European Journal of Clinical Nutrition (2000) 54, 203±208
ß 2000 Macmillan Publishers Ltd All rights reserved 0954±3007/00 $15.00
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Puberty begins with a characteristic subcutaneous body fat mass
in each sex
B Vizmanos* and C MartõÂ-Henneberg
Pediatrics Unit, Faculty of Medicine, University Rovira i Virgili, Reus, Spain
Objective: To observe whether there exists a characteristic body fat mass at pubertal onset.
Design: Longitudinal clinical follow-up (between ages of 10 and 15 y) with an annual visit in a sample of 469
children. They were grouped according to age of purbertal onset: boys with pubertal onset at the ages of 11
(n ˆ 59), 12 (n ˆ 88), 13 n ˆ 89) and 14 y (n ˆ 46), and girls with pubertal onset at the age of 10 (n ˆ 68), 11
(n ˆ 66), 12 (n ˆ 37) and 13 (n ˆ 16).
Methods: Height, weight, upper arm circumference and four skinfold thicknesses were recorded annually. In
boys testicular volume index was measured, and genital development was assessed on the Tanner scale; in girls
mammary development was measured also using the Tanner scale. The sum of four skinfolds, body mass index,
upper arm fat estimate and percentage body fat were calculated.
Results: Boys presented a positive relation between the age of pubertal onset and body mass index (P < 0.001),
which was not observed in girls. Body mass index thus varied according to the onset of puberty in boys
(P < 0.001), but not in girls. The sum of four skinfolds, the upper arm fat estimate index and the percentage of
body fat mass did not differ according to age of pubertal onset either in girls (P ˆ NS) or in boys (P ˆ NS). The
characteristic adiposity of the puberty onset is progressively acquired during the previous years in all the groups.
Conclusions: Puberty seems to begin with a characteristic subcutaneous body fat mass that is independent of the
age of onset. This study supports the hypothesis of a close link between maturation and the development of an
energy store in the form of adipose tissue in both sexes.
Descriptors: body fat mass; onset of puberty; skinfolds
European Journal of Clinical Nutrition (2000) 54, 203±208
Introduction
Traditional longitudinal studies on body fat mass during
child development have shown similarities in the growth
kinetics of the fat tissue in both sexes until the beginning of
puberty. From this moment onwards the kinetics varies:
there tends to be a decrease in boys, but an increase in girls,
although the amount of fat mass in girls is always higher
(Noran, 1998). Recent studies on the factors which regulate
this phenomenon, e.g. factors associated with leptin production (GarcõÂa Mayor et al, 1997), support this view.
Recent reports have suggested an association between
body fat mass and the onset of puberty: the leptin synthesized by the adipocytes accelerates the maturation of the
tissue (Ahima et al, 1997) and of the reproductive function
(Chehab et al, 1997). These reports rekindle the debate
initiated by Frisch and McArthur (1974) on the possibility
of a link between maturation and a speci®c accumulation of
energy for the organism, in the form of body fat mass,
although to date this link has not been completely demonstrated (de Ridder et al, 1992; GarcõÂa-Mayor et al, 1997;
Mantzoros et al, 1997; Blum et al, 1997).
*Correspondence: C MartõÂ-Henneberg, Pediatrics, Faculty of Medicine,
San Lorenzo 21, 43201 Reus, Spain. E-mail: [email protected]
Guarantor: C MartõÂ-Henneberg.
Contributors: BV did the ®eld work, analysis, writing and discussion. CMH did the study design, discussion and conclusions.
* This study was supported by a grant from Rovira i Virgili University and
Dr Vizmanos was in receipt of a fellowship from INSTITUTO DANONE
(Spain).
Received 26 April 1999; revised 16 September 1999; accepted
25 September 1999.
If leptin is the signal that connects energy stores in the
adipose tissue with the central nervous system (Camp®eld
et al, 1995), it seems plausible that attaining a characteristic
store of body fat mass may contribute to triggering puberty,
although the mechanisms related to the adipose tissue and
involved in the outbreak of puberty are still a matter of
discussion (Kelch & Beitins, 1994).
In this longitudinal study we observed pubertal onset at
very different ages both in boys and girls, grouping them
according to their age when puberty began. We analyzed
body fat mass in each of the groups at the moment of
pubertal onset, in order to assess the relationship between
the pubertal maturation changes and the development of fat
mass. We also studied the fat mass evolution along the
prepubertal period.
