Full text of DOI:10.1007/BF03343915

J. Endocrinol. Invest. 24: 708-715, 2001
REVIEW ARTICLE
Consequences of sport training during puberty
J.N. Roemmich*, E.J. Richmond**, and A.D. Rogol**
*Department of Pediatrics, Division of Behavioral Medicine, State University of New York at Buffalo,
Buffalo, NY; **Department of Pediatrics, Division of Endocrinology, University of Virginia Health
Sciences Center, Charlottesville, VA, USA
ABSTRACT. Growth at puberty depends on one’s
genetic potential, nutritional status and a series
of hormones. Energy expenditure may modify the
effects of these three factors on the linear growth
rate and the relative proportions of fat-free and
fat mass. Participation in sports where weight con-
trol is not required does not seem to affect pu-
bertal timing or alter linear growth rate. The
growth and maturation of athletes in weight con-
trol sports have the additional burden of energy
output greater than intake; however, in only a mi-
nority the energy deficit is great enough to slow
growth and maturation. Studies focusing on male
wrestlers and female gymnasts are reviewed. In
the wrestlers the hormonal picture is consistent
with mild-to-moderate GH resistance and perhaps
mild maturational delay, especially in the lower
weight classes. The deficits in lean body mass and
fat mass “catch-up” quickly following the end of
training and competitive season. The situation
with the gymnasts is somewhat different, the goal
being to develop muscular strength within a short-
er and lighter physique. Marked under-nutrition
can keep these adolescents pre-pubertal for many
years of training and competition. Whether sub-
sequent growth is disproportionate or not remains
indeterminate, but the marked delay in the onset
of estrogen action can permanently cause the
skeleton to be under-mineralized. In conclusion,
most athletes continue to track along the centiles
of their genetic potential. To define the mecha-
nisms of growth and maturational delay one must
longitudinally study children in weight-control
sports.
(J. Endocrinol. Invest. 24: 708-715, 2001)
©2001, Editrice Kurtis
INTRODUCTION
timing and tempo of puberty has been previously
reviewed and the data quite clearly show few ef-
fects on growth or maturation (5, 6).
Metabolic fuel availability modifies the timing and
tempo of pubertal maturation and growth. Over-
nutrition reduces the age of onset of pubertal mat-
uration and accelerates growth (1, 2), while under-
nutrition delays these linked processes (3, 4). The
current review will apply this physiological frame-
work to the combination of high energy expendi-
tures and limited nutritional intake of some athletes
and how under-nutrition may lead to delayed ado-
lescence and slowed growth. The influence of
moderate-to-vigorous physical activity and sport
training in the absence of energy restriction on the
GROWTH AND MATURATION
Growth and sexual maturation are controlled, in large
part, by the GH, IGF-I and hypothalamic-pituitary-go-
nadal (HPG) axes. GH is the primary hormone re-
sponsible for somatic growth, having, in addition, po-
tent actions on protein, carbohydrate and lipid
metabolism. Many of the effects of GH, including
long bone growth, are mediated through IGF-I, which
is locally synthesized by target tissues or by the liver,
the predominant source of circulating IGF-I (7).
Pre-pubertally, resting GH secretion is modulated
primarily through two hypothalamic hormones,
GHRH and somatostatin (8). From infancy to child-
hood genetic determinants and environmental in-
fluences, such as nutrition or chronic disease influ-
ence GH-IGF-I axis function, thereby affecting the
growth potential. Serum IGF-I concentrations may
Key-words: Sport training, puberty, gymnasts, wrestlers, growth, body
composition, nutrition, exercise, hormones.
Correspondence: Dr. James N. Roemmich, Department of Pediatrics,
Division of Behavioral Medicine, State University of New York at Buffalo,
Farber Hall, Room G56, 3435 Main Street, Building 26, Buffalo, New York
14214-3000, USA.
E-mail: roemmich@buffalo.edu
Accepted April 6, 2001.
708

Consequences of sport training during puberty
70
60
50
40
30
20
10
2.5
2.0
1.5
1.0
0.5
0.0
C
C
D
D
D
A, B
A, B
A, C
B, D
B, D
A, C
Fig. 1 - Relative intake of energy (kcal/
kg/day), protein (g/kg/day), fat (g/kg/day),
and carbohydrate (CHO, g/kg/day) for
wrestler (᭺, no.=9) and control (᭹, no.=7)
groups. All subjects were tested in mid-
November, one-to-two weeks prior to the
first wrestling match (early), 3.5-to-4
months later (late) depending on when
the wrestlers no longer qualified for tour-
2.5
2.0
1.5
1.0
0.5
C
8
6
4
2
C
D
A, B
nament competition, and 3.5-to-4 months
B, D
A, C
B, D
A, B
A, C
after the wrestling season ended (post).
