Since Title IX was passed in 1972, girls and young women's participation in sports has seen phenomenal growth. Currently, 3 million high school girls and a quarter of a million college women participate in all types and levels of sports, calling attention to the importance of healthy training practices and good coaching. There are many benefits that girls and young women receive from playing sports, including improved self-esteem, increased scholarly performance, a stronger immune system and reduced risk of illness, and a decreased risk of alcohol and drug abuse, and unwanted pregnancies (29). Being physically active at a young age can improve quality of life as health habits formed during childhood are likely to carry over into adulthood. Although there are risks involved with athletic participation (i.e., musculoskeletal injury, exercise-induced asthma), the rewards of being physically active often outweigh potential harms.
The growth of women's sports over the last 36 years has challenged coaches to focus on special considerations that relate to the female athlete. Sports that previously were male dominated or only available to male athletes, such as football, wrestling, and rugby, are now accessible to girls and young women. Female athletes have more opportunities to compete not only in different types of sports but also in a wide range of sport levels, including the elite level. Raising the bar in athletic competition has motivated many physically active young women to train harder and longer, pushing to new limits to achieve a personal best or contribute as a team player. The qualities of a “good athlete” are often highly regarded, but for some athletes, these positive attributes can develop into unhealthy behaviors with harmful consequences (42). Many female athletes, if not properly coached and trained, may be at risk for developing a syndrome known as the female athlete triad. To recognize at-risk behaviors and understand the complications that may affect sports performance, coaches need to have adequate knowledge of the female athlete triad and how to apply current research principles into practice.
This 2-part article is intended to (a) raise coach's awareness and understanding of the female athlete triad, presenting specific approaches that contribute to the treatment and prevention and the disorders, and (b) provide an understanding of topics for future consideration regarding the female athlete triad and a practical application of research related to the field of coaching.
FEMALE ATHLETE TRIAD
The focus of this review article is to provide coaches with an understanding of special concerns related to the female athlete, particularly the female athlete triad. The female athlete triad is a continuum of disorders that begin with the presence of low energy availability, resulting from inadequate dietary intake (because of intentional restriction of calories, as in disordered eating or an eating disorder, or inadequate compensation of energy output as a result of increased training). If a given threshold of low energy availability persists (the amount of expended energy through exercise exceeds the amount of dietary energy being taken in for a prolonged period (25)), the athlete may experience irregular or abnormal menstrual cycles, which can potentially disrupt normal reproductive function (26). When the body lacks certain nutrients and hormones that are essential for bone building (i.e., calcium, vitamin D, estrogen, and other micronutrients), bone mineral density (BMD) can become compromised, delaying or limiting the ability to reach peak bone mass during adolescence and young adulthood. At the extreme of the continuum of female athlete triad disorders is the development of osteoporosis, which could lead to progressive and irreversible long-term health consequences. The combined presence of low energy availability, menstrual dysfunction, and low BMD describes the syndrome known as the female athlete triad (25).
DISORDERED EATING AND LOW ENERGY AVAILABILITY
With increasing levels of competition, athletes may try to discover ways to improve their sports performance. Some athletes believe that their performance and success in sports will be enhanced by becoming leaner (40), which often leads to restrictive eating practices. The term disordered eating is used to describe a continuum of atypical and episodic eating patterns. The behaviors may include eating only low-fat or non-fat foods, skipping meals, fasting before a competition, and using diuretics or diet pills to lose weight (25,38,39,41). Disordered eating is a subclinical condition; the behaviors may be difficult to recognize or categorize because they are less distinct than clinical eating disorders (i.e., anorexia nervosa and bulimia nervosa), having specific diagnostic criteria (2).
