Participation of girls and women in sport has grown dramatically over the past decade. A recent report (2004–2005 data) on high school participation indicates that more than 2.9 million girls compete in high school sport . Although remarkable, this 13% increase from the late 1990s in high school rates is surpassed by the 51% increase in collegiate participation rates over the same period . It is clearly apparent that girls and women are training and competing for sport in record numbers. However, basic, applied, and clinical research on competitive female athletes and performance remains limited.
Researchers continue to investigate the response of girls and women to both acute and chronic exercise. The studies utilize a heterogeneous mix of women ranging from sedentary subjects to highly trained elite performers. Interpretation of findings as they relate to competitive female athletes is often difficult; therefore, an operational definition of competitive female athlete is used in this paper. A competitive female athlete is one who chronically trains with the primary aim of engaging competitively in an organized event or sport. Middle school-aged girls involved in club soccer programs and professional athletes alike are considered competitive athletes by this definition.
In the past several years there have been numerous topics of discussion related to elite female sport performance, including nutritional aids in endurance and power events, regulatory responses to thermal stress, and genotypic talent identification. Clinicians are forced to distill the plethora of materials into critical concepts for their female athletes and coaches. Three topics of debate and importance are the role of iron status in performance, female chronobiology and its role in performance, and the influence of energy status on sport performance. Each of these components is essential in the optimization of training outcomes for competitive female athletes.
Reductions in performance coupled with fatigue, lack of motivation to train, and physical decline are typical in competitive female athletes. Overtraining is a topic frequently discussed in both the lay media and in scholarly publications. Female athletes present to sport medicine physicians with short- and long-term fatigue. Poor iron status is often the cause of these symptoms . The iron status literature is overshadowed by inconsistent and often inappropriate usage of terminology making application of the findings difficult. Dilutional pseudoanemia is the common syndrome in athletes caused by plasma volume expansion. Typically, erythrocyte mass (RBC) is unchanged or slightly increased, resulting in a reduced hemoglobin concentration [4,5]. Both haptoglobin and ferritin are normal under these conditions. Exertional hemolysis was first reported in 1881 in soldiers following bouts of marching. Runners, swimmers, and triathletes have been reported with intravascular hemolysis with severity related to the intensity of the physical strain [4,6]. Hemolysis results in high erythrocyte volume, normal ferritin, and low haptoglobin . Iron deficiency with or without anemia has been extensively studied in athletes. Iron deficiency results from depletion of iron stores in concert with restricted iron supply to tissues . This trace mineral disorder is common in both athletes and nonathletes.
Iron status has been determined through several indicators with mixed results. Ferritin is often used and has been described as the most commonly used indicator of body iron stores [3,4,7]. Due to its rapid changes under conditions of inflammation, infection or disease, ferritin may not adequately reflect iron storage [3,4,8•]. Serum iron or transferrin (iron transport protein) show day to day variability causing difficulties in interpretation of the data [7,8•,9]. RBC, hemoglobin concentration (Hb), mean corpuscular volume (MCV), soluble transferring receptor concentration, and hematocrit (Hct) have all been used to provide a clear profile of iron status in female athletes [3,4].
Prevalence rates for iron deficiency in female athletes vary based on method, sport, age, and nutritional status. Risser et al.  reported 31% of female athletes with ferritin concentration below 12 ng/mL, transferring saturation less than 16%, or both. Others report rates as high as 82% of female athletes using a criterion of ferritin concentration below 25 μg/L . Our group reported rates exceeding 45% in elite competitive female swimmers using a combination of RBC, Hb, Hct, ferritin, and iron criteria [12,13]. Regardless, female athletes can develop iron deficiency with or without anemia, often resulting in reduced sport performance indicated through multiple mechanisms. Iron deficiencies in competitive female athletes are caused by blood loss or nutritional deficits [3,8•]. Our experience indicates a strong relationship between iron deficiencies and restrictive nutritional practices, including caloric restriction and vegetarian diets. The consequences of iron deficiency result in biochemical, physiologic, and morphologic changes in organs associated with reduced sport performance (Table 1).
Sport medicine professionals should educate female athletes and coaches regarding the recommended dietary allowance for iron. Nutritional education and monitoring of dietary intake by trained support staff should be included in the training program for all competitive female athletes. These efforts should be the initial intervention efforts. Use of iron supplementation should only be suggested following hematologic evaluation. Oral agents contain hydrated ferrous gluconate, ferrous fumarate, or ferrous sulfate  with varying doses of elemental iron. Iron supplementation should be prescribed with constant supervision due to the potential for gastrointestinal distress, constipation, or iron toxicity . Iron supplementation has been shown to produce ergogenic effects in athletes with normal iron status; however, the improvements in female athletes with poor iron status remain equivocal. Further research is necessary to more clearly delineate the improved endurance capacity in these clinically distressed female athletes.
