Pensar en Movimiento:
Revista de Ciencias del Ejercicio y la Salud
EISSN 1659-4436
Vol. 12, No.1, pp. 1- 24
Cierra el 30 de junio,2014
THE FEMALE ATHLETE TRIAD: A METABOLIC PHENOMENON
Anne B. Loucks, Ph.D., FACSMAnne B. Loucks, Ph.D., FACSM
loucks@ohio.edu
Ohio University, United States of America
Original Submission: 30/11/2013; resubmitted: 28/02/2014; accepted: 31/03/2014; published: 30/06/2014.
Abstract
Loucks, A. B. (2014). The Female Athlete Triad: A Metabolic Phenomenon. PENSAR EN MOVIMIENTO: Revista de Ciencias del Ejercicio y la Salud, 12 (1)1-23. The Female Athlete Triad (Triad) is a syndrome in which low energy availability triggers a broad range of endocrine mechanisms that conserve energy expenditure, and thereby impairs reproductive and skeletal health. Energy availability is the amount of dietary energy remaining after exercise training for all other physiological functions each day. The specific kind of reproductive dysfunctions caused by low energy availability are functional hypothalamic menstrual disorders. To ensure that affected athletes receive appropriate care, endocrine tests are required to diagnose these disorders by the exclusion of other types of menstrual disorders unrelated to the Triad. In addition, low energy availability impairs skeletal health by uncoupling bone turnover, in which the rate of bone resorption increases while the rate of bone formation declines. The result is a progressive loss or failure to accrue bone mass, which increases the risks of stress fractures and osteoporosis. Low energy availability originates in one or more of three sources: restrictive eating disorders, especially anorexia nervosa; intentional efforts to lose body weight or body fat to improve athletic performance or appearance; and the inadvertent suppression of appetite by exercise and diets containing a high percentage of carbohydrates. It is necessary to know the origin of low energy availability in a particular athlete in order to intervene effectively with her. The key behavior modification for preventing and treating the Triad is to increase energy availability, either by increasing dietary energy intake, reducing exercise energy expenditure, or both. Guidelines for doing so are provided.
Keywords: Female Athlete Triad, energy availability, menstrual function, bone mineral density, appetite, eating disorders, disordered eating, weight loss
Resumen
Loucks, A. (2014). La tríada de la atleta: un fenómeno metabólico. PENSAR EN MOVIMIENTO: Revista de Ciencias del Ejercicio y la Salud, 12 (1)1-23. La tríada de la atleta (tríada) es un síndrome en el cual la baja disponibilidad de energía dispara una amplia gama de mecanismos endocrinos para disminuir el gasto energético, lo cual perjudica la salud reproductiva y esquelética. La disponibilidad energética es la cantidad de energía de la dieta que queda cada día, después del entrenamiento o el ejercicio, para todas las demás funciones fisiológicas. El tipo específico de mal funcionamiento reproductivo provocado por la baja disponibilidad energética son los trastornos menstruales hipotalámicos. Para asegurarse de que las atletas afectadas reciban la atención apropiada es necesario realizar pruebas endocrinas que sirven para diagnosticar los trastornos mencionados mediante la exclusión de otros trastornos menstruales no asociados con la tríada. La baja disponibilidad energética perjudica la salud esquelética debido al desacoplamiento del recambio óseo, en el cual la tasa de resorción aumenta mientras la tasa de formación de hueso desciende. El resultado es una pérdida progresiva de hueso o la incapacidad de acumular masa ósea, lo cual aumenta el riesgo de fracturas por estrés y de osteoporosis. La baja disponibilidad energética tiene su origen en al menos una de las siguientes tres fuentes: trastornos de la alimentación de tipo restrictivo, especialmente la anorexia nerviosa; los esfuerzos intencionales orientados a la pérdida de peso corporal o grasa corporal, para mejorar el rendimiento deportivo o la apariencia; y la supresión inadvertida del apetito causada por el ejercicio y por las dietas con un alto porcentaje de carbohidratos. Para poder realizar una intervención eficaz con cada atleta es necesario conocer el origen de su baja disponibilidad energética. La modificación clave de la conducta para la prevención y tratamiento de la tríada es el aumento de la disponibilidad energética, ya sea mediante el incremento de la ingesta energética en la dieta, la reducción en el gasto energético por ejercicio, o ambos. Por lo tanto, se ofrecen algunas pautas para lograr la disponibilidad energética correcta.
Palabras clave: Tríada de la atleta, disponibilidad energética, función menstrual, densidad mineral ósea, apetito, trastornos de la alimentación, pérdida de peso
Introduction
All girls and women are encouraged to participate in physical activities and sports, because the benefits of participation far outweigh the risks (Nattiv, Loucks, Manore, Sundgot-Borgen, & Warren, 2007). One of those risks is the Female Athlete Triad, in which reproductive and skeletal health are impaired by energy deficiency (Loucks, 2011; Loucks, Kiens, & Wright, 2011). The prevalence of the Triad varies greatly from team to team and from sport to sport, but it tends to be highest in esthetic, endurance, and weight-class sports in which a thin build confers a competitive advantage or qualifies an athlete for participation (Nattiv et al., 2007).Each of the three components of the Triad spans a spectrum ranging from health to disease (Figure 1). The population of athletes is distributed across these spectrums, and individual athletes travel along them as changes in their diet and exercise habits affect the amount of energy they have available for reproductive and skeletal health. It should be understood that an athlete travels at different rates on each spectrum. She can change her diet and exercise behavior in a day, but changes in menstrual symptoms may not be noticed for a month, and changes in bone mineral density will not be measurable for at least 6 months. This review describes each component of the Triad, and the neuroendocrine mechanisms linking them together. It then explains how the Triad originates in unwise diet and exercise behavior, and closes with recommendations for prevention and treatment.
Figure 1. The spectrums of the Female Athlete Triad. (From Nattiv et al., American College of Sports Medicine Position Stand: the female athlete triad. Medicine and Science in Sports and Exercise, 39(10), 1867-1882, 2007. Used with permission. Promotional and commercial use of the material in print, digital or mobile device format is prohibited without the permission from the publisher Lippincott Williams & Wilkins. Please contact journalpermissions@lww.com for further information) (Nattiv et al., 2007). Each component of the Triad spans a range from health to disease, with low energy availability, hypothalamic amenorrhea and osteoporosis at the pathological end of the spectrums. The spectrums are linked by endocrine mechanisms. The effect of low energy availability on reproductive health is mediated by luteinizing hormone (LH), which regulates ovarian and thereby menstrual function. The resulting indirect effect of low energy availability on skeletal health is mediated by estrogen, which regulates the rate at which old bone is resorbed by osteoclasts. Energy availability also affects skeletal health directly by means of its influence on insulin, tri-iodothyronine (T3) and insulin-like growth factor-1, which regulate the rate at which new bone is formed by osteoblasts. An athlete’s current and history of diet and exercise behavior determine where she is located, and which direction she is moving, on each spectrum.
Components of the Triad
Energy Availability.
The concept of energy availability derives from the recognition that mammals expend dietary energy in several basic physiological processes, including thermoregulation, cellular maintenance, immunity, growth, reproduction and locomotion (Loucks, 2013). The energy expended in one of these processes is not available for the others. Therefore, energy availability can be defined for athletes as the amount of dietary energy remaining after exercise training for all of the body’s other physiological processes. Energy availability determines how well those processes function.
By contrast, energy balance is the amount of energy added to or removed from the body’s energy stores after all the body’s physiological systems have done all of their work for the day. Energy balance determines whether you gain or lose weight. The brain responds to chronic, severe low energy availability by altering a wide spectrum of metabolic hormones that suppress diverse energy-consuming physiological processes (Laughlin & Yen, 1996; Loucks & Thuma, 2003). This tends to restore energy balance, but it is a pathological state of equilibrium in which infertility and skeletal demineralization are only part of the price paid to preserve life.
Some investigators have been skeptical of the diet records of female athletes, because comparisons of such records to estimations or measurements of energy expenditure have found apparently huge negative energy balances, some exceeding 4 MJ/d, in athletes with stable body weights(Edwards, Lindeman, Mikesky, & Stager, 1993; Wilmore et al., 1992). Such large discrepancies have been interpreted as indicating that female athletes grossly under-report their dietary intake, but few of these studies have included biochemical measurements to validate this interpretation. Under-reporting would not account for biochemical evidence of energy deficiency, and several studies characterizing reproductive disorders in female athletes (Laughlin & Yen, 1996; Laughlin & Yen, 1997; Loucks et al., 1992) have found metabolic substrates and hormones telling a consistent story of a decline in glucose utilization, mobilization of fat stores, and a slow metabolic rate, with more extreme abnormalities in amenorrheic athletes than in regularly menstruating athletes. So the available biochemical data clearly demonstrate that some female athletes are, indeed, energy deficient.
Menstrual Function.
Low energy availability impairs reproductive health by disrupting the pulsatile secretion of gonadotropin-releasing hormone by certain neurons in the hypothalamus. This, in turn, disrupts the pulsatile secretion of luteinizing hormone (LH) by the pituitary gland. Ovarian function critically depends not on the concentration of LH, but rather on the frequency of LH pulses (Tsutsumi & Webster, 2009)Athletes with menstrual disorders should not be assumed to have such functional hypothalamic menstrual disorders, because menstrual disorders can be symptoms of many medical conditions. Moreover, functional hypothalamic menstrual disorders can be caused by insufficient intestinal absorption (as in Celiac disease) as well as by insufficient dietary intake, and they can conceal underlying polycystic ovary disease(Sum & Warren, 2009). Therefore, to ensure that they receive appropriate care, athletes with menstrual disorders should be properly diagnosed through a series of hormone measurements and neuroendocrine stimulation tests(American, 2008). Obviously, menstrual disorders due to other causes are not effectively treated by increasing energy availability.
Clinical menstrual disorders such as amenorrhea (no cycles for 3 or more months) and oligomenorrhea (cycles longer than 35 days) can be identified by interviewing athletes, but athletes with subclinical menstrual disorders such as anovulation (no ovulation) and luteal phase deficiency (inadequate progesterone secretion) menstruate regularly and are unaware that they have a menstrual disorder. One study of regularly menstruating runners found that almost 80% of them had subclinical menstrual disorders in one or more of three consecutive menstrual cycles (De Souza et al., 1998). Subclinical menstrual disorders can only be detected by measuring sex steroid hormones during the luteal phase of the menstrual cycle.
Reproductive function has been disrupted in rodents by dietary restriction; by administering drugs that block the oxidation of glucose and fatty acids; by insulin administration, which diverts blood glucose into storage while inhibiting the mobilization of fat stores; and by cold exposure, which consumes large quantities of metabolic fuels in thermogenesis; as well as by physical activity, which consumes metabolic fuels in muscular contractions ( Wade & Jones, 2004; Wade & Schneider, 1992). The energy costs of systemic infections and major trauma probably have similar effects. In monkeys, amenorrhea has been induced by increasing their exercise energy expenditure without restricting their dietary energy intake (Williams, Caston-Balderrama, et al., 2001); and then their menstrual cycles have been restored by increasing their dietary energy intake without moderating their exercise regimen (Williams, Helmreich, Parfitt, Caston-Balderrama, & Cameron, 2001). In healthy young women, LH pulsatility has been disrupted by extreme dietary restriction alone (Loucks & Heath, 1994), by extreme exercise energy expenditure alone (Loucks, Verdun, & Heath, 1998) and by the combination of moderate amounts of both (Loucks & Thuma, 2003). LH pulsatility has also been preserved in strenuously exercising women by increasing their dietary energy intake in compensation for their exercise energy expenditure(Loucks et al., 1998).Thus, exercise has no suppressive effect on reproductive function apart from the impact of its energy cost on energy availability.
The dose-response effects of energy availability on LH pulsatility have also been determined in a prospective experiment (Loucks & Thuma, 2003). Healthy, regularly menstruating, habitually sedentary, young women expended 15 kcal*kgFFM-1*d-1 walking on a motorized treadmill at 70% VO2max. They completed this exercise in about 100 min each day for 5 days in 2 trials, separated by at least 2 months to allow for the effects of the first trial to be washed out before the second trial began. One trial was performed with an energy intake of 60 kcal*kgFFM-1*d-1 (250 kJ*kgFFM-1*d-1) and one with an energy intake of 45, 35 or 25 kcal*kgFFM-1*d-1 (188, 146 or 105 kJ*kgFFM-1*d-1) for net energy availabilities of 45 and either 30, 20 or 10 kcal*kgFFM-1*d-1 (125, 96 or 48 kJ*kgFFM-1*d-1). LH pulsatility was disrupted below a threshold of energy availability at 30 kcal*kgFFM-1*d-1 (125 kJ*kgFFM-1*d-1). This threshold of energy availability is similar to resting metabolic rate, whereas energy balance in a healthy adult occurs at 45 kcal*kgFFM-1*d-1 (188 kJ*kgFFM-1*d-1).
By contrast, reproductive function does not depend on the amount of energy stored in body fat, as was also once believed. Almost all observational studies of amenorrheic and eumenorrheic athletes have found them to span a common range of body size and composition (Redman & Loucks, 2005).Moreover, after gastric bypass surgery women become amenorrheic while they are still greatly overweight (e.g., body weight = 97 kg, BMI = 35 kg/m2) (Di Carlo et al., 1999).
Bone Mineral Density.
Low energy availability impairs skeletal health by uncoupling the turnover of bone in a manner that lowers bone mineral density over time (Christo et al., 2008; De Souza et al., 2008; Pollock et al., 2010). Like other tissues, bone is constantly turning over as osteoclast cells resorb old bone and osteoblast cells form new bone. By disrupting ovarian function, low energy availability lowers estrogen levels. This increases the rate of bone resorption by osteoclasts. Low energy availability also lowers the levels of insulin and tri-iodothyronine (T3), and thereby insulin-like growth factor-1 (IGF-1). This suppresses the rate of bone formation by osteoblasts. Peripheral signals of low energy availability, such as falling insulin, rising ghrelin, rising peptide YY (PYY) and falling leptin levels, also act centrally to activate neuropeptide Y (NPY) secreting neurons in the hypothalamus, which act via sympathetic pathways on osteoblastic Y1 receptors to repress osteoblast activity and bone formation (Shi & Baldock, 2012). Amenorrheic athletes display elevated ghrelin and PYY, also known as peptide tyrosine tyrosine, as well as lower leptin levels (Ackerman et al., 2012; Scheid, Williams, West, VanHeest, & De Souza, 2009).Conversely, when energy availability increases, NPY expression is reduced, osteoblast activity is increased, bone formation is stimulated, and the mass of both cortical and cancellous bone increases in a generalized manner throughout the skeleton (Shi & Baldock, 2012). In adults, a greater rate of bone resorption than formation causes a progressive loss of bone mass. In adolescence, such uncoupling of the rates of bone resorption and formation prevents girls from accruing as much bone mass as other girls(Barrack, Rauh, & Nichols, 2010), The resulting bone loss predisposes women to stress fractures(Goolsby, Barrack, & Nattiv, 2012; Okamoto, Arai, Hara, Tsuzihara, & Kubo, 2010; Popp et al., 2009), in the near term and to the premature onset of osteoporosis later in life.
The dose-response effects of energy availability on bone turnover have also been determined(Ihle & Loucks, 2004). (Ihle & Loucks, 2004). The rate of bone resorption increased when energy availability was low enough to reduce estradiol levels. The rate of bone protein synthesis, indicated by the plasma concentration of the bone formation marker Type I procollagen carboxy-terminal propeptide (PICP), was found to decline linearly with energy availability, as did insulin. Insulin stimulates osteoblast differentiation(Lu, Kraut, Gerstenfeld, & Graves, 2003). Meanwhile, the rate of bone mineralization, indicated by the plasma concentration of the bone formation marker osteocalcin, was found to decline non-linearly with energy availability, with most of the decline occurring between 20 and 30 kcal*kgFFM-1*d-1 (96 and 125 kJ*kgFFM-1*d-1), in parallel with the non-linear responses of IGF-1 and T3. Osteocalcin is the glue that binds bone mineral to bone protein. Its secretion is mediated by IGF-1, the hepatic production of which is stimulated by growth hormone and modulated by T3 (Wolf, Ingbar, & Moses, 1989).
Origins of Low Energy Availability
In athletes, low energy availability originates from three sources that we might describe as obsessive, intentional and inadvertent. The obsessive source is anorexia nervosa and other restrictive eating disorders; the intentional source is purposeful effort to reduce weight or body fat; and the inadvertent source is the suppression of appetite by diet and exercise. It is important to identify the origin of low energy availability in an athlete in order to understand how to develop a strategy for modifying her diet and exercise behavior to correct it.
Obsessive Low Energy Availability.
The prevalence of anorexia nervosa has been reported to be higher in “thin build” sports (dance, gymnastics, light-weight rowing, long distance running, diving and swimming) than other sports (Byrne & McLean, 2002). and even higher in “aesthetic” sports (i.e., gymnastics, dance, figure skating, aerobics, and diving) than other sports (12% vs 1%) (Sundgot-Borgen & Torstveit, 2004). The highest prevalence has been found in dance (17%-33%) (Brooks-Gunn, Warren, & Hamilton, 1987; Evers, 1987; Gadpaille, Sanborn, & Wagner, 1987; Holderness, Brooks-Gunn, & Warren, 1994) and ice skating (48%) (Rucinski, 1989).
Anorexia nervosa is a clinical mental illness, often accompanied by other mental illnesses (Klump, Bulik, Kaye, Treasure, & Tyson, 2009) requiring psychiatric treatment and sometimes even unwilling inpatient treatment with forced feeding (Carney, Tait, Richardson, & Touyz, 2008). Anorexia nervosa also has one of the highest risks of premature death of any mental illness (Harris & Barraclough, 1998) with a mortality 10 times higher than that of age and sex matched peers(Birmingham, Su, Hlynsky, Goldner, & Gao, 2005). Sixty percent of deaths in anorexia nervosa are due to medical consequences of the disease, for which the mortality risk is increased four times (Harris & Barraclough, 1998).The other 40% of deaths due to accident, misadventure, homicide, and suicide are increased 11 times, and the specific risk of suicide is increased 32 times(Harris & Barraclough, 1998).
Intentional Low Energy Availability.
Coaches should employ their knowledge and skills to help cooperative athletes to perfect their performance. Athletic Because the mortality of anorexia nervosa is so high, and because coaches, sports dietitians and team physicians are not trained to care for clinical mental illnesses, they should not be expected to manage them, and they should not attempt to do so. Instead, sports organizations should establish procedures for identifying athletes who may have anorexia nervosa, referring them for psychiatric evaluation and care, and excluding them from participation until they receive psychiatric clearance. Athletes who do not comply with recommendations to modify diet and exercise behavior to increase energy availability should be referred. Performance is improved, in part, by acquiring an optimum sport-specific (and, in team sports, position-specific) body size, body composition and mix of energy stores. For many female athletes, these objectives may include a reduction in fat mass. Therefore, many of these athletes will need to pursue diet and exercise regimens that reduce their energy availability. Because of the dependence of reproductive and skeletal health on energy availability, this will place their reproductive and skeletal health at risk. That risk should be acknowledged, understood, and carefully minimized through the cooperation of coaches and dietitians to manage energy availability so that athletes achieve their athletic potential without sacrificing their reproductive and skeletal health.
When athletes seek to reduce their weight or body fat, they reduce their energy availability by reducing their dietary energy intake or by increasing their exercise energy expenditure. Many female athletes do both, but athletes in aesthetic sports tend to emphasize dietary restriction, while high energy expenditure is inherent in endurance sports. In physically active women, the compounding of exercise energy expenditure with cognitive dietary restraint is associated with an increased frequency of menstrual disorders and low bone mineral density (Barrack, Rauh, Barkai, & Nichols, 2008; Vescovi, Scheid, Hontscharuk, & De Souza, 2008). Some poorly informed athletes may also practice disordered eating behaviors (e.g., skipping meals, fasting, vomiting and using laxatives) in impatient pursuit of potentially unhealthful objectives (Rauh, Nichols, & Barrack, 2010; Thein-Nissenbaum, Rauh, Carr, Loud, & McGuine, 2011). Coaches and dietitians should cooperate to help athletes to correct disordered eating behaviors, to set healthful objectives, and to pursue these objectives on a healthful schedule.
Inadvertent Low Energy Availability.
Athletes of both sexes are susceptible to unintended and unnoticed reductions in energy availability due to the suppression of appetite by diet and exercise (Loucks et al., 2011). This appetite suppression is possible even during training periods when weight or fat loss is not a training objective, and even among athletes who do not suffer from eating disorders or practice disordered eating behaviors. Despite extensive evidence that appetite is not a reliable indicator of energy requirements in either trained or untrained men and women, this problem is entirely neglected in the current joint position stand on sports nutrition of the American College of Sports Medicine, the American Dietetic Association, and Dietitians of Canada (Rodriguez, DiMarco, & Langley, 2009)
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008). Appetite is further suppressed by diets containing a high percentage (65%) of carbohydrates (Horvath, Eagen, Ryer-Calvin, & Pendergast, 2000; Stubbs et al., 2004). The unexpected and unintended consequence of such diets is that ad libitum carbohydrate intake (Horvath, Eagen, Ryer-Calvin, et al., 2000), and athletic performance (Horvath, Eagen, Fisher, Leddy, & Pendergast, 2000), can be lower than with a lower percentage carbohydrate diet. In endurance sports, appetite can be so suppressed that energy availability is reduced below 30 kcal*kgFFM-1*d-1 (125 kJ*kgFFM-1*d-1). Just as thirst is an unreliable indicator of water requirements, appetite is an unreliable indicator of energy requirements in endurance sports. Therefore, coaches should warn endurance athletes to eat not according to their appetites, but according to a plan with specified amounts of selected foods at scheduled times. Dietitians can develop eating plans to achieve target energy availabilities for specified exercise regimens.
