The Future of Sex in Elite Sport

Sports science outlook ILLUSTRATION BY JONAS BERGSTRAND JONAS BY ILLUSTRATION n the excitement of leaving for the sex, based on chromosomes. People usually 1985 World University Games in Kobe, have 46 chromosomes arranged in 23 pairs. Japan, Spanish hurdler María José One of these pairs differs depending on the THE Martínez-Patiño forgot to pack her biological sex of the individual: women typi- doctor-issued ‘certificate of femininity’. cally have two X chromosomes, whereas men “You had to prove you were a woman in typically have an X and a Y. Genetic errors, FUTURE Iorder to compete,” she explains. Without it, mutations and interactions between DNA and she had to take a simple biological test. But hormones can, however, cause a panoply of it produced an unexpected result, and so exceptions to this arrangement. Although a she had to take a more thorough test — one person’s chromosomes might indicate one OF SEX that would take months to process. The team sex, their anatomy might suggest otherwise. physician advised her to fake an ankle injury This is known as intersex or differences of sex to silence suspicion around why she was not development (DSDs). IN ELITE running, so she sat in the stands with her foot The chromosome-based test required by bandaged and watched, wondering what the the IOC involved taking cells from inside the test result meant. cheek. In a cell containing two X chromo- SPORT Sport has a long history of policing who somes, one chromosome is inactive and there- counts as a woman. Blanket mandatory ‘sex fore shows up under the microscope as a dark Sex has long been used verification’ testing was put in place at events spot in the nucleus, known as a Barr body. If to divide many sporting in the 1960s (see ‘Policing sex’) — a time when the dark spot was not clearly identifiable, the women’s participation in sport was on the rise result could then be checked by cataloguing competitions in the name of and many were making huge performance the chromosomes present in a cell. fairness, but are the current improvements. Concerns that men might Martínez-Patiño’s chromosome testing be masquerading as women forced people revealed she was 46,XY — chromosomally rules and enforcement competing in women’s events to undergo a male. Further examinations showed that practices fit for purpose? demeaning visual and physical examination although her outward features were typ- by a panel of doctors. ically female she had internal testes. Her In 1968, the International Olympic Commit- cells, however, were unable to process the By Julianna Photopoulos tee (IOC) adopted a different test to determine hormone testosterone in her body that would

otherwise produce typical male anatomy — a successfully challenge a disqualification from condition known as complete androgen insen- athletics on the grounds of sex. As a result, sitivity syndrome. “I was stunned,” she says. World Athletics ended blanket genetic sex Following the results, Martínez-Patiño was testing in 1992, although it still investigates asked by her national federation to withdraw female athletes when competitors, coaches or from sport quietly. But she made a differ- the media raise questions. The IOC continued ent call, choosing instead to compete in the to routinely test for the SRY gene found on the Y Spanish Athletics Championships in 1986. chromosome until 2000. These tests have only She paid the price afterwards, however, when ever been directed at women with non-typical her medical record was leaked to the media. sex characteristics or intersex traits, never at “I lost everything,” she says. She was barred men, says Katrina Karkazis, a bioethicist at Yale from competition and had her university University in New Haven, Connecticut. fellowship, medals and records revoked. She lost her friends, fiancé, privacy and sense Changing regulations of self. “I felt guilty, like I was to blame for a DSDs are rare, but they have been found to genetic or medical matter,” she says. be more common in female athletes than in But even then, she was not ready to give up. women generally. A study1 involving athletes “You see yourself in the mirror every day. You who took part in the 2011 IAAF World Cham- grew up and developed as a woman — that does pionships in Daegu, South Korea, found that not change,” she says. “I was going to show I about 7 in 1,000 female competitors were

