar la fuerza muscular y/o la condición
aeróbica o a mejorar la composición corporal, dando lugar a mejoras en salud, es un tema
importante que considerar.
Todos los estudios relacionados con los efectos del entrenamiento físico en niños y
adolescentes con SD incluidos en esta revisión están resumidos en la Tabla 2.
1.3.1Entrenamientocardiovascular
Únicamente se han podido encontrar 3 estudios que examinen los efectos del
entrenamiento aeróbico estandarizado en niños y adolescentes con SD.
Varela y col.(51) desarrollaron un programa de 16 semanas de entrenamiento utilizando un
ergómetro de remo, en 16 adolescentes y adultos jóvenes con SD. A pesar de que el grupo
que entrenó alcanzó niveles más altos de carga de trabajo no encontraron cambios en el
peso ni en el porcentaje graso. De igual manera, no reportaron cambios a nivel
cardiovascular ni de respuesta fisiológica en el test de tapiz rodante ni en el de remo.
Andriolo y col.,(24) en una revisión sistemática, analizaron las mejoras en salud física y
psicosocial en adultos con SD obtenidas mediante programas de entrenamiento aeróbico,
y concluyeron que no hay suficientes evidencias para asegurar mejoras. Millar y col.(52)
diseñaron un programa de ejercicio de 10 semanas de caminata y trote, para 14 niños y
adolescentes con SD; al término de la intervención no encontraron cambios en la
-41-
capacidad aeróbica en ninguno de los dos grupos, posiblemente debido a la baja
intensidad del ejercicio, sin embargo el grupo de entrenamiento mostró una mejora en la
carga de trabajo y tiempo hasta el agotamiento. Ordóñez y col.(53) entrenaron con
orientación aeróbica a 22 adolescentes con SD durante 12 semanas, consiguiendo al final
del periodo de entrenamiento que el porcentaje de masa grasa (evaluado mediante
antropometría) disminuyera significativamente, aunque no informaron sobre los efectos
cardiovasculares del ejercicio.
A pesar de que las investigaciones son limitadas, los resultados parecen apuntar a que el
entrenamiento aeróbico de relativa corta duración puede tener efectos positivos sobre la
composición corporal, sin embargo, las adaptaciones cardiovasculares parecen requerir
periodos de entrenamiento más largos y/o intensidades de entrenamiento más altas.
Nuevos estudios diseñados específicamente podrían contribuir a validar estas hipótesis en
niños y adolescentes con SD, visto que es posible mejorar la capacidad aeróbica en
adultos con SD.(54)
1.3.2Entrenamientodefuerza
Sólo un estudio realizado con jóvenes con SD se centró únicamente en el entrenamiento
de fuerza. Weber y French(55) estudiaron un grupo de 14 adolescentes con SD y diseñaron
2 programas de entrenamiento: uno de levantamiento de cargas y otro de ejercicios
isométricos. Concluyeron que los jóvenes que entrenaron con levantamiento de cargas
incrementaron más su fuerza muscular que el grupo de ejercicios isométricos.
1.3.3Entrenamientocombinadocardiovascularydefuerza
En el estudio de caso llevado a cabo por Lewis y col.,(56) una niña con SD ejecutó un
programa de entrenamiento combinado (cardiovascular y fuerza) durante 6 semanas.
-42-
Después del entrenamiento los resultados mostraron mejoras en la capacidad aeróbica y la
potencia anaeróbica.
Estos estudios sobre programas de entrenamiento abren una puerta a futuras
investigaciones que pretendan mejorar los niveles de fuerza o resistencia cardiovascular
en niños y adolescentes con SD, lo que puede tener efectos muy positivos en la salud y
calidad de vida desde diferentes enfoques. Por ejemplo, el entrenamiento de fuerza podría
producir incrementos en la fuerza e hipertrofia muscular, lo que podría también reducir la
hipotonía, equilibrar las disfunciones e incrementar el V̇ O2max y parámetros relacionados
con la masa ósea.
En resumen, niños y adolescentes con SD son una población especial en cuanto a
variables de condición física relacionadas con la salud. La composición corporal, en esta
población específica, parece ser menos saludable que la observada en sus homólogos sin
SD, como queda confirmado por mayores cantidades de masa grasa, niveles más bajos de
masa magra y unos parámetros relacionados con la masa ósea reducidos.
Además de esto, niños y adolescentes con SD muestran niveles más bajos de su condición
aeróbica y fuerza muscular, lo que puede trascender en una peor calidad de vida. A pesar
de que no existe toda la información deseable sobre condición física y salud en jóvenes
con SD, es evidente que esta población podría beneficiarse considerablemente de la
práctica de AF y la prescripción de ejercicio físico. Los datos de los relativamente pocos
estudios disponibles hasta la fecha indican una mejora en la composición corporal (p.ej.,
reducción de la masa grasa) de los individuos pero no en su capacidad aeróbica cuando
realizan entrenamiento aeróbico medio. Una posible explicación a esta falta de mejora
cardiovascular podría ser la baja intensidad y/o la duración del programa de ejercicio
prescrito.
-43-
Futuras investigaciones sobre este tema podrán dirigirse hacia temas pendientes como la
duración e intensidad del entrenamiento aeróbico para mejorar la capacidad aeróbica, o si
de hecho, más intensidad y/o duración en un entrenamiento de fuerza podría ser más
beneficioso para niños y adolescentes con SD. Por tanto, sí como indican las
investigaciones previas, el ejercicio físico puede mejorar la salud de este grupo de
población, esta línea de intervención debería ser prioritaria para incrementar sus
posibilidades de desarrollo personal, esperanza y calidad de vida.
-44-
No
No
10 sujetos
8 sujetos
No
Control
Antropometría, test
submáximo de
tapiz, modificación
del MargariaKalamen, 10RM
para brazos y
piernas.
10 ejercicios para
evaluar fuerza
muscular
Test caminando de
tapiz rodante.
Mediciones
antropométricas,
test gradual de tapiz
rodante o de remo.
Mediciones
antropométricas
Metodología
- Sin cambios en la capacidad
aeróbica.
- El grupo ejercicio mejoró el
tiempo hasta el agotamiento y el
grado
- Sin diferencias en repuesta
cardiovascular o psicológica.
- el grupo de ejercicio alcanzó
niveles más altos de carga de
trabajo.
- Significativa reducción en el
porcentaje de masa grasa.
Resultadosa
6 sem. Aeróbico 60-80% FCmax, 10 a 60
min por sesión; 2 a 3 sesiones por sem.
Intensidad fuerza incrementaba el
número de repeticiones y el peso; 10 a
45 minutos por sesión, 2 a 3 sesiones
por semana.
- IMC sin cambios.
- Descenso de la FC y el CR en
todas las fases del test de tapiz
rodante.
- Mejoras en la potencia anaeróbica
y la fuerza del tronco, y
extremidades (superiores e
inferiores).
Dos grupos: A) levantamiento de
- El grupo de levantamiento de
cargas 80%, B) isométricos 15 minutos cargas consiguió mejoras más
por sesión
amplias en todas las pruebas de
fuerza muscular
10 semanas andando y trotando; 6575% FCmax, 30 minutos por sesión, 3
sesiones por semana.
16 semanas ergómetro de remo:
intensidades de 55 a 70 % V̇ O2pico; 15 a
25 minutos por sesión, 3 sesiones por
semana.
12 semanas, intensidad basada en la
FC, de 30 a 60 minutos por sesión, 3
sesiones por semana.
Programa de entrenamiento
: en los resultados, todas las comparaciones son: grupo con SD frente a grupo sin SD (con o sin discapacidad intelectual) si existe.
M = Mujer; V = Varón; SD = síndrome de Down; DE = desviación estándar; IMC = índice de masa corporal; VO2 = consumo de oxigeno; HR = frecuencia cardíaca; RER =
cociente respiratorio; RM = repetición máxima.
a
Entrenamiento combinado aeróbico y de fuerza
1M
10.5
Lewis and FragalaPinkham (2005)
13 a 18
17.7 ± 2.9
14; 3M, 11V
Millar y col. (1993)
Entrenamiento de fuerza
14
Weber and French
3M, 11V
(1988)
21.4 ± 3
16V
16.2 ± 1
Edad
Varela y col. (2001)
Estudio
Participantes
Entrenamiento Aeróbico
Ordoñez y col. (2006) 22V
Tabla 2. Estudios con respecto a entrenamiento físico en niños y adolescentes con síndrome de Down.
-45-
Los artículos que forman parte de esta Tesis Doctoral están dentro una misma unidad
temática como puede verse en el título de la misma: “Composición corporal y condición
física en niños y adolescentes con síndrome de Down; efectos de un programa de
acondicionamiento físico combinado con saltos pliométricos”
-46-
2.Hipótesis
Niños y adolescentes con síndrome de Down tienen una composición corporal y una
condición física peor respecto a sus homólogos sin discapacidad.
Un programa de entrenamiento individualizado de acondicionamiento físico combinado
con saltos pliométricos es beneficioso para estos jóvenes; ayudándoles a alcanzar una
composición corporal y unos niveles de condición física más saludables y cercanos a los
jóvenes de su misma edad sin discapacidad.
2.Hypotheses
Children and adolescents with Down syndrome have a worse body composition than their
counterparts without disabilities.
An individualized training program of conditioning combined with plyometric jumps is
positive for these youths; helping them to achieve a body composition and physical
fitness healthier, and closer to the youths without disabilities.
-47-
-48-
3.Objetivos
El objetivo general de la presente Tesis Doctoral es ampliar el conocimiento científico en
cuanto a condición física y composición corporal relacionado con la salud, en jóvenes con
síndrome de Down; y por otro lado observar el efecto de 21 semanas de entrenamiento
individualizado de acondicionamiento físico combinado con saltos pliométricos sobre
dichas variables. En detalle, los objetivos específicos de cada uno de los 9 artículos que
componen la Tesis Doctoral son:
Artículo I. Revisar la literatura científica, previa a esta Tesis Doctoral, en relación
con la condición física, la composición corporal y también con los efectos que el
entrenamiento físico tiene en niños y adolescentes con SD.
Artículo II. Describir los niveles de masa ósea total y regional (zona lumbar,
cadera y cuello femoral) de niños y adolescentes con SD, comparándolos con un
grupo de homólogos sin SD.
Artículo III. Comparar la distribución total y regional de masa grasa y magra en
niños y adolescentes con y sin SD; investigar si el perímetro de cintura es un buen
indicador de adiposidad y evaluar la presencia de dimorfismo sexual en niños y
adolescentes con SD.
Artículo IV. Obtener datos antropométricos de adolescentes con SD y valorar si
su dimorfismo sexual en masa grasa es similar al descrito previamente para
adolescentes sin SD.
Artículo V. Describir los niveles de masa muscular y fuerza isométrica y
dinámica en adolescentes con SD y estudiar la posible relación entre masa
muscular y fuerza en esta población.
-49-
Artículo VI. Averiguar cuál de las ecuaciones de predicción de porcentaje de
grasa mediante mediciones antropometricas es la más adecuada para ser aplicada
en niños y adolescentes con SD, comparándolo con pletismografía por
desplazamiento de aire.
Artículo VII. Establecer cuál es el efecto de 21 semanas de entrenamiento de
acondicionamiento físico combinado con saltos pliométricos sobre los tejidos
blandos de la composición corporal (masa grasa y masa magra) de niños y
adolescentes con SD.
Artículo VIII. Determinar si niños y adolescentes con SD pueden mejorar su
condición cardio-respiratoria, adquiriendo niveles cercanos a los de jóvenes sin
discapacidad, mediante un entrenamiento de 21 semanas de acondicionamiento
físico combinado con saltos pliométricos.
Artículo IX. Comprobar si niños y adolescentes con SD pueden incrementar su
masa ósea siguiendo un entrenamiento de acondicionamiento físico combinado
con saltos pliométricos, durante 21 semanas.
-50-
3.Objectives
The general aim of the present Doctoral Thesis is to enlarge the scientific knowledge in
terms of health-related physical fitness and body composition, in youths with Down
syndrome; and on the other hand, to observe the effect of 21 weeks of an individualized
conditioning training program combined with plyometric jumps over these variables. In
detail, the specific objectives of each of the 9 manuscripts which constitute this Doctoral
Thesis are:
Manuscript I. To review the scientific literature, previous to this Doctoral Thesis, in
relation with physical fitness, body composition and also the effects that physical
training has in children and adolescents with Down syndrome.
Manuscript II. To describe levels of total and regional (lumbar spine, hip and
femoral neck) bone mass of children and adolescents with Down syndrome
comparing with their counterparts without disabilities.
Manuscript III. To compare total and regional fat and lean masses distribution
between children and adolescent with and without Down syndrome; to investigate
whether waist circumference is a good indicator of adiposity and to evaluate the
presence of sexual dimorphism in children and adolescents with Down syndrome.
Manuscript IV. To obtain anthropometric data of adolescents with Down syndrome,
and to evaluate if their fat mass-sexual dimorphism is similar than the described for
adolescents without Down syndrome.
-51-
Manuscript V. To describe lean mass and isometric and dynamic strength in
adolescents with and without Down syndrome, and to study the possible relationship
between lean mass and strength in this population.
Manuscript VI. To find out which of the published prediction equations with
anthropometry is the most accurate to asses percentage of body fat in children and
adolescents with Down syndrome, comparing those with air displacement
plethysmography.
Manuscript VII. To establish what is the effect of 21 weeks of conditioning training
combined with plyometric jumps in the soft tissues of body composition (fat and lean
masses) in children and adolescents with Down syndrome.
Manuscript VIII. To determine whether children and adolescents with Down
syndrome are able to improve their cardiovascular fitness, reaching levels close to the
youths without disabilities, towards a 21-weeks conditioning combined with
plyometric jumps training.
Manuscript IX. To check if children and adolescents with Down syndrome can
increase their bone mass following a conditioning combined with plyometric jumps
training, during 21 weeks.
-52-
4.Materialymétodos[Materialandmethods]
A continuación se describe la metodología general del proyecto, si bien dentro de cada
artículo publicado aparece una descripción detallada acerca de la metodología concreta
utilizada en él.
4.1Comitédeética
El estudio se llevó a cabo siguiendo las Normas Deontológicas reconocidas por la
Declaración de Helsinki de 1975 (revisado en la 52ª Asamblea General en Edimburgo,
Escocia, Octubre 2000), las Normas de Buena Práctica Clínica y cumpliendo la
legislación y la normativa legal española que regula la investigación clínica en humanos
(Real Decreto 561/1993, sobre ensayos clínicos). El proyecto fue aprobado por el Comité
de Ética de Investigación Clínica de Aragón (CEICA). Además, previo a la participación
en el proyecto se organizaron reuniones donde se explicaron los objetivos y
procedimientos a llevar a cabo en el mismo. Finalmente, todos los padres tuvieron que
firmar un consentimiento informado para que sus hijos pudieran participar en el estudio.
4.2Muestraydiseñodelestudio
La muestra total del estudió fue de 67 niños y adolescentes (30 chicas y 37 chicos), 32
con SD y 35 sin SD. Los criterios de inclusión dentro del grupo con SD fueron los
siguientes: (a) tener una edad comprendida entre 10 y 18 años, (b) estar diagnosticado de
SD y (c) no tener contraindicaciones para la práctica de ejercicio físico. Los criterios de
inclusión para el grupo sin SD fueron: (a) tener una edad comprendida entre 10 y 18 años,
(b) no tener ninguna enfermedad conocida, y (c) no estar tomando medicación en el
momento de comenzar el proyecto ni durante los 3 meses previos.
-53-
El artículo I, al tratarse de una revisión tiene una metodología propia y diferente a los
estudios experimentales, explicada en detalle en dicho artículo. Los artículos II al IX
cuentan con la muestra descrita, si bien existen variaciones en el número de participantes
debidas a valores perdidos en alguna de las variables de análisis y/o debido a los criterios
de inclusión establecidos para cada estudio (p.ej. rango de edad, únicamente participantes
con SD, etc.)
La Figura 2 muestra, de manera esquemática, el diseño experimental del proyecto.
Durante las 3 evaluaciones de las que constó, se llevaron a cabo pruebas de análisis de la
composición corporal y de la condición física. Al tratarse de un proyecto mucho más
amplio que lo meramente reflejado en esta Tesis Doctoral, parte de la metodología aquí
explicada no forma parte de ninguno de los artículos que la componen. Sin embargo, se
explicarán brevemente todas las pruebas realizadas, haciendo especial mención en las que
forman parte de los artículos publicados.
Figura 2. Línea de trabajo general del proyecto.
-54-
4.3Pruebasdecomposicióncorporal
Todas las pruebas de composición corporal se realizaron en la misma tarde entre las 16 y
las 19 horas por el mismo personal cualificado:
1. Absorciometría dual de rayos-X (DXA): Se utilizó un DXA QDR-Explorer
(Hologic Corp. Software versión pediátrica 12.4, Bedford, MA, USA). El
equipamiento fue calibrado con un fantoma de espina lumbar y con un fantoma de
densidades siguiendo las recomendaciones del fabricante. Los sujetos se
colocaban en decúbito supino, y los escáneres se realizaban en alta resolución.
Con esta prueba se obtuvieron valores de masa grasa (g), masa magra (kg) y masa
ósea [contenido (CMO; gr) y densidad mineral ósea (DMO; gr/cm2)], tanto de
cuerpo completo como en análisis regionales. En concreto, se obtuvieron valores
de tejidos blandos de extremidades superiores e inferiores y de la región del
tronco; y valores de masa ósea de extremidades, cadera (con las subregiones
siguientes: trocanter, región intertrocantérica y cuello femoral) y zona lumbar
(calculada como la media de las vertebras lumbares L1 a L4).
2. Antropometría: se realizaron mediciones antropométricas a todos los participantes
siguiendo el protocolo de ISAK.(57) Todos los sujetos fueron pesados en ropa
interior en una báscula con una precisión 0.1 kg (SECA 861, SECA, Hamburg,
Germany) y tallados en un tallímetro con una precisión 0.1 cm (SECA 225,
SECA, Hamburg, Germany). Las medidas de pliegues, perímetros y diámetros se
tomaron por triplicado, en el lado derecho, con un calibre de pliegues (Holtain
Ltd. Crymmych, UK), cinta antropométrica y paquímetro (ambos Rosscraft
S.R.L., Canadá). Se tomo como válida la mediana de las tres medidas. Todas las
medidas fueron efectuadas por un antropometrista nivel 2 de ISAK.
-55-
3. Pletismografía por desplazamiento de aire: Conocido comercialmente como
BOD-POD® (Body Composition System, Life Measurement Instruments,
Concord, USA), se realizó dicha prueba a todos los sujetos en ropa interior.
Obteniéndose valores de densidad corporal total, la cual aplicada a las diferentes
fórmulas de predicción permite obtener valores del porcentaje graso corporal de
los participantes.
4. Impedancia bioeléctrica: Se utilizó para ello un equipo de impedancia cuatripolar
(Tanita BC-418MA, Tanita Corp. Tokyo Japan). Con esta prueba se estimaron los
valores de grasa corporal y masa libre de grasa.
5. Ultrasonografía cuantitativa: Se realizó esta prueba con un equipo de ultrasonido
Aquilles InSight (GE Healthcare, Waukesha, Wisconsin, USA). Se obtuvieron
valores de fortaleza y densidad ósea, realizando el examen a nivel del calcáneo.
4.4Pruebasdecondiciónfísica
Previo a la realización de cada prueba de esfuerzo, se realizó una exploración física a
cada participante, se completó una historia medico-deportiva, y se les practicó un examen
ecocardiográfico (solo a los participantes con SD) para incrementar de esta manera la
seguridad de la prueba.
También se evaluó la maduración sexual de todos los participantes, por observación
directa de un médico experimentado, siguiendo los 5 estadios propuestos por Tanner y
Whitehouse.(59)
Todas las pruebas de condición física fueron realizadas por cada participante en la misma
tarde por el mismo personal cualificado y dentro de la misma semana que se habían
practicado las pruebas de composición corporal:
-56-
1. Prueba de esfuerzo en tapiz rodante: los participantes se familiarizaron con el
laboratorio y probaron los aparatos antes de empezar a recoger ningún dato. La
toma de datos comenzaba cuando los niños eran capaces de andar cómodamente
en el tapiz rodante (Quasar Med 4.0, h/p/cosmos, Nussdorf-Traunstein, Germany)
con la máscara ajustada. Modificando ligeramente el protocolo propuesto por
Fernhall y col. para adultos en 1987(58) (Tabla 3), los participantes comenzaban a
caminar en la cinta a 3.2 km/h (2.8 km/h los sujetos más jóvenes) y cada dos
minutos la velocidad se incrementaba 0.8 km/h hasta que los participantes no eran
capaces de andar sin correr (4.8 ó 5.6 km/h). Una vez llegaban a ese punto, se
incrementaba la pendiente del tapiz cada minuto un 4% hasta que el participante
no podía continuar (máximo 24%). El protocolo de Fernhall ha demostrado
validez y fiabilidad;(40) la adaptación propuesta se debe a que comúnmente, los
niños necesitan menos tiempo para alcanzar un estadio estable en cada fase de la
prueba y además así se conseguía reducir el tiempo total de la prueba, evitando
aburrimiento por parte de los participantes. El intercambio gaseoso fue medido
con un analizador de gases ‘breath-by-breath’ de circuito abierto (Oxycon Pro,
Jaeger/Viasys Healthcare, Hoechberg, Germany). Los valores máximos de
consumo de oxígeno, volumen ventilatorio y cociente respiratorio fueron
registrados como los valores medios más altos, obtenidos de cualquier periodo
continuo de 30 segundos. El espirómetro se calibró cada día con un volumen y gas
conocido, como recomienda el fabricante. Se utilizó un electrocardiograma para
registrar la frecuencia cardíaca, usando un sistema de 12 derivaciones durante toda
la prueba. Además de valores durante toda la prueba, también se obtuvieron
valores en reposo, y durante los 3 primeros minutos de la recuperación.
-57-
Tabla 3. Protocolo de tapiz rodante de Fernhall
Velocidad (km/h) Inclinación Tiempo (min)
0.0
0º
3
2.4
0º
2
3.2
0º
2
4.0
0º
2
4.8
0º
2
5.6
0º
2
5.6
4º
1
5.6
8º
1
5.6
12º
1
5.6
16º
1
5.6
20º
1
5.6
24º
1
0.0
0º
3
2. Test de salto: Los tests de Counter Movement Jump (salto con contramovimiento; CMJ) y Abalakov (salto con ayuda de brazos, ABA) se utilizaron
para valorar la fuerza dinámica de las extremidades inferiores. Cada niño efectuó
tres saltos de cada tipo y se tomó como válido el valor más alto de los tres.
3. Test isométricos: Para medir la fuerza isométrica máxima de los músculos
extensores de la extremidad inferior se uso una célula de carga (Servicio de
Apoyo a la Investigación, Universidad de Zaragoza) anclada en la pared. Los
niños realizaban extensión máxima de extremidad inferior desde una posición de
sentados con las rodillas a 90º y las manos sobre los muslos. Para valorar la fuerza
isométrica de los músculos flexores del antebrazo y de la mano, los niños
efectuaron una dinamometría manual con un dinamómetro (Takei-Grip 5401).
Cada niño efectuó tres intentos de cada prueba y se tomó como válido el valor
más alto de los tres.
4. Test de equilibrio y marcha: incluyen reconocimiento morfoestático y dinámico
de todos los participantes. Realizados con plataformas de presiones y cámaras de
grabación.
-58-
4.5Otrosdatos
Además de los elementos que aparecen en la Figura 2, se obtuvieron otros datos de
interés, que aunque la mayoría no hayan sido incluidos en los artículos que componen
esta Tesis Doctoral, serán explicados sucintamente a continuación.
Se entregaron cuestionarios de baterías psico-sociales, a los padres de todos los
participantes, para futuros análisis psico-sociológicos.
Se recogió también muestra de mucosa bucal para análisis genético posterior a todos los
participantes.
Durante el periodo de entrenamiento, los participantes, con y sin SD, llevaron colocados,
durante una semana, acelerómetros uniaxiales (Actigraph GT1M, Manufacturing
Technology Inc. Pensacola, FL, USA) para medir, de manera objetiva, sus niveles de
actividad física.
Se completaron 2 recuentos de alimentos de 24 horas no consecutivos, usando el software
HELENA - DIAT(60) (HELENA – dietary assessment tool), para obtener valores de ingesta
de nutrientes de todos los participantes.
4.6Programadeentrenamiento
Después de una evaluación inicial (segunda evaluación en la Figura 2) una submuestra
aleatoria con SD (n=13; 7 chicas y 6 chicos) llevó a cabo el programa de ejercicio físico
durante 21 semanas y con una frecuencia de dos sesiones por semana, permaneciendo otra
submuestra con SD (n=19; 8 chicas y 11 chicos) y el grupo sin DI como grupo control.
Cada entrenamiento se llevó a cabo con un máximo de 10 niños. Un investigador, y de 1 a
3 ayudantes supervisaron cada entrenamiento para que el ratio monitor:niño fuera 1:3
como mínimo. Cada sesión consistió en un trabajo de acondicionamiento físico
-59-
combinado con saltos pliométricos. La primera semana se usó para familiarización con el
material y los ejercicios. Cada entrenamiento constaba de 5 minutos de actividades de
calentamiento, 10-15 minutos de sesión y 5 minutos de vuelta a la calma. El
entrenamiento consistía en 1 ó 2 rotaciones en un circuito de 4 estaciones. Los ejercicios
realizados en cada estación fueron:
1. Saltos: salto vertical en el sitio, saltos con carrera, saltos en caída (altura del
salto entre 40 y 50 cm), salto en caída + salto adelante (altura del salto entre 40
y 50 cm). Desde la tercera semana, los niños cargaban con balones
medicinales mientras hacían los saltos.
2. Flexiones en la pared: los participantes colocaban las manos en un muro y
hacían flexiones con los pies separados de la pared entre 30 y 50 cm.
3. Bandas elásticas de fitness: deltoides lateral, ejercicio de bíceps, deltoides y
pectoral frontal.
4. Balones medicinales adaptados: lanzamientos y recepciones en el sitio, con
una distancia entre participantes entre 3 y 4 metros.
Los participantes fueron divididos en 4 grupos de trabajo (según cuartiles dependiendo de
su peso corporal) y trabajaron grupalmente. Cuando un participante mostraba excesiva
facilidad para hacer los ejercicios se le transfería al siguiente grupo de intensidad. Hubo 4
colores diferentes de bandas elásticas de resistencia gradual y 4 balones medicinales (1, 2,
3 y 4kg), cada uno era asignado a un grupo de trabajo dependiendo de la fuerza
demandada para hacer los ejercicios.
Cada grupo siguió el mismo esquema de ejercicios pero con las diferentes bandas y
balones:
-60-
Semana 1:
Familiarización, práctica con todos los materiales y ejercicios.
Semanas 2 a 6:
1 serie de 10 repeticiones.
Semanas 7 a 11:
2 series de 10 repeticiones.
Semanas 12 a 16:
Semanas 17 a 21:
Al tratarse de ejercicios no excesivamente intensos, la recuperación entre estación y
estación se hacía durante el paso de una a otra. La asistencia mínima obligatoria para
incluir a un participante en el grupo de ejercicio fue del 70% de todas las sesiones. Los
datos de los participantes que al final del periodo de entrenamiento no alcanzaron la
asistencia mínima, fueron excluidos de los análisis posteriores.
4.7Análisisestadísticos
Brevemente se describen a continuación las pruebas estadísticas generales que se
efectuaron para obtener los resultados de esta Tesis Doctoral, si bien en cada artículo
publicado aparece una descripción detallada acerca de todas las pruebas utilizadas.
El análisis estadístico se realizó con el paquete informático Statistical Package for the
Social Sciences (SPSS versiones 14.0 y 15.0 para Windows). Los datos se presentan, en
general como media ± desviación estándar, a menos que se indiquen otros estadísticos. Se
estudió la normalidad en la distribución de las variables continuas mediante el test de
Kolmogorov-Smirnov. A priori, si la distribución de una variable era normal, las
diferencias entre grupos se establecían mediante el test de análisis de las varianzas
(ANOVA) o con el test para muestras independientes (test t de Student). En el caso de
algunas pruebas estadísticas, se utilizaron covariables para ajustar variables que pueden
estar influenciadas por otras, en esos casos se efectuó el test de análisis de las
covarianzas (ANCOVA) junto con el test de Bonferroni. Las variables nominales (estadio
-61-
de maduración sexual de Tanner) se analizaron con el test de Chi-cuadrado. Las
asociaciones entre variables se estudiaron mediante correlaciones bivariadas de Pearson
y regresiónes lineales. Para observar el posible efecto del ejercicio, se estudiaron las
interacciones tiempo x ejercicio con el test de medidas repetidas de ANOVA usando como
factor el momento de evaluación (pre- y post-entrenamiento). El nivel de significación
estadístico fue tomado, como norma general como p<0.05.
-62-
5.Referencias[References]
1. Down JLH. Observations on an ethnic classification of idiots. London Hospital.
Clinical Lectures and Reports 1866;3:259-262.
2. Roizen NJ, Patterson D. Down's syndrome. Lancet 2003;361(9365):1281-9.
3. Pueschel SM. Clinical aspects of Down syndrome from infancy to adulthood. Am J
Med Genet Suppl 1990;7:52-6.
4. Smith DS. Health care management of adults with Down syndrome. Am Fam Physician
2001;64(6):1031-8.
5. Pueschel SM, Werner JC. Mitral valve prolapse in persons with Down syndrome. Res
Dev Disabil 1994;15(2):91-7.
6. Hasle H, Clemmensen IH, Mikkelsen M. Risks of leukaemia and solid tumours in
individuals with Down's syndrome. Lancet 2000;355(9199):165-9.
7. Bittles AH, Glasson EJ. Clinical, social, and ethical implications of changing life
expectancy in Down syndrome. Dev Med Child Neurol 2004;46(4):282-6.
8. Glasson EJ, Sullivan SG, Hussain R, Petterson BA, Montgomery PD, Bittles AH. The
changing survival profile of people with Down's syndrome: implications for
genetic counselling. Clin Genet 2002;62(5):390-3.
9. Pitetti KH, Rimmer JH, Fernhall B. Physical fitness and adults with mental retardation.
An overview of current research and future directions. Sports Med 1993;16(1):2356.
-63-
10. Winnick J. Adapted Physical Education and Sport. Champaign, Illinois: Human
Kinetics, 1995.
11. Pueschel SM. Should children with Down syndrome be screened for atlantoaxial
instability? Arch Pediatr Adolesc Med 1998;152(2):123-5.
12. Fernhall B, Pitetti KH, Rimmer JH, McCubbin JA, Rintala P, Millar AL, Kittredge J,
Burkett LN. Cardiorespiratory capacity of individuals with mental retardation
including Down syndrome. Med Sci Sports Exerc 1996;28(3):366-71.
13. Fernhall BM, JA. Pitteti, KH. Rintala, P. Prediction of maximal heart rate in
individuals with mental retardation. Med Sci Sports Exerc 2001;33(10):1655-60.
14. Guerra M, Llorens N, Fernhall B. Chronotropic incompetence in persons with down
syndrome. Arch Phys Med Rehabil 2003;84(11):1604-8.
15. Sharav T, Bowman T. Dietary practices, physical activity, and body-mass index in a
selected population of Down syndrome children and their siblings. Clin Pediatr
(Phila) 1992;31(6):341-4.
16. Frey GC, Stanish HI, Temple VA. Physical Activity of Youth With Intellectual
Disability: Review and Research Agenda Adapt Phys Activ Q 2008;25(2):95-117.
17. Vicente-Rodriguez G, Ara I, Perez-Gomez J, Dorado C, Calbet JA. Muscular
development and physical activity as major determinants of femoral bone mass
acquisition during growth. Br J Sports Med 2005;39(9):611-6.
18. Franzoni F, Ghiadoni L, Galetta F, Plantinga Y, Lubrano V, Huang Y, Salvetti G,
Regoli F, Taddei S, Santoro G, Salvetti A. Physical activity, plasma antioxidant
-64-
capacity, and endothelium-dependent vasodilation in young and older men. Am J
Hypertens 2005;18(4 Pt 1):510-6.
19. Vicente-Rodriguez G. How does exercise affect bone development during growth?
Sports Med 2006;36(7):561-9.
20. Ara I, Moreno LA, Leiva MT, Gutin B, Casajus JA. Adiposity, physical activity, and
physical fitness among children from Aragon, Spain. Obesity (Silver Spring)
2007;15(8):1918-24.
21. Ara I, Vicente-Rodriguez G, Jimenez-Ramirez J, Dorado C, Serrano-Sanchez JA,
Calbet JA. Regular participation in sports is associated with enhanced physical
fitness and lower fat mass in prepubertal boys. Int J Obes Relat Metab Disord
2004;28(12):1585-93.
22. Ara I, Vicente-Rodriguez G, Perez-Gomez J, Jimenez-Ramirez J, Serrano-Sanchez
JA, Dorado C, Calbet JA. Influence of extracurricular sport activities on body
composition and physical fitness in boys: a 3-year longitudinal study. Int J Obes
(Lond) 2006;30(7):1062-71.
23. San Juan AF, Fleck SJ, Chamorro-Vina C, Mate-Munoz JL, Moral S, Perez M,
Cardona C, Del Valle MF, Hernandez M, Ramirez M, Madero L, Lucia A. Effects
of an intrahospital exercise program intervention for children with leukemia. Med
Sci Sports Exerc 2007;39(1):13-21.
24. Andriolo RB, El Dib RP, Ramos LR. Aerobic exercise training programmes for
improving physical and psychosocial health in adults with Down syndrome.
Cochrane Database Syst Rev 2005(3):CD005176.
-65-
25. Heyward VH. Advanced fitness assessment & Exercise prescription. fifth ed.
Champaign, Illinois: Human Kinetics, 2006.
26. Angelopoulou N, Souftas V, Sakadamis A, Mandroukas K. Bone mineral density in
adults with Down's syndrome. Eur Radiol 1999;9(4):648-51.
27. Mercer VS, Lewis CL. Hip Abductor and Knee Extensor Muscle Strength of Children
with and without Down Syndrome. Pediatr Phys Ther 2001;13(1):18-26.
28. Baptista F, Varela A, Sardinha LB. Bone mineral mass in males and females with and
without Down syndrome. Osteoporos Int 2005;16(4):380-8.
29. Luke A, Sutton M, Schoeller DA, Roizen NJ. Nutrient intake and obesity in
prepubescent children with Down syndrome. J Am Diet Assoc 1996;96(12):12627.
30. Guijarro M, Valero C, Paule B, Gonzalez-Macias J, Riancho JA. Bone mass in young
adults with Down syndrome. J Intellect Disabil Res 2008;52(Pt 3):182-9.
31. Heymsfield SB, Smith R, Aulet M, Bensen B, Lichtman S, Wang J, Pierson RN, Jr.
Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry.
Am J Clin Nutr 1990;52(2):214-8.
32. Pitetti KH, Boneh S. Cardiovascular fitness as related to leg strength in adults with
mental retardation. Med Sci Sports Exerc 1995;27(3):423-8.
33. Fernhall B, Figueroa A, Collier S, Goulopoulou S, Giannopoulou I, Baynard T.
Resting metabolic rate is not reduced in obese adults with Down syndrome. Ment
Retard 2005;43(6):391-400.
-66-
34. Guerra-Balic M, Cuadrado-Mateos E, Geronimo-Blasco C, Fernhall B. Physical
Fitness Levels of Physically Active and Sedentary Adults With Down Syndrome.
Adapt Phys Activ Q 2000;17(3):310-321.
35. Kao CH, Chen CC, Wang SJ, Yeh SH. Bone mineral density in children with Down's
syndrome detected by dual photon absorptiometry. Nucl Med Commun
1992;13(10):773-5.
36. Angelopoulou N, Matziari C, Tsimaras V, Sakadamis A, Souftas V, Mandroukas K.
Bone mineral density and muscle strength in young men with mental retardation
(with and without Down syndrome). Calcif Tissue Int 2000;66(3):176-80.
37. Halaba Z, Pyrkosz A, Adamczyk P, Drozdzowska B, Pluskiewicz W. Longitudinal
changes in ultrasound measurements: a parallel study in subjects with genetic
disorders and healthy controls. Ultrasound Med Biol 2006;32(3):409-13.
38. Eberhard Y, Eterradossi J, Rapacchi B. Physical aptitudes to exertion in children with
Down's syndrome. J Ment Defic Res 1989;33 ( Pt 2):167-74.
39. Baynard T, Pitetti KH, Guerra M, Unnithan VB, Fernhall B. Age-Related Changes in
Aerobic Capacity in Individuals with Mental Retardation: A 20-yr Review. Med
Sci Sports Exerc 2008;40(11):1984-9.
40. Fernhall B, Millar AL, Tymeson GT, Burkett LN. Maximal exercise testing of
mentally retarded adolescents and adults: reliability study. Arch Phys Med Rehabil
1990;71(13):1065-8.
-67-
41. Fernhall B, Pitetti K, Vukovich MD, Stubbs N, Hensen T, Winnick J, Short F.
Validation of cardiovascular fitness field test in children with mental retardation.
American Journal on Mental Retardation 1998;102(6):602-612.
42. Fernhall B, Millar AL, Pitetti K, Hensen T, Vukovich MD. Cross validation of the 20m shuttle run test for children and adolescents with mental retardation. Adapt Phys
Activ Q 2000;17(4):402-412.
43. Guerra M, Pitetti K, Fernhall B. Cross validation of the 20-meter shuttle run test for
adolescents with Down syndrome. Adapt Phys Activ Q 2003;20(1):70-79.
44. Pitetti K, Fernhall B. Comparing run performance of adolescents with mental
retardation, with and without Down syndrome. Adapt Phys Activ Q
2004;21(3):219-228.
45. Pitetti KH, Climstein M, Mays MJ, Barrett PJ. Isokinetic arm and leg strength of
adults with Down syndrome: a comparative study. Arch Phys Med Rehabil
1992;73(9):847-50.
46. Climstein M, Pitetti KH, Barrett PJ, Campbell KD. The accuracy of predicting
treadmill VO2max for adults with mental retardation, with and without Down's
syndrome, using ACSM gender- and activity-specific regression equations. J
Intellect Disabil Res 1993;37 ( Pt 6):521-31.
47. Frontera WR, Hughes VA, Lutz KJ, Evans WJ. A cross-sectional study of muscle
strength and mass in 45- to 78-yr-old men and women. J Appl Physiol
1991;71(2):644-50.
-68-
48. Brooks SV, Faulkner JA. Skeletal muscle weakness in old age: underlying
mechanisms. Med Sci Sports Exerc 1994;26(4):432-9.
49. Horvat M, Pitetti KH, Croce R. Isokinetic torque, average power, and
flexion/extension ratios in nondisabled adults and adults with mental retardation. J
Orthop Sports Phys Ther 1997;25(6):395-9.
50. Croce RV, Pitetti KH, Horvat M, Miller J. Peak torque, average power, and
hamstrings/quadriceps ratios in nondisabled adults and adults with mental
retardation. Arch Phys Med Rehabil 1996;77(4):369-72.
51. Varela AM, Sardinha LB, Pitetti KH. Effects of an aerobic rowing training regimen in
young adults with Down syndrome. Am J Ment Retard 2001;106(2):135-44.
52. Millar AL, Fernhall B, Burkett LN. Effects of aerobic training in adolescents with
Down syndrome. Med Sci Sports Exerc 1993;25(2):270-4.
53. Ordonez F, Rosety M, Rosety-Rodriguez M. Influence of 12-week exercise training
on fat mass percentage in adolescents with Down syndrome. Med Sci Monit
2006;12(10):CR416-9.
54. Tsimaras V, Giagazoglou P, Fotiadou E, Christoulas K, Angelopoulou N. Jog-walk
training in cardiorespiratory fitness of adults with Down syndrome. Percept Mot
Skills 2003;96(3 Pt 2):1239-51.
55. Weber R, French R. Down's syndrome adolescents and strength training. Clinical
Kinesiology 1988;42(1):13-21.
-69-
56. Lewis CL, Fragala-Pinkham MA. Effects of aerobic conditioning and strength
training on a child with Down syndrome: a case study. Pediatr Phys Ther
2005;17(1):30-6.
57. Norton K, Whittingham N, Carter L, Kerr D, Gore C, Marfell-Jones M. Measurement
techniques in anthropometry. In: Norton K, Olds T, editors. Antropométrica.
Sydney: UNSW, 1996:22-75.
