Abstract
The genetic potentials for growth can be fully expressed only under favourable environmental condi- tions. Excessive physical training may negatively affect growth, especially during puberty. Sports that require a strict control of energy input in the presence of a high energy output are of particular concern. In gymnastics, a different pattern in skeletal maturation was observed, leading to an atten- uation of growth potential ins Artistic Gymnasts (AG), more pronounced in males than in females, whereas in female Rhythmic Gymnasts (RG) the genetic predisposition to growth was preserved because of a late catch-up growth phenomenon. In all other sports not requiring strict dietary restric- tions, no deterioration of growth has been documented. Intensive physical training and negative energy balance modify 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 the prepu- bertal stage is prolonged and pubertal development is entirely shifted to a later age, paralleling the bone age rather than the chronological age. Bone formation, and, consequently, BMD are enhanced by physical activity. In athletes, high-impact loading activities have been shown to improve BMD, while in sports requiring a lean somatotype, the delay in skeletal maturation and pubertal develop- ment, resulting from hypoestrogenemia, predisposes athletes to osteopenia. In AG, an increase in bone density is observed using the bone age as denominator. Key words: Athletes, Gymnasts, Growth, Pubertal development, Skeletal maturation, Bone acquisition. Address correspondence and requests for reprints to: Apostolos G. Vagenakis: Dept. of Internal Medicine, Div. of Endocrinology, University of Patras Medical School, University Hospital, Rio-26500, Greece, Tel: 2610-999582, Fax: 2610-993982, e-mail: vag.inmd@med.upatras.gr Received 27-08-04, Revised 20-09-04, Accepted 25-09-04 INTRODUCTION Growth and physical maturation are dynamic
bone age as denominator. Key words: Athletes, Gymnasts, Growth, Pubertal development, Skeletal maturation, Bone acquisition. Address correspondence and requests for reprints to: Apostolos G. Vagenakis: Dept. of Internal Medicine, Div. of Endocrinology, University of Patras Medical School, University Hospital, Rio-26500, Greece, Tel: 2610-999582, Fax: 2610-993982, e-mail: vag.inmd@med.upatras.gr Received 27-08-04, Revised 20-09-04, Accepted 25-09-04 INTRODUCTION Growth and physical maturation are dynamic pro- cesses influenced by a variety of genetic and environ- mental factors. Although traditionally the main focus of growth evaluation has been placed on the assess- ment of stature, changes in body composition, in body proportions, in skeletal maturation and in pubertal development also constitute essential components in the evaluation of the growth process. Therefore, growth and physical maturation should be viewed as a com- plex and dynamic process that includes a broad spec- trum of cellular and somatic changes.
234 N.A. GEORGOPOULOS, ET AL Growth is a complex process and gene expression is maximally achieved only when favourable conditions operate throughout the entire period of growth. Among the environmental factors that can alter lin- ear growth are physical exercise and stress. The effect of stress and intensive physical training on growth is related to the combined effects of intensity, frequen- cy, and duration of prolonged exercise. Intensive ath- letic training of 18 hours per week is capable of atten- uating growth 5 . Moderate physical activity has bene- ficial effects on growth, as it is associated with cardio- vascular benefits and favourable changes in body com- position. Extensive physical training, however, may negatively affect growth, especially during puberty 6 . The impact of intense physical training on growth de- pends 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 specific type of exercising and is characterized by specific athletic requirements that favour a particular optimal soma- totype. The time of maximum training during the growth process is particularly important. For example, in fe- male gymnasts, the maximum intensity of training coincides with the period of pubertal development while in males, the greatest physical exertion is re- quired towards the end of puberty. The intensity of training, within the same sport, has substantially in- creased over the past few decades due to the demands for higher records. For example, it is known that gym- nasts are trained much more intensely nowadays than previously, usually 26-28 hours per week compared to 15 h during the seventies and 20 h during the eighties. Sports that require a strict control of energy input in combination with a high energy output are of par- ticular concern. Therefore, it is not reasonable to gen- eralize when seeking to identify the particular impact of each sports activity on linear growth. The athletes that require intensive physical training during child- hood and adolescence are mainly gymnasts (both Rhythmic and Artistic) and, to a lesser extent, wres- tlers, rowers, track athletes,
