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Ann. N.Y. Acad. Sci. ISSN 0077-8923
ANNALS OF THE NEW YORK ACADEMY OF SCIENCES
Issue: Women’s Health and Disease
The influence of intensive physical training on growth
and pubertal development in athletes
Neoklis A. Georgopoulos,1
Nikolaos D. Roupas,1
Anastasia Theodoropoulou,2
Athanasios Tsekouras,2
Apostolos G. Vagenakis,2
and Kostas B. Markou2
1
Division of Reproductive Endocrinology, Department of Obstetrics and Gynecology, University of Patras Medical School,
University Hospital, Patras, Greece. 2
Division of Endocrinology, Department of Medicine, University of Patras Medical School,
University Hospital, Patras, Greece
Address for correspondence: Neoklis A. Georgopoulos, Division of Reproductive Endocrinology, Department of Obstetrics
and Gynecology, University of Patras Medical School, University Hospital, Rio-26500, Patras, Greece. neoklisg@hol.gr
Genetic potential for growth can be fully expressed only under favorable environmental conditions. Although
moderate physical activity has beneficial effects on growth, excessive physical training may negatively affect it. Sports
favoring restricted energy availability, in the presence of high energy expenditure, are of particular concern. In
gymnastics, a different pattern in skeletal maturation and linear growth was observed, resulting in an attenuation
of growth potential in artistic gymnasts (AG), more pronounced in males than in females. In female rhythmic
gymnasts (RG), the genetic predisposition to growth was preserved owing to a late catchup growth phenomenon.
In all other sports not requiring strict dietary restrictions, no deterioration of growth has been documented so
far. Intensive physical training and negative energy balance alter the hypothalamic pituitary set point at puberty,
prolong the prepubertal stage, and delay pubertal development and menarche in a variety of sports. In elite RG and
AG, prepubertal stage is prolonged and pubertal development is entirely shifted to a later age, following the bone
maturation rather than the chronological age.
Keywords: athletes; gymnasts; growth; pubertal development; skeletal maturation; bone acquisition
Introduction
Somatic growth and biological maturation are dy-
namic processes regulated by a variety of genetic and
environmental factors. Changes in body composi-
tion, in body proportions, in skeletal maturation,
and in pubertal development constitute indispens-
able components in the evaluation of the growth
process,complementingthetraditionalaspectofthe
assessment of stature as the main focus of growth
evaluation. Thus, growth and physical maturation
should be regarded as a complex, and dynamic pro-
cess, including a large variety of molecular and so-
matic changes.
Genetic predisposition to growth can be fully
expressed only under favorable environmental
conditions.1
Environmental factors can act inde-
pendently or in combination to modify the individ-
ual genetic potential. Athletic training when exerted
during childhood and adolescence has a huge im-
pact on physical growth and pubertal maturation.
There is strong evidence that regular physical ac-
tivity is important for good body function and de-
velopment. At the same time, there is a growing
concern regarding the influence of stress and inten-
sivephysicaltrainingongeneralhealth.Beginningat
an early age, athletes performing at a high compet-
itive level are exposed to high levels of physical and
psychological stress resulting from many hours of
intense training and competitions. The damaging
effects of these factors on somatic growth, skele-
tal, and pubertal maturation, have been described
in individuals performing a variety of sports. Indi-
vidual sports exert unique influences on biological
maturation, depending on the sport-related specific
character, technical skills and training methods and
the stage of growth and sexual maturation of the
individual athlete. Therefore, the whole picture is
doi: 10.1111/j.1749-6632.2010.05677.x
Ann. N.Y. Acad. Sci. 1205 (2010) 39–44 c 2010 New York Academy of Sciences. 39
Growth in athletes Georgopoulos et al.
extremely complex and should be approached with
extreme caution and responsibility.
Somatic growth in athletes
The major factor influencing linear growth is ge-
netic predisposition. Both adult final height and the
rate of growth are greatly influenced by genetic fac-
tors.2
Studies involving twins, revealed that the aver-
age difference in final height between monozygotic
twins was less than 3 cm, compared to 12 cm for
dizygotic twins.3
Final height is best correlated to
target height (midparental height) especially when
parents are not of disparate heights.4
Environment
and heredity continuously interact throughout the
entire period of growth. Children with similar ge-
netic potential are expected to reach comparable
final height under optimal environmental condi-
tions. On the other hand, children with the same
genetic background exposed to entirely different en-
vironmental conditions, can end up with a different
adult height. Furthermore, children of parents from
underdeveloped areas, born and raised in industri-
alized countries, present taller as adults, compared
to their target height. In industrialized countries, an
increase in height has been documented, attributed
to the improvement in socioeconomic conditions.1
Growth and maturation are complex processes
and genetic predisposition is achieved only when
favorable conditions exist during the entire period
of growth. Major environmental factors that may
alter somatic growth are intensive physical exercise
and stress. The impact of stress and intensive phys-
ical training on growth depends on the combined
effects of intensity, frequency, and duration of exer-
cise. Intensive athletic training of 18 hours per week
is capable of attenuating growth.5
Although moder-
ate physical activity has beneficial effects on growth,
as it is associated with cardiovascular benefits and
favorable changes in body composition, extensive
physical training may negatively affect growth, es-
pecially during puberty.6
The effect of intense phys-
ical training on growth and maturation depends
on a variety of factors, including the type of phys-
ical training, the age of training initiation, and the
intensity of training. Each sport requires a spe-
cific type of exercise and is characterized by unique
athletic demands that favor a particular optimal
somatotype.
