Gender-related differences in elite gymnasts: the

female athlete triad

Edda Weimann
J Appl Physiol 92:2146-2152, 2002. doi:10.1152/japplphysiol.00572.2001

You might find this additional info useful...

This article cites 44 articles, 13 of which can be accessed free at:

http://jap.physiology.org/content/92/5/2146.full.html#ref-list-1

This article has been cited by 2 other HighWire hosted articles

Physiological responses to rock climbing in young climbers
Audry Birute Morrison and Volker Rainer Schöffl
Br J Sports Med, December , 2007; 41 (12): 852-861.
[Abstract] [Full Text] [PDF]

Growth and Skeletal Maturation in Male and Female Artistic Gymnasts

Neoklis A. Georgopoulos, Anastasia Theodoropoulou, Michel Leglise, Apostolos G. Vagenakis
and Kostas B. Markou
J Clin Endocrinol Metab, September 7, 2004; 89 (9): 4377-4382.
[Abstract] [Full Text] [PDF]

Downloaded from jap.physiology.org on April 4, 2011

Updated information and services including high resolution figures, can be found at:
http://jap.physiology.org/content/92/5/2146.full.html

Additional material and information about Journal of Applied Physiology can be found at:
http://www.the-aps.org/publications/jappl

This infomation is current as of April 4, 2011.

Journal of Applied Physiology publishes original papers that deal with diverse areas of research in applied physiology, especially
those papers emphasizing adaptive and integrative mechanisms. It is published 12 times a year (monthly) by the American
Physiological Society, 9650 Rockville Pike, Bethesda MD 20814-3991. Copyright © 2002 by the American Physiological Society.
ISSN: 0363-6143, ESSN: 1522-1563. Visit our website at http://www.the-aps.org/.
J Appl Physiol 92: 2146–2152, 2002;
10.1152/japplphysiol.00572.2001.
Gender-related differences in elite gymnasts:
the female athlete triad
EDDA WEIMANN
Medical Centre for Child Heath, Clinic for Pediatric Endocrinology and Metabolism,
Johann Wolfgang Goethe University, D-60590 Frankfurt, Germany
Received 5 June 2001; accepted in final form 28 November 2001
Weimann, Edda. Gender-related differences in elite gym-
nasts: the female athlete triad. J Appl Physiol 92: 2146–2152,
2002; 10.1152/japplphysiol.00572.2001.—High-intensity train-
ing can alter the normal pattern of pubertal development in
elite gymnasts. We investigated sex hormones, the ob gene
product leptin, body composition, nutrition, and eating habits
in female and male elite gymnasts from national cadres to
elucidate gender-related differences. Serum leptin levels
were decreased, particularly in pubertal girls, and did not
show the normal developmental pattern. After leptin levels
were transformed into standard deviation scores, mainly
pubertal female gymnasts had significantly lower values
than normal controls of the same gender, pubertal stage, and
body mass index. The percentage of body fat was reduced
compared with a normal age-matched population in both
genders but to a higher degree in female gymnasts. When
leptin standard deviation scores were based on percent body
fat instead of body mass index, mean values were still sig-
nificantly decreased compared with those of normal controls:
⫺1.05 in girls (P ⬍ 0.001) and ⫺0.60 in boys (P ⫽ 0.025). In
both genders, total energy consumption and nutritional in-
take were insufficient, although to a lesser extent in male
gymnasts. Pubertal development is influenced to a different
degree in female and male elite gymnasts. In contrast to their
male counterparts, high-intensity training takes place dur-
ing the sensitive phase of pubertal maturation in female
gymnasts. Whereas the girls displayed low estrogen levels,
hypoleptinemia, reduced body fat mass, insufficient caloric
intake, and retarded menarche, the pubertal development of
male gymnasts remained almost unaltered.
puberty; gymnastics; leptin; body composition
HIGH-INTENSITY TRAINING DISPLAYS gender-related differ-
ences in athletes. In addition, the influence of endur-
ance training on pubertal and physical development
varies greatly, depending on the nature of sports. Mild
hyperandrogenism can occur in female world-class
swimmers (47), whereas highly trained female long-
distance runners tend to develop cycle abnormalities
(8). In male long-distance runners, testosterone levels,
libido, and reproductive function are decreased (13,
29). When growth development of female gymnasts
and swimmers is compared, gymnasts present lower
Address for reprint requests and other correspondence: E.
Weimann, Medical Centre for Child Heath, Clinic for Pediatric
Endocrinology and Metabolism, Theodor-Stern-Kai 7, D-60590
Frankfurt/FRG (E-mail: eweimann@zki.uni-frankfurt.de).
2146 8750-7587/02 $5.00 Copyright © 2002 the American Physiological Society
growth velocity and a marked stunting of leg-length
growth, and they fail to reach full familial height (43).
Even metabolism differs between female and male
top athletes. Because of higher estrogen concentra-
tions, the oxidation of amino acids and carbohydrate is
lower during endurance training in girls, whereas
there is a higher proportion of lipid oxidation (41). In
ultra-endurance exercise, such as the Ironman triath-
Downloaded from jap.physiology.org on April 4, 2011
lon, estradiol (EE) was 58% increased and testosterone
was 58% decreased in men postrace, whereas no sig-
nificant changes were noted for these hormones in
women (20).
Practitioners of sport disciplines in which a thin
body is required for better performance are at risk for
developing the female athletic triad that is character-
ized by cycle abnormalities, eating disorders, and pre-
mature osteoporosis (37, 47). Various factors may
cause the known disturbances of pubertal and physical
development in athletes. High levels of physical activ-
ity result in increased secretion of endorphins (15),
which, in combination with caloric undernutrition (28,
46), causes an abnormal regulation of the hypothala-
mus (3). This dysregulation decelerates the pulse fre-
quency of gonadotropin secretion. The subsequent de-
crease in follicle-stimulating hormone (FSH) and
luteinizing hormone (LH) levels (13, 45, 46) is likely to
alter pubertal maturation. Furthermore, low estrogen
levels and insufficient protein and calcium intake,
combined with late menarche, potentially lead to an
increased incidence of spontaneous stress fractures,
scoliosis (48), and the development of premature
osteoporosis (35).
The ob gene product leptin that is secreted by adipo-
cytes is supposed to be involved in the regulation of
energy intake and energy expenditure (9). It inhibits
the synthesis of the appetite-stimulating neuropeptide
Y (NPY) after binding to a specific receptor on NPY-
producing neurons in the hypothalamus (40). Clinical
studies have demonstrated that serum leptin reflects
body fat mass (FM) in normal-weight and obese adults
(12). This constitutive regulation of leptin synthesis is
modulated by a number of nonhormonal and hormonal
variables that superimpose a short-term (several hours
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
http://www.jap.org
 GENDER-RELATED DIFFERENCES IN ELITE GYMNASTS
to 1 day) regulation (5). Leptin levels increase with
food intake and decrease during periods of starvation
(24, 30). Apart from its effects on energy homeostasis,
leptin also has a profound influence on the secretion of
pituitary hormones. During starvation, low leptin lev-
