Do sex hormones influence endurance running performance in elite female long-distance track and field athletes? The answer to this question requires an in-depth review of the physiological requirements for elite track and field athletes who participate in long-distance racing. It also requires an analysis of how sex hormones influence these key requirements for performance.
In the sport of track and field, distance running events require the athlete to race at a submaximal velocity, with the goal of finishing the race in the least amount of time possible (Kukolj, et al., 1999; Thiel, et al., 2012). Elite long-distance track and field athletes strive to succeed to the highest level in their races, which requires them to meet the minimal established standards for the quantifiable key performance indicators (KPIs) for their sport.
Maximal oxygen uptake (VO2max) is a commonly cited KPI for success, but there is evidence to show that VO2maxalone does not adequately predict performance in long-distance track and field (Bassett & Howley, 2000; Joyner, 1991; Thompson, 2017). Other KPIs which may predict performance outcomes are lactate threshold, running economy, and speed ability (Auersperger, Ulaga, & Škof, 2009; Joyner, 1991; Thompson, 2017). These KPIs for long-distance running performance may be improved by high testosterone levels in elite females.
Biological sex is usually assigned as either male or female at birth by a medical doctor, based on these medical criteria: sex hormones, genitals, and chromosomes (Gender and Gender Identity, 2019). Attributable biological differences between the sexes are differentiated because of inherent sex hormones in males and females. Sex hormones are defined as steroid hormones, such as estrogen or testosterone, which regulate the growth or function of reproductive organs or the development of secondary sex characteristics (Sex Hormone, n.d.).
In long-distance running, where men are on average 12% faster than females, it is important to consider whether the sex difference in performance can be attributed to higher levels of testosterone inherent to males (Coast, Blevins, & Wilson, 2004; Joyner, 2017). Although testosterone is produced in both males and females, higher quantities are produced in males (Federman, 2006). As testosterone supplementation has been used for the purpose of performance enhancement in sport, it is crucial to consider the implications of the relationship between male hormones and performance in long-distance running, particularly in females (Bahrke, et al., 1996).
Hyperandrogenic females, defined as those who produce atypically high levels of testosterone, may be subject to improvements in KPIs for long-distance running (Yildiz, 2006). This literature review aims to identify the factors involved in this problem, as well as to discuss the ethical considerations for hyperandrogenic females in elite track and field competition.
Brief Introduction to Track and Field
The sport of interest here is track and field, which is comprised of events involving running, jumping, and throwing. The running events include track races, road races, and cross-country races. Track and field meets may take place in either an outdoor or indoor setting. Due to their wider popularity and their relevance as Olympic events, this review focuses on long-distance running events, which take place at outdoor track and field competitions (Nelson, 2016).
Outdoor track races take place on a 400-metre rubberized oval, with competition distances ranging from 100m to 10,000m (Jordan, 2019). Road races are completed on paved roads, usually in cities, and typically include distances from 10-kilometres to 42.2-kilometres (the marathon) (IAAF Competition Rules 2009: Road Races, 2013). Cross-country races take place on courses which cover many types of terrain, such as dirt trails and grass, and typically range from 4-kilometres to 12-kilometres in distance (Cross Country, 2019). Road races and cross-country races may require athletes to complete hills and sharp turns (Jordan, 2019).
Race distances in outdoor track and field may be classified as either sprint or long-distance, with sprints being 100m, 200m, and 400m (Hamlin, Hopkins, & Hollings, 2015), and long-distance being the 1,500m, 5,000m, 10,000m, and the marathon (Maldonado, et al., 2002; Zemper, 2005). A sub-category of distance running events in track and field are middle-distance events, which are considered to involve the 800m, 1,500m, and 5,000m races (Di Prampero, et al., 1993).
Physiologically, a sprint requires rapid acceleration and constant high velocity, whereas a long-distance race requires the athlete to race at a submaximal velocity to complete the longer distance in the least amount of time possible, while using tactics to respond to their opponents in order to win the race (Kukolj, et al., 1999; Thiel, et al., 2012). Long-distance running also requires the ability to run at high speeds in the finishing stages of the race (Hayes & Caplan, 2012).
Defining the “Elite”
This literature review will focus on elite female distance runners who compete in the 1500m, 5,000m, 10,000m, and the marathon. Elite female distance runners are typically around 29 years of age, and so the focus of the literature will be contingent on adult female athletes (Hunter, et al., 2011). Elite is defined by the dictionary as the “best of a class,” or superior to the rest of the field (Elite, 2019). In the context of sports, elite athletes could be described as ones who have performed at the highest level in their sport: at the international competition level, such as World Championships or Olympic Games (Tammen, 1996).
Identifying what makes an athlete elite often involves defining key physiological variables which may differentiate the elite athletes from the sub-elite population in the same sport. There is an ongoing debate regarding what these variables are (Myburgh, 2003). It has been proposed that a high VO2maxis a prerequisite for the classification of an endurance athlete as “elite,” and there has even been a specific cut-off value proposed for females (63 ml kg -1min -1) (Sjödin & Svedenhag, 1985). Additionally, the ratio of oxygen cost during running at a fixed submaximal workload to the oxygen cost at a maximal workload (VO2:VO2max) was found to account for approximately 50% of variability in performance over distance races from 1,500m-5,000m (Myburgh, 2003). This implies that the VO2:VO2max ratio could be used to apply numerical values to the definition of an elite endurance runner by imposing some quantitative criteria.
Furthermore, elite athletes will be regarded as those who competed on their respective national team at an international competition. Though physiological factors are a determining factor of success in track and field, the debate regarding which physiological measure is the greatest determining factor regarding an athlete’s elite-ness can create confusion. For simplicity, the classification of elite will be based solely on athletes who compete at a high-level of competition, defined as belonging to their national team or having competed internationally.
Key Performance Indicators
KPIs can be defined as a quantifiable measure used to evaluate the success of an athlete in meeting physiological objectives for performance (Valle, 2011). Elite female long-distance runners are required to compete at high velocities while withstanding fatigue and ventilatory stress for the duration of their race, which can range from anywhere between 4 minutes to 2.5 hours. There are key physiological variables which have been found to be associated with long-distance running performance (Joyner, 1991; Thompson, 2017). KPIs for endurance running have been shown to include VO2max,blood lactate threshold, and running economy (Joyner, 1991; Thompson, 2017). Maximizing these variables through appropriate training will optimize performance for elite long-distance runners.
VO2max is defined as “the highest rate at which oxygen can be taken up and utilized by the body during severe exercise” (Bassett & Howley, 2000). As a KPI, high VO2max is cited as a prerequisite for success in distance running, as high VO2max values often characterize elite long-distance runners (Bassett & Howley, 2000; Morgan & Daniels, 1994). This parameter is measured as the millilitres of oxygen taken up by working muscles per every kilogram of body weight, per minute (ml kg -1min -1). Oxygen uptake (VO2) refers to the amount of oxygen transported from the lungs and delivered to working tissues during exercise (Xu & Rhodes, 1999). During predominantly aerobic exercise, there is an increase in oxygen delivery to working muscles (Vincent, 2008).
VO2max is determined by many different variables. As maximal endurance exercise continues, the athlete will also eventually reach their maximum heart rate, maximum breathing rate, maximum stroke volume, and maximum cardiac output (Vincent, 2008). The eventual plateau of these variables indicates that VO2 has reached its steady state maximal value, or VO2max (Vincent, 2008). VO2max presents an upper limit for endurance performance: specifically, the cardiorespiratory system’s ability to transport oxygen to working muscles limits VO2max (Bassett & Howley, 2000). Average VO2max values in elite female long-distance runners was found by a study to be 67.1 ml kg -1min -1(Pate, et al., 1987).
