As more young girls and women participate in sports , concern increases for the inadequate dietary intake to support physical demands on their bodies. Overall, inadequate dietary intake is the primary nutritional concern for today's female athlete. For interested readers, several books and research publications address nutritional concerns of the female athlete and those associated with the female athlete triad. For example, The Athletic Woman's Survival Guide  and Sports Nutrition for Women  address concerns for dietary inadequacies, symptoms of the female athlete triad (disordered eating, amenorrhea, and osteoporosis), and respective strategies to prevent harmful health behaviors that lead to the triad. This review summarizes recent research that addresses nutritional concerns, plus strategies to treat and potentially prevent the debilitating effects of inadequate nutrition and related comorbidities in female athletes.
Concern for Dietary Inadequacies
Although the limitations of food records have been identified , this commonly used methodology is one that reveals energy and nutrient inadequacies in the diets of female athletes. As an example of energy inadequacy, Koutedakis and Jamurtas  found that female dancers consume less than 70% of the recommended daily energy needs. In addition, the researchers reported that the female athlete triad was commonly seen in dancers. When dietary intakes of adolescent female athletes (n = 60) were compared with recommended intakes for Italian adolescents, Cupisti et al.  also found energy inadequacies. In a review of nutritional concerns for child and adolescent athletes, Petrie et al. [7•] identified female distance runners as athletes at highest risk for mineral deficiencies (eg, iron and calcium). These minerals were also found deficient in the diets of adolescents studied by Cupisti et al. .
To possibly counteract nutrient inadequacies, female athletes often report using supplements for general health benefits or to compensate for inadequate diets. Kristiansen et al.  questioned control subjects and athletes from 17 Canadian varsity teams to determine the prevalence of supplement use and reasons for using supplements, among other issues. Results indicated that 63% of female athletes (n = 89) consumed a vitamin/mineral supplement, 25% took an iron supplement and 43% used a protein supplement. Meeting nutrient needs in one's diet was the most common reason for taking vitamin/mineral products. However compared with previous supplement research reports, prevalence of supplement use was higher in this study: 98.6% of the varsity athletes reported using at least one supplement in the past month. As female athletes become more aware of the need for energy and nutrient needs to prevent the harmful effects of the female athlete triad, increased supplement use may be expected and should be addressed in educational programs.
Concern for the Female Athlete Triad: Who Is at Risk?
Concern for the female athlete triad has continued since its recognition in 1992 by the American College of Sports Medicine. Recent posting of a position stand on the female athlete triad by the International Olympic Committee's Medical Commission (IOCMC) confirms this [9••]. In addition, a recent survey of Southern California high school athletes confirms that disordered eating, menstrual irregularity, and osteopenia continue as challenges for active young women. Of 170 female athletes representing eight sports, Nichols et al.  found 18.2%, 23.5%, and 21.8% of the athletes met criteria for disordered eating, menstrual irregularity, and low bone mass, respectively.
A decade ago, the American College of Sports Medicine position statement on the female athlete triad  listed a wide range of female athletes potentially affected by this syndrome. Individuals ranging from elite female competitors to nonathletic physically active females were identified as potential candidates developing conditions associated with the female athlete triad. Researchers have recently attempted to identify who is specifically at risk. Torstveit and Sundgot-Borgen  surveyed the total population of elite female athletes in Norway (n = 938) to answer the question who is at greater risk for the syndrome'the elite athlete or nonathlete. For comparison, nonathlete control subjects (n = 900) of the same age (13–39 years of age) were also invited to participate in the study. The questionnaire contained queries about personal histories of diet, training, menstruation, oral contraceptive use, weight control methods, injuries, in addition to the Body Dissatisfaction and Drive for Thinness subscales of the Eating Disorder Inventory. Numbers of usable questionnaires totaled 669 for athletes and 607 for nonathletes. Results revealed a higher percentage of controls (69.2%) classified at risk for the syndrome than athletes (60.4%). When separating athletes based on leanness within a sport, a higher percentage of athletes competing in leanness sports (70.1%) were classified at risk for the syndrome as compared with nonleanness sports (55.3%; P < 0.001). The type of sport also reflected differences in the risk level for elite athletes. A greater percentage of athletes competing in esthetic sports (66.4%) than ball game sports (52.6%) was classified as being at risk for the triad (P < 0.001). In a companion study, Torstveit and Sundgot-Borgen  randomly selected a smaller sample of the original study of 1838 subjects to participate in bone mass density assessments and clinical interviews. Final numbers totaled 186 athletes and 145 controls for this part of the study. Subjects were stratified based on age and risk profile (at risk or not at risk for the syndrome). Out of this group, eight athletes (4.3%) met all criteria for the female athlete triad, with five control subjects (3.4%) also meeting the criteria. When considering presence of only two criteria of the triad, 5.4% to 26.9% of the athletes exhibited two conditions, whereas 12.4% to 15.2% of the control subjects did the same. Overall findings of these two studies support the concern for female athletes being at risk for the female athlete triad and illustrates that normal active females experience the same adverse effects as athletes. For this Norwegian population, it can be summarized that concern for developing the triad comorbidities continues for all women, whether they are competing at an elite level or not competing, but yet physically active.