58. Fernhall B, Tymeson G. Graded exercise testing of mentally retarded adults: a study
of feasibility. Arch Phys Med Rehabil 1987;68(6):363-5.
59. Tanner JM, Whitehouse RH. Clinical longitudinal standards for height, weight, height
velocity, weight velocity, and stages of puberty. Arch Dis Child 1976;51(3):170-9.
60. Vereecken CA, Covents M, Sichert-Hellert W, Alvira JM, Le Donne C, De Henauw
S, De Vriendt T, Phillipp MK, Beghin L, Manios Y, Hallstrom L, Poortvliet E,
Matthys C, Plada M, Nagy E, Moreno LA. Development and evaluation of a selfadministered computerized 24-h dietary recall method for adolescents in Europe.
Int J Obes (Lond) 2008;32 Suppl 5:S26-34.
-70-
6.Resultadosydiscusión
Los resultados y la discusión de la presente Tesis Doctoral se muestran como artículos
científicos, siguiendo el formato en que han sido publicados o sometidos.
6.Resultsanddiscussion
Results and discussion of this Doctoral Thesis are shown as research manuscripts,
following the format in which were published or submitted.
-71-
-72-
Scand J Med Sci Sports 2010: 20: 716–724
doi: 10.1111/j.1600-0838.2010.01120.x
& 2010 John Wiley & Sons A/S
Review
Health-related physical fitness in children and adolescents with Down
syndrome and response to training
A. González-Agüero1,2, G. Vicente-Rodrı́guez1,2, L. A. Moreno1,3, M. Guerra-Balic5, I. Ara1,4, J. A. Casajús1,2
1
GENUD (Growth, Exercise, NUtrition and Development) Research Group, University of Zaragoza, Zaragoza, Spain, 2Faculty of
Health and Sport Sciences, Huesca, University of Zaragoza, Zaragoza, Spain, 3School of Health Science, University of Zaragoza,
Zaragoza, Spain, 4University of Castilla La Mancha, Toledo, Spain, 5Fundacio Blanquerna, University Ramon Lull, Barcelona, Spain
Corresponding author: Jose´ Antonio Casajús, GENUD Group; Ed. Cervantes. Corona de Aragón St. 42, 2nd floor, 50009
Zaragoza, Spain. E-mail: [email protected]
Accepted for publication 1 February 2010
Physical fitness is related to health at all ages. Information
about physical fitness in the Down syndrome (DS) population, however, is scarce, especially when we consider children and adolescents. A review of the current data available
on this topic would be both timely and important as it would
serve as a starting point to stimulate new research perspectives. The data we reviewed from the literature showed a
general trend toward lower values of physical fitness parameters and worse body composition variables in children and
adolescents with DS compared with the population without
intellectual disability (ID) or even with the population with
ID without DS. Notably, children and adolescents with DS
have been described as less active or overprotected; however,
these factors may not be the cause of their poor physical
fitness. Many of the training programs carried out in
children and adolescents with DS did not yield the desired
responses, and the reasons are still unknown. The purpose of
this review is to summarize the current available literature
on health-related physical fitness in children and adolescents
with DS, and the effect of training on these variables. From
the literature available, it is clear that more data on this
population are necessary.
Down syndrome (DS) is a condition that is accompanied with intellectual disability (ID) and associated
with abnormalities in chromosome 21. Although the
triplication of the chromosome is the most common
defect, translocation and nondisjunction are also
described (Pueschel, 1990). Estimation of DS is
about one out of 700 –1000 live births (Smith,
2001; Roizen & Patterson, 2003), and its life expectancy is increasing, from an average of 9 years of age
in 1929 (Bittles & Glasson, 2004) to 55 years and
older in the present day (Smith, 2001; Glasson et al.,
2002).
More than 80 clinical characteristics have been
described in individuals with DS, including congenital heart diseases, which is present in approximately
40% of individuals with DS (Pueschel, 1990).
Pueschel and Werner (1994) found the mitral valve
prolapse to be the cause of around 80% of abnormal
echocardiographies in their sample of 36 homereared young individuals with DS. However, the
most common congenital heart disease is the atrioventricular septal defect, with a prevalence of 45%,
followed by a ventricular septal defect in 35% and an
isolated atrial septal defect in 8% of the cases (Frid et
al., 1999; Freeman et al., 2008; Vis et al., 2009).
Leukemia is another serious disease that occurs with
a higher frequency in children with DS than in their
peers without DS, although individuals with DS have
a decreased risk of developing solid tumors in all age
groups (Hasle et al., 2000).
Evidence suggests that some of the clinical characteristics of DS (Pitetti et al., 1993) such as muscle
hypotonicity, hypermobility of the joints or ligamentous laxity, light to moderate obesity, an underdeveloped respiratory and cardiovascular system
and short stature (short legs and arms in relation to
torso) are related to exercise. In addition, poor
balance and perceptual difficulties have been also
described (Winnick, 1995). Moreover, characteristics
associated with hypotonia and hypermobility, for
example lordosis, ptosis, dislocated hips, kyphosis,
flat pronated feet, forwarded head and atlantoaxial
instability have been observed in this population
(Winnick, 1995; Pueschel, 1998). One of the most
important concerns regarding sport participation is
atlantoaxial instability, as participation in contact
sport activities are contraindicated in those cases
(Pueschel, 1998).
Owing to their clinical characteristics, both youths
and adults with DS have lower levels of cardiovascular fitness compared with matched controls without DS (Fernhall et al., 1996, 2001; Guerra et al.,
716
-73-
Physical fitness in youth with Down syndrome
2003a, b). Studies on DS children indicate a more
sedentary lifestyle and more time spent indoors
compared with their siblings without DS (Sharav &
Bowman, 1992); however, Frey et al. (2008) attributed this to paternal overprotection. Low levels of
physical fitness may induce functional deterioration
due to an increase in the prevalence of overweight or
obesity, as well as a reduction in bone mass development, which may ultimately result in the aggravation of their clinical manifestations (Fig. 1).
Physical activity (PA) and sport participation
produce many health-related benefits in children
and adolescents: PA improves cardiovascular fitness
(Vicente-Rodriguez et al., 2005), it contributes to a
healthier lifestyle (Stewart et al., 2003), and it may
enhance the antioxidant defense system (Franzoni et
al., 2005) which delays cell aging. In children, regular
PA and sport, as well as physical fitness levels, are
associated with increased and higher accumulation of
bone mass (Vicente-Rodriguez, 2006), fat mass reduction (Ara et al., 2004, 2007) and a physiological
and healthy adiposity development (Ara et al., 2006).
PA interventions have also been shown to benefit
children with leukemia (San Juan et al., 2007).
Interestingly, the payback is not purely a physical
one, as benefits in social factors associated with sport
participation are also described (Andriolo et al.,
2005). Therefore, taking into account all these separate studies, it is suggested that PA could be a
potential factor in helping children with DS improve
their quality of life.
According to the American College of Sports
Medicine (ACSM), health-related physical fitness
includes body composition, aerobic capacity, muscular strength and flexibility (Heyward, 2006),
although flexibility is not a priority for the DS
population due to fact that augmented flexibility is
predominant in this group (Pitetti et al., 1993).
In order to stimulate more research in this field,
this paper aims to review the current literature on
physical fitness, body composition and also the
effects that training has on children and adolescents
with DS.
Method
Inclusion criteria
The inclusion criteria for this review were as follows: (a)
physical fitness or body composition had to be the main topic
of each study but not necessarily PA; (b) the studies had to
include participants with DS and not only with ID; (c)
participants aged between 10 and 18 had to be at least 10%
of the population studied; (d) only papers written entirely in
English were considered.
Data sources
Journal articles were sourced from MEDLINE (1965–present)
and SPORT Discus (1975–present). The keywords used to
identify the articles were ‘‘Down syndrome,’’ to restrict the
population on this review; these terms were combined with
‘‘exercise,’’ ‘‘body composition,’’ ‘‘physical fitness’’ and
‘‘training’’ to identify the articles on the topic of this review.
This produced a total of 101 citations from both databases.
Exclusion
The inclusion criteria were applied to the 101 citations by two
authors independently; in case of a disagreement, all authors
reviewed until a consensus was achieved. Of the 101 citations,
22 journal articles fulfilled the inclusion criteria. The remaining 81 citations were excluded for the following reasons: 11
were duplicated, 57 did not include physical fitness or body
composition as their main topic, five were not journal articles
and six had participants outside our established population
range.
Data extraction
All the studies were evaluated independently by the authors of
this review. General information about the title of the study,
author(s), journal and publication details were extracted.
Characteristics of the participants (age, sex), control group
(if available), data source and results were also extracted.
Studies including a training program were explained in detail.
Health-related physical fitness in children and
adolescents with DS
All the studies concerning health-related physical
fitness in children and adolescents with DS included
in this review are summarized in Table 1.
Body composition
Fig. 1. Relationship between Down syndrome physical fitness and clinical manifestation.
Body mass index (BMI) and different body compartments, such as body fat, lean mass and bone mass
[bone mineral content (BMC) and bone mineral
density (BMD)] have been studied in children
and adolescents with DS. Children with DS were
717
-74-
Participants (age)
19; 7 F, 12 M (14.8 3)
133 (9–45)
7 (9.6 1.8)
67; 33 F, 34 M (14–40)
13; 6 F, 7 M (18.5 2.3)
119; 57 F, 62 M (14.8 2.6)
89 (14.5); 47 obese
26, 11 F, 15 M (15.3 2.7)
97 (9–46)
Authors
Guerra et al. (2009)
Baynard et al. (2008)
Halaba et al. (2006)
Baptista et al. (2005)
Baynard et al. (2004)
Pitetti and Fernhall (2004)
Fernhall et al. (2003)
Guerra et al. (2003a, b)
179 subjects with MR without DS
196 subjects without MR
No
84 MR without DS; 22 obese
395 subjects with MR without DS;
17 subjects with MR without DS
180 subjects with MR without DS;
No
Control group
Table 1. Studies concerning health-related physical fitness including children and adolescents with Down syndrome
Multicenter study with the treadmill
test
20 m shuttle run test and treadmill
test
Treadmill test
20 m shuttle run test
Individualized treadmill test to
exhaustion
DXA
Ultrasound at hand phalanges
Data collection of the last 20 years
using the validated treadmill test
Wingate anaerobic test
Data source
Reliability between tests was questionable
DS adolescents showed low levels of
WAnT performance compared with
published data
.
Lower relative and absolute ðVO2peak Þ
across
all age groups
.
ðVO2peak Þ did not change after 16 years
Lower amplitude-dependent speed of
sound over ages and remained stable with
time
Female group had lower muscle mass,
higher percentage of body fat and BMI
Lower BMC, BMD and volumetric BMD in
the upper and lower limbs and the lumbar
spine in the whole group with DS
Determination of VT is difficult in this
population
.
.
Lower ðVO2peak Þ, ðVEpeak Þ, HRpeak and
RERpeak
Subjects with DS showed lower running
performance than subjects without DS,
with or without MR
Lower maximal HR in the DS group, no
differences between obese and nonobese
Controlled for maximal HR, no changes in
aerobic capacity between obese and
nonobese DS
Regression formula for children and
adolescents with MR is not valid in their
sample of adolescents with DS
Prediction
. formula. for HRmax
Lower ðVO2peak Þ, ðVEpeak Þ, HRpeak and
RERpeak
Results*
González-Agüero et al.
718
-75-
-76-
17; 11 F, 6 M (11.2 2.4)
17; 8 F, 9 M, all with MR (13.7)
34; eight with DS (14.3 2.3)
10; 6 F, 4 M (8.8 2.5)
30; 16 F, 14 M (F5.1 2.8,
M4.1 2.5)
10; 3 F, 7 M (10–16)
14; 3 F, 11 M (17.7)
10; 3 F, 7 M (14.8 2.2)
Mercer and Lewis (2001)
Luke et al. (1996)
Sharav and Bowman (1992)
Eberhard et al. (1989)
Eight subjects without MR
No
Reference without MR
Siblings without DS
No
No
Control group
Bicycle ergometry test
Treadmill tests
Anthropometric measurements,
bioelectrical impedance and
deuterium dilution
accelerometers and questionnaires
DPX
Treadmill test and the 20 m shuttle
run test
Treadmill test and field tests (600yard run-walk, 20 m shuttle run and
16 m shuttle run)
Anthropometric measurements
Hand-held dynamometer to
evaluate muscle forces
Data source
No differences in BMI
Less active, more time indoors
Lower BMD at the lumbar spine
Delay in the distribution curve of BMD
against ages
Treadmill test validation
High reliability between the two tests
(r 5 0.94)
Lower VO2max
Shorter performance time and lower
maximal workload
Blood pressure did not increase regularly
Higher BMI and percentage of body fat
Lower mean peak torque values for hip
abduction and knee extension
Reliability high between test (0.89–0.95)
Weight, height, gender, BMI and activity
levels were significant predictors for peak
torque production in DS
Validation
of the formula to predict
.
ðVO2peak Þ with the 20. m shuttle run test
Formula to predict ðVO2peak Þ
Validation against 600-yard run-walk, 20 m
shuttle run and a modified 16 m shuttle run
tests
No differences in fat-free mass
Results*
F, female; M, male; DS, Down syndrome; MR, mental retardation; SD, standard deviation; DXA, dual energy x-ray absorptiometry; DPX, dual photon x-ray absorptiometry; BMI, body mass index; BMC, bone mineral
content; BMD, bone mineral density; VO2, oxygen consumption; VE, ventilation; HR, heart rate; RER, respiratory exchange ratio.
*In the results, all the comparisons are as follows: the group with DS compared with the group without DS (with or without MR) when existing.
Kao et al. (1992)
Participants (age)
Authors
Table 1. (continued)
719
described as less active and more prone to spending
more time indoors, but no differences were found in
the BMI values between children with DS and their
siblings without ID (Sharav & Bowman, 1992).
However, several other investigations, some of
them including adults in the sample, have shown a
tendency toward a higher BMI and percentage of
body fat in groups with DS compared with those
without ID (Mercer & Lewis, 2001; Baptista et al.,
2005). It is notable that Luke et al. (1996) found no
difference in the fat-free mass (measured with deuterium dilution and other methods) between children
with and without DS. On the other hand, Baptista et
al. (2005), estimating the total muscle mass as suggested by Heymsfield et al. (1990) using data from
Dual energy x-ray absorptiometry, found lower values in both males and females with DS compared
with males and females without ID.
Common to both children and adolescents with
DS is a lower BMC and BMD at the lumbar spine
(Kao et al., 1992; Baptista et al., 2005) and the upper
and lower limbs (Baptista et al., 2005). Furthermore,
lower volumetric BMD has been found in other areas
such as the upper and lower limbs (Baptista et al.,
2005).
Similarly, a study with ultrasonography found
lower amplitude-dependent speed of sound, which
depends on BMD, in 24 children with genetic disorders (including seven children with DS) compared
with age-matched children without ID; however, the
difference remained stable with time (Halaba et al.,
2006), indicating low bone mass but normal development.
In conclusion, although there have been several
important reports on body composition in children
and adolescents with DS, more studies are required
to describe not only the body composition of children and adolescents with DS, but also the effect of
exercise on the lean, fat and bone compartments in
this population.
treadmill test method for adolescents and adults with
ID (including DS). The findings of the study showed
a high reliability coefficient of 0.94 between two
repeated tests. In further studies, Fernhall et al.
(1998) developed a regression
. equation to predict a
peak oxygen consumption ðVO2peak Þ in children and
adolescents with ID (including DS) with field tests
(600-yard run-walk, 20 m shuttle run and a modified
16 m shuttle run), and in 2000, they validated the
equation again with the 20 m shuttle run test (Fernhall et al., 2000). However, Guerra et al. (2003a, b)
found
that the regression equation to predict
.
ðVO2peak Þ in children with ID was not valid for their
sample of adolescents with DS, and attributed this to
the low number of children with DS in the sample of
Fernhall. Also, Fernhall et al. (2001) developed an
equation to predict the maximum heart rate (HRmax)
in individuals with ID (including children and adolescents with DS). Baynard .et al. (2004) and Fernhall
et. al. (2001) found lower ðVO2peak Þ, peak ventilation
ðVEpeak Þ, HRpeak and peak respiratory exchange
ratio (RERpeak) in children and adolescents with
DS compared with peers without DS, with or without ID. In more recent studies, Baynard et al. (2008)
divided their sample of a multicenter study into age
groups,
and found lower relative and absolute
.
ðVO2peak Þ across all age groups in the individuals
with DS compared with both groups (the group with
ID without DS and the group
. without ID). Crucially,
for the DS group, their ðVO2peak Þ did not change
after 16 years of age. Pitetti and Fernhall (2004)
found lower running performance in their subjects
with DS compared with the ones without DS, with or
without ID.
Low cardiovascular fitness is considered to be a
risk factor for cardiovascular diseases, and can result
in a shortened lifespan for children and adolescents
with DS. However, due to the lack of studies that
include only the pediatric population in this regard,
more studies are required to corroborate this assumption.
Cardiovascular fitness
Lower levels of cardiovascular fitness have been
reported several times in children and adolescents
with DS compared with their peers without DS, with
or without ID (Eberhard et al., 1989; Fernhall et al.,
1996, 2001; Guerra et al., 2003a, b; Pitetti & Fernhall,
2004; Baynard et al., 2008).
Eberhard et al. (1989)
. found a lower maximal
oxygen consumption ðVO2 max Þ, a shorter time and
a lower maximal workload in children with DS
compared with the control, age-matched children.
In the last two decades, considerable progress has
been made in the assessment of cardiovascular fitness
in children and adolescents with ID but specifically
with DS. Fernhall et al. (1990) developed a validated
Strength
Correct levels of muscular strength are related to
health (Heyward, 2006) and help people to be more
autonomous and independent; however, especially in
old age, it is difficult to maintain those levels (Frontera et al., 1991; Brooks & Faulkner, 1994). As the
lifespan of the DS population is increasing, it is
important to study the actual level of strength in
this population and, if necessary, promote programs
to improve it.
Only one study related to muscular strength fulfilled all the inclusion criteria for this review. Mercer
and Lewis (2001) found a lower mean peak torque
for hip abduction and knee extension for children
720
-77-
-78-
16 M (21.4 3)
14; 3 F, 11 M
(17.7 2.9)
Varela et al. (2001)
Millar et al. (1993)
No
No
Four subjects with
DS, no exercise
Eight subjects with
DS, no exercise
No
Control
submaximal treadmill stress test,
modification of Margaria–Kalamen
test, 10 RM to upper and lower
limbs
Ten exercises to evaluate muscular
strength: Dorsi pull down, leg
press, upright row, leg extension,
shoulder press, calf raise, arm curl,
leg curl, chest press and dead lift
Walking treadmill test
treadmill or rowing ergometer
peak-graded exercise test
Anthropometric measurements
Data source
6-week combined aerobic and
strength training
Aerobic intensity 60–80% HRmax,
10–60 min per session; two to three
sessions per week
Strength intensity increased by the
number of repetitions and weight;
10–45 min per session, two to three
sessions per week
Two groups: group A performed a
6-week (three times per week)
weight training treatment at 80%
1 RM; group B performed a 6-week
(three times per week) strength
treatment 15 min per session
12-week physical activity program;
intensity level on the basis of HR;
30–60 min per session, three
sessions per week
16-week rowing ergometer;
.
intensities 55–70% ðVO2peak Þ; 15–
25 min per session; three sessions
per week
10-week walking jogging exercise
program; 65–75% HRmax; 30 min
per session; three sessions per
week
Training
BMI did not change
Decreased HR and RER in all the
stages of the treadmill test
Higher anaerobic power and
strength in the trunk, the upper and
lower limbs
Weight training had greater effects
in all muscular strength tests than
the strength treatment
No differences in cardiovascular or
physiological responses
Exercise group achieved higher
levels of work performance
No changes in cardiovascular
capacities
Exercise group improved the time
to exhaustion and grade
Significant reduction in the fat mass
percentage
Results*
F, female; M, male; DS, Down syndrome; MR, mental retardation; SD, standard deviation; BMI, body mass index; VO2, oxygen consumption; HR, heart rate; RER, respiratory exchange ratio; RM, maximum repetition.
*In the results, all the comparisons are as follows: the group with DS compared with the control group when existing.
Combined aerobic and strength training
Lewis and Fragala1 F (10.5)
Pinkham (2005)
14; 3 F, 11 M (13–18)
22 M (16.2 1)
Aerobic training
Ordoñez et al. (2006)
Strength training
Weber and French
(1988)
Participants
Study
Table 2. Studies concerning physical training including children and adolescents with Down syndrome
721
and adolescents with DS compared with their peers
without ID, where weight, height, gender, PA level
and BMI serve as significant predictors for peak
torque production in children and adolescents with
DS.
Effects of training in children and adolescents with DS
From the wealth of articles in the literature, it can be
concluded that children and adolescents with DS
have lower levels of strength and cardiovascular
fitness, coupled with higher levels of body fat when
compared with their peers without DS, both with and
without ID.
As the PA level is a significant predictor of
strength in the population with DS (Mercer & Lewis,
2001), testing whether supervised exercise interventions could improve muscular strength, cardiovascular fitness and body composition, which could also
result in a concomitant health enhancement, is an
important issue that needs to be addressed.
All the studies related to the effect of physical
training programs in children and adolescents
with DS included in this review are summarized in
Table 2.
are nonconclusive due to the contradictory outcomes
of each independent investigation. The studies have
not shown improvements in cardiovascular fitness in
the children and adolescents with DS, leading investigators to postulate that perhaps adaptations may
require longer training periods and/or higher training
intensities. New, specifically designed studies could
contribute toward the validation of the hypothesis
that cardiovascular capacity in children and adolescents with DS can be improved, as this has already
been shown in adults with DS (Tsimaras et al., 2003).
Strength training
Only one study was found which exercised youth
with DS with a training program focused exclusively
on strength. Weber and French (1988) studied a
group of 14 adolescents with DS and designed two
strength training programs: a weight training treatment and a strength exercise treatment. The participants performed 10 tests to evaluate their muscular
strength before and after the treatment program. The
results of this study were very clear and found that
the group that performed the weight training program achieved significant improvement in muscular
strength.
Cardiovascular training
Combined cardiovascular and strength training
To the best of our knowledge, three studies have
examined the effects of standardized aerobic training
in children and/or adolescents with DS.
Varela et al. (2001) conducted a 16-week rowing
ergometer training study, which was carried out on
16 adolescents and young adults with DS. Even
though the exercise group achieved higher levels of
work performance, no evidence of physical changes
was found either in the body weight or in the
percentage of body fat. Additionally, no changes in
cardiovascular or physiological responses were found
either in the treadmill test or in the rowing test.
Similarly, Millar et al. (1993) designed a 10-week
walking–jogging exercise program for 14 children
and adolescents with DS, and yet again no changes
were found in the cardiovascular capacities in any of
the two groups, possibly due to the low exercise
intensity; however, the exercise group showed an
improvement in the time to exhaustion.
Ordoñez et al. (2006) focused on the aerobic
training of 22 male adolescents with DS for 12 weeks,
concluding at the end of the training period that they
found a significant decrease in the percentage of fat
mass (assessed by anthropometry) but reported no
cardiovascular effects.
There have been several investigations only regarding the effects of training on body composition over a
relatively short duration and the results of the studies
In a case study by Lewis and Fragala-Pinkham
(2005), a child with DS performed a 6-week home
exercise program combining aerobic and strength
training. After the training period, the results showed
improvements in aerobic capacity and anaerobic
power.
These studies related to training programs may
pave the way toward to new research looking into
increased strength levels that could have positive
effects on health from several different approaches.
For example, strength training could produce both
neural and muscular-related strength increase and
muscular hypertrophy, which in turn could reduce
hypotonicity and balance dysfunctions and increase
VO2max and bone mass-related parameters. Because
there are a number of significant benefits to be
attained, efforts to elucidate the real effects of
strength or cardiovascular-strength combined training should be promoted.
Conclusions
Children and adolescents with DS are a unique
population in relation to their health-related physical
fitness variables. Body composition in this specific
population is, in general, less healthy than that
observed in their peers without DS, as proven by
722
-79-
higher BMI, lower levels of lean mass and reduced
bone mass-related parameters.
Furthermore, children and adolescents with DS
show lower levels of cardiovascular and strength
capacities, which can result in a worse quality of
life. Although there is a significant lack of information on youths with DS, it is evident that this
population could benefit considerably from PA and
exercise prescription. Data from the few studies
available till now are contradictory in relation to
improvements in body fat composition of the individuals. Adaptations have not been achieved in cardiovascular fitness when mild aerobic training is
performed. One possible explanation for the lack of
cardiovascular improvement may be a result of the
low intensity and/or duration characteristics of the
program described.
Further research in this topic would help to
address pending issues such as the duration and
intensity of aerobic training on improvement in
cardiovascular fitness, or whether type, intensity
and duration of strength training could be the most
beneficial to children and adolescents with DS.
Importantly, the life expectancy of the population
with DS is increasing with time; hence, cases of
diseases some illnesses and diseases related to age
(until now relatively unreported for the DS population) such as osteoporosis or cellular aging begin to
appear earlier than in the population without DS.
Consequently, the main characteristics associated
with DS can become more pronounced. The ultimate
objective of future research in this field should be to
test whether exercise (aerobic, strength and/or a
combination of both) could benefit children and
adolescents with DS, and help them have a healthier
body composition and physical fitness, all of which
result in a healthier and a better quality of life in this
population.
Key words: exercise, body composition, cardiovascular fitness, aerobic, strength, training.
Acknowledgements
Special thanks are due to Scott G. Mitchell from the University of Glasgow for his work of reviewing the English style
and grammar. This review was supported by Gobierno de
Aragon (Proyecto PM 17/2007) and Ministerio de Ciencia e
Innovación de España (Red de investigación en ejercicio fı́sico
y salud para poblaciones especiales-EXERNET-DEP200500046/ACTI). There are no potential conflicts of interest
that may affect the contents of this review.
References
Andriolo RB, El Dib RP, Ramos LR.
Aerobic exercise training programmes
for improving physical and
psychosocial health in adults with
Down syndrome. Cochrane Database
Syst Rev 2005; CD005176.
Ara I, Moreno LA, Leiva MT, Gutin B,
Casajus JA. Adiposity, physical
activity, and physical fitness among
children from Aragon, Spain. Obesity
(Silver Spring) 2007: 15: 1918–1924.
Ara I, Vicente-Rodriguez G, JimenezRamirez J, Dorado C, SerranoSanchez JA, Calbet JA. Regular
participation in sports is associated
with enhanced physical fitness and
lower fat mass in prepubertal boys. Int
J Obes Relat Metab Disord 2004: 28:
1585–1593.
Ara I, Vicente-Rodriguez G, PerezGomez J, Jimenez-Ramirez J, SerranoSanchez JA, Dorado C, Calbet JA.
Influence of extracurricular sport
activities on body composition and
physical fitness in boys: a 3-year
longitudinal study. Int J Obes
(London) 2006: 30: 1062–1071.
Baptista F, Varela A, Sardinha LB. Bone
mineral mass in males and females with
and without Down syndrome.
Osteoporos Int 2005: 16: 380–388.
Baynard T, Pitetti KH, Guerra M,
Fernhall B. Heart rate variability at
rest and during exercise in persons with
Down syndrome. Arch Phys Med
Rehabil 2004: 85: 1285–1290.
Baynard T, Pitetti KH, Guerra M,
Unnithan VB, Fernhall B. Age-related
changes in aerobic capacity in
individuals with mental retardation: a
20-yr review. Med Sci Sports Exerc
2008: 40: 1984–1989.
Bittles AH, Glasson EJ. Clinical, social,
and ethical implications of changing
life expectancy in Down syndrome.
Dev Med Child Neurol 2004: 46: 282–
286.
Brooks SV, Faulkner JA. Skeletal muscle
weakness in old age: underlying
mechanisms. Med Sci Sports Exerc
1994: 26: 432–439.
Eberhard Y, Eterradossi J, Rapacchi B.
Physical aptitudes to exertion in
children with Down’s syndrome. J
Ment Defic Res 1989: 33(Part 2): 167–
174.
Fernhall B, Millar AL, Pitetti K, Hensen
T, Vukovich MD. Cross validation of
the 20-m shuttle run test for children
and adolescents with mental
retardation. Adapted Phys Act Q 2000:
17: 402–412.
Fernhall B, Millar AL, Tymeson GT,
Burkett LN. Maximal exercise testing
of mentally retarded adolescents and
adults: reliability study. Arch Phys
Med Rehabil 1990: 71: 1065–1068.
Fernhall B, Pitetti K, Vukovich MD,
Stubbs N, Hensen T, Winnick J, Short
F. Validation of cardiovascular fitness
field test in children with mental
retardation. Am J Mental Retard 1998:
102: 602–612.
Fernhall B, Pitetti KH, Guerra M. Impact
of obesity and down syndrome on
maximal heart rate and work capacity
in youth with mental retardation.
Revista portuguesa de Ciencias do
Desporto 2003: 3: 73–118.
Fernhall B, Pitetti KH, Rimmer JH,
McCubbin JA, Rintala P, Millar AL,
Kittredge J, Burkett LN.
Cardiorespiratory capacity of
individuals with mental retardation
including Down syndrome. Med Sci
Sports Exerc 1996: 28: 366–371.
Fernhall B, McCubbin JA, Pitteti KH,
Rintala P. Prediction of maximal heart
rate in individuals with mental
retardation. Med Sci Sports Exerc
2001: 33: 1655–1660.
Franzoni F, Ghiadoni L, Galetta F,
Plantinga Y, Lubrano V, Huang Y,
723
-80-
Salvetti G, Regoli F, Taddei S, Santoro
G, Salvetti A. Physical activity, plasma
antioxidant capacity, and endotheliumdependent vasodilation in young and
older men. Am J Hypertens 2005: 18:
510–516.
Freeman SB, Bean LH, Allen EG, Tinker
SW, Locke AE, Druschel C, Hobbs
CA, Romitti PA, Royle MH, Torfs CP,
Dooley KJ, Sherman SL. Ethnicity,
sex, and the incidence of congenital
heart defects: a report from the
National Down Syndrome Project.
Genet Med 2008: 10: 173–180.
Frey GC, Stanish HI, Temple VA.
Physical activity of youth with
intellectual disability: review and
research agenda adapted physical
activity quarterly. Adapt Phys Activ Q
2008: 25: 95–117.
Frid C, Drott P, Lundell B, Rasmussen F,
Anneren G. Mortality in Down’s
syndrome in relation to congenital
malformations. J Intellect Disabil Res
1999: 43(Part 3): 234–241.
Frontera WR, Hughes VA, Lutz KJ,
Evans WJ. A cross-sectional study of
muscle strength and mass in 45- to 78yr-old men and women. J Appl Physiol
1991: 71: 644–650.
Glasson EJ, Sullivan SG, Hussain R,
Petterson BA, Montgomery PD, Bittles
AH. The changing survival profile of
people with Down’s syndrome:
implications for genetic counselling.
Clin Genet 2002: 62: 390–393.
Guerra M, Gine-Garriga M, Fernhall B.
Reliability of Wingate testing in
adolescents with Down syndrome.
Pediatr Exerc Sci 2009: 21:
47–54.
Guerra M, Llorens N, Fernhall B.
Chronotropic incompetence in
persons with down syndrome. Arch
Phys Med Rehabil 2003a: 84: 1604–
1608.
Guerra M, Pitetti K, Fernhall B. Cross
validation of the 20-meter shuttle run
test for adolescents with Down
syndrome. Adapted Phys Activity
Quart 2003b: 20: 70–79.
Halaba Z, Pyrkosz A, Adamczyk P,
Drozdzowska B, Pluskiewicz W.
Longitudinal changes in ultrasound
measurements: a parallel study in
subjects with genetic disorders and
healthy controls. Ultrasound Med Biol
2006: 32: 409–413.
Hasle H, Clemmensen IH, Mikkelsen M.
Risks of leukaemia and solid tumours
in individuals with Down’s syndrome.
Lancet 2000: 355: 165–169.
Heymsfield SB, Smith R, Aulet M,
Bensen B, Lichtman S, Wang J, Pierson
RN Jr. Appendicular skeletal muscle
mass: measurement by dual-photon
absorptiometry. Am J Clin Nutr 1990:
52: 214–218.
Heyward VH. Advanced Fitness
Assessment & Exercise Prescription,
5th ed. Champaign, Illinois: Human
Kinetics, 2006, p. 278.
Kao CH, Chen CC, Wang SJ, Yeh SH.
Bone mineral density in children with
Down’s syndrome detected by dual
photon absorptiometry. Nucl Med
Commun 1992: 13: 773–775.
Lewis CL, Fragala-Pinkham MA. Effects
of aerobic conditioning and strength
training on a child with Down
syndrome: a case study. Pediatr Phys
Ther 2005: 17: 30–36.
Luke A, Sutton M, Schoeller DA, Roizen
NJ. Nutrient intake and obesity in
prepubescent children with Down
syndrome. J Am Diet Assoc 1996: 96:
1262–1267.
Mercer VS, Lewis CL. Hip abductor and
knee extensor muscle strength of
children with and without Down
syndrome. Pediatr Phys Ther 2001: 13:
18–26.
Millar AL, Fernhall B, Burkett LN.
Effects of aerobic training in
adolescents with Down syndrome. Med
Sci Sports Exerc 1993: 25: 270–274.
Ordoñez F, Rosety M, Rosety-Rodriguez
M. Influence of 12-week exercise
training on fat mass percentage in
adolescents with Down syndrome. Med
Sci Monit 2006: 12: CR416–CR419.
Pitetti K, Fernhall B. Comparing run
performance of adolescents with
mental retardation, with and without
Down syndrome. Adapted Phys Act
Quart 2004: 21: 219–228.
Pitetti KH, Rimmer JH, Fernhall B.
Physical fitness and adults with mental
retardation. An overview of current
research and future directions. Sports
Med 1993: 16: 23–56.
Pueschel SM. Clinical aspects of Down
syndrome from infancy to adulthood.
Am J Med Genet 1990: 7(Suppl.): 52–56.
Pueschel SM. Should children with Down
syndrome be screened for atlantoaxial
instability? Arch Pediatr Adolesc Med
1998: 152: 123–125.
Pueschel SM, Werner JC. Mitral valve
prolapse in persons with Down
syndrome. Res Dev Disabil 1994: 15:
91–97.
Roizen NJ, Patterson D. Down’s syndrome.
Lancet 2003: 361: 1281–1289.
San Juan AF, Fleck SJ, Chamorro-Vina
C, Mate-Munoz JL, Moral S, Perez M,
Cardona C, Del Valle MF, Hernandez
M, Ramirez M, Madero L, Lucia A.
Effects of an intrahospital exercise
program intervention for children with
leukemia. Med Sci Sports Exerc 2007:
39: 13–21.
Sharav T, Bowman T. Dietary practices,
physical activity, and body-mass index
in a selected population of Down
syndrome children and their siblings.
Clin Pediatr (Philadelphia) 1992: 31:
341–344.
Smith DS. Health care management of
adults with Down syndrome. Am Fam
Physician 2001: 64: 1031–1038.
Stewart KJ, Turner KL, Bacher AC,
DeRegis JR, Sung J, Tayback M,
Ouyang P. Are fitness, activity, and
fatness associated with health-related
quality of life and mood in older
persons? J Cardiopulm Rehabil 2003:
23: 115–121.
Tsimaras V, Giagazoglou P, Fotiadou E,
Christoulas K, Angelopoulou N. Jogwalk training in cardiorespiratory
fitness of adults with Down syndrome.
Percept Mot Skills 2003: 96: 1239–
1251.
Varela AM, Sardinha LB, Pitetti KH.
Effects of an aerobic rowing training
regimen in young adults with Down
syndrome. Am J Ment Retard 2001:
106: 135–144.
Vicente-Rodriguez G. How does exercise
affect bone development during growth?
Sports Med 2006: 36: 561–569.
Vicente-Rodriguez G, Ara I, PerezGomez J, Dorado C, Calbet JA.
Muscular development and physical
activity as major determinants of
femoral bone mass acquisition during
growth. Br J Sports Med 2005: 39: 611–
616.
Vis JC, Duffels MG, Winter MM,
Weijerman ME, Cobben JM, Huisman
SA, Mulder BJ. Down syndrome: a
cardiovascular perspective. J Intellect
Disabil Res 2009: 53: 419–425.
Weber R, French R. Down’s syndrome
adolescents and strength training. Clin
Kinesiol 1988: 42: 13–21.
Winnick J. Adapted physical education
and sport. Champaign, Illinois: Human
Kinetics, 1995.
724
-81-
-82-
Osteoporos Int (2011) 22:2151–2157
DOI 10.1007/s00198-010-1443-7
ORIGINAL ARTICLE
Bone mass in male and female children and adolescents
with Down syndrome
A. González-Agüero & G. Vicente-Rodríguez &
L. A. Moreno & J. A. Casajús
Received: 13 July 2010 / Accepted: 13 September 2010 / Published online: 22 October 2010