EFE/PA IMAGES EFE/PA didn’t cheat anyone.” With the support of sev- 46,XY — a prevalence that is around 140 times eral scientists, Martínez-Patiño proved to the higher than in the general population. Hurdler María José Martίnez-Patiño in 1989. medical commission at what was then called Individuals with this genetic make-up can the International Amateur Athletic Federation produce high levels of testosterone. Known as Athletics meant that, to compete in women’s (IAAF) that she did not have any unfair advan- hyperandrogenism, this can also result from events, individuals had to lower their blood tage over other female athletes. In 1988, her other conditions in women, such as polycystic testosterone levels to below 10 nanomoles licence to compete was restored, but it was ovary syndrome and congenital adrenal hyper- per litre by either hormone treatment or sur- too late for her Olympic dream. After failing plasia. Testosterone makes muscles bigger, gery. Martínez-Patiño, who was part of the IOC to qualify for the 1992 Olympics in Barcelona strengthens bones and increases levels of Medical Commission that adopted similar by one-tenth of a second, she retired to focus oxygen-carrying haemoglobin in the blood. rules in 2012, says that although it was not a on sports science. Its synthetic form is used in doping. perfect solution it was an improvement on past Even before chromosome analysis was attempts to ensure fairness in women’s sport. introduced to determine sex in sport, However, the policy did not remain in force geneticists warned that it was unreliable, for long. In 2014, on the eve of the Common- discriminatory and ill-suited for detecting wealth Games in Glasgow, UK, Indian sprinter people who might have an ‘unfair’ advan- Dutee Chand discovered that her blood tage in the women’s category. Reliance on I FELT GUILTY, LIKE I WAS testosterone level was above the 10-nanomole the presence of multiple X chromosomes to threshold. Rather than take the option of hor- signify being female would not, for example, TO BLAME FOR A GENETIC mone therapy or surgery, as other athletes are identify the roughly 0.2% of men born with thought to have done around this time2, she 47,XXY genetics. Similarly, it would not iden- OR MEDICAL MATTER.” instead chose to fight the ruling at the Court tify women with hormonal conditions that can of Arbitration for Sport. In July 2015, the court cause them to have increased muscle, such as found in her favour and gave World Athletics congenital adrenal hyperplasia. The typical testosterone level in women two years to present clearer scientific evidence Over the decades, sports governing bod- ranges from 0.12 to 1.79 nanomoles per litre, that natural testosterone provides an athletic ies’ regulations have evolved in an effort to whereas in adult men it ranges from 7.7 to advantage. The hyperandrogenism rules were ensure that for a person to participate as a 29.4 nanomoles per litre. This difference suspended, allowing Chand and women with women, they must be a “biological female”, manifests after puberty, when men typically DSDs to compete without restriction. says Stéphane Bermon, a sports physician produce considerably more testosterone than and the director of health and science at World do women. “Testosterone is the main driver Controversial evidence Athletics (formerly the IAAF) in Monaco. “The explaining the difference between male and Attempts to use testosterone as a marker female classification in sports is a protected female performances,” says Bermon. In 2011, of whether an individual can compete in a category,” he says. World Athletics’ current World Athletics became the first international women’s event or has an unfair sporting advan- definition of a biological female is largely based sports federation to adopt regulations govern- tage have been the subject of much criticism. on levels of testosterone. But some researchers ing the competition eligibility of women with One objection is that the typical testoster- doubt the validity of using testosterone to seg- hyperandrogenism, stressing that it was not a one ranges for men and women might not be regate athletes. More broadly, the process of form of sex testing. The move was triggered by as distinct as they first appear. A 2014 study3 sorting athletes by their sex has raised difficult controversy around the sex of South African of 693 elite female and male athletes across questions around medical ethics and human middle-distance runner Caster Semenya in 15 sports found significant overlap in testos- rights that are a long way from being answered. 2009, which forced her to withdraw from sport terone levels between the two groups. Around Martínez-Patiño was the first woman to for 11 months. The rules adopted by World 14% of women had levels higher than what is

Sports science outlook considered the typical female range — some even had levels considered high for a man. And around 17% of men had testosterone levels below the typical male range. Another major concern is a lack of direct evidence linking high levels of testosterone in women to a competitive edge. Among elite athletes, competitors in men’s categories seem to run or swim 10–12% faster than those competing in women’s categories, and they jump 20% farther or higher. But it is not clear how much testosterone contributes to these differences. This uncertainty was central to the court’s decision to uphold Chand’s appeal. In the case of women with DSDs, some anec- dotal evidence supports the idea that elevated testosterone levels provide a benefit. Bermon notes that three distance runners who under- went hormone therapy saw their performance