Structure of the Study.
The study began in 1987, and this report is part of a larger
program investigating growth and development during
puberty, completed in 1997. All boys (n ˆ 323) and girls
(n ˆ 244) identi®ed from the population census as being
born in Reus (an industrial town in N. E. Spain, with a
population of around 100,000) in the ®rst six months of
1976 (in the case of boys) and in the ®rst six months of
1977 (in the case of girls) were contacted. When consent
was obtained from both the subjects and their parents or
guardians, the children were enroled in the study (boys
n ˆ 299 and girls n ˆ 223). Subjects who developed speci®c
pathologies were excluded. An annual clinical visit was
scheduled for each child during the month of their birthday.
Puberty begins with a characteristic subcutaneous body fat mass in each sex
B Vizmanos and C MartõÂ-Henneberg
204
A total of 282 boys and 187 girls remained in the study
until pubertal onset, and were classi®ed as described in the
section `study subjects'
Variables studied
All measurements were conducted annually. At the clinical
visit, boys' genital development stage on the Tanner scale
(Tanner, 1962) and testicular volume index (TVI)
( 01ml) (Burr et al. 1970) were evaluated. In girls,
mammary development stage on the Tanner scale
(Tanner, 1962) was recorded. Height (0.1 cm) and weight
(0.1kg) were recorded for both sexes (Lohman et al, 1988).
At the conclusion of the study, the growth curve was
plotted for each individual subject and annual height
velocity was entered. Three measurements of the same
skinfold (0.1mm) were also conducted carefully in each
child, at the tricipital, bicipital, subscapular and suprailiac
sites, after standardization of the technique (Lohman et al,
1988), and the mean for each skinfold value (TRI, BIC,
SUB, SUP, respectively) was recorded. Upper arm circumference (UAC) (0.1 cm) was measured at the same level as
the tricipital skinfold (Lohman et al, 1988). A range of
indices were calculated: body mass index (BMI, weight
(kg)=height (m)2), the sum of four skinfolds (SUM
TRI ‡ BIC ‡ SUB ‡ SUP), upper arm fat estimate (UFE,
UAC6TRI=2) (Rolland-Cachera et al, 1997), and percentage of body fat (%BF), eqn (1); (Siri, 1956), with values of
body density (BD) obtained by Durnin's formula eqn (2);
(Durnin & Rahaman, 1967).
%BF ˆ
Statistical analysis
After verifying the normality of the distribution of the age
of pubertal onset in both samples (boys and girls) using the
Kolmogorov ± Smirnof test, and after checking the homogeneity of the variances, we compared the means of
different variables or indices between the subgroups of
the same sex, using analysis of variance (ANOVA). When
there were differences between the groups with different
ages of pubertal onset, we performed Pearson's simple
correlations. To analyze the signi®cance of the annual
changes that take place during prepubertal period in each
group, we used the paired t-test.
Unless otherwise stated, all values are presented as
mean s.e.m. All statistical analyses were conducted
using the Statistical Package for the Social Sciences
(SPSS=PC) and signi®cance was set at P < 0.05.
Results
Distribution of age of onset of puberty
The distribution of ages at pubertal onset is shown in Figure
1 (girls in the upper panel and boys in the lower one).
Weight and height at onset of puberty
Mean weights of subjects at pubertal onset in the different
age-of-onset groups are shown in Table 1. The later the
age of onset, the higher the mean weight, in both boys
(P < 0.001) and girls (P ˆ 0.003). There are signi®cant
100 …4:95=BD ÿ 4:5†
Boys :
BD ˆ 1:1533 ÿ 0:0643 log10 SUM
Girls :
BD ˆ 1:1369 ÿ 0:0598 log10 SUM
Study subjects
Criteria for subgrouping girls with different ages of pubertal onset were explained elsewhere (MartõÂ-Henneberg &
Vizmanos, 1997). Only girls that started puberty from 10 y
on (onset at 10 (n ˆ 68), at 11 (n ˆ 66), at 12 (n ˆ 37) and at
13 y of age (n ˆ 16)) were included in the analysis of body
composition at pubertal onset.
The retrospective age-group assignment of boys, based
on the annual follow-ups, was calculated so that in each
group there would be boys who had started puberty at the
time of the clinical visit (Stage G2 and testicular volume
index TVI  4 ml) together with boys who would be starting puberty immediately afterwards (Stage G1 with
TVI < 4 ml at the time of observation but who were at
Stage G3 and TVI > 4 ml at the subsequent clinical visit
one year later). An increase in the annual rate of height
velocity (i.e. faster height velocity than the previous year)
was needed to con®rm the correct age-at-onset assignment.
This is particularly true for the groups with onset at 12
(n ˆ 88), at 13 (n ˆ 89) and at 14 y of age (n ˆ 46).
Boys who presented genital Stage G2 at 11 y
(TVI  4 ml), or Stage G1 at 11 (TVI < 4 ml) and a G3
Stage at 12 y of age (TVI > 4 ml), were recorded as having
started puberty at 11 y of age (n ˆ 59). In these boys the
height increase between 11 and 12 y of age was con®rmed
as being greater than 5 cm=y.
*TRI ˆ tricipital skinfold; BIC ˆ bicipital skinfold; SUB ˆ subscapular
skinfold; SUP ˆ suprailiac skinfold; UAC ˆ upper arm circumference.
European Journal of Clinical Nutrition
Figure 1 Distribution of age of pubertal onset in girls (upper panel) and
boys (lower panel).
Puberty begins with a characteristic subcutaneous body fat mass in each sex
B Vizmanos and C MartõÂ-Henneberg
205
Table 1 Height, weight and BMI at pubertal onset in subgroups of boys and girls starting puberty at different ages
Subjects
Height
Weight
BMI
Age of onset
Males
Females
Males
Females
Males
Females
Males
Females
Total sample
282
187
149.8 (6.4)*
142.8 (6.5)
43.9 (9.1)
37.0 (6.5)
19.4 (0.2)
18.1 (0.2)
±
59
88
89
46
68
66
37
16
±
±
146.5 (6.1)
148.9 (5.8)
151.0 (5.8)
153.8 (6.3)
139.5 (5.7)
142.4 (5.3)
146.3 (3.2)
149.9 (6.1)
±
±
39.4 (6.3)
42.8 (8.2)
46.1 (9.7)
48.0 (9.4)
35.9
35.5
40.0
40.6
±
18.3 (0.3)
19.2 (0.3)
20.1 (0.4)
20.1 (0.5)
18.4
17.5
18.7
18.0
±
±
±
0.001
0.001
At
At
At
At
At
10
11
12
13
14
years
years
years
years
years
ANOVA p
0.001
(6.3)
(4.9)
(7.3)
(8.2)
0.003
0.001
(0.3)
(0.2)
(0.5)
(0.8)
0.087
*mean (SD)
positive correlations (P < 0.001) between weight and age of
pubertal onset in both sexes (girls r ˆ 0.26, boys r ˆ 0.33).
With respect to height, the pattern is similar: the later the
age of pubertal onset, the higher the mean height at this
maturation stage in both sexes (P < 0.001). There were
signi®cant positive correlations (P < 0.001) between these
two parameters both in girls (r ˆ 0.5) and in boys
(r ˆ 0.37).
Body mass index at onset of puberty
Body mass at pubertal onset is shown in Table 1. There
were no differences between the girls' groups with pubertal
onset at different chronological ages (P ˆ NS). In contrast,
the boys' subgroups did show differences in BMI according
to the age of pubertal onset (P < 0.001). There was also a
signi®cant positive correlation between the age of onset and
BMI in boys (r ˆ 0.22; P < 0.001), indicating a tendency
towards higher BMIs at pubertal onset when onset is later.
Adiposity at pubertal onset
At pubertal onset, as Table 2 shows, the sums of the four
subcutaneous skinfolds, SUM, did not differ either in the
girls' subgroups (P ˆ NS) or in the boys' groups (P ˆ NS).
Study of the upper arm fat estimate (UFE), as Table 2
shows, revealed no signi®cant differences at pubertal onset
between the different groups in either sex: neither between
the boys (P ˆ NS), nor between the girls (P ˆ NS). Comparison of percentage of body fat mass at pubertal onset
(see Table 2) revealed no signi®cant differences either
between the boys' subgroups (P ˆ NS) or between the
girls' groups (P ˆ NS).
Adiposity at prepubertal period
Figure 2 shows the progressive and statistically signi®cant
(P < 0.001) changes of the mean of the fat mass (UFE
(Figure 2a); SUM (Figure 2b) and %BF (Figure 2c)) during
the prepubertal stage in girls whose pubertal onset was at
11, 12 and 13 y, respectively.