In the United States, similar research questions about athletes at risk for the female athlete triad were answered by Reinking and Alexander . Their population consisted of 84 collegiate athletes and 62 nonathletes at a National Collegiate Athletic Association Division I institution in the United States. Subjects completed a questionnaire containing questions about anthropometric measures, menstrual and exercise histories, and questions from the Eating Disorders Inventory. Results revealed no significant difference in the average body weights between athlete and nonathlete groups. For both athletes and nonathletes, 21% of the subjects reported either oligomenorrhea or amenorrhea; however, no difference in menstrual status existed between the two groups, or between lean and nonlean sport athletes.
Amenorrhea and Oligomenorrhea Among Female Athletes
Prevalence of menstrual irregularities in female athletes range from 6% to 79% and vary with type of athlete and intensity of activity . Identified causes of amenorrhea include energy deficit, severe emotional stress, and athletic training in which leanness is emphasized. Although early research indicated a relationship between body composition and amenorrhea, recent evidence support changes in energy balance and potentially the composition of calories as influences on menstrual irregularities in female athletes. A review by Stafford [16•] of the altered hypothalamic-pituitary-ovarian axis and its relationship to menstrual irregularities supports energy balance as the determining factor for menstrual dysfunction. This is also supported by previous reviewers . Research cited from animal and human models support a negative energy balance as the likely cause of exercise associated menstrual disturbances. The IOCMC position stand [9••] also supports the concept of insufficient energy availability as the reason for most cases of exercise-associated amenorrhea. When related to diet composition, the practice of restricting fat has been reported to be 50% greater in amenorrheic athletes than those who were eumenorrheic [16•].
Concerns for the nutritional status of a female athlete are obviously raised when one observes fasting, skipping of meals, consumption of hypocaloric meals, and low fat intakes by the athlete. All of these behaviors can lead to negative energy balances in combination with increased physical training; hence, the potential beginning of menstrual irregularities and eventual bone loss. Gibson et al.  showed that disordered eating was strongly correlated with menstrual irregularities in a cross sectional study of 50 British national and international middle- and long-distance female runners. As expected by the researchers, the menstrual status determined the bone mineral density (BMD) at three measurement sites; therefore, the effect of disordered eating to reduce BMD was explained by its relationship to menstrual irregularities. If health professionals can arrest disordered eating in female athletes, potential exists to decrease the proliferation of the female athlete triad in today's female athletes.
Is Low Bone Density a Concern for Female Athletes?
Physical activity has traditionally been recognized to maintain and increase BMD. The question asked by health professionals working with athletes is “does this generalization apply to female athletes?”
Through the 1980s and 1990s, several researchers reported young amenorrheic athletes with low bone density . Of all athletes, female runners have been recognized as high risk for amenorrhea and low bone density. After controlling for differences in body size and age in female runners, Burrows et al.  found that the distance run per week was negatively associated with lumbar spine BMD (P = 0.035) and femoral neck BMD (P = 0.006). Of the 52 athletes, 23% were classified as oligo- or amenorrheic and 77% as eumenorrheic. In contrast to what one might expect, no significant correlation (r = 0.004) existed between energy intake and distance run per week. In review of mechanisms in which nutritional disorders cause reduced bone mass, disordered eating behavior has been identified as the predominant factor in causing osteopenia . Cobb et al.  agreed with this finding in their study of 91 competitive female distance runners aged 18 to 26 years of age. Disordered eating was strongly related to menstrual irregularity, which was associated with low BMD. Disordered eating was also associated with low BMD in the absence of menstrual irregularity. From a nutritional perspective, disordered eating, whether initiated by dieting or self-imposed beliefs, can lead to the negative energy intake that contributes to decreased dietary mineral support for healthy bone.
