Effects of Sports Training in Adolescence on Growth, Puberty and Bone Health

Written By: Sam Savage

Published Date: January 5, 2007 Last Edited: January 5, 2007

By Bertelloni, Silvano; Ruggeri, Silvia; Baroncelli, Giampiero I

Abstract

Athletic training in adolescent females is important for their well-being; indeed, it may have both positive and negative effects on some physiological processes, as growth, reproductive axis and bone health. Adequate physical activity likely exerts neither a positive nor a negative effect on growth. By contrast, intensive training and insufficient diet may have a negative influence on growth, probably due to energy deficiency and impairment of the growth hormone-insulin-like growth factor-I axis; net long term- effects of such alterations remain to be established. Adolescents who perform regular athletic training present with normal or slightly advanced sexual maturation, because increased strength and power associated with earlier maturation advantage them. However, intensive training and inadequate energy intake may induce delayed menarche and menstrual dysfunctions. The consequent hypoestrogenism, in association with the nutritional deficiencies, may affect bone health. On the contrary, regular physical activity increases the amount of bone mass gained during childhood and adolescence mainly at the bone sites which are trained. Since the number of adolescent females involved in strenuous sports from an early age is increasing, physicians must be aware of such effects, explain to girls and their parents the ‘right’ sports training and appropriate dietary regimens, and recognize problems due to excessive training as soon as possible. These issues should not be a cause of lesser involvement in athletic participation of young people.

Keywords: Female adolescents, sport, growth, puberty, reproduction, bone health, intensive training

Introduction

In adolescents, regular physical activity is important for good body function and development. In addition, involvement in sport may improve socialization, emotive control, respect for rules and scholastic learning, and may contribute to prevent or reduce overweight and abnormal social behaviors. Physical training in childhood may also represent an ‘imprinting’ for athletic activity, contributing to the prevention of cardiovascular and metabolic diseases in older age [1].

Unfortunately, levels of physical activity fall as young people become older, particularly among girls [2], in whom a progressive decline in athletic training has been documented during adolescence [3]. The decrease in physical activity is likely due, at least in part, to an increase in the time teenagers spend engaged with media. A recent Italian survey in 11-15-year-old adolescents showed a decrease in regular physical activity by about 5% in 2002 compared with 2000, while television viewing increased by 6% and use of personal computers increased by about 40% in the same period [4], suggesting that Western models induce a sedentary lifestyle.

In addition to risks posed by inactivity, some girls are also exposed to the risks of excessive physical training from an early age, which may have an impact on growth, reproductive function and bone mineralization [5].

Sports activity and growth

Adolescence is a crucial period for linear growth, and sports training during this time may have positive or negative effects on some physiological processes as growth.

The first stage of infancy is characterized by rapid growth in stature, followed by its progressive reduction (growth velocity declines from 25 cm/year in the first year to 9 cm/year in the third year) [6]; at this age, children do not engage in sports training. In the second stage of infancy, growth in stature is slow and regular (about 5-6 cm/year) [6]; in this period of life many children start athletic training but intensive physical activity is usually not performed, at least until the prepubertal years. During puberty, growth velocity increases again (pubertal spurt, 10-12 cm/ year) [6]; in this period, intensive training is experienced by many girls and it may have some impact on growth.

To address this issue, pioneering studies compared longitudinal pubertal growth patterns in active and inactive boys [7,8]. A Canadian study followed 14 active and 11 inactive boys from 10 to 16 years [7], and a Belgian trial compared 32 active and 32 nonactive boys from 12 to 18 years [8]. Active and inactive Canadian and Belgian boys did not differ in their mean stature, peak height velocity and age at peak height velocity, suggesting no significant effect of training during adolescence on these parameters [7,8]. Damsgaard and colleagues [9] studied 184 children (96 girls, 88 boys, age 9-13 years, sport competitions: swimming, tennis, team handball, gymnastics) and found significant differences in height among 9-13-year-old children participating in the four different sports, but these differences also existed at the age of 2-4 years, long before the children of both sexes started their sports training [9].

Malina [10] concluded that regular training has neither a positive nor a negative effect on growth, but that it could represent a selection factor. Adolescents having specific auxological characteristics more likely engage in sport activities that permit them to attain better athletic results [10]; for example, tall girls are likely to play basketball, while short girls usually engage in gymnastics.

However, intensive training in this period of life should be avoided, because excessive physical activity may have a negative impact on growth, mainly in females.