Figure 3 shows the prepubertal evolution of the same
parameters in boys (UFE (Figure 3a); SUM (Figure 3b) and
%BF (Figure 3c)), who started their puberty at the age of
12, 13 and 14 y, respectively. For all these variables the
changes observed each year were statistically signi®cant in
all the groups (P < 0.001).
Discussion
The results of longitudinal studies of growth have traditionally been expressed according to chronological age.
Another way of analyzing the results is to differentiate
between early and late maturers. Different criteria have
been used: the age at which peak height velocity (PHV) is
observed (Beunen et al, 1994), the advance or delay in bone
maturation as regards chronological age, and also menarcheal age (van Lenthe et al, 1996). In our study the criterion
used for the creation of subgroups with different rhythms of
maturation was the age of clinical onset of puberty. We
analyzed the data according to an equivalent moment of
maturation in all groups: pubertal onset, a criterion that few
authors have used (de Ridder et al, 1992). Studies that use
PHV as their reference point for maturation do not describe
the characteristics of their sample at pubertal onset (Buckler, 1990).
We did not attempt to perform comparisons of boys and
girls because the onset of puberty corresponds to different
maturation stages in the development of each sex. Genital
Table 2 SUM, UFE and % body fat, at pubertal onset in subgroups of boys and girls starting puberty at different
ages.
SUM
UFE
% body fat
Age of onset
Males
Females
Males
Females
Males
Females
Total sample
42.0 (1.3)*
42.1 (1.3)
18.3 (0.6)
17.6 (0.6)
20.4 (0.4)
25.1 (0.3)
At
At
At
At
At
35.5
42.3
43.5
47.0
45.8 (2.5)
37.7 (1.5)
42.0 (3.5)
44.9 (4.6)
±
±
15.6 (1.1)
19.5 (1.2)
18.0 (1.1)
19.6 (1.5)
18.9 (1.1)
15.9 (0.7)
17.9 (1.5)
18.2 (1.9)
±
±
18.8 (0.6)
20.7 (0.6)
20.7 (0.7)
21.0 (1.0)
26.0 (0.3)
24.2 (0.4)
24.9 (0.8)
25.9 (0.9)
±
10
11
12
13
14
years
years
years
years
years
ANOVA p
±
(2.1)
(2.3)
(2.6)
(3.8)
0.055
0.07
0.115
0.154
0.106
0.088
European Journal of Clinical Nutrition
Puberty begins with a characteristic subcutaneous body fat mass in each sex
B Vizmanos and C MartõÂ-Henneberg
206
Figure 2 Mean fat mass evolution during the prepubertal period in each
group of girls: (a) upper arm fat estimate (UFE); (b) sum of four skinfolds
(SUM); (c) percentage of body fat (%BF). The analysis was made three
(3 y), two (2 y) and one (1 y) year before puberty and at the moment of the
pubertal onset (onset). The paired t-test between each pair of consecutive
years was signi®cant (P < 0.001) in all the cases.
stage G2 in males represents an earlier situation in pubertal
development than Tanner's breast stage M2 in girls (Marshall & Tanner, 1986). The estradiol levels at M2 in girls
are already high in relation to the values they will reach at
later stages, while in males the increase in testosterone
levels does not take place until G3 (Argente et al, 1986).
Equally, in girls the peaks of human growth hormone
(HGH) and insulin-like growth factor-1 (IGF-1) tend to
appear at stage M2; this may account for the earlier growth
peak in this sex (Kawai et al, 1999). Furthermore, morphological studies show that even at pubertal stage M2
there is a clear growth of the volume of female reproductive organs (Buzi et al, 1998).
Weight, height and BMI increase with age in both
sexes. Our mean values of BMI are slightly higher than
those recorded in other European studies (Buckler, 1990;
Rolland-Cachera et al, 1982), a tendency also reported in
another Spanish study (HernaÂndez et al, 1988). Our results
indicate that in girls we found no signi®cant differences in
the body mass of those who start puberty at 10, 11, 12 or
European Journal of Clinical Nutrition
Figure 3 Fat mass evolution (mean) during the prepubertal period in
each group of boys: (a) upper fat mass estimate (UFE); (b) sum of four
skinfolds (SUM) and (c) percentage of body fat (%BF). The analysis was
made three (3 y), two (2 y) and one (1 y) year before puberty and at the
moment of the pubertal onset (onset). The paired t-test between each pair
of consecutive years was signi®cant (P < 0.001) in all the cases.