els influence the secretion of gonadotropins and, sub-
sequently, sex steroids, possibly through a lack of sup-
pression of NPY (1). Thus a decline in serum leptin
exerts an overall suppressive effect on the reproductive
axis, which can be restored by exogenous leptin admin-
istration in rodents (10, 21). These experimental find-
ings are consistent with clinical observations. In an-
orexia nervosa, amenorrhea is a typical feature, and
there is evidence that this disturbance is related to the
very low leptin levels in this clinical condition (33).
Leptin is postulated to be the link among fat stores,
pubertal development, and LH-releasing hormone
(LHRH) secretion. There is evidence that in humans a
rise in leptin can serve as a permissive signal for the
onset of puberty (31). The regulation and variation of
leptin levels may influence the development and main-
tenance of reproductive functions observed in athletes
involved in aesthetically based sports. Leptin increases
in the luteal phase of the menstrual cycle. In amenor-
rheic athletes, the diurnal pattern of 24-h leptin levels
is absent (26). Up to now, sex hormones have not been
found to regulate leptin secretion directly in female
athletes (44). Only physically powerful changes in en-
ergy expenditure, such as a marathon run, seem to
influence the regulation of serum leptin levels in men
(27), and, accordingly, leptin levels do not mirror rela-
tive training stress in athletes (36).
We want to test whether there is a link among
energy stores, leptin levels, and the pattern of pubertal
development that can lead to gender-related differ-
ences in the pubertal and physical development of elite
gymnasts.
SUBJECTS AND METHODS
Subjects. All German elite gymnasts training in national
cadres gather and train on a regular basis at the Olympic
Training Centre in Frankfurt/Main. During one common
workout, the participating gymnasts (22 girls: 13.6 ⫾ 1.0 yr;
and 18 boys: 12.4 ⫾ 1.6 yr) were enrolled in this study.
Informed consent was obtained from both gymnasts and
parents. The physical training load (number of hours per
week) and the age at the start of the intensive training
regime were recorded.
Assessments. Body mass index (BMI) was calculated as
weight (kg)/height2 (m). Body height of gymnasts was mea-
sured with a stadiometer (Seneca). Pubertal clinical staging
was performed according to Marshall and Tanner (32).
Plasma LH (Enzymun, Boehringer Mannheim) and FSH
(Enzymun, Boehringer Mannheim) responses to a 100-␮g
intravenous bolus of LHRH (Ferring) were measured in all
patients after 0 and 30 min. Additionally, EE (RIA, Biodata
Diagnostics), testosterone (RIA, Biodata Diagnostics), and
insulin-like growth factor I (IGF-I; RIA, Nichols) were ascer-
tained to provide information about the gonadal and hypo-
physeal axes (7). In addition, the ratio of LH to FSH (LH/
FSH) after 30 min was used to further grade the prepubertal
(LH/FSH ⬍ 1) and pubertal (LH/FSH ⱖ 1) stage (22).
J Appl Physiol • VOL
2147
Skinfold thickness and bioelectric impedance analysis
(BIA) were used as indirect methods for the determination of
body composition and to evaluate peripubertal changes in
FM and fat free mass (FFM). Triceps skinfold measurement
was performed with a Holtain caliper; FM and FFM were
calculated by using the Slaughter formula (39). Body compo-
sition by BIA was determined with the regression model
of Schäfer et al. (38). The percentage of body fat (%BF)
was calculated by the following equation: %BF ⫽ 100 ⫻
[(weight ⫺ FFM)/weight].
To examine the nutritional status, caloric intake was re-
corded and assessed over 3 days, including 1 day without
training, and analyzed by the computer program DIET 2000.
Eating habits of female and male gymnasts were evaluated
by a standardized interview.
Leptin RIA. Serum leptin levels were measured by a sen-
sitive RIA by using recombinant human leptin (Mediagnost,
Tübingen, Germany) for standards and tracer preparation
(6). In brief, tracer was prepared with 2.5-␮g leptin, as
described in detail with the use of the chloramine T method
(4). The radiolabeled protein was further purified by exclu-
sion chromatography on a 1.5 ⫻ 90 cm column of Sephadex
G-50 (Pharmacia, Freiburg, Germany) and was stored at
Downloaded from jap.physiology.org on April 4, 2011
⫺20°C. Standards were prepared by geometrical dilutions of
recombinant human leptin in assay buffer [0.05 mol/l sodium
phosphate, pH 7.4, 0.1 mol/l NaCl, 0.1% (vol/vol) gelatine
from teleost fish (Sigma Chemical, Munich, Germany), 0.1%
(vol/vol) Triton X-100 (Serva, Heidelberg, Germany), 0.05%
(wt/vol) NaN3] between 12.5 and 0.049 ␮g/l. Serum samples
were diluted 1:3 with assay buffer before measurement. Sen-
sitivity with undiluted samples was 0.03 ␮g/l, corresponding
to 0.003 ng per tube. The intra- and interassay coefficients of
variations were 0.8 and 8.5%, respectively (n ⫽ 10). Excellent
parallelism with the standard curve was obtained with serial
dilutions of human sera. Spiking experiments with 0.1 ng per
tube yielded a recovery of 97 ⫹ 2.1%. Leptin levels were
adjusted for gender, pubertal stage, and BMI by calculating
leptin standard deviation scores (SDS) (BMI based) (6).
Statistics. Statistical analysis comparing the prepubertal
and pubertal groups was performed with the Wilcoxon Mann-
Whitney U-test; further analysis was done by using Spear-
man’s rank correlation test. Results are reported as means ⫾
SD; P values ⬍ 0.05 were considered statistically significant.
For comparison, leptin levels in a large cohort of healthy
normal children and adolescents were used. To correct for
gender, pubertal stage, and BMI, SDS (Z score) were calcu-
lated, applying the formulas given by Blum et al. (6). For
calculation of leptin SDS referred to %BF, the following
equations were derived from sufficiently large cohorts of
healthy children and adolescents of corresponding age as the
gymnasts, applying a similar approach as for SDS based on
BMI (6): leptin(SDS) ⫽ [ln (leptin) ⫺ ln (0.8952) ⫺ 0.06877 ⫻
%BF]/0.48952 for girls (n ⫽ 108) and leptin(SDS) ⫽ [ln(lep-
tin) ⫺ ln(0.4836) ⫺ 0.07315 ⴱ %BF]/0.53849 for boys (n ⫽ 71).
RESULTS
Training intensity. Female gymnasts started at an