The period of maximum training during the
growth process is of particular importance. For ex-
ample, in female gymnasts, the greatest physical ex-
ertion coincides with the period of pubertal devel-
opment, whereas in male gymnasts, the maximum
training is required toward the end of puberty. Over
the past few decades, the demands of high compe-
tition level have increased the intensity of training
within the same sport. For example, it is known that
gymnasts are trained much more intensely nowa-
days than previously, usually 26–32 hours per week
compared to 15 h during the seventies and 20 h
during the eighties.
Sports that require a strict control of energy in-
put in combination with a high energy output are of
particular concern. Thus, it is not reasonable to gen-
eralize when trying to evaluate the particular effects
of the activity of each sport on somatic growth. The
major sports that require intensive physical training
during childhood and adolescence are mainly gym-
nastics (both Rhythmic and Artistic), and to a lesser
extent swimming, rowing, wrestling, track and field
athletism, and tennis.
Rhythmic gymnasts (RG) and artistic gymnasts
(AG)aretwodistinctgroupswithinthefieldofgym-
nastics. They include different training methods,
athleticperformanceobjectives,andrequirespecial-
ized and distinct skills. Each sport is characterized
by specific athletic requirements that favor a partic-
ularoptimalsomatotype.Ashort-limbedindividual
would have a greater mechanical advantage in artis-
tic gymnastic performance, whereas a long-limbed
individual could benefit from a similar advantage in
rhythmic gymnastics. Indeed, performance scores
in elite female artistic gymnasts are negatively cor-
related with the degree of fatness or endomorphy
of the individual.7
Therefore, trainers (coaches) ex-
pectedly select individuals that best match certain
anthropometric criteria for each sport. The sport-
specific selection criteria for artistic gymnastics im-
ply that a short stature with relatively short limbs,
broad shoulders, and narrow hips is due to deter-
mined genetic predisposition, rather than a result
of the specific sport training and performance.8
Thus, genetic predisposition should always be con-
sidered when studying the impact of gymnastics on
growth.
Artistic gymnasts
Until recently, AG anthropometric measurements
andprospectivegrowthpredictionsappearedwithin
normal limits.9–12
In all these reports, the adult
40 Ann. N.Y. Acad. Sci. 1205 (2010) 39–44 c 2010 New York Academy of Sciences.
Georgopoulos et al. Growth in athletes
height of AG remained proportional for the re-
ported target height despite the method used to
estimate predicted adult height. Another prospec-
tive study documented a reduction of growth po-
tential and a decrease in mean height predictions
over time, in a smaller group of AG.13
However,
in another study by the same group evidence was
provided that the predicted adult height was not
reduced in AG, demonstrating the inherent inac-
curacy of height predictions.14
Although these data
provide useful information, no definite conclusions
should be made until adult height has been attained.
In a large cross-sectional study, we have shown
that female AG were shorter and lighter than aver-
age, with mean height and weight SD scores below
0 (the 50% percentile), following their respective
target height SD score, which was also below 0.15
However, the actually measured height was lower
than their target height. The major factors nega-
tively affecting height in AG were low weight, low
body fat, and intensity of training.
The majority of previously reported data referred
only to female AG. We, therefore, evaluated compar-
atively both male and female AG.16
At the time of ex-
amination, although both female and male AG were
shorter than their age-related population mean, fe-
male AG showed a greater height deviation from
their age-related population mean. Male AG pre-
senting with a height closer to their age-related pop-
ulation mean, had a genetic predisposition toward
a much higher final height than female AG. As a re-
sult, the difference between target height and actual
height SD score ( Target height − Actual height SD
score) was greater in males than in females. Consid-
eringthesedata,itisreasonabletoassumethatinAG
the growth process in males might be more suscep-
tible to the detrimental effects of intensive physical
training.
For both sexes, current measured height was cor-
related positively to target height, indicating that
genetic predisposition to growth, although altered,
was not disrupted. In the group of athletes—of both
sexes—that have reached their final adult height, fi-
nalheightfailedtomeettheirgeneticpredisposition,
providing additional evidence for growth attenua-
tion in AG.