# International Osteoporosis Foundation and National Osteoporosis Foundation 2010
Abstract
Summary Children and adolescents with Down syndrome
(DS) have lower levels of bone mass compared with youths
without DS. Their sexual dimorphism in bone mass also
differs from that observed in children and adolescents
without Down syndrome.
Introduction This study aimed to compare bone mass and
sexual dimorphism in bone mass between male and female
youths with DS and age- and sex-matched controls
without DS.
Methods Bone mineral density (BMD), volumetric BMD,
bone mineral apparent density (BMAD), BMD/height
(BMDH), and total lean mass were measured or calculated
from DXA. Thirty-two youths (15 females) with DS and 32
youths (13 females) without DS participated in the study.
A. González-Agüero : G. Vicente-Rodríguez : L. A. Moreno :
J. A. Casajús (*)
GENUD (Growth, Exercise, Nutrition and Development)
research group, University of Zaragoza,
Ed. Cervantes. Corona de Aragón St. 42, 2nd floor,
50009 Zaragoza, Spain
e-mail: [email protected]
A. González-Agüero
G. Vicente-Rodríguez
L. A. Moreno
A. González-Agüero : G. Vicente-Rodríguez : J. A. Casajús
Faculty of Health and Sport Sciences, Huesca,
University of Zaragoza,
Zaragoza, Spain
L. A. Moreno
School of Health Sciences, University of Zaragoza,
Zaragoza, Spain
Results ANOVA tests showed lower BMAD and BMDH in
females with DS compared with females without DS.
ANCOVA tests revealed lower BMD in the whole body
of males and females as well as BMD in the hip region of
the females with DS compared with their counterparts
without DS. Within the group with DS, females had greater
lumbar spine BMD than the males.
Conclusions The low values of BMD and related parameters, together with the differences in the sexual dimorphism,
indicate a non-standard bone development in this specific
population of children and adolescents with DS.
Keywords Body composition . DXA . Hip . Lumbar spine .
Sexual dimorphism . Trisomy 21
Introduction
Life expectancy in Down syndrome (DS) population has
increased over the last 70 years, rising from 9 years of age to as
much as 55 years and older, and this trend is expected to
continue [1–3]. As the life expectancy of populations with DS
increases, a reasonable prediction would show an increased
incidence in osteoporosis, bone fragility and related problems
(which appear mainly with age) over the coming years.
High bone mass acquisition during childhood and
adolescence is a key determinant for adult skeletal health
[4, 5], and populations with DS have shown decreased bone
mass compared with subjects without intellectual disabilities (ID) [6–11] as well as others with ID but without DS
[12, 13]. However, only a few of these studies have included
children and adolescents with DS [7, 8], or specifically
examined a pediatric population [10, 13], that commonly
display lower values of bone mineral content (BMC) and
bone mineral density (BMD) compared with peers without
-83-
2152
DS. Despite these studies, information concerning bone mass
in pediatric population with DS is scarce [14] and should
therefore be given greater attention, since low bone mass
(osteopenia or osteoporosis) in adulthood may be a direct
result of low acquisition during growth.
Previous studies showed sexual dimorphism in bone
mass during growth in healthy populations [15]. In adults
with DS, lower lumbar spine BMC, BMD, and volumetric
BMD (vBMD) in males compared with females [6, 8, 12]
have been observed; however, there is a lack of information
in children or adolescents with DS. Since adult population
with DS generally possess low bone mass, it would be of
significant benefit to elucidate whether the acquisition of
bone mass could be identified earlier, for example, in
childhood and adolescence. Furthermore, one crucial aspect
of such a study would investigate and detect sensitive
growth periods that could correspond to a reduced level of
bone mass acquisition.
The law of Wolff postulates that bones adapt to
mechanical loads [16], and bone development seems to be
site-specific [17, 18]. Consequently, it is very important to
describe bone mass for the different regions of the body,
which have not been previously studied in children and
adolescents with DS. A study of this latter population could
help to detect critical zones with low BMD in populations
with DS in order to establish targeted interventions to
improve bone mass. The aim of this study is to describe the
total and regional (lumbar spine, hip, and femoral neck)
bone mass in male and female children and adolescents
with DS compared with age-matched subjects without DS.
Materials and methods
Subjects
A total sample of 32 children (15 females, 17 males)
and adolescents with DS living at home, between 10 and
19 years were recruited from different special schools and
institutions within the same region of Aragón in Spain.
Another individually age-matched sample of 32 subjects
(13 females, 19 males) without DS was also recruited from
regular schools in this region. All the children without DS
were healthy and without known illness, and all subjects
had been medication-free for at least 3 months before the
tests. A full clinical history, including illnesses or surgical
interventions and stays in a hospital, was collected for each
individual. Eight participants with DS had been diagnosed
of hypothyroidism in the past; however, during the study,
they were taking medication (levothyroxine sodium: four of
them taking Levothroid and the other four, Eutirox). Both
parents and children were informed about the aims and
procedures of the study, as well as the possible risks and
-84-
Osteoporos Int (2011) 22:2151–2157
benefits, and then, a letter of written informed consent was
obtained from all the included subjects and their parents or
guardians. The study was performed in accordance with the
Helsinki Declaration 1961 (revised in Edinburgh, 2000) and
was approved by the Research Ethics Committee of the
Government of Aragón (CEICA, Spain).
Anthropometric
All subjects were measured with a stadiometer without
shoes and the minimum clothes to the nearest 0.1 cm
(SECA 225, SECA, Hamburg, Germany), and weighted to
the nearest 0.1 kg (SECA 861, SECA, Hamburg, Germany). WC was measured to the nearest 0.1 cm with an
anthropometric tape (Rosscraft, Canada). Body mass index
(BMI) was calculated as weight (in kilograms) divided by
height (square meters).
Pubertal status assessment
Pubertal development was determined by direct observation
according to the five stages proposed by Tanner and
Whitehouse [19].
Bone and lean masses
The bone and lean masses of the subjects were measured
with dual-energy X-ray absorptiometry (DXA) using a
pediatric version of the software QDR-Explorer (Hologic
Corp. Software version 12.4, Waltham, MA). DXA equipment was calibrated with a lumbar spine phantom and step
densities phantom following the Hologic guidelines. Subjects were scanned in supine position, and the scans were
performed in high resolution. Osseous area (square centimeters), BMC (in grams), and lean mass (in kilograms)
were calculated from total and regional analysis of the
whole body scan. BMD (grams per square centimeter) was
calculated using the formula BMD=BMCarea−1.
Two additional examinations were conducted to estimate
bone mass at the lumbar spine (L1–L4) and proximal region of
the femur (hip and femoral neck). Volumetric BMD (vBMD)
was estimated for the lumbar spine and femoral neck using
simple geometric cylindrical models [20], previously used
with this population [8]. Bone mineral apparent density
(BMAD) was calculated as previously described [21], using
the formula whole body BMAD=BMC/(area2/body height).
The expression BMD/height (BMDH) was calculated to
adjust bone mass for whole body bone size [22].
Statistical analysis
Mean and standard deviation are given as descriptive
statistics, otherwise stated.
Osteoporos Int (2011) 22:2151–2157
2153
The variables showed normal distributions. ANOVA was
used to test hypothesis regarding the equality of the means
between groups for the following characteristics: age,
weight, height, BMI, total lean mass, vBMD of the lumbar
spine and femoral neck, BMAD, and BMDH. Analyses of
covariance were performed to evaluate differences in BMD,
entering Tanner stage, height, and whole body lean mass as
covariates. The use of these covariates is based on evidence
identifying pubertal status, height, and total lean mass as
influential factors on muscle mass and bone mass in the
growing skeleton [23–25]. Effect size statistics using
Cohen's d (standardized mean difference) were calculated
[26]. Taking into account the cutoff established by Cohen,
the effect size can be small (~0.2), medium (~0.5), or large
(~0.8).
The SPSS 15.0 software for Windows (SPSS Inc.
Chicago, IL) was used for the analyses and the significance
level was 5%.
Results
All the analyses were conducted from the whole sample,
and, in addition, excluding the eight subjects that reported
past disease of hypothyroidism (data not shown); as results
did not substantially change, the data presented herein
correspond to the whole sample to keep sample size.
Additionally, no differences were observed in any of the
studied variables between DS subjects with and without
past disease of hypothyroidism within our sample (data not
shown).
Physical characteristics
The characteristics of the groups with and without DS
are summarized in Table 1. In general, subjects, both male
and female with DS were lighter, smaller, and had lower
lean mass compared with non-DS peers (all p<0.05,
Table 1).
Bone mass
Appendix 1 summarizes the raw values of BMD of the
subjects.
After adjusting the raw values by Tanner stage, height,
and total lean mass, females and males with DS showed
lower BMD in whole body than their counterparts without
DS; females with DS also presented lower BMD in the hip
(all p<0.05; Fig. 1).
Females with DS showed lower BMAD and BMDH
than the females without DS (all p< 0.05; Table 2).
However, no differences were found in vBMD of lumbar
spine or femoral neck between females or males with and
without DS (Table 2).
Differences between sexes within the same group
Figure 2 shows the differences in BMD between females
and males within the groups with and without DS after
adjusting by Tanner stage, height, and total lean mass.
Lumbar spine BMD was higher in females than in males in
the group with DS (both p<0.05; Fig. 2a).
All the previous comparisons exhibited large effect sizes
(Cohen's d ranged from 0.9 to 1.5).
Discussion
The principal finding of the present study is that children
and adolescents with DS showed lower values of BMD and
related parameters compared with age-matched subjects
without DS. In doing so, it also shows that males with DS
have lower BMD in lumbar spine than females with DS.
Differences between with and without DS
To date, several studies have described lower bone mass in
populations with DS compared with others without DS,
with or without ID [6–13]. Osteoporotic problems in
Table 1 Subject age, anthropometrics, total lean, and maturation status results (mean±standard deviation)
Down syndrome
All (n=32)
Age (years)
Sexual maturation: Tanner (%)
stages I/II/III/IV/V
Weight (kg)
Height (cm)
Body mass index (kg/m2)
Total lean mass (kg)
15.3±2.9
16/6/22/9/47
46.0*±11.8
145.2*±11.8
21.5±3.4
32.6*±8.3
Without Down syndrome
Female (n=15)
Male (n=17)
14.9±3.2
42.8±12.5
138.5*†±10.1
21.8±4.0
27.7*†±7
15.6±2.7
48.7*±10.9
150.7*±10.3
21.2±2.8
36.6*±7.2
All (n=32)
14.7±2.3
13/6/13/19/50
55.6±13.1
163.3±12.3
20.6±3.6
39.4±9.8
Female (n=13)
Male (n=19)
14.6±2.4
14.8±2.2
53.2±13.8
156.7†±9.6
21.4±4.5
34.2†±6.7
57.3±12.7
167.8±12.1
20.1±2.7
42.9±10.2
*p<0.05 between groups; †p<0.05 between genders within the same group
-85-
2154
Osteoporos Int (2011) 22:2151–2157
Fig. 1 a Females bone mass. Tanner stage-, total lean mass-, and
height-adjusted BMD from the whole body, lumbar, and femoral scans
in females with and without DS. *p<0.05. b Males bone mass. Tanner
stage-, total lean mass-, and height-adjusted BMD from the whole
body, lumbar, and femoral scans in males with and without DS.
*p<0.05
populations with DS are well documented in adults [6, 9,
11, 12]; however, very few studies have included children
or adolescents [7, 8], and even fewer have studied them
specifically [10, 13].
The current investigation analyzes the biggest sample of
children and adolescents with DS to date and considering
bone regions in the analysis. Our results showed lower
BMD in male and female children and adolescents with DS
compared with children and adolescents without DS. The
results also suggest that differences in height—therefore in
bone size—between children and adolescents with and
without DS are largely responsible for the differences in
BMD.
The studies from Sepulveda et al. [9] and Guijarro et al.
[11] described lower BMD in the pelvic region and whole
body, respectively, in individuals with DS compared with
those without DS. Our results corroborate these findings as
we also found lower values of BMD in the whole body of
males and females with DS compared with those without
DS.
Previous studies in individuals with DS [6–11] clearly
observed lower BMD in the lumbar spine of adults and
young adult females with DS compared with females
without DS. From all of them, only Kao et al. [10] studied
an exclusive sample of only ten children with DS. Baptista
et al. [8] divided their sample in age groups older and
younger than 20 years and did not find differences in
lumbar spine BMD in the younger group. In agreement
with Baptista et al. [8], we found no observable differences
in the lumbar spine of children and adolescents with DS
compared with children and adolescents without DS. Most
of the previous studies in adults with DS observed lower
BMD in lumbar spine compared with adults without DS,
which may therefore suggest that this decreased BMD
could appear after puberty, since this period may be a key
moment to enhance bone mass.
Regions such as the hip, especially the femoral neck,
are very important areas to be studied because they are
considered as ‘risk regions’ for osteoporosis and bone
fracture. Guijarro et al. [11] found lower values of BMD
in the femoral neck and total hip in the group with DS
compared with the group without DS. Our results
reinforce these, as we also described lower values of
Table 2 Calculated variables of bone mass (mean±standard deviation)
Down syndrome
Lumbar spine vBMD (g/cm3)
Femoral neck vBMD (g/cm3)
Bone mineral apparent density (g/cm3)
BMDH (g/cm3)
Without Down syndrome
All (n=32)
Female (n=15)
Male (n=17)
All (n=32)
0.26±0.05
0.32±0.04
0.088*±0.008
0.61±0.05
0.24±0.05
0.33±0.03
0.085*±0.008
0.61*±0.04
0.27±0.05
0.32±0.04
0.090±0.008
0.61±0.06
0.27±0.05
0.32±0.05
0.092±0.006
0.63±0.05
vBMD volumetric bone mineral density, BMDH bone mineral density/height
*p<0.05 between groups
-86-
Female (n=13)
Male (n=19)
0.27±0.06
0.33±0.06
0.092±0.004
0.64±0.04
0.27±0.04
0.31±0.03
0.092±0.006
0.62±0.06
Osteoporos Int (2011) 22:2151–2157
2155
BMDH. This tends to suggest that young females with DS
have a poorer bone development than young males with DS
when each sex is separately compared with their counterparts without DS. Therefore, low BMD is already detected
in females and partially in males with DS, although this
disadvantage clinical situation may aggravate with growth.
Several authors described childhood and adolescence as the
most important periods to accumulate BMD in the skeleton
[24] and, specifically, peak BMD is reached between 20
and 25 years. As children and adolescents with DS already
have lower values of BMD, efforts to develop physical
activity programs, which may enhance bone mass, should
be considered. Strength or plyometric exercise may be
beneficial for this population, although more detailed
research on this topic is required.
Sexual dimorphism in children and adolescents with DS
Fig. 2 a Down syndrome bone mass. Tanner stage-, total lean mass-,
and height-adjusted BMD from the whole body, lumbar, and femoral
scans in males and females with DS. *p<0.05. b Controls bone mass.
Tanner stage-, total lean mass-, and height-adjusted BMD from the
whole body, lumbar, and femoral scans in males and females without
DS. *p<0.05
BMD in the hip of females with DS compared with their
peers without DS.
Although BMD has been shown to be a useful predictor
of future fracture risk, vBMD provides a better approach to
the real bone due to the limitations of the projected bone
when very different populations (differences in height) are
evaluated [27]. Guijarro et al. [11] and Baptista et al. [8]
found lower vBMD at lumbar spine and femoral neck of
adults with DS; as we did not find this, it is plausible to
think that the lower vBMD in the population with DS
appears with age and is not present during childhood and
adolescence possibly due to impaired mineralization. To the
best of our knowledge, the bone parameters BMAD and
BMDH had not been used previously in populations with
DS; these better reflect bone apparent density and take into
account the height of the subjects [21, 22]. In the present
study, females with DS showed lower levels of BMAD and
Previous comparisons between bone mass of males and
females, mainly in adults, with DS have been conducted
[6, 8]. Angelopuolou et al. [6] and Baptista et al. [8]
observed higher values of BMD in lumbar spine in adult
females with DS compared with males with DS. Our study
shows that those findings are already detectable in children
and adolescents, showing higher values of BMD in the
females with DS at the lumbar spine compared with males
with DS.
Additionally, the differences between males and females in
the group without DS were not the same of that observed
between males and females with DS. These results indicate
that bone mass acquisition during puberty seems to be different
in children and adolescents with DS than in those without, also
in terms of sexual dimorphism. Therefore, an independent
study of this population is required in order to understand
specific bone development and growth within the group.
Some limitations should be recognized. Despite that the
number of participants is bigger than the majority of the
previous published studies in children and adolescents with
DS, the specificity of the condition and the age range
become complicated, increasing the sample size. Therefore,
the group may not be large enough to generalize the results
of gender comparison. As strength of our study, the large
effect size observed in the differences (between groups and
between sexes) indicates a substantial biological magnitude
of the results, which, in turn, may point out the direction of
future research. The cross-sectional design is another
limitation of this study; therefore, bone development cannot
be studied. A longitudinal research of children with DS
could help to corroborate the hypothesis that the low bone
mass observed is due to a lower acquisition in the population
with DS during the most important years of accumulation.
However, this is the first investigation assessing BMD,
-87-
2156
Osteoporos Int (2011) 22:2151–2157
estimated vBMD, and apparent density in whole body and
key subregions in a relatively large sample of male and
female children and adolescents with DS and could serve as
a starting point for further, even more detailed research.
Conclusions
The current study provides evidence that children and
adolescents with DS have a clear tendency towards lower
BMD and vBMD in several regions of their bodies
compared with age- and sex-matched subjects without
DS. The lower values in BMAD and BMDH suggest that
young females with DS are poorer at acquiring bone mass
than young males with DS, when compared with their ageand sex-matched controls. Importantly, this is the first
time that differences in bone mass between male and
female children and adolescents with DS have been
studied and compared. These results show that sexual
dimorphism in bone mass is evident, and it is different
than that observed in the children and adolescents without
DS. The low levels of BMD, together with the differences
in the sexual dimorphism, indicate a different bone
development in this specific population of children and
adolescents with DS.
Longitudinal studies aiming to identify critical periods of
bone development specifically in population with DS may
corroborate the hypothesis presented in this study.
Further studies assessing other factors related to bone
mass development during puberty, such as physical activity,
physical fitness, or diet, could be beneficial in helping us
understand the importance of lifestyle on the lower bone
mass observed in populations with DS.
Acknowledgment The authors want to thank all the children and
their parents who participated in the study, for their understanding and
dedication to the project. Special thanks are given to Fundación Down
Zaragoza and Special Olympics Aragon for their support. We also
thank Scott G. Mitchell from the University of Glasgow for his work
of reviewing the English style and grammar, and Paula Velasco from
the University of Zaragoza for her great technical assistance. This
work was supported by Gobierno de Aragón (Proyecto PM 17/2007)
and Ministerio de Ciencia e Innovación de España (Red de
investigación en ejercicio físico y salud para poblaciones especialesEXERNET-DEP2005-00046/ACTI). There are no potential conflicts
of interest that may affect the contents of this work.
Conflicts of interest None.
Appendix 1
Table 3 Mean and standard deviation in raw values of bone mineral density of children and adolescents with and without Down syndrome
Female
DS (n=15) mean±SD
Male
Non-DS (n=13) mean±SD
DS (n=17) mean±SD
Non-DS (n=19) mean±SD
1.014±0.109
0.873±0.154
0.847±0.198
0.786±0.153
0.928±0.127
0.788±0.146
0.834±0.115
0.741±0.113
1.049±0.128
0.857±0.151
0.888±0.177
0.858±0.112
Bone mineral density (g/cm2)
Whole body
Lumbar spine
Hip zone
Femoral neck
0.845±0.086
0.762±0.118
0.697±0.086
0.680±0.070
DS Down syndrome, non-DS without Down syndrome, SD standard deviation
References
1. Bittles AH, Glasson EJ (2004) Clinical, social, and ethical
implications of changing life expectancy in Down syndrome.
Dev Med Child Neurol 46:282–286
2. Glasson EJ, Sullivan SG, Hussain R, Petterson BA, Montgomery
PD, Bittles AH (2002) The changing survival profile of people
with Down's syndrome: implications for genetic counselling. Clin
Genet 62:390–393
3. Smith DS (2001) Health care management of adults with Down
syndrome. Am Fam Physician 64:1031–1038
-88-
4. Rizzoli R, Bonjour JP (1999) Determinants of peak bone mass
and mechanisms of bone loss. Osteoporos Int 9(Suppl 2):S17–
S23
5. Rizzoli R, Bianchi ML, Garabedian M, McKay HA, Moreno LA
(2010) Maximizing bone mineral mass gain during growth for the
prevention of fractures in the adolescents and the elderly. Bone
46:294–305
6. Angelopoulou N, Souftas V, Sakadamis A, Mandroukas K (1999)
Bone mineral density in adults with Down's syndrome. Eur Radiol
9:648–651
7. Sakadamis A, Angelopoulou N, Matziari C, Papameletiou V,
Souftas V (2002) Bone mass, gonadal function and biochemical
Osteoporos Int (2011) 22:2151–2157
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
assessment in young men with trisomy 21. Eur J Obstet Gynecol
Reprod Biol 100:208–212
Baptista F, Varela A, Sardinha LB (2005) Bone mineral mass in
males and females with and without Down syndrome. Osteoporos
Int 16:380–388
Sepulveda D, Allison DB, Gomez JE, Kreibich K, Brown RA,
Pierson RN Jr, Heymsfield SB (1995) Low spinal and pelvic bone
mineral density among individuals with Down syndrome. Am J
Ment Retard 100:109–114
Kao CH, Chen CC, Wang SJ, Yeh SH (1992) Bone mineral
density in children with Down's syndrome detected by dual
photon absorptiometry. Nucl Med Commun 13:773–775
Guijarro M, Valero C, Paule B, Gonzalez-Macias J, Riancho JA
(2008) Bone mass in young adults with Down syndrome. J
Intellect Disabil Res 52:182–189
Angelopoulou N, Matziari C, Tsimaras V, Sakadamis A, Souftas
V, Mandroukas K (2000) Bone mineral density and muscle
strength in young men with mental retardation (with and without
Down syndrome). Calcif Tissue Int 66:176–180
Halaba Z, Pyrkosz A, Adamczyk P, Drozdzowska B, Pluskiewicz
W (2006) Longitudinal changes in ultrasound measurements: a
parallel study in subjects with genetic disorders and healthy
controls. Ultrasound Med Biol 32:409–413
González-Agüero A, Vicente-Rodriguez G, Moreno LA,
Guerra-Balic M, Ara I, Casajus JA (2010) Health-related
physical fitness in children and adolescents with Down
syndrome and response to training. Scand J Med Sci Sports
20:716–724
Nguyen TV, Maynard LM, Towne B, Roche AF, Wisemandle W,
Li J, Guo SS, Chumlea WC, Siervogel RM (2001) Sex differences
in bone mass acquisition during growth: the Fels Longitudinal
Study. J Clin Densitom 4:147–157
Wolff J (1892) The law of bone formation. Hirschwald, Berlin
Vicente-Rodriguez G, Jimenez-Ramirez J, Ara I, SerranoSanchez JA, Dorado C, Calbet JA (2003) Enhanced bone mass
2157
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
and physical fitness in prepubescent footballers. Bone 33:853–
859
Vicente-Rodriguez G, Ara I, Perez-Gomez J, Serrano-Sanchez JA,
Dorado C, Calbet JA (2004) High femoral bone mineral density
accretion in prepubertal soccer players. Med Sci Sports Exerc
36:1789–1795
Tanner JM, Whitehouse RH (1976) Clinical longitudinal standards
for height, weight, height velocity, weight velocity, and stages of
puberty. Arch Dis Child 51:170–179
Gravholt CH, Lauridsen AL, Brixen K, Mosekilde L, Heickendorff
L, Christiansen JS (2002) Marked disproportionality in bone size
and mineral, and distinct abnormalities in bone markers and
calcitropic hormones in adult turner syndrome: a cross-sectional
study. J Clin Endocrinol Metab 87:2798–2808
Katzman DK, Bachrach LK, Carter DR, Marcus R (1991) Clinical
and anthropometric correlates of bone mineral acquisition in
healthy adolescent girls. J Clin Endocrinol Metab 73:1332–1339
Bachrach LK, Hastie T, Wang MC, Narasimhan B, Marcus R
(1999) Bone mineral acquisition in healthy Asian, Hispanic,
Black, and Caucasian youth: a longitudinal study. J Clin
Endocrinol Metab 84:4702–4712
Faulkner RA, Bailey DA, Drinkwater DT, McKay HA, Arnold C,
Wilkinson AA (1996) Bone densitometry in Canadian children 8–
17 years of age. Calcif Tissue Int 59:344–351
Vicente-Rodriguez G (2006) How does exercise affect bone
development during growth? Sports Med 36:561–569
Slemenda CW, Miller JZ, Hui SL, Reister TK, Johnston CC Jr
(1991) Role of physical activity in the development of skeletal
mass in children. J Bone Miner Res 6:1227–1233
Nakagawa S, Cuthill IC (2007) Effect size, confidence interval
and statistical significance: a practical guide for biologists. Biol
Rev Camb Philos Soc 82:591–605
Carter DR, Bouxsein ML, Marcus R (1992) New approaches for
interpreting projected bone densitometry data. J Bone Miner Res
7:137–145
-89-
-90-
Author's personal copy
Research in Developmental Disabilities 32 (2011) 1685–1693
Contents lists available at ScienceDirect
Research in Developmental Disabilities
Fat and lean masses in youths with Down syndrome: Gender differences
Alejandro González-Agüero a,b,*, Ignacio Ara a,c, Luis A. Moreno a,d,
Germán Vicente-Rodrı́guez a,b, José A. Casajús a,b
a
GENUD (Growth, Exercise, NUtrition and Development) Research Group, University of Zaragoza, Spain
Faculty of Health and Sport Sciences, Huesca, University of Zaragoza, Spain
c
GENUD Toledo Research Group, University of Castilla La Mancha, Spain
d
School of Health Sciences, University of Zaragoza, Spain
b
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 18 February 2011
Received in revised form 22 February 2011
Accepted 22 February 2011
Available online 24 March 2011
The present study aimed at comparing fat and lean masses between children and
adolescents with and without Down syndrome (DS) and evaluating the presence of sexual
dimorphism. Total and regional fat and lean masses were assessed by dual energy X-ray
absorptiometry (DXA) and the percentage of body fat (%BF) by air-displacement
plethysmography (ADP) in 31 participants with DS and 32 controls. Waist circumference
(WC) was also measured. Analysis of covariance and the Student’s t-test were used to
compare variables between groups and between sexes within the same group. There were
no significant differences in %BF, WC or body mass index (BMI) between groups. Females
with DS showed higher fat and lean masses in the trunk, and lower fat and lean masses in
the lower limbs compared with females without DS (all p 0.05). Males with DS showed
higher fat masses in the whole body and upper limbs, and lower lean masses in the whole
body and lower limbs compared with males without DS (all p 0.05). Females in both
groups showed higher levels of fat, and lower levels of lean than did their respective males
(all p 0.05). Youths with DS showed higher fat and lower lean than their non-DS peers.
The increased truncal fat in females with DS might indicate a higher risk of metabolic
syndrome in this group. Sexual dimorphism in youths with and without DS was very
similar. BMI, WC and %BF were not effective indicators of increased risk in youths with DS.
ß 2011 Elsevier Ltd. All rights reserved.
Keywords:
Trisomy 21
DXA
Obesity
Body composition
1. Introduction
Increased adiposity characterized by a higher percentage of body fat (%BF) during childhood and adolescence is related to
a greater risk of premature illnesses, death from coronary heart disease, hypertension and type 2 diabetes mellitus later in
life (Dietz, 1998; Ebbeling, Pawlak, & Ludwig, 2002; Maffeis & Tato, 2001). Low lean mass is associated with decreased
skeletal muscle tissue (Calbet et al., 2008), which that in turn, reduces the functional capacity and the maximum oxygen
consumption that is a marker of health in youth and is also associated with increased cardiovascular health later in life
(Ortega et al., 2005; Ortega, Ruiz, Castillo, & Sjostrom, 2008). Although certain clinical studies indicate that a common
characteristic of youths with Down syndrome (DS) is to have light to moderate obesity (Chumlea & Cronk, 1981; Cronk,
Chumlea, & Roche, 1985; Hawn, Rice, Nichols, & McDermott, 2009; Rubin, Rimmer, Chicoine, Braddock, & McGuire, 1998),
and that no difference in fat-free mass can be found when compared with youths without DS (Luke, Sutton, Schoeller, &
* Corresponding author at: C/Corona de Aragón 42, Edificio Cervantes 2a planta, Grupo GENUD, 50006 Zaragoza, Spain. Tel.: +34 976400338x301;
fax: +34 976400340.
E-mail address: [email protected] (A. González-Agüero).
0891-4222/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ridd.2011.02.023
-91-
1686
A. González-Agüero et al. / Research in Developmental Disabilities 32 (2011) 1685–1693
Roizen, 1996), soft-tissue body composition in children and adolescents with DS has not been sufficiently studied (GonzálezAgüero et al., 2010).
Although cardiovascular disease is not one of the most common disorder related to mortality in this population (Coppus
et al., 2008; Prasher, 1993; Thase, 1982) and despite the fact that persons with DS may have fewer atherosclerotic risk factors
than others with intellectual disability without DS (Draheim, McCubbin, & Williams, 2002), the continuous increase in life
expectancy in the DS population (from 9 to 55 years and older during the last 70 years) (Bittles & Glasson, 2004; Glasson
et al., 2002; Smith, 2001) together with high levels of adipose tissue (especially in the trunk) (Dietz, 1998; Ebbeling et al.,
2002; Maffeis & Tato, 2001; Ortega et al., 2005, 2008) might be a future health issue.
In this regard, Bronks and Parker (1985) described that although the %BF assessed with anthropometry in participants
with DS did not significantly change with age, it was consistently high at all ages, suggesting that fat mass accumulation
occurs prior to adulthood.
In adults, studies assessing the %BF by dual energy X-ray absorptiometry (DXA) showed higher levels of fat mass and
lower levels of lean mass in participants with DS compared with age- and sex-matched controls without DS (Baptista, Varela,
& Sardinha, 2005; Guijarro, Valero, Paule, Gonzalez-Macias, & Riancho, 2008).
Air-displacement plethysmography (ADP) has been used to assess body composition in children and adolescents because
of its accuracy and validity of estimation at the individual level (Fields & Goran, 2000; Parker, Reilly, Slater, Wells, & Pitsiladis,
2003). However, to our knowledge only one study assessed DS adults with ADP (Usera, Foley, & Yun, 2005). In addition, DXA
offers the possibility of performing regional analyses (trunk, upper and lower limbs) of fat and lean masses.
On the other hand, due to the high cost and large dimensions of those two methods, a limited number of studies have been
performed on DS populations (Angelopoulou, Souftas, Sakadamis, & Mandroukas, 1999; Baptista et al., 2005; Guijarro et al.,
2008).
The difficult conditions of these two methods make them unsuitable for field and clinical use; therefore other methods
such as anthropometry are also widely used. Waist circumference (WC) seems to be one of the best anthropometric indicator
for increased risk of metabolic syndrome in healthy children (Moreno et al., 2002); however no data on populations with DS
can be found on this regard. It is important to note that we used a combination of three methods (DXA, ADP and WC) in order
to better evaluate the body composition of this population, and to assess the effectiveness of WC as a predictor of high
adiposity levels in a population with DS.
Lastly, due to the lack of information related to body composition in youths with DS, it is still unknown whether the
common sexual dimorphism presents in youths without DS is also present in children and adolescents with DS.
Thus the aims of the present study were: (1) to compare total and regional distributions of fat and lean masses between
male and female children and adolescents with and without DS; (2) to investigate whether WC can accurately detect those
individuals with an elevated level of adiposity; and (3) to evaluate the presence of sexual dimorphism in children and
2. Materials and methods
2.1. Participants
A total sample of 31 children and adolescents with DS (14 females/17 males, aged 10–19 years) were recruited from
different schools and institutions of Aragón (Spain). An age- and sex-matched control group composed of 32
participants (13 females/19 males) without DS was recruited from a public school also in Aragón. All participants
without DS were healthy, without known illness and free of medication for at least 3 months before the beginning of the
study.
Full clinical histories, including illnesses, surgical interventions and stays in a hospital, were collected for all individuals.
Both parents and children were informed about the aims and procedures, as well as the possible risks and benefits of the
study. Written informed consent was obtained from all the participants and their parents or guardians. The study was
performed in accordance with the Helsinki Declaration of 1961 (revised in Edinburgh, 2000) and was approved by the
Research Ethics Committee of the Government of Aragon (CEICA, Spain).
2.2. Anthropometry
All participants were measured with a stadiometer without shoes and minimum clothing to the nearest 0.1 cm (SECA 225,
SECA, Hamburg, Germany), and weighted to the nearest 0.1 kg (SECA 861, SECA, Hamburg, Germany). WC was measured to
the nearest 0.1 cm with an anthropometric tape (Rosscraft, Canada). The body mass index (BMI) was calculated as weight
(kg) divided by height squared (m2).
2.3. Pubertal status assessment
Pubertal development was determined by direct observation by a physician according to the 5 stages proposed by Tanner
and Whitehouse (1976).
-92-
1687
2.4. Fat and lean masses
Total fat (kg) and lean (kg) masses were determined from a whole-body scan by DXA, using a pediatric version of the QDRExplorer software (Hologic Corp. Software version 12.4, Waltham, MA). The validity of DXA was established by comparison
with chemical analysis (Svendsen, Haarbo, Hassager, & Christiansen, 1993), and its reliability was demonstrated by an intraclass correlation of 0.998 for repeated measurements of the %BF in children (Gutin et al., 1996). DXA equipment was
calibrated using a lumbar spine and step densities phantom and following Hologic guidelines. Participants were scanned in
the supine position and scans performed with high resolution. Fat and lean masses were calculated also from regional
analyses of the whole body scan: upper and lower limbs and trunk. The %BF was calculated as total body fat divided by body
mass and multiplied by 100.
2.5. Air-displacement plethysmography
ADP measurements were obtained immediately after the anthropometric and DXA assessments. A BODPOD1 Body
Composition System (Life Measurement Instruments, Concord, CA) was used to assess total body density as previously
described (Fields & Goran, 2000). Measurements with BODPOD1 were performed with the participant in minimum clothing
(underwear or swimwear) and with a swim cap. All assessments were carried out with the same device and software and
performed by the same technician who had been fully trained in the operation. The %BF was obtained by introducing the total
body density into the equation of Siri (1961).
2.6. Statistical analysis
Mean and standard deviation are given as descriptive statistics; otherwise they are stated. All variables included in the
study showed a normal distribution, assessed by Kolmogorov–Smirnov tests. Differences between groups (with and without
DS), separately by genders (females with DS vs. females without DS; males with DS vs. males without DS) and between
gender within the same group for age, physical characteristics (height, weight, BMI and WC) and %BF (both DXA and ADP)
were established using the Student’s unpaired t-tests. The degree of agreement in the %BF between methods (ADP and DXA)
was graphically examined by plotting the difference between methods against the ‘‘gold standard’’ (ADP), according to the
Bland–Altman method (Bland & Altman, 1986). Differences were plotted against the ‘‘gold standard’’ instead of the mean
value because the ‘‘gold standard’’ was expected to be closer to the ‘‘true value’’ than the mean (Krouwer, 2008). Validity and
lack of agreement with ADP were assessed by calculating the systematic error (i.e. that is the inter-methods difference) and
the SD of the difference. The 95% limits of agreement (systematic error 1.96 SD) were also calculated. Additionally, the