earlier age compared with male gymnasts and, there-
fore, had a longer history of high-impact training at the
time of investigation (6.8 ⫾ 1.3 vs. 3.9 ⫾ 1.6 yr in boys).
Also, they trained more hours per week than their
male counterparts (22.1 ⫾ 1.7 vs. 15.9 ⫾ 5.0 h in boys).
These differences, years of intensive training (P ⫽
0.003), and number of training hours per week (P ⫽
0.006) were statistically significant.
92 • MAY 2002 • www.jap.org
2148 GENDER-RELATED DIFFERENCES IN ELITE GYMNASTS
Table 1. Hormone levels in female and male elite gymnasts
Girls
Prepubertal
n 7
Estradiol, pg/ml 17.6 ⫾ 4.2
Testosterone, ng/dl 28.4 ⫾ 5.4
IGF-I, ␮g/l 347.8 ⫾ 145.9
Values are means ⫾ SD scores (SDS); n, no. of subjects. IGF-I, insulin-like growth factor I. * Significant statistical difference between
prepubertal and pubertal male gymnasts, P ⬍ 0.05.
Hormone levels. According to the LH/FSH in the
LHRH test and Tanner stages, prepubertal and puber-
tal stages were classified (Table 1). A significant pu-
bertal rise of EE levels indicating undisturbed sexual
maturation did not occur in female gymnasts (17.6 ⫾
4.2 pg/ml prepubertal vs. 23.9 ⫾ 13.4 pg/ml pubertal).
In contrast, the male gymnasts mirrored their corre-
sponding age-matched peers in that they showed a
significant pubertal rise in testosterone levels (26.4 ⫾
8.1 to 145.6 ⫾ 135.8 ng/dl), which were normal for age.
IGF-I showed normal age-dependent serum levels, ex-
cluding severe growth hormone deficiency. LHRH test-
ing exhibited normal hypophyseal stimulation in ei-
ther gender, excluding the possibility of true secondary
hypogonadism. Pubertal elevation of LH/FSH (LH/
FSH ⱖ 1) showed a delay of 2.3 yr in female gymnasts
compared with nonathletic counterparts (14), whereas
no pubertal delay was seen in male gymnasts.
Body composition. With the use of BIA and skinfold
thickness to examine body composition indirectly, sig-
nificant peripubertal changes in FM and FFM occurred
(Table 2). BMI, FM, and FFM were significantly differ-
ent in prepubertal and pubertal female gymnasts,
whereas in boys only BMI and FFM were different.
Body composition exhibited a dimorphic pattern dur-
ing sexual maturation: in girls, there was a dispropor-
tionate increase in FM, whereas in boys FFM increased
in relation to body weight. The percentage of FM (%BF)
by BIA was, on average, significantly higher in girls
than in boys (14.4 vs. 10.4%, P ⬍ 0.05). In both gen-
ders, %BF was significantly lower than in normal (non-
gymnasts) children and adolescents of the same age
(6): 14.4 vs. 21.9% in girls (P ⬍ 0.01) and 10.4 vs. 15.2%
in boys (P ⬍ 0.05). Whereas in female gymnasts the
Table 2. Body composition of prepubertal and
pubertal elite gymnasts
Girls Boys
Prepubertal Pubertal Prepubertal Pubertal
n 7 15 6 12
BMI, kg/m2 16.5 ⫾ 1.4* 18.0 ⫾ 1.2* 16.2 ⫾ 1.15† 17.9 ⫾ 1.6†
FM BIA, kg 3.0 ⫾ 2.3* 5.3 ⫾ 2.5* 3.1 ⫾ 2.3 2.3 ⫾ 1.4
FM SF, kg 3.3 ⫾ 1.0* 4.8 ⫾ 1.2* 2.9 ⫾ 1.0 3.3 ⫾ 0.6
FFM BIA, kg 30.0 ⫾ 3.5* 35.5 ⫾ 3.3* 30.6 ⫾ 3.9† 39.5 ⫾ 7.2†
FFM SF, kg 29.6 ⫾ 4.2* 35.8 ⫾ 3.3* 30.8 ⫾ 4.5† 38.6 ⫾ 6.4†
Values are means ⫾ SDS; n, no. of subjects. BMI, body mass index
(weight/height2); FM, fat mass; FFM, fat-free mass; BIA, bioelectric
impedance analysis; SF, skinfold. Significant statistical difference
within groups: for *girls and †boys, P ⬍ 0.05.
J Appl Physiol • VOL
Boys
Pubertal Prepubertal Pubertal
15 6 12
23.9 ⫾ 13.4 9.0 ⫾ 3.7 14.0 ⫾ 6.3
36.3 ⫾ 15.1 26.4 ⫾ 8.1* 145.6 ⫾ 135.8*
422.9 ⫾ 171.4 197.2 ⫾ 84.8* 338.1 ⫾ 67.0*
mean percentage of FM increased from 12.3 to 15.3%
during pubertal development, the male gymnasts
showed a decrease from 13.0 to 9.2%. The relatively
higher increase in FFM during puberty in boys was at
least partially due to a more pronounced increase in
muscle mass, as indicated by circumference measure-
ments of the upper arm (22.9 cm in girls vs. 24.0 cm in
boys).
Nutrition. As a heavy load of training takes place in
elite gymnasts during the sensitive phase of pubertal
Downloaded from jap.physiology.org on April 4, 2011
growth and development, daily food intake was fol-
lowed over 3 days and was examined on the basis of the
national recommendations of the German Society for
Nutrition. The percentage of the various consumed
nutritional components was as follows: 54.9% carbohy-
drate, 13.5% protein, and 30.8% fat in girls, and 46.9%
carbohydrate, 13.3% protein, and 36.2% fat in boys.
Whereas in girls the proportion of the nutritional com-
ponents was well compliant with the recommendations
given by the German Society for Nutrition, the boys did
not meet these guidelines. In both genders, total caloric
intake was markedly insufficient, considering total en-
ergy expenditure during training, although less so in
boys (female gymnasts: 1,418.4 ⫾ 525.3 kcal/day vs.
male gymnasts: 2,159.1 ⫾ 42.4 kcal/day). This is re-
flected in the diminished %BF of gymnasts compared
with the German age-matched population: 14.4 vs. 22%
in girls and 10.4 vs. 20% in boys. Female gymnasts
showed an average nutritional intake that was ⬍50%
for vitamin A, vitamin B complex, vitamin D, magne-
sium, calcium, and iodine, whereas male elite gym-
nasts showed a reported mean intake that was ⱖ50%
less than the recommendation for vitamin A, vitamin
D, iodine, and carbohydrates. In elite gymnasts, an
increased utilization was observable for vitamin C,
which was being consumed as a prophylactic anti-
influenza supplementation.
Leptin levels. Mean leptin levels were 1.4 ⫾ 0.9 and
0.7 ⫾ 0.7 ␮g/l in girls and boys, respectively. Leptin
levels in elite gymnasts did not follow the normal
developmental pattern, with a steady increase in girls
and a peak in boys of pubertal stage 2. Whereas leptin
levels increased in female gymnasts with a peak at the
pubertal stages of breast stage 2 and pubic hair stage
2, leptin levels slightly decreased in boys. In all gym-
nasts, leptin levels correlated with the amount of FM
(r ⫽ 0.60, P ⫽ 0.005 in girls and r ⫽ 0.44, P ⫽ 0.038 in
boys). Furthermore, in female but not in male gym-
nasts, leptin levels were significantly correlated with
92 • MAY 2002 • www.jap.org
 GENDER-RELATED DIFFERENCES IN ELITE GYMNASTS 2149