Rhythmic gymnasts
In RG, female RG were taller and thinner than av-
erage for age, with height velocity SD score for each
age group above 0 (50% percentile) for all ages.17,18
Interestingly, although linear growth in normal girls
comes to an end by the year of 15, in RG growth con-
tinued up to the age of 18. Their final adult height
was identical to the estimated predicted height at
first evaluation, and higher than the genetically de-
termined target height, denoting that genetic po-
tentials to final height was not only achieved, but
even exceeded. Furthermore, target height was the
only independent parameter proved to positively
influence height velocity, therefore genetic predis-
position remained the main driving force for the
observed efficient catch-up growth. Comparing AG
with RG leads to the conclusion that their reported
target height SD score was similar to their own mea-
sured heights (above 0 for the RG and below 0 for
the AG), indicating once more the determining role
of genetic predisposition and preselection. RG fol-
lowed a growth pattern that was higher than their
reportedtargetheight,whereasAGexhibitedalower
growth pattern.
In conclusion, studies in gymnasts performing at
thehighestcompetitivelevel,documentedadeterio-
ration of growth potential in AG, more pronounced
in males than in females; whereas, in female RG,
the genetic predisposition to growth was not only
preserved, but even exceeded.
Other sports
In all other sports, no deterioration of growth has
been reported. In swimmers, probably due both to
preselection bias by trainers and to high energy in-
put, the currently measured height was well above
the population mean.19–21
Another longitudinal
study, found no impact of regular intensive physical
training on the final height of female swimmers and
tennis players.22
In young distance runners, mean
height for both males and females approximates the
reference medians and estimated height velocities
are, on average, similar to age and sex-specific pop-
ulation means.23
Girls training for approximately 12
hours per week in sports including rowing, track,
and swimming for an average of 4 years during
puberty, revealed no difference in height velocity
compared to the population means, although a ten-
dency towarda slightly laterpeakheightvelocity was
noted.24
Female swimmers training for 8 hours per
week presented, after a follow-up of 2–3 years, nor-
mal heights and normal height velocities compared
to their population means, whereas AG training
Ann. N.Y. Acad. Sci. 1205 (2010) 39–44 c 2010 New York Academy of Sciences. 41
Growth in athletes Georgopoulos et al.
for 22 hours per week showed significantly lower
growth velocities.13
Assessment of anthropometric
data of elite junior tennis players, revealed signifi-
cantly taller top ranked, compared to lower ranked,
female tennis players.25
No difference in growth has
been found between seasonal wrestlers and controls
as all changes in dietary intake, body composition,
and muscular strength were reversed during the
post seasonal period.26
Growth rate was assessed
as normal in a large cohort of school wrestlers, al-
though no information was provided whether or
not a lower growth rate was observed during the
sport season followed by a catch-up growth during
the nontraining season.27
Anthropometric charac-
teristics showed that male rowers were similar in
most aspects to a student control sample, whereas
data on a large sample of elite junior rowers showed
a tendency toward a taller height, more pronounced
among finalists compared to nonfinalists, indicating
the influence of preselection bias.28,29
Inconclusion,intensivephysicaltrainingandath-
letic performance at high level did not negatively af-
fect somatic growth in all sports not requiring strict
dietaryrestrictionsleadingtoenergyimbalance.The
attention should be drawn to elite AG of both sexes,
engaged in highly strenuous competitions.
Pubertal development in athletes
Growth specifically refers to increase in body size,
whereas maturation includes the progress leading to
the biologically mature state. Thus, growth cannot
be fully evaluated without determining the timing
and tempo of biological maturation. Puberty is a
dynamic period of development with rapid changes
in body size, shape, and composition. The onset of
puberty corresponds to a specific biological age, as
determined by skeletal maturation, and namely, a
bone age of 13 years for boys and 11 years for girls.30
Prolonged intensive physical training has great im-
pact on skeletal maturation, leading to a signifi-
cant delay in bone age compared to chronological
age. As in the general population, pubertal devel-
opment in highly trained athletes seems to follow
bone age rather than chronological age.31
However,
genetic predisposition and variation among indi-
viduals should always be considered. Specific sports
favor the early matures, whereas others, such as
gymnastics, offer advantage to the later develop-
ing individuals. Therefore, any assessment of sexual
maturation must take into account the biological
indicators of bone age and peak height velocity.
Delayed pubertal development and sexual mat-
uration has been observed in a variety of sports,
mainly gymnastics, dancing, and long-distance run-
ning.32
The documented delay is determined by the
type, the frequency, the intensity, and the duration
of exercise and is more pronounced in sports requir-
ing strict dietary restrictions that result in higher
energy expenditure in the presence of a deficient
energy input. In the case of gymnasts performing
in the high competitive level of the Olympic games,
delayedmenarchehasbeennoted, comparedtohigh
school, college, and club-level athletes.7
Young girls
or adolescents engaged in sports requiring training
less than 15 hours per week do not show menstrual
disturbances or delay in sexual maturation.33
In elite RG and AG, the prepubertal stage was
prolonged and pubertal development was shifted to
a later age, retaining a normal progression rate.15–18
Expectedly, the progression of puberty followed the
bone age rather than the chronological age.16,17
It
is to be underlined that for both RG and AG, pu-
bertal progression, although delayed, was not pro-
longed. Normal girls require an average of 1.96 ±
0.93 years (mean±SD) for their breast development
toprogressfromTannerstageIItoTannerstageIV.34
A comparable period of time was observed for both
RG and AG in our study. Therefore, pubertal matu-
ration was entirely shifted to a later age, maintaining
a normal rate of progression.