presence of systematic error was analyzed by one sample t-test against zero.
Analyses of covariance (ANCOVA) were performed to evaluate differences in fat and lean masses, entering Tanner stage,
height and weight as covariates. The reason for using these covariates is based on evidence in previous studies identifying
them as influential factors on body composition (Slemenda, Miller, Hui, Reister, & Johnston, 1991). The analyses were
conducted separately by gender (male and female) since sex-interactions were found between gender and DS status. Effectsize statistics using Cohen’s d (standardized mean difference) were calculated for all the comparisons in fat and lean masses
(Nakagawa & Cuthill, 2007). Taking into account the cut-off established by Cohen, the effect size can be small (0.2), medium
(0.5) or large (0.8). The SPSS 15.0 software for Windows (SPSS Inc. Chicago, IL) was used for the analyses and the
significance level was 5%.
3. Results
3.1. Physical characteristics
Age and physical characteristics of the participants are summarized in Table 1. In general, participants with DS were
lighter and smaller than those without DS (all p 0.05). No differences in age, BMI and WC were observed between groups or
between genders within the same group.
Table 1
Participants’ age and physical characteristics (mean standard deviation).
Down syndrome
Age (year)
Weight (kg)
Height (cm)
Waist circumference (cm)
Body mass index (kg/m2)
*
#
Non-Down syndrome
All (n = 31)
Female (n = 14)
Male (n = 17)
All (n = 32)
Female (n = 13)
Male (n = 19)
15.2 2.9
46.7* 12.2
145.2* 11.6
75.4 11.1
21.7 3.9
14.8 3.2
42.9 13.5
138.9*,# 9.9
78.1 14.1
22.4 4.8
15.5 2.7
48.7* 10.9
150.8* 10.3
72.9 7.1
21.0 2.9
14.7 2.3
55.6 13.1
163.2 12.4
74.6 8.3
20.7 3.5
14.6 2.4
53.2 13.8
156.3# 9.6
75.1 10.1
21.5 4.4
14.8 2.2
57.3 12.7
167.8 12.1
74.2 7.1
20.1 2.7
p 0.05 between groups.
p 0.05 between sexes within the same group.
-93-
1688
Table 2
Percentage of body fat assessed by ADP and DXA (mean standard deviation).
Down syndrome
Body fat by DXA (%)
Body fat by BODPOD (%)
#
Non-Down syndrome
All (n = 31)
Female (n = 14)
Male (n = 17)
All (n = 32)
Female (n = 13)
Male (n = 19)
24.7 7.8
25.8 10.1
30.4# 5.2
29.9# 11.5
19.9 6.3
22.1 7.0
24.4 7.4
24.3 9.8
30.2# 6.1
31.1# 8.3
20.4 5.4
19.4 7.8
p 0.05 between sexes within the same group.
3.2. Percentage of body fat
The %BF assessed by ADP and DXA is presented in Table 2. Females in both groups (with and without DS) had a higher %BF
than the males from their respective groups (all p 0.05). No differences between groups were observed in the %BF. The 95%
limits of agreement between the %BF with ADP and that with DXA were 16.4 and the presence of a systematic error was not
observable (p > 0.05; data not shown).
[()TD$FIG]
Fig. 1. Tanner stage-, height- and weight-adjusted fat and lean masses from the whole body, trunk, upper and lower limbs, in females with and without
Down syndrome; *p 0.05.
-94-
1689
After adjusting by Tanner stage, height and weight, females with DS showed higher fat and lean masses in the trunk,
accompanied by lower fat and lean masses in the lower limbs, compared with females without DS (all p 0.05; Fig. 1). Males
with DS had higher fat masses in the whole body and in the upper limbs than males without DS (both p 0.05; Fig. 2) and
showed a tendency towards higher fat mass in the lower limbs (p = 0.06; Fig. 2). Lower lean masses in the whole body and
lower limbs of males with DS, compared with males without DS were found (both p 0.05; Fig. 2).
3.4. Gender differences within the same group
Females in both groups (with and without DS), showed higher levels of fat and lower levels of lean in all the studied
regions: whole body, trunk, upper and lower limbs (all p 0.05; Figs. 3 and 4).
All the previous comparisons (between groups and between genders within the same group) exhibited large effect sizes
(Cohen’s d ranged from 0.8 to 2.0).
[()TD$FIG]
Fig. 2. Tanner stage-, height- and weight-adjusted fat and lean masses from the whole body, trunk, upper and lower limbs, in males with and without Down
syndrome; *p 0.05.
-95-
[()TD$FIG]
1690
Fig. 3. Tanner stage-, height- and weight-adjusted fat and lean masses from the whole body, trunk, upper and lower limbs, in males and females with Down
syndrome; #p 0.05 between sexes within the same group.
4. Discussion
Although some previous studies have evaluated body composition in adults with DS using either DXA or ADP (Baptista
et al., 2005; Usera et al., 2005), to our knowledge, this is the first study that includes body composition assessment in
children and adolescents with DS using DXA, ADP and WC at the same time. The main finding of the present study is that,
despite similar values of WC, BMI and %BF (both with DXA and ADP) between populations with and without DS, different
distributions of fat and lean masses were present. Moreover, our results shown that the sexual dimorphism present in the
population with DS was similar to that present in the population without DS.
4.1. Waist circumference, BMI, total and regional adiposity in DS children and adolescents
Most epidemiological studies use anthropometric measurements (WC and BMI) to assess body composition, because it is
the most feasible and economic method when large samples need to be assessed (Moreno et al., 2006; Vicente-Rodriguez
et al., 2008). However, more sophisticated body composition methods such as ADP or DXA are required in order to minimize
the error of measurement and increase the body composition-related data that can be obtained. Regional fat distribution
may have even more relevant implications for health than the %BF or the total amount of body fat; in fact, visceral fat or the
accumulation of intra-abdominal adipose tissue increases cardiovascular risk (Kissebah & Krakower, 1994) and is negatively
associated with muscular and cardiorespiratory fitness (Moliner-Urdiales et al., 2011). Little is known concerning these
-96-
[()TD$FIG]
1691
Fig. 4. Tanner stage-, height- and weight-adjusted fat and lean masses from the whole body, trunk, upper and lower limbs, in males and females without
Down syndrome; #p 0.05 between sexes within the same group.
factors in children and adolescents with DS. In the present study, WC, BMI and %BF were similar between groups with and
without DS (also separately by gender); however, different fat and lean mass distributions were present. This latter
observation indicates that in this population, especially for females, a more accurate assessment of body soft tissue is needed
in order to detect those children with increased health risk.
Previous studies in adult females with DS showed that higher levels of fat compared to females without DS were found
(Baptista et al., 2005). Moreover, lower levels of lean mass were also present in both males and females with DS (Baptista
et al., 2005; Guijarro et al., 2008). Accordingly, in our study the increase in truncal fat in females, but not in males, with DS
might indicate a higher risk of metabolic syndrome and cardiovascular disease in this group (Despres & Lemieux, 2006). On
the other hand, males with DS showed higher total and regional (both in lower and upper limbs) fat masses compared to
their peers without DS. Furthermore, lower total and regional (lower limbs) lean masses were also present in males with DS
which is also considered a cardiovascular risk factor (Ortega et al., 2005, 2008). Additionally, the lower lean mass observed
might partly explain the lower strength that is commonly present in this population (Guerra-Balic, Cuadrado-Mateos,
Geronimo-Blasco, & Fernhall, 2000; Mercer & Lewis, 2001; Morris, Vaughan, & Vaccaro, 1982; Pitetti, Climstein, Mays, &
Barrett, 1992), although further research is needed in this regard.
Our results in children and adolescents are in line with the studies mentioned for adults, as shown by the fact that an
excess of adiposity, along with lower lean mass, especially in the lower limbs, was found in both males and females with DS
-97-
1692
(Baptista et al., 2005; Guijarro et al., 2008). The excess of fat mass at the trunk level present in females with DS is an
interesting finding that might have special clinical relevance, due to the associated increase in the risk of cardiovascular
diseases. As previously described by Bronks and Parker (1985), excessive fat mass accumulation in populations with DS most
likely starts prior to adulthood and, consequently, would be better treated earlier in life.
4.2. Sexual dimorphism in children and adolescents with DS
In a previous study in adults Baptista et al. (2005) observed higher levels of fat mass and lower levels of lean mass in
females compared with males with DS, as normally occurs in populations without DS. Our study shows that these differences
are already detectable in children and adolescents. Although some data indicate that an unusual sexual dimorphism in
children and adolescents with DS in relation to bone mass could be present in this population (González-Agüero, VicenteRodriguez, Moreno, & Casajús, in press), fat and lean masses seem to have a common sexual differentiation. We found higher
levels of fat mass and lower levels of lean mass in females, compared with males in all the studied regions in the group with
DS, similar to what occurred in the group without DS.
The large effect size observed in the differences in fat and lean masses between children and adolescents with and
without DS, and also between sexes within the same group indicate substantial biological magnitude of the results
(Nakagawa & Cuthill, 2007).
4.3. Limitations and strengths of the study
Due to the design of the study, the nature of the association between body composition and DS condition cannot be
established. In future work, this study will benefit from longitudinal investigation in order to assess changes in body
composition in this specific population.
Although the number of participants and, as a consequence the power of the study, was limited, to our knowledge this is
the largest sample of male and female children and adolescents with DS that has been included in a single study to date
(González-Agüero et al., 2010). Moreover, the fact that two different reference body composition methods (DXA and ADP),
and a good anthropometric predictor for metabolic syndrome (WC) were included adds value to the present study. Finally,
the large effect size observed with Cohen’s d statistics demonstrates the consistency of our data.
5. Conclusions
The current investigation provides evidence that children and adolescents with DS have higher levels of total and regional
fat mass than their counterparts without DS. Furthermore, BMI, WC and %BF seem not to be accurate enough to detect an
excess of adiposity in this population. As a consequence, more precise studies of the body composition in this specific
population are required, with particular attention being paid in evaluating regional adiposity levels and the implications for
future health. Similar sexual dimorphism in fat and lean compartments between youths with DS and (age- and sex-matched)
youths without DS was found.
Further studies assessing how other factors, such as physical activity, sedentary time, physical fitness or diet, can affect fat
and lean mass development during puberty will be key in helping us to understand the importance of lifestyle for the
accumulation of fat mass in populations with DS, since its occurrence in populations without DS has already been well
documented (Ara, Moreno, Leiva, Gutin, & Casajus, 2007; Ara et al., 2004, 2006; Vicente-Rodriguez et al., 2008).
Acknowledgments
The authors want to thank all the children and their parents that participated in the study for their understanding and
dedication to the project. Special thanks are given to Fundación Down Zaragoza and Special Olympics Aragon for their
support. We also thank Scott G Mitchell from the University of Glasgow and Steven J James for his work of reviewing the
English style and grammar, and Paula Velasco from the University of Zaragoza for her great technical assistance. This work
was supported by Gobierno de Aragón (Proyecto PM 17/2007) and Ministerio de Ciencia e Innovación de España (Red de
investigación en ejercicio fı́sico y salud para poblaciones especiales-EXERNET-DEP2005-00046/ACTI). These authors declare
that they have no conflicts of interest that may affect the contents of this work.
References
Angelopoulou, N., Souftas, V., Sakadamis, A., & Mandroukas, K. (1999). Bone mineral density in adults with Down’s syndrome. European Radiology, 9, 648–651.
Ara, I., Moreno, L. A., Leiva, M. T., Gutin, B., & Casajus, J. A. (2007). Adiposity, physical activity, and physical fitness among children from Aragon, Spain. Obesity
(Silver Spring), 15, 1918–1924.
Ara, I., Vicente-Rodriguez, G., Jimenez-Ramirez, J., Dorado, C., Serrano-Sanchez, J. A., & Calbet, J. A. (2004). Regular participation in sports is associated with
enhanced physical fitness and lower fat mass in prepubertal boys. International Journal of Obesity and Related Metabolic Disorders: Journal of the International
Association for the Study of the Obesity, 28, 1585–1593.
Ara, I., Vicente-Rodriguez, G., Perez-Gomez, J., Jimenez-Ramirez, J., Serrano-Sanchez, J. A., Dorado, C., et al. (2006). Influence of extracurricular sport activities on
body composition and physical fitness in boys: A 3-year longitudinal study. International Journal of Obesity (London), 30, 1062–1071.
Baptista, F., Varela, A., & Sardinha, L. B. (2005). Bone mineral mass in males and females with and without Down syndrome. Osteoporosis International, 16, 380–388.
-98-
1693
Bittles, A. H., & Glasson, E. J. (2004). Clinical, social, and ethical implications of changing life expectancy in Down syndrome. Developmental Medicine & Child
Neurology, 46, 282–286.
Bland, J. M., & Altman, D. G. (1986). Statistical methods for assessing agreement between two methods of clinical measurement. Lancet, 1, 307–310.
Bronks, R., & Parker, A. W. (1985). Anthropometric observation of adults with Down syndrome. American Journal of Mental Deficiency, 90, 110–113.
Calbet, J. A., Perez-Gomez, J., Vicente-Rodriguez, G., Ara, I., Olmedillas, H., Chavarren, J., et al. (2008). Look before you leap: On the issue of muscle mass assessment
by dual-energy X-ray absorptiometry (reply to Jordan Robert Moon comments). European Journal of Applied Physiology, 104, 587–588.
Chumlea, W. C., & Cronk, C. E. (1981). Overweight among children with trisomy. Journal of Mental Deficiency Research, 25(4), 275–280.
Coppus, A. M., Evenhuis, H. M., Verberne, G. J., Visser, F. E., Oostra, B. A., Eikelenboom, P., et al. (2008). Survival in elderly persons with Down syndrome. Journal of
the American Geriatric Society, 56, 2311–2316.
Cronk, C. E., Chumlea, W. C., & Roche, A. F. (1985). Assessment of overweight children with trisomy 21. American Journal of Mental Deficiency, 89, 433–436.
Despres, J. P., & Lemieux, I. (2006). Abdominal obesity and metabolic syndrome. Nature, 444, 881–887.
Dietz, W. H. (1998). Health consequences of obesity in youth: Childhood predictors of adult disease. Pediatrics, 101, 518–525.
Draheim, C. C., McCubbin, J. A., & Williams, D. P. (2002). Differences in cardiovascular disease risk between nondiabetic adults with mental retardation with and
without Down syndrome. American Journal of Mental Retardation, 107, 201–211.
Ebbeling, C. B., Pawlak, D. B., & Ludwig, D. S. (2002). Childhood obesity: Public-health crisis, common sense cure. Lancet, 360, 473–482.
Fields, D. A., & Goran, M. I. (2000). Body composition techniques and the four-compartment model in children. Journal of Applied Physiology, 89, 613–620.
Glasson, E. J., Sullivan, S. G., Hussain, R., Petterson, B. A., Montgomery, P. D., & Bittles, A. H. (2002). The changing survival profile of people with Down’s syndrome:
Implications for genetic counselling. Clinical Genetics, 62, 390–393.
González-Agüero, A., Vicente-Rodriguez, G., Moreno, L. A., & Casajús, J. A. Bone mass in male and female children and adolescents with Down syndrome.
Osteoporosis International, in press, doi:10.1007/s00198-010-1443-7.
González-Agüero, A., Vicente-Rodriguez, G., Moreno, L. A., Guerra-Balic, M., Ara, I., & Casajus, J. A. (2010). Health-related physical fitness in children and
adolescents with Down syndrome and response to training. Scandinavian Journal of Medicine and Science in Sports, 20, 716–724.
Guerra-Balic, M., Cuadrado-Mateos, E., Geronimo-Blasco, C., & Fernhall, B. (2000). Physical fitness levels of physically active and sedentary adults with Down
syndrome. Adapted Physical Activity Quarterly, 17, 310–321.
Guijarro, M., Valero, C., Paule, B., Gonzalez-Macias, J., & Riancho, J. A. (2008). Bone mass in young adults with Down syndrome. Journal of Intellectual Disability
Research, 52, 182–189.
Gutin, B., Litaker, M., Islam, S., Manos, T., Smith, C., & Treiber, F. (1996). Body-composition measurement in 9-11-y-old children by dual-energy X-ray
absorptiometry, skinfold-thickness measurements, and bioimpedance analysis. American Journal of Clinical Nutrition, 63, 287–292.
Hawn, J., Rice, C., Nichols, H., & McDermott, S. (2009). Overweight and obesity among children with Down syndrome: A descriptive study of children attending a
Down syndrome clinic in South Carolina. Journal of the South Carolina Medical Association, 105, 64–68.
Kissebah, A. H., & Krakower, G. R. (1994). Regional adiposity and morbidity. Physiological Reviews, 74, 761–811.
Krouwer, J. S. (2008). Why Bland–Altman plots should use X, not (Y + X)/2 when X is a reference method. Statistics in Medicine, 27, 778–780.
Luke, A., Sutton, M., Schoeller, D. A., & Roizen, N. J. (1996). Nutrient intake and obesity in prepubescent children with Down syndrome. Journal of the American
Dietetic Association, 96, 1262–1267.
Maffeis, C., & Tato, L. (2001). Long-term effects of childhood obesity on morbidity and mortality. Hormone Research, 55(Suppl. 1), 42–45.
Mercer, V. S., & Lewis, C. L. (2001). Hip abductor and knee extensor muscle strength of children with and without Down syndrome. Pediatric Physical Therapy, 13,
18–26.
Moliner-Urdiales, D., Ruiz, J. R., Vicente-Rodriguez, G., Ortega, F. B., Rey-Lopez, J. P., Espana-Romero, V., et al. (2011). Associations of muscular and
cardiorespiratory fitness with total and central body fat in adolescents; The HELENA Study. British Journal of Sports Medicine, 45, 101–108.
Moreno, L. A., Mesana, M. I., Gonzalez-Gross, M., Gil, C. M., Fleta, J., Warnberg, J., et al. (2006). Anthropometric body fat composition reference values in Spanish
adolescents, The AVENA Study. European Journal of Clinical Nutrition, 60, 191–196.
Moreno, L. A., Pineda, I., Rodriguez, G., Fleta, J., Sarria, A., & Bueno, M. (2002). Waist circumference for the screening of the metabolic syndrome in children. Acta
Paediatrica, 91, 1307–1312.
Morris, A. F., Vaughan, S. E., & Vaccaro, P. (1982). Measurements of neuromuscular tone and strength in Down’s syndrome children. Journal of Mental Deficiency
Research, 26, 41–46.
Nakagawa, S., & Cuthill, I. C. (2007). Effect size, confidence interval and statistical significance: A practical guide for biologists. Biological Reviews of the Cambridge
Philosophical Society, 82, 591–605.
Ortega, F. B., Ruiz, J. R., Castillo, M. J., Moreno, L. A., Gonzalez-Gross, M., Warnberg, J., et al. (2005). Low level of physical fitness in Spanish adolescents. Relevance
for future cardiovascular health (AVENA study). Revista Española de Cardiologıá, 58, 898–909.
Ortega, F. B., Ruiz, J. R., Castillo, M. J., & Sjostrom, M. (2008). Physical fitness in childhood and adolescence: A powerful marker of health. International Journal of
Obesity (London), 32, 1–11.
Parker, L., Reilly, J. J., Slater, C., Wells, J. C., & Pitsiladis, Y. (2003). Validity of six field and laboratory methods for measurement of body composition in boys. Obesity
Research, 11, 852–858.
Pitetti, K. H., Climstein, M., Mays, M. J., & Barrett, P. J. (1992). Isokinetic arm and leg strength of adults with Down syndrome: A comparative study. Archives of
Physical Medicine and Rehabilitation, 73, 847–850.
Prasher, V. P. (1993). Down’s syndrome, longevity, and Alzheimer’s disease. British Journal of Psychiatry, 162, 711.
Rubin, S. S., Rimmer, J. H., Chicoine, B., Braddock, D., & McGuire, D. E. (1998). Overweight prevalence in persons with Down syndrome. Mental Retardation, 36, 175–
181.
Siri, W. E. (1961). Body composition from fluid spaces and density: Analysis of methods. In J. Brozek & A. Henzchel (Eds.), Techniques for measuring body
composition (pp. 224–244). Washington: National Academy of Sciences.
Slemenda, C. W., Miller, J. Z., Hui, S. L., Reister, T. K., & Johnston, C. C., Jr. (1991). Role of physical activity in the development of skeletal mass in children. Journal of
Bone and Mineral Research, 6, 1227–1233.
Smith, D. S. (2001). Health care management of adults with Down syndrome. American Family Physician, 64, 1031–1038.
Svendsen, O. L., Haarbo, J., Hassager, C., & Christiansen, C. (1993). Accuracy of measurements of body composition by dual-energy X-ray absorptiometry in vivo.
American Journal of Clinical Nutrition, 57, 605–608.
Tanner, J. M., & Whitehouse, R. H. (1976). Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Archives of
Disease in Childhood, 51, 170–179.
Thase, M. E. (1982). Longevity and mortality in Down’s syndrome. Journal of Mental Deficiency Research, 26, 177–192.
Usera, P. C., Foley, J. T., & Yun, J. (2005). Cross-validation of field based assessments of body composition for individuals with Down syndrome. Adapted Physical
Activity Quarterly, 22, 198–206.
Vicente-Rodriguez, G., Rey-Lopez, J. P., Martin-Matillas, M., Moreno, L. A., Warnberg, J., Redondo, C., et al. (2008). Television watching, videogames, and excess of
body fat in Spanish adolescents: The AVENA study. Nutrition, 24, 654–662.
-99-
-100-
Artículo original
Dimorfismo sexual en grasa corporal
en adolescentes con síndrome de Down
Alejandro González-Agüero1,2 , Germán Vicente-Rodríguez1,2 ,
Luis A. Moreno1,3, José A. Casajús1,2
1
Grupo GENUD. Universidad de Zaragoza
2
Facultad de Ciencias de la Salud y del Deporte. Universidad de Zaragoza. Huesca
3
Escuela Universitaria de Ciencias de la Salud. Universidad de Zaragoza
Introducción: Las personas con síndrome
de Down (SD) tienen un índice de masa corporal (IMC) y un porcentaje de grasa corporal
(%GC) más altos que personas sin SD de su
misma edad y sexo. La composición corporal
de esta población durante la adolescencia es
prácticamente desconocida.
Objetivo: Valorar el dimorfismo sexual de
masa grasa en adolescentes con SD.
Material y métodos: 31 adolescentes (12-19
años; 13 chicas y 18 chicos) con SD tomaron
parte en este estudio. Se midió peso, talla,
pliegues cutáneos (bíceps, tríceps, subescapular, suprailíaco, muslo anterior, abdominal
y pierna medial) y perímetros de cintura y cadera. Se calculó el IMC, %GC, índice cintura
cadera (ICC), sumatorio de 6 pliegues (∑6P),
la proporción de adolescentes con sobrepeso + obesidad y la puntuación Z-score de IMC
para cada participante. Se analizaron estadísticamente los datos mediante pruebas t
de Student.
Resultados: Las chicas con SD obtuvieron
valores más altos que los chicos con SD en
IMC, %GC, ∑6P y en 5 de los 7 pliegues (todos
p < 0,05). También observamos una mayor
proporción de sobrepeso + obesidad en las
chicas (50% vs. 21%).
Discusión: El dimorfismo sexual observado
en esta muestra de adolescentes con SD es
similar al descrito previamente en población
adolescente sin SD. Sin embargo, los valores
de IMC, %GC y la proporción de adolescentes
con sobrepeso + obesidad en las chicas con SD
son superiores a los de las chicas sin SD de su
misma edad. El 40% de los participantes tuvieron un Z-score de IMC por encima de 1 punto.
Palabras clave: Composición corporal. Trisomía 21. Porcentaje graso. ISAK.
Sexual body fat dimorphism in
adolescents with Down syndrome
Introduction: Persons with Down syndrome
(DS) have higher body mass index (BMI) and
body fat percentage (%BF) than age- and sexmatched persons without DS. Body composition of this population during adolescence is
almost unknown.
Aim: To study fat mass sexual dimorphism in
DS adolescents.
Material and methods: 31 adolescents
(12-19 years; 13 girls and 18 boys) with DS
INTRODUCCIÓN
El síndrome de Down (SD) es una condición genética causada
por anormalidades en el cromosoma 21 y caracterizada por una
discapacidad intelectual de gradación variable (1). La incidencia
214
Correspondencia:
Dr. José Antonio Casajús
c/ Corona de Aragón, 42. Edificio Cervantes. 2.ª planta
50009 Zaragoza
Correo electrónico: [email protected]
participated in this study. Weight, height,
skinfold thicknesses (biceps, triceps, subscapular, iliac crest, front thigh, abdominal
and medial calf skinfold) and waist and hip
circumferences were measured. BMI, %BF,
waist/hip index (WHI), 6 skinfolds addition
(∑6S), the proportion of adolescents with
overweight + obesity and Z-score for BMI
were calculated. The data were statistically
analysed with Student’s t tests.
Results: Girls with DS showed higher values than the boys with DS in BMI, %BF, ∑6S,
in 5 of the 7 skinfolds (all p < 0,05). Also
higher proportion of adolescents with overweight + obesity was observed in the girls
compared to boys (50% vs. 21%).
Discussion: The sexual dimorphism observed
in this sample of DS adolescents is similar than
the previously described in adolescent population without DS. However, the values for BMI,
%BF and the proportion of overweight + obesity in the girls are higher compared with the agematched girls without DS. Forty per cent of the
sample showed Z-score for BMI over 1 point.
Key words: Body composition. Trisomy 21. Fat
percentage. ISAK.
del SD es de aproximadamente 1 de 700 a 1 de 1.000 nacidos
vivos (2). Se han descrito más de 80 características clínicas en
individuos con SD, incluidos problemas cardiacos congénitos,
presentes aproximadamente en el 40% de los individuos(1). Su
esperanza de vida ha aumentado considerablemente: desde los
Revista Española de Obesidad • Vol. 8 • Núm. 1 • Marzo 2010 (xxx-xxx)
-101-
A. González-Agüero, G. Vicente-Rodríguez, L.A. Moreno, J.A. Casajús
9 años de media que tenían en 1929(3) hasta 55 años o más en
la actualidad (4).
Debido al aumento de su esperanza de vida, algunos problemas asociados a la población con SD, como el exceso de peso y
de grasa corporal, los bajos niveles de densidad mineral ósea o
el envejecimiento celular están empezando a ser estudiados en
profundidad, ya que las enfermedades asociadas disminuyen
la calidad de vida de estas personas.
En numerosos estudios se ha observado que niños, adolescentes y adultos con SD tienen un índice de masa corporal
(IMC) y un porcentaje de grasa corporal (%GC) más altos que
la población sin SD (5,6). El exceso de grasa constituye un factor de riesgo asociado con problemas metabólicos en cualquier
tipo de población (7,8). En personas con SD, el exceso de grasa
puede influir de manera negativa en algunas de sus características propias, como defectos cardiacos congénitos, hipotonía muscular o bajos niveles de masa ósea (1,9,10). La temprana
detección del sobrepeso u obesidad en estas personas podría
mejorar las expectativas de tratamiento.
Algunos estudios atribuyen este exceso de peso y/o masa
grasa a una predisposición genética que provoca niveles más
bajos de secreción de leptina (11), factores fisiológicos como la
hipotonía muscular(12) o la disfunción del tiroides que acompañan al SD(13). Otros han descrito a los niños y adolescentes
con SD como menos activos que sus homólogos sin SD (14,15); y
se ha podido comprobar que el entrenamiento físico mejora la
composición corporal en personas con SD (16-18). Esto nos está
indicando que la falta de actividad física que caracteriza a esta
población podría motivar también el excesivo almacenamiento de grasa. Aunque existen varias hipótesis, las causas del
exceso de grasa en estas personas no han sido todavía descritas
con certeza.
En población general, existe un claro dimorfismo sexual relacionado con la composición corporal desde el momento del
nacimiento, que tiene un drástico aumento durante la pubertad,
y que continúa durante la edad adulta aunque se suaviza (19).
El dimorfismo sexual en composición corporal de adolescentes con SD no se ha estudiado. Estudios previos realizados en
nuestro laboratorio indican un dimorfismo sexual diferente al
de los adolescentes de su misma edad sin SD en otros compartimentos de la composición corporal (por ejemplo, masa ósea;
A. González-Agüero et al., datos no publicados), lo que sugiere que podría ocurrir lo mismo con la grasa corporal.
En población sin SD, durante la adolescencia, las chicas tienden a acumular más grasa que los chicos(20), sin que esto afecte
al IMC(21,22). Sería, por tanto, interesante comprobar si, como
ocurre en masa ósea, los adolescentes con SD tienen patrones
específicos de desarrollo de la masa grasa.
Vol. 8 • Núm. 1 • Marzo 2010
-102-
Por todo esto, los objetivos de este estudio son obtener datos
antropométricos de adolescentes con SD y valorar si su dimorfismo sexual en masa grasa es similar al descrito previamente
para adolescentes sin SD.
MÉTODOS
Muestra
La muestra del estudio está compuesta por 31 adolescentes (1219 años; 13 chicas y 18 chicos) aragoneses con SD. Se recogió
información sobre enfermedades y operaciones anteriores y
estancias en hospitales. También se recogió información sobre
actividad física actual, años de práctica y nivel. Ambos, padres
y niños fueron informados sobre el objetivo y procedimientos
del estudio, así como de los posibles riesgos y beneficios del
mismo. Se obtuvo un consentimiento informado de todos los
adolescentes y de sus padres o tutores.
El estudio se realizó de acuerdo con la Declaración de Helsinki de 1961 (revisión de Edimburgo en 2000) y fue aprobado por
el Comité de Ética en Investigación del Gobierno de Aragón.
Medidas antropométricas
Para la determinación de las medidas antropométricas se utilizaron las normas, recomendaciones y técnicas de medición de
la Sociedad Internacional de Avances en Cineantropometría
(ISAK, International Society for the Advancement of Kinanthropometry)(23). Todas las mediciones fueron realizadas por el mismo
antropometrista (nivel 2 ISAK), cuyo error técnico de medición
está dentro de los límites recomendados por ISAK. A continuación se detallan las medidas tomadas y material utilizado.
Medidas básicas
Se midieron paso y talla con precisión 0,1 cm y 0,1 kg respectivamente. Tallímetro KaWe (Asperg, Alemania); balanza
SECA (Hamburgo, Alemania).
Pliegues cutáneos
Se midieron los pliegues bíceps, tríceps, subescapular, supraíliaco, abdominal, muslo anterior y pierna medial. Compás de pliegues, precisión 0,2 mm, Holtain Ltd. (Crosswell, Reino Unido).
Perímetros
Se midieron perímetro de cintura y de cadera. Cinta antropométrica, precisión 1 mm, Rosscraft.
215
Tabla 1. EDAD Y CARACTERÍSTICAS ANTROPOMÉTRICAS EN LOS CHICOS
Y CHICAS CON SD ESTUDIADOS Y DIFERENCIAS ENTRE SEXOS
Variable
Edad (años)
Chicas (n=13)
Chicos (n=18)
Media
±
DT
Media
±
DT
16,72
±
2,54
16,43
±
2,46
con el paquete estadístico SPSS (versión 15.0 para Windows). Se tomó como nivel de significación de p < 0,05.
p
0,754
Peso (kg)
49,15
±
9,54
50,56
±
10,56
0,707
Talla (cm)
143,00*
±
7,18
153,05
±
8,01
0,001
RESULTADOS
En la Tabla 1 se muestran los datos de
edad, antropométricos básicos y %GC
23,89*
±
3,47
21,39
±
2,99
0,040
IMC (kg/m2)
de los chicos y chicas adolescentes
Normopeso/sobrepeso/obesidad (%)
50/50/0
79/21/0
con SD. Los chicos con SD resultaron
Perímetro de cintura (cm)
78,8
±
8,8
74,6
±
9,4
0,218
10 cm más altos que las chicas con SD;
y las chicas obtuvieron valores más elePerímetro de cadera (cm)
92,2
±
9,3
85,9
±
9,3
0,079
vados en %GC e IMC (todas p < 0,05).
ICC
0,86
± 0,06
0,87
±
0,05
0,563
Un 50% de las chicas, frente a un 21%
Porcentaje de grasa
26,95*
±
7,51
19,71
±
6,43
0,010
de los chicos, fueron clasificadas con
Z-score IMC
0,82
± 0,84
0,17
±
0,91
0,052
sobrepeso. No encontramos diferenEdad, medidas antropométricas básicas y porcentaje de grasa entre chicos y chicas adolescentes con SD. *p < 0,05;
cias significativas en edad, peso, períDT = desviación típica; IMC = índice de masa corporal; ICC = índice cintura/cadera.
metro de cintura, perímetro de cadera
ni ICC. El 40% de los participantes (8
Cálculos posteriores
chicas y 4 chicos) obtuvieron un Z-score mayor de 1 punto.
El IMC se calculó como kilogramos de peso divididos por la
La Figura 1 muestra el perfil de pliegues y el ∑6P. Se obsertalla (m) al cuadrado. Teniendo en cuenta el IMC, sexo y edad
van valores de entre un 36% y un 83% más altos en los pliegues
se dividió a los adolescentes en tres grupos: “normopeso”, “sobíceps, tríceps, subescapular, muslo anterior y pierna medial, y
brepeso” y “obesidad” de acuerdo con los criterios publicados
también en el ∑6P (29%) de las chicas con SD comparadas con
por Cole et al.(24) para menores de 18 años. Se calculó el valor
los chicos (todos p < 0,05).
de Z-score de IMC para cada adolescente tomando como referencia los valores de la Organización Mundial de la Salud
DISCUSIÓN
de 2007 para cada edad y sexo (25,26). El índice cintura-cadera
(ICC) se calculó dividendo el perímetro de la cintura (cm) por
El hallazgo principal de este estudio es que en este grupo de
el perímetro de la cadera (cm). Se obtuvo también el sumatorio
adolescentes con SD las chicas tienen un %GC y un IMC más
de 6 pliegues cutáneos (∑6P): tríceps, subescapular, supraialtos que los chicos. Sin embargo, no encontramos diferencias
líaco, muslo anterior, pierna medial y abdominal. Para hallar
en los perímetros de cadera, cintura ni en el ICC, por lo que pael porcentaje de grasa corporal seguimos las indicaciones de
rece que estas variables no muestran un dimorfismo sexual en
Rimmer et al. (27) para adultos con discapacidad intelectual;
calculando la densidad mediante las fórmulas de Durnin y
adolescentes con SD, al contrario que en la población sin SD.
Womersley(28) para los chicos y de Jackson y Pollock(29) para
Ningún trabajo hasta la fecha había estudiado el dimorfismo
(30)
las chicas, y aplicando después la fórmula de Siri et al. para
sexual en la grasa corporal de adolescentes con SD. Sin embarhallar el %GC.
go, en adolescentes sin SD está bien documentado que las chicas
tienen un %GC y un ∑6P más alto que los chicos(20,31,32), y que el
IMC es semejante en ambos sexos(21,22,31,33). A tenor de nuestros
Análisis estadístico
resultados, parece que los adolescentes con SD de nuestro estudio tienen un dimorfismo sexual en masa grasa similar al detecLos datos se muestran como media ± desviación típica. Todas
tado en adolescentes sin SD, aunque los perímetros de cadera y
las variables mostraron una distribución normal. Se realizaron
cintura podrían ser menos sensibles en esta población.
pruebas t de Student para estudiar las diferencias en edad, peso,
Valores de referencia en niños y adolescentes españoles sin
talla, IMC, ICC, pliegues cutáneos, ∑6P, %GC y puntuación ZSD muestran un IMC (kg/m 2) que varía entre 20,61 y 22,91
en chicos, y entre 21,33 y 21,72 en chicas; un %GC con un
score de IMC entre chicos y chicas. Los análisis se realizaron
216
Vol. 8 • Núm. 1 • Marzo 2010
-103-
Chicas
200
Chicos
180
Abdominal
160
*
Pierna medial
*
*
Muslo anterior
140
120
Suprailíaco
100
Subescapular
80
*
Tríceps
60
*
Bíceps
40
*
5
10
20
15
20
25
30
35
40
45
0
mm
Figura 1. Pliegues cutáneos y sumatorio de pliegues en chicos y chicas adolescentes con síndrome de Down. *p < 0,05.
rango de 18,28-20,79 en chicos y de 24,89-26,30 en chicas; un
∑6P (mm) con un rango de 67,8-80,29 en chicos y de 96,94102,31 en chicas y una proporción de adolescentes con sobrepeso + obesidad de un 25,69% en chicos y un 19,13% en chicas (22,32). Comparando estos datos con los de nuestro estudio
observamos que el IMC de los chicos con SD está dentro del
rango establecido en población sin SD, pero el de las chicas
está muy por encima de ese rango. La proporción de adolescentes con sobrepeso + obesidad alcanza en los chicos con SD
un porcentaje menor que en población sin SD y en las chicas
sobrepasa considerablemente ese porcentaje. El ∑6P es mayor
tanto en chicas como en chicos con SD comparado con el rango de referencia indicado para población sin SD, siendo el de
las chicas mucho más elevado. El %GC de los chicos con SD
entra dentro del margen establecido en población sin SD y el
de las chicas está muy por encima de ese margen.
El grupo de adolescentes con SD incluidos en el estudio son
muy activos, y gran número de ellos toman parte desde hace
años en un programa de actividad física semanal (34). A pesar
de esto, el IMC, el %GC y la proporción de adolescentes con
sobrepeso y obesidad en el grupo de chicas se encuentran muy
por encima de los valores de referencia para su misma edad y
sexo sin SD. Además, un 40% de la muestra tiene un Z-score
de IMC mayor de 1 punto.
Sería conveniente estudiar la posible relación entre composición corporal, condición física y niveles de actividad física en
Vol. 8 • Núm. 1 • Marzo 2010
-104-
adolescentes con SD y valorar si es de la misma magnitud que
en la población sin SD(35).
El %GC y la proporción de adolescentes con sobrepeso + obesidad en los chicos de nuestro estudio se encuentran
dentro del rango de referencia para su misma edad y sexo sin
SD y, sin embargo, el ∑6P se encuentra considerablemente por
encima. Esto nos hace pensar que tal vez los puntos de corte de
Cole et al.(24) no sean los más adecuados para este estudio, ya
que no son específicos para población pediátrica con SD, pero
se adecuan más a los sujetos de nuestro estudio al estar diseñados para niños y adolescentes de 2 a 18 años. Por otra parte, las
ecuaciones utilizadas para hallar el %GC tampoco son específicas para esta población. Sin embargo, decidimos usarlas, por
ser la población que más se ajusta a la de nuestro estudio.
Sería interesante, por lo tanto, la realización de nuevos estudios con métodos de referencia de valoración de la masa grasa, para elaborar puntos de corte específicos para sobrepeso
y obesidad, y también fórmulas para el cálculo del %GC con
pliegues cutáneos en población pediátrica con SD.
En conclusión, se puede considerar que esta muestra de adolescentes con SD tiene un dimorfismo sexual en masa grasa similar al observado en adolescentes sin SD. Sin embargo, pese a
que los valores de IMC, %GC y proporción de sobrepeso + obesidad en los chicos son similares a los descritos en población
sin SD, las chicas tienen unos valores muy superiores para estas
variables, y el Z-score de IMC de ambos grupos es positivo,
217