Of interest to young female athletes currently diagnosed with low BMD, Fredericson and Kent [23•] report the case of a distance runner initially presenting with primary amenorrhea, low body weight (body mass index [BMI] = 15.8 kg/m2) and low BMD in the spine (74% normal) at the age of 22.9 years. After initial use of oral contraceptives for 2 years to correct menstrual status, BMD did not change. At the age of 25.1 years, the runner began to improve her diet and eventually gained weight. A healthy BMI of 21.3 kg/m2 was achieved at the age of 30.8 years and her BMD increased to almost normal levels (spine: 94% of normal; hips: 96% of normal). This case reinforces the primary need for sufficient energy intakes to meet energy demands of exercise and to prevent menstrual irregularities and bone reduction.
What Are Other Challenges and Concerns for Female Athletes?
The adverse consequences of the female athlete triad are recognized as significant contributors to the incidence of stress fractures in the female athlete . Cross-country runners, who are commonly known to possess a high incidence of stress fractures, have been determined to be at higher risk than gymnasts for low bone mass .
A recently identified concern for female athletes is the association of amenorrhea and osteoporosis with cardiovascular disease. In a review paper Prather and Hunt  report work by Zeni Hoch et al.  who studied 20 female runners who had amenorrhea and oligomenorrhea. Those runners with athletic amenorrhea exhibited a reduced endothelium-dependent dilation of the brachial artery. This suggests that afflicted female athletes may be predisposed to the development of heart disease. Jorgensen et al.  found low bone mass associated with an increased risk of echogenic calcified atherosclerotic plaques in postmenopausal women. Together, this evidence of an association of amenorrhea and low bone mass with heart disease suggests a more insidious effect of the female athlete triad.
Another potential disease that is more frequently diagnosed in athletes is celiac disease, a hereditary disorder that causes malabsorption of gluten- or gliadin-containing foods and eventual weight loss. Two recent case reports of collegiate female athletes diagnosed with this common intestinal disorder highlight the need for health professionals and athletic trainers to be aware of the diagnosis and treatment of celiac disease [29,30].
Strategies to Treat and Prevent the Female Athlete Triad
In relation to sports performance, the IOCMC position stand emphasizes the female athletes' health as primary importance [9••]. Sherman and Thompson [31•] provide a useful case presenting common issues that a health professional might encounter when working with female athletes. The case illustrates application of principles for referral, evaluation, and treatment of a hypothetical female athlete.
Several researchers [10,32] suggest preparticipation screening as part of a preventive approach to identify high-risk athletes. Once identified and diagnosed with the female athlete triad or a component of the triad, the athlete should be treated by a team of health professionals: physician, dietitian, and psychologist (psychiatrist for athletes diagnosed with a clinical eating disorder). Other professionals who can contribute to or participate in the treatment plan include athletic trainers, exercise physiologists, and the athlete's coach and parents.
In the preparticipation screening to determine presence of symptoms of the female athlete triad, Waldrop  includes the following dietary behavior questions that ask if the athlete is 1) happy with her current weight (if not, why?); 2) vegetarian or vegan (if yes, identify possible nutrient deficiencies); 3) dieting (if yes, at what age dieting began); 4) skipping meals (if yes, which meals?); 5) attempting to lose weight with laxatives, diet pills or diuretics, vomiting, or extra exercise (if yes, determine reason); 6) taking any vitamin or mineral supplements; and 7) eating for the last 24 hours (or record of 3 days). A food record can reveal irregular eating patterns and energy/nutrient inadequacies.
Ziegler et al.  found dieting to begin at the age 12 ± 3 years in their study of US and international synchronized female figure skaters. Energy intakes of the skaters were found to be below the recommended 2000 to 2500 kcal/d and 47 kcal/kg for this population. From results of this study, the researchers recommended adding self appraisals about physical self, emotions, and satisfaction with body shape and weight to the screening process. By using multiple indicators of body image and body weight concerns, it was felt that health professionals could better assess a high-risk athlete. Overall, a comprehensive assessment including a diet history, physical examination, mental health screening, exercise history, and a bone density test, is recommended to identify symptoms of the female athlete triad. This assessment can be used to target any female athlete at risk for developing disordered eating, plus monitor and possibly prevent the proliferation of harmful behaviors within teams.