13 y; in contrast, the boys show progressively higher BMIs
the later puberty begins (P < 0.001). In our study we have
found that at the beginning of puberty the variables weight,
height and BMI are more closely related to chronological
age than to maturational stage.
However, the BMI, which is widely used as an expression of adiposity (Guillaume, 1999) because its two components (weight and height) are more frequently measured
than skinfold thickness, does not re¯ect the difference
between the compartments of body composition (SarrõÂa
et al, 1998).
Provided observers are adequately trained, measuring
subcutaneous body fat mass is an appropriate technique
in studies with broad samples (van Lenthe et al, 1996;
Buckler, 1990) and has proved to be a useful reference in
epidemiological studies for the exploration of adolescents
(Hammond et al, 1994). In addition, subcutaneous body fat
mass measured in this way has been correlated with total
body fat mass assessed using other methods (Durnin &
Rahaman, 1967; Brook, 1971; Deurenberg et al, 1990;
Puberty begins with a characteristic subcutaneous body fat mass in each sex
B Vizmanos and C MartõÂ-Henneberg
SarrõÂa et al, 1998). At the onset of the study (1987),
anthropometry was the best known technique, and also
the cheapest, fastest and least invasive at our disposal.
Our sample show slightly higher mean values of the sum
of four skinfolds according to age than those reported
in another study (Buckler, 1990), although there are no
differences between our results and those of other Spanish
studies (HernaÂndez et al, 1988; SarrõÂa et al, 1998). We did
not ®nd signi®cant differences as regards age of pubertal
onset in either boys or girls when comparing the SUM
variable. The mean of the SUM in the 187 girls at stage
S2 of mammary development was 42.1 ( 1.3 mm), very
similar to that obtained in another study in a group of 68
girls in the same stage (46.0 3.2 mm; de Ridder et al,
1992).
The use of the upper arm fat estimate, validated by
magnetic resonance (Rolland-Cachera et al, 1997), is in
agreement with our SUM data, although the reference
values obtained in a small sample born during the 1950s
were lower than those obtained in the same way in our
study.
When percentage of body fat was analyzed in each sex,
no signi®cant differences were found between the subgroups of different age of pubertal onset. The average
percentage obtained in the males is similar to that obtained
with the same formula in another study (Hammond et al,
1994).
We analyzed during the prepuberty and for both sexes
(Figures 2 and 3), the evolution of the parameters taken as
adiposity indicators; however, in this analysis we only
could include the girls and boys whose onset of puberty
took place after the beginning of the study.
We saw a progressive increase in the skinfolds thickness
and in the UFE, showing similar quantitative values both in
boys and girls. The percentage of fat mass also increased
during the prepubertal period but in this case the values
differ between sexes, maybe due to the different development of the other body tissues.
This data support the idea that the characteristic fat mass
storage at the onset of puberty is progressively made during
the prepubertal period, and it happens independently of the
timing of puberty.
The onset of puberty could imply an increase in the total
daily energy expenditure (TDEE). Some investigators
relate this fact with the increase in the fat-free mass
(FFM), especially in boys, but not with the progression of
the pubertal stages (Molnar & Schutz, 1997; Bitar et al,
1999). On the other hand, other investigators think that the
energy balance plays an important role during the events
leading to the onset of puberty, a fact that involves an
increase of the energy expenditure tightly related to the
pubertal maturation (Brown et al 1996a, b) expressed as
testicular size. All these factors could be related to the
existence of a well-de®ned energy reserve at the pubertal
onset.
In conclusion, this study shows the relationship between
body fat mass measured anthropometrically and the beginning of pubertal maturation in both sexes.
Finding a body fat mass that is characteristic of pubertal
onset in both sexes suggests a link between the energy store
in the adipose tissue and the triggering of a new stage in
life, puberty. This study reinforces the hypothesis of a close
relation between the body's maturation process and a
speci®c energy store in the form of adipose tissue in both
sexes.
Acknowledgements ÐWe thank the children and parents for their continued
support over the protracted period of the study. The assistance of Drs Rosa
ClivilleÂ, Aurelia Moreno and Joan FernaÂndez in the early stages of the
study is gratefully acknowledged. We gratefully acknowledge Michael
Maudsley for improving the manuscript.
207
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Puberty begins with a characteristic subcutaneous body fat mass in each sex
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