Bass and associates [11] studied 83 prepubertal and peripubertal female gymnasts (training 8-36 h/ week) and 110 sedentary girls. The former group showed significantly lower growth velocity and pubertal growth spurt than the latter. Skeletal maturation in the active gymnasts was delayed by 1.3 years, while there was no difference between bone age and chronological age in the control subjects [11]. The delay in skeletal maturation in the gymnasts worsened with increased duration of training [11]. The lower height in active gymnasts was related to both reduced leg length and deficit in trunk growth [11]. The reduced leg length was likely due to selection bias because it was present at baseline; during follow-up, leg length increased at the same rate as it did in control subjects, tracking at the lower part of the normal population but remaining unchanged [11]. The acquired component of the height deficit in gymnasts resulted from progressive impairment of trunk length, which became clearly detectable when training lasted for more than 1-2 years [11]. These data indicate that in adolescent girls excessive training may interfere with the normal growth pattern and likely with the development of normal body proportion.

However, disagreement exists regarding the ultimate effect of intense physical training on final adult height. By studying female elite rhythmic gymnasts (n = 104, age 12-23 years, mean sports training 32 h/ week), Georgopoulos’s group [12] demonstrated that adult height was not significantly different from predicted height estimated at first evaluation and was significantly higher than target height (Figure 1). In addition, the examined gymnasts continued to increase in height up to the age of 18 years, when final adult height has already been reached in normal growing girls [6]. This study suggests that elite rhythmic gymnasts compensated reduced intensity of the pubertal growth spurt by delayed menarche, which drives the achievement of adult height at a later age. Both advanced- and intermediate-level competitive female gymnasts may experience a blunted pubertal growth spurt with later attainment of adult height [13], suggesting that involvement in lower-intensity training during adolescence may also have a transitory impact on growth.

Theintz and collaborators [14] compared young elite female gymnasts (n = 22, age 12.3 0.2 years, average training 22 h/week) and moderately trained swimmers (n = 21, age 12.3 0.3 years, average training 8 h/week). In swimmers, height predictions did not change significantly with age, whereas height prediction decreased significantly in gymnasts during follow-up, leading to an adult height below genetic target (Figure 1) [14].

From the hormonal point of view, excessive training may induce a derangement of the growth-controlling axis. Eliakim and co-workers [15] followed a group of adolescent males involved in sport and a sedentary control group; after 5 weeks of training, the active boys showed a significant decrease in some growth factors (growth hormonebinding protein, insulin-like growth factor-I (IGF-I) and IGF- binding protein-3 (IGFBP3)), while IGFBP-2 increased and growth hormone (GH) secretion remained unchanged. Similar data have been reported in trained prepubertal, early pubertal and late adolescent girls [16-18]. This endocrine pattern, suggesting a GH resistance state [15], resembles that reported in children with undernutrition and stunted growth for atypical celiac disease [19]. So3 poor nutrient intake and related energy deficiency may impair the GH-IGF- I axis and growth in adolescents exposed to intensive physical training [15,16]. Findings in adolescent boys affected by anorexia nervosa seem to confirm this hypothesis. Such patients showed a stunted growth as the result of nutritional deficiencies; catch-up growth after recovery from the disease occurred, but it was unable to fully restore the growth potenti\al – in fact, final height was reduced in comparison with target height [2O]. In prepubertal and pubertal girls, stunted growth is very frequent sign of anorexia nervosa as well [21,22]. Catch-up growth of different degrees has been observed during nutritional rehabilitation, but some girls did not reach their pre-disease centile [21] and near-final adult height has been reported to be reduced compared with patient genetic height potential [22]. Taken together, these data suggest that nutritional and/or energy deficiency during the peripubertal period may impair growth pattern and final height depending on its degree and duration. Associated psychological stress is an adjunctive factor to be considered [23]. In summary, adequate physical activity in adolescent girls likely does not exert any positive or negative effect on growth. Regarding intensive training, a critical review on this issue concluded that elite female gymnasts may experience attenuated growth during the years of training and competition, followed by catch-up growth in periods of reduced training or after retirement, but evidence remains inconclusive on whether negative effects on adult height are actually operative [16]. Thus, definite conclusions on this matter can only be obtained by well-designed longitudinal studies taking into account several variables such as training volume and intensity, nutrition, energy expenditure, stage and progression of puberty, genetic background and growth potential, and social and psychological factors.

Figure 1. Target height and adult height in female elite rhythmic gymnasts (a; drawn from data reported in [12]) and female elite artistic gymnasts (b; drawn from data reported in [14]); while the former subjects reached their genetic target height, the latter subjects did not (see text). (Data represent mean + 1 SD.)