a high energy output are of par- ticular concern. Therefore, it is not reasonable to gen- eralize when seeking to identify the particular impact of each sports activity on linear growth. The athletes that require intensive physical training during child- hood and adolescence are mainly gymnasts (both Rhythmic and Artistic) and, to a lesser extent, wres- tlers, rowers, track athletes, tennis players, and swim- mers. Rhythmic Gymnastics (RG) and Artistic Gymna- stics (AG) are two distinct sports within the field of gymnastics. Their programme includes specific gym- nastics and requires specialized and distinct skills. Each sport is characterized by specific athletic requirements Genetic predisposition to growth can be fully ex- pressed only under favourable environmental condi- tions 1 . Environmental factors can act independently or in combination to modify an individuals genetic potentials. Athletic training and performance when exerted during childhood and adolescence have a tre- mendous impact on growth and maturation. There is strong evidence that moderate exercise is an important health habit. At the same time, there is a general concern regarding the influence of stress and intensive physical training on general health. Begin- ning at a young age, athletes performing at a high agonistic level are exposed to high levels of physical and psychological stress from the many hours of in- tense training and competitions. The detrimental ef- fects of these factors on growth, skeletal maturation, and pubertal development have been documented in individuals involved in a variety of sports. Individual sports exert unique influences on biological matura- tion that are related to the heterogeneity of the sport- specific demands of training and the stage of growth and sexual maturation of the individual athlete. There- fore the whole picture is a complex one and should be approached with extreme caution. SOMATIC GROWTH IN ATHLETES The major determinant of linear growth is genetic predisposition. Both adult final height and the rate of growth are significantly influenced by genetic factors 2 . Studies in twins revealed that the average difference in final height between monozygotic twins was less than 3 cm, compared to 12 cm for dizygotic twins 3
with extreme caution. SOMATIC GROWTH IN ATHLETES The major determinant of linear growth is genetic predisposition. Both adult final height and the rate of growth are significantly influenced by genetic factors 2 . Studies in twins revealed that the average 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 with target height (mid- parental height), especially when parents are not of disparate heights 4 . Heredity and environment contin- uously interact throughout the entire period of growth. Children with similar genetic predisposition should reach comparable final height under optimal environ- mental conditions. By contrast, children with the same genetic background when exposed to entirely differ- ent environmental conditions, can reach a different adult height. Children of parents from underdevel- oped areas, born and bred in industrialized countries, present higher adult height than their target height. In industrialized countries, an increase in height has been observed which has been attributed to the im- provement of the socio-economic conditions 1 .
235Growth and maturation in athletes mean height and weight SD scores below 0 (Table 1), in harmony with their respective target height SD score, which was also below 0 15 . However, the actually measured height was lower than the Target height (Table 1). Among factors that negatively affected height in AG were low weight, low body fat, and in- tensity of training. Most previously reported data referred only to fe- male AG. We, therefore, evaluated comparatively both male and female AG 16 . At the time of examina- tion, both female and male AG were shorter than their age-related population mean and they both present- ed with a considerable delay in skeletal maturation. However, female AG showed a greater height devia- tion from their age-related population mean, with a greater delay in their skeletal maturation. Male AG, however, who presented with a height closer to their age-related population mean, had a genetic predis- position towards a much higher final height than fe- male AG (Table 2). Therefore, the difference between target height and actual height SD score (D Target height actual Height SD score) was greater in males than in females. It is thus reasonable to assume that, in male and female artistic gymnasts, the growth pro- cess in males might be more vulnerable to the detri- mental effects of intensive physical training. For both sexes, the measured current height was correlated to target height, a finding indicating that genetic predisposition to growth, although altered, was not disrupted. In a smaller subgroup of athletes, in whom final adult height was available for both sexes, final height fell short of genetic predisposition, pro- viding additional evidence for growth deterioration in AG. RG ATHLETES In Rhythmic Gymnastics, female RG were taller that favour a particular optimal somatotype. A short- limbed individual would have a greater mechanical advantage in artistic gymnastic performance, while a long-limbed individual could benefit from a similar advantage in rhythmic gymnastics. Indeed, perfor- mance scores in elite female artistic gymnasts are neg- atively correlated with the degree of fatness or endo- morphy of the individual 7 .
taller that favour a particular optimal somatotype. A short- limbed individual would have a greater mechanical advantage in artistic gymnastic performance, while a long-limbed individual could benefit from a similar advantage in rhythmic gymnastics. Indeed, perfor- mance scores in elite female artistic gymnasts are neg- atively correlated with the degree of fatness or endo- morphy of the individual 7 . It is reasonable, therefore, for trainers (coaches) to select those individuals who best match the appropriate anthropometric criteria for each sport. The sport-specific selection criteria for artistic gymnastics suggests that a short stature with relatively short limbs, broad shoulders, and narrow hips is derived from genetic predisposition rather than a result of the specific sport activity 8 . Therefore, ge- netic predisposition should always be taken into ac- count when studying the impact of gymnastics on growth. AG ATHLETES In AG, earlier anthropometric measurements and prospective growth predictions appeared within nor- mal limits 9-12 . In all these reports the adult height of AG remained proportional to the reported target height regardless of the method used to estimate pre- dicted adult height. In another prospective study 13 , ev- idence for a reduction of growth potential and a de- crease in mean height predictions over time was pro- vided in a smaller group of AG. However, in another study by the same group 14 , it was reported that the predicted adult height was not reduced in AG, which demonstrates the inherent inaccuracy of height pre- dictions. Although these data are highly informative, no definite conclusions should be drawn unless adult height has been attained. In a large cross-sectional study, we have shown that female AG were shorter and lighter than average, with Table 1. Derived height and weight data (Mean± SD) of examined Rhythmic and Artistic Gymnasts 16 . Variable Rhythmic Artistic Mean ± SD n Mean ± SD n Height SD score +0.70 ± 0.8 129 -1.27 ± 1.1 142 Reported Target height (cm) 165.0 ± 4.7 121 161.1 ± 4.7 124 Target height SD score +0.48 ± 0.8 121 -0.18 ± 0.8 125 Ä Height-Target height SD
(Mean± SD) of examined Rhythmic and Artistic Gymnasts 16 . Variable Rhythmic Artistic Mean ± SD n Mean ± SD n Height SD score +0.70 ± 0.8 129 -1.27 ± 1.1 142 Reported Target height (cm) 165.0 ± 4.7 121 161.1 ± 4.7 124 Target height SD score +0.48 ± 0.8 121 -0.18 ± 0.8 125 Ä Height-Target height SD score +0.10 ± 0.9 121 -0.89 ± 1.9 125 Weight SD score -0.95 ± 0.6 129 -0.92 ± 0.7 142
236 N.A. GEORGOPOULOS, ET AL Table 2. Collected somatometric data (Mean± SD) of male and female Artistic Gymnasts 16 . Age Bone age Ä CA-BA Height SDS Weight SDS (years) (years) Female 15.7 ± 2.0 13.4 ± 1.8 2.26 ± 2.2 -1.52 ± 1.1 -1.09 ± 0.7 n=169 n=138 n=138 n=168 n=168 Male 16.9 ± 2 16.2 ± 1.6 0.76 ± 1.2 -0.97 ± 1.0 -0.13 ± 0.7 n=93 n=83 n=83 n=93 n=93 p p <0.001 p <0.001 p <0.001 p <0.001 p <0.001 t=-5,03 t=-11,99 t=5,78 t=-3,53 t=-11,06 Target Predicted PH-TH BMI Body fat Height SDS Height SDS SDS (kg/m 2 ) (%) Female -0.18 ± 0.7 -0.70 ± 0.9 -0.6 ± 0.9 19.0 ± 1.7 19.5 ± 4.2 n=123 n=136 n=105 n=168 n=160 Male +1.91 ± 0.7 -0.35 ± 0.8 -2.3 ± 0.8 21.5 ± 1.7 10.6 ± 5.0 n=83 n=82 n=77 n=93 n=91 p p <0.001 p=0.007 p <0.001 p <0.001 p <0.001 t=-18,9 t=-2,7 t=13,03 t=-11,5 t=14,95 CA; Chronological age, BA; Bone age, PH; Predicted height, TH; Target height. and thinner than average for age (Table 1) 17,18 , with height velocity SD score for each age group above 0 at all ages 18 . Interestingly, although growth in normal girls comes to an end by the year of 15, in RG growth continued up to the age of 18 (Figure 1). The RG presented a significant delay in skeletal maturation of 1.8 years, which was compensated towards the end of puberty. Their final adult height was identical to the estimated predicted height at first evaluation, and higher than the genetically determined target height, denoting that genetic potentials for final height was not only achieved but even exceeded. Moreover, tar- get height was the only independent parameter which has been proved to positively influence height veloci- ty, therefore genetic predisposition remained the main driving force for the observed efficient catch-up growth. Comparison of AG with RG revealed that their reported target height SD score was similar to their own measured heights (above 0 for the RG and below 0 for the AG), indicating once more the
parameter which has been proved to positively influence height veloci- ty, therefore genetic predisposition remained the main driving force for the observed efficient catch-up growth. Comparison of AG with RG revealed that their reported target height SD score was similar to their own measured heights (above 0 for the RG and below 0 for the AG), indicating once more the influ- ence of genetic predisposition and preselection (Ta- ble 1). RG followed a growth pattern that was higher than their reported target height, while AG exhibited a lower growth pattern. The delay in skeletal maturation both in AG and RG is probably multifactorial. Low serum concentra- tions of sex steroids due to a delay in pubertal devel- opment, lower GH secretion or a disturbance in insu- Figure 1. Height velocity mean values per chronological age in Rhythmic Gymnasts. Lines represent the 3 rd , 10 th , 25 th , 50 th , 75 th , 90 th and 97 th centiles of height velocity. The dark line represents the height velocity of our examined gymnasts. The dark gray area includes the velocity curves of all children who have their peak velocities up to two standard deviations of age before and after this average age. The arrows and diamonds mark the 3 rd , 50 th , and 97 th centiles of peak velocity when the peak takes place at these early and late limits 18 . lin-like growth factor homeostasis 19 are capable of al- tering the hormonal control of growth. Intensive phys- ical training, chronic psychological stress, and modifi- cations in nutrition resulting in inadequate energy intake relative to energy output 20,21 are well known fac- tors. Nevertheless, overuse lesions of growth plates,
237Growth and maturation in athletes especially in the lower limbs, could add an additional end-organ effect 22 . In conclusion, studies in gymnastics of the highest competitive level have revealed, a deteriorating of growth potential in AG that is more pronounced in males than in females, while in female RG the genet- ic predisposition to growth was promoted. 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 input, the measured height was well above the population mean 23-25 . In young distance runners, mean height for both males and females approximate the reference medians and estimated height velocities were, on av- erage, similar to age and sex-specific population means 26 . Girls training for approximately 12 hours per week in sports including rowing, track, and swimming for an average of 4 years during puberty presented no difference in height velocity from their population means, although a tendency towards a slightly later peak height velocity was noted 27 . Female swimmers training for 8 hours/week presented at a follow-up of 2-3 years normal heights and normal height velocities compared to their population means, while AG train- ing for 22 hours/week showed significantly lower growth velocities 13 . No difference in growth has been found between seasonal wrestlers and controls as all changes in dietary intake, body composition, and mus- cular strength were reversed during the post-seasonal period 28 . Growth rate was assessed as normal in a large cohort of school wrestlers, although no information was provided as to whether or not a lower growth rate was observed during the sport season followed by a catch-up growth during the nontraining season 29 . An- thropometric characteristics showed the male rowers to be similar in most respects to a student control sam- ple 30 , while data on a large sample of elite junior row- ers showed a tendency towards a taller height, more pronounced among finalists, compared to non-fina- lists indicating the influence of preselection bias 31 . In conclusion, intensive physical training
An- thropometric characteristics showed the male rowers to be similar in most respects to a student control sam- ple 30 , while data on a large sample of elite junior row- ers showed a tendency towards a taller height, more pronounced among finalists, compared to non-fina- lists indicating the influence of preselection bias 31 . In conclusion, intensive physical training did not negatively affect somatic growth in sports not requir- ing strict dietary restrictions which lead to energy im- balance. Caution should be exercised in the case of elite Artistic Gymnasts of both sexes engaged in highly strenuous competitions. PUBERTAL DEVELOPMENT IN ATHLETES Growth specifically refers to increase in body size, whereas maturation refers to the progress towards the biologically mature state. Therefore, growth cannot be fully assessed 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 corre- sponds to a specific biological age, as determined by skeletal maturation, namely, a bone age of 13 years for boys and 11 years for girls 32 . Intensive physical training has profound effects on skeletal maturation leading to a significant delay in bone age compared to chronological age. As in the general population, pubertal development in highly trained athletes seems to follow bone age rather than chronological age 33 . However, genetic predisposition and interindividual variation should always be considered. Certain sports offer advantages to early maturers, and others, like gymnastics, favour the later developing individuals. Therefore, any assessment of sexual maturation must consider the biological indicators of bone age and peak height velocity. Delay in pubertal development and sexual matu- ration has been documented in various types of ath- lets, mainly gymnasts, dancers, and long-distance run- ners 34 . The observed delay is related to the type, the intensity, the frequency and the duration of exercise and is more pronounced in sports requiring strict di- etary restrictions that lead to a deficient energy input in the face of higher energy output. For example, Gym- nasts competing in the Olympic Games have
Description
This review discusses the impact of physical training on growth and maturation in athletes.