The current world record holder for the female marathon, Paula Radcliffe, had a recorded VO2max value of about 70 ml kg -1min -1, a value which remained relatively stable over eleven years worth of measurements (Jones, 2006). Despite her VO2max values being relatively stable, Radcliffe was improving her race performance throughout these eleven years, which indicates that KPIs other than VO2max must have been improved (Jones, 2006). A paper by Joyner stated that elite male long-distance runners had average VO2max values of 76.9 ml kg -1min -1, with some of the highest values reported as being greater than 84 ml kg -1min -1(1991). It would be expected that marathon world record holders would have the highest VO2max values, but the male marathon world record holder has a reported VO2max value of about 70 ml kg -1min -1(Joyner, 1991).
Furthermore, elite athletes who have the same VO2max often perform differently (Morgan & Daniels, 1994). In highly trained long-distance runners, VO2max is unlikely to change with years of training, despite performance improvements (Tjelta, Tjelta, & Dyrstad, 2012). This is an indication that, while VO2max is a KPI for endurance running performance, it is not solely adequate to predict long-distance running performance on its own; there are other relevant physiological variables which may also affect performance.
Blood Lactate Threshold
As a KPI, lactate threshold contributes to performance in elite distance running (Joyner, 1991; Thompson, 2017). Lactate threshold is defined as the percentage of VO2max at which lactate begins to accumulate in the blood (Iwaoka, et al., 1988). Lactate is a byproduct of the glycolysis reaction, wherein glycogen is used by the working muscle to produce ATP via oxidative phosphorylation (Dill, 2018b). Produced within the mitochondria, pyruvate, a primary product of the glycolysis reaction, is converted to lactate in a reaction facilitated by lactate dehydrogenase (Dill, 2018b). Lactate is produced through anaerobic glycolysis, which does not require oxygen (Dill, 2018b). When the intensity of endurance exercise increases from moderate intensity to heavy intensity, lactate threshold has likely been surpassed (Dill, 2018a). Work rates beyond that of the lactate threshold prompts lactate to accumulate in the blood, a result of lactate production being greater than lactate removal.
The high energy demands required for high velocities in elite long-distance track and field athletes often require large numbers of fast twitch (type II) muscle fibers, additional to the slow twitch (type I) muscle fibers already recruited (Tesch, et al., 1982). This promotes lactate formation because fast twitch muscle fibers have a greater potential for lactate formation, compared to that of slow twitch muscle fibers (Tesch, et al., 1982). Fast twitch muscle fibers in elite distance runners have likely been trained so that lactate threshold occurs at higher proportions of VO2max, or at higher speeds, allowing them to perform at higher velocities without accumulating lactate (Tesch, et al., 1982).
Lactate threshold is an important physiological variable with implications for performance ability in endurance athletes. The faster an athlete can run without reaching lactate threshold, reducing the need for lactate metabolism, the more successful they will be in endurance events (Joyner, 1991). The percentage of maximal oxygen uptake (%VO2max) where lactate threshold occurs is a common way to quantify lactate threshold (Dill, 2018a; Joyner, 1991). The most elite endurance runners, male and female alike, experience lactate threshold at 85-90 %VO2max(Davies & Thompson, 1979; Dill, 2018a; Iwaoka et al., 1988; Joyner, 1991).
Some studies have indicated that the ability to run at high velocity without accumulating lactate as a fatigue substance in active muscles is more vital than a high VO2max (Abe, et al., 1999). Lactate threshold has been shown to increase over time with endurance training in elite athletes and may be a KPI for long-distance running performance (Rabadán, et al., 2011). Competitive 10,000m races are often completed at high intensities, which emphasizes the importance of long-distance runners having lactate threshold occur at a high %VO2max, so that they can compete at high intensities, but perhaps delay lactate accumulation (Tharp, et al., 1997).
Lactate threshold occurring at higher %VO2max measurements are often measured in elite long-distance runners who have faster racing times and have years of training at intensities which correspond to their lactate threshold (Tjelta, et al., 2012). Lactate threshold at high %VO2max values is predictive of endurance running performance ability, as these elite athletes are able to run at high velocities for longer periods of time without accumulating lactate and are able to forego the fatiguing effects of acidosis in the muscle (Coyle, 1999).
Running economy is a variable which has been shown to be predictive of endurance running performance. Running economy can be defined as the steady state oxygen cost for a given running speed, measured in ml kg -1min -1, where a low oxygen cost at a running speed indicates high running economy, and high oxygen cost for a given running speed indicates low running economy (Helgerud, Støren, & Hoff, 2010; Larsen, 2003). To measure this variable, athletes have their VO2 values measured while running at incrementally increased submaximal running speeds (Helgerud, et al., 2010). In theory, running economy should increase proportionally to running velocity.
Specialty in race distance has been found to affect running economy values (Berg, 2003). Runners tend to have better running economy in the velocities that they train to compete (Berg, 2003). Marathon runners seem to be more economical when running at marathon pace than middle-distance runners are at this pace, and middle-distance runners seem to be more economical at 800m and 1,500m paces than marathoners are (Berg, 2003; Helgerud, et al., 2010). There has not been any established relationship between the biological sexes and differences in running economy (Helgerud, et al., 2010; Morgan, Martin, & Krahenbuhl, 1989). Variability between individuals in this measure is likely caused by anatomical, mechanical, and neuromuscular differences (Helgerud, et al., 2010).
Ability to Run Maximally at the End of Long-Distance Races
In elite long-distance track and field, the ability to run maximally at the end of the race is an additional KPI (Auersperger, et al., 2009). The ability to develop and sustain relatively high speeds at the end of long-distance races, specifically the 1,500m and 5,000m, has been cited as equally important as high aerobic capacity for long-distance running performance (Auersperger, et al., 2009). Elite-level long-distance races are completed at high speeds, and speed ability becomes especially important in the latter stages of the race wherein the runners begin to accelerate and eventually run maximally (Bushnell & Hunter, 2007). The athlete must be able to accelerate in the last stages of their race, when they are fatigued, to the fastest speed that they physiologically can. It has been observed that elite males have greater ability, and higher likelihood, than elite females to accelerate and run at higher speeds at the end of long-distance races (Sandbakk, Solli, & Holmberg, 2018).
As will be discussed, speed ability may be increased through the improvement of determining physiological factors, such as muscle mass and musculotendinous stiffness. Increased muscle strength via increased muscle mass, especially fast twitch muscle fiber size, may be associated with increased speed ability, but sustained high running speeds may require the fatigue resistant slow twitch muscle fibers (Caminiti, et al., 2009; Korhonen, et al., 2009; Weyand & Davis, 2005).
Additional skeletal muscle may allow runners to apply greater forces on the ground, decreasing ground contact duration, enabling the athlete to reach faster velocities (Hayes & Caplan, 2012; Korhonen, et al., 2009;Weyand & Davis, 2005; Wong & de Heer, 2008). Increased musculotendinous stiffness in the lower leg increases energy return and therefore may decrease ground contact time, increase stride frequency, and consequently increase the ability to run maximally (Murphy, Lockie, & Coutts, 2003). The ability to run maximally at the end of a race, and factors which determine it, may be positively associated with testosterone, as will be further discussed.