Reasons for Focusing Attention on Female Athletes.
The physiological mechanisms linking the components of the Triad operate in men as well as women, but more women than men engage in diet and exercise behaviors that reduce energy availability. Coaches should keep in mind that before female athletes are athletes, they are female. Worldwide, about twice as many college women as college men at every decile of body mass index perceive themselves to be overweight (Wardle, Haase, & Steptoe, 2006). (Wardle, Haase, & Steptoe, 2006). The numbers of women and men actively trying to lose weight are even more disproportionate, and the disproportion increases as BMI declines. As a result, 5-9 times as many women as men in the three lowest deciles of BMI are actively trying to lose weight(Wardle et al., 2006). Indeed, more young female athletes report improvement of appearance than improvement of performance as a reason for dieting(Martinsen, Bratland-Sanda, Eriksson, & Sundgot-Borgen, 2010). This means that social issues may need to be addressed before female athletes will reform their diet and exercise behavior to increase energy availability.
Furthermore, although severe dietary restriction alone is sufficient to disrupt reproductive function, the more physically active a woman is, the less dietary restriction is required, and if she expends enough energy in exercise, she does not need to restrict her diet at all (Loucks et al., 1998). The health and longevity of experimental animals have been improved by restricting their energy intake by as much as 30% (Mattison, Lane, Roth, & Ingram, 2003), but restrictions of 40% have consistently caused both infertility (Holehan & Merry, 1985; McShane & Wise, 1996) and skeletal demineralization(Talbott, Rothkopf, & Shapses, 1998). (Talbott, Rothkopf, & Shapses, 1998). In exercising women, reproductive function begins to be suppressed when energy availability falls more than 33% (Loucks & Thuma, 2003), and amenorrheic athletes have been reported to practice diet and exercise regimens that reduce energy availability by as much as 65% (Loucks & Thuma, 2003)(Thong, McLean, & Graham, 2000).
Managing Energy Availability
Historically, dietitians have sought to assess the dietary energy needs of athletes by measuring their energy expenditure. In practice, an athlete’s total energy expenditure would be measured, or the athlete’s resting metabolic rate would be measured and multiplied by an activity factor to estimate her total energy expenditure. However, measures of energy expenditure convey no information about whether the functioning of physiological systems and, thereby, energy expenditure, have been suppressed by low energy availability. Therefore, the energy requirements of athletes cannot be determined by measuring their total energy expenditure or by measuring their resting metabolic rate and multiplying by an activity factor. In contrast, because energy availability measures only an athlete’s diet and exercise behavior, it is not confounded by the athlete’s physiological responses to that behavior. As the amount of dietary energy governing the function of physiological systems, energy availability is the quantity that athletes, trainers, coaches and sports dietitians need to know and manage.
Thus, the key behavior modification for preventing and treating the Triad is to keep energy availability above 30 kcal*kgFFM-1*d-1. Energy availability (EA) is determined by measuring dietary energy intake (EI), exercise energy expenditure (EEE), and fat free mass (FFM). Various inexpensive methods are available for making these measurements. Then:
EA = (EI – EEE)/FFM
(See the EA Calculation box.) Conversely, the EI required to achieve a target energy availability for any particular EEE can be determined by rearranging Equation 1:
EI = EEE + EA × FFM
Figure 2. Calculation of exercise energy expenditure (EEE). (A. Top) EEE is the amount of energy that a woman expends because she is an athlete, and does not include the energy she expends in resting metabolism and other waking activities. (B. Middle) Ergometers measure total energy expenditure during exercise (TEEE), which overestimates EEE by ~2 kcal*kgFFM-1*d-1 per hour of exercise. For high intensity exercise of short duration, the resulting error in calculating energy availability as EA = (EI – TEEE)/FFM is negligibly small for clinical purposes. (C. Bottom) For low intensity exercise of long duration, however, the error in EA = (EI – TEEE)/FFM is very large and will lead to unwarranted changes in diet and exercise behavior.
Having chosen EEE and EA to achieve the purposes of a particular period of training, the athlete should then consume the calculated EI. Coaches and dietitians should be aware that when EEE is large, as it is in endurance sports, consuming the EI necessary to achieve even EA > 30 kcal*kgFFM-1*d-1 (125 kJ*kgFFM-1*d-1) may require athletes to eat far beyond their appetites. Therefore, the willingness of an athlete to eat enough to protect her health may limit her EEE.
Coaches and dietitians should also be aware that EEE in Equations 1 and 2 is not the total energy expenditure during exercise that would be measured by an ergometer. Rather, it is the extra energy expenditure beyond the energy that the athlete would have expended if she had not exercised (See Figure 2 and the EEE Calculation box.). To determine EEE, energy expenditure in non-exercise activities (NEEE) during waking hours should be subtracted from total energy expenditure during exercise (TEEE):
EEE = TEEE - NEEE
Coaches and dietitians should be aware, too, that some devices measure the work done by an athlete rather than the amount of energy she expends; the latter is 4-5 times bigger due to the chemical-to-mechanical energy conversion efficiency of skeletal muscle being only 20% to 25%. Another caution is also warranted. Measurement errors in EI, EEE and FFM have different effects on the error in estimating EA. (See the Error Analysis box.) A few simple calculations with realistic values quickly reveal that the greatest efforts should be made to record EI accurately.
ABesides coaches and dietitians, parents, team physicians and sport-governing bodies all have roles to play for preventing and treating the Triad. Everyone will need to experiment with educational programs, training regimens, intervention strategies and rule changes to achieve this objective, and to publicize the results of their experiments to teach others the lessons learned. Different challenges will emerge in different sports, requiring different solutions. For example, the rule changes adopted by US collegiate men’s wrestling aim to prevent harmful weight-loss practices by controlling athlete behavior (NCAA, 2013).The associated procedures are intrusive, complicated, bureaucratic, time-consuming, labor-intensive and expensive. By contrast, the rules adopted by international ski-jumping aim to achieve the same objective by reducing the competitive incentive for athletes to engage in harmful weight loss behavior, and are elegantly simple (Muller, Groschl, Muller, & Sudi, 2006). Experience will teach whether initial reforms need further refinement(Muller, 2009; Oggiano & Saetran, 2008).
Conclusion
To prevent the Triad, female athletes should seek to improve their athletic performance by managing energy availability in a periodized training program that aims to achieve interim goals on the way to long-term objectives. The goals for some periods will call for energy availability to be raised and others will call for it to be lowered, but there is a floor below which it cannot be reduced without impairing reproductive and skeletal health. The first aim of treatment for the Triad is to increase energy availability. This requires an understanding of the origins of low energy availability affecting particular athletes. Inexpensive commercial devices are available for facilitating the management of energy availability, and guidelines are offered here for achieving that objective.
References
Ackerman, K. E., Slusarz, K., Guereca, G., Pierce, L., Slattery, M., Mendes, N., . . . Misra, M. (January, 2012). Higher Ghrelin and Lower Leptin Secretion is Associated with Lower LH Secretion in Young Amenorrheic Athletes Compared with Eumenorrheic Athletes and Controls. American Journal of Physiology Endocrinology and Metablism, 302, E800-E806. doi: 10.1152/ajpendo.00598.2011 Ir a artículo: http://ajpendo.physiology.org/content/ajpendo/302/7/E800.full.pdf
Peripheral signals of low energy availability, such as falling insulin, rising ghrelin, rising peptide YY (PYY) and falling leptin levels, also act centrally to activate neuropeptide Y (NPY) secreting neurons in the hypothalamus, which act via sympathetic pathways on osteoblastic Y1 receptors to repress osteoblast activity and bone formation (Shi & Baldock, 2012). Amenorrheic athletes display elevated ghrelin and PYY, also known as peptide tyrosine tyrosine, as well as lower leptin levels (Ackerman et al., 2012; Scheid, Williams, West, VanHeest, & De Souza, 2009).
American Society of Reproductive Medicine Practice Committee. (November, 2008). Current evaluation of amenorrhea. Fertility and Sterility, 90(5 Suppl 3), S219-S225. doi: 10.1016/j.fertnstert.2008.08.038 Ir a artículo: http://www.sciencedirect.com/science/article/pii/S0015028208035279
Low energy availability impairs reproductive health by disrupting the pulsatile secretion of gonadotropin-releasing hormone by certain neurons in the hypothalamus. This, in turn, disrupts the pulsatile secretion of luteinizing hormone (LH) by the pituitary gland. Ovarian function critically depends not on the concentration of LH, but rather on the frequency of LH pulses (Tsutsumi & Webster, 2009)Athletes with menstrual disorders should not be assumed to have such functional hypothalamic menstrual disorders, because menstrual disorders can be symptoms of many medical conditions. Moreover, functional hypothalamic menstrual disorders can be caused by insufficient intestinal absorption (as in Celiac disease) as well as by insufficient dietary intake, and they can conceal underlying polycystic ovary disease(Sum & Warren, 2009). Therefore, to ensure that they receive appropriate care, athletes with menstrual disorders should be properly diagnosed through a series of hormone measurements and neuroendocrine stimulation tests(American, 2008).
Ballard, T. P., Melby, C. L., Camus, H., Cianciulli, M., Pitts, J., Schmidt, S., & Hickey, M. S. (August, 2009). Effect of resistance exercise, with or without carbohydrate supplementation, on plasma ghrelin concentrations and postexercise hunger and food intake. Metabolism, 58(8), 1191-1199. doi: 10.1016/j.metabol.2009.03.018 Ir a artículo: http://www.sciencedirect.com/science/article/pii/S0026049509001280
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008). Appetite is further suppressed by diets containing a high percentage (65%) of carbohydrates (Horvath, Eagen, Ryer-Calvin, & Pendergast, 2000; Stubbs et al., 2004).
Barrack, M. T., Rauh, M. J., Barkai, H. S., & Nichols, J. F. (2008). Dietary restraint and low bone mass in female adolescent endurance runners. The American Journal of Clinical Nutrition, 87(1), 36-43. Ir a artículo: http://ajcn.nutrition.org/content/87/1/36.abstract
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008). Appetite is further suppressed by diets containing a high percentage (65%) of carbohydrates (Horvath, Eagen, Ryer-Calvin, & Pendergast, 2000; Stubbs et al., 2004).In adults, a greater rate of bone resorption than formation causes a progressive loss of bone mass. In adolescence, such uncoupling of the rates of bone resorption and formation prevents girls from accruing as much bone mass as other girls(Barrack, Rauh, & Nichols, 2010), The resulting bone loss predisposes women to stress fractures(Goolsby, Barrack, & Nattiv, 2012; Okamoto, Arai, Hara, Tsuzihara, & Kubo, 2010; Popp et al., 2009), in the near term and to the premature onset of osteoporosis later in life.
