© Springer Science+Business Media New York 2016
Diana Vaamonde, Stefan S du Plessis and Ashok Agarwal (eds.)Exercise and Human Reproduction10.1007/978-1-4939-3402-7_1515. Impact of Intense Physical Activity on Puberty and Reproductive Potential of Young Athletes
(1)
Department of Obstetrics and Gynecology, Division of Reproductive Endocrinology, University of Patras, Medical School, University Hospital, 26500 Patras, Greece
Keywords
Menstrual functionReproductive functionAthleteExercisePubertal developmentPrimary amenorrheaSecondary amenorrheaAmenorrheaEnergy homeostasisIntroduction
Over the past decades, major social changes allowed the development of a positive attitude towards physical activity , highlighting the beneficial role of exercise on mental and physical health. Thus, individuals are becoming increasingly involved in physical activities, ranging from regular mild exercise to highly competitive performance requiring intensive and strenuous training. However, as the duration, frequency, and intensity of exercise increases, great concern and major reactions arouse regarding the deleterious effects of intensive physical activity on somatic growth, pubertal development , and biological maturation.
Individual sports exert unique impacts on body composition and development, depending on the sport-related specific features, technical skills and training methods, and the state of growth and maturation of the athlete. Beginning at an early age, athletes performing at a high competitive 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, skeletal and pubertal maturation have been described in individuals performing a variety of sports. Therefore, the whole picture is extremely complex and should be approached with extreme caution and responsibility.
The aim of this chapter is to provide an overview of our current understanding and recent development in the field of exercise-induced disorders of pubertal development and reproductive function.
Exercise and Pubertal Development
Puberty is the period of transition from childhood to adolescence and is marked by the development of secondary sexual characteristics, accelerated growth, behavioral changes, and eventual attainment of reproductive capacity [1]. Moreover, puberty is a dynamic period of development with rapid changes in body size, shape, and composition.
Available approaches for the assessment of pubertal onset and progression include the use of Tanner stages for female breast and pubic hair development and male gonadal and pubic hair development, while menarche is also an important marker used for assessing puberty in girls [1]. More specifically, 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 [2]. Prolonged intensive physical training has great impact 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 [3]. However, genetic predisposition and variation among individuals should always be considered. Specific sports favor the early matures, while others, like gymnastics, offer advantage to the later-developing individuals. Therefore, any assessment of sexual maturation must take into account the biological indicators of bone age and peak height velocity.
It should be noted that the vast majority of the published data involve the influence of physical activity on sexual maturation of female athletes . This inconsistency possibly reflects the sensitivity of the female reproductive system, which is been shown to be highly vulnerable to changes regarding intrinsic and extrinsic factors.
Delayed pubertal development in female athletes has been observed in a variety of sports, mainly gymnasts, dancers, and long-distance runners [4]. The documented delay is determined by the type, the frequency , the intensity, and the duration of exercise and is more pronounced in sports requiring strict dietary restrictions that result in higher energy expenditure in the presence of inadequate energy input.
In the case of gymnasts performing in the high competitive level of the Olympic Games, delayed menarche has been noted, compared to high school, college, and club-level athletes [5]. On the other hand, young girls or adolescents engaged in sports requiring training less than 15 h/week do not show menstrual disturbances or delay in sexual maturation [6].
In elite rhythmic (RG) and artistic (AG) gymnasts, the prepubertal stage was prolonged and pubertal development was shifted to a later age, retaining a normal progression rate [7–10]. Expectedly, the progression of puberty followed the bone age rather than the chronological age [8, 9]. It should be underlined that, for both RG and AG, pubertal progression, although delayed, was not prolonged. Normal girls require an average of 1.96 ± 0.93 years (mean ± SD) for their breast development to progress from Tanner stage II to Tanner stage IV [11]. A comparable period of time was observed for both RG and AG in our study. Therefore, pubertal maturation 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 reflects an energy deficit, prominent in both sports, as a result of intensive physical training (high energy expenditure) on the one side and inadequate caloric consumption (low energy input) on the other. Gymnasts indeed are subjected to a significant energy drain, occurring early in prepubertal age, and are highly motivated to achieve low body weights consistent with their sports requirements for a lean somatotype.
On the other hand, in ballet dancers under high energy drain and low energy intake, a delayed thelarche and a normal pubarche were documented [12]. These findings suggest the existence of independent central mechanisms involved in triggering these aspects of pubertal development . Indeed, breast development and subsequently menarche are related to estrogen levels, while pubarche is mainly related to adrenal androgen production [13]. In conditions of energy imbalance and consequent reduction in adipose tissue mass, estrogen production is decreased and breast development and menarche are delayed. It is the onset, the duration, and the extent of energy deficit that determines the degree of involvement of 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 h of training per week [12], while our examined RG and AG started their training at the age of 6.4–7.7 years with more than 30 h of training per week.
With regard to age of menarche, athletes involved in a large variety of sports, including runners, swimmers, tennis players, ballet dancers, and gymnasts, present a well-documented delayed menarche [12–20]. Although similar trends depending on type of sport are apparent, menarche is more delayed in gymnasts than in swimmers or tennis players who began training at a comparable age [3]. In RG, menarche was significantly delayed compared to their mothers and not trained sisters, an observation arguing against a genetic predisposition towards delayed menarche [10]. 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 prolonged intensive physical training (high energy output) were the major factors influencing menarche. Low body weight, however, remained the most significant factor in delaying the onset of puberty. In addition, it is to be noted that in both RG and AG, older athletes without menarche presented lower height, weight, and body mass index (BMI) compared to their contemporaries with menarche.
Finally, with regard to the effect of physical activity on pubertal development and sexual maturation of male athletes, the data are scarce. In general, boys who participate in sports are normal or advanced for their state of skeletal and sexual maturation, and the advanced states of maturation may be attributed to the power and performance advantages associated with maturation or the existence of preselection bias in terms of sports that favor athletes who are more physically mature than other athletes of the same age [3, 21]. More specifically, in sports where large physiques were necessary for performance success (i.e., swimming and tennis), these athletes tended to have advanced sexual maturation [22]. However, for sports that may create an energy drain, the effects on pubertal development remain inconclusive. In the case of male gymnasts, a sport in which the prepubertal physique confers a performance advantage, there are studies suggestive of a late maturation status [22], while other studies reported no significant influence of intense exercise on pubertal development [21]. These discrepancies should be attributed to methodological differences, mainly regarding the competition level of the studied athletes and the pubertal development assessment methods.
Energy Homeostasis and Pubertal Development
The hallmark of puberty is the reactivation of the hypothalamic pulsatile secretion of gonadotropin-releasing hormone (GnRH), which activates the hypothalamic–pituitary–gonadal (HPG) axis and establishes the production of sex steroids. This reactivation of GnRH production, known to characterize the fetal and neonatal stages, takes place under the influence of several stimuli that are yet to be fully elucidated.
It is well known that a minimum weight-to-height and a critical lean-to-fat-mass ratio are required 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 [23, 24]. Although the principle of a critical percentage of body fat is no longer considered valid, the issue of energy balance and the status of metabolic fuel and energy stores is one of the cornerstones in the control of pubertal onset and progression [25]. Subsequently, several peripherally produced hormones related to energy homeostasis control have been shown to mediate the regulatory role of neural circuits involved in the control of pubertal development.
Among the numerous peripherally produced hormones, leptin has the most prominent and well-studied role connecting energy status with the initiation of puberty and the maintenance of the reproductive function [25] . Although leptin has been considered to play a pivotal role in signaling a metabolic interaction between body composition and reproductive function [26], the available data are inconclusive as to whether leptin is a signal for the initiation of pubertal development or if a critical leptin level is a condition for pubertal onset, acting as a permissive factor so that other critical processes of sexual maturation can occur [25]. With regard to other adipokines, there are conflicting data regarding a possible role of resistin and adiponectin in connecting energy homeostasis and sexual maturation [25].
Furthermore, the gut-derived hormone ghrelin has a well-established role in the regulation of appetite and energy balance , while there are sufficient data to support the possible involvement of ghrelin in the regulation of puberty and sexual function [25]. More specifically, it has been suggested that ghrelin signals energy availability and determines the onset and the progression of pubertal development, and this effect is predominant in males and dependent on the pubertal stage.
Exercise and Reproductive Dysfunction in Females
It is well documented that the female reproductive system is highly sensitive to changes regarding intrinsic and extrinsic factors. Thus, female athletes exposed to intensive training, psychological stress, and strict dietary restrains are vulnerable to developing reproductive dysfunction.
Prevalence
Reproductive abnormalities are present in 6–79 % of females involved in sports activities [27]. Female athletes involved in a large variety of sports, including runners, swimmers, tennis players, ballet dancers, and gymnasts, present a well-documented delayed menarche [12–20]. The prevalence of menstrual dysfunction has been studied widely and varies with the specific sport and the level of competition [27].
Considering the sport-related specific features, the training methods and the technical skills, the sports could be divided into technical, endurance , aesthetics, weight class, ball game, power, and antigravitation sports. Moreover, taking into account the optimal for the specific sport somatotype, the athletic events can be divided into leanness and non-leanness sports [28].
Clinical Patterns of Exercise-Related Menstrual Abnormalities
Menstruation represents a particularly delicate function, indicating normal reproductive activity. Interrelated functions of the hypothalamus, pituitary, ovaries, and endometrium give rise to predictable, cyclic menses that indicate regular ovulation. Ovarian function and menstrual regularity depend on normal cyclic pituitary gonadotropin stimulation. The secretion of gonadotropins occurs in response to pulsatile GnRH release from the hypothalamus. The secretion of GnRH is regulated by various neurotransmitter and neuropeptide pathways.
Female athletic performance has been associated with a broad spectrum of menstrual dysfunction. The dysfunction ranges from primary amenorrhea or delayed menarche to luteal phase deficiency, oligomenorrhea , anovulation, and secondary amenorrhea .
The term amenorrhea refers to the absence or abnormal cessation of the menses. The reproductive dysfunction in amenorrhea is characterized of deranged, abnormal, infrequent or absent luteinizing hormone (LH) pulses, suppressed follicular development, ovulation and luteal activity, leading to persistently low levels of estrogens and progesterone and absence of endometrial proliferation [29]. Primary amenorrhea is indicated when there has been a failure to menstruate by the age of 15 years, in the presence of normal secondary sexual development (two standard deviations above the mean of 13 years) or within 5 years after breast development if that occurs before the age of 10 [30]. Secondary amenorrhea is defined as the absence of three or more consecutive menstrual cycles after menarche (given that pregnancy is excluded), while oligomenorrhea describes menstrual cycles of 35 days or more (alternatively, menstrual intervals of 45–90 days).
Luteal phase deficiency denotes asymptomatic subclinical menstrual disturbances, resulting in low estradiol levels in the early follicular phase, decreased but normal LH pulse frequency with increased pulse amplitude. Ovulation occurs, but the developed corpus luteum produces reduced progesterone support for proper endometrial development in the secretory phase. Thus, successful implantation of fertilized egg is prevented and infertility ensues.
Anovulation is a more severe asymptomatic reproductive dysfunction, characterized by suppressed follicular maturation leading to lack of ovulation. Both estrogen and progesterone levels are low, but some proliferation of endometrium is achieved, resulting in profuse bleeding at unexpected times.
Pathophysiology of Exercise-Related Menstrual Abnormalities
During the past decades, many studies have been conducted regarding sports activities and athletic performance, focusing on the influence of physical activity on reproductive function. The main factors etiologically correlated with menstrual disturbances in athletes are energy balance (energy availability) and body composition , stress (physical exercise and psychological stress), diet, training methods (sports character), and reproductive maturity.
Weight and Body Composition and Energy Availability
One of the earliest and most interesting approaches to menstrual dysfunction in athletes was made by Frisch et al., who theorized that the onset of menarche is achieved when body fat reaches a “critical threshold” of 17 % of body weight and that menstruation is disrupted when body fat falls below a “critical threshold” of 22 % of body weight. 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 [24]. Since then, weight and body composition have been considered the most common and most convincing explanation of female reproductive dysfunction in athletes.
Recent studies, however, argue the existence of a critical body weight or fat percentage in order to achieve menstruation, introducing dispute over theoretical and statistical issues [31–33]. Furthermore, available data suggest a central role for energy availability (defined as dietary energy input, minus exercise-induced energy expenditure), rather than body weight, in the pathogenesis of reproductive dysfunction in female athletes [33]. It has been proposed that negative energy balance (failure to meet the metabolic requirements) causes an alteration in brain function that disrupts the GnRH pulse generator.
Researchers studying monkeys concluded that exercise-induced amenorrhea was reversed by diet and caloric supplementation, without any modification of their exercise regimen [34]. It appears that energy deprivation leads to a disruption in LH pulsatility, in contrast to exercise stress, while LH pulsatility is suppressed in the presence of energy depletion, regardless of the cause. In addition, caloric imbalance prevents the normal pulsatile secretion of LH in exercising women [35]. Thus, it is proposed that exercise has no detrimental effects on female reproductive regulation, apart from the cost on energy balance.