The type of sport the athlete engages in and certain personality traits may predict individuals who will develop clinical and subclinical eating disorders (13,40,43,44). Long-distance runners and ballet dancers, for example, may use weight control measures because they have a particular perception about what their ideal body weight should be to achieve optimal performance (16). Athletes who feel pressure to manipulate their eating to control their weight for their appearance, performance, or to meet a body weight class may be most susceptible to disordered eating (40). Sociocultural pressures to be thin and comments about weight loss by coaches, parents, and friends may reinforce a cycle of training and weight loss in the athlete (9,40,42). Athletes who diet without supervision by a medical professional are more likely to develop disordered eating (often progressing to an eating disorder) than athletes who receive proper guidance and follow-up for a healthy weight loss (9,40). Some athletes' self-esteem relies on their degree of success in sports. Many of these individuals have perfectionist and body dissatisfaction qualities, which make them more likely to control their dietary intake and exercise, without allowing for proper amounts of nutrition, rest, and recovery (6,13,40). In elite Division I college athletes, Engel et al. (13) found that disordered eating was positively correlated with the athletes' perception that teammates engaged in disordered eating. The athlete might falsely perceive that teammates are practicing disordered eating to excuse their own behavior. If disordered eating is being practiced by other teammates, it illustrates the powerful influence that teammates can have in modeling and encouraging disordered eating behaviors (13,42). Although sports having a competitive or aesthetic value on leanness (gymnastics, figure skating, and ballet) are thought to precipitate abnormal patterns of eating and training (36,40,44), more recent results indicate the contrary (6). Larger athletic populations spanning different ages and sports need to be studied before definitive conclusions regarding the type of sport and prevalence of disordered eating are made.
Reasons athletes may unintentionally take in fewer calories than their body needs could result from increased endorphin levels and a loss of appetite that often accompany endurance/aerobic-type exercise. Feelings of well-being may further motivate the athlete to exercise more (14). Athletes may not be aware that their nutritional needs are not being met because appetite does not necessarily indicate dietary needs. Whether dietary restriction is intentional or inadvertent, inadequate vitamin, mineral, and nutrient intake can lead to serious energy deficits (25). A state of low energy availability occurs when the amount of expended energy through exercise exceeds the amount of dietary energy being taken in (25). The dietary energy that is left after exercise energy needs are compensated for is the energy that fuels other important physiologic functions, including those of the reproductive system (26). Regardless of whether abnormal patterns of eating are present or not, if the energy after exercising is not sufficient to support normal physiologic functions, then normal reproductive function can become disrupted (26).
When energy deficits reach a certain threshold, menstrual cycles can become irregular, causing oligomenorrhea (menstrual cycles occur at intervals >35 days), or they can altogether cease, causing amenorrhea (menstrual cycles are absent for >3 months) (3,35,38). Average menstrual cycles in healthy women occur at an interval of 28 ± 7 days (1). Girls who fail to menstruate by age 15 have primary amenorrhea (1); secondary amenorrhea is the cessation of menstruation after at least 1 menstrual cycle has begun (3). Before oligomenorrhea and amenorrhea are diagnosed, other causes for menstrual dysfunction (i.e., tumors, anabolic steroid use, pregnancy, hormonal imbalances) must be ruled out (8).
When menstrual dysfunction, caused by low energy availability, occurs during adolescence, it can limit new bone formation causing a decline in BMD and an increase in stress fracture risk (20,21,32). Achieving peak bone mass may be hindered by a decline in new bone formation and BMD causing more serious consequences, such as osteoporosis and osteoporotic fractures (45-47).
The female athlete triad can occur even if disordered eating or an eating disorder is not present. When not treated appropriately, the conditions can progress along a continuum of increasing severity (25,33), highlighting the importance of early intervention. Preventing osteoporosis, the most severe and harmful effect of the syndrome, is a major goal of treatment. When low BMD is present during adolescence and young adulthood, bone loss and the likelihood of osteoporotic fractures in adulthood are greater and may occur at accelerated rates after menopause (5,21,30). A family history of osteoporosis, diets that are deficient in dairy intake (vitamin D and calcium intake), vegan diets, and chronic steroid use further complicate fracture risk and the development of osteoporosis (15,20,32).
DEVELOPMENT OF THE FEMALE ATHLETE TRIAD
Although the mechanisms in which low energy availability affects menstrual function and bone density are not completely understood, it is thought that energy deficiencies suppress the release of gonadotropin-releasing hormone (GnRH) from the hypothalamus (28,46). Gonadotropin-releasing hormone normally triggers luteinizing hormone (LH) and follicle-stimulating hormone to be secreted from the pituitary gland (27). When GnRH is suppressed, normal concentrations of LH in the blood get disrupted, inhibiting the release of estrogen and progesterone by the ovaries (8). Low energy availability may also decrease the secretion of leptin, a hormone secreted by fat cells that is needed to maintain normal menstruation (8). Eventually, a low estrogen state (hypoestrogenemia) leads either to irregular cycles or to amenorrhea, the loss of menstruation. When amenorrhea results from increasing energy expenditure (without reducing dietary intake) and can be reversed by increasing energy intake (without modifying exercise), it is known as functional hypothalamic amenorrhea (25). A critical level of low energy availability must be reached for hormonal disruption to occur; however, once the critical level is reached and maintained, hormonal disruption can occur in as quickly as 5 days (25).
Nutrient and hormone deficiencies can ultimately affect bone health because adequate amounts of calcium, vitamin D, estrogen, and other micronutrients are essential for bone building. During puberty, rapid skeletal maturation and bone growth leading to peak bone mass are dependent on available nutrient resources and hormone secretion (5,21). The rate of bone formation will be slowed or delayed if nutritional deficits and low levels of circulating hormones are present during adolescence. With severe and persistent nutrient deficiencies, bone resorption will start to exceed the rate of bone formation (26), causing low BMD and porous bones. Low BMD and failure to reach peak bone mass can lead to stress fractures during adolescence (7,15,20), and accelerated rates of bone loss and osteoporotic fractures with aging might be expected (5,31), although there is no clear evidence to support this.
Research has indicated that decreases in BMD are directly proportional to the length of time in which amenorrhea is present (11), stressing again that early intervention can prevent substantial declines in bone mass. The decline in BMD may also be influenced by genetics, bone size, the degree of skeletal loading (based on type of sport), and social history (smoking and alcohol consumption) (35,36). Individual differences in genetic makeup or environmental influences may explain why there might be varied outcomes in bone health of amenorrheic athletes. For example, some athletes with amenorrhea have normal bone mass; other amenorrhea athletes with low BMD have been treated successfully with dietary supplementation (resumption of normal BMD) (27), whereas some athletes suffer irreversible bone mass losses (45).
In recent years, scientific breakthroughs have determined that a certain threshold of available energy (calories) is required to prevent the disruption of LH release and menstrual dysfunction. This means that abnormal or absent menstruation can be avoided as long as caloric intake does not fall below a critical threshold of energy availability (i.e., <30-45 kcal per kg of fat-free body mass per day) (26). Making sure that the amount of energy the athlete expends through exercise is sufficiently compensated for with energy (nutrient) intake is one way of assuring that energy availability stays above this threshold.
PREVALENCE OF THE FEMALE ATHLETE TRIAD
Current evidence suggests that the incidence of having all 3 components of the female athlete triad simultaneously is less than 4.3% (6,10,17,23,34,44). But it has been reported that a significant number of female athletes and physically active young women have individual triad disorders (1 or 2 components), placing them at risk for developing the full triad (6,10,17,34,44). Perhaps the reason female athletes develop low energy availability and menstrual dysfunction (the first two triad components), but have little change in bone density (the third component) is because losses in BMD may be negated by the effect that high-impact sports (high weight bearing loads) have on bone density. Athletes participating in high-impact sports (i.e., gymnastics, cross-country) experience greater mechanical joint loading and may have higher BMD values when compared with athletes in non-impact sports (i.e., swimming, diving) and age- and sex-matched sedentary controls (4,12). It has been documented that athletes involved in impact sports may have BMD values that are up to 15% higher than nonathletes of the same age and skeletal maturation (31,37). Because impact sports raise BMD values higher than is normal for this population, declines in BMD may not be recognized because lower values may still be within “normal range” when compared with normative data.