Barrack, M. T., Rauh, M. J., & Nichols, J. F. (August, 2010). Cross-sectional evidence of suppressed bone mineral accrual among female adolescent runners. Journal of Bone and Mineral Research, 25(8), 1850-1857. doi: 10.1002/jbmr.63 Available from: http://onlinelibrary.wiley.com/doi/10.1002/jbmr.63/abstract
Bergouignan, A., Momken, I., Schoeller, D. A., Normand, S., Zahariev, A., Lescure, B., . . . Blanc, S. (March, 2010). Regulation of Energy Balance during Long-Term Physical Inactivity Induced by Bed Rest with and without Exercise Training. The Journal of Clinical Endocrinology & Metabolism, 95(3), 1045-1053. doi: http://dx.doi.org/10.1210/jc.2009-1005
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008). Appetite is further suppressed by diets containing a high percentage (65%) of carbohydrates (Horvath, Eagen, Ryer-Calvin, & Pendergast, 2000; Stubbs et al., 2004).
Birmingham, C. L., Su, J., Hlynsky, J. A., Goldner, E. M., & Gao, M. (September, 2005). The mortality rate from anorexia nervosa. International Journal of Eating Disorders, 38(2), 143-146. doi: 10.1002/eat.20164 Available from: http://onlinelibrary.wiley.com/doi/10.1002/eat.20164/abstract?deniedAccessCustomisedMessage=&userIsAuthenticated=false
Borer, K. T. (July, 2010). Nonhomeostatic Control of Human Appetite and Physical Activity in Regulation of Energy Balance. Exercise and Sports Science Reviews, 38(3), 114-121. doi: 10.1097/JES.0b013e3181e3728f Ir a artículo: http://journals.lww.com/acsm-essr/Abstract/2010/07000/Nonhomeostatic_Control_of_Human_Appetite_and.4.aspx
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008). Appetite is further suppressed by diets containing a high percentage (65%) of carbohydrates (Horvath, Eagen, Ryer-Calvin, & Pendergast, 2000; Stubbs et al., 2004).
Brooks-Gunn, J., Warren, M. P., & Hamilton, L. H. (February, 1987). The relation of eating problems and amenorrhea in ballet dancers. Medicine and Science in Sports and Exercise, 19(1), 41-44. Ir a artículo: http://journals.lww.com/acsm-msse/Abstract/1987/02000/The_relation_of_eating_problems_and_amenorrhea_in.9.aspx
The prevalence of anorexia nervosa has been reported to be higher in “thin build” sports (dance, gymnastics, light-weight rowing, long distance running, diving and swimming) than other sports (Byrne & McLean, 2002). and even higher in “aesthetic” sports (i.e., gymnastics, dance, figure skating, aerobics, and diving) than other sports (12% vs 1%) (Sundgot-Borgen & Torstveit, 2004). The highest prevalence has been found in dance (17%-33%) (Brooks-Gunn, Warren, & Hamilton, 1987; Evers, 1987; Gadpaille, Sanborn, & Wagner, 1987; Holderness, Brooks-Gunn, & Warren, 1994) and ice skating (48%) (Rucinski, 1989).
Byrne, S., & McLean, N. (June, 2002). Elite athletes: effects of the pressure to be thin. Journal of Science and Medicine in Sport, 5(2), 80-94. Ir a artículo: http://www.jsams.org/article/S1440-2440%2802%2980029-9/abstract
The prevalence of anorexia nervosa has been reported to be higher in “thin build” sports (dance, gymnastics, light-weight rowing, long distance running, diving and swimming) than other sports (Byrne & McLean, 2002). and even higher in “aesthetic” sports (i.e., gymnastics, dance, figure skating, aerobics, and diving) than other sports (12% vs 1%) (Sundgot-Borgen & Torstveit, 2004). The highest prevalence has been found in dance (17%-33%) (Brooks-Gunn, Warren, & Hamilton, 1987; Evers, 1987; Gadpaille, Sanborn, & Wagner, 1987; Holderness, Brooks-Gunn, & Warren, 1994) and ice skating (48%) (Rucinski, 1989).
Carney, T., Tait, D., Richardson, A., & Touyz, S. (may-june, 2008). Why (and when) clinicians compel treatment of anorexia nervosa patients. European Eating Disorders Review, 16(3), 199-206. doi: 10.1002/erv.845 Ir a artículo: http://onlinelibrary.wiley.com/doi/10.1002/erv.845/abstract
Anorexia nervosa is a clinical mental illness, often accompanied by other mental illnesses (Klump, Bulik, Kaye, Treasure, & Tyson, 2009) requiring psychiatric treatment and sometimes even unwilling inpatient treatment with forced feeding (Carney, Tait, Richardson, & Touyz, 2008). Anorexia nervosa also has one of the highest risks of premature death of any mental illness (Harris & Barraclough, 1998) with a mortality 10 times higher than that of age and sex matched peers(Birmingham, Su, Hlynsky, Goldner, & Gao, 2005). Sixty percent of deaths in anorexia nervosa are due to medical consequences of the disease, for which the mortality risk is increased four times (Harris & Barraclough, 1998).The other 40% of deaths due to accident, misadventure, homicide, and suicide are increased 11 times, and the specific risk of suicide is increased 32 times(Harris & Barraclough, 1998).
Christo, K., Prabhakaran, R., Lamparello, B., Cord, J. Miller, K. K., Goldstein, M. A., . . . Misra, M. (June, 2008). Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics, 121(6), 1127-1136. doi: 10.1542/peds.2007-2392 Ir a artículo: http://pediatrics.aappublications.org/content/121/6/1127.full?sid=260386d9-2e70-469e-bd2a-73e7959f1221
Low energy availability impairs skeletal health by uncoupling the turnover of bone in a manner that lowers bone mineral density over time (Christo et al., 2008; De Souza et al., 2008; Pollock et al., 2010). Like other tissues, bone is constantly turning over as osteoclast cells resorb old bone and osteoblast cells form new bone. By disrupting ovarian function, low energy availability lowers estrogen levels. This increases the rate of bone resorption by osteoclasts. Low energy availability also lowers the levels of insulin and tri-iodothyronine (T3), and thereby insulin-like growth factor-1 (IGF-1). This suppresses the rate of bone formation by osteoblasts.
De Souza, M. J., Miller, B. E., Loucks, A. B., Luciano, A. A., Pescatello, L. S., Campbell, C. G., & Lasley, B. L. (1998). High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. Journal of Clinical Endocrinology and Metabolism, 83(12), 4220-4232. doi: http://dx.doi.org/10.1210/jcem.83.12.5334 Ir a artículo: http://press.endocrine.org/doi/full/10.1210/jcem.83.12.5334?queryID=20%2F123796
Clinical menstrual disorders such as amenorrhea (no cycles for 3 or more months) and oligomenorrhea (cycles longer than 35 days) can be identified by interviewing athletes, but athletes with subclinical menstrual disorders such as anovulation (no ovulation) and luteal phase deficiency (inadequate progesterone secretion) menstruate regularly and are unaware that they have a menstrual disorder. One study of regularly menstruating runners found that almost 80% of them had subclinical menstrual disorders in one or more of three consecutive menstrual cycles (De Souza et al., 1998).
De Souza, M. J., West, S. L., Jamal, S. A., Hawker, G. A., Gundberg, C. M., & Williams, N. I. (July, 2008). The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone, 43(1), 140-148. doi: http://dx.doi.org/10.1016/j.bone.2008.03.013 Ir a artículo: http://www.thebonejournal.com/article/S8756-3282%2808%2900166-X/abstract?cc=y=?cc=y=
Low energy availability impairs skeletal health by uncoupling the turnover of bone in a manner that lowers bone mineral density over time (Christo et al., 2008; De Souza et al., 2008; Pollock et al., 2010). Like other tissues, bone is constantly turning over as osteoclast cells resorb old bone and osteoblast cells form new bone. By disrupting ovarian function, low energy availability lowers estrogen levels.
Di Carlo, C., Palomba, S., De Fazio, M., Gianturco, M., Armellino, M., & Nappi, C. (November, 1999). Hypogonadotropic hypogonadotropism in obese women after biliopancreatic diversion. Fertility and Sterility, 72(5), 905-909. doi: http://dx.doi.org/10.1016/S0015-0282(99)00358-1 Ir a artículo: http://www.fertstert.org/article/S0015-0282%2899%2900358-1/abstract
By contrast, reproductive function does not depend on the amount of energy stored in body fat, as was also once believed. Almost all observational studies of amenorrheic and eumenorrheic athletes have found them to span a common range of body size and composition (Redman & Loucks, 2005).Moreover, after gastric bypass surgery women become amenorrheic while they are still greatly overweight (e.g., body weight = 97 kg, BMI = 35 kg/m2) (Di Carlo et al., 1999).
Edwards, J. E., Lindeman, A. K., Mikesky, A. E., & Stager, J. M. (December, 1993). Energy balance in highly trained female endurance runners. Medicine and Science in Sports and Exercise, 25(12), 1398-1404. Ir a artículo: http://journals.lww.com/acsm-msse/Abstract/1993/12000/Energy_balance_in_highly_trained_female_endurance.14.aspx
Some investigators have been skeptical of the diet records of female athletes, because comparisons of such records to estimations or measurements of energy expenditure have found apparently huge negative energy balances, some exceeding 4 MJ/d, in athletes with stable body weights(Edwards, Lindeman, Mikesky, & Stager, 1993; Wilmore et al., 1992).
Evers, C. (1987). Dietary intake and symptoms of anorexia nervosa in female university dancers. Journal of the American Dietetic Association, 87(1), 66-68.
The prevalence of anorexia nervosa has been reported to be higher in “thin build” sports (dance, gymnastics, light-weight rowing, long distance running, diving and swimming) than other sports (Byrne & McLean, 2002). and even higher in “aesthetic” sports (i.e., gymnastics, dance, figure skating, aerobics, and diving) than other sports (12% vs 1%) (Sundgot-Borgen & Torstveit, 2004). The highest prevalence has been found in dance (17%-33%) (Brooks-Gunn, Warren, & Hamilton, 1987; Evers, 1987; Gadpaille, Sanborn, & Wagner, 1987; Holderness, Brooks-Gunn, & Warren, 1994) and ice skating (48%) (Rucinski, 1989).
Gadpaille, W. J., Sanborn, C. F., & Wagner, W. W., Jr. (July, 1987). Athletic amenorrhea, major affective disorders, and eating disorders. The American Journal of Psychiatry, 144(7), 939-942. Ir a artículo http://ajp.psychiatryonline.org/article.aspx?articleid=164343
The prevalence of anorexia nervosa has been reported to be higher in “thin build” sports (dance, gymnastics, light-weight rowing, long distance running, diving and swimming) than other sports (Byrne & McLean, 2002). and even higher in “aesthetic” sports (i.e., gymnastics, dance, figure skating, aerobics, and diving) than other sports (12% vs 1%) (Sundgot-Borgen & Torstveit, 2004). The highest prevalence has been found in dance (17%-33%) (Brooks-Gunn, Warren, & Hamilton, 1987; Evers, 1987; Gadpaille, Sanborn, & Wagner, 1987; Holderness, Brooks-Gunn, & Warren, 1994) and ice skating (48%) (Rucinski, 1989).
Goolsby, M. A., Barrack, M. T., & Nattiv, A. (2012). A displaced femoral neck fracture in an amenorrheic adolescent female runner. Sports Health, 4(4), 352-356. doi: 10.1177/1941738111429929 Ir a artículo http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3435922/
In adults, a greater rate of bone resorption than formation causes a progressive loss of bone mass. In adolescence, such uncoupling of the rates of bone resorption and formation prevents girls from accruing as much bone mass as other girls(Barrack, Rauh, & Nichols, 2010), The resulting bone loss predisposes women to stress fractures(Goolsby, Barrack, & Nattiv, 2012; Okamoto, Arai, Hara, Tsuzihara, & Kubo, 2010; Popp et al., 2009), in the near term and to the premature onset of osteoporosis later in life.
Harris, E. C., & Barraclough, B. (1998). Excess mortality of mental disorder. British Journal of Psychiatry, 173(1), 11-53. doi: 10.1192/bjp.173.1.11 Ir a artículo http://bjp.rcpsych.org/content/173/1/11.abstract
Anorexia nervosa is a clinical mental illness, often accompanied by other mental illnesses (Klump, Bulik, Kaye, Treasure, & Tyson, 2009) requiring psychiatric treatment and sometimes even unwilling inpatient treatment with forced feeding (Carney, Tait, Richardson, & Touyz, 2008). Anorexia nervosa also has one of the highest risks of premature death of any mental illness (Harris & Barraclough, 1998) with a mortality 10 times higher than that of age and sex matched peers(Birmingham, Su, Hlynsky, Goldner, & Gao, 2005). Sixty percent of deaths in anorexia nervosa are due to medical consequences of the disease, for which the mortality risk is increased four times (Harris & Barraclough, 1998).The other 40% of deaths due to accident, misadventure, homicide, and suicide are increased 11 times, and the specific risk of suicide is increased 32 times(Harris & Barraclough, 1998).
Holderness, C. C., Brooks-Gunn, J., & Warren, M. P. (March, 1994). Eating disorders and substance use: a dancing vs a nondancing population. Medicine and Science in Sports and Exercise, 26(3), 297-302. Ir a artículo: http://journals.lww.com/acsm-msse/Abstract/1994/03000/Eating_disorders_and_substance_use__a_dancing_vs_a.5.aspx
The prevalence of anorexia nervosa has been reported to be higher in “thin build” sports (dance, gymnastics, light-weight rowing, long distance running, diving and swimming) than other sports (Byrne & McLean, 2002). and even higher in “aesthetic” sports (i.e., gymnastics, dance, figure skating, aerobics, and diving) than other sports (12% vs 1%) (Sundgot-Borgen & Torstveit, 2004). The highest prevalence has been found in dance (17%-33%) (Brooks-Gunn, Warren, & Hamilton, 1987; Evers, 1987; Gadpaille, Sanborn, & Wagner, 1987; Holderness, Brooks-Gunn, & Warren, 1994) and ice skating (48%) (Rucinski, 1989).
Holehan, A. M., & Merry, B. J. (1985). The control of puberty in the dietary restricted female rat. Mechanisms of Ageing and Development, 32(2-3), 179-191. doi: 10.1016/0047-6374(85)90078-8 Ir a artículo: http://www.sciencedirect.com/science/article/pii/0047637485900788
Furthermore, although severe dietary restriction alone is sufficient to disrupt reproductive function, the more physically active a woman is, the less dietary restriction is required, and if she expends enough energy in exercise, she does not need to restrict her diet at all (Loucks et al., 1998). The health and longevity of experimental animals have been improved by restricting their energy intake by as much as 30% (Mattison, Lane, Roth, & Ingram, 2003), but restrictions of 40% have consistently caused both infertility (Holehan & Merry, 1985; McShane & Wise, 1996) and skeletal demineralization(Talbott, Rothkopf, & Shapses, 1998). (Talbott, Rothkopf, & Shapses, 1998). In exercising women, reproductive function begins to be suppressed when energy availability falls more than 33% (Loucks & Thuma, 2003), and amenorrheic athletes have been reported to practice diet and exercise regimens that reduce energy availability by as much as 65% (Loucks & Thuma, 2003)(Thong, McLean, & Graham, 2000).
Horvath, P. J., Eagen, C. K., Ryer-Calvin, S. D., & Pendergast, D. R. (2000). The effects of varying dietary fat on the nutrient intake in male and female runners. Journal of the American College of Nutrition, 19(1), 42-51. doi: 10.1080/07315724.2000.10718913 Ir a artículo: http://www.tandfonline.com/doi/full/10.1080/07315724.2000.10718913#.U62P_JR5On8
The unexpected and unintended consequence of such diets is that ad libitum carbohydrate intake (Horvath, Eagen, Ryer-Calvin, et al., 2000), and athletic performance (Horvath, Eagen, Fisher, Leddy, & Pendergast, 2000), can be lower than with a lower percentage carbohydrate diet. In endurance sports, appetite can be so suppressed that energy availability is reduced below 30 kcal*kgFFM-1*d-1 (125 kJ*kgFFM-1*d-1). Just as thirst is an unreliable indicator of water requirements, appetite is an unreliable indicator of energy requirements in endurance sports. Therefore, coaches should warn endurance athletes to eat not according to their appetites, but according to a plan with specified amounts of selected foods at scheduled times. Dietitians can develop eating plans to achieve target energy availabilities for specified exercise regimens.
Horvath, P. J., Eagen, C. K., Ryer-Calvin, S. D., & Pendergast, D. R. (2000). The effects of varying dietary fat on the nutrient intake in male and female runners. Journal of the American College of Nutrition, 19(1), 42-51. doi: 10.1080/07315724.2000.10718913 Ir a artículo: http://www.tandfonline.com/doi/full/10.1080/07315724.2000.10718913#.U62P_JR5On8
The unexpected and unintended consequence of such diets is that ad libitum carbohydrate intake (Horvath, Eagen, Ryer-Calvin, et al., 2000), and athletic performance (Horvath, Eagen, Fisher, Leddy, & Pendergast, 2000), can be lower than with a lower percentage carbohydrate diet. In endurance sports, appetite can be so suppressed that energy availability is reduced below 30 kcal*kgFFM-1*d-1 (125 kJ*kgFFM-1*d-1). Just as thirst is an unreliable indicator of water requirements, appetite is an unreliable indicator of energy requirements in endurance sports. Therefore, coaches should warn endurance athletes to eat not according to their appetites, but according to a plan with specified amounts of selected foods at scheduled times. Dietitians can develop eating plans to achieve target energy availabilities for specified exercise regimens.
Ihle, R., & Loucks, A. B. (2004). Dose-response relationships between energy availability and bone turnover in young exercising women. Journal of Bone and Mineral Research, 19(8), 1231-1240. doi: 10.1359/JBMR.040410 Ir a artículo: http://onlinelibrary.wiley.com/doi/10.1359/JBMR.040410/abstract
The dose-response effects of energy availability on bone turnover have also been determined(Ihle & Loucks, 2004). (Ihle & Loucks, 2004). The rate of bone resorption increased when energy availability was low enough to reduce estradiol levels. The rate of bone protein synthesis, indicated by the plasma concentration of the bone formation marker Type I procollagen carboxy-terminal propeptide (PICP), was found to decline linearly with energy availability, as did insulin. Insulin stimulates osteoblast differentiation(Lu, Kraut, Gerstenfeld, & Graves, 2003).
King, J. A., Miyashita, M., Wasse, L. K., & Stensel, D. J. (June, 2010). Influence of prolonged treadmill running on appetite, energy intake and circulating concentrations of acylated ghrelin. doi: 10.1016/j.appet.2010.02.002 Appetite, 54(3), 492-498. Ir a artículo: http://www.sciencedirect.com/science/article/pii/S0195666310000449
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008).
King, N. A., Caudwell, P. P., Hopkins, M., Stubbs, J. R., Naslund, E., & Blundell, J. E. (2009). Dual-process action of exercise on appetite control: increase in orexigenic drive but improvement in meal-induced satiety. The American Journal of Clinical Nutrition, 90(4), 921-927. doi: 10.3945/ajcn.2009.27706 Ir a artículo: http://ajcn.nutrition.org/content/90/4/921.full?sid=a2b7a313-afc6-4464-9e54-b06ddb539d81
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008). Appetite is further suppressed by diets containing a high percentage (65%) of carbohydrates (Horvath, Eagen, Ryer-Calvin, & Pendergast, 2000; Stubbs et al., 2004).
King, N. A., Hopkins, M., Caudwell, P., Stubbs, R. J., & Blundell, J. E. (2008). Individual variability following 12 weeks of supervised exercise: identification and characterization of compensation for exercise-induced weight loss. International Journal of Obesity, 32(1), 177-184. doi:10.1038/sj.ijo.0803712 Ir a artículo: http://www.nature.com/ijo/journal/v32/n1/full/0803712a.html
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008). Appetite is further suppressed by diets containing a high percentage (65%) of carbohydrates (Horvath, Eagen, Ryer-Calvin, & Pendergast, 2000; Stubbs et al., 2004). The unexpected and unintended consequence of such diets is that ad libitum carbohydrate intake (Horvath, Eagen, Ryer-Calvin, et al., 2000), and athletic performance (Horvath, Eagen, Fisher, Leddy, & Pendergast, 2000), can be lower than with a lower percentage carbohydrate diet. In endurance sports, appetite can be so suppressed that energy availability is reduced below 30 kcal*kgFFM-1*d-1 (125 kJ*kgFFM-1*d-1). Just as thirst is an unreliable indicator of water requirements, appetite is an unreliable indicator of energy requirements in endurance sports.
Klump, K. L., Bulik, C. M., Kaye, W. H., Treasure, J., & Tyson, E. (March, 2009). Academy for eating disorders position paper: Eating disorders are serious mental illnesses. International Journal of Eating Disorders, 42(2), 97-103. doi: 10.1002/eat.20589 Ir a artículo: http://onlinelibrary.wiley.com/doi/10.1002/eat.20589/abstract
Anorexia nervosa is a clinical mental illness, often accompanied by other mental illnesses (Klump, Bulik, Kaye, Treasure, & Tyson, 2009) requiring psychiatric treatment and sometimes even unwilling inpatient treatment with forced feeding (Carney, Tait, Richardson, & Touyz, 2008).
Laughlin, G. A., & Yen, S. S. C. (1996). Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. The Journal of Clinical Endocrinology and Metabolism, 81(12), 4301-4309. doi: http://dx.doi.org/10.1210/jcem.81.12.8954031 Ir a artículo: http://press.endocrine.org/doi/abs/10.1210/jcem.81.12.8954031
By contrast, energy balance is the amount of energy added to or removed from the body’s energy stores after all the body’s physiological systems have done all of their work for the day. Energy balance determines whether you gain or lose weight. The brain responds to chronic, severe low energy availability by altering a wide spectrum of metabolic hormones that suppress diverse energy-consuming physiological processes (Laughlin & Yen, 1996; Loucks & Thuma, 2003).
Under-reporting would not account for biochemical evidence of energy deficiency, and several studies characterizing reproductive disorders in female athletes (Laughlin & Yen, 1996; Laughlin & Yen, 1997; Loucks et al., 1992) have found metabolic substrates and hormones telling a consistent story of a decline in glucose utilization, mobilization of fat stores, and a slow metabolic rate, with more extreme abnormalities in amenorrheic athletes than in regularly menstruating athletes. So the available biochemical data clearly demonstrate that some female athletes are, indeed, energy deficient.
Laughlin, G. A., & Yen, S. S. C. (1997). Hypoleptinemia in women athletes: absence of a diurnal rhythm with amenorrhea. Journal of Clinical Endocrinology and Metabolism, 82(1), 318-321. Ir a artículo: http://press.endocrine.org/doi/abs/10.1210/jcem.82.1.3840
Under-reporting would not account for biochemical evidence of energy deficiency, and several studies characterizing reproductive disorders in female athletes (Laughlin & Yen, 1996; Laughlin & Yen, 1997; Loucks et al., 1992) have found metabolic substrates and hormones telling a consistent story of a decline in glucose utilization, mobilization of fat stores, and a slow metabolic rate, with more extreme abnormalities in amenorrheic athletes than in regularly menstruating athletes. So the available biochemical data clearly demonstrate that some female athletes are, indeed, energy deficient.
Loucks, A. B. (2011). The Endocrine System: Integrated Influences on Metabolism, Growth, and Reproduction. In P. A. Farrell, M. J. Joyner & V. J. Caiozzo (Eds.), ACSM's Advanced Exercise Physiology (Second ed., pp. 466-506). Philadelphia: Wolters Kluwer. . Ir a libro: http://www.acsmstore.org/ProductDetails.asp?ProductCode=9780781797801
All girls and women are encouraged to participate in physical activities and sports, because the benefits of participation far outweigh the risks (Nattiv, Loucks, Manore, Sundgot-Borgen, & Warren, 2007). One of those risks is the Female Athlete Triad, in which reproductive and skeletal health are impaired by energy deficiency (Loucks, 2011; Loucks, Kiens, & Wright, 2011).
Loucks, A. B. (2013). Energy Balance and Energy Availability. In R. J. Maughan (Ed.), The Encyclopaedia of Sports Medicine: An IOC Medical Commission Publication, Sports Nutrition (pp. 72-87). U.S.A.: Wiley-Blackwell. Ir a http://www.wiley.com/WileyCDA/WileyTitle/productCd-1118692357.html
The concept of energy availability derives from the recognition that mammals expend dietary energy in several basic physiological processes, including thermoregulation, cellular maintenance, immunity, growth, reproduction and locomotion (Loucks, 2013).
Loucks, A. B., & Heath, E. M. (April, 1994). Dietary restriction reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young menstruating women. The Journal of Clinical Endocrinology and Metabolism, 78(4), 910-915. Ir a artículo http://press.endocrine.org/doi/abs/10.1210/jcem.78.4.8157720
In healthy young women, LH pulsatility has been disrupted by extreme dietary restriction alone (Loucks & Heath, 1994), by extreme exercise energy expenditure alone (Loucks, Verdun, & Heath, 1998) and by the combination of moderate amounts of both (Loucks & Thuma, 2003). LH pulsatility has also been preserved in strenuously exercising women by increasing their dietary energy intake in compensation for their exercise energy expenditure(Loucks et al., 1998).Thus, exercise has no suppressive effect on reproductive function apart from the impact of its energy cost on energy availability.
Energy balance determines whether you gain or lose weight. The brain responds to chronic, severe low energy availability by altering a wide spectrum of metabolic hormones that suppress diverse energy-consuming physiological processes (Laughlin & Yen, 1996; Loucks & Thuma, 2003). This tends to restore energy balance, but it is a pathological state of equilibrium in which infertility and skeletal demineralization are only part of the price paid to preserve life.
Loucks, A. B., Kiens, B., & Wright, H. H. (August, 2011). Energy availability in athletes. Journal of Sports Sciences, (S1), S7-S15. doi: 10.1080/02640414.2011.588958 Ir a artículo: http://www.tandfonline.com/doi/full/10.1080/02640414.2011.588958#.U63U_JR5MYk
Athletes of both sexes are susceptible to unintended and unnoticed reductions in energy availability due to the suppression of appetite by diet and exercise (Loucks et al., 2011).
Loucks, A. B., Laughlin, G. A., Mortola, J. F., Girton, L., Nelson, J. C., & Yen, S. S. (1992). Hypothalamic-pituitary-thyroidal function in eumenorrheic and amenorrheic athletes. The Journal of Clinical Endocrinology and Metabolism, 75(2), 514-518. doi: http://dx.doi.org/10.1210/jcem.75.2.1639953. Ir a artículo: http://press.endocrine.org/doi/abs/10.1210/jcem.75.2.1639953
Such large discrepancies have been interpreted as indicating that female athletes grossly under-report their dietary intake, but few of these studies have included biochemical measurements to validate this interpretation. Under-reporting would not account for biochemical evidence of energy deficiency, and several studies characterizing reproductive disorders in female athletes (Laughlin & Yen, 1996; Laughlin & Yen, 1997; Loucks et al., 1992) have found metabolic substrates and hormones telling a consistent story of a decline in glucose utilization, mobilization of fat stores, and a slow metabolic rate, with more extreme abnormalities in amenorrheic athletes than in regularly menstruating athletes. So the available biochemical data clearly demonstrate that some female athletes are, indeed, energy deficient.
Loucks, A. B., & Thuma, J. R. (January, 2003). Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. The Journal of Clinical Endocrinology and Metabolism, 88(1), 297-311. . Ir a artículo: http://press.endocrine.org/doi/abs/10.1210/jc.2002-020369
In healthy young women, LH pulsatility has been disrupted by extreme dietary restriction alone (Loucks & Heath, 1994), by extreme exercise energy expenditure alone (Loucks, Verdun, & Heath, 1998) and by the combination of moderate amounts of both (Loucks & Thuma, 2003). LH pulsatility has also been preserved in strenuously exercising women by increasing their dietary energy intake in compensation for their exercise energy expenditure(Loucks et al., 1998).Thus, exercise has no suppressive effect on reproductive function apart from the impact of its energy cost on energy availability.
The dose-response effects of energy availability on LH pulsatility have also been determined in a prospective experiment (Loucks & Thuma, 2003).
Furthermore, although severe dietary restriction alone is sufficient to disrupt reproductive function, the more physically active a woman is, the less dietary restriction is required, and if she expends enough energy in exercise, she does not need to restrict her diet at all (Loucks et al., 1998).
Loucks, A. B., Verdun, M., & Heath, E. M. (1998). Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. Journal of Applied Physiology, 84(1), 37-46. Ir a artículo: http://jap.physiology.org/content/84/1/37
In healthy young women, LH pulsatility has been disrupted by extreme dietary restriction alone (Loucks & Heath, 1994), by extreme exercise energy expenditure alone (Loucks, Verdun, & Heath, 1998) and by the combination of moderate amounts of both (Loucks & Thuma, 2003). LH pulsatility has also been preserved in strenuously exercising women by increasing their dietary energy intake in compensation for their exercise energy expenditure(Loucks et al., 1998).
In exercising women, reproductive function begins to be suppressed when energy availability falls more than 33% (Loucks & Thuma, 2003), and amenorrheic athletes have been reported to practice diet and exercise regimens that reduce energy availability by as much as 65% (Loucks & Thuma, 2003)(Thong, McLean, & Graham, 2000).
Lu, H., Kraut, D., Gerstenfeld, L. C., & Graves, D. T. (January, 2003). Diabetes interferes with the bone formation by affecting the expression of transcription factors that regulate osteoblast differentiation. Endocrinology, 144(1), 346-352. doi: http://dx.doi.org/10.1210/en.2002-220072 Ir a artículo http://press.endocrine.org/doi/abs/10.1210/en.2002-220072
The dose-response effects of energy availability on bone turnover have also been determined(Ihle & Loucks, 2004). (Ihle & Loucks, 2004). The rate of bone resorption increased when energy availability was low enough to reduce estradiol levels. The rate of bone protein synthesis, indicated by the plasma concentration of the bone formation marker Type I procollagen carboxy-terminal propeptide (PICP), was found to decline linearly with energy availability, as did insulin. Insulin stimulates osteoblast differentiation(Lu, Kraut, Gerstenfeld, & Graves, 2003).
Martinsen, M., Bratland-Sanda, S., Eriksson, A. K., & Sundgot-Borgen, J. (2010). Dieting to win or to be thin? A study of dieting and disordered eating among adolescent elite athletes and non-athlete controls. British Journal of Sports Medicine, 44(1), 70-76. doi: 10.1136/bjsm.2009.068668 Ir a artículo: http://bjsm.bmj.com/content/44/1/70.abstract
As a result, 5-9 times as many women as men in the three lowest deciles of BMI are actively trying to lose weight(Wardle et al., 2006). Indeed, more young female athletes report improvement of appearance than improvement of performance as a reason for dieting(Martinsen, Bratland-Sanda, Eriksson, & Sundgot-Borgen, 2010). This means that social issues may need to be addressed before female athletes will reform their diet and exercise behavior to increase energy availability.
Mattison, J. A., Lane, M. A., Roth, G. S., & Ingram, D. K. (January, 2003). Calorie restriction in rhesus monkeys. Experimental Gerontology, 38(1-2), 35-46. doi: 10.1016/S0531-5565(02)00146-8 Recuperado de: http://www.sciencedirect.com/science/article/pii/S0531556502001468
The health and longevity of experimental animals have been improved by restricting their energy intake by as much as 30% (Mattison, Lane, Roth, & Ingram, 2003), but restrictions of 40% have consistently caused both infertility (Holehan & Merry, 1985; McShane & Wise, 1996) and skeletal demineralization(Talbott, Rothkopf, & Shapses, 1998).
McShane, T. M., & Wise, P. M. (1996). Life-long moderate caloric restriction prolongs reproductive life span in rats without interrupting estrous cyclicity: effects on the gonadotropin-releasing hormone/luteinizing hormone axis. Biology of Reproduction, 54(1), 70-75. . Ir a artículo: http://www.biolreprod.org/content/54/1/70.full.pdf+html
Furthermore, although severe dietary restriction alone is sufficient to disrupt reproductive function, the more physically active a woman is, the less dietary restriction is required, and if she expends enough energy in exercise, she does not need to restrict her diet at all (Loucks et al., 1998). The health and longevity of experimental animals have been improved by restricting their energy intake by as much as 30% (Mattison, Lane, Roth, & Ingram, 2003), but restrictions of 40% have consistently caused both infertility (Holehan & Merry, 1985; McShane & Wise, 1996) and skeletal demineralization(Talbott, Rothkopf, & Shapses, 1998).