If the athlete is diagnosed with any symptom of the triad, the primary goal of therapy is to increase energy availability, either by increasing food intake or decreasing energy expenditure, for the eventual restoration of the reproductive and metabolic hormones. If therapy does not succeed, use of low-dose oral contraceptives can potentially raise estrogen levels and prevent bone loss . Because osteopenia is a result of the female athlete triad, the American Academy of Pediatrics  also recommends a dietary supplement of calcium carbonate (1500 mg/d) to reduce bone loss in the amenorrheic female athlete. Consumed for one year, the addition of 800 mg/d of supplemental calcium to diets of young adult female distance runners with habitual calcium intake of 1000 mg/d has been shown to prevent cortical bone loss, but not that of trabecular bone . After examining the contribution of meals and snacks to energy and nutrient intakes of elite figures skaters during their competitive season, Ziegler et al.  recommends that athletes be encouraged to consume more energy- and nutrient-dense small meals throughout day to ensure sufficient intakes.
Counseling athletes and using structured programs can be used to change and possibly prevent harmful behaviors central to the female athlete triad. Commonly used in nutritional counseling, the Stages of Change Model is also recommended to reduce harmful behavior in female athletes diagnosed with disordered eating and associated comorbidities [33,38]. A recommended approach for teams, rather than individual athletes, involves a scripted structured program that requires minimal training. After defining the curriculum from a survey of 1178 self reported female athletes from 13 Oregon schools, Elliot et al. [39••] developed the Athletes Targeting Healthy Exercise and Nutrition Alternatives (ATHENA) intervention to deter disordered eating and body-shaping drug use. The scripted, coach-facilitated, peer-led eight-session program reduced ongoing and new use of diet pills, in addition to decreasing female athletes' intentions toward disordered eating behaviors and body-shaping drug use. Awareness programs about the female athlete triad to athletes, trainers, coaches, doctors, judges, and sports governing bodies are also recommended to decrease the prevalence of this debilitating syndrome [32,40].
With expectations that the numbers of female athletes will increase, health professionals have an obligation to promote awareness and provide education about the female athlete triad to individuals and organizations associated with girls and woman participating in athletics. Because the female athlete triad originates from harmful behaviors that lead to insufficient energy intake for performance and health, increased attention to the nutritional concerns of all female athletes, regardless of level of competition, is required to prevent the triad. Comprehensive preparticipation screening and structured education programs can target at-risk athletes for counseling and promote positive health behaviors in this population.
References and Recommended Reading
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
1. Tammelin T, Nayha S, Hills AP, Jarvelin MR: Adolescent participation in sports and adult physical activity.Am J Prev Med
2. Otis CL, Goldingay R: The Athletic Woman's Survival Guide. Champagne, IL: Human Kinetics; 2000.
3. Bean A, Wellington P: Sports Nutrition for Women. London: A & C Black; 2001.
4. Braakhuis AJ, Meredith K, Cox GR, et al.
: Variability in estimation of self-reported dietary intake data from elite athletes resulting from coding by different sports dietitians.Int J Sport Nutr Exerc Metab
5. Koutedakis Y, Jamurtas A: The dancer as a performing athlete: Physiological considerations.Sport Med
6. Cupisti A, D'Alessandro C, Castrogiovanni S, et al.
: Nutrition knowledge and dietary composition in Italian adolescent female athletes and non-athletes.Int J Sport Nutr Exerc Metab
7.• Petrie HJ, Stover EA, Horswill CA: Nutritional concerns for the child and adolescent competitor.Nutrition
For those working with children and adolescents, this review presents general nutritional needs for young athletes in endurance sports, strength and weight-class sports, and nutrition specific to team sports.
8. Kristiansen M, Levy-Milne R, Barr S, Flint A: Dietary supplement use by varsity athletes at a Canadian University.Int J Sport Nutr Exerc Metab
9.•• International Olympic Committee Medical Commission Working Group on Women in Sport: Position stand on the female athlete triad.
Available at: http://multimedia.olympic.org/pdf/en_report_917.pdf
. Accessed June 9, 2006.
This position stand should be viewed as required reading for any health professional working with female athletes. Information in the appendices can be helpful to coaches and health professionals.
10. Nichols JF, Rauh MJ, Lawson MJ, et al.
: Prevalence of the female athlete triad syndrome among high school athletes.Arch Pediatr Adolesc Med
11. Otis CL, Drinkwater B, Johnson M, et al.
: American College of Sports Medicine position stand. The female athlete triad.Med Sci Sports Exerc
12. Torstveit MK, Sundgot-Borgen J: The female athlete triad: Are elite athletes at increased risk?Med Sci Sport Exerc
13. Torstveit MK, Sundgot-Borgen J: The female athlete triad exists in both elite athletes and controls.Med Sci Sport Exerc
14. Reinking MF, Alexander LE: Prevalence of disordered-eating behaviors in undergraduate female collegiate athletes and nonathletes.J Athl Train
15. Warren MP, Perlroth NE: The effects of intense exercise on the female reproductive system.J Endocrinol
16.• Stafford DEJ: Altered hypothalamic-pituitary-ovarian axis function in young female athlete: Implications and recommendations for management.Treat Endocrinol
This review addresses the hypothalamic-pituitary-ovarian axis as central to menstrual irregularities in young female athletes and therapeutic recommendations to correct the irregularity. Treatment is aimed at restoring normal menstrual function by increasing energy intake.