The major factor responsible for the delay in the
onset of breast and pubic hair development in both
sports was low body weight. Low body weight re-
flects an energy deficit, prominent in both sports, as
a result of intensive physical training (high energy
expenditure) on the one side and caloric under-
nutrition (low energy input) on the other. Gym-
nasts indeed are subject to a significant energy
drain, occurring early in prepubertal age, and are
highly motivated to achieve low body weight con-
sistent with their sports requirements for a thin
somatotype.
On the other hand, in ballet dancers under high-
energy drain and low-diet intake, a delayed the-
larche and a normal pubarche were noted.35
This
implies that independent central mechanisms are
involved in triggering these aspects of pubertal de-
velopment. Indeed, breast development and sub-
sequently menarche are related to estrogen levels,
42 Ann. N.Y. Acad. Sci. 1205 (2010) 39–44 c 2010 New York Academy of Sciences.
Georgopoulos et al. Growth in athletes
whereas pubarche is mainly related to adrenal an-
drogen production.36
In conditions of energy im-
balance and consequent reduction in adipose tissue
mass, estrogen production is decreased and breast
development and menarche are delayed. It is the on-
set,theduration,andtheextentofenergydeficitthat
determine the degree of involvement in all aspects of
pubertal development. Indeed, ballet dancers with
a normal pubarche start their training at the age of
8–9 years of age with only 3.5–7.3 hours per week,
whereas the RG and AG we examined started their
training at the age of 6.4–7.7 years of age with more
than 30 hours of training per week.35
Female athletes involved in a large variety of
sports, including runners, swimmers, tennis play-
ers, ballet dancers, and gymnasts, present a well-
documented delayed menarche.22,35,36–38
In RG,
menarche was significantly delayed compared to
their mothers and not trained sisters, an observa-
tion arguing against a genetic predisposition toward
delayed menarche.18
It is well known that a minimum weight, for,
height and a critical lean, to, fat mass ratio is re-
quired for menarche. According to Frisch theory,
the attainment of a critical percentage of body fat
lowers the metabolic rate and induces a sensitization
of the hypothalamus to gonadal steroids.39
Indeed,
leptin and estrogen production by the adipose tissue
play a central role in triggering menarche.40
These
adjustments reflect a natural adaptation of the body
to high energy demands. In AG and RG, low body
fat, low body weight (low energy input), and pro-
longed intensive physical training (high energy out-
put) were the major factors influencing menarche.
Low body weight, however, remained the most sig-
nificant factor in delaying the onset of puberty. It is
to be noted that in both RG and AG, older athletes
without menarche presented lower height, weight,
and BMI compared to their contemporaries with
menarche.
In conclusion, in RG and AG intensive physical
training and negative energy balance prolong the
prepubertal stage and delay pubertal development,
by regulating the hypothalamic pituitary set point
at puberty, without affecting the duration of the
pubertal process.
Conclusions
Genetic predisposition to growth can be fully ex-
pressed only under favorable environmental con-
ditions. Moderate physical exercise has beneficial
effects on growth as it is associated with cardiovas-
cularbenefitsandfavorablechangesinbodycompo-
sition. Conversely, extensive physical training may
attenuate growth, especially during puberty.
The effect of stress and intensive physical training
on growth and maturity is related to the combined
effects of age of exercise onset, exercise intensity,
exercise frequency, and exercise duration.
Sports that require a strict control of energy con-
sumption, combined with a high-energy expendi-
ture, are of particular concern. In gymnastics of the
highest competitive level, a delay in skeletal mat-
uration was observed, leading to a deterioration of
growth potential in AG, more pronounced for males
than for females, whereas in female RG the genetic
potential for growth was finally achieved by com-
pensation via a late catch-up growth phenomenon.
In all other sports not requiring strict dietary re-
strictions, no deterioration of growth has been
documented.
Intensive physical training and negative energy
balance, by modulating the hypothalamic pituitary
set point at the expected time of puberty, prolong
theprepubertalstageanddelaypubertalprogression
in a variety of sports.
In elite RG and AG, prepubertal stage was pro-
longed and pubertal development was entirely
shifted to a later age, following the bone age
rather than the chronological age and maintain-
ing a normal rate of progression. Female ath-
letespresentawell-documenteddelayedmenarcheal
age, compared to their mothers and nontrained
sisters.