Sports activity and reproductive function

During puberty, development of secondary sexual features occurs [6]. The timing of pubertal onset and progression is due to genetic determinants as well as environmental factors, such as climate, nutritional status and chronic diseases [6]. Sports training may be an additional factor affecting pubertal progression and reproductive function [24]. The relationship between the hypothalamic-pituitary- gonadal axis and athletic training in girls is of interest because today they begin intensive physical activity in the peripubertal period and are involved in elite competition from early puberty [1,16,23].

Adolescents who perform regular physical activity may present normal or slightly advanced secondary sexual maturation [24]. Greater body size and slightly advanced pubertal maturation may be advantage factors, because selection for adolescent sport is based on chronological age, not on biological age, and the higher muscle strength and power associated with earlier maturation can determine sports success and better possibility of selection by the coaches [25].

However, as for growth, early intensive physical training may have a negative impact on pubertal development and reproductive function [23,26-28]; it is associated with late onset of menarche mainly in sports that emphasize lean body phenotype [29,30].

Frisch and colleagues [26] found that a group of premenarcheal- trained swimmers and runners (n=18) showed a mean age at menarche of 15.1 0.5 years, whereas a comparable group of postmenarcheal- trained athletes (n – 20) had a mean age at menarche of 12.8 0.2 years. An untrained control group attained menarche at 12.7 0.4 years, an age significantly lower than that of the first group but similar to that of the second group [26]. Each year of training before menarche delayed its onset by 5 months [26]. A delay in the age of menarche ranging from 0.4 to 1.5 years as been confirmed in several studies, depending on the type of sports activity and the country of origin [16,29-31]. The pubertal delay seems to be mainly a characteristic of female sex, since both trained and untrained adolescent males showed similar genitalia stage and testosterone levels [32]. Indeed, differences in pubertal development between the two sexes and difficulties in assessing reproductive function in males may contribute to the different results in male and female adolescent athletes.

The presence of menstrual dysfunction in about 30% of adolescent female adiletes has been shown, but with a wide range (3-60%) related to training intensity and the age of its commencement [5,26,283O]. Frisch’s group [26] reported that 61% of the premenarcheal-trained athletes had irregular menstrual cycles and 22% were affected by amenorrhea. By contrast, 60% of the postmenarcheal-trained athletes had regular menstrual cycles and none had amenorrhea [26]. In 69 competitive female swimmers (aged 16.4 0.5 years), Costantini and associates [27] found that, in addition to older age at menarche, postmenarcheal adolescent swimmers reported more menstrual irregularities immediately post menarche than the control group (82% vs. 40%, respectively); in addition, while in the control population there was constant decrease in menstrual dysfunctions with the increase of gynecological years, they remained constant in the trained girls [27]. Oligo/amenorrhoea is the commonest menstrual disturbance in high-level athletes, but abnormal bleeding, delayed menses, corpus luteum dysfunction and anovulation also occur [5,27,28]. These abnormalities usually remained unperceived and largely undiagnosed in the majority of these adolescents [5,28,29].

In addition to menstrual disturbances, CasteloBranco and co- workers [30] demonstrated lower level of painful menstruations and lower breast circumference in a group of trained adolescent girls in comparison with a group of untrained controls, adding to data on reproductive axis dysfunction in the former group.

Body weight 10-15% below ideal has been reported in over-trained females with reproductive dysfunction [5,29], and vigorous exercise seems to induce menstrual abnormalities more frequently in underweight subjects than in normal-weight subjects, suggesting that dietary restriction and related energy deficiency may represent a key factor for ovarian dysfunctions of young athletes [5,16,28,30,33]. Chronic energy imbalance between caloric intake and caloric expenditure may impair the activity of the gonadotropin- releasing hormone (GnRH) pulse generator by modifications in the production of neuromodulators in specific brain areas via body hormonal signals [33]. The adipose-tissue hormone leptin may have a key role. Body fat [33,34] and circulating leptin values were found to be significantly reduced in elite female athletes (n = 22, age 13.6 1.0 years, training 22.1 1.7 h/week, mean body fat, %: 14.4 (controls 21.9%)) and did not follow the typical female pattern of leptin increase during puberty (Figure 2) [34,35]. Reduced leptin values are also found in young athletic males, but to a lesser extent, explaining the less impaired gonadal function in this sex [36]. Ghrelin, a hormone produced predominantly by the stomach that stimulates GH secretion and food intake [37], might play an additional role in hypothalamic-hypophyseal-ovarian axis dysfunction in over-trained athletes [33]. In fact, ghrelin levels have been found to be 100% higher in physically active women than in inactive controls [38]. The low level of leptin associated with increased ghrelin resembles that of amenorrheic patients with anorexia nervosa [33,38,39], confirming the role of food intake-regulating hormones on GnRH generator function. Psychological stress, and the related increase in stress hormones due to intensive training and competitions, may be an adjunctive factor affecting the reproductive axis in adolescent female athletes [16,23,29].