drop by nearly 6% over the course of two years, VIA GETTY SARKAR/AFP DIBYANGSHU which he thinks suggests that testosterone has Sprinter Dutee Chand (right) fought a ruling that would have prevented her from competing. a significant role4. And David Handelsman, an endocrinologist at ANZAC Research Insti- for the study to be retracted7. “As many as Africa. “An athlete would be legal on a Satur- tute in Sydney, Australia, says that research5 one-third of the data were bad,” Pielke says. day and illegal on a Sunday just because she is involving transgender athletes shows that For example, some performance times were running in a different event.” some people can continue to benefit from past duplicated, other times did not exist in the Karkazis also points out that the 2017 study6 testosterone levels — such as increased height official competition results, and athletes dis- showed a significant performance difference and muscle mass — after hormone therapy. qualified for doping were included in the study correlated with testosterone in 5 of the 21 In the wake of the Chand decision, Bermon data set. Bermon says he and his colleagues events assessed, including hammer throw and his colleague undertook a study to quan- published a letter8 addressing some of these and pole vault. But these two events were tify the influence of testosterone on perfor- issues in 2018, but Pielke remains dissatisfied. excluded from the final regulations, whereas mance in elite athletes. Published in 2017, the The 2018 regulations have also come under the 1,500 metres, for which a correlation was study, which was funded by World Athletics fire for being unduly discriminatory. Karkazis not seen, was included. and the World Anti-Doping Agency, found that explains that the rules explicitly exclude The details of the regulations have led elite female athletes with the highest testoster- women with high testosterone levels due some to question whether they are targeted one levels performed as much as 3% better in to polycystic ovarian syndrome — the most at Semenya. Bermon denies this, saying that events (including middle-distance races) than common cause of high testosterone — and, the limited number of cases in throwing events did those with the lowest levels6. These results following a 2019 court challenge, women with led World Athletics “to take a conservative formed the basis of new regulations in 2018, congenital adrenal hyperplasia. Now, they approach” for these sports. He also acknowl- requiring women competing in certain events target only those with a Y chromosome who edges criticism about the decision to include to have testosterone levels of below five nano- are sensitive to testosterone. Those individu- the 1,500 metres, but says it was because moles per litre for at least six months before als “have an innate physical advantage”, says athletes competing in middle-distance run- a competition. Handelsman. ning often run the longer distance, too. The study has been criticized, however. “It’s In addition, the rules apply only to runners But the debate over what level of testoster- deeply flawed,” says Roger Pielke Jr, a sports competing internationally in 400 metres one gives an advantage in which sports could be governance and policy researcher at the Uni- to one-mile events. “It’s bizarre,” says Ross missing the point. Ruth Wood, an endocrinolo- versity of Colorado Boulder, who has called Tucker, a sports scientist in Cape Town, South gist at the University of Southern California in

1936 1946 1966 1967 1985 POLICING SEX US sprinter Helen The International Women are subjected Chromosome testing is Spanish hurdler A HISTORY OF Stephens undergoes an Amateur Athletic to nude inspections by trialled at the European María José Martínez- SEX TESTING examination to verify Federation (IAAF) a panel of physicians at Cup. Polish sprinter Ewa Patiño is banned from her sex after journalists requires individuals the European Athletics Kłobukowska is the first competing after a IN WOMEN’S questioned her victory to have a medical Championships, to be disqualified as a chromosome test SPORT in the 100 metres at certificate proving their and undergo result. The IOC adopts reveals she is 46,XY. the Olympic Games eligibility to compete gynaecological checks the tests for the 1968 She appeals on the in Berlin. The result of in women’s events. The at the Commonwealth Winter Olympics, at grounds that she has the unspecified test, International Olympic Games. The tests are which Austrian skier Erik androgen insensitivity which confirms she is a Committee (IOC) unpopular, and some Schinegger (who was syndrome and therefore woman, is announced adopts the same rule athletes choose not to then living as a woman) gained no advantage. publicly. for the 1948 games. compete. is also disqualified. Her ban is lifted in 1988.

Los Angeles, argues that the issue is whether He and others think that the scrutiny given sports sociologist at Lincoln University in these naturally occurring hormones need to be to the sex of someone competing in women’s Canterbury, New Zealand. Kerr suggests that regulated in athletics in the first place. “There events is about making women conform to categories could be informed by the physical are no other sports in which we deliberately expected norms; the 2011 regulations, he characteristics required to excel in a particular limit an athlete’s natural abilities in service of points out, detailed physical features such sport. For example, sprinters could compete some idea of fairness,” she says. as breast size and shape that could be used against those with similar muscle mass and to identify athletes due to be investigated. proportion of fast-twitch fibres, or endurance Special treatment Some athletes have even been advised to wear athletes by muscle mass and lung capacity. Tucker thinks that the impact testosterone can padded bras when competing. “Sport is just Implementing such a system would be hard, have makes regulation necessary. “Male attrib- reflecting the society that we’ve always been, she admits — the systems in place in disability utes are such powerful contributors to perfor- and it’s discriminating against people we’ve sport are not without their critics. mance that, if you didn’t control them, they always discriminated against,” Pielke says. Other researchers propose an approach would dominate and drown out all the other similar to the golfing handicap system, or a cat- performance contributors,” he says. Wood egory, alongside men’s and women’s events, acknowledges that testosterone improves for athletes with DSDs. World Athletics has athletic performance, but stresses that these already provisioned for such a category in their women are not misrepresenting themselves or regulations, but Bermon thinks society is not using performance-enhancing drugs. “They’ve THEY’VE ALWAYS BEEN ready for it yet and introducing it could cause always been women and they’re competing as athletes to be stigmatized. “It’s impossible to women,” she says. WOMEN AND THEY’RE find a solution that will satisfy everyone,” he Alun Williams, a sports geneticist at says. “You have to go with the most reasona- Manchester Metropolitan University, UK, COMPETING AS WOMEN.” ble, which is based on science, to protect the agrees that women with DSDs and hyperan- female category.” drogenism should be treated no differently Martínez-Patiño, now a sports science from those with any other genetic trait that In 2020, international advocacy organiza- researcher at the University of Vigo in Spain, increases athletic ability. Celebrated Finnish tion Human Rights Watch documented some agrees that only concrete scientific evidence cross-country skier Eero Mäntyranta, who of the physical, social and psychological harm will resolve this debate, just as it helped to won three gold medals in the early 1960s, had a inflicted on women whose test results have led overturn her ban. But Patel sees a bigger genetic mutation that increased his red blood to disqualification from events. Indian athlete challenge. “This isn’t just about science,” she cells’ oxygen-carrying capacity by 25–50%, Santhi Soundarajan, for example, attempted says. “For there to be some progress, we have Williams points out. “The mutations found to take her own life after results of a sex test to tackle this issue from a science, ethics, law in DSD athletes don’t affect performance to were leaked to the media in 2006. Another and human-rights perspective.” an exceptional degree,” he says. Indian athlete ended her life in 2001 after Many commentators also question the finding out her results. Julianna Photopoulos is a science writer in ethics of policing an athlete’s sex. In 2019, the Sports governing bodies should be legally Bristol, UK, and near Thessaloniki, Greece.