Male and Female: Biological Sex Differences
The question of what classifies an individual as a male or a female is not a simple one to answer. The definition of femaleness in terms of biology is necessary to determine how sex hormones, which usually occur in higher levels in males, may affect female athletes. The differences between males and females have revolved around arguments concerned with social context, specifically regarding differing gender norms and gender identity, as well as the strictly biological explanations of sex differences (Kaplan & Rogers, 2010).
Males and females have fundamental structural and hormonal discrepancies which determine their diagnostic biological sex. Female is defined by the Merriam-Webster dictionary as “the sex that typically has the capacity to bear young or produce eggs” (Female, 2019). Males are defined by the same dictionary as “an individual of the sex that is typically capable of producing small, motile gametes (such as sperm) which fertilize the eggs of a female” (Male, 2019). Biological sex is typically assigned at birth by a medical doctor and is based on these medical criteria: hormones, genitals, and chromosomes (Gender and Gender Identity, 2019).
Individuals with XX sex chromosomes are usually defined as the female sex and have female reproductive organs, whereas individuals with XY sex chromosomes are usually defined as the male sex and have male reproductive organs (Gender and Gender Identity, 2019). Sex chromosome determination occurs following conception when one of the two X chromosomes contributed to the fertilized egg is inactivated; if the inactivation occurs completely, the fetus will be male, but if the inactivation does not complete, the fetus will be female (Federman, 2006). Biological sex assignment of a child at birth may affect the trajectory of an individual’s life; the individual is expected to conform to societal norms associated with their assigned sex (Kaplan & Rogers, 2010).
Occurring at puberty, the development of secondary sex characteristics magnifies the biological distinction between the two sexes. Male secondary sex characteristics are mitigated by a sudden increase in testosterone production, and effects include spermatogenesis, increased muscularity, deepening of the voice, and beard growth (Federman, 2006). Female secondary sex characteristics are caused by the increase of estrogen production at puberty, which stimulates breast development, menarche, and terminal hair growth (Federman, 2006).
- Body Composition Differences
Biological sex differences are also evident in body composition. Sex dimorphism exists at birth, but it is exaggerated markedly during puberty (Wells, 2007). Rapid growth patterns exclusive to males and females can be attributed to the dramatic hormonal fluctuations which are associated with puberty (Siervogel, et al., 2003). Following puberty, shape differences between males and females are exceedingly present. Patterns of lean mass and fat depositions differ between the sexes (Wells, 2007). After puberty, males typically develop an inverted triangle shape, with broad, muscular shoulders and narrow hips, often with little overall fat mass (Wells, 2007). Following puberty, females typically develop an hourglass shape, consisting of wider hips, with more fat deposits at the breast and thigh areas, and less muscle mass than males (Wells, 2007).
Total body fat increases in both sexes at puberty, but males experience a simultaneous increase in lean body mass (Siervogel, et al., 2003). This augmented lean body mass is associated with increased strength and metabolic rate in males (Siervogel, et al., 2003). Improved testosterone production may be attributable to the larger energy expenditure in active post-pubertal males (Siervogel, et al., 2003).Following puberty, a female’s body composition will be altered so that there will be a greater relative increase in fat mass than in lean, or muscular, mass (Wells, 2007).
After puberty, biological sex differences exist in terms of bone length; males tend to have longer bones with greater diameter following puberty, but bone mineral density is proportionally equal to that of female bones (Seeman, 2001). Male bones are considered stronger primarily due to bone length and width, rather than bone mineral density (Seeman, 2001). Height differences between males and females occur primarily due to male leg length being greater than female leg length (Seeman, 2001). Testosterone likely regulates this process in males, accelerating periosteal apposition (Nelson & Bulun, 2001; Seeman, 2001). In females, estrogen inhibits periosteal bone formation, decreasing the potential for bone length (Seeman, 2001). Differences between the biological sexes are increased after puberty and are critical to the biological differentiation of males and females.
- Sex Hormone Differences
There are hormones which exist in higher quantities exclusively in males or females (Friedl, 2005; Pietrangelo, 2018). Attributable biological differences between the sexes are propagated because of these sex hormones. The main sex hormone produced among males, via the testes, is testosterone (Friedl, 2005). In females, estrogen is considered the major sex hormone and is predominantly produced in the ovaries (Pietrangelo, 2018).
Testosterone is produced by both males and females, in the testes and ovaries respectively, but the key difference between the sexes is determined both by the quantity of testosterone which is produced and by how much is converted to estrogen by the aromatase enzyme (Federman, 2006). The sex hormone difference can be exemplified by a large discrepancy between testosterone and estrogen production in males and females (Federman, 2006). Males produce at least twenty times the quantity of androgens than females do, which shows that androgens, specifically testosterone, are typically male hormones (Federman, 2006).
Although testosterone may be classified as the “male” hormone, and estrogen as the “female” counterpart, both sexes produce and utilize each hormone. For example, estrogen is instrumental for both males and females as a necessary component for bone growth, bone density, and epiphyseal plate closure at the conclusion of the pubertal growth spurt (Federman, 2006). Additionally, progesterone is a female sex hormone, also produced in the ovaries (Pietrangelo, 2018). The normal levels and actions of each sex hormone differ between males and females, and the distinction is important when considering the effects of male hormones on female physiology and performance effects in long-distance running.
Endogenous testosterone is defined as testosterone which is produced within the organism and is highly associated with attributable biological differences related to the male sex (Bahrke, Yesalis, & Wright, 1996; Endogenous, n.d.). At puberty, endogenous testosterone levels rise markedly in males (Federman, 2006). Normal serum levels of testosterone in males have been found to be 8.7-33.0 nanomoles per litre (nmol/L) (Ramasamy, et al., 2015; Testosterone, Total, Bioavailable, and Free, Serum, n.d.). In females, normal serum levels of testosterone were found to be significantly less, at 0.3-2.0 nmol/L (Testosterone, Total, Bioavailable, and Free, Serum, n.d.).
Testosterone is derived from cholesterol, classifying it as a steroid hormone, and can cause a response in virtually any cell in the human body (Wood & Stanton, 2012). The production of testosterone from cholesterol in males occurs in the Leydig cells of the testes, a reaction catalyzed by enzymes (Friedl, 2005). The testes produce about 7,000 micrograms (µg) of testosterone per day, and about a quarter of a percent of this is converted to estrogen (Federman, 2006). In females, testosterone is produced in the ovaries and acts as a precursor to estrogen synthesis (Wood & Stanton, 2012). Female ovaries produce 300 µg of testosterone per day, and half is converted to estrogen (Federman, 2006).
The production of testosterone from the testes is regulated by multiple hormones, such as insulin-like growth factor (IGF-1) and luteinizing hormone, in conjunction with circulating testosterone in a negative feedback loop (Friedl, 2005). When low testosterone is detected in the blood, the hypothalamus secretes gonadotropin-releasing hormone, which, in turn, signals the pituitary gland to secrete luteinizing hormone (Friedl, 2005). Luteinizing hormone is the key regulator in testosterone production in male testes (Friedl, 2005). Testosterone effects are seen in most tissues, acting through specific androgen receptors which are present in virtually every human cell (Friedl, 2005).
Testosterone has androgenic effects, including the development of male characteristics, as well as anabolic effects (Celotti & Negri-Cesi, 1992). Androgenic effects associated with increased testosterone include lowered voice, and pubic and axillary hair development (Zitzmann & Nieschlag, 2001). Testosterone is an anabolic hormone; it increases total body mass, building muscle mass and muscle strength while also reducing body fat, effectively increasing the lean mass proportion of body composition (Friedl, 2005; Wood & Stanton, 2012).
Anabolic steroid supplementation is often used to synthesize these effects, with users aiming to build large amounts of muscle mass quickly (Bahrke, et al., 1996). Uses of these synthetic testosterones are usually associated with sports that require large stature and have power and speed components, such as sprinting and football (Cronin & Hansen, 2005). Benefitting sports performance, testosterone activates IGF-I and erythropoietin which increases muscle and bone mass and increases red blood cell formation, respectively (Friedl, 2005). Mostly occurring in supplementation trials, testosterone has also been associated with aggression and hostility (Friedl, 2005). Testosterone may also modulate performance-enhancing effects in long-distance running, an effect which will be discussed in sections to follow.
Estrogen, a steroid hormone, is considered the major female sex hormone and is responsible for many endocrine actions which result in typified female physiology (Pietrangelo, 2018). However, estrogen is also produced in males and has important non-sex specific functions in both males and females (Pietrangelo, 2018). Premenopausal adult females have previously measured serum estrogen levels which range from 0.052-0.9 nmol/L (Serum Estradiol, 2019). Levels of estrogen are variable and dependent on phases in the menstrual cycle (Pietrangelo, 2018). Postmenopausal females and adult males have similar serum estrogen levels at less than 0.035 nmol/L and 0.035-0.139 nmol/L respectively (Serum Estradiol, 2019).
In premenopausal adult females, estrogen is synthesized from androgens through the action of the aromatase enzyme, which is localized in the highest concentrations in the ovarian granulosa cells (Erhmann, et al., 1992; Nelson & Bulun, 2001). Estrogen production through aromatase action occurs in many locations within the body and is not limited to female reproductive organs. Smaller amounts of estrogen are produced in premenopausal females in the adrenal glands and lipocytes (Pietrangelo, 2018).
Males and postmenopausal females also produce estrogen, wherein aromatase action occurs mainly in the adipose tissue and in the skin. (Nelson & Bulun, 2001). In males, estrogen production has been found in the testes, but this only accounts for a relatively small proportion of their total circulating concentration (Nelson & Bulun, 2001). Aromatase has been found in many different locations, including neurons and astrocytes in the brain, and in osteoblasts, chondrocytes, and adipose fibroblasts in the bones (Nelson & Bulun, 2001). Regarding the systemic action of estrogen, the concentration of estrogen produced in peripheral, or non-ovarian, tissues relies on circulating androgens (Nelson & Bulun, 2001).
Estrogen exerts its endocrine actions most notably in premenopausal females, due to the high concentration of the steroid hormone produced, resulting in typically female characteristics. Secondary sex characteristics, which occur at puberty and are estrogen-derived, in females include breast development, and pubic and axillary hair growth (Federman, 2006). Estrogen levels also help to regulate the menstrual cycle, as well as the regulation of gonadotropin secretion for the purpose of ovulation and preparation of tissues to respond to progesterone (Pietrangelo, 2018; Nelson & Bulun, 2001).
Additional to the well-known major functions of estrogen, it also has diverse applications beyond the puberty and the female reproductive system. In females, estrogen sustains important bodily functions such as the maintenance of bone mass, lipoprotein synthesis, cognitive function, and regulation of responsiveness to insulin (Nelson & Bulun, 2001).
As discussed previously, females are likely to have greater fat mass than males. This increased fat storage may be useful for maintaining adequate energy storage for a regular menstrual cycle to occur (Márquez & Molinero, 2013). Estrogen has been shown to play a causal role in the stimulation of fat cell formation, increasing total adipose tissue and body weight (Nelson & Bulun, 2001). Aging has also been found to be exaggerated by the presence of estrogen, accelerating the aging process especially in obese females who produce estrogen both via the ovaries and additively their large adipose tissue mass (Nelson & Bulun, 2001).
As mentioned previously, estrogen is instrumental in the maintenance of bone mass and growth plate closure. Specifically, estrogen exerts its effects through the inhibition of bone remodeling, the suppression of bone resorption, and through stimulating bone formation (Syed & Khosla, 2005). This affects both males and females. Adults with either a lack of estrogen receptors or deficiency in the aromatase enzyme are likely to experience osteopenia and unfused epiphyses and may be more likely to experience bone fractures (Syed & Khosla, 2005).
Estrogen exerts cardioprotective effects; the hormone acts as a vasodilator and has been associated with increasing high-density lipoprotein concentrations, effectively reducing the chance for atherosclerosis and cardiovascular disease (Mendelsohn, 2002). Beyond estrogen’s association with maintaining female reproductive function and development of secondary sex characteristics, the hormone’s previously discussed systemic effects are unlikely to impose any performance advantages in long-distance running (Tokish, Kocher, & Hawkins, 2004).
Another female sex steroid hormone, progesterone, is produced primarily after ovulation and has functions regarding the maintenance of reproductive health. This includes preparing the uterine lining for a fertilized egg following ovulation and supporting pregnancy and lactation (Pietrangelo, 2018). Progesterone is produced primarily in the placenta and the ovarian corpus luteum (Young & Lessey, 2010). In menstrual cycles where conception does not occur, progesterone prepares the endometrium for menstruation (Young & Lessey, 2010).
Progesterone and estrogen mediate the secretion and action of the other, creating a cyclical pattern which maintains the health of the endometrium (Young & Lessey, 2010). This balance between the main female sex hormones is instrumental in maintaining health, as disruption of the cycle causes many problems such as endometriosis, abnormal bleeding, cancer, and miscarriage (Young & Lessey, 2010).
A study by Brinton, et al. highlighted the multiple effects of progesterone which are not related to reproduction. These functions occur in the central nervous system and regulate cognition, mood, mitochondrial function, inflammation, neurogenesis and regeneration, myelination, and recovery from traumatic brain injury (Brinton, et al., 2008). Although progesterone does have some functions beyond reproductive health, it may not significantly affect performance indicators in long-distance running (de Jonge, 2003).
Sex Differences in Long-Distance Running Performance
In most sports, males are often regarded as physically superior: stronger, faster, and more powerful than females (Thibault, et al., 2010). Long-distance track and field running is no exception to this (Thibault, et al., 2010). When comparing running speeds recorded during the world record 5,000m and marathon performances, it was observed that elite male runners are 12% faster than their female counterparts (Coast, et al., 2004; Joyner, 2017).
In the past, the female disadvantage in endurance running perhaps has been highlighted by the fact that females had been competing at high levels for significantly fewer years than males. The female Olympic marathon event was not added to the Games until 1984, whereas males have been competing in the marathon since the event was invented (Cheuvront, et al., 2005). This likely widened the performance gap between males and females, since males have had adequate time to reach their potential for training and racing (Cheuvront, et al., 2005). After females began high-level competition in distance running, females showed improvement at a more rapid rate than males for three decades, but the discrepancy between males and females, even in world record performances, still exists (Hunter, et al., 2011). It seems that recently females’ performance values in long-distance track events have reached a plateau after steadily increasing for many years (Cheuvront, et al., 2005).