Circamensal Rhythms and Performance
Sport periodization is based on the utilization of cycles, from microcycles to macrocycles or annual to quadrennial programs. Investigations into optimizing physical performance at critical competitive windows have helped many achieve success in sport. Recent work to identify differences within physiologic cycles (sleep-arousal, menstrual, temperature cycles) will help further our understanding and applicability of training programs to exploit these endogenous rhythms. Clinical aspects surround appropriate stress responses, seasonal hormonal alterations, and reproductive health. Of particular interest to sport scientists are the hormonal fluctuations across the female reproductive cycle. As Birch  discussed, delineation of the role fluctuating hormones (estradiol, progesterone, follicle-stimulating hormone, luteinizing hormone) may have on performance will require control of numerous factors including nutritional and training status along with ensuring consistent menstrual cyclicity.
Though continued interest exists in menstrual cycle variations and muscular activity, evidence to date supports no variation in maximal isometric strength  and peak torque in knee extension and flexion between phases of the menstrual cycle [16,17]. Birch and Reilly  discuss the influence of circadian rhythm in body temperature and level of arousal on muscle performance. They observed a significant difference in luteal phase versus follicular phase temperature (circamensal), and between the morning and evening temperature (diurnal) . A circamensal-diurnal interaction was reported (luteal phase only) with maximal power performance greatest in early evening during the luteal phase .
With the current level of sophistication in technology, menstrual cycle fluctuations boast little support for influencing performance (aerobic or intermittent). Oosthuyse et al.  observed no significant difference across the menstrual phase in cycling time trial finishing time in trained and untrained women. When the groups were combined a trend for a faster time was observed in the late follicular phase. Intermittent testing is used to mimic sport activity. Middleton and Wenger  utilized a 10 × 6 second cycle ergometer sprint test to evaluate total work output, work drop-off, and oxygen consumption (VO2) across the menstrual cycle. The average 6-second work and recovery VO2 was greater in the luteal phase than in the follicular phase. In contrast, numerous authors report no difference in physical or sport performance between menstrual phases .
One aspect of performance potentially affected by menstrual phase is fuel utilization during activity. Historically, female athletes have been suggested to possess higher lipid oxidation capacity thereby reducing reliance on carbohydrates during endurance activities. Evaluation of substrate utilization during physical performance under experimental conditions of altered estradiol and progesterone concentrations resulted in reduced carbohydrate oxidation during 60 minutes of submaximal exercise with high estradiol . Under conditions of elevated estradiol (232 pg/mL) and progesterone (47 ng/mL), no influence of carbohydrate oxidation was observed. Whether these findings occur during normal cycle fluctuations of progesterone and estradiol remains to be determined.
Data from studies assessing performance at different phases of the menstrual cycle yield varying results; this may be due to inconsistent menstrual cycle evaluation, lack of estradiol, and progesterone determination. In addition, studies divide the menstrual cycle into the luteal phase and follicular phase, whereas others further divide the cycle into early and late follicular and mid luteal. Performance assessments have ranged from maximal strength to endurance events. Most research identifies no affect of menstrual cycle on VO2max [23,24]. Submaximal aerobic performance reports similarly no difference across the menstrual cycle in VO2, heart rate, and rate of perceived exertion [23–26].
Currently there is insufficient evidence to recommend any treatment to alter an athlete's menstrual cycle for the purpose of performance maintenance or improvement. Education for athletes and coaches on the necessity for maintaining a consistent menstrual cycle and for appropriate energy intake would prove beneficial and time effective. Understanding the endogenous rhythms complementing and working in concert to ensure consistent sleep-wake, eating, basal body temperature, and reproduction cycles may help to develop more effective training strategies for the female athlete.
Importance of Energy in Performance
Over 15 years ago, scientists began to report a clustering of disorders presenting in female athletes more frequently than the general public [27–29]. The interrelated conditions included disordered eating, amenorrhea, and osteoporosis [29,30••,31,32]. With the rapid increase in participation of women in sport, more sport scientists began to investigate issues related to women's adaptation to physical exercise stress. The American College of Sports Medicine published a position stand on the female athlete triad in 1997 . Since that time, hundreds of published papers have described the prevalence, etiology, and treatment of the female athlete triad. Recently, significant debate has surrounded the triad, including its scientific underpinnings and potential implications to broad public health concerns for women [33–35]. The clinical implications of this debate remain to be seen, yet sport medicine professionals are pressured to enhance sport performance for competitive female athletes. To date, there is limited research into the role of the triad or its components on competitive sport performance.