17. Eliakim A, Beyth Y: Exercise training, menstrual irregularities and bone development in children and adolescents.J Pediatr Adolesc Gynecol
18. Gibson JH, Mitchell A, Harries MG, Reeve J: Nutritional and exercise-related determinants of bone density in elite female runners.Osteopos Int
19. Rencken M, Chestnut III CH, Drinkwater BL: Decreased bone density at multiple skeletal sites in amenorrheic athletes.JAMA
20. Burrows M, Nevill AM, Bird S, Simpson D: Physiological factors associated with low bone mineral density in female endurance runners.Br J Sport Med
21. Miller KK: Mechanisms by which nutritional disorders cause reduced bone mass in adults.J Womens Health (Larchmt)
22. Cobb KL, Bachrach LK, Greendale G, et al.
: Disordered eating, menstrual irregularity, and bone mineral density in female runners.Med Sci Sports Exerc
23.• Fredericson M, Kent K: Normalization of bone density in a previously amenorrheic runner with osteoporosis.Med Sci Sports Exerc
Interesting case report of athlete returning to normal bone levels after missing the window for bone growth. Emphasizes the importance of energy intake in recovery.
24. Joy EA, Campbell D: Stress fractures in the female athlete.Curr Sports Med Rep
25. Bemben DA, Buchanan TD, Bemben MG, Knehans AW: Influence of type of mechanical loading, menstrual status, and training season on bone density in young women athletes.J Strength Cond Res
26. Prather H, Hunt D: Issues unique to the female runner.Phys Med Rehabil Clin N Am
27. Zeni Hoch A, Dempsey RL, Carrera GF, et al.
: Is there an association between athletic amenorrhea and endothelial cell dysfunction?Med Sci Sports Exerc
28. Jorgensen L, Joakimsen O, Rosvold-Bernstsen GK, et al.
: Low bone mineral density is related to echogenic carotid artery plaques: a population-based study.Amer J Epidemiol
29. Leone JE, Gray KA, Massie JE, Rossi JM: Celiac disease symptoms in a female collegiate tennis player: Case report.J Athl Train
30. Eberman LE, Cleary MA: Celiac disease in an elite female collegiate volleyball athlete: case report.J Athl Train
31.• Sherman RT, Thompson RA: Practical use of the International Olympic Committee Medical Commission position stand on the female athlete triad: a case example.Int J Eat Disord
Implications of the International Olympic Committee Medical Commission position stand on the female athlete triad are discussed in terms of the athlete's health being primary to her performance.
32. Loucks AB, Nattiv A: Essay: the female athlete triad.Lancet
33. Waldrop J: Early identification and interventions for female athlete triad.J Pediatr Health Care
34. Ziegler PJ, Kannan S, Jonnalagadda SS, et al.
: Dietary intake, body image perceptions, and weight concerns of female US International synchronized figure skating teams.Int J Sport Nutr Exerc Metab
35. American Academy of Pediatrics: Committee on sports medicine and fitness. Medical concerns in female athletes. Pediatrics
36. Winters-Stone KM, Snow CM: One year of oral calcium supplementation maintains cortical bone density in young adult female distance runners.Int J Sport Nutr Exerc Metab
37. Zeigler PJ, Jonnalagadda SS, Nelson JA, et al.
: Contribution of meals and snacks to nutrient intake of male and female elite figure skaters during peak competitive season.J Am Coll Nutr
38. Bass M, Turner L, Hunt S: Counseling female athletes: application of the stages of change model to avoid disordered eating, amenorrhea, and osteoporosis.Psychol Rep.
39.•• Elliot DL, Moe EL, Goldberg L, et al.
: Definition and outcome of a curriculum to prevent disordered eating and body-shaping drug use.J Sch Health
This program holds promise as a preventive program for disordered eating and related behaviors in athletes. Programs for females (ATHENA) and males (ATLAS, prevention of steroid use) are presented.
40. De La Torre DM, Snell, BJ: Use of the preparticipation physical exam in screening for the female athlete triad among high school athletes.J School Nurs