Conflicts of interest
The authors declare no conflicts of interest.
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The influence of intensive physical training on growth and puberty in young athletes

  • 1. Ann. N.Y. Acad. Sci. ISSN 0077-8923 ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue: Women’s Health and Disease The influence of intensive physical training on growth and pubertal development in athletes Neoklis A. Georgopoulos,1 Nikolaos D. Roupas,1 Anastasia Theodoropoulou,2 Athanasios Tsekouras,2 Apostolos G. Vagenakis,2 and Kostas B. Markou2 1 Division of Reproductive Endocrinology, Department of Obstetrics and Gynecology, University of Patras Medical School, University Hospital, Patras, Greece. 2 Division of Endocrinology, Department of Medicine, University of Patras Medical School, University Hospital, Patras, Greece Address for correspondence: Neoklis A. Georgopoulos, Division of Reproductive Endocrinology, Department of Obstetrics and Gynecology, University of Patras Medical School, University Hospital, Rio-26500, Patras, Greece. neoklisg@hol.gr Genetic potential for growth can be fully expressed only under favorable environmental conditions. Although moderate physical activity has beneficial effects on growth, excessive physical training may negatively affect it. Sports favoring restricted energy availability, in the presence of high energy expenditure, are of particular concern. In gymnastics, a different pattern in skeletal maturation and linear growth was observed, resulting in an attenuation of growth potential in artistic gymnasts (AG), more pronounced in males than in females. In female rhythmic gymnasts (RG), the genetic predisposition to growth was preserved owing to a late catchup growth phenomenon. In all other sports not requiring strict dietary restrictions, no deterioration of growth has been documented so far. Intensive physical training and negative energy balance alter the hypothalamic pituitary set point at puberty, prolong the prepubertal stage, and delay pubertal development and menarche in a variety of sports. In elite RG and AG, prepubertal stage is prolonged and pubertal development is entirely shifted to a later age, following the bone maturation rather than the chronological age. Keywords: athletes; gymnasts; growth; pubertal development; skeletal maturation; bone acquisition Introduction Somatic growth and biological maturation are dy- namic processes regulated by a variety of genetic and environmental factors. Changes in body composi- tion, in body proportions, in skeletal maturation, and in pubertal development constitute indispens- able components in the evaluation of the growth process,complementingthetraditionalaspectofthe assessment of stature as the main focus of growth evaluation. Thus, growth and physical maturation should be regarded as a complex, and dynamic pro- cess, including a large variety of molecular and so- matic changes. Genetic predisposition to growth can be fully expressed only under favorable environmental conditions.1 Environmental factors can act inde- pendently or in combination to modify the individ- ual genetic potential. Athletic training when exerted during childhood and adolescence has a huge im- pact on physical growth and pubertal maturation. There is strong evidence that regular physical ac- tivity is important for good body function and de- velopment. At the same time, there is a growing concern regarding the influence of stress and inten- sivephysicaltrainingongeneralhealth.Beginningat an early age, athletes performing at a high compet- itive level are exposed to high levels of physical and psychological stress resulting from many hours of intense training and competitions. The damaging effects of these factors on somatic growth, skele- tal, and pubertal maturation, have been described in individuals performing a variety of sports. Indi- vidual sports exert unique influences on biological maturation, depending on the sport-related specific character, technical skills and training methods and the stage of growth and sexual maturation of the individual athlete. Therefore, the whole picture is doi: 10.1111/j.1749-6632.2010.05677.x Ann. N.Y. Acad. Sci. 1205 (2010) 39–44 c 2010 New York Academy of Sciences. 39
  • 2. Growth in athletes Georgopoulos et al. extremely complex and should be approached with extreme caution and responsibility. Somatic growth in athletes The major factor influencing linear growth is ge- netic predisposition. Both adult final height and the rate of growth are greatly influenced by genetic fac- tors.2 Studies involving twins, revealed that the aver- age difference in final height between monozygotic twins was less than 3 cm, compared to 12 cm for dizygotic twins.3 Final height is best correlated to target height (midparental height) especially when parents are not of disparate heights.4 Environment and heredity continuously interact throughout the entire period of growth. Children with similar ge- netic potential are expected to reach comparable final height under optimal environmental condi- tions. On the other hand, children with the same genetic background exposed to entirely different en- vironmental conditions, can end up with a different adult height. Furthermore, children of parents from underdeveloped areas, born and raised in industri- alized countries, present taller as adults, compared to their target height. In industrialized countries, an increase in height has been documented, attributed to the improvement in socioeconomic conditions.1 Growth and maturation are complex processes and genetic predisposition is achieved only when favorable conditions exist during the entire period of growth. Major environmental factors that may alter somatic growth are intensive physical exercise and stress. The impact of stress and intensive phys- ical training on growth depends on the combined effects of intensity, frequency, and duration of exer- cise. Intensive athletic training of 18 hours per week is capable of attenuating growth.5 Although moder- ate physical activity has beneficial effects on growth, as it is associated with cardiovascular benefits and favorable changes in body composition, extensive physical training may negatively affect growth, es- pecially during puberty.6 The effect of intense phys- ical training