The remaining sex difference in elite long-distance runners is likely related solely to the biological differences between males and females (Hunter, et al., 2011). Sex differences exist in many factors which may increase the discrepancy in performance between the sexes, such as body weight, body composition, and thermoregulation (Cheuvront, et al., 2005).
For the purpose of this literature review, it is useful to highlight the factors which have been classified as both highly associated with long-distance running performance and differing between males and females. In terms of physiological factors, it is likely that males outperform females in KPIs for long-distance running, and in factors which directly contribute to KPIs.
Differing VO2max values may be the best explanation for endurance running performance differences based on sex (Cheuvront, et al., 2005). The largest ever recorded VO2max values in males and females, both found in cross-country skiers, were 94 ml kg -1min -1 and 77 ml kg -1min-1, respectively (Astrand & Rodahl, 1986).
Cheuvront, et al. (2005) cited that the VO2max sex difference in elite long-distance runners in races ranging from 1,500m to the marathon as roughly 10%. Elite male distance runners were found to have higher VO2max values compared to values recorded in elite female distance runners in an analysis of Spanish national team runners who competed in events ranging from the 800m to the marathon, as shown in Table 1 (Legaz-Arrese, et al., 2007).
|Event||Male VO2max (ml kg -1 min -1)||Female VO2max (ml kg -1 min -1)|
|800m||68.5 ± 5.0||63.4 ± 6.6|
|1,500m||73.9 ± 5.7||61.7 ± 5.8|
|5,000m||78.9 ± 8.5||69.8 ± 11.5|
|10,000m||77.1 ± 5.6||71.1 ± 8.3|
|Marathon||80.1 ± 4.0||73.7 ± 6.7|
A study by Billat, et al. (2003) found that elite male 10,000m runners from Kenya had higherVO2max values than their female counterparts. Increased fat mass in females may be a contributing factor to their lower VO2max when compared to males, who are typically leaner (Helgerud, et al., 2010). This is caused by fat mass interfering with the physiological ability of muscle to consume oxygen via infiltration of fat within skeletal muscle fibers, compromising the contractile proteins within the muscle (Vargas, et al., 2018).
High VO2max values seen in elite male long-distance runners may be partially attributable to the high hemoglobin and hematocrit typically observed within this population (Coast, et al., 2004). Hemoglobin levels have been found to be higher in males compared to females by 12% (Handelsman, et al., 2018). A study found that elite male long-distance runners had hemoglobin values of 14.9 ± 0.4 grams per decilitre (g dL -1), and their female counterparts had hemoglobin values of 13.4 ± 0.4 g dL -1 (Foster, et al., 2014).
High hemoglobin content in the blood and high concentration of red blood cells positively affect oxygen uptake into working muscles by increasing the oxygen-carrying capacity in the blood (Handelsman, et al., 2018). In general, VO2max values increased linearly with an increase in race distance, reflecting the relative contribution of the aerobic energy system (Joyner, 2017). The male-associated higher oxygen-carrying capacity becomes increasingly beneficial for longer endurance running events because the aerobic metabolic demands can be met with less cardiovascular effort.
Sex differences in VO2max may also be attributable to the greater cardiac output observed in males (Cheuvront, et al., 2005; Pelliccia, 1996). Cardiac output is the product of heart rate and stroke volume (Sandbakk, et al., 2018). There are no observed sex differences in heart rate; cardiac output differences are likely explained by the greater stroke volume in males (Sandbakk, et al., 2018). The larger male heart can push out a higher volume of blood per heartbeat, resulting in higher cardiac output, compared to the cardiac output of the female heart (Ramsbottom, Nute, & Williams, 1987).
Also positively contributing to stroke volume, elite endurance-trained males have larger blood volume than their female counterparts (Sandbakk, et al., 2018). Because of this advantage, elite males may be able to perform long races at high velocities without reaching oxygen debt and muscular fatigue, because their cardiac output, and therefore VO2max, is adequate to saturate the muscle with oxygen for the purpose of oxidative phosphorylation and subsequent ATP production (Dill, 2018a).
To match oxygen supply to oxygen demand during exercise, oxygenated blood must efficiently perfuse the working muscle (Pittman, 2011). To increase oxygen uptake into the muscle, high capillary density is required (Pittman, 2011). Therefore, capillary density is a factor which contributes to VO2max. Capillary density has been found to be lower in endurance-trained females than in endurance-trained males (Robbins, et al., 2009). By contrast, a study found that male and female athletes of equally high endurance training status had practically identical capillary density values (Ingjer & Brodal, 1978).High capillary density in elite long-distance runners is likely a product of training, rather than sex. Click To Tweet
Similarly, a study on aerobically active males and females found no significant sex difference in capillary density (Gries, et al., 1985). It seems that, when compared to sex, endurance training status has a greater influence on capillary density (Ingjer & Brodal, 1978). Endurance training has been shown to significantly improve capillary density in skeletal muscle, suggesting that high capillarization in elite long-distance runners is likely a product of training, rather than sex (Costill, et al., 1987).
Sex differences in running economy are less commonly recognized in the literature. A study by Daniels and Daniels (1992) tested elite male and female distance runners for this parameter and concluded that males had better running economy; they consumed less oxygen than females at common absolute velocities. Another study also highlighted that males often have greater economy than females, but these results should be adjusted to be relative to body mass, which would equate the values between sexes (Bourdin, et al., 1993).
Contrarily, research by Cunningham (1990) found that male and female cross-country athletes have a similar running economy and extrapolated that primary performance differences are associated with the VO2max discrepancy. Morgan, et al. (1989) also noted that a running economy sex dichotomy does not exist. In general, it is noted that elite female shave higher oxygen uptake measurements for a given standard submaximal speed, putting them at a disadvantage to males for performance in distance running, but when these values are adjusted for body mass, running economy is equalized (Bourdin, et al., 1993; Helgerud, Ingjer, & Strømme, 1990). Based on a review of the available literature, sex differences in running economy are not consistently studied nor recognized and may require additional standardized testing with large sample sizes (Helgerud, et al., 2010).
Lactate threshold is highly associated with endurance running performance, but there is no established evidence for sex differences in this parameter (Cheuvront, et al., 2005; Iwaoka, et al., 1988; Joyner, 2017). Lactate threshold in female runners has not been studied extensively, but available research does indicate that elite female runners can run marathons at about 75-85% of their VO2max, which is essentially equal to lactate threshold in elite male marathoners (Davies & Thompson, 1979; Iwaoka, et al., 1988).Males and females can train to maximize the training adaptations equally, which would improve lactate threshold. Click To Tweet
Improvement of lactate threshold involves adaptations which increase the number of mitochondria in the skeletal muscle, effectively increasing the rate of glycolysis and pyruvate oxidation (Joyner, 2017). Time spent training at intensities higher than lactate threshold is likely the major determinant of lactate threshold (Joyner, 2017). Sex differences are unlikely to be a significant factor, as there are no significant findings to show that males and females do not have the same capability to generate mitochondrial adaptations in response to training (Joyner, 2017). Males and females are equally able to train to maximize the training adaptations which would improve lactate threshold.
Ability to Run at High Speed at the End of a Long-Distance Race
The ability to run at high speeds in the latter stages of a long-distance race was previously defined as a KPI. Additional to the VO2max differences between males and females in long-distance running, factors which affect the ability to run at high speed may differ based on sex. Speed ability at the end of the race requires muscle mass and may be attributable to the high power output of fast twitch muscle fibers (Weyand & Davis, 2005). Males are capable of higher power output and therefore have greater ability for running at high speeds than females do (Perez-Gomez, et al., 2008). Sprinting ability in males has been quantified as about 10% greater than in females (Cheuvront, et al., 2005). Sex differences in speed ability may be attributed to factors which contribute to this KPI.
Greater muscle fiber cross-sectional area (CSA) has been found to decrease ground contact time and therefore increase capacity to race at high velocities (Hayes & Caplan, 2012; Korhonen, et al., 2009;Weyand & Davis, 2005; Wong & de Heer, 2008). Sex differences exist in muscle fiber CSA, where males generally have greater CSA than females (Cheuvront, et al., 2005). Both strength and running speed are positively correlated with CSA, creating a performance advantage for males in running events which rely on high velocities at the end of the race (Cheuvront, et al., 2005). Factors which affect muscle fiber CSA and speed ability, and therefore performance, in elite long-distance running may be attributable to biological sex hormone differences.
As previously noted, musculotendinous stiffness has also been defined as a contributing physiological factor in speed ability for finishing stages of long-distance races (Murphy, et al., 2003). In general, musculotendinous stiffness is proportional to the strength and mass of the muscle, which differs between males and females (Perez-Gomez, et al., 2008). Musculotendinous stiffness sex differences have been described for muscles in the leg, including the gastrocnemius, that are highly utilized in running (Perez-Gomez, et al., 2008). A study found that males have higher musculotendinous stiffness than that of females in the hamstring muscle group (Bell, et al., 2012). High musculotendinous stiffness in males likely contributes to increased ability to run maximally at the end of elite long-distance track and field races.
Some females are born with hyperandrogenism, a condition defined by the production of testosterone in higher quantities than a typical female would normally produce (Yildiz, 2006). Females with hyperandrogenism experience deviations from typical female physiology (Yildiz, 2006). Elite female long-distance runners who produce high levels of testosterone, near the normal male range, may experience improvements in distance running performance. In general, males outperform females in distance running (Coast, et al. 2004). Previously, KPIs for which males outperform females were identified. The sex differences associated with VO2max and speed ability at the end of a race may be attributable to high levels of testosterone inherent to biological males (Billat, et al., 2003; Perez-Gomez, et al., 2008).
The subsequent section of this literature review will aim to describe the relationship between females with naturally high testosterone and improved KPI values, and the potential improvements in long-distance running performance.
Hyperandrogenism is an endocrine disorder which affects 5-10% of premenopausal adult females (Yildiz, 2006). Hyperandrogenism is an umbrella term for a group of disorders which share a common diagnostic criterion: above normal levels of androgen production, specifically testosterone, comparable to concentrations present in males (Handelsman, et al., 2018; Yildiz, 2006). The most commonly diagnosed hyperandrogenic disorder is polycystic ovarian syndrome (Erhmann, et al., 1992; Yildiz, 2006). Other hyperandrogenic diagnoses include idiopathic hirsutism, hirsutism and hyperandrogenemia, non-classical congenital adrenal hyperplasia, and hyperandrogenism, among others (Yildiz, 2006).
Individuals who are classified as Intersex, more recently termed as having Disorder(s) of Sex Development (DSD), are among those who experience hyperandrogenism (Handelsman, et al., 2018; Karkazis, et al., 2012; Ritchie, Reynard, & Lewis, 2008). Individuals with DSD are classified as having an atypical appearance of external genitalia at birth, making the assignment of biological sex a difficult task (Ritchie, et al., 2008). Females with DSD usually experience virilization, which can be defined as the development of physical characteristics usually associated with males, such as male-pattern muscle mass and deepening of the voice (Handelsman, et al., 2018; Virilization, 2019). Clinically recognized symptoms used for diagnosis of hyperandrogenism, other than directly measured blood testosterone levels, include hirsutism, acne, and virilization (Yildiz, 2006). In clinical diagnoses, these criteria are rated based on the rate of onset and severity (Yildiz, 2006).
Hirsutism is observed in 80% of females with hyperandrogenism and is defined as the growth of excessive male-pattern terminal hair in females (Yildiz, 2006). Females with this condition will often display male-pattern thick, dark hair on the face, chest, armpits, back, and pubic areas (Yildiz, 2006). Androgens affect hair follicles in these areas differently than at other areas where terminal hair does not develop. These hair follicles are highly sensitive to androgen concentration and take many years to eventually transform vellus (soft hair, such as on the scalp) into terminal hair (Yildiz, 2006). Although the presence of hirsutism does not elicit diagnosis of hyperandrogenism on its own, the presence of this condition is very likely in hyperandrogenic females (Yildiz, 2006).
Acne is a skin condition which affects many people, from adolescence into adulthood. The development of acne seems to be related to the autocrine and paracrine effects of androgens (Yildiz, 2006). Acne is not solely associated with male levels of testosterone; it exists in both sexes due to androgen levels increasing in both males and females at puberty. The adrenal glands produce more testosterone beginning at puberty in both sexes (Yildiz, 2006). Due to the link between androgens and acne, the skin condition is considered a symptom of hyperandrogenism, but acne alone is not considered indicative of hyperandrogenism (Held, et al., 1984; Yildiz, 2006). Because acne is exceedingly common, the presence of excessively severe acne in conjunction with hirsutism or irregular menstruation should be considered when searching for symptoms of hyperandrogenism (Yildiz, 2006).
An additional diagnostic criterion for hyperandrogenism includes virilization. Compared to other diagnostic criteria, virilization is much less common for females with high androgen levels (Yildiz, 2006). This condition is characterized based on several symptoms, such as male-pattern hair loss, enlarged clitoris, deepening of the voice, increased muscle mass, decreased breast size, and amenorrhea (Yildiz, 2006). These characteristics are quite physically masculinizing and can drastically change the appearance of hyperandrogenic females.
Sex Hormones and Distance Running KPIs
Supplementary to the changes in skin and hair, the masculinizing effects of hyperandrogenism in females may positively affect long-distance running performance (Celotti & Negri-Cesi, 1992). Testosterone has both androgenic and anabolic actions mediated through a single hormonal receptor type, which is present on many different cell types (Celotti & Negri-Cesi, 1992). Therefore, the masculinizing actions of testosterone are difficult to separate from the anabolic actions, and improvements in KPIs for long-distance running performance may accompany the physically male characteristics seen in hyperandrogenic females (Celotti & Negri-Cesi, 1992).
In fact, the International Association of Athletics Federations (IAAF) has imposed regulations prohibiting hyperandrogenic female track and field athletes who have testosterone levels higher than 5 nmol/L from competing in distance events at high-level competitions, under claims that levels above this would impose a performance advantage (IAAF, 2018).
In the preceding discussion, it was outlined that among defined KPIs, differences in VO2max in males and females had the most merit in explaining sex differences in long-distance running (Cheuvront, et al., 2005). There are multiple factors which determine VO2max values, such as hemoglobin concentration, hematocrit, and cardiac output (Vincent, 2008).
At puberty when testosterone concentrations rise to typical adult male levels, hemoglobin concentrations also rise (Handelsman, et al., 2018). One study found that hemoglobin concentration, a factor which limits VO2max, was positively associated with testosterone, although the relationship had some intra-individual differences (Slind, 2014). This improvement in production of hemoglobin occurs because of the positive influence of androgens on erythropoietin and red blood cell production (Genel, Simpson, & de la Chapelle, 2016; Goswami, et al., 2014; Handelsman, et al., 2018; Slind, 2014).