estando el 40% de la muestra por encima de 1 punto. Por todo
esto, se hace evidente la necesidad de valores de referencia específicos para este grupo de población, tanto en %GC como en
puntos de corte, para definir sobrepeso y obesidad.
AGRADECIMIENTOS
Los autores agradecen a todos los participantes y a sus padres el esfuerzo realizado. También nos gustaría agradecer a
Paula Velasco Martínez, de la Universidad de Zaragoza, su
inestimable ayuda en la realización de las antropometrías.
Una parte sustancial de los participantes procedían de Fundación Down Zaragoza y Special Olympics Aragón; también
nos gustaría agradecer a estas instituciones su participación
en el estudio. Este estudio está financiado por el Gobierno de
Aragón (proyecto PM 17/2007) y por el Ministerio de Ciencia e Innovación de España (Red de investigación en ejercicio físico y salud para poblaciones especiales –EXERNET–
DEP2005-00046/ACTI).
BIBLIOGRAFÍA
1. Pueschel SM. Clinical aspects of Down syndrome from infancy to adulthood. Am J Med Genet Suppl 1990; 7: 52-6.
2. Roizen NJ, Patterson D. Down’s syndrome. Lancet 2003; 361
(9365): 1281-9.
3. Bittles AH, Glasson EJ. Clinical, social, and ethical implications of changing life expectancy in Down syndrome. Dev
Med Child Neurol 2004; 46 (4): 282-6.
4. Glasson EJ, Sullivan SG, Hussain R, Petterson BA, Montgomery PD, Bittles AH. The changing survival profile of people
with Down’s syndrome: implications for genetic counselling.
Clin Genet 2002; 62 (5): 390-3.
5. Bronks R, Parker AW. Anthropometric observation of adults
with Down syndrome. Am J Ment Defic 1985; 90 (1): 110-3.
6. Chumlea WC, Cronk CE. Overweight among children with
trisomy. J Ment Defic Res 1981; 25 (Pt 4): 275-80.
7. Dietz WH. Health consequences of obesity in youth: childhood predictors of adult disease. Pediatrics 1998; 101 (3 Pt
2): 518-25.
8. Ebbeling CB, Pawlak DB, Ludwig DS. Childhood obesity:
public-health crisis, common sense cure. Lancet 2002; 360
(9331): 473-82.
9. Baptista F, Varela A, Sardinha LB. Bone mineral mass in
males and females with and without Down syndrome. Osteoporos Int 2005; 16 (4): 380-8.
218
10. Morris AF, Vaughan SE, Vaccaro P. Measurements of neuromuscular tone and strength in Down’s syndrome children. J
Ment Defic Res 1982; 26 (Pt 1): 41-6.
11. Proto C, Romualdi D, Cento RM, Romano C, Campagna G,
Lanzone A. Free and total leptin serum levels and soluble
leptin receptors levels in two models of genetic obesity: the
Prader-Willi and the Down syndromes. Metabolism 2007; 56
(8): 1076-80.
12. Winnick J. Adapted Physical Education and Sport. Champaign, Illinois: Human Kinetics; 1995.
13. Thiel R, Fowkes SW. Down syndrome and thyroid dysfunction: should nutritional support be the first-line treatment?
Med Hypotheses 2007; 69 (4): 809-15.
14. Shields N, Dodd KJ, Abblitt C. Do children with Down syndrome
perform sufficient physical activity to maintain good health? A
pilot study. Adapt Phys Activ Q 2009; 26 (4): 307-20.
15. Sharav T, Bowman T. Dietary practices, physical activity, and
body-mass index in a selected population of Down syndrome
children and their siblings. Clin Pediatr (Phila) 1992; 31 (6):
341-4.
16. Shields N, Taylor NF, Dodd KJ. Effects of a community-based
progressive resistance training program on muscle performance and physical function in adults with Down syndrome:
a randomized controlled trial. Arch Phys Med Rehabil 2008;
89 (7): 1215-20.
17. Ordóñez F, Rosety M, Rosety-Rodríguez M. Influence of
12-week exercise training on fat mass percentage in adolescents with Down syndrome. Med Sci Monit 2006; 12 (10):
CR416-9.
18. Rimmer JH, Heller T, Wang E, Valerio I. Improvements in
physical fitness in adults with Down syndrome. Am J Ment
Retard 2004; 109 (2): 165-74.
19. Wells JC. Sexual dimorphism of body composition. Best Pract
Res Clin Endocrinol Metab 2007; 21 (3): 415-30.
20. Loomba-Albrecht LA, Styne DM. Effect of puberty on body
composition. Curr Opin Endocrinol Diabetes Obes 2009; 16
(1): 10-5.
21. Wells JC. The evolution of human fatness and susceptibility to
obesity: an ethological approach. Biol Rev Camb Philos Soc
2006; 81 (2): 183-205.
22. Moreno LA, Mesana MI, González-Gross M, Gil CM, Ortega
FB, Fleta J, et al. Body fat distribution reference standards in
Spanish adolescents: the AVENA Study. Int J Obes (Lond)
2007; 31 (12): 1798-805.
23. Norton K, Whittingham N, Carter L, Kerr D, Gore C, MarfellJones M. Measurement techniques in anthropometry. En:
Norton K, Olds T (eds.). Antropométrica. Sydney: UNSW;
1996. pp. 22-75.
Vol. 8 • Núm. 1 • Marzo 2010
-105-
24. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity
worldwide: international survey. BMJ 2000; 320 (7244):
1240-3.
25. BMI for age GIRLS; 5 to 19 years (z-scores). World Health
Organization, 2007. (Accessed 30th January, 2010, at http://
www.who.int/growthref/bmifa_girls_5_19years_z.pdf.)
26. BMI for age BOYS; 5 to 19 years (z-scores). World Health
Organization, 2007. (Accessed 30th January, 2010, at http://
www.who.int/growthref/bmifa_boys_5_19years_z.pdf.)
27. Rimmer JH, Kelly LE, Rosentswieg J. Accuracy of anthropometric equations for estimating body composition of mentally
retarded adults. Am J Ment Defic 1987; 91 (6): 626-32.
28. Durnin JV, Womersley J. Body fat assessed from total body
density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years. Br J
Nutr 1974; 32 (1): 77-97.
29. Jackson AS, Pollock ML, Ward A. Generalized equations
for predicting body density of women. Med Sci Sports Exerc
1980; 12 (3): 175-81.
Vol. 8 • Núm. 1 • Marzo 2010
-106-
30. Siri WE. Body composition from fluid spaces and density:
Analysis of methods. En: Brozek J, Henzchel A (eds.). Techniques for Measuring Body Composition. Washington: National Academy of Sciences; 1961. pp. 224-44.
31. Maynard LM, Wisemandle W, Roche AF, Chumlea WC, Guo
SS, Siervogel RM. Childhood body composition in relation to
body mass index. Pediatrics 2001; 107 (2): 344-50.
32. Moreno LA, Mesana MI, González-Gross M, Gil CM, Fleta J,
Warnberg J, et al. Anthropometric body fat composition reference values in Spanish adolescents. The AVENA Study. Eur J
Clin Nutr 2006; 60 (2): 191-6.
33. Shen W, Punyanitya M, Silva AM, Chen J, Gallagher D,
Sardinha LB, et al. Sexual dimorphism of adipose tissue distribution across the lifespan: a cross-sectional whole-body magnetic resonance imaging study. Nutr Metab (Lond) 2009; 6: 17.
34. Casajús JA. Salud, ejercicio físico y síndrome de Down. Zaragoza: Edelvives; 2007.
35. Ara I, Moreno LA, Leiva MT, Gutin B, Casajus JA. Adiposity,
physical activity, and physical fitness among children from
Aragon, Spain. Obesity (Silver Spring) 2007; 15 (8): 1918-24.
219
Biomecánica, 17 (2), 2009, pp. 46-51
Masa muscular, fuerza isométrica y dinámica en
las extremidades inferiores de niños y adolescentes
con síndrome de Down
A. GONZÁLEZ-AGÜERO1,2, M.A. VILLARROYA1,3, G. VICENTE-RODRÍGUEZ1,2, J.A. CASAJÚS1,2.
1
Grupo GENUD (Growth, Exercise, NUtrition and Development).
2
Facultad de Ciencias de la Salud y del Deporte de Huesca, Universidad de Zaragoza.
3
Escuela Universitaria de Ciencias de la Salud, Universidad de Zaragoza.
Resumen
En general se ha observado que las personas con síndrome de Down (SD) tienen valores
inferiores de fuerza muscular comparados con personas sin SD. También existe un déficit de masa
muscular en los adultos con SD comparados con otros sin SD. Sin embargo, ningún estudio hasta
la fecha había evaluado esta masa muscular en población pediátrica. Nuestro estudio pretende
poner de manifiesto si también a edades tempranas existe un déficit de masa muscular y además
relacionar ambos valores. Los niños y adolescentes con y sin SD (15±3 y 14±3 años respectivamente)
de nuestro estudio obtuvieron valores similares de masa muscular ajustada por talla y estadio
puberal, pero el grupo con SD obtuvo valores inferiores de fuerza (p<0.05). Además de esto, el
grupo con SD ejerció menos kilogramos de fuerza por cada kilogramo de masa muscular. Alguna
causa fisiológica o de transmisión podría explicar esta falta de fuerza ya que, al menos en esta
franja de edad no existe un déficit de masa muscular. Deberían incentivarse los programas de
entrenamiento específicos para este tipo de población para comprobar si es posible un incremento
en su fuerza muscular.
Palabras clave: Composición corporal, condición física, trisomía 21, DXA.
Abstract
Generally it has been observed that population with Down syndrome (DS) has lower levels of
muscular strength compared with others without DS. It is also known a deficit between muscular
mass between adults with and without DS. However, there are no studies until the date which
evaluated muscular mass in paediatric populations. Our study pretends to show whether also in
earlier ages it does exist a deficit in the muscular mass and also to relate both values. Children and
adolescents with and without DS (15±3 y 14±3 years respectively) from the study had similar
values of muscular mass adjusted by height and puberal status, but DS group obtained lower
values in all strength parameters. In addition, DS group also performed less kilograms of strength
by kilogram of muscular mass. Some physiological or transmission impairment could explain this
lack of strength as it known that there are not deficit in the muscular mass. Specific and adapted
for this population training programs should be promoted to check whether an enhancement in
their muscular strength is possible.
Keywords: Body composition, physical fitness, trisomy 21, DXA.
Correspondencia:
Dr. José Antonio Casajús
Ed. Cervantes, Calle Corona de Aragón 42, 2a planta
50009, Zaragoza, España
Email: [email protected]
46
-107-
Introducción
El síndrome de Down (SD) es una condición
genética caracterizada por un retraso mental a
diferentes niveles, y está asociada con
anormalidades en el cromosoma 21. Se han descrito
más de 80 características clínicas en individuos con
SD, incluidos problemas cardiacos congénitos,
presentes aproximadamente en el 40% de los
individuos con SD.[1]
Las evidencias científicas[2, 3] sugieren que
algunas de las características del SD pueden
afectar a la práctica de ejercicio, como pueden ser
la hipotonía, hipermovilidad de las articulaciones,
hiperlaxitud de los ligamentos, ligera a moderada
obesidad, sistema respiratorio y cardiovascular
poco desarrollado, estatura más baja (brazos y
piernas cortas en relación al torso). Además
también se ha descrito un equilibrio muy pobre y
dificultades en la percepción.[3] Asociadas a la
hipotonía y a la hipermovilidad encontramos lordosis,
ptosis, caderas dislocadas, pies planos, cabeza
adelantada e inestabilidad atlantoaxial.[3, 4] La
inestabilidad atlantoaxial contraindica la
participación de personas con SD en actividades
deportivas de contacto.[4]
Además de estas características clínicas, los
niños, adolescentes y adultos con SD presentan
niveles más bajos de condición física que los
controles de su misma edad sin SD, con o sin retraso
mental.[5-7]
Existen muy pocos estudios sobre masa magra
o muscular y/o fuerza muscular en niños y
adolescentes con SD, pero se pueden inferir algunos
resultados obtenidos en adultos con SD, aunque no
hay certeza de que en población pediátrica se
repliquen.
Luke et al.[8] no encontraron diferencias en la
masa libre de grasa entre niños prepúberes con y
sin SD usando para ello una dilución de deuterio,
impedancia bioeléctrica y pliegues cutáneos.
Guijarro et al.[9] y Baptista et al.[10] estudiaron
adultos con SD y encontraron niveles más bajos de
masa magra y masa muscular medida con
absorciometría fotónica dual de rayos X (DXA) en
el grupo con SD, comparados con hombres y
mujeres sin SD. Angelopoulou et al.[11] midieron
la fuerza de las extremidades inferiores con un
dinamómetro isocinético a diferentes velocidades
angulares y encontraron niveles de fuerza más bajos
en cuadriceps de jóvenes adultos con SD
comparados con otros sin SD, con o sin retraso
mental. También Mercer et al.[12] demostraron que
los niños y niñas con SD tienen un pico de fuerza
para la abducción de la cadera y la extensión de la
rodilla más bajo que los niños y niñas sin SD. Estos
estudios nos sugieren que, los niños y niñas con SD
tienen menos fuerza muscular que sus homólogos
sin SD; y que los adultos con SD tienen menos
masa magra y muscular que los adultos sin
SD.
Los estudios que evalúan la masa magra en
niños y adolescentes con SD son escasos y no
proporcionan datos sobre la masa muscular en las
extremidades[8], que además es uno de los factores
determinantes de la fuerza. El DXA es un método
relativamente extendido, que además se utiliza con
niños y adolescentes por su baja radiación, tiempo
de exposición y precisión en los resultados. Además
proporciona análisis regionales de composición
corporal y nos informa de la masa muscular de las
extremidades[13]. Los estudios sobre fuerza
también son escasos en esta población, sugiriendo
niveles más bajos en personas con SD de cualquier
edad[11, 12]. Tampoco se conoce la relación entre
masa muscular y fuerza en niños y adolescentes
con SD. El estudio de esta relación podría aportar
información relevante sobre las causas de los
niveles de fuerza reducidos observados en esta
población.
Objetivo
Describir los niveles de masa muscular y fuerza
isométrica y dinámica de las extremidades inferiores
de niños y adolescentes con SD, y estudiar la
relación entre masa muscular y fuerza en esta
población.
Material y Métodos
Muestra
La muestra está compuesta por 32 niños y
adolescentes (15 chicas y 17 chicos) con SD, entre
9 y 19 años. El grupo control sin SD (no-SD) lo
forman 35 sujetos (15 chicas y 20 chicos),
emparejados por edad y sexo. En el grupo con SD
los criterios de inclusión fueron, niños y adolescentes
con SD, en el grupo no-SD todos los niños y
adolescentes eran sanos, sin enfermedad conocida
y ninguno de ellos estuvo tomando medicamentos
los 3 meses anteriores a las pruebas. En ambos
grupos se recogió toda la información sobre
enfermedades u operaciones anteriores y estancias
en hospitales. También se recogió la información
sobre actividad física actual, años de práctica y
nivel. Ambos, padres y niños fueron informados
sobre el objetivo y procedimientos del estudio, así
47
-108-
como de los posibles riesgos y beneficios del mismo.
Se obtuvo un consentimiento informado de todos
los sujetos y de sus padres o tutores.
El estudio se realizó de acuerdo con la
Declaración de Helsinki de 1961 (revisión de
Edimburgo en 2000) y fue aprobado por el Comité
de Ética en Investigación del Gobierno de
Aragón.
Medidas antropométricas y masa muscular
Se midió el peso (0.1 kg) y talla (0.1 cm) de
todos los sujetos descalzos y en ropa interior. El
índice de masa corporal (IMC) se calculó como
kilogramos de peso divididos por la talla al cuadrado
(m). La masa muscular se evaluó mediante una
DXA, usando una versión pediátrica del software
QDR-Explorer (Hologic Corp. Software version
12.4, Waltham, MA). El equipamiento DXA fue
calibrado con un fantoma de espina lumbar
siguiendo las indicaciones del fabricante. Los sujetos
fueron escaneados en posición supina y el escáner
se realizó en máxima resolución. Se midió la masa
muscular del cuerpo completo y después se realizó
un análisis regional separando, cabeza, tronco,
zonas lumbares y extremidades.
Maduración sexual
El estadio de maduración sexual se determinó
por observación, de acuerdo con los 5 estadios
propuestos por Tanner y Whitehouse[14].
Fuerza
Para medir la fuerza isométrica máxima (FI) de
los músculos extensores de la extremidad inferior
se uso una célula de carga anclada en la pared.
Los niños realizaban extensión máxima de
extremidad inferior desde una posición de sentados
con las rodillas a 90º y las manos sobre los muslos.
Los tests de Counter Movement Jump (salto con
contra-movimiento; CMJ) y Abalakov (ABA) se
utilizaron para valorar la fuerza dinámica de las
extremidades inferiores. Cada niño efectuó tres
intentos con cada pierna y tres saltos de cada tipo,
tomamos como válido el valor más alto de los tres.
Se calculó un Índice de Fuerza Relativa (IFR)
dividiendo los kilogramos de fuerza efectuados en
el test de FI por los kilogramos de masa muscular
que tenían en las extremidades inferiores, medida
con DXA.
Análisis estadístico
Los datos se muestran como media ± desviación
típica. Todas las variables mostraron una
distribución normal. Se realizó la prueba t de Student
para estudiar las diferencias en edad, peso, talla,
IMC, FI, CMJ, ABA, IFR y masa muscular en
extremidades inferiores entre los grupos SD y noSD. Las diferencias en la maduración sexual se
establecieron mediante la prueba de Chi cuadrado.
Para estudiar las diferencias en la masa muscular
de extremidades inferiores entre ambos grupos se
efectuó un análisis de covarianza (ANCOVA),
usando como covariables la altura y el estado de
maduración sexual. En todos los análisis se
estudiaron a todos los sujetos como grupo y también
divididos por género.
Los análisis se realizaron con el paquete
estadístico SPSS (versión 14.0 para Windows). Se
tomo como nivel de significación de p<0.05.
Resultados
El grupo con SD pesó 8 kg menos y midió 15
cm menos que el grupo no-SD (p<0.05), sin
embargo no se encontraron diferencias en el IMC
ni tampoco en los estadios de maduración sexual
de Tanner (Tabla 1). El grupo SD obtuvo valores
inferiores en todas las variables (FI, CMJ, ABA e
IFR) comparado con el grupo no-SD (p<0.05). Estas
diferencias persistían al dividir la muestra por sexos
(p<0,05); Tabla 2).
En valores netos, el grupo SD obtuvo valores
inferiores en masa muscular de las extremidades
inferiores (p<0.05; Figura 1), sin embargo, al ajustar
por talla y estadio Tanner estas diferencias
desaparecían, tanto como grupo como separado por
sexos (p<0.05; Figura 2).
Discusión
Diversos autores han descrito previamente
niveles más bajos de fuerza en grupos de población
con SD comparados con poblaciones sin SD con o
sin RM[2, 11, 12, 15-19]. No obstante, no todos
ellos estudiaron poblaciones en edad de crecimiento
como es nuestro caso. Nuestros resultados se
encuentran en la línea de los referidos por Morris
et al.[19] y Mercer et al.[12], con niveles más bajos
de fuerza muscular en niños con SD comparados
con otros sin SD. Sus test valoraban otro tipo de
fuerza muscular, pero siempre fuerza de las
extremidades inferiores en niños y adolescentes.
Angelopoulou et al.[11] trabajó con adultos jóvenes
y también encontró valores significativamente bajos
de fuerza en las extremidades inferiores de los
sujetos con SD. Otros autores [2, 15-18] estudiaron
adultos y obtuvieron las mismas conclusiones, la
población con SD tiene un claro déficit de fuerza
48
-109-
Síndrome de Down
Chicas
Chicos
Total
Total
No Síndrome de Down
Chicas
Chicos
Edad (a)
15.18±2.93
14.77±3.24
15.54±2.68
14.25±2.64
13.89±2.94
Peso (kg)
46.00*±12.56
43.74*±13.72
48.10*±11.45
53.86±13.78
50.58±14.50
Talla (cm)
145.24*±11.62 138.94*±9.90
IMC
Tanner (%)
I/II/III/IV/V
21.66±3.94
22.37±4.80
13/6/13/19/50
20/7/20/13/40
14.52±2.44
56.33±13.03
150.79*±10.28 160.69±14.44
153.26±12.08 166.27±13.77
21.00±2.95
21.20±4.21
6/6/6/24/59
20.57±3.39
20/9/20/9/43
20.10±2.64
27/0/27/0/47 15/15/15/15/40
* p<0.05
Tabla 1. Descripción de la muestra, datos antropométricos y de maduración sexual
Síndrome de Down
Chicas
Chicos
Total
Total
No Síndrome de Down
Chicas
Chicos
FI (kg)
38.18*±17.08
33.15*±11.98
42.32*±19.75
61.34±22.25
56.31±21.88
65.04±22.37
CMJ (cm)
14.53*±6.04
11.52*±4.92
16.66*±5.96
26.78±9.83
22.05±6.92
30.92±10.31
ABA (cm)
16.64*±6.93
11.98*±4.35
19.94*±6.57
31.46±9.18
26.62±7.03
35.69±8.89
7.02*±2.06
7.38*±1.92
6.75*±2.18
8.94±2.04
9.71±1.99
IFR
8.38±1.93
FI = fuerza isométrica, CMJ = salto con contramovimiento, ABA = salto con ayuda de brazos, IFR = índice de fuerza relativa
* p<0.05
Tabla 2. Valores de fuerza, saltos e índice de fuerza relativa
Figura 1. Valores netos de masa muscular de las extremidades inferiores
49
-110-
muscular en todos los ejercicios en que se ha
valorado, extremidades superiores, extremidades
inferiores, zona abdominal, espalda baja, etc… Las
diferencias que existen entre nuestra población con
SD y el grupo control no-SD es posible que no sean
únicamente de fuerza en términos absolutos, es
decir, a músculos más grandes, más fuerza ejercida.
Es muy probable que también exista un problema
de eficiencia muscular. Para averiguar esto
elaboramos el IFR, el cual nos indicó que los
adolescentes con SD no fueron capaces de
practicar tantos kilogramos de fuerza por cada
kilogramo de masa muscular de sus extremidades
inferiores, comparados con los adolescentes sin SD.
Es posible que otras causas fisiológicas o de
transmisión neuromuscular incidan en esta falta de
eficiencia, siendo necesaria más investigación en
esta línea.
En población en crecimiento con SD, el estudio
de Luke et al.[8] demostró que no existían
diferencias en la masa libre de grasa entre niños y
niñas prepúberes con y sin SD. En jóvenes adultos
de 26 años de edad media, el estudio de Guijarro et
al.[9] encontró niveles inferiores de masa libre de
grasa entre sujetos con y sin SD. Por último, en
una muestra muy heterogénea que incluía personas
con SD desde 14 hasta 44 años de edad,
describieron niveles más bajos de masa muscular
en los sujetos con SD comparándolos con otros sin
SD [10].
Como se ha observado, los niveles de fuerza
muscular en población con SD comparados con
población sin SD son más bajos en todos los grupos
de edad; en la niñez, la adolescencia y también en
la edad adulta. Sin embargo, las diferencias en
masa magra o muscular que existen en grupos de
adultos con SD no se observan en la franja de edad
de nuestro estudio. Esto podría sugerir que el déficit
de masa muscular que aparece en edad adulta no
sea debido a un problema inherente de la población
con SD, sino más bien debido al desuso de los
músculos desde la niñez. Existen varias causas que
podrían explicar estas diferencias entre niños y
adolescentes con los adultos. Es posible que al
contar con menos fuerza muscular, los niños y
adolescentes con SD sean menos dados a usar sus
músculos y no provocan la hipertrofia necesaria
para alcanzar niveles óptimos de masa muscular
en edad adulta. Quizá el mayor sedentarismo y
menor participación n programas de ejercicio físico
podría también explicarlo. Incluso podría ocurrir que
necesitaran entrenamientos específicos y adaptados
a su condición. En cualquier caso, se necesitan
estudios que lo corroboren. De hecho, un estudio
longitudinal sería mucho más efectivo para
determinar si realmente ocurre esta pérdida de
masa muscular al llegar a la edad adulta o si,
los sujetos adultos de los otros estudios ya tenían
déficit de masa muscular durante la niñez y la
adolescencia.
Figura 2. Valores ajustados por talla y estadio puberal de masa muscular de las extremidades inferiores
50
-111-
Conclusión
Los niños y adolescentes con SD de nuestro
estudio mostraron una masa muscular similar a los
niños y adolescentes sin SD, una vez ajustada por
talla y desarrollo puberal. Sin embargo mostraron
valores significativamente inferiores en todas las
variables relacionadas con la fuerza. Los niños y
adolescentes con SD tampoco fueron capaces de
ejercer los mismos kilogramos de fuerza por cada
kilogramo de masa muscular que sus homólogos
sin SD. Es importante incidir en estos aspectos ya
que niveles bajos de fuerza en la niñez y
adolescencia les pueden conducir, en edad adulta a
niveles inferiores de masa muscular, impidiendo
finalmente un adecuado desempeño de las tareas
y labores, y por tanto dificultando su inclusión social
y laboral.
7.
8.
9.
10.
11.
12.
Agradecimientos
Agradecemos a Paula Velasco el excelente
trabajo técnico realizado en las densitometrías. Este
estudio está financiado por el Gobierno de Aragón,
(proyecto PM 17/2007) y por el Ministerio de
Innovación y Ciencia de España (Red de
investigación en ejercicio físico y salud para
poblaciones especiales-EXERNET-DEP200500046/ACTI).
13.
14.
Bibliografía
15.
1.
2.
3.
4.
5.
6.
Pueschel SM. Clinical aspects of Down syndrome
from infancy to adulthood. Am J Med Genet Suppl.
1990;7:52-6.
Pitetti KH, Boneh S. Cardiovascular fitness as
related to leg strength in adults with mental
retardation. Med Sci Sports Exerc. 1995
Mar;27(3):423-8.
Winnick J. Adapted Physical Education and Sport.
Champaign, Illinois: Human Kinetics; 1995.
Pueschel SM. Should children with Down
syndrome be screened for atlantoaxial instability?
Arch Pediatr Adolesc Med. 1998 Feb;152(2):1235.
Fernhall B, Pitetti KH, Rimmer JH, McCubbin
JA, Rintala P, Millar AL, et al. Cardiorespiratory
capacity of individuals with mental retardation
including Down syndrome. Med Sci Sports Exerc.
1996 Mar;28(3):366-71.
Fernhall BM, JA. Pitteti, KH. Rintala, P.
Prediction of maximal heart rate in individuals with
mental retardation. Med Sci Sports Exerc. 2001
October;33(10):1655-60.
16.
17.
18.
19.
Guerra M, Llorens N, Fernhall B. Chronotropic
incompetence in persons with down syndrome.
Arch Phys Med Rehabil. 2003 Nov;84(11):1604-8.
Luke A, Sutton M, Schoeller DA, Roizen NJ.
Nutrient intake and obesity in prepubescent
children with Down syndrome. J Am Diet Assoc.
1996 Dec;96(12):1262-7.
Guijarro M, Valero C, Paule B, Gonzalez-Macias
J, Riancho JA. Bone mass in young adults with
Down syndrome. J Intellect Disabil Res. 2008
Mar;52(Pt 3):182-9.
Baptista F, Varela A, Sardinha LB. Bone mineral
mass in males and females with and without Down
syndrome. Osteoporos Int. 2005 Apr;16(4):380-8.
Angelopoulou N, Matziari C, Tsimaras V,
Sakadamis A, Souftas V, Mandroukas K. Bone
mineral density and muscle strength in young men
with mental retardation (with and without Down
syndrome). Calcif Tissue Int. 2000 Mar;66(3):17680.
Mercer VS, Lewis CL. Hip Abductor and Knee
Extensor Muscle Strength of Children with and
without Down Syndrome. Pediatr Phys Ther. 2001
Spring;13(1):18-26.
Calbet JA, Perez-Gomez J, Vicente-Rodriguez
G, Ara I, Olmedillas H, Chavarren J, et al. Look
before you leap: on the issue of muscle mass
assessment by dual-energy X-ray absorptiometry
(reply to Jordan Robert Moon comments). Eur J
Appl Physiol. 2008 Oct;104(3):587-8.
Tanner JM, Whitehouse RH. Clinical longitudinal
standards for height, weight, height velocity,
weight velocity, and stages of puberty. Arch Dis
Child. 1976 Mar;51(3):170-9.
Rimmer JH, Heller T, Wang E, Valerio I.
Improvements in physical fitness in adults with
Down syndrome. Am J Ment Retard. 2004
Mar;109(2):165-74.
Pitetti KH, Rimmer JH, Fernhall B. Physical
fitness and adults with mental retardation. An
overview of current research and future directions.
Sports Med. 1993 Jul;16(1):23-56.
Guerra-Balic M, Cuadrado-Mateos E, GeronimoBlasco C, Fernhall B. Physical Fitness Levels of
Physically Active and Sedentary Adults With
Down Syndrome. Adapted Physical Activity
Quarterly. 2000;17(3):310-21.
Horvat M, Pitetti KH, Croce R. Isokinetic torque,
average power, and flexion/extension ratios in
nondisabled adults and adults with mental
retardation. J Orthop Sports Phys Ther. 1997
Jun;25(6):395-9.
Morris AF, Vaughan SE, Vaccaro P. Measurements
of neuromuscular tone and strength in Down’s
syndrome children. J Ment Defic Res. 1982
Mar;26(Pt 1):41-6.
51
-112-
Research in Developmental Disabilities 32 (2011) 1764–1769
Accuracy of prediction equations to assess percentage of body fat in
children and adolescents with Down syndrome compared to air
displacement plethysmography
A. González-Agüero a,b,*, G. Vicente-Rodrı́guez a,b, I. Ara a,c, L.A. Moreno a,d, J.A. Casajús a,b
a
GENUD (Growth, Exercise, NUtrition and Development) Research Group, University of Zaragoza, Zaragoza, Spain
c
GENUD Toledo Research Group, University of Castilla-La Mancha, Spain
d
b
A B S T R A C T
Article history:
Received 3 March 2011
Accepted 3 March 2011
Available online 1 April 2011
To determine the accuracy of the published percentage body fat (%BF) prediction equations
(Durnin et al., Johnston et al., Brook and Slaughter et al.) from skinfold thickness compared to
air displacement plethysmography (ADP) in children and adolescents with Down syndrome
(DS). Twenty-eight children and adolescents with DS (10–20 years old; 12 girls, 16 boys)
participated in the study. Anthropometric measurements height, weight, and skinfolds
biceps, triceps, subscapular and suprailiac were performed following ISAK recommendations. Total body density (TBD) was estimated using three equations and was also measured
with ADP; while %BF was calculated from all densities using the Siri equation and from
skinfolds using the Slaughter et al. equation. Finally, the agreement between methods was
assessed by plotting the results in Bland–Altman graphs. The presence of heteroscedasticity
was also examined. Despite the equation of Slaughter et al. had a large 95% limits of
agreement, it was the only one without a significant inter-methods difference and without
heteroscedasticity. The equation of Slaughter seems to be, from the studied, the most
accurate for estimating %BF in children and adolescents with DS.
Keywords:
Trisomy 21
Body composition
ISAK
Fat mass
1. Introduction
It is well documented that children and adolescents with Down syndrome (DS) tend towards obesity and accumulate
higher amounts of fat compared to the population without DS (Bronks & Parker, 1985; Chumlea & Cronk, 1981; Cronk,
Chumlea, & Roche, 1985; González-Agüero, Ara, Moreno, Vicente-Rodriguez, & Casajús, in press; Ordonez, Rosety, & RosetyRodriguez, 2006). Both, childhood obesity and increased fat mass are factors associated with future diseases (Despres &
Lemieux, 2006; Dietz, 1998; Ebbeling, Pawlak, & Ludwig, 2002; Maffeis & Tato, 2001). Therefore, as the life expectancy of this
population has increased by more than 40 years within the last seven decades (nowadays, DS individuals frequently live to
around 50 years and older) (Bittles & Glasson, 2004; Glasson et al., 2002; Smith, 2001), health-related body composition is a
concerning issue which should be accurately studied and controlled in order to assist individuals with this genetic condition
(González-Agüero, Vicente-Rodriguez, Moreno, Guerra-Balic, et al., 2010).
* Corresponding author at: C/Corona de Aragón 42, Edificio Cervantes 2 planta, Grupo GENUD, ZIP: 50006, Zaragoza, Spain. Tel.: +34 976400338x301;
fax: +34 976400340.
E-mail address: [email protected] (J.A. Casajús).
doi:10.1016/j.ridd.2011.03.006
-113-
1765
Several methods such as underwater weighing, air displacement plethysmography (ADP), labelled water techniques or
dual energy X-ray absorptiometry (DXA) have been used to study body composition in children and adolescents because of
their accuracy in assessing body compartments at the individual level (Ara et al., 2004, 2006; Fields & Goran, 2000; Fields,
Hunter, & Goran, 2000; Parker, Reilly, Slater, Wells, & Pitsiladis, 2003). However, due to their high cost and practical issues,
those methods are not always practical or suitable for field and clinical use. Anthropometry is widely used to assess the
percentage body fat (%BF) in large populations and is particularly useful when the available economic resources are
relatively low (Ara, Moreno, Leiva, Gutin, & Casajus, 2007; Wang, Thornton, Kolesnik, & Pierson, 2000). Prediction equations
such as Durnin and Rahaman (Durnin & Rahaman, 1967), Brook (Brook, 1971), Durnin and Womersley (Durnin & Womersley,
1974), Johnston et al. (Johnston et al., 1988) or Slaughter et al. (Slaughter et al., 1988) are often used to predict total body
density (TBD) or %BF from anthropometric measurements in children and adolescents. Prediction equations are selected
based on specific characteristics of the measured participants (Roche, Heymsfield, & Lohman, 1996). Several studies have
compared the abovementioned equations with reference methods such as DXA or ADP in order to determine which is the
most accurate calculation for specific population groups (Bell, Cobner, & Evans, 2000; De Lorenzo et al., 1998; Espana Romero
et al., 2009; Radley et al., 2003; Rodriguez et al., 2005; Usera, Foley, & Yun, 2005). Children and adolescents with DS are a
unique population in terms of body composition (González-Agüero, Vicente-Rodriguez, Moreno, Guerra-Balic, et al., 2010)
and their bodily proportions are different compared to the general population (Cronk et al., 1988; Myrelid, Gustafsson,
Ollars, & Anneren, 2002). In fact, studies in our laboratory have shown that although children and adolescents with DS have a
similar %BF and sexual dimorphism than their counterparts without DS (González-Agüero, Vicente-Rodriguez, Moreno, &
Casajús, 2010), they display a different amount and distribution of body fat (González-Agüero et al., in press). Previous
studies in persons with DS assessed their %BF by using general prediction equations by skinfold thickness, with unknown
errors for this specific population (Bronks & Parker, 1985; Grammatikopoulou et al., 2008; Magge, O’Neill, Shults, Stallings, &
Stettler, 2008; Ordonez et al., 2006). A prediction equation has been validated on adults with intellectual disability, but not
for children or adolescents with DS (Rimmer, Kelly, & Rosentswieg, 1987).
The aim of the present study was to investigate the accuracy of the published prediction equations to estimate %BF from
skinfold thickness comparing with ADP in children and adolescents with DS.
2. Material and methods
2.1. Participants
A total sample of 28 children and adolescents (12 females/16 males) with DS living at home and aged 10–20 years old
were recruited from various schools and institutions in the region of Aragón (Spain). Both parents and children were
informed about the aims and procedures, as well as the possible risks and benefits of the study. Written informed consent
was obtained from all the included participants and their parents or guardians. The study was performed in accordance with
the Helsinki Declaration of 1961 (revised in Edinburgh, 2000) and was approved by the Research Ethics Committee of the
Government of Aragon (CEICA, Spain).
2.2. Anthropometry
All participants were measured without shoes and the minimum clothes to the nearest 0.1 cm (SECA 225, SECA, Hamburg,
Germany), and weighted to the nearest 0.1 kg (SECA 861, SECA, Hamburg, Germany). The body mass index (BMI) was
calculated as weight (kg) divided by height squared (m2).
Biceps, triceps, subescapular and suprailiac skinfold thicknesses were measured in triplicate on the right side of the body
to the nearest 0.2 mm with a skinfold calliper (Holtain Ltd. Crymmych, UK) following the recommendations of the
International Society for the Advance of Kinanthropometry (ISAK) (Norton et al., 1996). The median of the three measures
was taken as the valid measure. The same trained person (certified level 2 ISAK) carried out all the measurements, and her
technical error of measurement was within the recommended limits by ISAK.
2.3. Total body density and body fat percentage assessment by skinfold thickness
The equations of Durnin and Rahaman (Durnin & Rahaman, 1967) and Durnin and Womersley (Durnin & Womersley,
1974) (depending on the age of the participant), Johnston et al. (Johnston et al., 1988) and Brook (Brook, 1971) were used to
assess TBD from skinfold thickness. The equations of Slaughter et al. (Slaughter et al., 1988) were used to assess %BF by
skinfold thickness. The TBD was converted into %BF via Siri’s equation (Siri, 1961). All the equations used in this study are
summarized in Table 1.
2.4. Air displacement plethysmography measurements
ADP measurements were obtained immediately after the anthropometric study to assess TBD with a BODPOD1 (Body
Composition System, Life Measurement Instruments, Concord, CA) as previously described (Fields & Goran, 2000). All
studies, which were completed with the same device and software, were performed by the same technician who had been
-114-
1766
Table 1
Published equations used to calculate total body density and percentage of body fat in children and adolescents from skinfold thickness.
Authors
Population
Durnin and Rahaman (1967)
Durnin and Womersley (1974)
13–15.9 y
16–19.9 y
Johnston et
8–14 y
al. (1988)
Brook (1971)
1–11 y
Slaughter et al. (1988)
10–17 y
Siri (1961)
Adults
Equations
F (13–15.9): D = 1.1369 0.598 log
M (13–15.9): D = 1.1533 0.0643 log
F (16–19.9): D = 1.1549 0.0678 log
M (16–19.9): D = 1.162 0.063 log
F: D = 1.144 0.06 log
M: D = 1.166 0.07 log
F: D = 1.2063 0.0999 log
M: D = 1.169 0.0788 log
All F: %BF = 1.33(tric + subsc) 0.013(tric + subsc)2 2.5
Prepubertal M: %BF = 1.21(tric + subsc) 0.008(tric + subsc)2 1.7
Pubertal M: %BF = 1.21(tric + subsc) 0.008(tric + subsc)2 3.4
Post-pubertal M: %BF = 1.21(tric + subsc) 0.008(tric + subsc)2 5.5
All F when (tric + subsc) > 35 mm: %BF = 0.546(tric + subsc)2 + 9.7
All M when (tric + subsc) > 35 mm: %BF = 0.783(tric + subsc)2 + 1.7
M and F: %BF = (4.95/D 4.5) 100
%BF: percentage of body fat; y: years; F: female; M: male; D: density; log: log10 (sum of biceps, triceps, subscapular and suprailiac skinfolds); tric: triceps
skinfold; subsc: subscapular skinfold.
Table 2
Physical characteristics of the participants (mean sd).
Age (y)
Weight (kg)
Height (cm)
BMI (kg/m2)
All (n = 28)
Males (n = 16)
Females (n = 12)
16.3 2.6
50.1 10.5
148.7 9.9
22.5 3.3
16.1 2.8
51.0 11.2
152.7 9.7
21.6 2.9
16.5 2.5
48.8 9.9
143.3 7.4
23.6 3.5
BMI: body mass index.
fully trained in the operation. Participants were measured with minimal clothes and with a swim cap. The pulmonary
capacity was calculated by the software of the BODPOD1 based on the characteristics of the participant. The BODPOD1
calculated the %BF by introducing the TBD measured by ADP in the equation of Siri (Siri, 1961).
All the statistical analyses were performed with the Statistical Package for the Social Sciences (SPSS) version 15.0 for
Windows (SPSS Inc., Chicago, IL, USA). Results were presented as mean standard deviation (sd), otherwise stated. The
distribution of the variables was tested with the Kolmogorov–Smirnov test, all exhibited normal distribution. Agreement between
ADP and each prediction equation was determined according to Bland–Altman plots (Bland & Altman, 1986). Differences were
plotted against the ‘gold standard’ (in this case %BF measured with the BODPOD1) instead of the mean value because the ‘gold
standard’ was expected to be closer to the ‘‘true value’’ than the mean (Krouwer, 2008). Validity and lack of agreement between
ADP and equations was assessed by calculating the inter-methods difference and the sd of the differences. The 95% limits of
agreement (inter-methods difference 1.96 sd) of each equation were also calculated. Differences between methods (each
equation vs. ADP) were analysed by paired t-test. Heteroscedasticity was examined by linear regression to determine whether the
