The Female Athlete Triad

SUMMARY The female athlete triad (Triad) refers to the interrelationships among energy availability, menstrual function, and bone mineral density, which may have clinical manifestations including eating disorders, functional hypothalamic amenorrhea, and osteoporosis. With proper nutrition, these same relationships promote robust health. Athletes are distributed along a spectrum between health and disease, and those at the pathological end may not exhibit all these clinical conditions simultaneously. Energy availability is defined as dietary energy intake minus exercise energy expenditure. Low energy availability appears to be the factor that impairs reproductive and skeletal health in the Triad, and it may be inadvertent, intentional, or psychopathological. Most effects appear to occur below an energy availability of 30 kcal·kg−1 of fat-free mass per day. Restrictive eating behaviors practiced by girls and women in sports or physical activities that emphasize leanness are of special concern. For prevention and early intervention, education of athletes, parents, coaches, trainers, judges, and administrators is a priority. Athletes should be assessed for the Triad at the preparticipation physical and/or annual health screening exam, and whenever an athlete presents with any of the Triad's clinical conditions. Sport administrators should also consider rule changes to discourage unhealthy weight loss practices. A multidisciplinary treatment team should include a physician or other health-care professional, a registered dietitian, and, for athletes with eating disorders, a mental health practitioner. Additional valuable team members may include a certified athletic trainer, an exercise physiologist, and the athlete's coach, parents and other family members. The first aim of treatment for any Triad component is to increase energy availability by increasing energy intake and/or reducing exercise energy expenditure. Nutrition counseling and monitoring are sufficient interventions for many athletes, but eating disorders warrant psychotherapy. Athletes with eating disorders should be required to meet established criteria to continue exercising, and their training and competition may need to be modified. No pharmacological agent adequately restores bone loss or corrects metabolic abnormalities that impair health and performance in athletes with functional hypothalamic amenorrhea. INTRODUCTION Because the benefits of exercise far outweigh the risks, the American College of Sports Medicine (ACSM) encourages all girls and women to participate in physical activities and sports. In 1992, however, an association of disordered eating, amenorrhea, and osteoporosis seen in activities that emphasize a lean physique was recognized as the female athlete triad (Triad) (148,215). This Position Stand replaces the 1997 ACSM Position Stand (155), updates our understanding, and makes new recommendations for screening, diagnosis, prevention, and treatment of the Triad. EVIDENCE CLASSIFICATION This Position Stand presents clinical recommendations for guiding primary care (Table 1). We used criteria proposed by the American Academy of Family Physicians (52) for evaluating the strength of scientific evidence supporting these clinical recommendations. These criteria categorize the strength of scientific evidence as follows: A, consistent and good-quality evidence for clinical outcomes on mortality, morbidity, symptoms, cost, and quality of life; B, inconsistent or limited quality evidence for these same clinical outcomes; and C, evidence on biochemical, histological, physiological and pathophysiological outcomes, which include hormone concentrations, bone mineral density (BMD), and asymptomatic menstrual disorders such as short luteal phase and anovulation; and evidence based on case studies, consensus, usual practice, and opinion. To avoid misunderstanding, this Position Stand differentiates between two subcategories of evidence: C-1, evidence based on biochemical, histological, physiological, and pathophysiological outcomes; and C-2, evidence based on case studies, consensus, usual practice, and opinion. This Position Stand also presents evidence statements about the current state of knowledge (Table 1). Although the clinical recommendation criteria were not developed for evaluating evidence supporting statements about the current state of knowledge (52), we used these same criteria to evaluate this evidence, as well.TABLE 1: Strength of evidence taxonomy.THREE INTERRELATED SPECTRUMS Low energy availability (with or without eating disorders), amenorrhea, and osteoporosis, alone or in combination, pose significant health risks to physically active girls and women. The potentially irreversible consequences of these clinical conditions emphasize the critical need for prevention, early diagnosis, and treatment. Each clinical condition is now understood to comprise the pathological end of a spectrum of interrelated subclinical conditions between health and disease. Figure 1 illustrates the full range of the Triad. A glossary of terms pertaining to the Triad appears in Table 2.FIGURE 1: Female athlete triad. The spectrums of energy availability, menstrual function, and bone mineral density along which female athletes are distributed (narrow arrows). An athlete's condition moves along each spectrum at a different rate, in one direction or the other, according to her diet and exercise habits. Energy availability, defined as dietary energy intake minus exercise energy expenditure, affects bone mineral density both directly via metabolic hormones and indirectly via effects on menstrual function and thereby estrogen (thick arrows).TABLE 2: Glossary of terms pertaining to the female athlete triad.The goal of ACSM is for every girl and woman's physical condition to be coincident with the upper right corner of Figure 1, which represents the healthy athlete who adjusts her dietary energy intake to compensate for exercise energy expenditure. Thick arrows in this triangle indicate that energy availability promotes bone health and development indirectly by preserving eumenorrhea (Table 2) and estrogen production that restrains bone resorption, and directly by stimulating production of hormones that promote bone formation. As a result, BMD is often above average for the athlete's age. The triangle in the lower left corner of Figure 1 represents the unhealthy condition of athletes who exercise for prolonged periods without increasing dietary energy intake, who severely restrict their diet, or who have clinical eating disorders. Thick arrows in this triangle indicate that low energy availability impairs bone health and development indirectly by inducing amenorrhea and removing estrogen's restraint on bone resorption, and directly by suppressing the hormones that promote bone formation. Bone mineral accrual has slowed or reversed for so long that BMD is below average for age, and one or more stress fractures may have occurred. The narrow arrows in Figure 1 indicate the spectrums of intermediate levels of energy availability, menstrual status, and BMD where other athletes' health status may be distributed. Moderately or recurrently reduced energy availability may induce subclinical menstrual disorders and less severely suppress estrogen and metabolic hormones, and sufficient time may not yet have passed for these athletes to fall far behind their age group in BMD. Energy availability, menstrual status, and BMD move along these spectrums in one direction or the other at different rates according to an athlete's diet and exercise habits. Energy availability can change in a day, but an effect on menstrual status may not become evident for a month or more, and an effect on BMD may not be detectable for a year. 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Low BMD The primary of osteoporosis in women is estrogen which bone also to disorders such as and for a of the bone in athletes with functional hypothalamic amenorrhea As is the case with estrogen in athletes with functional hypothalamic amenorrhea is often by which the of bone 1). In a clinical the of bone and the of bone energy availability was reduced below 30 kcal·kg−1 in women energy availability was to suppress and bone was at energy in relationships those of and that bone Low energy availability may also suppress bone via effects on other hormones, including and and on BMD in female athletes is clinical for the and treatment of Triad disorders are in Table for the Triad can be health consequences are not Although athletes are in sports where is to be one or more clinical consequences of the Triad can occur in in any or physical for the Triad an of the relationships among the spectrum each and rates of along each spectrum 1). screening occur at the preparticipation physical and annual health occur athletes are for such as amenorrhea, stress or or An athlete who presents with one component of the Triad should be assessed for the clinical for the and treatment of Triad eating disorders appear to be and should be to for their and treatment in primary care screening for in primary care should be to meet all criteria for or should not the health-care early and intervention, early and with can athletes eating disorders in the of a clinical eating and behaviors are of energy of these behaviors are of their effects on bone are disordered eating behaviors are also of may indicate a to and behaviors or of eating for the Triad should occur at the preparticipation or annual health screening Athletes with one component of the Triad should be assessed for the on energy intake, dietary weight eating and exercise energy should be of weight and menstrual are in athletes with disordered eating or eating disorders. Athletes with disordered eating should be to a mental health for diagnosis, and recommendations for treatment. status and and other with low such as stress should also be Athletes with disordered eating should be to a mental health for and recommendations for treatment. An athlete with a of one or more of the Triad should have a physical The health-care should be for and of an eating and should be is seen as as include and and the athlete is with an eating by a mental health an should be as the is in the of With functional hypothalamic amenorrhea, the physical is but with may be on In the athlete with disordered eating or an eating an should include a a with rate, function and for can be in severely health-care should not be by is for functional hypothalamic amenorrhea, this condition is by other of amenorrhea for amenorrhea a stimulating hormone and to rule and for the seen in a to rule a and a stimulating hormone for disease. is evidence of on physical exam, and may be to evaluate for an of the or or In to the of that can be seen in functional hypothalamic amenorrhea, indicate can be or a can be to estrogen indirectly by for In functional hypothalamic amenorrhea, are low or is and stimulating hormone are in the A athlete may not to a athletes with this as Additional may be based on and physical and for of primary amenorrhea. with a physician in female athletes or a reproductive is are not of the athlete has a To functional hypothalamic amenorrhea, other of amenorrhea be Bone A of disordered eating or eating disorders for a of or more, and/or a of stress fractures or fractures BMD by is in in those with Triad disorders. should be on the same may an to or for the effects of low energy availability on BMD. in BMD among athletes and are seen between sports and skeletal of low BMD or osteoporosis is based on the BMD of the or the or not or and both should be In less of age, and are the BMD may be in athletes with functional hypothalamic amenorrhea, BMD is often BMD should be assessed a stress or low and a of of amenorrhea, disordered eating or an eating The of bone and the of to BMD in athletes with functional hypothalamic amenorrhea our and recommendations for of the Triad. of bone