Table 3. Leptin levels in female gymnasts at various

pubertal stages
Tanner Stage

1 2 3 4

Pubes 1.51 ⫾ 0.59 1.72 ⫾ 1.17 1.18 ⫾ 0.5 1.15 ⫾ 1.07

Breast 1.31 ⫾ 0.45 2.02 ⫾ 1.23 1.24 ⫾ 0.65 1.15 ⫾ 1.07

Prepubertal ⬍ 1 Pubertal ⱖ 1

LH-to-FSH ratio 1.1 ⫾ 0.4 1.5 ⫾ 1.0

Values are means ⫾ SDS in ␮g/l. LH, luteinizing hormone; FSH,
follicle-stimulating hormone.

BMI (r ⫽ 0.33, P ⫽ 0.049). Leptin was significantly

inversely correlated with IGF-I (r ⫽ ⫺0.47, P ⫽ 0.027)
in boys but not in girls. Leptin did not correlate further
with any other parameter examined. The results are
summarized in Tables 3 and 4. To compare leptin
levels of the examined groups of gymnasts with those
of “normal” (nongymnasts) controls, leptin values were
transformed into SDS (Z score) by using the equations

Downloaded from jap.physiology.org on April 4, 2011

derived previously from large cohorts of healthy chil-
dren and adolescents, accounting for gender, pubertal
stage, and BMI (6). In both genders, mean SDS values
were clearly decreased: ⫺2.77 ⫾ 1.96 (range ⫺7.39–
0.69) in girls and ⫺0.93 ⫾ 1.03 (range ⫺2.68–1.07) in
boys. To obtain sufficiently large cohorts for the com-
parison of prepubertal and pubertal groups, Tanner
stages 1 and 2 (prepubertal) and Tanner stages 3, 4,
and 5 (pubertal) were combined. Whereas in girls ad-
justed leptin SDS decreased markedly from ⫺1.21 ⫾
1.32 to ⫺3.99 ⫾ 1.62, leptin SDS remained unchanged
in boys (⫺0.94 ⫾ 1.14 vs. ⫺0.91 ⫾ 1.10) during puber-
tal development. Because leptin SDS were related to
BMI and because BMI is a less reliable measure of
body fat, leptin levels were also related to %BF deter-
mined by BIA and were compared with those in normal
controls of corresponding age (6) (Fig. 1). Again, there
was a significant decrease in leptin levels compared
with that in the controls in both genders, although less
marked: leptin SDS ⫽ ⫺1.05 ⫾ 1.31 in girls (P ⬍ 0.001)
and ⫺0.60 ⫾ 1.12 in boys (P ⫽ 0.025).
DISCUSSION
More than two decades ago, clinical studies pro-
posed a link between body FM and sexual matura-
Table 4. Leptin levels in male gymnasts at various
pubertal stages
Tanner Stage
1 2 3 4
Pubes 1.2 ⫾ 1.12 0.63 ⫾ 0.4 0.63 ⫾ 0.24
Prepubertal
⬍3 ml
Testicle volume 1.1 ⫾ 1.36
⬍1
LH-to-FSH ratio 1.02 ⫾ 1.06
Values are means ⫾ SDS in ␮g/l.
J Appl Physiol • VOL
Fig. 1. Serum leptin levels vs. percentage of body fat determined by
bioelectric impedance analysis. A: girls. B: boys. E, Healthy normal
(nongymnast) children and adolescents between 5 and 16 yr of age
(controls); ■, elite gymnasts. Solid line, regression line of the control
group.
tion. An early onset of pubertal development was
observed in obese children (49), whereas delayed
puberty occurred in lean ballet dancers (19). In this
context, Frisch and Revelle postulated the “critical
weight” hypothesis for the induction of sexual mat-
uration (18) and, thereby, provoked a controversial
discussion (23). In the meantime, various investiga-
tions established an association between body FM
and fertility (16, 17). In light of the discovery of
leptin and its role as a permissive signal for the
normal functioning of the hypothalamus-pituitary-
gonadal axis (2), there is good reason to assume that
leptin is the molecular link, the decisive permissive
signal, among adequate energy stores, adipose tis-
0.39 ⫾ 0.26 sue, and the onset of puberty. The question remains
whether this mechanism plays a role in the retarded
Pubertal pattern of sexual maturation in elite gymnasts.
ⱖ3 ml In the conducted study, leptin levels were low in
0.63 ⫾ 0.31 elite gymnasts and did not follow the developmental
ⱖ1 pattern in normal children and adolescents, exhibit-
0.59 ⫾ 0.3
ing a steady increase during sexual maturation in
girls and a peak at Tanner stage 2 in boys (6, 11, 31,
92 • MAY 2002 • www.jap.org
2150 GENDER-RELATED DIFFERENCES IN ELITE GYMNASTS
34). Leptin was associated with body fat, consistent
with numerous reports on other cohorts. Because
leptin levels in normal children and adolescents de-
pend not only on FM but also on gender and pubertal
stage (11), they were adjusted for gender, pubertal
stage, and BMI by calculating leptin SDS (BMI
based) (6). These adjusted leptin values were dimin-
ished compared with those in normal controls, espe-
cially in pubertal female gymnasts in whom leptin
levels were clearly subnormal. However, BMI is not
a very reliable measure of body fat for groups under-
going differing degrees of physical exercise. In highly
trained athletes, an increase in BMI is due to an
increase in muscle mass rather than FM as shown in
this study. To circumvent this pitfall, leptin levels
were also compared with %BF determined by BIA.
Because the control groups were not large enough to
stratify according to pubertal stage, the adjustment
of leptin levels was performed only for gender and
%BF. Again, the adjusted leptin levels [leptin SDS
(%BF based)] were significantly reduced, especially
in female gymnasts, although to a smaller degree.
That is, the elite gymnasts had relatively lower lep-
tin levels than normal nongymnast controls of the
same age and %BF. This finding indicates the pres-
ence of additional suppressive regulators or the ab-
sence of stimulating regulators. However, to draw
generally valid conclusions, a lack of statistical
power related to the small sample sizes has to be
taken into consideration. In particular, the groups
become fairly small when the sample is divided into
the four Tanner stages or into a prepubertal and
pubertal category for both boys and girls. To obtain
a bigger sample size and get a deeper insight into
the physiological aspects of leptin secretion in elite
gymnasts, it would be a challenge to set up a simi-
lar study including gymnasts from other European
cadres.
Intense physical training can alter the normal
pattern of pubertal development of athletes. Factors
