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
b
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

A R T I C L E I N F O A B S T R A C T

Article history: The present study aimed at comparing fat and lean masses between children and
Received 18 February 2011 adolescents with and without Down syndrome (DS) and evaluating the presence of sexual
Received in revised form 22 February 2011 dimorphism. Total and regional fat and lean masses were assessed by dual energy X-ray
Accepted 22 February 2011 absorptiometry (DXA) and the percentage of body fat (%BF) by air-displacement
Available online 24 March 2011 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
Keywords: compare variables between groups and between sexes within the same group. There were
Trisomy 21
no significant differences in %BF, WC or body mass index (BMI) between groups. Females
DXA
with DS showed higher fat and lean masses in the trunk, and lower fat and lean masses in
Obesity
Body composition
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.

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: alexgonz@unizar.es (A. González-Agüero).

0891-4222/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ridd.2011.02.023
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 (González-
Agüero 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
adolescents with DS.

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).
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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 QDR-
Explorer 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 intra-
class 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. Effect-
size 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 Non-Down syndrome

All (n = 31) Female (n = 14) Male (n = 17) All (n = 32) Female (n = 13) Male (n = 19)

Age (year) 15.2  2.9 14.8  3.2 15.5  2.7 14.7  2.3 14.6  2.4 14.8  2.2
Weight (kg) 46.7*  12.2 42.9  13.5 48.7*  10.9 55.6  13.1 53.2  13.8 57.3  12.7
Height (cm) 145.2*  11.6 138.9*,#  9.9 150.8*  10.3 163.2  12.4 156.3#  9.6 167.8  12.1
Waist circumference (cm) 75.4  11.1 78.1  14.1 72.9  7.1 74.6  8.3 75.1  10.1 74.2  7.1
Body mass index (kg/m2) 21.7  3.9 22.4  4.8 21.0  2.9 20.7  3.5 21.5  4.4 20.1  2.7
*
p  0.05 between groups.
#
p  0.05 between sexes within the same group.
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Table 2
Percentage of body fat assessed by ADP and DXA (mean  standard deviation).

Down syndrome Non-Down syndrome

All (n = 31) Female (n = 14) Male (n = 17) All (n = 32) Female (n = 13) Male (n = 19)

Body fat by DXA (%) 24.7  7.8 30.4#  5.2 19.9  6.3 24.4 7.4 30.2#  6.1 20.4  5.4
Body fat by BODPOD (%) 25.8  10.1 29.9#  11.5 22.1  7.0 24.3  9.8 31.1#  8.3 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.
 A. González-Agüero et al. / Research in Developmental Disabilities 32 (2011) 1685–1693 1689

3.3. Fat and lean masses

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.
[()TD$FIG]
1690 A. González-Agüero et al. / Research in Developmental Disabilities 32 (2011) 1685–1693

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
[()TD$FIG] A. González-Agüero et al. / Research in Developmental Disabilities 32 (2011) 1685–1693 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
1692 A. González-Agüero et al. / Research in Developmental Disabilities 32 (2011) 1685–1693

(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, Vicente-
Rodriguez, 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.

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