Defining the Term ‘Female Athlete Triad’

Introduction
The female athlete triad refers to the interrelationships among energy availability, menstrual function, and bone mineral density (BMD), which may have clinical manifestations including eating disorders, functional hypothalamic amenorrhea, and osteoporosis (Nattiv et al. 1994). It is unfortunately a disorder which often goes unrecognised in female athletes.
The female athlete triad is caused by an energy drain where there is a caloric deficitdue to the athlete’s energy expenditure exceeding herdietary energy intake (Nattiv et al. 1994). Whether known to the athlete or not, thislow level of energy availability causes disruption of the hypothalamic-pituitary-ovarian axis,which results in decreased gonadotropin-releasing hormone (GnRH)pulsatility and low luteinizing hormone (LH) and follicle-stimulating hormone (FSH) levels (Loucks 1990). This then leads to a decreased estrogen production which causes menstrual dysfunction. These decreased estrogen levels in turn affect calcium resorption and bone accretion, which cause decreased bone health (Gottschlich & Young, 2006).

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The 3 components of the triad are all inter-related through physiological and psychological means as shown in Fig. 1. The common psychological pressures to repeatedly put in a performance of optimal standard and often the perceived requirement to maintain a low body mass for certain sports, result in a large amount of training. This large amount of training combined with a low energy intake, and also in addition to the stress hormones produced by psychological stress, may lead to a physiological alteration in the endocrinological control of the menstrual cycle, which may lead to the athlete becoming amenorrhoeic. The consequence of becoming amenorrhoeic through dysfunction of the hypothalamus and pituitary is that the production of oestrogen will decrease. This hormone has a major role in maintaining adequate BMD. Therefore, a hypo-oestrogenic state is associated with a low BMD and an increased risk of osteoporosis (Birch, 2005).
Not all sufferers have all 3 components of the female athlete triad however. In recent years, new studies are continuing to emerge indicating that even having just1 or 2 elements of the triad significantly increases these women’s long-term morbidity. In addition to this, a study by Burrows et al. (2007) has suggested that the current triad elements do not identify allwomen at risk from the syndrome,rather thatcriteria such as exercise-related menstrual alterations, disordered eating, and osteopenia may be more appropriate (Gottschlich & Young, 2006).
Eating disorders
There is a reduced energy availability (the amount of dietary energy remaining for other body functions after exercise training such as cellular maintenance, thermogenesis, immunity, growth, reproduction, and locomotion) associated with disordered eating which is the result of an exercise energy expenditure greater than a dietary energy intake. This compensation by physiological mechanisms to reduce the amount of energy made available to these functions tends to restore energy balance in the body and promote survival, but consequently impairs health.
Extreme cases of eating disorders could include anorexia nervosa and bulimia nervosa. Many athletes do not meet the strict criteria for anorexia nervosa or bulimia nervosa that are listed by the American Psychiatric Association (1994) in the Diagnostic and Statistical Manual of Mental Disorders (Fig. 2) but will however, manifest similar disordered eating behaviours as part of the triad syndrome (Hobart and Smucker, 2000).
The term “anorexia athletica” or “disordered eating” has been used to distinguish between pathological anorexia and eating disorders associated with training and sports performance. The criteria for this include perfectionism, compulsiveness, competitiveness, high self motivation, menstrual disturbances, and at least one unhealthy method of weight control such as fasting, vomiting, and use of diet pills, laxatives, or diuretics (Birch 2005). The Diagnostic and Statistical Manual of Mental Disorders as mentioned above was reviewed by the American Psychiatric Association (2000) to include a more comprehensive classification of eating disorders not otherwise specified (EDNOS) for athletes who do not meet the criteria for anorexia nervosa or bulimia nervosa (Fig. 3).
Functional hypothalamic amenorrhea
Some clinical menstrual disorders are obvious to affected women such as oligomenorrhea (menstrual cycles ≥ 35 days) and amenorrhea (no cycles for > 90 days), but sub-clinical menstrual disorders are not, e.g. luteal deficiency and anovulation. Amenorrhea may be caused by a wide range of organic diseases, genetic abnormalities, energy deficiency, and stress. Medical tests are required to diagnose the etiology of amenorrhea so that appropriate care can be offered to sufferers of the syndrome (Manore et al. 2007).
Amenorrhea that is related to athletic training and weight fluctuation is caused by changes in the hypothalamus which result in decreased levels of estrogen. Amenorrhea in the female athlete triad, according to (Hobart and Smucker, 2000), can be classified as primary or secondary:

Primary amenorrhea: no spontaneous uterine bleeding in the following situations: (a) by the age of 14 years without the development of secondary sexual characteristics, or (b) by the age of 16 years with otherwise normal development.
Secondary amenorrhea: the absence of menstrual bleeding in a female for (a) 6 months with primary regular menses, or (b) 12 months with previous oligomenorrhea.