As previously discussed, hemoglobin is a major factor for oxygen delivery to muscles; it increases the blood’s binding affinity for oxygen (Slind, 2014), effectively increasing VO2max and athletic performance (Handelsman, et al., 2018). While this association is well known, the physiological mechanism regarding how testosterone increases hemoglobin levels in the blood is less well understood (Handelsman, et al., 2018).
Testosterone improves sensitivity and secretion of erythropoietin, the main hormone involved in red blood cell production, which consequently improves hemoglobin concentration (Handelsman, et al., 2018). Improving circulating hemoglobin levels on red blood cells facilitates oxygen transport from the lungs to working tissues, improving VO2max values and aerobic capacity (Handelsman, et al., 2018). This effect is often the goal of endurance athletes who participate in blood doping. In hyperandrogenic females, this may be a key factor which provides a performance advantage in distance running.
Cardiac output, the product of stroke volume and heart rate, has been identified as an important factor in the determination of VO2max (Goswami, et al., 2014; Slind, 2014). As a determinant of VO2max, cardiac output may be affected by testosterone. Males have larger hearts than females, consisting of larger atria and ventricles, and greater cardiac muscle mass (Ramsbottom, et al., 1987). These factors increase stroke volume by filling the heart with a larger volume of blood, the blood to be pumped more forcefully by the heart into the systemic vasculature, thereby carrying larger volumes of oxygen saturated blood to working muscles, improving oxygen uptake (Vincent, 2008).
In males and females of equally high endurance training status, males will have a larger stroke volume and cardiac output (Pelliccia, 1996). Androgen receptors have been identified in cardiac muscle cells and are associated with the promotion of cardiac protein synthesis and subsequent increases in left ventricular mass (Pelliccia, 1996; Steding, et al., 2010). High ventricular muscle mass would increase contractility, a determinant of cardiac output (Vincent, 2008).
Testosterone supplementation in hypogonadal treatment has also been associated with increases in blood volume, which would increase cardiac output (Friedl, 2005). In a study which administered testosterone treatment, cardiac output was increased, principally through testosterone’s vasodilator effect, compared to the placebo group (Pugh, Jones, & Channer, 2003). Considering these findings were achieved using acute therapy in vitro, there could be implications for the presence of a relationship between chronically high testosterone seen in hyperandrogenic females and cardiac output (Pugh, et al., 2003).
Optimal performance in the finishing stages of a long-distance race requires the ability to run at high speeds, a component which is dependent on muscle mass, a factor previously classified as differing based on sex (Bushnell & Hunter, 2007). Testosterone is widely recognized as an anabolic hormone, meaning that it is skeletal muscle mass-developing (Caminiti, et al., 2009; Greene, et al., 2006; Kadi, 2008; Slind, 2014). Testosterone facilitates hypertrophy of skeletal muscle by activating androgen receptors expressed on satellite cells and muscle fiber nuclei, enhancing muscle protein synthesis and causing a proliferation of myogenic pathways (Griggs, et al., 1985; Kadi, 2008). Testosterone may also reverse the effects of the catabolic hormone cortisol, decreasing muscle breakdown (Silver, 2001).
In a study on female hyperandrogenism, an association was found between testosterone and muscle mass development (Douchi, Yoshimitsu, & Nagata, 2001). Improvements specifically in the mass of weight-bearing, large leg muscles, which are necessary for running, have been shown after testosterone supplementation (Caminiti, et al., 2009). Barring that muscle CSA does not increase massively, it may be beneficial for hyperandrogenic females in elite distance running.
Furthermore, through research regarding muscle mass increase, it seems that testosterone therapy has been shown to increase the number and size of slow twitch muscle fibers specifically, increasing the overall oxidative capacity of the muscle and consequentially resulting in higher aerobic capacity and delayed fatigue, perhaps also increasing lactate threshold (Caminiti, et al., 2009; Volterrani, Rosano, & Iellamo, 2012). Upregulated expression of slow twitch muscle fibers has been shown to result from testosterone and androgen receptor pathways (Altuwaijri, et al., 2004).
One study found that slow twitch muscle fibers are relatively more sensitive to testosterone supplementation than fast twitch muscle fibers, which may be particularly beneficial for long-distance running performance by increasing aerobic potential (Volterrani, Rosano, & Iellamo, 2012). Testosterone may also facilitate the conversion of fast twitch muscle fibers to slow twitch muscle fibers, improving overall oxidative qualities in the muscle (Volterrani, et al., 2012). This effect will improve sustained speed ability and speed ability in the finishing stages of a race, which are necessary for competition in elite long-distance running.
Testosterone has been found to be positively associated with musculotendinous stiffness (Bell, et al., 2012). As discussed previously, musculotendinous stiffness has been associated with increases in muscle mass, a factor which is improved through testosterone supplementation (Caminiti, et al., 2009; Murphy, Lockie, & Coutts, 2003; Wood & Stanton, 2012). A study found that testosterone does enhance musculotendinous stiffness due to increased collagen production (Hansen & Kjaer, 2016). Furthermore, as a response to training, musculotendinous stiffness was found to increase much more in individuals who had higher levels of testosterone (Hansen, & Kajer, 2016). This could be associated with speed ability improvement in individuals who have high testosterone levels.
Based on a review of the literature, male-level testosterone levels in hyperandrogenic females are likely to enhance performance in endurance running on the basis of improving VO2max and its determining factors, as well as by increasing finishing speed ability and its determining factors. The male sex hormone has been shown to increase hemoglobin concentrations, cardiac output, muscle mass, musculotendinous stiffness, and potentially increase oxidative qualities in the muscle fibers.We need more research about the effects of endogenous testosterone in females; most studies assessed effects of exogenous testosterone treatments. Click To Tweet
In the existing literature, there is evidence that androgen sex hormones have positive performance effects for distance running performance. However, further research regarding the effects of endogenous testosterone in females is warranted, as the literature was predominantly comprised of studies which assessed the effect of exogenous testosterone treatments, and there may be an alternate mechanism of action.
Ethical Considerations for Hyperandrogenic Females in Elite Track and Field
Since the emergence of Caster Semenya onto the international level of track and field in 2009, she has been a dominant athlete. The female middle-distance athlete’s prowess and physical differences have raised concerns, complaints, and controversy which led to major ruling changes within the IAAF and the International Olympic Committee (IOC) (Genel, et al., 2016). Semenya, who identifies as a female, is a South African multiple-time world and Olympic medalist in the 800m and 1,500m (Genel, et al., 2016). The combination of her masculine appearance and sudden dominance in the sport prompted complaints and subsequent medical testing (Genel, et al., 2016).
In 2009, Semenya won the 800m race at the Berlin World Championships by about two and a half seconds; virtually unknown at the time, she was immediately subjected to intense speculation and criticism from her competitors and onlookers (Karkazis, et al., 2012). The complaints were centred around her appearance; she was called “butch,” “not a woman,” and “a man,” with competitors claiming that it was unfair for Semenya to be competing with them (Karkazis, et al., 2012; Sudai, 2017). Her case received massive amounts of attention from the media (Karkazis, et al., 2012). After winning the 2009 World Championship, Semenya underwent “sex testing,” wherein she was under the impression that she was undergoing standard doping tests (Karkazis, et al., 2012). These tests showed that Semenya had a DSD, and therefore hyperandrogenism (Karkazis, et al., 2012).
