Introduction

As more and more women engage in competitive and recreational sport, the incidence of injury and nutritionally derived disorders in this population have increased as well. One such clinical entity, the "female-athlete triad", is a recently characterized disorder that not only has negative implications on physical performance, but short- and long-term health implications as well.

We polled four experts who have studied the female athlete triad from both a clinical and scientific perspective about the signs and symptoms of the triad, and what coaches, trainers, and other health professionals can do to recognize and prevent the occurrence of this syndrome in the athletes with whom they work.

Can you explain the "female-athlete triad", and discuss the prevalence of this condition in athletes.

Steen: A growing body of research suggests that the prevalence of excessive training regimens and the emphasis on thinness is increasing. Driven to meet these demands in her chosen sport, the female athlete may be at risk of developing disordered eating, amenorrhea, and bone loss. Collectively, these potential clinical disorders are referred to as the female-athlete triad.

Johnson: It is generally accepted that the development of amenorrhea and subsequent osteoporosis occur secondary to the disordered eating, which includes restrictive food intake, binging and purging by vomiting, laxative use, and diuretic use.

The prevalence of the "triad" is unknown. Studies performed to determine the prevalence of disordered eating behavior among athletes have been difficult to interpret. Most studies have utilized surveys; few have utilized clinical interview. Of course, there are drawbacks to this type of research. Athletes may not be truthful in answering questionnaires, as many deny their behavior and, in addition, it's difficult to quantify behavior such as food restriction, binging, and excessive exercise.

Loucks: The female athlete triad syndrome does have long term health-related implications. The failure of young athletic women to develop strong bones, leading to premature skeletal demineralization and osteoporotic fractures, implies a very negative prognosis for their future bone health. Research has found that bone density in women is directly proportional to the number of menstrual cycles they have experienced.

Restrictive and bulimic eating behaviors occur in one-half to one percent of the general population of young women, and the prevalence in athletes is thought to be as high or higher. Our own research indicates that because of their high energy expenditure during exercise female athletes may not need to practice the extreme eating behaviors of sedentary women in order to suffer energy deficiencies capable of disrupting their reproductive function. Amenorrhea occurs in two to five percent of the general population of women of reproductive age, but various studies have found the prevalence of amenorrhea in athletes in some sports to be as high as 40 percent or more. So far as we know, hypoestrogenism causes skeletal demineralization in all amenorrheic athletes.

Eichner: As Dr. Steen suggested, women and girls at higher risk appear to be those in the "low weight" or "appearance" sports, notably distance running, gymnastics, ballet, figure skating, diving, and possibly even swimming.

I agree with Dr. Johnson's assertion that the true prevalence of the female athlete triad is uncertain and debatable; even the prevalence of its most common feature, disordered eating, is unclear. For example, most clinical articles cite the prevalence of disordered eating among female athletes as between 15% and 62%. This range comes not from solid research, but from symptoms self-rated by non-elite athletes on non-validated questionnaires, usually without non-athletic controls. So far, we have few or no scientifically sound studies on the prevalence of the female athlete triad.

Is the female athlete triad a new clinical entity? Has there been a lot of research done on the female triad?

Johnson: The female athlete triad is not a new clinical entity. Clinicians who have worked with adolescents and women with eating disorders have known about the association between caloric deprivation / weight loss and amenorrhea for many years. Clinicians have also known about exercise-associated amenorrhea for many years, and have been aware that weight loss, high intensity training, and eating disorders are often seen in these athletes. Osteoporosis in athletes has been studied for the last 10-15 years. Although there has been a lot of research done in the individual areas of eating disorders, amenorrhea, and osteoporosis, there has been little research done on the collective occurrence of the three disorders.