on growth and maturation depends on a variety of factors, including the type of phys- ical training, the age of training initiation, and the intensity of training. Each sport requires a spe- cific type of exercise and is characterized by unique athletic demands that favor a particular optimal somatotype. The period of maximum training during the growth process is of particular importance. For ex- ample, in female gymnasts, the greatest physical ex- ertion coincides with the period of pubertal devel- opment, whereas in male gymnasts, the maximum training is required toward the end of puberty. Over the past few decades, the demands of high compe- tition level have increased the intensity of training within the same sport. For example, it is known that gymnasts are trained much more intensely nowa- days than previously, usually 26–32 hours per week compared to 15 h during the seventies and 20 h during the eighties. Sports that require a strict control of energy in- put in combination with a high energy output are of particular concern. Thus, it is not reasonable to gen- eralize when trying to evaluate the particular effects of the activity of each sport on somatic growth. The major sports that require intensive physical training during childhood and adolescence are mainly gym- nastics (both Rhythmic and Artistic), and to a lesser extent swimming, rowing, wrestling, track and field athletism, and tennis. Rhythmic gymnasts (RG) and artistic gymnasts (AG)aretwodistinctgroupswithinthefieldofgym- nastics. They include different training methods, athleticperformanceobjectives,andrequirespecial- ized and distinct skills. Each sport is characterized by specific athletic requirements that favor a partic- ularoptimalsomatotype.Ashort-limbedindividual would have a greater mechanical advantage in artis- tic gymnastic performance, whereas a long-limbed individual could benefit from a similar advantage in rhythmic gymnastics. Indeed, performance scores in elite female artistic gymnasts are negatively cor- related with the degree of fatness or endomorphy of the individual.7 Therefore, trainers (coaches) ex- pectedly select individuals that best match certain anthropometric criteria for each sport. The sport- specific selection criteria for artistic gymnastics im- ply that a short stature with relatively short limbs, broad shoulders, and narrow hips is due to deter- mined genetic predisposition, rather than a result of the specific sport training and performance.8 Thus, genetic predisposition should always be con- sidered when studying the impact of gymnastics on growth. Artistic gymnasts Until recently, AG anthropometric measurements andprospectivegrowthpredictionsappearedwithin normal limits.9–12 In all these reports, the adult 40 Ann. N.Y. Acad. Sci. 1205 (2010) 39–44 c 2010 New York Academy of Sciences.
  • 3. Georgopoulos et al. Growth in athletes height of AG remained proportional for the re- ported target height despite the method used to estimate predicted adult height. Another prospec- tive study documented a reduction of growth po- tential and a decrease in mean height predictions over time, in a smaller group of AG.13 However, in another study by the same group evidence was provided that the predicted adult height was not reduced in AG, demonstrating the inherent inac- curacy of height predictions.14 Although these data provide useful information, no definite conclusions should be made until adult height has been attained. In a large cross-sectional study, we have shown that female AG were shorter and lighter than aver- age, with mean height and weight SD scores below 0 (the 50% percentile), following their respective target height SD score, which was also below 0.15 However, the actually measured height was lower than their target height. The major factors nega- tively affecting height in AG were low weight, low body fat, and intensity of training. The majority of previously reported data referred only to female AG. We, therefore, evaluated compar- atively both male and female AG.16 At the time of ex- amination, although both female and male AG were shorter than their age-related population mean, fe- male AG showed a greater height deviation from their age-related population mean. Male AG pre- senting with a height closer to their age-related pop- ulation mean, had a genetic predisposition toward a much higher final height than female AG. As a re- sult, the difference between target height and actual height SD score ( Target height − Actual height SD score) was greater in males than in females. Consid- eringthesedata,itisreasonabletoassumethatinAG the growth process in males might be more suscep- tible to the detrimental effects of intensive physical training. For both sexes, current measured height was cor- related positively to target height, indicating that genetic predisposition to growth, although altered, was not disrupted. In the group of athletes—of both sexes—that have reached their final adult height, fi- nalheightfailedtomeettheirgeneticpredisposition, providing additional evidence for growth attenua- tion in AG. Rhythmic gymnasts In RG, female RG were taller and thinner than av- erage for age, with height velocity SD score for each age group above 0 (50% percentile) for all ages.17,18 Interestingly, although linear growth in normal girls comes to an end by the year of 15, in RG growth con- tinued up to the age of 18. Their final adult height was identical to the estimated predicted height at first evaluation, and higher than the genetically de- termined target height, denoting that genetic po- tentials to final height was not only achieved, but even exceeded. Furthermore, target height was the only independent parameter proved to positively influence height velocity, therefore genetic predis- position remained the main driving force for the observed efficient catch-up growth. Comparing AG with RG leads to the conclusion that their reported target height SD score was similar to their own mea- sured heights (above 0 for the RG and below 0 for the AG), indicating once more the determining role of genetic predisposition and preselection. RG fol- lowed a growth pattern that was higher than their reportedtargetheight,whereasAGexhibitedalower growth pattern. In conclusion, studies in gymnasts performing at