The studies conducted on the combined prevalence of the triad disorders (6,10,17,23,34,44) are limited in that they are cross-sectional studies and do not reflect potential changes that can occur in the athlete over time. This is an important consideration because the triad conditions occur along a continuum of increasing dysfunction, and the effects on bone health are usually not immediate. Unless diagnostic tests (x-rays, bone scans) reveal that a stress fracture is present or the presence of low BMD is confirmed (through dual-energy x-ray absorptiometry or DXA scanning), there are no observable signs of declining BMD. Many of the prevalence studies have used different criteria to diagnose or interpret measures of BMD (stress fracture history versus DXA, different diagnostic procedures, and different interpretations of DXA values) and therefore cannot be compared. Studies using a more strict definition of low BMD or osteoporosis may underestimate the actual occurrence of the third triad component. Until standardized methods of measurement are used to assess the prevalence of the triad and large longitudinal studies are conducted, it is difficult to know the precise frequency in which the female athlete triad occurs.
INSTRUMENTS USED TO ASSESS THE PRESENCE OF THE TRIAD
THE SELF-REPORT QUESTIONNAIRE VERSUS DIRECT INTERVIEW
Frequently, disordered eating behaviors are withheld by the athlete for fear of negative consequences (restricted practice or game playing). Underreporting abnormal eating patterns and distortion of the results are more likely to occur when self-report questionnaires are used as a tool to measure the behaviors. Conducting interviews and asking athletes direct questions, rather than trying to uncover disordered eating behaviors through self-report questionnaires, may improve the accuracy of reporting. Obtaining a menstrual history, which should include age at menarche; frequency and duration of menstrual cycles; last menstrual period; and longest period without menstruation, may help identify athletes who are in need of further medical follow-up by a physician. Coaches and clinicians need to take into account the deleterious effects that low energy availability and menstrual dysfunction can have on bone health, recognizing that the potential outcomes of these conditions are usually not immediate and therefore should not be ignored when suspected or first recognized. If the triad conditions are left unchecked, there is a strong possibility that sports performance and long-term bone health will be compromised (15). Although low body weight and low body fat may be considered risk factors for energy deficiencies that lead to amenorrhea or oligomenorrhea, they are not responsible for disrupting menstrual function (23), and this fact should be taken into consideration when risk factors are assessed.
CRITERIA FOR MEASURING BONE DENSITY
In July 2008, the International Society for Clinical Densitometry (ISCD) published new guidelines for the diagnosis of osteoporosis and the interpretation of BMD values in children and adolescents using DXA (18,19). The Pediatric position statement suggests that low BMD for this population be compared with newly established pediatric normative data (established for ages 6-16 years) (22) that are adjusted for chronological age (Z scores) (19). The report emphasized that the term osteoporosis can only be used in children and adolescents when BMD Z scores are ≤−2.0 and when there is a clinically significant fracture history. When Z scores are ≤−2.0, but there is no fracture history, the term low bone mass for chronological age is recommended (18,19). The criterion for osteoporosis previously established by the World Health Organization (WHO) is based on normative data in healthy, young, normal adults (a T score below −2.5 defines osteoporosis) (24). Although the WHO classifications may continue to be used, the ISCD reports that WHO standards should only apply to postmenopausal women (and not children and adolescents) (18,19,22). Studies have compared abnormal BMD values in children and adolescents with the recently published normative data because Z scores are considered to be more appropriate for diagnosis, treatment, and prevention of low BMD in this population; however, they cannot be directly compared with studies using the WHO classification.
Coaches can be instrumental in detecting risk factors that may lead to the development of the female athlete triad; subsequently, they play an important role in facilitating treatment through early detection. Additionally, through proper coaching and training, they can assist in the prevention of the condition. This article provides a foundational understanding of the female athlete triad and sets the stage to discuss future research considerations, as well as the application of research to the field of coaching in the next section (part 2).
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