Like letters are significantly different.
Values expressed as mean ( SE). Modified
from (28), with permission.
Early
Late
Post
Early
Late
Post
decline with poor nutrition or chronic illness open-
ing up the negative feedback loop to increase GH
release. The net result is relative GH resistance.
At the onset of puberty, a marked acceleration in
growth velocity results from a complex network of
interactions between the GH-IGF-I and HPG axes.
Total GH secretion increases 2-to-3-fold controlled
by rising estrogen concentrations, even in the male
(9-11). Increases in serum IGF-I concentrations par-
allel the augmented GH secretion. Thus, at low con-
centrations, sex steroids act synergistically with GH
to mediate skeletal growth. At greater concentra-
tions, sex steroids, especially estrogen, induce epi-
physeal fusion in boys and girls (12, 13).
weight at menarche remained stable (14). The sig-
nals that reawaken the HPG axis at the onset of
puberty and keep it operative during puberty re-
main unclear. The hormone leptin, secreted pri-
marily from adipocytes in direct relation to lipid
content (15), acts as a nutritional signal to the re-
productive centers of the brain (14, 16-18) in-
cluding GnRH neurons of the mouse (19). Release
of GnRH is necessary for pubertal onset and prop-
er leptin signaling may be necessary for adeguate
GnRH release. Mutations in the leptin protein or
leptin receptor genes (20-23) prevent pubertal
maturation in humans. However, leptin does not
act as the sole trigger of puberty, but rather as
one of several metabolic signals necessary for pu-
bertal onset and progression (14, 16, 18). For in-
stance, Wade et al. (24), have established the im-
portance of metabolic fuel availability, especially
glucose, for maintaining reproductive function.
Serum IGF-I concentrations decrease with under-
nutrition and may modulate pubertal onset.
Serum IGF-I levels increase before puberty in pri-
mates (25) and central IGF-I infusions accelerate
pubertal onset in rats (26).
NUTRITION MODIFIES GROWTH AND
PUBERTAL TIMING
Pubertal timing and tempo are integrated through
genetic, nutritional, and environmental cues (14),
and are more a function of metabolic fuel avail-
ability than chronological age. For instance, age
at menarche declined from the mid-1800 to mid-
1900 in developed nations even though the body
66
64
62
60
58
56
54
52
50
48
46
4000
3500
3000
2500
2000
1500
1000
500
Pre-season body weight
E
C
C
AB
D
D
A
B
AB
AB
B
AB
AB
Fig. 2 - Daily energy intake (kcal/day) and
body weight (kg) for the wrestler (᭺,
no.=9) and control (᭹, no.=7) groups dur-
ing one week with a weight certification
for the wrestlers on Saturday. Like letters
are significantly different. Values ex-
pressed as mean ( SE). Modified from
(28), with permission.
A
A, B, E
Mon Tue Wed Thr Fri Sat Sun
Match
Mon Tue Wed Thr Fri Sat Sun
Match
709

J.N. Roemmich, E.J. Richmond, and A.D. Rogol
28
enough to slow growth and maturation. The re-
mainder of this review will focus on the growth and
maturation of two of these athletic groups: male
wrestlers and female gymnasts.
B
A
26
24
22
20
18
C
Male wrestlers
Wrestlers compete in weight classes and must weigh-
in before each competition to certify that their body
weight is less than the upper limit of the weight class.
Wrestlers reduce their body weight through a com-
bination of exercise and dietary restriction to com-
pete in a lower weight class in the hope of gaining a
competitive advantage against a younger, less ex-
perienced opponent. The typical wrestler practices 2
h to 2.5 h/day, 5 to 6 days/week and, after correction
for the basal metabolic rate, expends about 800 kcals
per practice (27). Despite great energy expenditures,
Roemmich et al. (28) found that wrestlers had nutrient
intakes 50% below recommended amounts (Fig. 1).