Specifically, Semenya’s condition left her with undescended testes which produced three times the amount of testosterone as compared to typical females(Karkazis, et al., 2012). They also found that she had no uterus or ovaries (Karkazis, et al., 2012). Her testosterone levels were classified as within the normal range for males (Karkazis, et al., 2012). After the media released the intensely personal details about her body, Semenya’s case was a topic of public debate, and she understandably disappeared from the world of sport (Karkazis, et al., 2012).
In 2011, in efforts to prevent the recurrence of a similar situation, the IAAF imposed new regulations regarding testosterone levels for female athletes (Sudai, 2017). The policy stated that females must be under the imposed limit of 10 nmol/L of testosterone to be eligible to compete as a female and that the affected seek medical treatments, either hormone therapy or surgery, to lower their testosterone levels (IAAF, 2011). The policy aimed to preserve the sex separation in athletics, keeping males and females in discrete categories for competition (Sudai, 2017).
The recommendation for hyperandrogenic females to lower their testosterone levels in order to compete in professional competition, or otherwise be barred from competing until they do so, is controversial. The Court of Arbitration for Sport even suspended the policy for a two-year period after an athlete protested and refused to comply with the ruling (Sudai, 2017).
The sprinter, Dutee Chand, stated that she felt the ruling was unfair on the grounds that she was not doping, her body was natural, and she had no intention of cheating (Sudai, 2017). She went on to state her concerns regarding whether the recommended therapy intervention would decrease her performance level, or even her health (Sudai, 2017). It was then recommended that the IAAF revise their policy, because of claims that it was not based on established scientific evidence (Sudai, 2017).
In 2015, the policy was revised and reinstated; it no longer recommended surgery, and included rulings so that male to female transgender athletes and hyperandrogenic females may compete as females if they showed that their serum testosterone levels were below 10 nmol/L for at least 12 months prior to competing (Sudai, 2017).
IAAF hyperandrogenism regulations are currently pending modification. In November of 2018, the IAAF imposed regulations for female athletes with a DSD pertaining to the 400m, 400m hurdles, 800m, 1,500m, and the mile (IAAF, 2018). These regulations require female athletes who have serum testosterone levels above 5 nmol/L, or are “androgen sensitive” and wish to compete in these events, to meet certain criteria in order to be eligible (IAAF, 2018).
These criteria include that she must be recognized by law as female or as having a DSD, she must reduce her serum testosterone levels, through hormone therapy, to below 5 nmol/L for at least 6 months, and she must maintain this testosterone level continuously for as long as she wishes to continue to be eligible (IAAF, 2018). Additionally, the IAAF stated that they had conducted research and found that there is a performance advantage for hyperandrogenic female athletes in the events for which the restriction is imposed (IAAF, 2018). As implied by the ruling, female athletes who do not wish to comply with the ruling may compete in events outside of the specifically restricted ones.
The most recent regulations are interesting in that they seem to be pointed towards Semenya. Semenya specializes in middle-distance events—the 800 and 1,500—and has raced at a high level in the 400m. These are the same events which she is restricted from competing in if she does not lower her testosterone levels. The unreleased research conducted by the IAAF apparently found adequate evidence for an association between high endogenous testosterone in females and a competitive advantage in these middle-distance events.
These findings are in conjunction with the findings of this literature review, wherein the performance requirements for distance running, high VO2max and the ability to run maximally at the end of a race, were found to both be subject to sex differences and to be positively affected by testosterone. The IAAF may have been biased by the Semenya case; in their efforts to reduce the chance of another comparable incident, they conducted studies which found testosterone to be beneficial only in her main events.
Semenya protested this ruling, saying it was “discriminatory, irrational, [and] unjustifiable” (Zaccardi, 2018). Since her protest, the IAAF delayed implementing the rule, and an appeal hearing date was set for the end of February 2019, with a final decision regarding the regulation to be expected for the end of April 2019 (Decision in Caster Semenya case delayed until end of April, 2019).
Considering the continuously unresolved issues regarding the IAAF regulations, the question pertaining to fairness remains. If the IAAF decides hyperandrogenic females are allowed to compete with females without lowering their testosterone, this would be deemed unfair for other female competitors, as they may be at a performance disadvantage. In juxtaposition, if hyperandrogenic females are restricted to either using hormone treatment to reduce their testosterone levels, or to not compete at all, this is unfair to them.The link between endogenous testosterone and performance enhancement in females is not scientifically proven. Click To Tweet
While the use of exogenous testosterone for doping may be commonly used by female athletes, hyperandrogenic females made no decision to have high testosterone. While their hormone profile may not be deemed “normal” for females, they are natural, and the recommendation by the IAAF to use hormone therapy to reduce testosterone levels may have negative health implications and is inherently unfair (Karkazis, et al., 2012). Furthermore, according to Karkazis, et al. (2012), the link between endogenous testosterone and performance enhancement in females is not scientifically proven.Why are hyperandrogenic females discriminated against for a factor which may not have performance-enhancing effects? Click To Tweet
Why are hyperandrogenic females discriminated against for something they cannot control? And why are they discriminated against for a factor which may not have performance-enhancing effects? The IAAF regulation promotes speculation and criticism of females who do not conform to traditional physical standards of femininity, such as Semenya (Schultz, 2012).The IAAF regulation promotes speculation and criticism of females who do not conform to traditional physical standards of femininity. Click To Tweet
The regulations are inherently sexist and may dissuade females who may not fit the typical female stereotype from participating in sport (Schultz, 2012). The implications of the regulations include that females are not supposed to be good at sport; when a woman excels in competition compared to the rest of the field, she will likely be tirelessly scrutinized and have her sex questioned. The fairness of the IAAF regulations remains to have biological and cultural considerations.
This literature review determined that, of the identified KPIs for long-distance running performance in elite females, onlyVO2max and finishing speed ability were found to be divergent based on sex, and positively associated with testosterone levels. The available research was predominantly concerned with testosterone supplementation, which is not the same mechanism by which hyperandrogenic females have high testosterone, and thus the research findings should be taken with caution when considering the specificity to the literature review topic.The only KPIs for long-distance running that differed based on sex & testosterone levels—mostly supplemented—were VO2 max and finishing speed ability. Click To Tweet
Equal opportunity for females in elite sport should be prioritized. Hyperandrogenic females should be treated humanely and should not have to necessitate medical treatment to permit their performance in high-level athletics (Karkazis, et al., 2012). Biological advantages for performance may exist within many individuals, such as leg length, naturally high VO2max, or a genetic predisposition for fast twitch muscles, but these aspects of the human body are not policed in the same way that high testosterone in females is.Effects of high testosterone in a hyperandrogenic female may not equal the performance effects seen in females who deliberately use androgens to dope. Click To Tweet
The mechanism by which testosterone affects performance may differ based on whether it is endogenous or exogenous, and therefore it may not be correct to assume that the effects of high testosterone in a hyperandrogenic female will equate to the performance effects seen in a female who deliberately uses androgens to dope. Perhaps, hyperandrogenic females should be allowed to compete in the societal gender in which they were raised.
Hyperandrogenism has inter-individual variability and possible performance-enhancing effects in long-distance running (Karkazis, et al., 2012). As such, each case should be treated individually, and with the utmost respect and discretion for the athlete involved. More investigation is required to determine whether endogenous testosterone in elite female athletes imposes a performance advantage in elite long-distance running.
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