Loucks: The term "female athlete triad" was first promulgated in a special American College of Sports Medicine conference on the subject in Washington, D.C. in June of 1992. Clinicians and physiologists had associated energy deficiency with menstrual disorders in the mid-70s, and extreme low bone densities were first observed in amenorrheic athletes in the mid-80s. Since then, certain tragic cases of eating disorders in athletes have been widely publicized. In addition, research has found that critical hormones regulating menstrual function are disrupted by low energy availability, and that exercise has no disruptive effect on these hormones beyond the impact of its energy cost on energy availability.

Steen: As Drs. Johnson and Loucks suggested, one of the interrelated problems of the triad is the loss of bone mineral density. Both amenorrhea and oligomenorrhea can reduce bone mineral density and subsequently increase the risk of stress fractures. Some important studies conducted during the past 10 years or so have suggested that reducing exercise, improving dietary intake, and increasing body weight can help to restore menstruation and improve bone mineral density in amenorrheic athletes. It should be pointed out, however, that bone mineralization may never return completely to normal in the amenorrheic athlete. Further, a recent study by Mickelsfield and associates suggested that ultramarathoners who were oligomenorrheic might still suffer bone loss during training, and may never be able to catch-up on the bone loss they suffer. Certainly more research needs to be done, but there is a growing body of data on the interrelated clinical entities that comprise the female-athlete triad.

Eichner: In the cosmic scheme of things, this triad is "new." Probably stress-related amenorrhea has occurred since the dawn of humanity, but during war or famine (when fertility bowed to survival), not during training for the Ironman. And in antiquity, a 35-year old was a tribal elder, so those women died before they got osteoporosis. Dr. Steen mentioned the increase of both excessive training and an emphasis on thinness. It seems to me that the triad has surfaced over the past two decades, as our society adopted a "thin-is-in" view of the ideal woman, as reflected by waif supermodels. This view, alas, also influenced the "appearance" sports. Girls and young women driven to excel were led to believe that the thinner they were, the better they would perform and the better they would look doing so. They increased training and cut calories in a race to win and a race to be thin. As Dr. Steen stated, research on the triad is limited but growing. Our awareness of it increased sharply since the American College of Sports Medicine conference that Dr. Loucks mentioned.

Are there specific nutrient deficiencies or dietary concerns that would predispose one to the development of this condition?

Loucks: This question crosses the frontier of our knowledge. We're pretty confident that reproductive function depends on energy availability in women as it does in other mammals. By energy availability I mean dietary calorie intake minus exercise calorie expenditure, and not energy stores in the form of fat. We don't know yet whether there is a particular threshold of energy required to maintain normal reproductive health in women. Nor do we know whether the macronutrient composition of the diet is important. The effects of certain drugs in animal experiments appear to suggest that reproductive function depends specifically on carbohydrate availability, perhaps because the brain relies on glucose for energy.

Eichner: It is, of course, important to consume enough calcium to keep bones strong, but as I read the literature on the triad I tend to agree more with Dr. Louck's assertion that the key element is energy-in versus energy-out. If a female athlete consumes insufficient energy for her needs she can develop menstrual problems, and then maybe osteoporosis. If she increases energy intake (or cuts training) by 10-20%, normal menses tends to return and presumably the triad is averted.

Johnson: My clinical impression supports Dr. Loucks's research-based statement that the female athlete triad is a condition of "energy deficiency." The athlete's energy expenditure is not being met by her energy intake. This may be intentional or unintentional, but it adds up to the same problem. When treating these athletes I invariably find that they resume menses once they have consistently increased their caloric intake.

Steen: Disordered eating tends to go hand-in-hand with amenorrhea and bone loss. For the athlete who is willing to make lifestyle changes, the following guidelines can be used to increase weight gradually: 1) decrease training activity by 10-20%; 2) increase energy intake gradually; 3) increase weight by 2-3% of current body weight; 4) increase calcium intake to 1500 mg/day. Dueck employed this intervention program to address amenorrhea in an endurance athlete that reduced the athlete's training regimen by one day per week, and included the use of a sports nutrition beverage (GatorPro) to provide 360 additional calories per day. This non-pharmacological approach was associated with a transition from negative to positive energy balance, increased percentage of body fat, increased lutenizing hormone and decreased fasting cortisol, resumption of menses, and improved performance.