that influence sexual maturation are the time when
heavy impact training starts, the amount of training
hours per week, and whether a lean body shape is
considered important to practice this sport. Athletes
of leanness-related sport disciplines, such as gym-
nastics, ballet, rowing, figure skating, or long-dis-
tance running, belong to a high-risk category for
developing eating disorders. Consequently, we eval-
uated the eating habits of female and male gymnasts
by a standardized interview. In contrast to the boys,
the girls, particularly slightly older ones, were aware
of their daily body weight, took extreme care regard-
ing low-caloric food products, were knowledgeable
about the nutritional components of their daily diet,
and were susceptible to altering their eating behav-
ior. On the other hand, the nutritional intake of the
boys reflected the unhealthy eating habits of the
normal population, consuming too much fat and too
few complex carbohydrates. A study in elite rowers
revealed that the risk for eating disorders is moder-
ated by age, gender, and the weight category. Regu-
J Appl Physiol • VOL
lar evaluation of mood by using standardized ques-
tionnaires, such as the Profile of Mood States, may
act as useful tools in identifying athletes at risk for
developing eating disorders (42).
Nutritional deficiency certainly contributes to the
development of various neuroendocrine and meta-
bolic aberrations underlying exercise-related and
psychogenic hypothalamic amenorhea (25). Even
psychogenic functional hypothalamic amenorrhea is
associated with multiple endocrine-metabolic alter-
ations that are very similar with highly trained
female athletes with cycle abnormalities. Because
food restriction has a profound, suppressive effect on
leptin levels, which already becomes apparent after
1 day (24), it is most likely that the inappropriately
low leptin levels in the gymnasts are due to their
restrained eating behavior.
Typical hallmarks, such as reduced FM, delayed
menarche, and delayed bone maturation, underline the
inadequate metabolic reserve of female elite gymnasts.
In addition, endocrine deficiencies such as low mean
Downloaded from jap.physiology.org on April 4, 2011
EE levels in pubertal girls were found. The elevated
levels of testosterone in most of the examined female
subjects might be caused by the low body FM, which is
associated with diminished aromatase activity, leading
to an insufficient conversion of androgens to estrogens.
In contrast, the male counterparts displayed nearly
unaltered pubertal development. The observed differ-
ences between female and male gymnasts are likely
due to a later start of high-impact training, reduced
training intensity during pubertal growth spurt, and
more appropriate FM and energy intake of the male
gymnasts.
In conclusion, the synopsis of recent scientific devel-
opments on the role of leptin and the findings of this
study in elite gymnasts suggest the following scenario:
high physical training load and, consequently, high-
energy expenditure impair the development of FM
appropriate for age. The lack of fat reserves per se
leads to low leptin levels. This effect is further ag-
gravated by insufficient caloric intake due to current
aesthetic standards in this special sports discipline,
particularly in girls. As a result, leptin levels are
substantially decreased, which, in turn, does not allow
the hypothalamus-pituitary-gonadal axis to be acti-
vated to induce puberty in a timely manner. As a
consequence, pubertal development and the pubertal
growth spurt are delayed or, in severe cases, never
occur properly. Thus leptin may close the gap between
the clinical observation of low FM and restrained eat-
ing behavior on one side and delayed sexual matura-
tion and growth on the other side in elite gymnasts.
Elite female gymnasts are at risk for developing the
female athletic triad showing late menarche, re-
strained eating behavior, and an increased rate of
stress fractures. For that reason, it is advisable to
monitor prepubertal and pubertal female gymnasts at
short intervals, estimating individual training volume
and training capacity to avoid harmful long-term side
effects of high-intensity training.
92 • MAY 2002 • www.jap.org
 GENDER-RELATED DIFFERENCES IN ELITE GYMNASTS
The author thanks W. F. Blum for support in measuring the leptin
levels and discussing the data.
REFERENCES
1. Ahima RS, Prabakaran D, Mantzoros C, Qu D, Lowell B,
Maratos-Flier E, and Flier JS. Role of leptin in the neuroen-
docrine response to fasting. Nature 382: 250–252, 1996.
2. Barash IA, Cheung CC, Weigle DS, Ren H, Kabigting EB,
Kuijper JL, Clifton DK, and Steiner RA. Leptin is a meta-
bolic signal to the reproductive system. Endocrinology 137:
3144–3147, 1996.
3. Barron JL, Noakes TD, Levy W, Smith C, and Millar PR.
Hypothalamic dysfunction in overtrained athletes. J Clin Endo-
crinol Metab 60: 803–806, 1985.
4. Blum WF and Breier BH. Radioimmunoassay for IGFs and
IGFBPs. Growth Regul 4, Suppl 1: 11–19, 1994.
5. Blum WF, Englaro P, Attanasio AM, Kiess W, and Rascher
W. Human and clinical perspectives on leptin. Proc Nutr Soc 57:
477–485, 1998.
6. Blum WF, Englaro P, Hanitsch S, Juul A, Hertel NT, Mül-
ler J, Skakkebaek NE, Heiman ML, Birkett M, Attanasio
AM, Kiess W, and Rascher W. Plasma leptin levels in healthy
children and adolescents: dependence on body mass index, body
fat mass, gender, pubertal stage, and testosterone. J Clin Endo-
crinol Metab 82: 2904–2909, 1997.
7. Burr IM, Sizonenko PC, Kaplan SL, Grumbach SL, and
Grumbach MM. Hormonal changes in puberty. I. Correlation of
serum luteinizing hormone and follicle stimulating hormone
with stages of puberty, testicular size, and bone age in normal
boys (Abstract). Pediatr Res 4: 25, 1970.
8. Burrows M and Bird S. The physiology of the highly trained