absolute inter-methods difference was associated with the magnitude of the measurement. Statistical significance was set at
p < 0.05.
3. Results
Physical characteristics of the participants are shown in Table 2. The equations were plotted according to the Bland–
Altman approach (Bland & Altman, 1986) (Fig. 1(a)–(d)). Calculated TBD and %BF, inter-methods difference and 95% limits of
agreement of each prediction equation against ADP are shown in Table 3. Only the Slaughter’s %BF equation did not show a
significant difference against ADP (p = 0.583, Table 3); although higher 95% limits of agreement compared with the others
(25.8 vs. 18, 19.3 and 22.6; Table 3). Heteroscedasticity (increase in the variance with increase in the magnitude) is present in
Durnin et al., Johnston et al. and Brook equations (all p < 0.05), but not in Slaughter et al. (p = 0.596).
4. Discussion
The aim of the present study was to assess which of the published anthropometric equations fits better the %BF in children
and adolescents with DS; derived from our results, the equation of Slaughter et al. is the best compared with ADP
measurements.
-115-
[()TD$FIG]
1767
Fig. 1. Comparison of predicted %BF between skinfold-thickness equations [(a) Durnin et al., (b) Johnston et al., (c) Brook and (d) Slaughter et al.] and ADP by
Bland–Altman plots. Central line represents the inter-methods difference. Upper and lower broken lines represent the 95% limits of agreement (intermethods difference 1.96 sd of the differences). The solid line in each plot represents the linear regression between %BF by ADP and differences between
methods, its correlation (r) and significance (p). In (a)–(c), total body density was calculated by each equation and then converted into %BF via Siri’s equation. Note:
ADP: air displacement plethysmography; %BF: percentage of body fat.
Table 3
Percentage of body fat (%BF; mean sd), inter-methods difference and 95% limits of agreement for %BF predicted by using body density equations and ADP.
Prediction equation
TBD
Percentage of body fat
Durnin and Womersley, Durnin and Rahaman
Johnston et al.
Brook
Slaughter et al.
ADP
1.0420
1.0427
1.0317
–
1.0369
25.1 6.9
24.8 6.2
29.9 7.9
26.8 9.9
27.5 8.2
Inter-methods
difference
2.34*
2.73*
2.45*
0.69
–
p
95% Limits
of agreement
0.012
0.007
0.031
0.583
–
18.0
19.6
22.3
25.8
–
TBD: total body density; ADP: air displacement plethysmography.
*
p < 0.05.
As mentioned previously, children and adolescents with DS are a unique population in terms of body composition
(González-Agüero, Vicente-Rodriguez, Moreno, Guerra-Balic, et al., 2010) and, to our knowledge this is the first study
designed to determine the most effective prediction equation to assess their %BF from skinfold thickness.
The findings provide some useful and relevant information about the accuracy of the most commonly used equations for
estimating %BF in children and adolescents with DS. Whether this can be applied to other populations with DS is an
important issue that requires some further investigation.
Comparing the results we observed that Slaughter’s equation is the most accurate for predicting %BF in this very specific
population. Despite this equation shows an elevated 95% limits of agreement, this is the only one that did not present
significant differences against the ‘gold standard’. This equation is also the only one without heteroscedasticity, so the
magnitude of the variable does not affect the difference with the BODPOD1. Consequently, we propose using the equation of
Slaughter et al. for assessing %BF in children and adolescents with DS, although further investigations with a higher sample
size could help to develop a new equation specifically designed for this population.
Some of the strengths of our study include the use of ADP as reference method for TBD assessment and the harmonization
of anthropometric methodology in order to reduce the technical error of measurement. On balance, some limitations should
be recognized. The hydration status of the participants was not taken into account; however, as measurements were taken
within some minutes this should not affect the results. Despite the number of participants is bigger than the majority of the
-116-
1768
previous published studies in children and adolescents with DS, (González-Agüero, Vicente-Rodriguez, Moreno, GuerraBalic, et al., 2010) the specificity of the condition and the age range make complicated to increase the sample size.
5. Conclusion
The results of the present study suggest that a substantial amount of inter-methods difference and under or
overestimation may be expected when using Johnston et al., Brook or Durnin et al. equations to estimate %BF in children and
adolescents with DS. The equation of Slaughter et al. significantly increase the accuracy for estimating %BF in this specific
population compared to the other published prediction equations. Further research on this topic could help to develop a new
specifically designed equation even more accurate for children and adolescents with DS.
Conflicts of interest
There are no conflicts of interest or financial disclosures for any author of this manuscript. None of the authors have any
financial interest.
Acknowledgments
The authors want to thank all the children and their parents that participated in the study for their understanding and
dedication to the project. Special thanks are given to Fundación Down Zaragoza and Special Olympics Aragon for their
support. We also thank Scott G Mitchell from the University of Glasgow for his work of reviewing the English style and
grammar, and Paula Velasco from the University of Zaragoza for her great technical assistance. This work was supported by
Gobierno de Aragón (Proyecto PM 17/2007) and Ministerio de Ciencia e Innovación de España (Red de investigación en
ejercicio fı́sico y salud para poblaciones especiales-EXERNET-DEP2005-00046/ACTI). There are no potential conflicts of
interest that may affect the contents of this work.
References
(Silver Spring), 15, 1918–1924.
Ara, I., Vicente-Rodriguez, G., Jimenez-Ramirez, J., Dorado, C., Serrano-Sanchez, J. A., & Calbet, J. A. (2004). Regular participation in sports is associated with
enhanced physical fitness and lower fat mass in prepubertal boys. International Journal of Obesity and Relate Metabolic Disorders, 28, 1585–1593.
Ara, I., Vicente-Rodriguez, G., Perez-Gomez, J., Jimenez-Ramirez, J., Serrano-Sanchez, J. A., Dorado, C., et al. (2006). Influence of extracurricular sport activities on
body composition and physical fitness in boys: a 3-year longitudinal study. International Journal of Obesity (London), 30, 1062–1071.
Bell, W., Cobner, D. M., & Evans, W. D. (2000). Prediction and validation of fat-free mass in the lower limbs of young adult male Rugby Union players using dualenergy X-ray absorptiometry as the criterion measure. Ergonomics, 43, 1708–1717.
Bittles, A. H., & Glasson, E. J. (2004). Clinical, social, and ethical implications of changing life expectancy in Down syndrome. Developmental Medicine & Child
Neurology, 46, 282–286.
Bland, J. M., & Altman, D. G. (1986). Statistical methods for assessing agreement between two methods of clinical measurement. Lancet, 1, 307–310.
Brook, C. G. D. (1971). Determination of body composition of children from skinfold measurements. Archives of Disease in Childhood, 46, 182–184.
Cronk, C., Crocker, A. C., Pueschel, S. M., Shea, A. M., Zackai, E., Pickens, G., et al. (1988). Growth charts for children with Down syndrome: 1 month to 18 years of
age. Pediatrics, 81, 102–110.
Cronk, C. E., Chumlea, W. C., & Roche, A. F. (1985). Assessment of overweight children with trisomy 21. American Journal of Mental Deficiency, 89, 433–436.
Chumlea, W. C., & Cronk, C. E. (1981). Overweight among children with trisomy. Journal of Mental Deficiency Research, 25(Pt. 4), 275–280.
De Lorenzo, A., Bertini, I., Candeloro, N., Iacopino, L., Andreoli, A., & Van Loan, M. D. (1998). Comparison of different techniques to measure body composition in
moderately active adolescents. British Journal of Sports Medicine, 32, 215–219.
Despres, J. P., & Lemieux, I. (2006). Abdominal obesity and metabolic syndrome. Nature, 444, 881–887.
Dietz, W. H. (1998). Health consequences of obesity in youth: childhood predictors of adult disease. Pediatrics, 101, 518–525.
Durnin, J. V., & Rahaman, M. M. (1967). The assessment of the amount of fat in the human body from measurements of skinfold thickness. British Journal of
Nutrition, 21, 681–689.
Durnin, J. V., & Womersley, J. (1974). Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women
aged from 16 to 72 years. British Journal of Nutrition, 32, 77–97.
Ebbeling, C. B., Pawlak, D. B., & Ludwig, D. S. (2002). Childhood obesity: public-health crisis, common sense cure. Lancet, 360, 473–482.
Espana Romero, V., Ruiz, J. R., Ortega, F. B., Artero, E. G., Vicente-Rodriguez, G., Moreno, L. A., et al. (2009). Body fat measurement in elite sport climbers:
comparison of skinfold thickness equations with dual energy X-ray absorptiometry. Journal of Sports Sciences, 27, 469–477.
Fields, D. A., & Goran, M. I. (2000). Body composition techniques and the four-compartment model in children. Journal of Applied Physiology, 89, 613–620.
Fields, D. A., Hunter, G. R., & Goran, M. I. (2000). Validation of the BOD POD with hydrostatic weighing: influence of body clothing. International Journal of Obesity
and Related Metabolic Disorders, 24, 200–205.
implications for genetic counselling. Clinical Genetics: An International Journal of Genetics and Molecular Medicine, 62, 390–393.
González-Agüero, A., Ara, I., Moreno, L. A., Vicente-Rodriguez, G., & Casajús, J. A. (in press). Fat and lean masses in youths with Down syndrome: gender differences.
Research in Developmental Disabilities, doi:10.1016/j.ridd.2011.02.023.
González-Agüero, A., Vicente-Rodriguez, G., Moreno, L. A., & Casajús, J. A. (2010). Dimorfismo sexual en grasa corporal en adolescentes con sı́ndrome de Down.
Revista Española de Obesidad, 8, 28–33.
Grammatikopoulou, M. G., Manai, A., Tsigga, M., Tsiligiroglou-Fachantidou, A., Galli-Tsinopoulou, A., & Zakas, A. (2008). Nutrient intake and anthropometry in
children and adolescents with Down syndrome—a preliminary study. Developmental Neurorehabilitation, 11, 260–267.
Johnston, J. L., Leong, M. S., Checkland, E. G., Zuberbuhler, P. C., Conger, P. R., & Quinney, H. A. (1988). Body fat assessed from body density and estimated from
skinfold thickness in normal children and children with cystic fibrosis. American Journal of Clinical Nutrition, 48, 1362–1366.
-117-
1769
Krouwer, J. S. (2008). Why Bland–Altman plots should use X, not (Y + X)/2 when X is a reference method. Statistics in Medicine, 27, 778–780.
Magge, S. N., O’Neill, K. L., Shults, J., Stallings, V. A., & Stettler, N. (2008). Leptin levels among prepubertal children with Down syndrome compared with their
siblings. Journal of Pediatrics, 152, 321–326.
Myrelid, A., Gustafsson, J., Ollars, B., & Anneren, G. (2002). Growth charts for Down’s syndrome from birth to 18 years of age. Archives of Disease in Childhood, 87,
97–103.
Norton, K., Whittingham, N., Carter, L., Kerr, D., Gore, C., & Marfell-Jones, M. (1996). Measurement techniques in anthropometry. In K. Norton & T. Olds (Eds.),
Antropométrica (pp. 22–75). Sydney: UNSW.
Ordonez, F., Rosety, M., & Rosety-Rodriguez, M. (2006). Influence of 12-week exercise training on fat mass percentage in adolescents with Down syndrome.
Medical Science Monitor, 12, CR416–419.
Parker, L., Reilly, J. J., Slater, C., Wells, J. C., & Pitsiladis, Y. (2003). Validity of six field and laboratory methods for measurement of body composition in boys. Obesity
Research, 11, 852–858.
Radley, D., Gately, P. J., Cooke, C. B., Carroll, S., Oldroyd, B., & Truscott, J. G. (2003). Estimates of percentage body fat in young adolescents: a comparison of dualenergy X-ray absorptiometry and air displacement plethysmography. European Journal of Clinical Nutrition, 57, 1402–1410.
Rimmer, J. H., Kelly, L. E., & Rosentswieg, J. (1987). Accuracy of anthropometric equations for estimating body composition of mentally retarded adults. American
Journal of Mental Deficiency, 91, 626–632.
Roche, A. F., Heymsfield, S. B., & Lohman, T. G. (1996). Human body composition. Champaign, IL: Human Kinetics.
Rodriguez, G., Moreno, L. A., Blay, M. G., Blay, V. A., Fleta, J., Sarria, A., et al. (2005). Body fat measurement in adolescents: comparison of skinfold thickness
equations with dual-energy X-ray absorptiometry. European Journal of Clinical Nutrition, 59, 1158–1166.
Siri, W. E. (1961). Body composition from fluid spaces and density: Analysis of methods. In J. Brozek & A. Henzchel (Eds.), Techniques for measuring body
composition (pp. 224–244). Washington: National Academy of Sciences.
Slaughter, M. H., Lohman, T. G., Boileau, R. A., Horswill, C. A., Stillman, R. J., Van Loan, M. D., et al. (1988). Skinfold equations for estimation of body fatness in
children and youth. Human Biology, 60, 709–723.
Smith, D. S. (2001). Health care management of adults with Down syndrome. American Family Physician, 64, 1031–1038.
Usera, P. C., Foley, J. T., & Yun, J. (2005). Cross-validation of field based assessments of body composition for individuals with Down syndrome. Adapted Physical
Activity Quarterly, 22, 198–206.
Wang, J., Thornton, J. C., Kolesnik, S., & Pierson, R. N., Jr. (2000). Anthropometry in body composition. An overview. Annals of the New York Academy of Sciences, 904,
317–326.
-118-
G Model
RIDD-1314; No. of Pages 6
Research in Developmental Disabilities xxx (2011) xxx–xxx
A combined training intervention programme increases lean mass in
youths with Down syndrome
Alejandro González-Agüero a,b,*, Germán Vicente-Rodrı́guez a,b, Alba Gómez-Cabello a,b,
Ignacio Ara a,c, Luis A. Moreno a,d, José A. Casajús a,b
a
GENUD (Growth, Exercise, NUtrition and Development) Research Group, University of Zaragoza, Zaragoza, Spain
GENUD Toledo Research Group, University of Castilla-La Mancha, Toledo, Spain
d
b
c
A B S T R A C T
Article history:
Received 17 July 2011
Accepted 18 July 2011
Aim: The present study aimed to determine whether youths with Down syndrome (DS) are
able to increase lean mass and decrease fat mass, after 21 weeks of conditioning combined
with a plyometric jumps training program. Methods: Twenty-six participants with DS (15
males) aged 10–19 years joined the study. Participants were divided into two comparable
groups, exercise (EG; n = 13) and control (CG). Total and regional (trunk, upper and lower
limbs) lean and fat masses were assessed by dual energy X-ray absorptiometry (DXA), at
baseline and after the intervention. ANCOVA tests were used to evaluate differences
between groups in pre- and post-training moments. Repeated measures of ANOVA
adjusted by the increments in height and Tanner were applied to test the differences
between pre and post-training moments. Adjusted percentages of change were calculated
and differences between groups evaluated with Student’s t test. Results: After the training
period, EG showed an increase in total and lower limbs lean mass, while no changes in
adiposity depots were observed. CG did not change neither the lean mass nor the fat mass
except for decreased upper limbs fat mass (all p < 0.05) during the same period of time. As
a result, time by exercise interactions were found for whole body and lower limbs lean
mass (both p < 0.05). No differences in the percentage of fat were observed between
groups at baseline or post-training. Overall, 21 weeks of conditioning combined with
plyometric jumps training was an effective method for increasing lean mass in youths with
DS; however, no changes in fat mass were observed.
Keywords:
Exercise
DXA
Trisomy 21
Down’s syndrome
Training
Muscle mass
1. Introduction
Body composition is an important marker of health at all ages, especially during childhood and adolescence; larger
amounts of fat during these periods are related to a greater risk of premature illness, death from coronary heart disease,
hypertension and type 2 diabetes later in life (Dietz, 1998; Ebbeling, Pawlak, & Ludwig, 2002; Maffeis & Tato, 2001).
In addition, low lean mass is associated with decreased skeletal muscle tissue (Calbet et al., 2008), which in turn is related
with the functional capacity and the maximum oxygen consumption that is a marker of health in youths, and
* Corresponding author at: C/Corona de Aragón 42, Edificio Cervantes 2 planta, Grupo GENUD, 50006 Zaragoza, Spain. Tel.: +34 976400338x301;
fax: +34 976400340.
E-mail address: [email protected] (A. González-Agüero).
doi:10.1016/j.ridd.2011.07.024
Please cite this article in press as: González-Agüero, A., et al. A combined training intervention programme increases lean
mass in youths with Down syndrome. Research in Developmental Disabilities (2011), doi:10.1016/j.ridd.2011.07.024
-119-
G Model
2
A. González-Agüero et al. / Research in Developmental Disabilities xxx (2011) xxx–xxx
is associated with cardiovascular health during adulthood (Ortega et al., 2005; Ortega, Ruiz, Castillo, & Sjostrom,
2008).
Less healthy body composition has been observed in children and adolescents with DS compared with their counterparts
without DS, with or without intellectual disabilities (González-Agüero, Vicente-Rodriguez, Moreno, Guerra-Balic, et al.,
2010), having lower levels of lean mass and higher levels of fat mass (Bronks & Parker, 1985; González-Agüero, Ara, Moreno,
Vicente-Rodriguez, & Casajús, 2011; González-Agüero, Vicente-Rodriguez, Moreno, & Casajús, 2010; González-Agüero,
Villarroya, Vicente-Rodriguez, & Casajús, 2009; Luke, Sutton, Schoeller, & Roizen, 1996). Due to the increment in the lifespan
of persons with DS (Glasson et al., 2002), some diseases such as diabetes or metabolic syndrome, that did not usually occur in
this population due to premature death, are likely to appear within the coming years. Therefore, strategies trying to prevent
these diseases by reducing fat mass and increasing lean mass seem to be a key factor to be promoted from childhood and
adolescence in persons with DS.
It is well known that regular physical activity and training programs improve body composition in healthy children and
adolescents (Ara, Moreno, Leiva, Gutin, & Casajus, 2007; Ara et al., 2010; Heyward, 2006; McArdle, Katch, & Katch, 2007);
however researchers have not established whether this occurs in the same manner in children and adolescents with DS
(González-Agüero, Vicente-Rodriguez, Moreno, Guerra-Balic, et al., 2010).
Training programs have been applied in children and/or adolescents with DS (Lewis & Fragala-Pinkham, 2005; Millar,
Fernhall, & Burkett, 1993; Ordonez, Rosety, & Rosety-Rodriguez, 2006; Varela, Sardinha, & Pitetti, 2001; Weber & French,
1988), however, only one has focused to improve their body composition (Ordonez et al., 2006) showing reductions in
the percentage of body fat in adolescents with DS with aerobic exercise. Training use to take 45–90 min 3 times per
week, which is a great effort for youths and families, taken into account the number of extra-lessons, especial programs
and medical visits they have to deal with in their normal life. To find low-time consuming but effective training
programs, being able to improve body composition in children and adolescents with DS may be of great interest and
applicability.
Thus, the aim of the present study was to determine the effect of 21 weeks of conditioning and plyometric jumps training
in soft tissues body composition in youths with DS.
2. Materials and methods
2.1. Participants
A total sample of 26 children and adolescents with DS (13 females) aged 10–19 years at baseline were recruited from
different schools and institutions in Aragón (Spain). Thirteen participants (8 females and 5 males) were randomly assigned to
the exercise group (EG) and performed the training program; the remaining 13 participants were the control group (CG).
Both parents and children were informed about the aims and procedures, as well as the possible risks and benefits of the
study. Written informed consent was obtained from all the participants and their parents or guardians. The study was
performed in accordance with the Helsinki Declaration of 1961 (revised in Edinburgh, 2000) and was approved by the
Research Ethics Committee of the Government of Aragon (CEICA, Spain).
2.2. Anthropometry
All participants were measured with a stadiometer without shoes and minimum clothing to the nearest 0.1 cm (SECA 225,
SECA, Hamburg, Germany), and weighted to the nearest 0.1 kg (SECA 861, SECA, Hamburg, Germany). The body mass index
(BMI) was calculated as weight (kg) divided by height squared (m2).
2.3. Pubertal status assessment
Pubertal development was determined by direct observation by a physician according to the 5 stages proposed by Tanner
and Whitehouse (1976).
Total fat (kg) and lean (kg) masses were determined from a whole-body scan by dual energy X-ray absorptiometry
(DXA), using a paediatric version of the QDR-Explorer software (Hologic Corp. Software version 12.4, Bedford, MA
01730). The validity of DXA was established by comparison with chemical analysis (Svendsen, Haarbo, Hassager, &
Christiansen, 1993), and its reliability was demonstrated by an intra-class correlation of 0.998 for repeated
measurements of the %BF in children (Gutin et al., 1996). DXA equipment was calibrated using a step densities
phantom and following Hologic guidelines. Participants were scanned in the supine position and scans performed
with high resolution. Fat and lean masses were also calculated from regional analyses of the whole body scan: trunk
(only for fat mass), upper and lower limbs. Percentage of fat was calculated with the formula ‘‘Percentage of fat = [total
fat mass (kg)/body weight (kg)] 100’’. Evaluations were performed in both groups at baseline and after the
intervention.
-120-
G Model
3
2.5. Training program
Those participants allocated in the EG exercised twice a week, and each session was conducted with a maximum of 10
participants. One researcher and one to three assistants supervised the exercise sessions. Each session consisted of combined
conditioning and plyometric jumps training. The first week was used to familiarization how to use the material/equipment
and how to perform the exercises. Each training session consisted of 5 min warm-up activities, 10–15 min session, and 5 min
cool-down. The training consisted of 1 or 2 rotations in a circuit of 4 stages.
The exercises performed in each stage were:
1. Jumps: standing vertical jump, jump with run-in, drop jump, drop jump + horizontal jump. From the third week,
participants carried adapted-medicine balls while performing the jumps.
2. Press-ups on the wall: participants placed their hands on a wall and performed press-ups standing with their feet separate
from the wall.
3. Elastic-fitness bands: lateral rows, bicep curls and frontal rows.
4. Adapted-medicine balls: standing throw and catch.
The 13 participants were divided into four intensity-groups (quartiles) depending on their body weight, and they worked
out individually. When participants showed excessive facility for performing exercises, they were transferred to the next
intensity-group. There were 4 fitness bands colours (yellow, green, blue and purple) of increasing resistance and 4 medicine
balls (1, 2, 3 and 4 kg), each one being assigned to a group depending on the strength demanded to perform the exercises.
Every group followed the same schedule of exercises with a different band colour and ball: Weeks 1–5: 1 set of 10
repetitions; Weeks 6–10: 2 sets of 10 repetitions; Weeks 11–15: 2 sets of 15 repetitions; and Weeks 16–21: 2 sets of 20
repetitions.
A minimum attendance of 70% was required to be included in the exercise group. If minimum assistance was not
achieved, the participant was excluded from the statistical analyses.
All statistical analyses were performed with the Statistical Package for the Social Sciences (SPSS) version 15.0 for
Windows (SPSS Inc., Chicago, IL, USA). Mean and standard deviations are given as descriptive statistics; otherwise they are
stated. Kolmogorov–Smirnov tests showed normal distribution of the studied variables. Chi square test was performed to
evaluate differences in Tanner maturational status. Student’s t tests were used to evaluate the differences between groups
for physical characteristics. Analysis of covariance (ANCOVA) were used to test the differences between groups for fat and
lean masses in pre- and post-training moments, including height and Tanner as covariates. Analysis of variance (ANOVA) for
repeated measures was performed to evaluate sex by training interactions and the time by exercise interactions for fat and
lean masses; including as covariates the increments (percentage of change pre-post) in height and in Tanner status, which
have been identified as influential factors on body composition. Every adjusted value of total and regional fat and lean was
recorded in the database, and then an adjusted percentage of change was calculated, with these values, for each participant.
Student’s t test was used to evaluate the differences between the adjusted percentage of change between EG and CG.
Statistical significance was set at p < 0.05.
3. Results
3.1. Adherence to training and possible adverse effects
Adherence to training averaged 81.8 9.2%, ranged from 70% to 97%. Only one participant (female) did not achieve the
minimum 70% assistance to the intervention program (attended 45% of the trainings) and her data were excluded of the analyses.
No withdrawals from the EG or CG occurred. Noticeably, no adverse effects and no health problem were noted in the participants
of both groups over the 21-week period.
3.2. Physical characteristics
Age, Tanner status and physical characteristics of the participants are summarized in Table 1. EG showed lower BMI than
CG at baseline (p < 0.05; Table 1). Participants in both groups showed similar age, height, weight, percentage of fat and
Tanner stage distribution at both, baseline and post-intervention points.
3.3. Effects of training on body composition
As no sex by training interactions were found (data not shown) analyses were performed including males and females as a
whole. Adjusted values of total and regional fat and lean masses are shown in Table 2. The EG group showed lower levels of
fat and lean masses in pre- and post-training moments for all the variables except for the truncal fat in post-training
-121-
G Model
4
Table 1
Descriptive characteristics of the participants.
Control group (n = 13)
Age (years)
Weight (kg)
Height (cm)
Tanner (I/II/III/IV/V)
BMI (kg/m2)
Percentage of fat (%)
Exercise group (n = 12)
Pre-training
Post-training
Pre-training
Post-training
15.4 2.5
48.7 10.7
146.8 10.7
1/2/1/5/6
22.4 3.4*
25.2 8.1
16.0 2.5
49.5 10.6
148.3 10.2
0/3/1/3/8
22.3 3.2
24.3 8.0
13.7 2.6
40.1 9.6
141.9 12.5
3/0/3/2/5
19.6 2.7
24.3 6.0
14.3 2.6
41.8 9.8
142.8 12.4
3/0/2/3/5
20.2 2.6
24.4 5.6
BMI: body mass index.
*
p < 0.05 control group vs. exercise group.
Table 2
Values of fat and lean masses measured by dual energy X-ray absorptiometry, adjusted by increments in height and in Tanner, before and after the training.
DXA measurement
Fat mass (kg)
Whole body
Trunk
Lower limbsa
Upper limbsa
Lean mass (kg)
Whole body
Lower limbsa
Upper limbsa
Control group (n = 13)
Pre-training
Post-training
Mean SD
Mean SD
12.35 1.31*
4.53 0.58*
2.76 0.30*
0.78 0.08*
12.01 1.25*
4.41 0.53
2.69 0.29*
0.75 0.08*,y
35.45 2.03*
5.71 0.38*
1.72 0.14*
35.88 2.18*
5.75 0.41*
1.75 0.13*
Exercise group (n = 12)
Adjusted %
change
Pre-training
Post-training
Mean SD
Mean SD
2.75*
2.65*
2.54*
4.52*
9.19 1.36
3.32 0.60
2.01 0.31
0.56 0.08
1.21*
0.70*
2.06
29.21 2.11
4.48 0.40
1.43 0.15
Interaction group
by time
Adjusted %
change
9.65 1.30
3.58 0.56
2.09 0.30
0.57 0.08
5.01
7.83
3.98
2.09
p = 0.061
p = 0.113
p = 0.100
p = 0.060
30.75 2.28y
4.83 0.43y
1.46 0.14
5.27
7.81
2.18
p = 0.027
p = 0.021
p = 0.935
In bold significant interaction.
a
The values for upper and lower limbs are the mean of right and left limb.
*
p < 0.05 control group vs. exercise group.
y
p < 0.05 pre vs. post.
compared to CG (all p < 0.05, Table 2). EG group significantly increased total and lower limbs lean mass after the training
with no significant changes in fat mass, CG significantly decreased upper limbs fat mass (all p < 0.05, Table 2). Changes in fat
and lean masses were significantly higher in the EG compared to CG (all p < 0.05, Table 2). Time by exercise interactions in
whole body and lower limbs lean mass and in upper limbs fat mass were found (all p < 0.05, Table 2).
4. Discussion
Children and adolescents with DS were able to increase their total, upper and lower limbs lean mass following 21 weeks of
conditioning and plyometric jumps training, whereas no effect in fat mass were observed. Although a previous study
evaluated changes in body composition in adolescents with DS (Ordonez et al., 2006), to the best of our knowledge, this is the
first study reporting changes in soft tissues measured with DXA, in youths with DS as a consequence of a training program. As
there were not withdrawals in the EG, it seems that the training program was attractive and easily adherent for this specific
population.
The increments in whole body and in lower limbs lean mass observed in the EG may be a direct effect of the muscular
adaptation to the exercise, suggested by the significant group by time interactions. This point could indicate that the
characteristic low lean mass of this population might be compensated thorough specific training programs. The association
of lean mass with cardiovascular fitness and, as a consequence with health (Ortega et al., 2005, 2008), let us think that
exercising is an effective method of improving health from childhood and adolescence in persons with DS.
Due to the kind of training performed changes in fat mass were less likely to happen. In fact, no significant changes in fat
mass occurred in the EG, and only a significant change in upper limbs fat mass was observed in the CG which may be due to
some other factors, such as dietary intake, physical activity levels or sedentary time during the training period which are
important variables to be controlled in future studies. Perhaps the training increased appetite in those that exercised with
their fat intake being higher. Another alternating was that the EG were more tired, due to the trainings and so they spent
more sedentary time the rest of the day. Contrarily to our results, Ordonez et al. (2006) showed a reduction on the percentage
of fat of adolescents with DS, however some important differences between studies can be found; they measured percentage
of fat using skinfolds thickness (instead of DXA) and the participants exercised 30–60 min three times per week (instead of
-122-
G Model
5
25 min twice per week) which result in at least almost double time of work out per week (90 vs. 50 min). In addition, the
exercise mode (aerobic vs. combined) was also different. Finally, the fact that the participants from the Ordoñez et al. study
had a higher percentage of fat compared to ours at baseline (31.8% vs. 24%) could also influence the adiposity changes
observed.
A limitation to this study may be that we did not perform traditional strength training based on percentages of 1maximum repetition; otherwise too difficult to deal with this population. However, our protocol was well established and
defined, and therefore can be easily replicated. The strengths of this study were the inclusion of both genders in the design,
the use of a control group of youths with DS, and the sample size, which although not a very large one, is larger than that of
any other intervention study including training with children and adolescents with DS.
5. Conclusions
Our findings suggest that a 21-week training program consisting of 2 sessions of 25 min of conditioning combined with
jumps training is an effective method to increase lean mass in youths with DS.
The association between lean mass with cardiovascular fitness makes these results promising for this population. Further
research should be conducted to explore other training methods using less family time, being easier to perform by the
participants and easier to control by the specialists.
Conflict of interest
There are no conflicts of interest or financial disclosures for any author of this manuscript. None of the authors have any
financial interest.
Acknowledgements
The authors want to thank
and dedication to the project.
their support. This work was
Innovación de España (Red de
00046/ACTI).
all the children and their parents that participated in the study for their understanding
Special thanks are given to Fundación Down Zaragoza and Special Olympics Aragon for
supported by Gobierno de Aragón (Proyecto PM 17/2007) and Ministerio de Ciencia e
investigación en ejercicio fı́sico y salud para poblaciones especiales-EXERNET-DEP2005-
References
(Silver Spring), 15, 1918–1924.
Ara, I., Sanchez-Villegas, A., Vicente-Rodriguez, G., Moreno, L. A., Leiva, M. T., Martinez-Gonzalez, M. A., et al. (2010). Physical fitness and obesity are associated in a
dose-dependent manner in children. Annals of Nutrition and Metabolism, 57, 251–259.
Calbet, J. A., Perez-Gomez, J., Vicente-Rodriguez, G., Ara, I., Olmedillas, H., Chavarren, J., et al. (2008). Look before you leap: On the issue of muscle mass assessment
by dual-energy X-ray absorptiometry (reply to Jordan Robert Moon comments). European Journal of Applied Physiology, 104, 587–588.
Dietz, W. H. (1998). Health consequences of obesity in youth: Childhood predictors of adult disease. Pediatrics, 101, 518–525.
Ebbeling, C. B., Pawlak, D. B., & Ludwig, D. S. (2002). Childhood obesity: Public-health crisis, common sense cure. Lancet, 360, 473–482.
Implications for genetic counselling. Clinical Genetics, 62, 390–393.
González-Agüero, A., Ara, I., Moreno, L. A., Vicente-Rodriguez, G., & Casajús, J. A. (2011). Fat and lean masses in youths with Down syndrome: Gender differences.
Research in Developmental Disabilities, 32, 1685–1693.
González-Agüero, A., Vicente-Rodriguez, G., Moreno, L. A., & Casajús, J. A. (2010). Dimorfismo sexual en grasa corporal en adolescentes con sı́ndrome de Down.
Revista Española de Obesidad, 8, 28–33.
González-Agüero, A., Villarroya, M. A., Vicente-Rodriguez, G., & Casajús, J. A. (2009). Masa muscular, fuerza isométrica y dinámica en las extremidades inferiores
de niños y adolescentes con sı́ndrome de Down. Biomecánica, 17, 46–51.
Gutin, B., Litaker, M., Islam, S., Manos, T., Smith, C., & Treiber, F. (1996). Body-composition measurement in 9-11-y-old children by dual-energy X-ray
absorptiometry, skinfold-thickness measurements, and bioimpedance analysis. American Journal of Clinical Nutrition, 63, 287–292.
Heyward, V. H. (2006). Advanced fitness assessment & exercise prescription (5th ed.). Champaign, IL: Human Kinetics.
Lewis, C. L., & Fragala-Pinkham, M. A. (2005). Effects of aerobic conditioning and strength training on a child with Down syndrome: A case study. Pediatric Physical
Therapy, 17, 30–36.
Luke, A., Sutton, M., Schoeller, D. A., & Roizen, N. J. (1996). Nutrient intake and obesity in prepubescent children with Down syndrome. Journal of the American
Dietetic Association, 96, 1262–1267.
McArdle, W., Katch, F., & Katch, V. (2007). Exercise physiology: Energy nutrition and human performance (6th ed.). Baltimore, MD: Lippincott Williams & Willkins.
Millar, A. L., Fernhall, B., & Burkett, L. N. (1993). Effects of aerobic training in adolescents with Down syndrome. Medicine and Science in Sports and Exercise, 25, 270–
274.
Ordonez, F., Rosety, M., & Rosety-Rodriguez, M. (2006). Influence of 12-week exercise training on fat mass percentage in adolescents with Down syndrome.
Medical Science Monitor, 12, CR416–CR419.
Ortega, F. B., Ruiz, J. R., Castillo, M. J., Moreno, L. A., Gonzalez-Gross, M., Warnberg, J., et al. (2005). Low level of physical fitness in Spanish adolescents. Relevance
for future cardiovascular health (AVENA study). Revista Española de Cardiologıá, 58, 898–909.
Ortega, F. B., Ruiz, J. R., Castillo, M. J., & Sjostrom, M. (2008). Physical fitness in childhood and adolescence: A powerful marker of health. International Journal of
Obesity (London), 32, 1–11.
-123-
G Model
6
Svendsen, O. L., Haarbo, J., Hassager, C., & Christiansen, C. (1993). Accuracy of measurements of body composition by dual-energy X-ray absorptiometry in vivo.
American Journal of Clinical Nutrition, 57, 605–608.
Tanner, J. M., & Whitehouse, R. H. (1976). Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Archives of
Disease in Childhood, 51, 170–179.
Varela, A. M., Sardinha, L. B., & Pitetti, K. H. (2001). Effects of an aerobic rowing training regimen in young adults with Down syndrome. American Journal of Mental
Retardation, 106, 135–144.
Weber, R., & French, R. (1988). Down’s syndrome adolescents and strength training. Clinical Kinesiology, 42, 13–21.
-124-
Workflow 4
Conditioning including plyometric jumps training improves
cardiovascular fitness in youths with Down syndrome.
Journal:
Manuscript ID:
Adapted Physical Activity Quarterly
APAQ-2011-0105
rP
Fo
Manuscript Type:
Keywords:
Article
exercise training, functional performance, trisomy 21, maximal treadmill
test, health
r
ee
ew
vi
Re
ScholarOne, 375 Greenbrier Drive, Charlottesville, VA, 22901
-125-
Page 1 of 27
Workflow 4
Abstract (143 words)
2
We aimed to determine whether youths with Down syndrome (DS) were able to
3
improve their cardiovascular fitness (CVF) after 21 weeks of physical conditioning
4
including plyometric training. Twenty-six participants with DS aged 10 to 19 years
5
participated in the study. Participants were divided into two groups: exercise (DS-E)
6
and non-exercise (DS-NE). Time of exercise, peak of oxygen consumption (VO2peak),
7
respiratory exchange ratio (RERpeak), heart rate (HRpeak) and minute ventilation (VEpeak)
8
of the participants were assessed thorough a maximal treadmill test, at baseline and after
9
the intervention. After intervention, DS-E group increased all their cardiovascular
r
Fo
1
parameters compared to baseline levels (all p<0.05). Additionally, and despite similar
11
baseline values, DS-E showed higher VO2peak, RERpeak and HRpeak than the DS-NE after
12
training (all p<0.05). Overall, 21 weeks of physical conditioning including plyometric
13
jumps seem to be an effective method to improve CVF in youths with DS.
15
Keywords: exercise, functional capacity, trisomy 21, maximal treadmill test, health