Are there additional preventive steps that a woman can take to help to diminish her chances of developing this syndrome?

Eichner: Additional preventive steps would include the standard dietary advice on how to get enough calcium from the diet-and how to hold on to it. Estrogen levels are key to bone mineralization, and most clinicians now treat amenorrhea in female athletes with oral contraceptives, even though support for this therapy is limited to one small randomized trial and a few other inconclusive studies. Dr. Steen's straightforward diet and exercise guidelines outlined in her previous response makes sense to me. In addition, I might recommend resistance training as a means of boosting muscle strength and aiding in bone mineralization.

We still have much to learn about how the features of this triad interrelate. Surely genetics plays a role, and so does impact loading. Consider gymnasts. Recent studies from Sweden, from the University of Oregon, and from the University of Georgia agree that, as a group, college-aged gymnasts, despite a high prevalence of disordered eating and menstrual problems, have higher bone density than controls. And follow-up from the University of Georgia show that, 15 years after college, former female gymnasts still have higher bone density than controls. We also should be careful not to scare women away from athletic lifestyles by extrapolating too widely from limited studies finding osteopenia in small numbers of elite athletes. Reassuring is a recent Danish study of 205 female runners, mostly in their late 20s or early 30s and ranging from recreational runners to elite distance runners. Sex hormone and menstrual disturbances paralleled the amount and intensity of running, but almost all of the recreational runners and 90% of the elite runners had normal bone density.

Loucks: Women can educate themselves about nutrition, and they should consume a nutritionally complete diet. They can also forego striving for a body weight that is unrealistically low for their frame size, even if competitive, aesthetic or technical success in certain sports demand such weight reduction.

This, of course, raises the question of whether there is any energy level below energy balance where one can maintain normal reproductive health. In light of the fact that half the women in America on any given day are on a diet, and the prevalence of amenorrhea is increased in dieting women as well as in athletes, this question is important and warrants an answer. Additional research should help to provide a more adequate response.

Steen: Prevention involves educating athletes, coaches, parents, training staffs, administrators, and health care professionals about the female triad. According to Benson and colleagues, such an education program may address the following: 1) giving athletes the message that sports participation is congruous with physical and mental health; 2) encouraging a change in thinking on the part of coaches, parents, and administrators about winning at all costs; 3) establishing and promoting eating habits for health (with emphasis on adequate calories, protein, calcium, and iron) and successful performance; 4) emphasizing strength and stamina, and de-emphasizing body weight; 5) addressing misconceptions about weight, dieting, and performance; 6) helping young athletes to accept that sexual maturation and development are normal and desirable; and 7) encouraging athletes to discuss changes in menstrual and/or eating patterns with a confidential contact person.

Johnson: An additional point worth stressing is the fact that women need to realize that we are all genetically different- -some of us may be predisposed to carrying more body fat than others, and may not be able to lose below a particular percentage of body fat without significantly restricting food intake. Women who keep this in mind, and accept their body type and shape, will be much less likely to try to change their shape via unhealthy dietary practices. Many of the women that I see with the "triad syndrome" also have psychological issues that result in the development of their eating disorder. These issues can include poor coping skills, low self-esteem, lack of identity, and even abuse issues such as rape, among other things.

Are there any warning signs that might alert a coach or trainer to the development of habits that could result in the manifestation of the female athlete triad?

Johnson: Yes. Eating or exercise-related behaviors that can act as a warning sign would include the athlete's making frequent comments about her weight or shape, a decrease in food intake at meals, refusing to eat with other people (i.e., teammates on a road trip), bathroom visits after meals, criticism about the eating patterns of others, and excessive exercise outside of the normal training regimen. Non-food related behaviors to watch for include the athlete's inability to relax (she's in constant motion), her tendency to be highly self-critical, her need for a very structured daily schedule, abnormal anxiety about an injury, and her preference to be alone.