The emerging role of adipose tissue as an active endocrine organ has attracted the scientific concern and revealed a number of adipose-secreted factors (known as adipokines) involved in signaling and regulating homeostasis , energy balance , insulin action, reproductive function, and inflammation process. For instance, leptin has an established role in energy homeostasis , metabolism, and reproductive function, while adiponectin attracts growing interest as a mediator in metabolism and reproduction.
The discovery of leptin boosted the interest on the body composition hypothesis and provided the missing link with the energy availability hypothesis. Leptin has been investigated as a mediator between the adipose and the reproduction system [26] and has been considered to play a pivotal role in signaling a metabolic interaction between body composition and reproductive function . Serum leptin levels reflect the dietary status and caloric balance: Rapid and profound declines in leptin levels were documented in response to fasting and dietary restrictions, while extreme increases were noted in response to overfeeding and refeeding after caloric deprivation [33]. Furthermore, in severely undernourished women, the preservation of neuroendocrine control of reproductive function is mediated by leptin [36]. In addition, a critical level of leptin is required for the maturation and maintenance of menstruation [37]. Moreover, it has been reported that serum leptin levels were reduced in highly trained athletes and the diurnal pattern of leptin secretion was lost in amenorrheic, compared to menstruating athletes [38]. Finally, exogenous leptin (recombinant r-metHuLeptin) administration managed to improve the reproductive function of a small cohort of women with hypothalamic amenorrhea, due to strenuous exercise or low body weight [39].
In contrast with leptin, adiponectin is markedly reduced in obesity and rises with prolonged fasting and severe weight reduction. Despite a well-described role in metabolism, cardiovascular protection, and inflammatory process, recent studies suggest a potential role in the regulation of neuroendocrine reproductive processes. More specifically, it has been reported that adiponectin inhibits both basal and GnRH-stimulated LH secretion in short-term treated rat pituitary cells [40]. Furthermore, Lu et al. reported that adiponectin acutely reduced basal and GnRH-stimulated LH secretion but had no impact on follicle-stimulating hormone (FSH) levels [41]. Consequently, high levels of adiponectin (as found in lean and energy-restrained female athletes) may contribute to suppression of LH levels and chronic anovulation . Thus, adiponectin could be considered as a link between adiposity and reproduction.
In addition to the role of the aforementioned adipokines, there are gut-derived hormones signaling energy homeostasis implicated in normal reproductive function [25]. Among them, ghrelin has a well-studied role in the regulation of puberty and sexual function. Studies in rodents and humans have shown that ghrelin reduces baseline LH secretion, with reductions in both pulse amplitude and frequency [25].
Physical Stress
The hypothesis that menstrual disturbances in athletes might be caused by the stress of exercise was originally based on animal experiments and recently on studies of amenorrheic athletes. The interaction between HPA axis and reproductive system was studied in rats and monkeys [42, 43], demonstrating that the hormones of the HPA axis could disrupt the reproductive function by both central and peripheral mechanisms [44].
A few decades ago, Bullen et al. reported the induction of menstrual disorders in regularly menstruating women, by imposing strenuous exercise [45]. Regularly menstruating, untrained women were exposed to high-volume aerobic exercise, which leads to a large prevalence of luteal phase deficiency and anovulation. Since then, a mild degree of elevated cortisol levels has been documented in amenorrheic athletes [29, 45, 46].
HPA axis activation provides a hormonal mechanism of reproductive dysfunction in female athletes. Cortisol can suppress gonadotropin secretion from the pituitary [47] and corticotropin-releasing hormone (CRH) can suppress GnRH secretion from the hypothalamus by increasing the hypothalamic opiate inhibition [48]. Furthermore, it has been suggested that athletes presenting more profound menstrual disorders exhibit a greater activation of the HPA axis [29].
Psychological Stress
Psychological stress is another factor commonly implicated in the etiology and pathogenesis of exercise-induced menstrual disturbances. Although there are studies correlating behavioral and psychological parameters in women with functional hypothalamic amenorrhea , few data exist to support this hypothesis in athletes [49]. Amenorrheic athletes exhibit similar psychological profile compared with menstruating athletes [50], while studies regarding musicians, with a competitive lifestyle similar to that of athletes, concluded that the psychological stress of competitions has no causative role in reproductive dysfunction of most individuals [12].
Diet
Few data exist regarding a possible role of diet composition on the pathogenesis of menstrual disorders in athletes. Apart from the influence of inadequate caloric intake (insufficient to compensate the increased energy expenditure), the diet composition has been studied separately regarding a possible correlation with reproductive dysfunction in female athletes. Protein and fat intake appears to be decreased in amenorrheic athletes. The controversial data resulting from studies attempting to correlate the incidence of menstrual disorders with vegetarian diets—favored by some athletes—might imply the synergic effect of other factors (such as energy balance, training intensity, or emotional stress) in the development of reproductive dysfunction [51, 52].
Training Methods/Sports Characteristic Features
It is well known that the unique character of each sport consists of specific skills requirements, favorable somatotype, and special training methods. The age of training onset, the optimal somatotype, the specific sports demands as well as the intensity, frequency, and duration of training determine dietary restrictions and certain energy and metabolic profile, influencing the menstrual status of female athletes.
Heavy training load appears to exert more harmful effect on menstrual function when initiated abruptly, compared with a gradual acceleration [53]. Moreover, long-term training at levels of energy expenditure above the lactate threshold affects menstrual function more than long-term training at or below the lactate threshold [54]. Furthermore, exercise-induced menstrual disorders are more common in endurance runners and ballet dancers than in swimmers and cyclists [17, 55, 56]. This observation could be interpreted considering the optimal somatotype demands, attracting individuals of certain body characteristics to different types of elite competitive sports (e.g., thinness in ballet dancers and long-distance runners), combined with dietary adaptations and restrictions.
Reproductive Maturity
It has been suggested that intense training has less effect on menstrual function of previously sedentary menstruating individuals, compared with premenarcheal adolescents [57]. This might be due either to a sensitivity of reproductively immature females to the influence of intense exercise or as a predisposition of young individuals to exercise-mediated reproductive disorders [58]. Nevertheless, it seems very difficult to isolate and evaluate reproductive maturity as a factor interfering in the pathogenesis of exercise-induced reproductive dysfunction, separated from energy availability, body fat, and body weight [33].
Menstrual Disorders in Specific Sports
Somatic growth and biological maturation in runners have been well studied and described. Although in the same sport field, runners are divided in recreational, small distance, and long distance, considering the training methods, the technical skills, the favorable somatotype, and the specific requirements of each event. Athletes participating in power events (e.g., sprints, hurdles) train at maximal or near-maximal intensity in short bursts. Conversely, athletes participating in endurance events (e.g., middle-distance and long-distance running) train at lower intensity levels for extended periods. Power athletes are heavier and have more total lean mass than their endurance counterparts [59].
Menstrual disorders characterize as much as 24–26 % of female runners [60, 61]. Within distance runners, prevalence of amenorrhea increased from 3 to 60 % as training distance increased from < 13 to > 113 km/week, while their body weights decreased from > 60 to < 50 kg [56]. Furthermore, subclinical menstrual disorders are present in both highly trained [29] and recreational [62] eumenorrheic athletes; luteal deficiency or anovulation was found in 78 % of eumenorrheic recreational runners in at least one menstrual cycle out of three [62]. On the other hand, in sub-elite moderately exercising female runners, no effect on pubertal development was demonstrated [63].
Dance training has been shown to be associated with a high incidence of menstrual dysfunction, particularly in disciplines such as ballet [55]. Ballet dancers begin strenuous training at an early age, undergo intensive exercise and heavy caloric restrictions leading to energy deficit, in order to perform at a competitive level and retain a lean physique. Teenage ballet dancers are lighter, with less body fat and higher incidence of delayed puberty and primary and secondary amenorrhea, compared with less physically active girls [53, 55].
Swimmers present normal weight, less fat, and more muscle mass than nonathletic girls but a greater percentage of fat than that of amenorrheic athletes in other sports [12]. The latter reflects an adjustment to the sport-specific requirements, as in aquatic sports, subcutaneous fat helps floatation, reducing energy expenditure for water surface maintenance. Constantini et al. studied swimmers of competitive level and demonstrated that menstrual cycles were more irregular or anovulatory rather than absent. Considering the greater amount of fat in swimmers, functioning as an estrogen producer and reservoir, the observed menstrual disturbances could not be attributed to hypoestrogenism and might be due to mild hyperandrogenism [64].
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