Moreover, when the energy intake and body weight
were monitored one week before a competition, on
no day did the wrestlers consume adequate energy
to meet the combined requirements of resting
metabolism, sport training, and growth (Fig. 2). When
repeated each week of a 12-to-16 week sport sea-
son, a chronic period of under-nutrition occurs as con-
firmed by reductions in protein nutritional status
(Fig. 3) (28-30).
A, B, C
Early
Late
Post
Fig. 3 - Serum prealbumin concentration (mg/dl) for the wrestler
(᭺, no.=9) and control (᭹, no.=7) groups. Like letters are signifi-
cantly different. Values expressed as mean ( SE). For definitions
see Figure 1. Modified from (28), with permission.
GROWTH AND MATURATION OF ATHLETES
IN WEIGHT CONTROL SPORTS
Participation in sports where weight control is not re-
quired does not appear to delay pubertal timing or al-
ter growth. Youth who participate in these sport are
normal or slightly advanced in their rates of growth
and maturation (5). Greater body size and pubertal
maturation are probably self-selected because the
strength and power advantages associated with ear-
lier maturation are major factors attracting children
to sport and for their success at sport (5).
Although all athletes participating in weight con-
trol sports such as wrestling, gymnastics, distance
running, and dance are at risk for energy drain and
limited metabolic fuel availability, only a small num-
ber actually experience a combination of high en-
ergy expenditure and restricted energy intake great
The under-nutrition of adolescent wrestlers may lead
to alterations in the HPG and GH-IGF-I axes, which,
as described above, control the rate of growth and
pubertal maturation. Roemmich et al. (31) found that
at the end of a sport season, wrestlers had low
testosterone and free-testosterone concentrations
while their serum LH concentrations remained un-
changed (Fig. 4) suggesting a central disruption of
12
10
8
8
7
6
5
4
3
2
A
A
6
A
4
Fig. 4 - Mean ( SE) concentrations of
testosterone, free testosterone, LH, and
DHEAS in the wrestler (᭺, no.=9) and
control (᭹, no.=7) groups during the ear-
ly and late portions of the wrestling sea-
son and during the post-season. Like let-
ters are significantly different (p<0.05).
2
40
35
30
25
20
15
350
325
B
B
Serum hormone concentrations are the
200
150
100
A
A, B
A
mean of 8 samples drawn every 20 min-
utes. Like letters indicate pꢀ0.05. Dashed
lines indicate upper and lower normal
range for each hormone concentration.
For definitions see Figure1. Modified from
A, B
10
Early
Late
Post
Early
Late
Post
(28), with permission.
710

Consequences of sport training during puberty
9
8
7
6
5
4
70
65
60
55
50
45
A
A
A
B
A
A
B
B
A
14
12
10
8
60
55
50
45
40
B
A
A
B
C
Fig. 5 - Body weight, percentage of body
fat, fat mass, and fat-free mass (FFM) for
D
A
C, D
the wrestler (᭺, no.=9) and control
(᭹, no.=7) groups. Like letters are signif-
icantly different. Values expressed as
A
6
mean ( SE). For definitions see Figure 1.
Early
Late
Post
Early
Late
Post
the HPG axis. Similar data have also been reported
for collegiate wrestlers (32). Reduced serum testos-
terone concentrations would reduce protein accrual
and the wrestlers had slowed growth in fat-free mass
(Fig. 5) as well as mid-arm and mid-thigh muscle plus
bone cross-sectional areas, two anthropometric mea-
sures of lean tissue accrual (28-30).
GH-IGF-I axis function was also disrupted during
the wrestling season (Fig. 6). A partial GH resistance
was indicated by late-season elevations in the
wrestlers’ serum GH concentrations while their
serum IGF-I concentrations were reduced due to
an opening of the IGF-I-mediated feedback inhibi-
tion of GH release. Decreases in serum growth hor-
mone-binding protein (GHBP) concentration may
have also modulated serum GH concentrations.
GHBP enhances the growth promoting effects of
GH and GH secretion is modified to account for the
GHBP concentration to ensure genetically deter-
mined growth continues (33). When GHBP con-
centrations are reduced, more GH is released to
continue growth at its genetically determined rate.
Reductions in GHBP concentrations may also sig-
nify a down-regulation of GH receptors, since
GHBP is an index of GH tissue receptor number
(34). Down-regulation would result in GH resistance
and reduced growth, so that even with increased
GH concentrations, growth will be slowed to con-
serve energy for critical body functions.
