Sex, gender, and sportsBMJ 2019; 364 doi: https://doi.org/10.1136/bmj.l1120 (Published 20 March 2019) Cite this as: BMJ 2019;364:l1120
All rapid responses
Dear Dr. Dixon, Dr. Bermon et al.,
Thank you for your comments on our Editorial. Individual-level analyses would perhaps enhance our understanding of the link between serum testosterone levels and athletic performance among intersex women compared to non-intersex women. However, even if privacy laws permitted access to these data, it would still prove difficult to show causal associations independent of so many other contributing biological and non-biological correlations.1 Requiring athletes with naturally high testosterone levels to reduce their blood level of testosterone with hormone suppression or surgery is unscientific - and not without potential risk- since by definition, individuals with differences of sex development have alterations in the way they process androgens at the cellular and tissue level, as explained in detail in Dr. Bermon et al.’s review article.2
A nuanced understanding of endocrinology and sex hormone physiology indeed facilitates informed opinions on the IAAF’s deliberations for categorizing female athletes, because the intracellular metabolism and downstream effects of androgens and estrogens are extremely complex. One of the authors of our editorial includes an internal medicine specialist and gender medicine scientist who has previously published on sex hormone variability, measurement error and the sensitivity/specificity of blood hormone samples at a given point in time.3 The other author is a sports science, injury prevention policy scholar and gender equity advocate. Both authors believe in data-informed decision-making, scientific integrity and merit-based, equitable access to discipline-specific recognitions and awards.
Having credentials does not mean that interpretation of the literature is straightforward or that decisions about eligibility for the sex category, or any other category in sport, are easy to make; different views need to be acknowledged, considered and respected. To this end, our editorial clearly acknowledged the bimodal distribution of testosterone in non-athletes but also cited additional studies that showed overlap among athletes, the lack of a validated test for androgen sensitivity, and the questionable relationship between testosterone levels alone and real-time sports performance. Because of BMJ’s restriction on the number of citations for editorials, we regretfully were unable to include Dr. Bermon et al’s review.
Cara Tannenbaum MD, MSc (internal medicine, epidemiology and biostatistics)
Sheree Bekker PhD (sports science, injury prevention)
1. Healy ML, Gibney J, Pentecost C, Wheeler MJ, Sonksen PH. Endocrine profiles in 693 elite athletes in the postcompetition setting. Clin Endocrinol 2014;81: 294–305.
2. Handelsman DJ, Hirschberg AL, Bermon S. