The female athlete triad refers to the interrelated problems of disordered eating, amenorrhoea and osteoporosis as determined by the Task Force of the American College of Sports Medicine in 1992.
Those at risk of developing the triad are adolescents, women under stress and athletes (Talbott 1996, Otis and Goldingay 2000). In the athletic world, young female athletes appear to be most at risk as they are driven to excel in their chosen sport and pressured to fit a specific athletic image in order to achieve their goals. This puts them at risk of developing disordered eating patterns, which may lead to menstrual dysfunction and subsequent premature osteoporosis (Nattiv et al 1994, Thein and Thien 1996, Otis and Goldingay 2000). It is thought that the underlying cause of this problem is not exercising or participating in sports but rather the drive of girls and women to be unrealistically thin by restricting calorific intake in a misguided attempt to improve performance (Nattiv et al 1994, Otis and Goldingay 2000, Warren and Goodman 2003).
What is disordered eating?
Disordered eating, which includes skipping meals, eating less, vomiting, the use of laxatives and the use of diuretics, varies from mild to severe (Van de Loo and Johnson 1995, Thein and Thien 1996). Severe disordered eating can lead to the clinically recognised eating disorders of anorexia nervosa or bulimia nervosa (Johnson 1994, Sanborn et al 2000).
Sports where disordered eating is prevalent include gymnastics, dancing, figure skating, long-distance running and where the athlete is judged by appearance or low body fat is seen as an advantage (Yurth 1995, Smith 1996, Thein and Thien 1996, Otis and Goldingay 2000, Byrne and McLean 2002,Sundgot-Borgen and Torstveit 2004).
As athletes with disordered eating tend to be secretive about their behaviour, friends, parents, coaches and physicians must remain alert, looking for changes in behaviour such as eating alone, making trips to the bathroom during or after meals, or the use of laxatives (Smith 1996). Symptoms may include fatigue, anaemia, depression, intolerance to cold, lanugo (down like hair that appears all over the body to act as insulation in the absence of body fat), eroded tooth enamel from vomiting, dry skin and hair loss (Yurth 1995, Smith 1996, Thein and Thien 1996).
What is amenorrhoea?
Amenorrhoea is a spectrum of menstrual irregularities that may be seen in female athletes, the three principal types observed being anovulation, luteal phase deficiency and athletic amenorrhoea (Otis 1992, Van de Loo and Johnson 1995, Talbott 1996).
Anovulation is characterised by low progesterone levels, although the levels of oestrogen are adequate, resulting in no ovulation (Otis 1992, Thein and Thein 1996). Luteal phase deficiency is a shortened luteal phase and insufficient progesterone (Otis 1992). The total menstrual cycle is usually of normal length making the deficiency difficult to detect.
Athletic amenorrhoea is classified as primary, whereby puberty is delayed and menses has not occurred, and secondary, whereby menstruation has stopped for three months, if cycles were regular, or six months if irregular (Otis and Goldingay 2000, Warren and Goodman 2003).
Athletic amenorrhoea is thought to be hypothalamic-induced: production of the hypothalamic gonadotropin-releasing hormone (GnRH) is reduced, leading to a reduction of oestrogen and progesterone release from the ovaries (Wolman 1994, Wiggins and Wiggins 1997, Warren and Goodman 2003).
A decrease in GnRH levels has been linked with higher levels of cortisol in amenorrheic athletes (Kanaley et al 1992, Wiggins and Wiggins 1997, Francis-Cheung 1998). Although of possible short-term benefit, long-term elevated levels of cortisol accentuates loss of calcium from the bone, leading to a possibility of osteoporosis (Kanaley et al 1992).
It is important to note that menstrual irregularities can also occur in the absence of an eating disorder (Manore 1999, Manore 2002). This may occur when demands for energy are high due to exercise, and the athlete may be energy-deficient even though she may be consuming meals that would be considered normal for a healthy sedentary woman (Drinkwater 1996). This has been observed in vegetarian athletes (Otis 1992). Furthermore, menstrual irregularities can occur before any substantial weight loss or in the presence (versus absence) of body fat, as the threshold for onset of menstrual disturbances varies from person to person and from sport to sport (Arena et al 1995, Yurth 1995, Thein and Thien 1996, Skierska et al 1996).
Athletic amenorrhoea is said to usually be reversible when the stresses responsible for its development are eliminated (Arena et al 1995). However, prolonged amenorrhoea may result in a shortfall in bone density, not necessarily restored after resumption of menses (Carbon 1994, Keen and Drinkwater 1997, Warren and Goodman 2003).
What is osteoporosis?
Osteoporosis is a disease characterised by low bone mass, bone fragility and subsequent increased risk of non-traumatic fractures, often associated with post-menopausal women (Heaney 1993, Wiggins and Wiggins 1997, Furia 1999). The diagnostic criterion for osteoporosis is bone mineral density (BMD) more than 2.5 standard deviation below the mean of young adults, as measured by dual energy x-ray absorptiometry. Osteopenia describes BMD between 1 and 2.5 standard deviation below the mean of young adults. As this condition is significantly more prevalent than osteoporosis, it is suggested that osteopenia, and not osteoporosis, should be among the criteria for defining the female athlete triad syndrome (Burke and Deakin 1994, Khan et al 2002).