Figure 2. Pattern of serum leptin values ([black triangle up]) from pubertal stage 1 to 4 in female gymnasts (n = 22, mean age 13.6 1.0 years, training intensity 22.1 1.7 h/week; drawn from data reported in [34]). For comparison, normal leptin values ([black circle]) in healthy girls in the same pubertal stages are shown (drawn from data reported in [35]). (Data represent 1 SD.)

Sports activity and bone health

Bone mass increases during childhood until the second to third decade of life, with peak bone mass usually reached 2-3 years after the attainment of adult height [4O]. During the pubertal spurt about 30-50% of total bone mass is achieved [40,41].

Active load forces, such as the pull on bone from muscle contractions, and static load forces, such as those due to weight, mechanically strain and deform bone. When these mechanical strains are greater than needed for steady-state remodeling, a modeling response occurs that increases bone mass and improves the internal structural supports at the high-strain locations [42]. Participation in sport could not only have a direct osteogenic effect, but also an indirect effect by enhancing muscle mass and hence the tension generated on bone [41]. Thus physical activity has double positive effects on bone health, and they seem to be site-specific and exerted mainly during prepuberty and early puberty [41]. Greater bone density in the dominant arm of elite female adolescent tennis and squash players (n= 105) has been reported with side-to-side differences ranging from 8.5 to 16.2%; the difference between dominant and non-dominant arms being significantly higher than that found in a group of healthy female controls [43]. The benefit of playing was about two times greater when the athletes started their activity before or around menarche rather than after it [43]. Following 113 children (females, n = 53; males, n = 60) annually for 6 years, Bailey and collaborators [44] found that both active girls and boys attained greater total body and femoral peak mass, assessed by dual-energy X-ray absorptiometry, than inactive subjects. Major gain was detected in girls in comparison with boy\s (total body peak mass: active girls +17%, active boys +9% vs. controls; femoral neck: active girls +11%, active boys +7% vs. controls) [44]. In addition, adolescent females who perform predominantly weight-bearing activity characterized by high axial compressive forces had higher bone mass density and larger site-specific bone mass density than athletes involved in sports that are not-weight-bearing and controls (Figure 3) [45]. Longitudinal studies confirmed these cross-sectional data. In young female gymnasts (n = 16, age 8-13 years, physical training 12-18 h/week), higher increases in lumbar and femoral bone mineral density (BMD) were reported in comparison with a control group not involved in agonistic training during a 3-year follow-up [46]. In an other study, areal BMD increased from age 13 to 16 years in trained adolescent girls (n = 21) in comparison with peers with low-level activity (n = 21) while volumetric BMD remained stable in both groups, suggesting that exercise may act on bone mass by inducing an increase in bone dimensions more than affecting bone mineralization [47].

A training effect on bone anabolism is also demonstrated by the higher values of biochemical markers of bone deposition, such as osteocalcin, bone alkaline phosphatase and propeptide of type 1 procollagen, after brief endurance training (2 h/day for 5 days/ week for 5 weeks) in mid-adolescent females (age 15-17 years) in comparison with untrained controls [48].

The age-dependent effects of sport on bone mass and metabolism may be mediated, at least in part, by the higher levels of growth factors enhancing bone formation in the premenarcheal years, such as GH, IGF-I and 1,25-dihydroxyvitamin D, in association with the combined effect of mechanical loading and muscle exercise [40,41,42,48]. The circulating levels of these hormonal factors decline sharply during the postmenarcheal years, as does the effect of training on bone [40,42,49]. So, a window of opportunity likely is operative from early puberty to menarche to optimize the positive effect of sport on bone health and peak bone mass attainment [49]. External factors, like nutrition, vitamin D status, age at menarche and stress hormones, may act in such a window, impairing the positive effect of weight-bearing and exercise on bone. However, such a hypothesis remains largely speculative and should be confirmed.

Figure 3. Total-body bone mineral density (BMD) (mean and 95% confidence interval) in adolescent female volunteers (age 15-18 years, subdivided as controls, swimmers, cyclists, runners and triathletes, n= 15 per group; drawn from data reported in [45]). *Significantly greater than swimmers and cyclists (p

Table I. Prevalence of female athlete triad (FAT) syndrome among high-school and collegiate female athletes.