What effect do these hormonal alterations have on
the growth and maturation of wrestlers? Generally,
wrestlers are shorter than the average for their age
but this is probably due to self-selection (5). For in-
stance, a cross-sectional study (35) found that a ref-
erence group of boys was taller (1.9%) than a large
group of wrestlers after the age of 16.4 years, but
that the slope values for gain in height did not dif-
fer. However, these data do not address whether
10
8
500
400
300
200
100
B
A
A, B
6
B
A
4
Fig. 6 - Mean ( SE) concentrations of GH,
IGF-I, GH-binding protein (GHBP), and
IGFBP-3 in the wrestler (᭺, no.=9) and
control (᭹, no.=7) groups during the ear-
ly and late portions of the wrestling sea-
son and during the post-season. Like let-
ters are significantly different (p<0.05).
Serum hormone concentrations are the
mean of 8 samples drawn every 20 mi-
nutes. Like letters indicate pꢀ0.05. Dashed
lines indicate upper and lower normal
range for each hormone concentration.
For definition see Figure 1. Modified from
(28), with permission.
A, B
2
0
400
8
7
6
5
B
A
200
100
0
A, B
1
Pre
Late
Post
Pre
Late
Post
711

J.N. Roemmich, E.J. Richmond, and A.D. Rogol
linear growth is slowed during the sport season or
if there is catch-up growth during the off-season.
In a series of longitudinal studies, Roemmich et al.
(28, 30) have shown that the incremental growth in
stature and rate of skeletal maturation of wrestlers
is similar to that of controls during both the sport
season and post-season (Fig. 7). However, growth
of fat-free mass and other soft tissues are slowed
during the sport season followed by catch-up
growth in the post-season (Fig. 6) (28, 29, 36).
tively short lower limbs of female (36) and male (40)
gymnasts. Similar to wrestlers, the growth and mat-
uration of gymnasts may be explained by self-se-
lection, as gymnasts tend to be the children of short
parents who also had later than average puberty
(41) and shorter limb lengths are present at base-
line and do not worsen with training (36).
A
180
170
160
150
140
Female gymnasts
Gymnasts gain a competitive advantage if they are
able to develop muscular strength within a shorter
and lighter frame. The performance of female gym-
nasts often decreases after the onset of puberty due
to increases in height and fat mass and develop-
ment of the secondary sexual characteristics. Gym-
nasts, then, often utilize exercise and dieting to
maintain a lean physique in the hope of maximizing
their strength/ weight ratio, for esthetics, and to de-
lay puberty and growth. A controversial longitudi-
nal study found that female gymnasts training 18
h/week had a delayed age at menarche, slowed lin-
ear growth, and reduced growth potential (37).
Height standard deviation scores and predicted
adult height (Fig. 8) continued to decrease and the
gymnasts failed to have a pubertal growth spurt (Fig.
9). Leg length velocity slowed at puberty with al-
most no growth after a bone age of 12 years (Fig.
10). Growth reduction was speculated to be due to
a reduction in sex steroids and IGF-I production, but
that enough estrogens were released to fuse the
growth plates of the lower limbs. Although addi-
tional longitudinal studies have not yet replicated
these results, others have observed reduced serum
IGF-I concentrations in gymnasts (38, 39) and rela-
130
8
10
12
14
16
18
B 180
170
160
150
140
130
175
170
165
160
8
10
12
14
16
18
Bone age (yr)
Fig. 8 - Predicted and measured height plotted against bone
age in female gymnasts (A) and female swimmers (B). Target
height is represented by area within solid horizontal lines cen-
tered by dashed line. The gymnasts had a significant drop
(p<0.001) in height predictions. From (37), with permission.
Pre
Late
Post
Fig. 7 - Height for the wrestler (᭺, no.=9) and control (᭹, no.=7)
groups. Like letters are significantly different. Values expressed
as mean ( SE). For definitions see Figure 1.