Müller, W. (February, 2009). Determinants of ski-jump performance and implications for health, safety and fairness. Sports Medicine, 39(2), 85-106. . Ir a artículo: http://link.springer.com/article/10.2165/00007256-200939020-00001
The associated procedures are intrusive, complicated, bureaucratic, time-consuming, labor-intensive and expensive. By contrast, the rules adopted by international ski-jumping aim to achieve the same objective by reducing the competitive incentive for athletes to engage in harmful weight loss behavior, and are elegantly simple (Muller, Groschl, Muller, & Sudi, 2006). Experience will teach whether initial reforms need further refinement(Muller, 2009; Oggiano & Saetran, 2008).
Müller, W., Gröschl, W., Müller, R., & Sudi, K. (2006). Underweight in Ski Jumping: The solution of the problem. International Journal of Sports Medicine, 27(11), 926-934. doi: 10.1055/s-2006-923844 Ir a artículo https://www.thieme-connect.de/products/ejournals/abstract/10.1055/s-2006-923844
The associated procedures are intrusive, complicated, bureaucratic, time-consuming, labor-intensive and expensive. By contrast, the rules adopted by international ski-jumping aim to achieve the same objective by reducing the competitive incentive for athletes to engage in harmful weight loss behavior, and are elegantly simple (Muller, Groschl, Muller, & Sudi, 2006). Experience will teach whether initial reforms need further refinement(Muller, 2009; Oggiano & Saetran, 2008).
Nattiv, A., Loucks, A. B., Manore, M. M., Sanborn, C.F., Sundgot-Borgen, J., & Warren, M. P. (October, 2007). American College of Sports Medicine Position Stand: The female athlete triad. Medicine and Science in Sports and Exercise, 39(10), 1867-1882. doi: 10.1249/mss.0b013e318149f111 Ir a artículo: http://journals.lww.com/acsm-msse/Fulltext/2007/10000/The_Female_Athlete_Triad.26.aspx
All girls and women are encouraged to participate in physical activities and sports, because the benefits of participation far outweigh the risks (Nattiv, Loucks, Manore, Sundgot-Borgen, & Warren, 2007). One of those risks is the Female Athlete Triad, in which reproductive and skeletal health are impaired by energy deficiency (Loucks, 2011; Loucks, Kiens, & Wright, 2011).
Promotional and commercial use of the material in print, digital or mobile device format is prohibited without the permission from the publisher Lippincott Williams & Wilkins. Please contact journalpermissions@lww.com for further information) (Nattiv et al., 2007).
National Collegiate Athletic Association. (2013). Wrestling Playing Rules. 2013-14 NCAA Weight Management Program. Retrieved fromhttps://www.ncaa.org/wps/wcm/connect/public/ncaa/playing+rules+administration/ncaa+rules+sports/wrestling/playing+rules/2013_14_weight_management_packet_08122013
ABesides coaches and dietitians, parents, team physicians and sport-governing bodies all have roles to play for preventing and treating the Triad. Everyone will need to experiment with educational programs, training regimens, intervention strategies and rule changes to achieve this objective, and to publicize the results of their experiments to teach others the lessons learned. Different challenges will emerge in different sports, requiring different solutions. For example, the rule changes adopted by US collegiate men’s wrestling aim to prevent harmful weight-loss practices by controlling athlete behavior (NCAA, 2013).
Oggiano, L., & Saetran, L. (2008). Effects of body weight on ski jumping performances under the new FIS Rules (P3). In M. Estivalet & P. Brisson (Eds.), The Engineering of Sport 7 (Vol. 1, pp. 1-9). Paris: Springer. Available from: http://link.springer.com/chapter/10.1007/978-2-287-09411-8_1
The associated procedures are intrusive, complicated, bureaucratic, time-consuming, labor-intensive and expensive. By contrast, the rules adopted by international ski-jumping aim to achieve the same objective by reducing the competitive incentive for athletes to engage in harmful weight loss behavior, and are elegantly simple (Muller, Groschl, Muller, & Sudi, 2006). Experience will teach whether initial reforms need further refinement(Muller, 2009; Oggiano & Saetran, 2008).
Okamoto, S., Arai, Y., Hara, K., Tsuzihara, T., & Kubo, T. (2010). A displaced stress fracture of the femoral neck in an adolescent female distance runner with female athlete triad: a case report. Sports Medicine, Arthroscopy, Rehabilitation, Therapy & Technology, 2, 6. doi: 10.1186/1758-2555-2-6 Ir a artículo: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2844364/
In adolescence, such uncoupling of the rates of bone resorption and formation prevents girls from accruing as much bone mass as other girls(Barrack, Rauh, & Nichols, 2010), The resulting bone loss predisposes women to stress fractures(Goolsby, Barrack, & Nattiv, 2012; Okamoto, Arai, Hara, Tsuzihara, & Kubo, 2010; Popp et al., 2009), in the near term and to the premature onset of osteoporosis later in life.
Pollock, N., Grogan, C., Perry, M., Pedlar, C., Cooke, K., Morrissey, D., & Dimitriou, L. (October, 2010). Bone-mineral density and other features of the female athlete triad in elite endurance runners: A longitudinal and cross-sectional observational study. International Journal of Sport Nutrition and Exercise Metabolism, 20(5), 418-426. Ir a artículo: http://journals.humankinetics.com/ijsnem-back-issues/ijsnem-volume-20-issue-5-october-2010/bone-mineral-density-and-other-features-of-the-female-athlete-triad-in-elite-endurance-runners-a-longitudinal-and-cross-sectional-observational-study
Low energy availability impairs skeletal health by uncoupling the turnover of bone in a manner that lowers bone mineral density over time (Christo et al., 2008; De Souza et al., 2008; Pollock et al., 2010).
Popp, K. L., Hughes, J. M., Smock, A. J., Novotny, S. A., Stovitz, S. D., Koehler, S. M., & Petit, M. A. (2009). Bone geometry, strength, and muscle size in runners with a history of stress fracture. Medicine and Science in Sports and Exercise, 41(12), 2145-2150. doi: 10.1249/MSS.0b013e3181a9e772 Ir a artículo: http://journals.lww.com/acsm-msse/Abstract/2009/12000/Bone_Geometry,_Strength,_and_Muscle_Size_in.6.aspx
The resulting bone loss predisposes women to stress fractures(Goolsby, Barrack, & Nattiv, 2012; Okamoto, Arai, Hara, Tsuzihara, & Kubo, 2010; Popp et al., 2009), in the near term and to the premature onset of osteoporosis later in life.
Rauh, M. J., Nichols, J. F., & Barrack, M. T. (May-June, 2010). Relationships among injury and disordered eating, menstrual dysfunction, and low bone mineral density in high school athletes: a prospective study. Journal of Athletic Training, 45(3), 243-252. doi: 10.4085/1062-6050-45.3.243 Ir a artículo: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2865962/
In physically active women, the compounding of exercise energy expenditure with cognitive dietary restraint is associated with an increased frequency of menstrual disorders and low bone mineral density (Barrack, Rauh, Barkai, & Nichols, 2008; Vescovi, Scheid, Hontscharuk, & De Souza, 2008). Some poorly informed athletes may also practice disordered eating behaviors (e.g., skipping meals, fasting, vomiting and using laxatives) in impatient pursuit of potentially unhealthful objectives (Rauh, Nichols, & Barrack, 2010; Thein-Nissenbaum, Rauh, Carr, Loud, & McGuine, 2011). Coaches and dietitians should cooperate to help athletes to correct disordered eating behaviors, to set healthful objectives, and to pursue these objectives on a healthful schedule.
Redman, L. M., & Loucks, A. B. (September, 2005). Menstrual disorders in athletes. Sports Medicine, 35(9), 747-755. Ir a artículo: http://link.springer.com/article/10.2165/00007256-200535090-00002
By contrast, reproductive function does not depend on the amount of energy stored in body fat, as was also once believed. Almost all observational studies of amenorrheic and eumenorrheic athletes have found them to span a common range of body size and composition (Redman & Loucks, 2005).
Rodriguez, N. R., DiMarco, N. M., & Langley, S. (March, 2009). Position of the American Dietetic Association, Dietitians of Canada, and the American College of Sports Medicine: Nutrition and athletic performance. Journal of the American Dietetic Association, 109(3), 509-527. Ir a artículo: http://www.sciencedirect.com/science/article/pii/S0002822309000066
Athletes of both sexes are susceptible to unintended and unnoticed reductions in energy availability due to the suppression of appetite by diet and exercise (Loucks et al., 2011). This appetite suppression is possible even during training periods when weight or fat loss is not a training objective, and even among athletes who do not suffer from eating disorders or practice disordered eating behaviors. Despite extensive evidence that appetite is not a reliable indicator of energy requirements in either trained or untrained men and women, this problem is entirely neglected in the current joint position stand on sports nutrition of the American College of Sports Medicine, the American Dietetic Association, and Dietitians of Canada (Rodriguez, DiMarco, & Langley, 2009)
Rucinski, A. (1989). Relationship of body image and dietary intake of competitive ice skaters. Journal of the American Dietetic Association, 89(1), 98-100.
The highest prevalence has been found in dance (17%-33%) (Brooks-Gunn, Warren, & Hamilton, 1987; Evers, 1987; Gadpaille, Sanborn, & Wagner, 1987; Holderness, Brooks-Gunn, & Warren, 1994) and ice skating (48%) (Rucinski, 1989).
Scheid, J. L., Williams, N. I., West, S. L., VanHeest, S. L., & De Souza, M. J. (February, 2009). Elevated PYY is associated with energy deficiency and indices of subclinical disordered eating in exercising women with hypothalamic amenorrhea. Appetite, 52(1), 184-192. doi: 10.1016/j.appet.2008.09.016 Ir a artículo: http://www.sciencedirect.com/science/article/pii/S0195666308005709
This suppresses the rate of bone formation by osteoblasts. Peripheral signals of low energy availability, such as falling insulin, rising ghrelin, rising peptide YY (PYY) and falling leptin levels, also act centrally to activate neuropeptide Y (NPY) secreting neurons in the hypothalamus, which act via sympathetic pathways on osteoblastic Y1 receptors to repress osteoblast activity and bone formation (Shi & Baldock, 2012). Amenorrheic athletes display elevated ghrelin and PYY, also known as peptide tyrosine tyrosine, as well as lower leptin levels (Ackerman et al., 2012; Scheid, Williams, West, VanHeest, & De Souza, 2009)
Shi, Y. C., & Baldock, P. A. (February, 2012). Central and peripheral mechanisms of the NPY system in the regulation of bone and adipose tissue. Bone, 50(2), 430-436. doi: 10.1016/j.bone.2011.10.001Ir a artículo: http://www.sciencedirect.com/science/article/pii/S8756328211012804
Amenorrheic athletes display elevated ghrelin and PYY, also known as peptide tyrosine tyrosine, as well as lower leptin levels (Ackerman et al., 2012; Scheid, Williams, West, VanHeest, & De Souza, 2009).Conversely, when energy availability increases, NPY expression is reduced, osteoblast activity is increased, bone formation is stimulated, and the mass of both cortical and cancellous bone increases in a generalized manner throughout the skeleton (Shi & Baldock, 2012).