Although regular physical activity improves bone health [42], some girls who are over-trained may develop reduced BMD (i.e. osteopenia, BMD

The prevalence of female athlete triad syndrome differs among various studies (range from 1 to ~60%) [28,50], the highest values being reported in sports in which low body weight conveys a competitive advantage [5]. In particular, the prevalence of reduced BMD in young female athletes is largely unknown, and may be related to the difficulties in correct assessment of BMD in children and adolescents and the uncertainty in the definition of osteopenia and osteoporosis in childhood [51]. Recent surveys among high-school and collegiate athletes found that disordered eating and menstrual dysfunctions are relatively frequent, while the prevalence of reduced BMD is low [52,53] (Table I). Only a minority of examined adolescent and young adult subjects met the criteria for all three components of female athlete triad syndrome [52,53] (Table I). These data, together with the evidence of a similar occurrence of the complete triad in elite Norwegian athletes and non-athletic controls [54], may suggest that the real incidence of the complete syndrome as well as the related clinical concerns are less than previously reported [55]. In addition, the long-term effects of the syndrome on adult women’s health remain unknown [55]. Large prospective investigations in homogeneous groups of adolescent athletes using strict and well-applied criteria should be urged to clarify these issues.

Figure 4. Possible pathogenetic mechanisms of long-term consequences of excessive physical training during adolescence. Intensive training and the often associated disordered eating habits may induce inadequate energy intake and related caloric deficiency, which deranges the growth hormone (GH)-insulin-like growth factor-I (IGF-I) axis, impairing linear growth and eventually the attainment of genetically adequate adult height. In addition, intensive training and inadequate energy intake may interfere with the hypothalamic-hypophysealgonadal (HHG) axis, leading to reduced secretion of gonadal sex steroids and so to delayed puberty and menstrual dysfunctions. Nutritional deficiencies, low energy intake, GH-IGF-I axis alterations, HHG axis dysfunctions and delayed puberty may affect bone mass. Chronic stress due to intensive training may contribute in GH-IGF-I axis and HHG axis alteration, acting by derangement of hypothalamic-pituitaryadrenal axis. Altogether these mechanisms may result in complete clinical manifestation of the female athlete triad syndrome (LH, luteinizing hormone; FSH, follicle-stimulating hormone).

Conclusion

The concept that sport training is important for adolescents’ physical and psychological development is well-known, but further studies should address the exact physiological role of athletic training on growth, pubertal development and bone health. Indeed, it remains not completely understood whether there is an excessive level of training during adolescence that may cause long-term detrimental effects (Figure 4).

Since the number of prepubertal girls and young adolescents involved in strenuous sports is increasing, physicians should be made aware of the myriad of beneficial effects as well as some of the potential risks linked to training, so as to provide appropriate counseling to young athletes and their parents on the ‘right’ athletic training and appropriate dietetic regimens. All physicians involved with the care of adolescent females must also be able to recognize, as soon as possible, physical signs and psychological issues due to intensive training and propose appropriate care [50]. However, these risks should not induce physicians to counsel a lesser involvement in athletic participation [55].

Note added in proof

A deterioration in final adult height has been recently documented in artistic gymnasts in both sexes, but more pronounced in males (n= 102; final height -2.28 0.95 SDs vs target height) than in females (n= 117; final height -0.44 1.17 SDs vs target height). Georgopoulos NA, Theodoropoulou A, Rottstein L, Koukkou E, Mylonas P, Vagenakis G, Labropoulou E, Polikarpou G, Tsekouras A, Giamalis P, Kourounis G, Vagenakis AG, Markou K. Final height in rhythmic and artistic gymnasts. Proceedings 12th European Meeting of the International Association for Adolescent Health, Athens, September 21-23, 2006:65 (abs).

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SILVANO BERTELLONI, SILVIA RUGGERI, & GIAMPIERO I. BARONCELLI

Adolescent Medicine, Department of Pediatrics, University of Pisa, Pisa, Italy

(Received 22 March 2006; revised 28 August 2006; accepted 8 September 2006)

Correspondence: S. Bertelloni, Division of Paediatrics, Department of Reproductive Medicine and Paediatrics, University of Pisa, Santa Chiara Hospital, Via Roma 67, 1-56125 Pisa, Italy. Tel: 39 050 992743. Fax: 39 050 550595. E-mail: [email protected]

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