ev
16
R
er
14
Pe
10
There are no conflicts of interest or financial disclosures for any author of this
18
manuscript. None of the authors have any financial interest.
w
ie
17
-126-
Workflow 4
Page 2 of 27
1
Introduction
2
Down syndrome (DS) is a genetic condition accompanied with intellectual disability
3
and more than 80 clinical characteristics (Pueschel, 1990), some of them related to
4
exercise (Pitetti, Rimmer, & Fernhall, 1993). Several authors have described lower
5
levels of cardiovascular fitness (CVF) in individuals with DS as compared with their
6
counterparts without DS, with or without intellectual disability, at all ages (Baynard,
7
Pitetti, Guerra, Unnithan, & Fernhall, 2008; Baynard, Unnithan, Pitetti, & Fernhall,
8
2004; Fernhall et al., 1996; Guerra-Balic, Cuadrado-Mateos, Geronimo-Blasco, &
9
Fernhall, 2000; Pitetti, Climstein, Campbell, Barrett, & Jackson, 1992). This fact seems
rP
Fo
1
to be especially relevant, since CVF is considered a powerful marker of health during
11
childhood and adolescence, mainly due to its inverse relationship with total and
12
abdominal adiposity, and direct relation with reduced cardiovascular disease risk factors
13
and increased skeletal health (Ortega, Ruiz, Castillo, & Sjostrom, 2008). In addition, it
14
is also known that adequate CVF favors daily autonomy in persons with special
15
requirements (like persons with DS) later in life (Toulotte, Fabre, Dangremont, Lensel,
16
& Thevenon, 2003; Verschuren et al., 2007), and predicts functional tasks in persons
17
with DS (Cowley et al., 2010). Thus, due to the increase in the lifespan of persons with
18
DS (Glasson et al., 2002), and in order to sustain long-term employment, independence
19
and quality of life, CVF seems to be a key factor that should be promoted from
20
childhood and adolescence.
21
It is well established that training programs improve CVF in children and adolescents
22
with or without special requirements (such as type 1 diabetes or cerebral palsy patients)
23
(D'Hooge et al.; Heyward, 2006; McArdle, Katch, & Katch, 2007; Verschuren et al.,
24
2007); however, it has not been entirely established whether this occurs also in children
25
and adolescents with DS (González-Agüero et al., 2010). A systematic review
r
ee
10
ew
vi
Re
-127-
Page 3 of 27
Workflow 4
2
emphasized the effectiveness of training programs designed to improve CVF among
2
people with DS (Dodd & Shields, 2005), including some studies with adults in which
3
their ability to improve some functional characteristics was observed following exercise
4
training programs (Rimmer, Heller, Wang, & Valerio, 2004; Tsimaras, Giagazoglou,
5
Fotiadou, Christoulas, & Angelopoulou, 2003).
6
However, only a few studies carried out training programs exclusively with children
7
and/or adolescents with DS (Lewis & Fragala-Pinkham, 2005; Millar, Fernhall, &
8
Burkett, 1993; Ordonez, Rosety, & Rosety-Rodriguez, 2006; Varela, Sardinha, &
9
Pitetti, 2001; Weber & French, 1988), and their information regarding improvements in
r
Fo
1
CVF was inconclusive. The previously performed training programs take from 45
11
minutes to more than one hour per training session, most of them 3 times per week.
12
Since youths with DS have several extra-classes to attend (such as speech therapy and
13
phoniatrics), time used in training is an important factor to be taken into account in this
14
population. Other types of training could be interesting to study in youths with DS,
15
since aerobic training may result repetitive for those children and take more than a few
16
time. Plyometric training is a type of exercise that requires various jumps in place or
17
rebound jumping, and it has been demonstrated that enhances strength and power in
18
lower limbs, as well as running and jumping performance (Johnson, Salzberg, &
19
Stevenson; Markovic & Mikulic; Perez-Gomez et al., 2008). It has been also
20
demonstrated that plyometric depth jumping has similar energy system requirements
21
(termed “aerobic power” by Willmore and Costill) which should enhance maximal
22
oxygen consumption (VO2max) (Brown, Ray, Abbey, Shaw, & Shaw).
23
Therefore, the aim of the present study was to determine whether youths with DS are
24
able to improve their CVF, following a 21-week training program consisting of 2
w
ie
ev
R
er
Pe
10
-128-
Workflow 4
Page 4 of 27
3
1
sessions per week of 25 minutes of physical conditioning including plyometric jumps
2
training.
3
Material and method
5
Participants
6
A total sample of 27 children and adolescents with DS (12 females and 15 males) aged
7
10 to 19 years at baseline were recruited from different schools and institutions in
8
Aragón (Spain). Fourteen participants (8 females and 6 males) were randomly assigned
9
to the exercise group (DS-E) and performed the training program (in addition to their
10
common weekly activities); the remaining 13 participants (DS-NE) continued with their
11
common weekly activities. A full clinical history, including illnesses or surgical
12
interventions, was collected for each individual. Seven participants had been diagnosed
13
of hypothyroidism in the past (3 in the DS-E group) and they were taking medication
14
during the study (levothyroxine sodium: 3 of them taking Levothroid, the other 4
15
Eutirox). In addition, eleven participants had congenital heart disease (7 in DS-E
16
group), nine of them needing surgery (6 in the DS-E group).
17
Both parents and children were informed about the aims and procedures, as well as the
18
possible risks and benefits of the study. Written informed consent was obtained from all
19
the participants and their parents or guardians. The study was performed in accordance
20
with the Helsinki Declaration of 1961 (revised in Edinburgh, 2000) and was approved
21
by the Research Ethics Committee of the Government of Aragon (CEICA, Spain).
22
Anthropometry
23
All participants were measured for height with a stadiometer without shoes and
24
minimum clothing to the nearest 0.1 cm (SECA 225, SECA, Hamburg, Germany), and
r
ee
rP
Fo
4
ew
vi
Re
-129-
Page 5 of 27
Workflow 4
4
weighed to the nearest 0.1 kg (SECA 861, SECA, Hamburg, Germany). The body mass
2
index (BMI) was calculated as weight (kg) divided by height squared (m2).
3
4
Pubertal development was determined by direct observation by a physician according to
5
the 5 stages proposed by Tanner and Whitehouse (Tanner & Whitehouse, 1976).
6
Testing procedures before and after the 21-week period
7
Previous to maximal testing, an experienced cardiologist examined each participant,
8
giving permission to participate in the study. Participants were familiarized with the
9
laboratory and testing protocols prior to any data collection. Data collection started
r
Fo
1
when participants were able to easily walk on the treadmill (Quasar Med 4.0,
11
h/p/cosmos, Nussdorf-Traunstein, Germany) with the mask fitted. A walking-graded
12
protocol was employed to assess CVF (Table 1). Starting at a comfortable walking pace
13
for each participant (2.4 or 3.2 km/h), speed was increased by 0.8 km/h every 2 minutes
14
until participants were not able to walk without running (4.8 or 5.6 km/h). Then the
15
grade was increased 4% every minute until exhaustion (until a maximum of 24%). A
16
medicine doctor, specialist in sports medicine, supervised the whole test, and also
17
examined the participants prior exercising.
18
Respiratory gas-exchange data were measured ‘breath-by-breath’ using an open circuit
19
spirometry (Oxycon Pro, Jaeger/Viasys Healthcare, Hoechberg, Germany). Peak oxygen
20
uptake (VO2peak), peak respiratory exchange ratio (RERpeak) and peak minute ventilation
21
(VEpeak) were recorded as the highest average values obtained for any continuous 30-
22
second period. The metabolic cart was calibrated with a known gas and volume prior to
23
the first test each day as recommended by the company. Electrocardiogram (ECG) was
24
used to record heart rate, utilizing a 12-lead system before, and during the whole test.
25
Blood pressure was also measured for safety purposes prior any testing (M3, HEM-
w
ie
ev
R
er
Pe
10
-130-
Workflow 4
Page 6 of 27
5
7200-E, Omron Healthcare Europe, Hoofddorp, the Netherlands). These tests were
2
performed at baseline and after the intervention, and the increments in VO2peak, RERpeak,
3
HRpeak, VEpeak, and time of exercise between baseline and post-intervention points were
4
calculated for each group using the formula [(post-pre)/pre]x100.
5
Intervention: training program
6
Those participants allocated to the intervention group exercised 2 days per week, each
7
session was conducted with a maximum of 10 participants. The exercise sessions were
8
supervised by one researcher and one to three assistants. The training sessions took
9
place in three different places: 2 rooms in 2 different gyms of the city, and 1 adapted
rP
Fo
1
room in the institution were the children attended other classes; the same material was
11
carried out by the researcher at the different places. The first week (2 trainings) was
12
used as familiarization on how to use the material/equipment and how to perform the
13
exercises. Each training session consisted of 5 minutes warm-up activities, 10 to 15
14
minutes session, and 5 minutes cool-down. The training consisted of several sets in a
15
circuit of 4 stages according to the training plan (Figure 1).
16
r
ee
10
ew
vi
Re
17
1. Jumps: standing vertical jump, jump with run-in, drop jump (height jumped
18
between 40 and 50 centimetres), drop jump+horizontal jump (height jumped
19
between 40 and 50 centimetres). From the third week, participants carried
20
adapted-medicine balls while performing the jumps.
21
2. Press-ups on the wall: participants placed their hands on a wall and performed
22
press-ups standing but with their feet separate 30 to 50 centimetres from the
23
wall.
24
3. Elastic-fitness bands: lateral rows, bicep curls and frontal rows.
-131-
Page 7 of 27
Workflow 4
6
1
2
4. Adapted-medicine balls: standing throws and catches, with a distance between
participants of 3 to 4 meters.
The 13 participants were divided into four intensity-groups (quartiles) depending on
4
their body weight, and they worked out individually. When participants showed
5
excessive facility for performing exercises, they were transferred to the next intensity-
6
group. There were 4 fitness bands colours (yellow, green, blue and purple) of increasing
7
resistance and 4 medicine balls (1, 2, 3 and 4 kg), each one being assigned to a group
8
depending on the strength demanded to perform the exercises. Instructional and
9
motivational reinforcements were constant during the whole training period; with the
r
Fo
3
greatest efforts in the correct execution of the exercises and number of repetitions.
11
Every group followed the same schedule of exercises with a different band colour and
12
ball (Figure 1).
13
A minimum attendance of 70% was required to be included in the exercise group. If
14
minimum assistance was not achieved, the participant data were excluded of the
15
analyses.
16
Statistics
17
All statistical analyses were performed with the Statistical Package for the Social
18
Sciences (SPSS) version 15.0 for Windows (SPSS Inc., Chicago, IL, USA). Mean and
19
standard deviations are given as descriptive statistics; otherwise they are stated.
20
ANOVA tests were performed to evaluate whether sex-training interactions were
21
present within the participants. Chi square test was used to evaluate the differences in
22
Tanner maturational status. Due to the sample size (under 30 participants), non-
23
parametric statistical tests were applied. Mann-Whitney U tests were used to evaluate
24
differences between groups (DS-E vs. DS-NE), and Wilcoxon-Cox tests were used to
25
evaluate differences between baseline and post-intervention points within each group
w
ie
ev
R
er
Pe
10
-132-
Workflow 4
Page 8 of 27
7
1
for all the studied variables, and for the calculated increments. An additional ANCOVA
2
test, including percentage of change in HRpeak (pre- to post-training) as a covariate, to
3
prevent a possible poor effort during the pre-training effort test, was performed to test
4
differences between VO2peak. Statistical significance was set at p<0.05.
5
Results
7
Adherence to training and possible adverse effects
8
Adherence to training averaged 81.8±9.2%. Only one participant (female) did not
9
achieve the minimum 70% assistance to the intervention program (45%) and her data
10
were excluded of the analyses. No withdrawals from any group occurred. Noticeably,
11
no major adverse effects and no major health problem were noted in the participants of
12
both groups over the 21-week period.
13
14
Age and physical characteristics of the participants are summarized in Table 2. DS-E
15
and DS-NE groups showed similar values for height, weight, Tanner status and BMI at
16
both, baseline and post-intervention points.
17
Cardiovascular fitness
18
Table 3 lists peak cardiorespiratory data for DS-NE and DS-E groups at baseline and
19
post-intervention points. There were no differences at baseline between DS-E and DS-
20
NE groups in any of the studied variables.
21
Post-intervention, the DS-E group showed higher values for VO2peak, HRpeak and
22
RERpeak compared with the DS-NE group (all p<0.05; Table 3). Further adjustment for
23
percentage of change in HRpeak (pre- to post-training) did not substantially change the
24
results for VO2peak (data not shown).
r
ee
rP
Fo
6
ew
vi
Re
-133-
Page 9 of 27
Workflow 4
8
1
In addition, the DS-E group increased the time of exercise, VO2peak, RERpeak, HRpeak and
2
VEpeak from baseline to post-intervention, while the DS-NE group improved the VEpeak
3
(all p<0.05; Table 3).
4
Percentages of change for each group are plotted in Figure 2. Overall, the DS-E group
5
showed greater (but not significant) improvements in all outcome measures for CVF
6
compared with the DS-NE, the largest gains occurred in VEpeak and VO2peak (28 and 16
7
per cent, respectively; Figure 2).
9
Discussion
r
Fo
8
In general, our results show that children and adolescents with DS are able to improve
11
their CVF after a 21-week physical conditioning including plyometric jumps training.
12
To the best of our knowledge, this is the first study to report significant improvements
13
in CVF in children and adolescents with DS as a consequence of a training program. As
14
there were no withdrawals, it seems that the training program was attractive and easily
15
adhered to this specific population.
16
Previous studies in adolescents and young adults with DS showed improvements in
17
work capacity after training (Millar, Fernhall, & Burkett, 1993; Varela, Sardinha, &
18
Pitetti, 2001); however, this is the first evidence of improvements in CVF in youths
19
with DS as a consequence of a training program.
20
Millar et al.(Millar, Fernhall, & Burkett, 1993) performed a study with 14 participants
21
(11 males) with DS (17.5 mean age) and they did not achieve improvements in
22
cardiovascular parameters following a 10-week aerobic training program, although an
23
improvement in walking capacity was found. Similar results were obtained by Varela et
24
al. (Varela, Sardinha, & Pitetti, 2001) after a 16-week rowing training regimen in 16
25
young males with DS (21.3 mean age). On the other hand, studies in adults with DS
w
ie
ev
R
er
Pe
10
-134-
Workflow 4
Page 10 of 27
9
showed rather consistent findings on VO2peak improvements: Tsimaras et al. (Tsimaras,
2
Giagazoglou, Fotiadou, Christoulas, & Angelopoulou, 2003) showed improvements in
3
VO2peak, VEpeak and time of exercise in 25 adult males after a 12-week jog-walk interval
4
training program (3 days/week). Along the same line, Rimmer et al. (Rimmer, Heller,
5
Wang, & Valerio, 2004) found improvements in VO2peak, HRpeak, time of exercise and
6
work capacity following a 12-week combined aerobic and strength training (4
7
days/week) in 52 adults (23 males) with DS (39.4 mean age). Mendonca et al.
8
(Mendonca & Pereira, 2009) observed improvements in VO2peak, VEpeak and time of
9
exercise after a 28-week aerobic training (2 days/week) in 12 adult males with DS (34.5
10
mean age) and, in another study (Mendonca, Pereira, & Fernhall), increased VO2peak and
11
walking economy in 13 adults (36.5 mean age) with DS after a 12-week combined
12
aerobic and resistance training (3 days/week).
13
It is important to notice that, even before the training period, the values of VO2peak
14
achieved by the participants with DS in our study were higher than the values observed
15
in previous studies carried out in youths with DS. Mean values for VO2peak (mL/kg/min)
16
ranged from 30.1 to 36.4 in our study, compared with 31.1 to 32.1 in Varela (Varela,
17
Sardinha, & Pitetti, 2001), 25.5 to 26.9 in Millar (Millar, Fernhall, & Burkett, 1993) and
18
29.6 to 35.7 in Tsiamras (Tsimaras, Giagazoglou, Fotiadou, Christoulas, &
19
Angelopoulou, 2003). Indeed, according to the percentiles for VO2peak designed by
20
Baynard et al. (Baynard, Pitetti, Guerra, Unnithan, & Fernhall, 2008), our participants
21
showed levels above the 70th percentile. This fact makes our findings even more
22
relevant, as improvements in cardiovascular parameters were achieved in a population
23
with a high CVF, higher than the average for its condition.
24
Although the participants in our study were able to improve their CVF, our training did
25
not include a classical cardiovascular training program, as the participants performed
r
ee
rP
Fo
1
ew
vi
Re
-135-
Page 11 of 27
Workflow 4
10
physical conditioning including plyometric jumps training. Pitteti and Boneh found a
2
significant and strong positive relationship between VO2peak and leg strength in persons
3
with DS; they suggested that leg strength may be an important contributor to VO2peak in
4
persons with intellectual disabilities (Pitetti & Boneh, 1995). Plyometrics have been
5
showed as a type of training which enhances muscular strength (mainly in lower limbs)
6
and running performance (Markovic & Mikulic; Saez-Saez de Villarreal, Requena, &
7
Newton). Since the type of maximal test performed in this study requires great lower
8
limb strength, part of the increments in VO2peak could be due to increments in power
9
and/or muscular strength of the participants, and increments in the resistance to
r
Fo
1
peripheral fatigue. The studies of Rimmer (Rimmer, Heller, Wang, & Valerio, 2004)
11
and Mendonca (Mendonca, Pereira, & Fernhall) included strength conditioning in their
12
training programs with adults, and they obtained improvements in VO2peak and other
13
cardiovascular parameters. Furthermore, Rimmer proposed to explore the magnitude of
14
change in VO2peak that can be attained through an only-strength training program; the
15
magnitude of change (increment from baseline to post-intervention) in the VO2peak of
16
the present study (15.6%) is rather similar to that observed in the study of Rimmer et al.
17
(14.1%) (Rimmer, Heller, Wang, & Valerio, 2004) and is in the range of the results of
18
both studies by Mendonca et al. (6% and 27.8 %) (Mendonca & Pereira, 2009;
19
Mendonca, Pereira, & Fernhall).
20
Since persons with DS have a high oxygen cost of locomotion (Mendonca, Pereira, &
21
Fernhall, 2009; Mendonca, Pereira, Morato, & Fernhall), and physical fitness has been
22
demonstrated to predict the ability of adults with DS to perform functional tasks in daily
23
living (Cowley et al., 2010), these are important findings that will make possible
24
improve daily actions and independence, now and later in life, in this population. Given
25
that CVF is a component of physical fitness highly related with present and future
w
ie
ev
R
er
Pe
10
-136-
Workflow 4
Page 12 of 27
11
health in youths, and also with cardiovascular risk factors (Ortega, Ruiz, Castillo, &
2
Sjostrom, 2008), it is a very important factor to be enhanced in this specific population
3
at higher risk of cardiovascular and bone-related diseases (González-Agüero, Ara,
4
Moreno, Vicente-Rodriguez, & Casajús, 2011; González-Agüero, Vicente-Rodriguez,
5
Moreno, & Casajus, 2011). Even though persons with DS may have lower
6
atherosclerotic risk factors (Draheim, McCubbin, & Williams, 2002); the continuous
7
increase in life expectancy in the DS population (Bittles & Glasson, 2004), together
8
with high levels of adipose tissue found in this population (especially in the trunk)
9
(González-Agüero, Ara, Moreno, Vicente-Rodriguez, & Casajús, 2011) make the
rP
Fo
1
increments in CVF an important issue to be taken into account.
11
As stated above, our study showed similar results to those previous in adults with DS,
12
which achieved improvements in CVF (Mendonca & Pereira, 2009; Mendonca, Pereira,
13
& Fernhall; Rimmer, Heller, Wang, & Valerio, 2004; Tsimaras, Giagazoglou, Fotiadou,
14
Christoulas, & Angelopoulou, 2003). In contrast to ours, the absolute duration of those
15
was 12 weeks (3 or 4 times per week) or 28 weeks (2 times per week). Our results
16
indicate that improvements in CVF may be possible with a 21-week training program,
17
twice a week, in youths with DS. As free-time in families with DS children is reduced
18
due to the numerous extra activities they participate in, training programs that consume
19
the lowest possible time should be promoted. This is not against the promotion of
20
physical activity and other kind of studies, promoting adherence to physical activities
21
should be conducted within this population.
22
Study limitations and strengths
23
There were several limitations to this study that should be recognized. First, peak
24
treadmill exercise is effort-dependent; consequently, it was possible to hypothesize that
25
the participants with DS produced lower effort, or that struggled more in the post-
r
ee
10
ew
vi
Re
-137-
Page 13 of 27
Workflow 4
12
training assessment. However, the fact that our participants have performed 4 of 5
2
maximal tests previously makes us believe that our data were not influenced by a lack
3
of effort in participants. Also the differences in VO2peak even when adjusting by HRpeak
4
is a good indicative of the effort performed. The protocol that we used has been not
5
previously validated in this population; however, it meets the criteria for VO2peak
6
testing: progressive increments in effort to a point which the participant simply refuses
7
to continue exercising. Also related to the type of protocol used, as stated before, great
8
lower limbs strength could help participants to reach higher levels of exercise in this
9
graded walking protocol. Therefore, the plyometric training could have increased the
r
Fo
1
resistance of the participants to peripheral fatigue, being this, partially, the cause of the
11
increments in CVF. Secondly, the proposed training was not a usual strength training
12
based on working at different percentages of 1-maximum repetition in diverse
13
equipment in a gym; simple exercises, without complex material was considerate to be a
14
better training to work with people with intellectual disabilities. And finally, our
15
experimental design did not include a control group of youths without disabilities which
16
performed the same training than the DS-E group did; therefore, the degree to which
17
these findings would occur in the same manner in controls without DS remains
18
unknown. Although the inclusion of participants with congenital heart diseases may
19
difficult comparisons with previous studies, it is important to notice that, this decision
20
was based on the fact that approximately 40% of the persons with DS have congenital
21
heart diseases (Pueschel, 1990). The exclusion of these youths would make impossible
22
to generalize the results of this study to all the youth-population with DS. The strengths
23
in this study were: the inclusion of both genders in the design, the use of a control group
24
of youths with DS; the use of a laboratory treadmill exercise test to evaluate
25
cardiovascular parameters; and, finally, the sample size, which although not a very large
w
ie
ev
R
er
Pe
10
-138-
Workflow 4
Page 14 of 27
13
1
sample, is larger than that of any other reported study including training with children
2
and adolescents with DS.
3
Conclusions
5
In summary, our findings suggest that a 21-week training program consisting of 2
6
sessions per week of 25 minutes of physical conditioning including plyometric jumps
7
training is an effective method to improve CVF in youths with DS, as shown by the
8
increased VO2peak at the end of the training program. Furthermore, time to exhaustion
9
has also been increased, establishing work capacity as a variable able to be improved by
rP
Fo
4
training.
11
The association between fitness levels with autonomy and functional daily tasks later in
12
life in persons with special requirements (Cowley et al., 2010; Toulotte, Fabre,
13
Dangremont, Lensel, & Thevenon, 2003; Verschuren et al., 2007), and the relationship
14
of CVF with present and future health (Ortega, Ruiz, Castillo, & Sjostrom, 2008), make
15
these results promising for this population. Further research should be conducted to
16
explore other training methods, using less family time, making it easier to perform by
17
the participants and easier to control by the specialists.
ew
vi
Re
18
r
ee
10
-139-
Page 15 of 27
Workflow 4
14
Acknowledgments
2
The authors want to thank all the children and their parents that participated in the
3
study, for their understanding and dedication to the project. Special thanks are given to
4
Fundación Down Zaragoza, Special Olympics Aragon and Colegio Jesús-María El
5
Salvador, for their support. We also thank Scott G Mitchell from the University of
6
Glasgow for his work of reviewing the English style and grammar. This work was
7
supported by Gobierno de Aragón (Proyecto PM 17/2007). There are no potential
8
conflicts of interest that may affect the contents of this work.
9
10
r
Fo
1
w
ie
ev
R
er
Pe
-140-
Workflow 4
Page 16 of 27
15
1
References
2
Baynard, T., Pitetti, K. H., Guerra, M., Unnithan, V. B., & Fernhall, B. (2008). Age-
3
Related Changes in Aerobic Capacity in Individuals with Mental Retardation: A
4
20-yr Review. Medicine and Science in Sports Exercise, 40, 1984-1989.
5
Baynard, T., Unnithan, V. B., Pitetti, K., & Fernhall, B. (2004). Determination of
6
ventilatory threshold in adolescents with mental retardation, with and without
7
Down syndrome,. Pediatric Exercise Science, 16, 126-137.
9
10
11
Bittles, A. H., & Glasson, E. J. (2004). Clinical, social, and ethical implications of
rP
Fo
8
changing life expectancy in Down syndrome. Developmental Medicine and
Child Neurology, 46, 282-286.
Brown, G. A., Ray, M. W., Abbey, B. M., Shaw, B. S., & Shaw, I. (2010) Oxygen
r
ee
12
consumption, heart rate, and blood lactate responses to an acute bout of
13
plyometric depth jumps in college-aged men and women. Journal of Strength
14
and Conditioning Research, 24, 2475-2482.
ew
vi
Re
15
Cowley, P. M., Ploutz-Snyder, L. L., Baynard, T., Heffernan, K., Jae, S. Y., Hsu, S., et
16
al. (2010). Physical fitness predicts functional tasks in individuals with Down
17
syndrome. Medicine and Science in Sports and Exercise, 42, 388-393.
18
D'Hooge, R., Hellinckx, T., Van Laethem, C., Stegen, S., De Schepper, J., Van Aken,
19
S., et al. (2011) Influence of combined aerobic and resistance training on
20
metabolic control, cardiovascular fitness and quality of life in adolescents with
21
type 1 diabetes: a randomized controlled trial. Clinical Rehabilitation, 25, 349-
22
359.
23
Dodd, K. J., & Shields, N. (2005). A systematic review of the outcomes of
24
cardiovascular exercise programs for people with Down syndrome. Archives of
25
Physical Medicine and Rehabilitation, 86, 2051-2058.
-141-
Page 17 of 27
Workflow 4
16
1
Draheim, C. C., McCubbin, J. A., & Williams, D. P. (2002). Differences in
2
cardiovascular disease risk between nondiabetic adults with mental retardation
3
with and without Down syndrome. American Journal of Mental Retardation,
4
107, 201-211.
5
Fernhall, B., Pitetti, K. H., Rimmer, J. H., McCubbin, J. A., Rintala, P., Millar, A. L., et
al. (1996). Cardiorespiratory capacity of individuals with mental retardation
7
including Down syndrome. Medicine and Science in Sports Exercise, 28, 366-
8
371.
9
r
Fo
6
Glasson, E. J., Sullivan, S. G., Hussain, R., Petterson, B. A., Montgomery, P. D., &
Bittles, A. H. (2002). The changing survival profile of people with Down's
11
syndrome: implications for genetic counselling. Clinical Genetics, 62, 390-393.
12
Pe
10
González-Agüero, A., Ara, I., Moreno, L. A., Vicente-Rodriguez, G., & Casajús, J. A.
R
er
13
(2011). Fat and lean masses in youths with Down syndrome: gender differences.
14
Research in Developmental Disabilities, 32, 1685-1693.
González-Agüero, A., Vicente-Rodriguez, G., Moreno, L. A., & Casajus, J. A. (2011).
16
Bone mass in male and female children and adolescents with Down syndrome.
17
Osteoporosis International, 22, 2151-2157.
w
ie
18
ev
15
González-Agüero, A., Vicente-Rodriguez, G., Moreno, L. A., Guerra-Balic, M., Ara, I.,
19
& Casajus, J. A. (2010). Health-related physical fitness in children and
20
adolescents with Down syndrome and response to training. Scandinavian
21
Journal of Medicine and Science in Sports, 20, 716-724.
22
Guerra-Balic, M., Cuadrado-Mateos, E., Geronimo-Blasco, C., & Fernhall, B. (2000).
23
Physical Fitness Levels of Physically Active and Sedentary Adults With Down
24
Syndrome. Adapted Physical Activity Quarterly, 17, 310-321.
-142-
Workflow 4
Page 18 of 27
17
1
2
Heyward, V. H. (2006). Advanced fitness assessment & Exercise prescription (J. Padro,
Trans. fifth ed.). Champaign, Illinois: Human Kinetics.
3
Johnson, B. A., Salzberg, C. L., & Stevenson, D. A. (2011) A systematic review:
4
plyometric training programs for young children. Journal of Strength and
5
Conditioning Research, 25, 2623-2633.
6
Lewis, C. L., & Fragala-Pinkham, M. A. (2005). Effects of aerobic conditioning and
strength training on a child with Down syndrome: a case study. Pediatric
8
Physical Therapy, 17, 30-36.
9
rP
Fo
7
Markovic, G., & Mikulic, P. (2010) Neuro-musculoskeletal and performance
10
adaptations to lower-extremity plyometric training. Sports Medicine, 40, 859-
11
895.
r
ee
12
McArdle, W., Katch, F., & Katch, V. (2007). Exercise physiology: energy, nutrition and
13
human performance. (Sixth ed.). Baltimore, Maryland: Lippincott Williams &
14
Willkins.
ew
vi
Re
15
Mendonca, G. V., & Pereira, F. D. (2009). Influence of long-term exercise training on
16
submaximal and peak aerobic capacity and locomotor economy in adult males
17
with Down's syndrome. Medical Science Monitor, 15, CR33-39.
18
Mendonca, G. V., Pereira, F. D., & Fernhall, B. (2009). Walking economy in male
19
adults with Down syndrome. European Journal of Applied Physiology, 105,
20
153-157.
21
Mendonca, G. V., Pereira, F. D., & Fernhall, B. (2011). Effects of combined aerobic
22
and resistance exercise training in adults with and without Down syndrome.
23
Archives of Physical Medicine and Rehabilitation, 92, 37-45.
-143-
Page 19 of 27
Workflow 4
18
1
Mendonca, G. V., Pereira, F. D., Morato, P. P., & Fernhall, B. (2010). Walking
2
economy of adults with Down syndrome. International Journal of Sports
3
Medicine, 31, 10-15.
4
Millar, A. L., Fernhall, B., & Burkett, L. N. (1993). Effects of aerobic training in
5
adolescents with Down syndrome. Medicine and Science in Sports Exercise, 25,
6
270-274.
7
Ordonez, F., Rosety, M., & Rosety-Rodriguez, M. (2006). Influence of 12-week
exercise training on fat mass percentage in adolescents with Down syndrome.
9
Medical Science Monitor, 12, CR416-419.
10
r
Fo
8
Ortega, F. B., Ruiz, J. R., Castillo, M. J., & Sjostrom, M. (2008). Physical fitness in
Pe
11
childhood and adolescence: a powerful marker of health. International Journal
12
of Obesity (London), 32, 1-11.
R
er
13
Perez-Gomez, J., Olmedillas, H., Delgado-Guerra, S., Ara, I., Vicente-Rodriguez, G.,
Ortiz, R. A., et al. (2008). Effects of weight lifting training combined with
15
plyometric exercises on physical fitness, body composition, and knee extension
16
velocity during kicking in football. Applied Physiology, Nutrition and
17
Metabolism, 33, 501-510.
w
ie
18
ev
14
Pitetti, K. H., & Boneh, S. (1995). Cardiovascular fitness as related to leg strength in
19
adults with mental retardation. Medicine and Science in Sports and Exercise, 27,
20
423-428.
21
Pitetti, K. H., Climstein, M., Campbell, K. D., Barrett, P. J., & Jackson, J. A. (1992).
22
The cardiovascular capacities of adults with Down syndrome: a comparative
23
study. Medicine and Science in Sports and Exercise, 24, 13-19.
-144-
Workflow 4
Page 20 of 27
19
1
Pitetti, K. H., Rimmer, J. H., & Fernhall, B. (1993). Physical fitness and adults with
2
mental retardation. An overview of current research and future directions. Sports
3
Medicine, 16, 23-56.
4
5
6
Pueschel, S. M. (1990). Clinical aspects of Down syndrome from infancy to adulthood.
American Journal of Medical Genetics. Supplement, 7, 52-56.
Rimmer, J. H., Heller, T., Wang, E., & Valerio, I. (2004). Improvements in physical
fitness in adults with Down syndrome. Americal Journal of Mental Retardation,
8
109, 165-174.
9
rP
Fo
7
Saez-Saez de Villarreal, E., Requena, B., & Newton, R. U. (2010) Does plyometric
10
training improve strength performance? A meta-analysis. Journal of Science and
11
Medicine in Sport, 13, 513-522.
r
ee
12
Tanner, J. M., & Whitehouse, R. H. (1976). Clinical longitudinal standards for height,
13
weight, height velocity, weight velocity, and stages of puberty. Archives of
14
Disease in Childhood, 51, 170-179.
ew
vi
Re
15
Toulotte, C., Fabre, C., Dangremont, B., Lensel, G., & Thevenon, A. (2003). Effects of
16
physical training on the physical capacity of frail, demented patients with a
17
history of falling: a randomised controlled trial. Age Ageing, 32, 67-73.
18
Tsimaras, V., Giagazoglou, P., Fotiadou, E., Christoulas, K., & Angelopoulou, N.
19
(2003). Jog-walk training in cardiorespiratory fitness of adults with Down
20
syndrome. Perceptual & Motor Skills, 96, 1239-1251.
21
Varela, A. M., Sardinha, L. B., & Pitetti, K. H. (2001). Effects of an aerobic rowing
22
training regimen in young adults with Down syndrome. American Journal of
23
Mental Retardation, 106, 135-144.
24
25
Verschuren, O., Ketelaar, M., Gorter, J. W., Helders, P. J., Uiterwaal, C. S., & Takken,
T. (2007). Exercise training program in children and adolescents with cerebral
-145-
Page 21 of 27
Workflow 4
20
1
palsy: a randomized controlled trial. Archives of Pediatric and Adolescent
2
Medicine, 161, 1075-1081.
3
4
Weber, R., & French, R. (1988). Down's syndrome adolescents and strength training.
Clinical Kinesiology, 42, 13-21.
5
6
r
Fo
w
ie
ev
R
er
Pe
-146-
Workflow 4
Page 22 of 27
21
Figures legends
Figure 1.Trainig plan for the 21 weeks.
Figure 2. Percentage of change from baseline to post-intervention in cardiovascular
fitness variables (mean and standard error).
VO2peak: peak of oxygen uptake, RERpeak: peak of respiratory exchange ratio; VEpeak:
peak of minute ventilation; HRpeak: peak of heart rate.
r
ee
rP
Fo
ew
vi
Re
-147-
Page 23 of 27
Workflow 4
Table 1. Walking testing protocol.
Speed (km/h) Grade Time (min)
0º
3
2.4
0º
2
3.2
0º
2
4.0
0º
2
4.8
0º
2
5.6
0º
2
5.6
4º
1
5.6
8º
1
5.6
12º
1
5.6
16º
1
r
Fo
0.0
R
er
Pe
20º
1
5.6
24º
1
0.0
0º
3
w
ie
ev
5.6
-148-
Workflow 4
Page 24 of 27
Table 2. Descriptive characteristics of the participants.
BASELINE
POST-INTERVENTION
Exercise
Non-Exercise
Exercise
Non-Exercise
N = 13
N = 13
N = 13
N = 13
Mean ± SD
Mean ± SD
Mean ± SD
Mean ± SD
Age (years)
13.7 ± 2.6
15.6 ± 2.5
14.3 ± 2.6
16.2 ± 2.5
Weight (kg)
40.1 ± 9.6*
48.0 ± 10.7
41.8 ± 9.8
48.6 ± 10.4
141.9 ± 12.5 146.7 ± 11.1
rP
Fo
Height (cm)
Tanner (I/II/III/IV/V)
BMI
142.8 ± 12.4 148.1 ± 10.6
3/0/3/2/5
1/2/1/4/5
2/1/2/2/6
19.3 ± 2.5
22.1 ± 3.3
20.2 ± 2.6
0/3/1/3/6
21.39 ± 3.0
r
ee
BMI: Body mass index; * p<0.05 DS-E vs. DS-NE.
ew
vi
Re
-149-
Page 25 of 27
Workflow 4
1
Table 3. Cardiovascular fitness at baseline and post-intervention.
BASELINE
EXERCISE
POST-INTERVENTION
NO EXERCISE
EXERCISE
Mean ± SD
Time of Exercise (min)
14.4 ± 1.7
14.5 ± 1.7
15.5 ± 1.13†
14.6 ± 2.2
VO2peak (mL/kg/min)
33.1 ± 3.2
30.1 ± 7.2
36.4 ± 3.6†
33.1 ± 3.3*
RERpeak (VCO2/VO2)
1.02 ± 0.09
1.01 ± 0.09
1.10 ± 0.08†
1.04 ± 0.09*
VEpeak (L/min)
42.7 ± 14.8
44.6 ± 11.9
52.6 ± 15.1†
51.3 ± 13.8†
r
Fo
Mean ± SD
HRpeak (bpm)
167.4 ± 10.3 165.6 ± 8.9
Mean ± SD
NO EXERCISE
Mean ± SD
175.5 ± 10.1† 166.7 ± 12.6*
VO2peak: peak of oxygen uptake, RERpeak: peak of respiratory exchange ratio; VEpeak: peak of
Pe
minute ventilation; HRpeak: peak of heart rate.
† p<0.05 Baseline vs. Post-intervention; * p<0.05 DS-E vs. DS-NE
w
ie
ev
R
er
-150-
Workflow 4
Page 26 of 27
rP
Fo
Training plan for the 21 weeks.
307x122mm (150 x 150 DPI)
r
ee
ew
vi
Re
-151-
Page 27 of 27
Workflow 4
r
Fo
ev
R
er
Pe
w
ie
Percentage of change from baseline to post-intervention in cardiovascular fitness variables (mean and
standard error).
130x115mm (300 x 300 DPI)
-152-
Paper for DMCN
A 21-week bone deposition promoting exercise programme
increases bone mass in young people with Down syndrome
Developmental Medicine & Child Neurology
w
ie
ev
rR
Fo
Journal:
Manuscript ID:
Manuscript Type:
Date Submitted by the Author:
Complete List of Authors:
Keywords:
DMCN-OA-11-06-0417.R1
Original Article
n/a
González-Agüero, Alejandro; GENUD research group, Faculty of Health and
Sport Sciences, University of Zaragoza, Zaragoza, Spain
Vicente-Rodríguez, Germán; GENUD research group, Faculty of Health and
Sport Sciences, University of Zaragoza, Zaragoza, Spain
Gómez-Cabello, Alba; GENUD research group, Faculty of Health and Sport
Sciences, University of Zaragoza, Zaragoza, Spain
Ara, Ignacio; GENUD Toledo, University of CAstilla-La Mancha, Toledo,
Spain
Moreno, Luis; GENUD research group, School of Health Sciences, University
of Zaragoza, Zaragoza, Spain
Casajús, José; GENUD research group, Faculty of Health and Sport
Sciences, University of Zaragoza, Zaragoza, Spain
exercise, DXA, Down's syndrome, training, osteogenic
ly
On
Mac Keith Press
-153-
Page 1 of 20
Title page
Title
A 21-week bone deposition promoting exercise programme increases bone mass in
young people with Down syndrome.
Authors
Alejandro González-Agüero BSc1,2, Germán Vicente-Rodríguez PhD1,2, Alba GómezCabello BSc1,2, Ignacio Ara PhD1,3, Luis A. Moreno PhD1,4, José A. Casajús PhD1,2*
Institutions
rR
1
Fo
GENUD (Growth, Exercise, NUtrition and Development) Research Group, University
of Zaragoza, Zaragoza, Spain
ie
ev
2
3