thehighestcompetitivelevel,documentedadeterio- ration of growth potential in AG, more pronounced in males than in females; whereas, in female RG, the genetic predisposition to growth was not only preserved, but even exceeded. Other sports In all other sports, no deterioration of growth has been reported. In swimmers, probably due both to preselection bias by trainers and to high energy in- put, the currently measured height was well above the population mean.19–21 Another longitudinal study, found no impact of regular intensive physical training on the final height of female swimmers and tennis players.22 In young distance runners, mean height for both males and females approximates the reference medians and estimated height velocities are, on average, similar to age and sex-specific pop- ulation means.23 Girls training for approximately 12 hours per week in sports including rowing, track, and swimming for an average of 4 years during puberty, revealed no difference in height velocity compared to the population means, although a ten- dency towarda slightly laterpeakheightvelocity was noted.24 Female swimmers training for 8 hours per week presented, after a follow-up of 2–3 years, nor- mal heights and normal height velocities compared to their population means, whereas AG training Ann. N.Y. Acad. Sci. 1205 (2010) 39–44 c 2010 New York Academy of Sciences. 41
  • 4. Growth in athletes Georgopoulos et al. for 22 hours per week showed significantly lower growth velocities.13 Assessment of anthropometric data of elite junior tennis players, revealed signifi- cantly taller top ranked, compared to lower ranked, female tennis players.25 No difference in growth has been found between seasonal wrestlers and controls as all changes in dietary intake, body composition, and muscular strength were reversed during the post seasonal period.26 Growth rate was assessed as normal in a large cohort of school wrestlers, al- though no information was provided whether or not a lower growth rate was observed during the sport season followed by a catch-up growth during the nontraining season.27 Anthropometric charac- teristics showed that male rowers were similar in most aspects to a student control sample, whereas data on a large sample of elite junior rowers showed a tendency toward a taller height, more pronounced among finalists compared to nonfinalists, indicating the influence of preselection bias.28,29 Inconclusion,intensivephysicaltrainingandath- letic performance at high level did not negatively af- fect somatic growth in all sports not requiring strict dietaryrestrictionsleadingtoenergyimbalance.The attention should be drawn to elite AG of both sexes, engaged in highly strenuous competitions. Pubertal development in athletes Growth specifically refers to increase in body size, whereas maturation includes the progress leading to the biologically mature state. Thus, growth cannot be fully evaluated without determining the timing and tempo of biological maturation. Puberty is a dynamic period of development with rapid changes in body size, shape, and composition. The onset of puberty corresponds to a specific biological age, as determined by skeletal maturation, and namely, a bone age of 13 years for boys and 11 years for girls.30 Prolonged intensive physical training has great im- pact on skeletal maturation, leading to a signifi- cant delay in bone age compared to chronological age. As in the general population, pubertal devel- opment in highly trained athletes seems to follow bone age rather than chronological age.31 However, genetic predisposition and variation among indi- viduals should always be considered. Specific sports favor the early matures, whereas others, such as gymnastics, offer advantage to the later develop- ing individuals. Therefore, any assessment of sexual maturation must take into account the biological indicators of bone age and peak height velocity. Delayed pubertal development and sexual mat- uration has been observed in a variety of sports, mainly gymnastics, dancing, and long-distance run- ning.32 The documented delay is determined by the type, the frequency, the intensity, and the duration of exercise and is more pronounced in sports requir- ing strict dietary restrictions that result in higher energy expenditure in the presence of a deficient energy input. In the case of gymnasts performing in the high competitive level of the Olympic games, delayedmenarchehasbeennoted, comparedtohigh school, college, and club-level athletes.7 Young girls or adolescents engaged in sports requiring training less than 15 hours per week do not show menstrual disturbances or delay in sexual maturation.33 In elite RG and AG, the prepubertal stage was prolonged and pubertal development was shifted to a later age, retaining a normal progression rate.15–18 Expectedly, the progression of puberty followed the bone age rather than the chronological age.16,17 It is to be underlined that for both RG and AG, pu- bertal progression, although delayed, was not pro- longed. Normal girls require an average of 1.96 ± 0.93 years (mean±SD) for their breast development toprogressfromTannerstageIItoTannerstageIV.34 A comparable period of time was observed for both RG and AG in our study. Therefore, pubertal matu- ration was entirely shifted to a later age, maintaining a normal rate of progression. The major factor responsible for the delay in the onset of breast and pubic hair development in both sports was low body weight. Low body weight re- flects an energy deficit, prominent in both sports, as a result of intensive physical training (high energy expenditure) on the one side and caloric under- nutrition (low energy input) on the other. Gym- nasts indeed are subject to a significant energy drain, occurring early in prepubertal age, and are highly motivated to achieve low body weight con- sistent with their sports requirements for a thin somatotype. On the other hand, in ballet dancers under high- energy drain and low-diet intake, a delayed the- larche and a normal pubarche were noted.35 This implies that independent central mechanisms are involved in triggering these aspects of pubertal de- velopment. Indeed, breast development and sub- sequently menarche are related to estrogen levels, 42 Ann. N.Y. Acad. Sci. 1205 (2010) 39–44 c 2010 New York Academy of Sciences.