female endurance runner. Sports Med 30: 281–300, 2000.
9. Campfield LA, Smith FJ, and Burn P. The ob protein (leptin)
pathway—a link between adipose tissue mass and central neu-
ral networks. Horm Metab Res 28: 619–632, 1996.
10. Chehab FF, Lim ME, and Lu R. Correction of the sterility
defect in homozygous obese female mice by treatment with
recombinant human leptin. Nat Genet 12: 318–320, 1996.
11. Clayton PE, Gill MS, Hall CM, Tillmann V, Whatmore AJ,
and Price DA. Serum leptin through childhood and adoles-
cence. Clin Endocrinol (Oxf) 46: 727–733, 1997.
12. Considine RV, Sinha MK, Heiman ML, Kriaucciunas A,
Stephens TW, Nyce MS, Ohannesian JP, Marco CC, McKee
LJ, Bauer TL, and Caro JF. Serum immunoreactive leptin
concentrations in normal-weight and obese humans. N Engl
J Med 334: 292–295, 1996.
13. Cumming DC, Wheeler GD, and MacCall EM. The effects of
exercise on reproductive function in men. Sports Med 7: 1–17,
1989.
14. Dann TC and Roberts DF. Menarcheal age in University of
Warwick young women. J Biosoc Sci 25: 531–538, 1993.
15. Dixon G, Eurman P, Stern BE, Schwartz B, and Rebar RW.
Hypothalamic function in amenorrheic runners. Fertil Steril 42:
377–383, 1984.
16. Frisch RE. Fatness and fertility. Sci Am 3: 70–77, 1988.
17. Frisch RE. The right weight: body fat, menarche and ovulation.
Baillieres Clin Obstet Gynaecol 4: 419–439, 1990.
18. Frisch RE and Revelle R. Height and weight at menarche and
hypothesis of critical body weights and adolescent events. Sci-
ence 169: 397–398, 1970.
19. Frisch RE, Wyhak G, and Vincent L. Delayed menarche
and amenorrhea in ballet dancers. N Engl J Med 303: 17–21,
1980.
20. Ginsburg GS, O’Toole M, Rimm E, Douglas PS, and Rifai
N. Gender differences in exercise-induced changes in sex-
homone levels and lipid peroxidation in athletes participating
in the Hawaii Ironman triathlon. Ginsburg-gender and exer-
cise-induced lipid peroxidation. Clin Chim Acta 305: 131–139,
2001.
21. Gruaz NM, Lalaoui M, Pierroz DD, Englaro P, Sizonenko
PC, Blum WF, and Aubert ML. Chronic administration of
leptin into the lateral ventricle induces sexual maturation in
J Appl Physiol • VOL
2151
severely food-restricted female rats. J Neuroendocrinol 10: 627–
633, 1998.
22. Job JC, Chaussain JC, and Garnier PE. The use of luteiniz-
ing hormone-releasing hormone in pediatric patients. Horm Res
8: 171–187, 1977.
23. Johnson FE, Malina RM, and Galbrath MA. Height, weight
and age at menarche and the “critical weight” hypothesis. Sci-
ence 174: 1148–1149, 1971.
24. Kolaczynski JW, Considine RV, Ohannesian J, Marco C,
Opentanova I, Nyce MR, Myint M, and Caro JF. Responses
of leptin to short-term fasting and refeeding in humans: a link
with ketogenesis but not ketones themselves. Diabetes 45: 1511–
1515, 1996.
25. Laughlin GA, Dominguez CE, and Yen SS. Nutritional and
endocrine-metabolic aberrations in women with functional hy-
pothalamic amenorrhea. J Clin Endocrinol Metab 83: 25–32,
1998.
26. Laughlin GA and Yen SS. Hypoleptinemia in women athletes:
absence of a diurnal rhythm with amenorrhea. J Clin Endocrinol
Metab 82: 318–321, 1997.
27. Leal-Cerro A, Garcia-Luna PP, Astroga R, Parejo J, Peino
R, Diegu C, and Casanueva FF. Serum leptin levels in male
marathon athletes before and after the marathon run. J Clin
Endocrinol Metab 83: 2376–2379, 1998.
Downloaded from jap.physiology.org on April 4, 2011
28. Lindholm C, Hagenfeldt K, and Hagman U. A nutrition
study in juvenile elite gymnasts. Acta Paediatr Scand 84: 273–
277, 1995.
29. MacConnie SE, Barkan A, and Lampman RM. Decreased
hypothalamic gonadotropin-releasing hormone secretion in male
marathon runners. N Engl J Med 315: 411–417, 1986.
30. Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH,
Zhang Y, Fei H, Kim S, Lallone R, Ranganathan S, Kern
PA, and Friedman JM. Leptin levels in human and rodent:
measurement of plasma leptin and ob RNA in obese and weight-
reduced subjects. Nat Med 1: 1155–1161, 1995.
31. Mantzoros CS, Flier J, and Rogol AD. A longitudinal
assessment of hormonal and physiological alterations during
normal puberty in boys. V. Rising leptin levels may signal the
onset of puberty. J Clin Endocrinol Metab 82: 1066–1070,
1997.
32. Marshall WA and Tanner JM. Variations in pattern of
pubertal changes in girls (Abstract). Arch Dis Child 44: 291,
1969.
33. Matejek N, Weimann E, Witzel C, Mölenkamp S, Schwider-
gall S, and Böhles H. Hypoleptinemia in patients with an-
orexia nervosa and in elite gymnasts with anorexia athletica. Int
J Sports Med 20: 451–456, 1999.
34. Matkovic V, Ilich JZ, Skugor M, Badenhop NE, Goel P,
Clairmont A, Klisovic D, Nahhas RW, and Landoll JD.
Leptin is inversely related to age at menarche in human females.
J Clin Endocrinol Metab 82: 3239–3245, 1997.
35. Nichols DL, Bonnick SL, and Sanborn CF. Bone health and
osteoporosis. Clin Sports Med 19: 233–249, 2000.
36. Noland RC, Baker JT, Boudreau SR, Kobe RW, Tanner
CJ, Hickne RC, McCammon MR, and Houmard JA. Effect
of intense training on plasma leptin levels in male and female
swimmers. Med Sci Sports Exerc 33: 227–231, 2001.
37. Sanborn CF, Horea M, Simmers BJ, and Dieringer KI.
Disordered eating and the female athlete triad. Clin Sports Med
19: 199–213, 2000.
38. Schäfer F, Georgi M, Zieger A, and Schärer K. Usefulness of
bioelectric impedance and skinfold measurements in predicting
fat free mass derived from total body potassium in children.
Pediatr Res 35: 617–624, 1994.
39. Slaughter MH, Lohman TG, Boileau RA, Horswill CA,
Stillman RJ, van Loan MD, and Bemben DA. Skinfold equa-
tions for estimation of body fatness in children and youth. Hum
Biol 60: 709–723, 1988.
40. Stephens TW, Basinski M, and Bristow PK. The role of
neuropeptide Y in the anti-obesity action of the obese gene
product. Nature 377: 530–532, 1995.
92 • MAY 2002 • www.jap.org
2152 GENDER-RELATED DIFFERENCES IN ELITE GYMNASTS