712

Consequences of sport training during puberty
cause some athletes to temporarily change the per-
centile at which they track. Athletes who enter puberty
earlier than average will have an increased height per-
centile while those who enter puberty later than aver-
age will have a decrease in height percentile. The av-
erage height for participants in some sports may be
less than the 50th percentile, but this is probably due
to self-selection rather than sport training. For exam-
ple, boys and girls who participated in gymnastics as
children and became relatively tall may participate in
basketball or volleyball during adolescence because
greater height can be a disadvantage in gymnastics
but beneficial in other sports. Likewise, boys and girls
with genetically determined delayed puberty and/or
short stature would migrate towards gymnastics and
wrestling because they will be at a disadvantage in
some sports, but at a competitive (mechanical) ad-
vantage in gymnastics and wrestling. This situation is
especially prevalent in the lighter weight classes of
wrestling where boys with later maturity are recruited
by coaches to participate because the weight classes
often go unfilled or are filled by younger athletes be-
cause so few boys of the expected age are light
enough to compete. When wrestlers lose weight to
fill empty weight classes or to gain a competitive ad-
vantage or gymnasts try to delay puberty and growth
through dietary restriction, under-nutrition occurs.
Under-nutrition caused by wrestling training and di-
etary restriction appears to produce a disruption of
the pituitary-testicular axis and a partial GH resistance.
The effect of sport training and dietary restriction on
the neuroendocrine axes of gymnasts has not been
adequately studied. Wrestling training has little effect
12
10
8
f
+2 SD
6
-2 SD
*
*
4
*
2
4
6
8
10
12
14
16
18
Bone age (yr)
Fig. 9 - Height growth velocity in gymnasts (᭺) and swimmers (᭹).
Growth velocity was lower for the gymnasts at bone ages of 11,
12, and 13 years as indicated by the asterisks. The gray stippled
area represents the normal ( 2 SD) growth velocity as a function
of chronological age for normal French children. From (37), with
permission.
CONCLUSIONS
Training for most athletes is not detrimental to nor-
mal growth nor pubertal development. Normal linear
growth encompasses the 3rd to 97th percentile for
height and height velocity. If an athlete’s growth con-
tinues to track along the same percentile as before
initiating training, there is little cause for concern.
Individual differences in the timing of puberty may
90
85
80
75
70
65
A
90
85
80
75
70
65
B
Fig. 10 - Growth in sitting height (᭺) and
leg length (᭹) from bone age of 10 years
to bone age of 16 years. Gymnasts are
shown in panel A and swimmers in panel
B. Note the lack of increase in leg length
after bone age of 12 years in the gym-
nasts. From (37), with permission.
10 11 12 13 14 15 16
Bone age (yr)
10 11 12 13 14 15 16
Bone age (yr)
713

J.N. Roemmich, E.J. Richmond, and A.D. Rogol
9. Roemmich J.N., Clark P.A., Mai V., Berr S.S.,
Weltman A., Veldhuis J.D., Rogol A.D.
on linear bone growth or pubertal maturation. For
wrestlers, the 3- to-4 month period of under-nutrition
is followed by long periods of adequate nutrition such
that the period of under-nourishment may not be long
enough to slow growth or maturation or reduce the
final height of wrestlers. Female gymnasts who are
chronically training and limiting their dietary intake
may be at greater risk for limiting their growth.
Gymnastics training may slow growth of the lower
limbs but more data are needed to confirm this result.
The shorter limb lengths of gymnasts may be self-se-
lected as gymnasts have shorter limb lengths when
beginning training and the limb length discrepancy
does not increase with training. Longitudinal research
studies of athletes involved in wrestling, gymnastics,
and other weight control sports must include appro-
priate control groups and move beyond description-
al research to determine the independent and inter-
active effects of sport training, nutritional, and hor-
mones on their growth and maturation.
Alterations in growth and body composition dur-
ing puberty. III. Influence of maturation, gender,
body composition, body fat distribution, aerobic
fitness and total energy expenditure on nocturnal
growth hormone release during puberty.
J. Clin. Endocrinol. Metab. 1998, 83: 1440-1447.
10. Veldhuis J.D., Metzger D.L., Martha P.M., Mauras
N., Kerrigan J., Keenan B.
Estrogen and testosterone, but not a non-aroma-
tizable androgen, direct network integration of the
hypothalamo-somatotrope (growth hormone)-
insulin-like growth factor 1 axis in the human: ev-
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J. Clin. Endocrinol. Metab. 1997, 82: 3414-3420.
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Alterations in growth and body composition dur-
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(GH) secretion in male and female prepubertal
children and late adolescents: ultrasensitive
chemiluminescence-based assay of basal, pul-
satile, entropic, and rhythmic modes of GH re-
lease.
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