  • 5. Georgopoulos et al. Growth in athletes whereas pubarche is mainly related to adrenal an- drogen production.36 In conditions of energy im- balance and consequent reduction in adipose tissue mass, estrogen production is decreased and breast development and menarche are delayed. It is the on- set,theduration,andtheextentofenergydeficitthat determine the degree of involvement in all aspects of pubertal development. Indeed, ballet dancers with a normal pubarche start their training at the age of 8–9 years of age with only 3.5–7.3 hours per week, whereas the RG and AG we examined started their training at the age of 6.4–7.7 years of age with more than 30 hours of training per week.35 Female athletes involved in a large variety of sports, including runners, swimmers, tennis play- ers, ballet dancers, and gymnasts, present a well- documented delayed menarche.22,35,36–38 In RG, menarche was significantly delayed compared to their mothers and not trained sisters, an observa- tion arguing against a genetic predisposition toward delayed menarche.18 It is well known that a minimum weight, for, height and a critical lean, to, fat mass ratio is re- quired for menarche. According to Frisch theory, the attainment of a critical percentage of body fat lowers the metabolic rate and induces a sensitization of the hypothalamus to gonadal steroids.39 Indeed, leptin and estrogen production by the adipose tissue play a central role in triggering menarche.40 These adjustments reflect a natural adaptation of the body to high energy demands. In AG and RG, low body fat, low body weight (low energy input), and pro- longed intensive physical training (high energy out- put) were the major factors influencing menarche. Low body weight, however, remained the most sig- nificant factor in delaying the onset of puberty. It is to be noted that in both RG and AG, older athletes without menarche presented lower height, weight, and BMI compared to their contemporaries with menarche. In conclusion, in RG and AG intensive physical training and negative energy balance prolong the prepubertal stage and delay pubertal development, by regulating the hypothalamic pituitary set point at puberty, without affecting the duration of the pubertal process. Conclusions Genetic predisposition to growth can be fully ex- pressed only under favorable environmental con- ditions. Moderate physical exercise has beneficial effects on growth as it is associated with cardiovas- cularbenefitsandfavorablechangesinbodycompo- sition. Conversely, extensive physical training may attenuate growth, especially during puberty. The effect of stress and intensive physical training on growth and maturity is related to the combined effects of age of exercise onset, exercise intensity, exercise frequency, and exercise duration. Sports that require a strict control of energy con- sumption, combined with a high-energy expendi- ture, are of particular concern. In gymnastics of the highest competitive level, a delay in skeletal mat- uration was observed, leading to a deterioration of growth potential in AG, more pronounced for males than for females, whereas in female RG the genetic potential for growth was finally achieved by com- pensation via a late catch-up growth phenomenon. In all other sports not requiring strict dietary re- strictions, no deterioration of growth has been documented. Intensive physical training and negative energy balance, by modulating the hypothalamic pituitary set point at the expected time of puberty, prolong theprepubertalstageanddelaypubertalprogression in a variety of sports. In elite RG and AG, prepubertal stage was pro- longed and pubertal development was entirely shifted to a later age, following the bone age rather than the chronological age and maintain- ing a normal rate of progression. Female ath- letespresentawell-documenteddelayedmenarcheal age, compared to their mothers and nontrained sisters. Conflicts of interest The authors declare no conflicts of interest. References 1. Tanner,J.M.1989.FetusintoMan:PhysicalGrowthfromCon- ception to Maturity. Harvard University Press. Cambridge, MA. 2. Sinclair, D. 1978. Human Growth After Birth. Oxford Uni- versity Press. London, pp. 140–159. 3. Rogol, A.D., J.N. Roemmich & P.A. Clark. 2002. Growth at puberty. J. Adol. Health 31: 192–200. 4. Smith, D.W. 1977. Growth and its Disorders. WB Saunders Co. Philadelphia. 5. Tanner, J.M. ed. 1962. Growth at Adolescence, 2nd Ed. Black- well. Oxford. 6. Tanner,J.M.1986.Growthasatarget-seekingfunction:catch up and catch down growth in man. In: Human Growth. F. Ann. N.Y. Acad. Sci. 1205 (2010) 39–44 c 2010 New York Academy of Sciences. 43
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