with a of bone and an increase in bone can irreversible in BMD of bone by of energy availability also that of without clinical menstrual disorders may to their for BMD. and treatment of the Triad should a team including a physician or other health-care or a registered dietitian, and for athletes with disordered eating or an eating a with knowledge of disordered eating and eating disorders in sports be to the of those sports. Additional valuable team members may include a certified athletic trainer, an exercise physiologist, and the athlete's coach, parents and other family members. to the treatment of eating disorders in the should be recognized treatment for the Triad disorders should include a physician other health-care a registered dietitian, and, for athletes with disordered eating or an eating a mental health practitioner. administrators and the health-care team should aim to the Triad education should be on energy availability for prevention should also be to bone mineral accrual in and athletes and to bone health and should be on for their age, including and and on the benefits of exercise for bone health Athletes with menstrual disorders and/or low energy availability with or without disordered eating or eating disorders should be about the of bone mineral osteoporosis, and stress other ACSM that and of sports and athletic and in to potentially weight loss of female and are not may be in BMD of per have in weight in and case of athletes In in BMD of per have seen with weight in but not all the first aim of to menstrual and increase BMD is to diet and exercise to increase energy availability by increasing energy intake, reducing energy expenditure, or a according to the athlete's with recommendations. may be by increasing energy availability to more 30 kcal·kg−1 but the association between in BMD and in weight that increasing BMD may more kcal·kg−1 This to energy in healthy women Athletes eating behaviors should be that in weight may be to increase BMD. is to this is athletes should be to a for counseling and to have their energy availability diet, and weight should all be of such as and are for and may be is to of and increase BMD and fractures in female athletes with the Triad disorders. for female athletes in exercise training may also be those for the at energy availability should continue and be training and The treatment goal for athletes with disordered eating or eating disorders is to status, eating unhealthy that the and that for athletes a need for the is based on a between the athlete and the care The the the more the is In to counseling and treatment group and family An athlete in treatment for disordered eating or eating disorders should meet criteria to continue training and The athlete to with all treatment to be by health-care to on treatment training and and on her status to the and of training and competition A may be used to these of and with the health-care team are the athlete not her or her eating and weight not may need to be training and but should The first aim of treatment is to increase energy availability by increasing energy intake and/or reducing energy expenditure. Athletes without disordered eating or eating disorders should be for Athletes eating behaviors should be that in weight may be to increase BMD. for disordered eating and eating disorders counseling and psychotherapy. group and/or family may also be Athletes with disordered eating and eating disorders who not with treatment may need to be training and are often for weight and for and disorders but agent for in this has to BMD in women with functional hypothalamic amenorrhea. women with functional hypothalamic amenorrhea between two pharmacological or not menstrual was hormone and the and reduced the of menstrual No mass but all those Bone mineral density by less per in two of women with functional hypothalamic amenorrhea who were with but not in a In a of for weight effects of of the of for increasing BMD in athletes and other women with functional hypothalamic amenorrhea without eating disorders is also with clinical and and not but changes in weight were often not that the increase in BMD was by an increase in weight and that the effect of weight the effect of has BMD in any of women with be that pharmacological of menstrual with not metabolic that impair bone health and it is to the low BMD in this Bone mineral density should be in women with functional hypothalamic amenorrhea, disordered eating, and/or low BMD. BMD in an athlete of age with functional hypothalamic amenorrhea intake and may be with the of bone are established as to or to to the athlete less of age with functional hypothalamic amenorrhea to about of and of to this in this age for the treatment of osteoporosis should not be used in the athlete with functional hypothalamic amenorrhea for two The first is of their in women of age The is that the may in a woman's bone for many potentially to a a aim of is to in the athlete who to become of with such as and is the athlete should be about the risks and of a low weight an not her dietary more is to any or new of hormone is for increasing BMD in athletes with functional hypothalamic amenorrhea. In this BMD and other should be to pharmacological and is also on other of energy availability and of function are the of treatment for the Triad. In functional hypothalamic amenorrhea, in BMD are more with in weight with should be in an athlete with functional hypothalamic amenorrhea age BMD is with and Low energy availability with or without eating disorders, functional hypothalamic amenorrhea, and osteoporosis, alone or in combination, pose significant health risks to physically active girls and women. and treatment of these clinical conditions should be a of those who with female athletes to that the benefits of This was for the American College of Sports Medicine by the and by and Additional are to and for their with and this Position This Position Stand replaces the 1997 ACSM Position Female Sports