United Nations Human Rights Council con- accountable for their discriminatory actions, 1. Bermon, S. et al. J. Clin. Endocrinol. Metab. 99, demned the 2018 regulations for failing to says Seema Patel, a sports lawyer at Notting- 4328–4335 (2014). be “reasonable and objective”, and the World ham Trent University, UK. She has proposed 2. Fénichel, P. et al. J. Clin. Endocrinol. Metab. 98, E1055–E1059 (2013). Medical Association urged physicians to take establishing an international independent 3. Healy, M. L., Gibney, J., Pentecost, C., Wheeler, M. J. & no part in implementing the new rules, arguing anti-discrimination sports unit that would Sonksen, P. H. Clin. Encrinol. 81, 294–305 (2014). 4. Bermon, S. Curr. Opin. Endocrinol. Diabetes Obes. 24, that they violate medical ethics and human act as a watchdog. Other researchers suggest 246–251 (2017). rights. Both statements were led by contin- ending sex segregation in individual sport 5. Hilton, E. N. & Lundberg, T. R. Sports Med. 51, 199–214 gents from South Africa, Semenya’s home altogether, and adopting a system similar to (2021). 6. Bermon, S. & Garnier, P.-Y. Br. J. Sports Med. 51, 1309–1314 country. “You are turning healthy people into that used in disability sport. “Our society is (2017). patients, using protocols that have not been structured around sex and gender, but it isn’t 7. Pielke, R. Jr., Tucker, R. & Boye, E. Int. Sports Law J. 19, 18–26 (2019). approved or studied for any medical purpose,” inclusive in terms of performance at all — for 8. Bermon, S., Hirschberg, A. L., Kowalski, J. & Eklund, E. says Pielke. both men and women,” says Roslyn Kerr, a Br. J. Sports Med. 52, 1531–1532 (2018).

1992 2009 2011 2014 2018 2019 The IAAF ends blanket Caster Semenya wins The IAAF adopts a Indian authorities ban The IAAF announces The CAS rules sex testing, instead the 800 metres at policy on testosterone, sprinter Dutee Chand, regulations that specify against Semenya. investigating female the World Athletics limiting blood levels owing to her high a testosterone limit of The following year, athletes only when Championships. During for people competing testosterone levels. She 5 nanomoles per litre she loses again questions are raised. the competition, the in women’s events to appeals to the Court for people competing at a Swiss court. The IOC, however, IAAF and media reveal 10 nanomoles per litre. of Arbitration for Sport in women’s 400 metres Semenya appeals to introduces a test for all that the 18-year-old is Those above this level (CAS), which rules in to one-mile events. the European Court women, based on the subject to sex testing. who are androgen her favour in 2015. The Middle-distance runner of Human Rights SRY gene. This remains She is forced to sensitive have to take IAAF regulations are Semenya appeals to the and says she will run a requirement until the withdraw, but is cleared testosterone-lowering suspended, and Chand CAS, which suspends in the unregulated 2000 Olympic Games to compete again drugs or undergo can compete without the rules pending a full 200 metres at the in Sydney, Australia. 11 months later. surgery to compete. restrictions. hearing. 2021 Tokyo Olympics.