Stubbs, R. J., Hughes, D. A., Johnstone, A. M., Whybrow, S., Horgan, G. W., King, N., & Blundell, J. (2004). Rate and extent of compensatory changes in energy intake and expenditure in response to altered exercise and diet composition in humans. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 286(2), R350-358. doi: 10.1152/ajpregu.00196.2003 Ir a artículo: http://ajpregu.physiology.org/content/286/2/R350
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008). Appetite is further suppressed by diets containing a high percentage (65%) of carbohydrates (Horvath, Eagen, Ryer-Calvin, & Pendergast, 2000; Stubbs et al., 2004).
Sum, M., & Warren, M. P. (December, 2009). Hypothalamic amenorrhea in young women with underlying polycystic ovary syndrome. Fertility and Sterility, 92(6), 2106-2108. doi: http://dx.doi.org/10.1016/j.fertnstert.2009.05.063 Ir a artículo: http://www.fertstert.org/article/S0015-0282%2809%2901211-4/abstract
Athletes with menstrual disorders should not be assumed to have such functional hypothalamic menstrual disorders, because menstrual disorders can be symptoms of many medical conditions. Moreover, functional hypothalamic menstrual disorders can be caused by insufficient intestinal absorption (as in Celiac disease) as well as by insufficient dietary intake, and they can conceal underlying polycystic ovary disease(Sum & Warren, 2009).
Sundgot-Borgen, J., & Torstveit, M. K. (January, 2004). Prevalence of eating disorders in elite athletes is higher than in the general population. Clinical Journal of Sport Medicine, 14(1), 25-32. Ir a artículo: http://journals.lww.com/cjsportsmed/Abstract/2004/01000/Prevalence_of_Eating_Disorders_in_Elite_Athletes.5.aspx
The prevalence of anorexia nervosa has been reported to be higher in “thin build” sports (dance, gymnastics, light-weight rowing, long distance running, diving and swimming) than other sports (Byrne & McLean, 2002). and even higher in “aesthetic” sports (i.e., gymnastics, dance, figure skating, aerobics, and diving) than other sports (12% vs 1%) (Sundgot-Borgen & Torstveit, 2004).
Talbott, S. M., Rothkopf, M. M., & Shapses, S. A. (1998). Dietary restriction of energy and calcium alters bone turnover and density in younger and older female rats. The Journal of Nutrition, 128(3), 640-645. Ir a artículo: http://jn.nutrition.org/content/128/3/640.full
The health and longevity of experimental animals have been improved by restricting their energy intake by as much as 30% (Mattison, Lane, Roth, & Ingram, 2003), but restrictions of 40% have consistently caused both infertility (Holehan & Merry, 1985; McShane & Wise, 1996) and skeletal demineralization(Talbott, Rothkopf, & Shapses, 1998). (Talbott, Rothkopf, & Shapses, 1998).
Thein-Nissenbaum, J. M., Rauh, M. J., Carr, K. E., Loud, K. J., & McGuine, T. A. (2011). Associations between disordered eating, menstrual dysfunction, and musculoskeletal injury, among high school athletes. Journal of Orthopaedic and Sports Physical Therapy, 41(2), 60-69. doi:10.2519/jospt.2011.3312 Ir a artículo http://www.jospt.org/doi/full/10.2519/jospt.2011.3312#.U6yz20D5cXU
Some poorly informed athletes may also practice disordered eating behaviors (e.g., skipping meals, fasting, vomiting and using laxatives) in impatient pursuit of potentially unhealthful objectives (Rauh, Nichols, & Barrack, 2010; Thein-Nissenbaum, Rauh, Carr, Loud, & McGuine, 2011).
Thong, F. S., McLean, C., & Graham, T. E. (June, 2000). Plasma leptin in female athletes: relationship with body fat, reproductive, nutritional, and endocrine factors. Journal of Applied Physiology, 88(6), 2037-2044. . Ir a artículo http://jap.physiology.org/content/88/6/2037
Tsutsumi, R. & Webster, N. J. G. (2009). GnRH Pulsatility, the Pituitary Response and Reproductive Dysfunction. Endocrine Journal, 56(6), 729-737. doi: http://dx.doi.org/10.1507/endocrj.K09E-185 Available from: https://www.jstage.jst.go.jp/article/endocrj/56/6/56_K09E-185/_article
Ueda, S. Y., Yoshikawa, T., Katsura, Y., Usui, T., & Fujimoto, S. (December, 2009). Comparable effects of moderate intensity exercise on changes in anorectic gut hormone levels and energy intake to high intensity exercise. Journal of Endocrinology, 203(3), 357-364. doi:10.1677/JOE-09-0190 Ir a artículo: http://joe.endocrinology-journals.org/content/203/3/357.full
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).(Whybrow et al., 2008).
Vescovi, J. D., Scheid, J. L., Hontscharuk, R., & De Souza, M. J. (2008). Cognitive dietary restraint: impact on bone, menstrual and metabolic status in young women. Physiology and Behavior, 95(1-2), 48-55. doi: 10.1016/j.physbeh.2008.04.003 Ir a artículo http://www.sciencedirect.com/science/article/pii/S0031938408001005
Many female athletes do both, but athletes in aesthetic sports tend to emphasize dietary restriction, while high energy expenditure is inherent in endurance sports. In physically active women, the compounding of exercise energy expenditure with cognitive dietary restraint is associated with an increased frequency of menstrual disorders and low bone mineral density (Barrack, Rauh, Barkai, & Nichols, 2008; Vescovi, Scheid, Hontscharuk, & De Souza, 2008).
Wade, G. N., & Jones, J. E. (2004). Neuroendocrinology of nutritional infertility. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 287(6), R1277-1296. doi: 10.1152/ajpregu.00475.2004 Ir a artículo: http://ajpregu.physiology.org/content/287/6/R1277
Reproductive function has been disrupted in rodents by dietary restriction; by administering drugs that block the oxidation of glucose and fatty acids; by insulin administration, which diverts blood glucose into storage while inhibiting the mobilization of fat stores; and by cold exposure, which consumes large quantities of metabolic fuels in thermogenesis; as well as by physical activity, which consumes metabolic fuels in muscular contractions ( Wade & Jones, 2004; Wade & Schneider, 1992).
Wade, G. N., & Schneider, J. E. (1992). Metabolic fuels and reproduction in female mammals. Neuroscience and Biobehavioral Reviews, 16(2), 235-272. doi: 10.1016/S0149-7634(05)80183-6 Ir a artículo: http://www.sciencedirect.com/science/article/pii/S0149763405801836
Reproductive function has been disrupted in rodents by dietary restriction; by administering drugs that block the oxidation of glucose and fatty acids; by insulin administration, which diverts blood glucose into storage while inhibiting the mobilization of fat stores; and by cold exposure, which consumes large quantities of metabolic fuels in thermogenesis; as well as by physical activity, which consumes metabolic fuels in muscular contractions ( Wade & Jones, 2004; Wade & Schneider, 1992).
Wardle, J., Haase, A. M., & Steptoe, A. (2006). Body image and weight control in young adults: international comparisons in university students from 22 countries. International Journal of Obesity, 30(4), 644-651. doi:10.1038/sj.ijo.0803050 . Ir a artículo: http://www.nature.com/ijo/journal/v30/n4/full/0803050a.html
The numbers of women and men actively trying to lose weight are even more disproportionate, and the disproportion increases as BMI declines. As a result, 5-9 times as many women as men in the three lowest deciles of BMI are actively trying to lose weight(Wardle et al., 2006).
Whybrow, S., Hughes, D. A., Ritz, P., Johnstone, A. M., Horgan, G. W., King, N., . . . Stubbs, R. J. (2008). The effect of an incremental increase in exercise on appetite, eating behavior, and energy balance in lean men and women feeding ad libitum. British Journal of Nutrition, 100(5), 1109-1115. doi: http://dx.doi.org/10.1017/S0007114508968240 Ir a artículo: http://journals.cambridge.org/action/displayAbstract?fromPage=online&aid=2411284&fileId=S0007114508968240
Briefly, after exercise, ad libitum energy intake does not increase sufficiently to compensate for exercise energy expenditure(Ballard et al., 2009; Bergouignan et al., 2010; Borer, 2010; King, Miyashita, Wasse, & Stensel, 2010; King et al., 2009; King, Hopkins, Caudwell, Stubbs, & Blundell, 2008; Ueda, Yoshikawa, Katsura, Usui, & Fujimoto, 2009); athletes who expend the most energy are susceptible to the largest deficiencies (Whybrow et al., 2008).
Williams, N. I., Caston-Balderrama, A. L., Helmreich, D. L., Parfitt, D. B., Nosbisch, C., & Cameron, J. L. (June, 2001). Longitudinal changes in reproductive hormones and menstrual cyclicity in cynomolgus monkeys during strenuous exercise training: abrupt transition to exercise-induced amenorrhea. Endocrinology, 142(6), 2381-2389. doi: http://dx.doi.org/10.1210/endo.142.6.8113. Ir a artículo: http://press.endocrine.org/doi/abs/10.1210/endo.142.6.8113
The energy costs of systemic infections and major trauma probably have similar effects. In monkeys, amenorrhea has been induced by increasing their exercise energy expenditure without restricting their dietary energy intake (Williams, Caston-Balderrama, et al., 2001); and then their menstrual cycles have been restored by increasing their dietary energy intake without moderating their exercise regimen (Williams, Helmreich, Parfitt, Caston-Balderrama, & Cameron, 2001).
Williams, N. I., Helmreich, D. L., Parfitt, D. B., Caston-Balderrama, A. L., & Cameron, J. L. (November, 2001). Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. Journal of Clinical Endocrinology and Metabolism, 86(11), 5184-5193. Available from: http://press.endocrine.org/doi/abs/10.1210/jcem.86.11.8024
Wilmore, J. H., Wambsgans, K. C., Brenner, M., Broeder, C. E., Paijmans, I., Volpe, J. A., & Wilmore, K. M. (1992). Is there energy conservation in amenorrheic compared with eumenorrheic distance runners? Journal of Applied Physiology, 72, 15-22. Ir a artículo http://jap.physiology.org/content/72/1/15
Some investigators have been skeptical of the diet records of female athletes, because comparisons of such records to estimations or measurements of energy expenditure have found apparently huge negative energy balances, some exceeding 4 MJ/d, in athletes with stable body weights(Edwards, Lindeman, Mikesky, & Stager, 1993; Wilmore et al., 1992).
Wolf, M., Ingbar, S. H., & Moses, A. C. (December, 1989). Thyroid hormone and growth hormone interact to regulate insulin-like growth factor-I messenger ribonucleic acid and circulating levels in the rat. Endocrinology, 125(6), 2905-2914. doi: http://dx.doi.org/10.1210/endo-125-6-2905 Ir a artículo: http://press.endocrine.org/doi/abs/10.1210/endo-125-6-2905
Osteocalcin is the glue that binds bone mineral to bone protein. Its secretion is mediated by IGF-1, the hepatic production of which is stimulated by growth hormone and modulated by T3 (Wolf, Ingbar, & Moses, 1989).
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