The type of amenorrhea caused by low energy availability associated with eating disorders is classified as functional hypothalamic amenorrhea (FHA). In FHA, ovarian function is suppressed by an abnormally slow frequency of luteinising hormone (LH) pulses in the blood. LH pulsatility is regulated in part by neurological pathways originating in specialised neurons which can sense the availability of oxidisable metabolic fuels (Wade & Jones, 2004).
There are many causes of menstrual disorders, many of which are not completely understood. Pulsatile release of luteinising hormone is decreased, which leads initially to luteal phase defects. In addition, women with luteal phase defects and amenorrhoea will have higher concentrations of growth hormone and cortisol and lower concentrations of leptin, insulin, and triodothyronine when compared with sedentary women. These hormones are related to metabolism, which means they are also related to nutritional and metabolic status. When these hormones indicate that energy availability is low over a period of time, the menstrual cycle will be temporarily suppressed in order to conserve energy (Birch 2005).
Osteoporosis
Osteoporosis, as defined by the American College of Sports Medicine (ACSM), is a disease characterized by low bone mass and microarchitectural deterioration of bone tissue, leading to enhanced skeletal fragility and increased risk of fracture (Otis et al. 1997).
This is the final component of thefemale athlete triadwhich exists on a continuum from optimal bone health to osteoporosis and focuses on bone strength, which consists of BMD and bone quality. Bone quality refers to bone turnover rates (resorption versus formation, time for maturation of the new bone matrix, microarchitecture or trabeculae, bone geometry and size, etc.).The inability to measure bone quality at this time leaves one half of the equation for bone health empty and offers an explanation for why some athletes may suffer more fractures even if they have the same poor bone density as their peers. Therefore, dual energy x-ray absorptiometry (DXA) scans are used as a quantitative measure of bone health. (Gottschlich & Young, 2006).
The World Health Organization (WHO) has established guidelines on how to classify BMD using dual energy radiographic absortiometry (DXA). Osteoporosis is defined as BMD greater than 2.5 standard deviations below the mean of young adults. Osteopenia is defined by a BMD 1 to 2.5 standard deviations below the mean of young adults (Kanis et al. 1994). Recently however, the International Society for Clinical Densitometry (ISCD) published a statement (Lewiecki et al. 2004) that the WHO’s guidelines for osteoporosis should not actually be used on healthy premenopausal females. They suggest instead that Z-scores should be used rather than T-scores for the diagnosis of osteoporosis in this particular population.
According to Brunet (2005), there is an increased risk for fracture in the elderly population as well as the young in conjunction with osteoporosis. Some of the associated risk factors include: thyroid or corticosteroid medications, smoking, a low calcium diet, amenorrhea, a family history of osteoporosis, a sedentary lifestyle, and a lack of hormone replacement therapy (HRT) post menopause (Bellantoni, 1996). According to the American Academy of Orthopedic Surgeons (1991), gender can play a part with females being 8 times more likely to develop osteoporosis than males. The reason for this is a decreased baseline bone mass and also, an increased level of bone absorption associated with menopause.
Treatment
The clinical suspicion alone that someone is suffering from female athlete triad should be sufficient indication to start with therapeutic and preventive steps, such as a reduction in training loads, an increase in bodyweight, and improvements in diet. These clinical suspicions could be based on personal history such as previous stress fractures, or based on the presence of other factors such as amenorrhea. These steps aim at returning estrogen production to normal levels by normalizing the disturbed menstrual cycle.
If this goal is not achieved, the lack of estrogens has to be treated with exogenous estrogens administration, particularly in the case of secondary amenorrhea, to ensure achievement of peak bone mass (PBM). If osteoporosis is documented, it is an additional indication for hormonal substitution. There are two ways to carry this out, and can be selected in relation to the age or to special wishes of the athletes like contraception and cycle control. Either estrogens as a part of a birth control pill or a HRT with natural estrogens and progestins. Both treatments need to consider the minimal dose of estrogens necessary for prevention of osteoporosis. In addition, sufficient intake of calcium and vitamin D may not be neglected. Regarding the long-term results of the proposed hormonal treatment, it has to be admitted that prospective results from longitudinal studies are completely lacking, and that more research is urgently needed (Roth et al. 2000).
Conclusion
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. Prevention, recognition, and treatment of these clinical conditions should be a priority of those who work with female athletes to ensure that they maximize the benefits of regular exercise. (Nattiv et al. 1994).
Prevention of the triad, or at least an early diagnosis of it, is certainly better than the cure. More efforts should be undertaken to appropriately inform physicians, athletes, coaches, officials and parents on all the different aspects of the triad. Dealing with this syndrome, according to Roth et al. (2000), may offer a chance to the female athlete the opportunity for a deeper reflection about her bodily function and the relative importance and perspective of performance and success in sports.
References

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