GENUD Toledo Research Group, University of Castilla-La Mancha, Toledo, Spain
4
*Corresponding author
w
José A. Casajús
On
Email: [email protected]
Mailing address: C/ Corona de Aragón 42, Edificio Cervantes 2ªplanta, Grupo GENUD
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
50006, Zaragoza, Spain
Phone: +34 976400338 (ext. 301) Fax: +34 976400340
There are no conflicts of interest or financial disclosures for any author of this
manuscript. None of the authors have any financial interest.
Word count: 2331
1
Mac Keith Press
-154-
Paper for DMCN
Abstract (199 words)
Aim: To determine whether bone mass of young people with Down syndrome (DS) may
increase, following a supervised training program of conditioning including plyometric
jumps during 21 weeks.
Methods: Twenty-eight participants with DS (15 males) aged 10 to 19 years
participated. Participants were randomly divided into exercise (DS-E; n = 14) and nonexercise (DS-NE; n = 14) groups. Total and regional (hip and lumbar spine) bone
mineral content (BMC) and total lean mass were assessed by DXA, at baseline and after
w
ie
ev
rR
Fo
the intervention. Repeated measures ANOVA were applied to test differences between
pre and post-training values for BMC and total lean mass. Differences between
increments were studied with Student’s t-test. Linear regressions were calculated to test
independent relationships.
Results: After the intervention, higher increments in total and hip BMC and total lean
mass were observed in the DS-E group (all p<0.05). A time by exercise interaction was
found for total lean mass (p<0.05). The increment in total lean mass, in height and in
Tanner accounts almost for 60% in the increment in total BMC in the DS-NE group
On
(p<0.05).
Interpretation: Twenty-one weeks of training have a positive effect on the acquisition
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 2 of 20
of bone mass in young people with DS.
Running head: Bone acquisition in young people with Down syndrome
Keywords: exercise, DXA, Down’s syndrome, training, osteogenic
2
Mac Keith Press
-155-
Page 3 of 20
What this paper adds
· Young people with Down syndrome may increase their bone mass following a
physical exercise programme.
· The increment in bone mass could be mediated by an increment in total lean mass
which is also detectable.
rR
Fo
w
ie
ev
ly
On
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
3
Mac Keith Press
-156-
Paper for DMCN
Down syndrome (DS) is a genetic condition accompanied by intellectual disability and
more than 80 clinical manifestations some of them affecting body composition 1. Lower
levels of bone mineral content (BMC) have been observed not only in adults 2-6 but in
children and adolescents with DS 7, 8 compared with their non-DS counterparts. The
acquisition of high bone mass during childhood and adolescence is an important factor
in preventing osteoporosis later in life 9, 10. Since life expectancy of persons with DS has
increased over the last decades over 55 years 11 the incidence of osteoporosis, bone
fragility and related fractures is expected to increase in the coming years.
w
ie
ev
rR
Fo
It is well established that physical activity and, specifically, participation in sport during
growth has an osteogenic effect on growing skeleton in children and adolescents
without disabilities 12-14; however, studies have not yet been made of children and
adolescents with DS 15, who also may benefit from osteogenic exercising. Plyometric
training is a type of exercise that requires various jumps in place or rebound jumping,
and it may increases peak bone mass during adolescence 16. This type of exercise has
been shown to be an effective method for increasing lean mass in adolescents with DS
17
and as bone mass is closely associated with lean mass this is a positive finding. It has
On
also been suggested that in young people, that the mechanical impact resulting from the
plyometric exercise is one of the most osteogenic activities 12, and could enhance the
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 4 of 20
levels of osteocalcin 18, which is an established and extensively used biochemical
marker of bone formation 19.
Thus, the aim of the present study was to determine whether young people with DS are
able to increase their bone-related variables (total and regional BMC) following a 21week training program consisting of 2 sessions per week of 25 minutes of conditioning
and plyometric jumps training.
4
Mac Keith Press
-157-
Page 5 of 20
Material and methods
Participants
A total sample of 28 children and adolescents with DS (13 females and 15 males) aged
10 to 19 years at baseline were recruited from different schools and institutions in
Aragon (Spain). Participants were randomly assigned to the control group (DS-NE;
n=14: 5 females and 9 males) or to the exercise group (DS-E; n=14: 8 females and 6
males), who followed the training program. Seven participants were taking medication
during the study (levothyroxine sodium), 4 in the DS-NE group and 3 in the DS-E
Fo
group. Both parents and children were informed about the aims and procedures, as well
rR
as the possible risks and benefits of the study. Written informed consent was obtained
from all the participants and their parents or guardians. The study was performed in
ie
ev
accordance with the Helsinki Declaration of 1961 (revised in Edinburgh, 2000) and was
approved by the Research Ethics Committee of the Government of Aragon (CEICA,
Spain).
Anthropometry
w
All participants were measured with a stadiometer without shoes and minimum clothing
On
to the nearest 0.1 cm (SECA 225, SECA, Hamburg, Germany), and weighted to the
nearest 0.1 kg (SECA 861, SECA, Hamburg, Germany). The body mass index (BMI)
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
was calculated as weight (kg) divided by height squared (m2).
Pubertal development was determined by direct observation by a physician according to
the 5 stages proposed by Tanner and Whitehouse 20.
Bone and lean masses
The bone and lean mass of the subjects were measured with dual-energy X-ray
absorptiometry (DXA) using a paediatric version of the software QDR-Explorer
5
Mac Keith Press
-158-
Paper for DMCN
(Hologic Corp. Software version 12.4, Bedford, MA 01730). DXA equipment was
calibrated with a lumbar spine phantom following the Hologic guidelines. Subjects were
scanned in supine position and the scans were performed in high resolution. Three scans
were carried out with each participant: whole body, left hip and lumbar spine. Total lean
mass (TLM; kg) and BMC (g) were obtained from the whole body scan; BMC was
obtained from lumbar spine (L1-L4) and left hip (proximal region of the femur) scans.
Training program
Those participants allocated in the DS-E group exercised twice a week, and each session
w
ie
ev
rR
Fo
was conducted with a maximum of 10 participants. One researcher (experienced
exercise practitioner) and one to three assistants supervised the exercise sessions. Each
session consisted of combined conditioning and plyometric jumps training. The first
week was used as familiarization on how to use the material/equipment and how to
perform the exercises. Each training session consisted of 5 minutes warm-up activities,
10 to 15 minutes for the main part of the session, and 5 minutes cool-down. In the final
stage of training (the last 5 weeks), training was sometimes extended by 5 minutes.
Training consisted of 1 or 2 rotations in a 4-stage circuit.
Training protocol is summarized in Figure 1.
ly
On
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 6 of 20
1. Jumps: standing vertical jump, jump with run-in, drop jump (height jumped
between 40 and 50 centimetres), drop jump+horizontal jump (height jumped
between 40 and 50 centimetres). From the third week onwards, participants
carried adapted-medicine balls while performing the jumps.
2. Press-ups on the wall: participants placed their hands on a wall and performed
press-ups standing but with their feet separate 30 to 50 centimetres from the
wall.
6
Mac Keith Press
-159-
Page 7 of 20
3. Elastic-fitness bands:
a. Lateral rows: step onto the band; grasp ends with a neutral grip. Arms
should hang down to sides with elbows slightly bent. Rise band to side of
body at shoulder height keeping elbows only slightly bent. Return to start
position.
b. Bicep curls: Stand with feet shoulder width apart, knees slightly bent, and
at a staggered stance. Grasp ends with underhand grip with arms hanging
down at sides. Elbows should be close to sides. Flex at the elbows and
Fo
curl band up to approximately shoulder level. Keep elbows close to sides
rR
throughout movement. Return to start position.
c. Frontal rows: Stand upright, keep knees slightly flexed and grasp band
ie
ev
with hands held close in front of chest. Keep arms straight. Row one arm
back until elbow is behind shoulders. Flex shoulders and back. Return,
keep arm slightly flexed. Continue with opposite side.
w
4. Adapted-medicine balls: standing throw and catch, with a distance between
participants of 3 to 4 meters.
On
The DS-E group was divided into four intensity-groups (quartiles) depending on the
body weight of each participant, and they worked out individually within each group.
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
When participants showed excessive facility for performing exercises, they were
transferred to the next intensity-group. There were 4 fitness bands colours (yellow,
green, blue and purple) of increasing resistance and 4 medicine balls (1, 2, 3 and 4 kg),
each one being assigned to a group depending on the strength demanded to perform the
exercises.
Every group followed the same schedule of exercises with a different band colour and
ball (Figure 1).
7
Mac Keith Press
-160-
Paper for DMCN
A minimum attendance of 70% was required in order to be included in the exercise
group. If minimum assistance was not achieved, the participant was excluded from the
statistical analyses.
Statistical methods
All statistical analyses were performed with the Statistical Package for the Social
Sciences (SPSS) version 15.0 for Windows (SPSS Inc., Chicago, IL, USA). Mean and
standard deviations are given as descriptive statistics unless otherwise stated. Normal
distribution of the variables was established using the Kolmogorov-Smirnov test; also
w
ie
ev
rR
Fo
the assumption of homoscedasticity was confirmed. The Chi square test was used to
evaluate the differences in Tanner maturational status. Student’s t tests were used to
evaluate the differences between groups for physical characteristics. Repeated measures
ANOVA were performed to evaluate whether sex by training interactions were present
and to determine the time by exercise interactions for BMC and TLM; including as
covariates the increments in TLM (only for BMC variables), in height, and in Tanner
status. Every adjusted value of pre and post, BMC (total, hip and spine) and TLM were
recorded in the database and the percentage of change (increment of each variable, ∆)
On
calculated; Student’s t test was used to evaluate the differences between groups. To test
the independent relationship among the increments in BMC and the increments of
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 8 of 20
possible confounders, multiple linear regression models were applied including TLM
(Model 1), TLM + height (Model 2), TLM + height + Tanner maturational status
(Model 3) and TLM + height + Tanner + age at baseline (Model 4). Statistical
significance was set at p<0.05.
Results
Adherence to training and possible adverse effects
8
Mac Keith Press
-161-
Page 9 of 20
Adherence to training averaged 81.8 ± 9.2% and ranged from 70 to 97 per cent. Only
one participant (female) did not achieve the minimum 70% attendance at the
intervention program (attended 45% of the trainings) and her data were excluded from
the analyses. At the end of the training programme, 5 participants progressed to a higher
intensity-group. No withdrawals from the DS-E or DS-NE group occurred. Noticeably,
no adverse effects and no health problems were noted in the subjects of both groups
over the 21-week period.
Fo
Age, Tanner status and physical characteristics of the participants are summarized in
rR
Table 1. Participants in the DS-E group showed lower BMI than the DS-NE group at
baseline (p<0.05; Table 1). Participants in both groups showed similar age, height,
ie
ev
weight and Tanner stage distribution at both, baseline and post-intervention points.
Effects of training on body composition
As no sex by training interactions were found (data not shown) analyses were
w
performed including males and females as a whole.
Overall, the DS-E group showed greater increments in total BMC, TLM and in the hip
On
BMC (all p<0.05; Table 2). Repeated measures of ANOVA showed a time by exercise
interaction for TLM (p<0.05; Table 2), but no interactions were found for BMC
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
variables.
Multiple linear regressions revealed that in the DS-NE group, the ∆TLM accounts for
54%, the ∆height accounts for 5% and the ∆Tanner maturational status accounts for
0.6% of the variation in the increment of total BMC (all p<0.05; Table 3). No
associations were found for the total BMC in the DS-E group, nor for the hip or lumbar
spine in any of the two groups.
9
Mac Keith Press
-162-
Paper for DMCN
Discussion
The major finding of this study is that a 21-week training program may help to increase
the BMC of young people with DS. As far as we know, this is the first study reporting
the benefits in bone-related variables of an exercise training program in children and
adolescents with DS. The association between low bone mass with risk of osteoporosis
and related fractures, and the fact that childhood and adolescence are the most important
periods to achieve the peak of bone mass 9, 10 give more relevance to our study
especially in a population characterized by a reduced bone acquisition 7. The increments
w
ie
ev
rR
Fo
in total and hip region BMC in the DS-E group are 2 to 3 times higher than in the DSNE after the training period after adjustments by important confounders. The fact that
we did not find any significant time by exercise interaction in bone-related variables
could be due to the reduced number of subjects in the study. The present study is in line
with previous studies that obtained benefits from using plyometric training with
children and adolescents without disabilities 16, 21. However, the rate of improvement in
total and hip BMC was higher in the present study (6.7% vs. 3.7% and 1.6% in total,
and 14.6% vs. 4.5% in hip) and similar improvement was obtained in lumbar spine
On
region (6.4% vs. 6.6% and 3.1%).
Lean mass is highly correlated with bone mass 12 and, as found in the present study, a
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 10 of 20
time by exercise interaction was found for TLM in the DS-E group compared with the
DS-NE. The previous point could suggest that the higher increments observed in BMC
may be due more to the indirect effect of muscle hypertrophy on bone than to the direct
effect of exercise on bone. However, the fact that neither the increment in TLM, in
height or in Tanner, nor the age of the subjects in the DS-E group significantly accounts
for the increments in BMC, permits us to suppose that the training could have had an
effect on the bone mass of the participants. Due to the osteogenic effect of exercise or to
10
Mac Keith Press
-163-
Page 11 of 20
the higher increment in TLM, the results of the intervention were fairly satisfactory in
terms of bone mass acquisition with an intervention that was quite modest in terms of
time employed. In the future, the effect of longer and/or more intense trainings may
show whether the tendency of young people with DS to have reduced bone mass could
be compensated.
Another important issue is the feasibility of the program. As there were no withdrawals,
it seems that the training program was attractive and easily adhered to, and this is a
matter of great importance in this specific population.
Fo
There were some limitations to this study that should be recognized: we did not perform
rR
a traditional strength training based on percentages of 1-maximum repetition; however,
the protocol of our training program was well established and defined. Unfortunately,
ie
ev
exposure to sunlight and diet were not controlled in this study. The strengths of this
study were the inclusion of both genders in the design, the use of a control group of
young people with DS, and the sample size, which although not a very large one, is
w
larger than that of any other intervention study including training with children and
On
To conclude, our findings suggest that physical conditioning including plyometric
jumps may be a good strategy to increase BMC of young people with DS.
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
11
Mac Keith Press
-164-
Paper for DMCN
Acknowledgments
The authors want to thank all the children and their parents that participated in the study
for their understanding and dedication to the project. Special thanks are given to
Fundación Down Zaragoza, Special Olympics Aragon and Colegio Jesús-María El
Salvador, for their support. We also thank Paula Velasco Martínez from the University
of Zaragoza for her great technical assistance. This work was supported by Gobierno de
Aragón (Proyecto PM 17/2007) and Ministerio de Ciencia e Innovación de España (Red
de investigación en ejercicio físico y salud para poblaciones especiales-EXERNET-
w
ie
ev
rR
Fo
DEP2005-00046/ACTI). There are no potential conflicts of interest that may affect the
contents of this work.
ly
On
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 12 of 20
12
Mac Keith Press
-165-
Page 13 of 20
References
1.
Pueschel SM. Clinical aspects of Down syndrome from infancy to adulthood.
Am J Med Genet Suppl. 1990;(7)52-6.
2.
Baptista F, Varela A, Sardinha LB. Bone mineral mass in males and females
with and without Down syndrome. Osteoporos Int. 2005 Apr;(16)380-8.
3.
Sakadamis A, Angelopoulou N, Matziari C, Papameletiou V, Souftas V. Bone
mass, gonadal function and biochemical assessment in young men with trisomy 21. Eur
J Obstet Gynecol Reprod Biol. 2002 Jan 10;(100)208-12.
4.
Fo
Sepulveda D, Allison DB, Gomez JE, Kreibich K, Brown RA, Pierson RN, Jr.,
rR
et al. Low spinal and pelvic bone mineral density among individuals with Down
syndrome. Am J Ment Retard. 1995 Sep;(100)109-14.
5.
ie
ev
Angelopoulou N, Souftas V, Sakadamis A, Mandroukas K. Bone mineral
density in adults with Down's syndrome. Eur Radiol. 1999;(9)648-51.
6.
Guijarro M, Valero C, Paule B, Gonzalez-Macias J, Riancho JA. Bone mass in
w
young adults with Down syndrome. J Intellect Disabil Res. 2008 Mar;(52)182-9.
7.
González-Agüero A, Vicente-Rodriguez G, Moreno LA, Casajus JA. Bone mass
On
in male and female children and adolescents with Down syndrome. Osteoporos Int.
2011 Jul;(22)2151-7.
8.
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
Halaba Z, Pyrkosz A, Adamczyk P, Drozdzowska B, Pluskiewicz W.
Longitudinal changes in ultrasound measurements: a parallel study in subjects with
genetic disorders and healthy controls. Ultrasound Med Biol. 2006 Mar;(32)409-13.
9.
Rizzoli R, Bianchi ML, Garabedian M, McKay HA, Moreno LA. Maximizing
bone mineral mass gain during growth for the prevention of fractures in the adolescents
and the elderly. Bone. 2010 Feb;(46)294-305.
13
Mac Keith Press
-166-
Paper for DMCN
10.
Rizzoli R, Bonjour JP. Determinants of peak bone mass and mechanisms of
bone loss. Osteoporos Int. 1999;(9 Suppl 2)S17-23.
11.
Glasson EJ, Sullivan SG, Hussain R, Petterson BA, Montgomery PD, Bittles
AH. The changing survival profile of people with Down's syndrome: implications for
genetic counselling. Clin Genet. 2002 Nov;(62)390-3.
12.
Vicente-Rodriguez G. How does exercise affect bone development during
growth? Sports Med. 2006;(36)561-9.
13.
Gutin B, Kasper MJ. Can vigorous exercise play a role in osteoporosis
w
ie
ev
rR
Fo
prevention? A review. Osteoporos Int. 1992 Mar;(2)55-69.
14.
Nordstrom A, Karlsson C, Nyquist F, Olsson T, Nordstrom P, Karlsson M. Bone
loss and fracture risk after reduced physical activity. J Bone Miner Res. 2005
Feb;(20)202-7.
15.
González-Agüero A, Vicente-Rodriguez G, Moreno LA, Guerra-Balic M, Ara I,
Casajus JA. Health-related physical fitness in children and adolescents with Down
syndrome and response to training. Scand J Med Sci Sports. 2010 Oct;(20)716-24.
16.
Witzke KA, Snow CM. Effects of plyometric jump training on bone mass in
On
adolescent girls. Med Sci Sports Exerc. 2000 Jun;(32)1051-7.
17.
González-Agüero A, Vicente-Rodriguez G, Gómez-Cabello A, Ara I, Moreno
ly
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 14 of 20
LA, Casajús JA. A combined training intervention programme increases lean mass in
youths with Down syndrome. Res Dev Disabil. 2011;(In press).
18.
Lin CF, Huang TH, Tu KC, Lin LL, Tu YH, Yang RS. Acute effects of
plyometric jumping and intermittent running on serum bone markers in young males.
Eur J Appl Physiol. Aug 12.
19.
Lehtonen-Veromaa M, Mottonen T, Irjala K, Nuotio I, Leino A, Viikari J. A 1-
year prospective study on the relationship between physical activity, markers of bone
14
Mac Keith Press
-167-
Page 15 of 20
metabolism, and bone acquisition in peripubertal girls. J Clin Endocrinol Metab. 2000
Oct;(85)3726-32.
20.
Tanner JM, Whitehouse RH. Clinical longitudinal standards for height, weight,
height velocity, weight velocity, and stages of puberty. Arch Dis Child. 1976
Mar;(51)170-9.
21.
Fuchs RK, Bauer JJ, Snow CM. Jumping improves hip and lumbar spine bone
mass in prepubescent children: a randomized controlled trial. J Bone Miner Res. 2001
Jan;(16)148-56.
rR
Fo
w
ie
ev
ly
On
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
15
Mac Keith Press
-168-
Paper for DMCN
Tables
Table 1. Descriptive characteristics of the participants.
Age (years)
Down syndrome Non-Exercise
(n=14)
Pre-training
Post-training
p
p
mean (SD)
mean (SD)
16.0 (2.5)
0.067
15.4 (2.5) 0.067
Down syndrome Exercise
(n=13)
Pre-training
Post-training
mean (SD)
mean (SD)
13.7 (2.6)
14.3 (2.6)
Weight (kg)
48.7 (10.7) 0.057
49.5 (10.6)
40.1 (9.6)
Height (cm)
146.8 (10.7) 0.299
Tanner (I,II,III,IV,V)
2
BMI (kg/m )
0.095
41.8 (9.8)
148.3 (10.2)
0.243
1/1/1/5/6
0.361
0/2/1/3/8
0.407
141.9 (12.5) 142.8 (12.4)
3/0/3/2/5
3/1/1/3/5
22.4 (3.4)
0.028
22.3 (3.2)
0.136
19.6* (2.7)
20.2 (2.6)
w
ie
ev
rR
Fo
BMI: Body mass index. * p<0.05 between DS-E and DS-NE.
ly
On
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 16 of 20
16
Mac Keith Press
-169-
Page 17 of 20
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
Table 2. Bone mass adjusted by increments in total lean mass, height and Tanner, and
lean mass adjusted by increments in height and Tanner before and after the training, and
adjusted percentage of change.
DXA
Measurement
Total
Down syndrome Non-Exercise (n=14)
Adjusted %
Pre-training
Post-training
of Change
Down syndrome Exercise (n=13)
PostAdjusted %
Pre-training
training
of Change
Interaction
Group x Time
BMC, g
1110.3 (76.3)
1139.2 (77.3)
2.4*
803.3 (79.9)
852.3 (81.0)
6.7
p = 0.197
TLM, kg
32.4 (1.9)
32.7 (2.1)
1.9*
26.4 (2.0)
27.9 (2.2)
5.8
p = 0.008
22.7 (1.7)
24.4 (1.9)
6.2*
16.9 (1.9)
19.3 (2.2)
14.6
p = 0.587
44.1 (3.4)
47.6 (3.5)
6.4
28.6 (3.5)
30.1 (3.7)
6.4
p = 0.107
Hip
Lumbar spine
BMC, g
Fo
BMC, g
mass.
rR
Values are mean ± standard deviation. BMC, bone mineral content; TLM, total lean
w
ie
ev
*p<0.05 between percentage of change; in bold significant group by time interaction.
ly
On
17
Mac Keith Press
-170-
Paper for DMCN
Table 3. Relationships between the increments in bone-related variables and the
increments in total lean mass, height and Tanner maturational status, and age at
baseline.
∆Total BMC
∆Hip BMC
∆Lumbar spine BMC
Change R2
P
Change R2
P
Change R2
p
DS-E
Model 1
0.309
0.061
0.076
0.440
0.003
0.879
Model 2
0.000
0.189
0.006
0.740
0.024
0.909
0.004
0.901
Model 3
0.009
0.357
0.406
0.410
0.045
0.923
Model 4
0.056
0.449
0.112
0.264
0.013
0.741
DS-NE Model 1
0.540
0.004
0.014
0.509
0.319
0.200
Model 2
0.046
0.012
0.001
0.732
0.100
0.241
Model 3
0.006
0.037
0.051
0.780
0.014
0.399
Model 4
0.000
0.093
BMC, bone mineral content; DS-E, Down syndrome exercise; DS-NE, Down syndrome
non-exercise
w
ie
ev
rR
Fo
Model 1: ∆TLM
Model 2: Model 1+∆Height
Model 3: Model 2+∆Tanner
Model 4: Model 3+age at baseline
ly
On
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 18 of 20
18
Mac Keith Press
-171-
Page 19 of 20
Figure 1. Schedule of training protocol.
rR
Fo
w
ie
ev
ly
On
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Paper for DMCN
19
Mac Keith Press
-172-
Paper for DMCN
w
ie
ev
rR
Fo
307x122mm (150 x 150 DPI)
ly
On
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Page 20 of 20
Mac Keith Press
-173-
-174-
7.AportacionesprincipalesdelaTesisDoctoral
Artículo I. La condición física y composición corporal de jóvenes con síndrome de Down
es menos saludable que la de sus homólogos con o sin discapacidad. El entrenamiento
físico parece ser beneficioso para esta población. A pesar de que existen algunos datos al
respecto, el conocimiento actual en esta materia es escaso y se necesitan nuevos estudios
que clarifiquen algunos temas.
Artículo II. Los bajos valores de masa ósea presentes en adultos con síndrome de Down,
pueden ser detectados desde la niñez y adolescencia. El dimorfismo sexual en masa ósea
en jóvenes con síndrome de Down es atípico.
Artículo III. Los jóvenes con síndrome de Down tienen una distribución de tejidos
blandos diferente a sus homólogos sin discapacidad, sin embargo su dimorfismo sexual es
similar.
Artículo IV. El dimorfismo sexual de niños y niñas con síndrome de Down medido con
antropometría es muy parecido al de sus homólogos sin discapacidad, sin embargo los
valores de IMC y porcentaje de grasa de las niñas son muy superiores.
Artículo V. Los jóvenes con síndrome de Down tienen músculos menos eficaces que sus
homólogos sin discapacidad, ejercen menos fuerza por cada kilogramo de masa muscular.
Artículo VI. La fórmula de predicción de Slaughter y col. es la más correcta para evaluar
porcentaje de grasa corporal mediante antropometría en niños y adolescentes con SD.
Artículo VII. 21 semanas de entrenamiento de acondicionamiento físico combinado con
saltos pliométricos, son suficientes para incrementar la masa muscular de jóvenes con
síndrome de Down.
-175-
Artículo VIII. 21 semanas de entrenamiento de acondicionamiento físico combinado con
saltos pliométricos mejoran la condición aeróbica de jóvenes con síndrome de Down.
Artículo IX. La masa ósea de jóvenes con síndrome de Down se incrementa después de
21 semanas de entrenamiento de acondicionamiento físico combinado con saltos
pliométricos.
-176-
7.MaincontributionsoftheDoctoralThesis
Manuscript I. Physical fitness and body composition of youths with Down syndrome are
less healthy than in their control counterparts. Physical training seems to be beneficial for
this population. Some research has been done in this subject, however, the current
knowledge is yet scarce and new studies are needed in order to clarify some pending
issues on this topic.
Manuscript II. The low levels of bone mass present in adults with Down syndrome are
already detectable during the childhood and adolescence. The sexual dimorphism in
youths with Down syndrome is atypical.
Manuscript III. Children and adolescents with Down syndrome have a different soft
tissue distribution than their counterparts without Down syndrome; however, their sexual
dimorphism is quite similar.
Manuscript IV. The sexual dimorphism measured with anthropometry of male and
female children and adolescents with Down syndrome is quite similar than the observed
in others without Down syndrome, however, the values of BMI and body fat percentage
of girls are much higher.
Manuscript V. Youths with Down syndrome have less efficient muscles than their
counterparts without Down syndrome; they cannot achieve as much strength by kilogram
of muscle mass.
Manuscript VI. The prediction equation of Slaughter et al. is the most accurate to
evaluate body fat percentage with anthropometry in children and adolescents with Down
syndrome.
-177-
Manuscript VII. A 21-week conditioning combined with plyometric jumps training is
enough to increase lean mass of youths with Down syndrome.
Manuscript VIII. Twenty-one weeks of conditioning combined with plyometric jumps
training increase cardiovascular fitness levels of youths with Down syndrome.
Manuscript IX. The bone mass of youths with Down syndrome is increased towards 21
weeks of conditioning combined with plyometric jumps training.
-178-
8.Conclusiones
 Los niños y adolescentes con síndrome de Down tienen una condición física peor,
y una composición corporal menos saludable que sus homólogos sin síndrome de
Down; sin embargo, la literatura científica disponible al respecto es, cuando
menos, escasa.
 La composición corporal de jóvenes con síndrome de Down no parece adecuada,
dado que sus niveles de masa ósea y masa muscular son bajos, y su distribución
de grasa puede ser la causa de problemas cardiovasculares futuros.
 No solo preocupa el bajo nivel de contenido mineral óseo de estos jóvenes, sino
también el atípico dimorfismo sexual en relación a masa ósea que presentan.
 La poca eficiencia muscular de este grupo de jóvenes, agrava la presencia de
niveles bajos de masa muscular.
 Para evaluar la grasa corporal en niños y adolescentes con síndrome de Down
mediante antropometría, la ecuación de predicción que mejor se adapta a sus
característica morfológicas y a sus proporciones corporal es la de Slaughter y col.
 Cinco meses de entrenamiento de acondicionamiento físico combinado con
saltos pliométricos, pueden ayudar a niños y adolescentes con síndrome de Down
a incrementar su condición aeróbica, y a desarrollar su masa muscular y masa
ósea.
-179-
-180-
8.Conclusions
 Children and adolescents with Down syndrome have a worst physical fitness and
a less healthy body composition than their counterparts without Down syndrome;
however, the scientific literature available on the topic is, at least, sparse.
 Body composition of youths with Down syndrome seems not very adequate, since
their levels of bone and lean masses are low, and their fat distribution could be
the cause of future cardiovascular diseases.
 It is not only concerning the low level of bone mineral content, but the atypical
sexual dimorphism in terms of bone mass that these youths present.
 The low muscular efficiency of this group of youths, is concerning together with
the low levels of lean mass.
 To evaluate body fat in children and adolescents with Down syndrome with
anthropometry, the prediction equation that better adapts to their morphology and
bodily proportions is the one of Slaughter et al.
 Five months of conditioning combined with plyometric jumps training, may help
children and adolescents with Down syndrome to increase their aerobic capacity,
and to develop their bone and lean masses.
-181-
-182-
Apéndice[Appendix]
Factor de impacto y ranking de cada revista en 2010 en “ISI Web of Knowledge – Journal
Citation Reports” dentro de sus áreas correspondientes.
[Impact factor and ranking of each journal in 2010 in “ISI Web of Knowledge – Journal
Citation Reports” within their subject categories.]
Artículos aceptados [Accepted manuscripts]:
Artículo
[Manuscript]
Revista
[Journal]
I. Scandinavian Journal of Medicine and Science in Sports
Factor de impacto
[Impact factor]
2.779
Ranking in 2010 ISI – JCR: 8/79 (Sport Sciences)
II. Osteoporosis International
4.859
Ranking in 2010 ISI – JCR: 23/116 (Endocrinology and Metabolism)
III, VI y VII. Research in Developmental Disabilities
3.201
Ranking in 2010 ISI – JCR: 1/62 (Rehabilitation)
IV. Revista Española de Obesidad
No aplicable
Indexada en EMBASE
V. Biomecánica
No aplicable
Indexada en Latindex
Artículos sometidos [Submitted manuscripts]:
Artículo
[Manuscript]
Revista
[Journal]
VIII. Adapted Physical Activity Quarterly
Factor de
impacto
[Impact factor]
1.189
Ranking in 2010 ISI – JCR: 42/79 (Sport Sciences)
IX. Developmental Medicine and Child Neurology
3.264
Ranking in 2010 ISI – JCR: 6/107 (Pediatrics)
-183-
-184-
Agradecimientos[Acknowledgement]
Cuando hace tiempo oía hablar de directores de tesis siempre pensaba en gente
seria, con un trato impersonal hacia sus doctorandos, gente al fin y al cabo, a otro nivel.
Pues bien, no estaba del todo equivocado, mis tres directores están totalmente a otro
nivel, el nivel más alto y espectacular que he visto. Nunca llegaré a poder agradeceros
todo lo que habéis hecho/hacéis por mi durante todo este tiempo, creo sinceramente que
he recibido la mejor formación (en todos los sentidos) que un doctorando puede recibir.
Por eso, sirvan estas líneas como gesto público de AGRADECIMIENTO y
ADMIRACIÓN hacia vosotros tres. JAC, o mejor dicho (que esto es serio, que es una
Tesis), Dr. José Antonio Casajús, he tenido la inmensa suerte de sufrir a tu lado
kilómetros y kilómetros de carretera, y también muchas horas en Zaragoza y en el país del
whisky. Aprendiendo en esos viajes (y bares) lo indecible, intentando arreglar el mundo a
ratos, y sobre todo dándome cuenta, como tú dices, que “En este mundillo hay que tener
paciencia, hijo, que al final, si las cosas se hacen bien, salen bien…”. Parece que al final
tenías razón… Ger, no cabe aquí todo el reconocimiento que pueda deberte; espero, al
menos en parte, poder devolverte todo el tiempo que has invertido conmigo estos últimos
4 años. Desde que llegué al Cervantes, cito literal, ‘hecho un pipiolo’ hasta el día de hoy,
que finalmente leo mi Tesis, siempre has estado ahí para ayudarme con todo lo que se
ponía por delante y dándome ánimos en cada ‘rejection’… muchas gracias. Y como no
hay dos sin tres, el Dr. Ara merece también un reconocimiento; contigo Nacho, he
aprendido (al mismo tiempo que todo lo científico) esa parte de la investigación que no
aparece en los ‘papers’, eso que se nace y no se hace, ese saber hacer tan tuyo y que tan
buenos ratos nos ha hecho pasar. “No hay que dar puntada sin hilo” me decías, y cuánta
razón tenías Nacho… mil gracias a ti también.
-185-
Como principal responsable del grupo GENUD, muchas gracias Luis Moreno por tu
acogida, y por como consigues, incluso en este tiempo de crisis, que este barco siga a
flote. Muchas gracias a todos los compañeros que estáis o habéis formado parte del
grupo: Juan, Iris, Pilar M, Paula, Maribel, Theodora, Pablo, David, Esther, Maria
Luisa, Pilar de M, Alba S, Silvia, Diego, Fernanda, Alex León, Gerardo, Dorita,
Teresa, Jesús… Gracias y, sobre todo muchos ánimos a los nuevos doctorandos de
Ciencias del Deporte que estáis empezando, Alex Guillén, Alex Gómez, Silva y Ángel,
que sois los tenéis que tirar del carro ahora, se espera mucho de vosotros! Un
agradecimiento especial merecen mis compañeros de trabajo mas cercanos y compañeros
de congresos; Luis, que al final parece que lo conseguimos… y mira que estaba difícil!,
Hugo, gracias por todo en general, siempre es bueno tener un post-doc entre nosotros,
aunque fuera por poco tiempo! Y muchas gracias Alba, mi compi más “veterana”,
porque después de unos cuantos años, parece que el trabajo juntos, es trabajo, pero no
cansa tanto, verdad?
There is also a person that I would like to thank his help and support during my stay in
the University of Glasgow, Yannis Pitsiladis. Thank you very much for your kind
reception and supportive advice, I really enjoyed working with you and hope we’ll work
together again in a close future. Many thanks also to the Glasgow team, which made my
stay much more comfortable; Chris, Robert, John, Lukas, Cristina, Maria, Ramzy,
Ruth, Hannah, Lena, Robert, Carlos, Michael, Thelma, Farah…
Nada de esto hubiera sido posible, si los niños con y sin síndrome de Down, y
principalmente sus familias no se hubieran prestado a realizar todas las pruebas, ir a
entrenar todos los días, llamadas y más llamadas… Así que debo que agradecer,
inmensamente, la colaboración de todos ellos. En este mismo sentido, agradezco también
-186-
la inestimable colaboración de las instituciones (y sus trabajadores) con las que
trabajamos: Fundación Down, mil gracias Ruth por tu predisposición y eficacia, y
también muchas gracias a Marta, Carlos e Iván por esas “manillas” que me echasteis
con los entrenamientos. Special Olympics, gracias Asun por facilitarme los contactos. Y
gracias también al colegio Jesús María - El Salvador, especialmente a Manolo
Magdaleno por dejarnos interferir ahí y conseguir todos los niños control, por los
espacios cedidos para reuniones…
En el terreno más personal, me gustaría agradecer también, a mis padres principalmente
aguantarme todos estos años desde Alcalá de Henares hasta mi vuelta a Zaragoza, pero
también el haberme hecho tan fácil poder dedicarme a esto sin excesiva preocupación
externa.
También gracias a Lore y Scott (y a la pequeña Lucía); por el tiempo que estuve en
Glasgow como si estuviera en casa y, por supuesto, “thanks for reviewing the English
style and grammar…”
Muchas gracias también al resto de mi familia González de Agüero – Lafuente, y a mi
familia política Bueno – Fenero por vuestro apoyo todo este tiempo.
A mis amigos más cercanos, Carlos, Enrique, Héctor, Jaime y Javi, gracias por
entender, aunque fuera difícil, lo que suponía para mi esta Tesis y todo el tiempo que he
tenido que dedicarle.
Y cómo no agradecer, a la persona que sin duda más me sufre y me aporta, desde antes
incluso de comenzar ésta andadura, mi queridísima Sara; muchísimas gracias, contigo
TODO es mucho más sencillo…
-187-
-188-
-189-

Composición corporal y condición física en niños

Transcription

Similar documents

Supervisión de la salud de niños con síndrome de Down abstract

He is Risen…... - Catholic Charismatic Center

presentación

Mecanismo de transporte tubular

anuncios - Christian Community Church

Un Futuro Prometedor Juntos - National Down Syndrome Society

Neurodegeneración y neuroprotección en el sistema nervioso adulto

July 17, 2016

Obstrucción nasal unilateral en niños. Síndrome de Pai

MS MS/MS - Agilent Technologies

Lee la Revista Gráfica de Diciembre desde aquí

Fractura de acetábulo en ancianos: Artroplastia total de cadera en

Abrir - ACOG

Abordaje Lateral Indirecto Modificado (ALIM) Nueva

Descarga - Material Curricular Libre

Colombia en deuda con su infancia - Save the Children`s Resource

Ejemplar temático anual: Individualización

PDF TESIS DOCTORAL - Universidad de Alcalá

Catálogo Novogres cerámicas, azulejos, gres, porcelanicos. Wall

Educación especial y mundo digital

SERVICIOS DE CAPACITACIÓN DE IBM