41. Tarnopolsky MA. Gender differences in metabolism, nutrition
and supplements. J Sci Med Sport 3: 287–298, 2000.
42. Terry PC, Lane AM, and Warren L. Eating attitudes, body
shape perceptions and mood of elite rowers. J Sci Med Sport 2:
67–77, 1999.
43. Theintz GE, Howald H, Weiss U, and Sizonenko PC. Evi-
dence for a reduction of growth potential in adolescent female
gymnasts. J Pediatr 122: 306–312, 1993.
44. Thong FS, McLean C, and Graham TE. Plasma leptin in female
athletes: relationship with body fat, reproductive, nutritional and
endocrine factors. J Appl Physiol 88: 2037–2044, 2000.
45. Vigersky RA, Andersen AE, and Thompson RH. Hy-
pothalamic dysfunction in secondary amenorrhea associ-
ated with simple weight loss. N Engl J Med 297: 1141–1145,
1977.
46. Warren MP, Jewelewicz R, and Dyrenfurt I. The signifi-
cance of weight loss in the evaluation of pituitary response to
LHRH in women with secondary amenorrhea. J Clin Endocrinol
Metab 40: 601–611, 1975.
47. Warren MP and Shantha S. The female athlete. Baillieres
Best Pract Res Clin Endocrinol Metab 14: 37–53, 2000.
48. Warren MP and Stiehl AL. Exercise and female adolescents:
effects on the reproductive and skeletal systems. J Am Med
Womens Assoc 54: 115–120, 1999.
49. Zacharias L and Wurtman RJ. Age at menarche. N Engl
J Med 280: 868–875, 1969.

Downloaded from jap.physiology.org on April 4, 2011

J Appl Physiol • VOL 92 • MAY 2002 • www.jap.org