A causal relationship between reduced useable metabolic fuels and menstrual cycle dysfunction has been illustrated across species by several groups [36–45]. Bioenergetic parameters including energy intake and energy expenditure are difficult to measure in free-living athletes, resulting in reduced acceptance of data reported by researchers using these methods . Biomarkers, such as thyroid hormones (tri-iodothyronine [TT3]) and somatotropic axis hormones (insulin-like growth hormone 1 [IGF-1]) have been closely related to the nutritional status of individuals [47–49] and give researchers a method to support dietary intake records. Low TT3 has been reported in amenorrheic athletes compared with eumenorrheic athletes  and has been induced in exercising women under energy restriction resulting in luteinizing hormone pulsatility changes . The influence of energy status on menstrual function has been established, yet its link to athletic performance remains unclear.
Our group has evaluated the influence of fuel availability on sport performance in competitive swimmers. We worked on the premise that an energy deficit would result in an altered hormonal and metabolic environment (hypometabolism) resulting in the inability to improve performance at the same rate as energy stable individuals. A total of 13 US National Team swimmers (average age 20.8 years) were evaluated over a 6-month season ending in a major competition. The women trained together and were evaluated on several parameters: 1) energy intake and expenditure, 2) thyroid and somatotropic axis status, 3) menstrual status, 4) macronutrient status, and 5) maximal training and maximal competitive performance. As expected, the swimmers exhibited varied levels of energy deficit from near balanced (∼ 150 kcal/d deficit) to undernutrition (∼ 1000 kcal/d deficit). The level of energy deficit was tightly linked to reductions in TT3 and IGF-1 at each month evaluated. Sport performance was assessed both through a competition-like 200-m time trial in practice and during competition at their season ending major events. Figure 1 illustrates the relationship between TT3 at the end of the season and the change in performance from the previous season's best time.
Swimmers were clustered into two groups: high TT3, high performance improvement and low TT3, low performance improvement. Interestingly, the athletes in the low TT3, low performance group had either oligomenorrhea or amenorrhea whereas high TT3 athletes were eumenorrheic. Similar results are evident when plotting time trial practice performance versus TT3. These data support the hypothesis that undernutrition resulting in menstrual dysfunction reduces the rate of performance improvement in elite competitive female athletes. The relationship between hypometabolism, suppressed hypothalamic-pituitary-gonadal axis function, and sport performance are also evident in data from junior elite-caliber female swimmers  and elite male swimmers in our laboratory.
Oral contraceptive use has grown in women participating in sport and physical activity. Female athletes with menstrual dysfunction are frequently prescribed oral contraceptives. Although oral contraceptive use generally results in positive menstrual cycle outcomes, the influence on long-term bone health remains unclear [29,30••,34]. Furthermore, research examining the interplay between oral contraceptive use and sport performance remains limited. Early research into the influence of oral contraceptives use during sport performance reported limited ergogenic value. However, longer (4–6 months) use of monophasic or triphasic oral contraceptives resulted in depressions in maximal aerobic capacity [51•]. Examination of oral contraceptive use and anaerobic performance or strength development is equivocal with no differences or declines in performance associated with oral contraceptive use. The potential benefits of exogenous estrogen use on muscle damage in humans are unclear, although animal data support the protective role of estradiol showing antioxidant properties. The role that these exogenous ovarian hormones play in physical performance remains to be fully elucidated.
Clinicians are faced with female athletes presenting with menstrual irregularities, often coupled with bone health issues. It is essential that these women are screened for the organic cause of the menstrual dysfunction: energy deficit, polycystic ovarian syndrome, or even pregnancy. If the athlete is thought to have issues regarding energy intake, the sports medicine support team, including nutritionist and psychologist, should be utilized. Although the health of the female athlete is critical to the sport medicine staff, coaches and athletes are focused on performance; therefore, research supporting the link between adequate energy resources, normal menstrual function, and optimization of performance are critical.
Girls and women are competing in sport in record numbers. Regardless of the health-related benefits of sport participation, performance success is the primary focus of athletes and coaches alike. Although sport scientists continue to debate salient theoretical and semantic political issues, clinicians must provide medical support that optimizes performance. Education on the current nutritional recommendations provided by the International Olympic Committee related to energy consumption and both macro- and micronutrient intakes are essential. Female athletes should work to maintain energy balance (dietary caloric intake to equal estimated energy use during daily training) while consuming the recommended dietary allowance for iron is essential to optimal performance. The interaction of circamensal and other biologic rhythms in female athletes remains a point of interest for sport scientists. The influence of menstrual cycle phase on sport performance remains equivocal. Clinicians may find the utility of these data unimportant in daily practice as they are unable to ethically change cycles or competition schedules to optimize trivial phase benefits. Broad discussions between medical and coaching staffs could facilitate the use of circamensal biology in the development of periodization models for competitive female athletes. The working triad of sport coach, sport medicine physician, and sport scientist is critical in maximizing the potential of competitive female athletes in the future.
References and Recommended Reading
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
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Excellent review relationship between oral contraceptive use and sport performance. Discussion of topics ranging from heat tolerance to endurance performance.