Steen: In addition to the behaviors outlined by Dr. Johnson, there are various internal and external factors that may predispose athletes to the female triad. It is useful for coaches, trainers, and health care professionals to familiarize themselves with these factors. Internal factors include a focus on thinness or ideal body weight; life stress; perfectionism; sudden changes in body weight; and menstrual irregularities. External factors include pressure from parents/coaches/friends to win at all costs; frequent weigh-ins; over-controlling parents or coaches; and a family history of eating disorders.

Loucks: I believe that it is important for a coach or athletic trainer to look at his or her own behavior, and the type of pressure that he/she is putting on their athletes to reduce body weight. The first opportunity to screen for the female athlete triad is during the preparticipation medical examination. Later medical exams should also be occasions for inquiring about possible behaviors and symptoms that might be suggestive of the triad. In addition, coaches and athletic trainers should routinely monitor and record the menstrual cycles of their athletes so that they notice disruptions as soon as they occur.

Eichner: Besides the behavioral clues mentioned by the other respondents, there can be physical clues, although these are absent or subtle in early cases. Signs of anorexia can include major fat and muscle loss, dry hair and skin, cold hands and feet, slow pulse and low blood pressure, and fine hair (lanugo) on the face and body, giving a "furry" appearance. Signs of bulimia can include "chipmunk cheeks" (enlarged parotid glands), puffy face or ankles, and-from repeated, self-induced vomiting-knuckle scars, bloodshot eyes, and/or erosion of tooth enamel. Other practical articles about this triad are by Angela Smith in 1996 and Aurelia Nattiv in 1994 (see suggested reading list).

Selected Readings:
Benson, J.E., Engelbert-Fenton, K.A., Eisenman, P.A. Nutritional aspects of amenorrhea in the female athlete triad. Int. J. Sport Nutr. 1996, 6:134-145.
Dueck, C.A., Matt, K.S., Manore, M.M., Skinner, J.S. A diet and training intervention program or the treatment of athletic amenorrhea. Int. J. Sport Nutr. 1996, 6:24-40.
Heltand, M.L., Haarbo, J., Christiansen, C., Larsen, T. Running induces menstrual disturbances but bone mass is unaffected except in amenorrheic women. Am. J. Med. 1993, 95:53-60.
Johnson, M.D. Disordered eating in active and athletic women. Clin. Sport Med. 13(2): 355-369, 1994.
Kirchner, E.M., Lewis, R.D., O'Connor, P.J. Effect of past gymnastics participation on adult bone mass. J. Appl. Physiol. 1996, 80: 226-232.
Lindholm, C., Hagenfeldt, K., Ringhertz, H. Bone mineral content of young female former gymnasts. Acta Paediatr. 1995, 84:1109-1112.
Loucks, A.B. The reproductive system. In: Perspectives in Exercise Science and Sports Medicine, Vol. 9: Exercise and the Female- -A Life Span Approach., Bar-Or, O., D. Lamb, and P. Clarkson (Eds), Cooper Publishing Co., 41-71, 1996.
Micklesfield, L.K., Lambert, E.V., Fataar, A.B. et al. Bone mineral density in mature, premenopausal ultramarathon runners. Med. Sci. Sports Exerc. 1995, 27:688-696.
Nattiv, A. The female athlete triad: managing an acute risk to long-term health. Phys. Sportmed. 1994, 22(1):60-68.
Nattiv, A., Agostini, R., Drinkwater, B., Yaeger, K.K. The female athlete triad. Clin. Sport Med. 1994: 13(2): 405-418.
Smith, A.D. The female athlete triad: causes, diagnosis, and treatment. Phys. Sportmed. 1996, 24(7):67-86.