Bone mass is accumulated in the first three decades of life although peak mass is thought to be reached around 18 to 20 years (Burke and Deakin 1994, Yurth 1995, Talbott 1996, Warren and Goodman 2003). The lack of oestrogen in young athletes with primary amenorrhoea puts them at risk of osteopenia as a consequence of inadequate bone formation (Heany 1993, Thein and Thien 1996, Warren and Goodman 2003).
Any athlete presenting with any one of the disorders should be screened for the others (Manore 1999). Treatment lies in prevention and requires a multidisciplinary approach that includes psychological support and a reduction in training (Smith 1996, Keen and Drinkwater 1997, Furia 1999, Otis and Goldingay 2000).
Nutritional education is relevant to coaches, athletes and family members. The disadvantages of inadequate eating should be emphasised:
- Most weight loss is due to loss of muscle tissue
- Low levels of lean body tissue makes training ineffectual
- Carbohydrate is essential for muscle glycogen stores
- Low energy intake depresses resting metabolic rate
- Eating orders may lead to amenorrhea and possibly osteopenia (Burke and Deakin 1994)
Research has shown that nutrition may counteract or override the effects of an oestrogen deficiency on bone turnover (Zanker 1999). Women with anorexia nervosa have been seen to have a gradual increase in bone mineral density with feeding, even without resumption of menses (Zanker 1999).
Although studies differ on whether exercise alone is responsible for menstrual dysfunction, it is clear that athletes with an eating disorder, or not eating enough to meet energy demands, and following a strict exercise regime are at high risk of developing a menstrual disorder which may result in osteopenia.
Arena B, Maffulli N, Maffulli F, Morlea MA (1995) Reproductive hormones and menstrual changes with exercise in female athletes. Sports Medicine 19(4):278-87.
Burke L, Deakin V (1994) Clinical Sports Nutrition. McGraw-Hill Book Company, Australia.
Byrne S, McLean N (2002) Elite athletes: effects of the pressure to be thin. Journal of Science and Medicine in Sport 5(2):80-94.
Carbon R (1994) ABC of sports medicine: female athletes. British Medical Journal 309(6949): 254-258.
Drinkwater BL (1996) The female athlete triad. Strength and Conditioning 18(2):31.
Francis-Cheung T (1998) A Break in your Cycle – The Medical and Emotional Causes and Effects of Amenorrhea. Chronimed Publishing, Minneapolis.
Furia J (1999) The female athlete triad. Medscape Orthopaedics and Sports Medicine, 3(1), Medscape Inc.
Heaney RP (1993) Nutritional factors in osteoporosis. Annual Reviews in Nutrition 13:287-316.
Johnson M (1994) Disordered eating in active and athletic women. Clinics in Sports Nutrition 13(2):355-369.
Kanaley JA, Boileau RA, Bahr JM, Misner JE, Nelson RA (1992) Cortisol levels during prolonged exercise: the influence of menstrual phase and menstrual status. International Journal of Sports Medicine 13(4):332-6.
Keen AD, Drinkwater BL (1997) Irreversible bone loss in former amenorrheic athletes. Osteoporosis International 7(4):311-315.
Khan KM, Liu-Ambrose T, Sran MM, Ashe MC, Donaldson MG, Wark JD (2002) New criteria for female athlete triad syndrome? British Journal of Sports Medicine 36(1):10-13.
Manore MM (1999) Nutritional needs of the female athlete. Clinics in Sports Medicine 18(3): 549-563.
Manore MM (2002) Dietary recommendations and athletic menstrual dysfunction. Sports Medicine 32(14):887-901.
Nattiv A, Agostini R, Drinkwater B, Yeager KK (1994) The female athlete triad; the inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clinics in Sports Medicine, 13(2):405-418.
Otis CL (1992) Exercise-associated amenorrhea. Clinics in Sports Medicine 11(2):351-362.
Otis CL, Goldingay R (2000) The Athletic Woman’s Survival Guide. Human Kinetics, U.S.A.
Sanborn CF, Horea M, Siemers BJ, Dieringer KI (2000) Disordered eating and the female athlete triad. Clinics in Sports Medicine 19(2):199-213.
Skierska E, Socha T, Gajewski AK (1996) The risk of menstrual disorders in Polish elite swimmers. Biology of Sport 13(3):203-210.
Smith AD (1996) The female athlete triad: causes, diagnosis, and treatment. Physician and Sportsmedicine 24(7):67-86.
Sundgot-Borgen J, Torstveit MK (2004) Prevalence of eating disorders in elite athletes is higher than in the general population. Clinical Journal of Sport Medicine 14(1):25-32.
Talbott S (1996) The female athlete triad – not just for athletes. Strength and Conditioning 18(2):12-6.
Thein LA, Thien JM (1996) The female athlete. Journal of Orthopaedic and Sports Physical Therapy 23(2):134-48.
Van de Loo DA, Johnson MD (1995)The young female athlete. Clinics in Sports Medicine 14(3):687-707.
Warren MP, Goodman LR (2003) Exercise-induced endocrine pathologies. Journal of Endocrinological Investigation 26(9):873-878.
Wiggins DL, Wiggins ME (1997) The female athlete. Clinics in Sports Medicine 16(4):593-612.
Wolman RL (1994) Osteoporosis and exercise. British Medical Journal 309(6951):400-403.
Yurth EF (1995) Female athlete triad. Western Journal of Medicine, 162(2):149-50.
Zanker CL (1999) Bone metabolism in exercise associated amenorrhoea: the importance of nutrition. British Journal of Sports Medicine 33(4):228-229.