The Olympic Games and Athletic Sex Assignment ONLINE FIRST

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August 04, 2016

JAMA

At least 2 women athletes subjected to intense media scrutiny in the past several years—Caster Semenya and Dutee Chand—are likely to attract additional attention in the forthcoming 2016 Summer Olympic Games in Brazil. Both women had pivotal, although inadvertent, involvement in the evolution of the currently suspended hyperandrogenism (testosterone) policies of the International Olympic Committee (IOC) and of the International Association of Athletic Federations (IAAF). Competitors had raised concerns regarding their “masculine” appearance and eligibility, and these concerns were further amplified by an intrusive media and social media.

Semenya emerged suddenly at the IAAF’s 2009 World Games in Berlin, where she easily won the 800-meter event—even though her time was far from the world record. Her appearance prompted complaints from her competitors and provoked her suspension pending thorough medical evaluation. Upon return to competition several months later, Semenya’s appearance was unchanged and she remained highly competitive but no longer excelled. Ultimately her case contributed to development of the so-called hyperandrogenism policy, which established a testosterone eligibility threshold of 10 nmol/L (288 ng/dL) for female athletes, unless the athlete is demonstrated to be insensitive to testosterone. Semenya subsequently finished second in the same event at the 2011 World Games in Daegu, South Korea, as well as at the 2012 London Olympics.

Chand, a promising young Indian sprinter with some national and regional success in the 100-meter run, elicited similar concerns from her competitors, prompting investigation by the Athletic Federation of India and the Sports Authority of India (SAI) and her subsequent well-publicized suspension from the Indian team sent to the June 2014 Commonwealth Games. Supported by the SAI and a number of prominent bioethicists, Chand appealed to the international Court of Arbitration for Sport. On July 27, 2015, in an extensive 160-page brief,¹ the Court ruled in her favor while suspending the hyperandrogenism policies for 2 years pending demonstration that androgen-sensitive women with atypically high serum testosterone levels “enjoy such a substantial performance advantage”¹ that their participation is unfair. Although the IOC was not a formal party to the dispute, this ruling effects the IOC as well as other sport-specific athletic federations that had adopted the hyperandrogenism policies.

Subsequently, Chand qualified for the Indian Olympic team on June 25, 2016, with times just below the 100-meter Olympic qualifying threshold of 11.32 seconds, becoming the first Indian woman in 36 years to qualify in that event. She is unlikely to win a medal—her best time of 11.24 seconds would have placed 15th in the London semifinals. On the other hand, Semenya has had an excellent pre-Olympic year, setting world best times for the year in both the 400-meter and 800-meter events, the most recent was an 800-meter time of 1 minute, 55.43 seconds, just under her breakthrough victory time 7 years earlier. Semenya’s reestablished preeminence was ascribed by her coach to more rigorous and consistent training. In Rio, should she come close to replicating her recent performances, the intense scrutiny from the media and complaints from other athletes likely will resume. Some will surely call for restoration of the testosterone threshold.

This is just the latest chapter of a saga that has extended over 80 years,² in part reflecting societal changes fostering greater participation of women in competitive sports, more recently including athletes from resource-poor, less-developed countries. During the early Cold War era (1945-1966), for which international sport competition served as a surrogate for the tension between the Eastern Bloc and Western Bloc countries, speculation about the femininity of prominent Soviet bloc athletes prompted initiation of anatomical inspections, often derided as “nude parades.”¹ These were replaced at the 1968 Olympic Games by the more innocuous but unreliable buccal smear, which reflects the presence of 2 X chromosomes, identifying unsuspecting 46,XY young women with genetic disorders of sex development, such as androgen insensitivity, who were undeniably female.³

It required another 20 years and persistent advocacy—together with greater understanding of what are now termed as disorders of sex development—for the misapplication of buccal smear screening to be appreciated, culminating in a workshop convened in Monaco by the then International Amateur Athletic Federation in 1990.⁴ The workshop’s major recommendation was that laboratory-based gender—or rather—sex testing should be discontinued, in part because doping procedures required passage of a urine sample under direct visual observation. The workshop participants also recommended that individuals born with a disorder of sex development who were raised as females be permitted to compete in women’s events irrespective of their chromosomal pattern. Although buccal smear screening was discontinued by the IAAF and most of the other Olympic sport federations, the IOC maintained genetic-based testing, using a more specific procedure for the sex-determining gene, until its Athletes’ Commission called for its abolition just prior to the 2000 Summer Olympics in Australia.⁵

These revised policies still allowed for explicit examination of cases potentially ineligible for women’s competition, as in the event of a direct challenge, and were ultimately invoked after Semenya’s sudden emergence in 2009. The subsequent and often sensationalized media coverage compelled the IOC and IAAF to again assemble meetings of individuals with appropriate scientific, medical, regulatory, and bioethical expertise, including a number of the 1990 Monaco workshop participants, ultimately leading to the hyperandrogenism policy, now suspended by the arbitration court.

It is increasingly evident that many factors, aside from sex and hormone milieu—favorable genetics, height, muscle type, economic opportunities, access to facilities, and skilled coaching among them—contribute to competitive success in sport. With respect to genetics, factors on the Y chromosome controlling for height, lean body mass, and other favorable sports-related characteristics may account for an overrepresentation of successful athletes with disorders of sex development in elite sports than their frequency in the general population.⁶ Genetic conditions that enhance performance in sport include congenital mutations of the erythropoietin receptor gene leading to high levels of hemoglobin,⁷ which does not disqualify athletes. There is no fundamental difference between congenital disorders leading to elevated testosterone levels, functional or not, and an erythropoietin receptor mutation leading to high hemoglobin. The emerging participation of transgender athletes adds further complexity. However, all of these biological differences are minuscule compared with the suspected use of performance-enhancing substances.⁸

Given the recognized 10% to 12% difference in athletic performance between sexes, it is not unreasonable to separate most competition by sex, certainly at the elite level embodied in the Olympic Games, even though, inevitably, doing so would be arbitrary. However, with the passage of time and the recurring public spectacle of young women, often from less-developed areas of the world, having their underlying biology indiscriminately scrutinized in the world media, it has become evident that the hyperandrogenism policies are no more salutary than earlier attempts to define sharp sex boundaries. In that respect, much more must be done to adequately inform all stakeholders—participating athletes, sports officials, team physicians, the media, fans, and the public at large—regarding the complexity and fluidity of factors that contribute to competitive success as well as to sex or gender identity. One of the fundamental recommendations published almost 25 years ago⁴ that athletes born with a disorder of sex development and raised as females be allowed to compete as women remains appropriate.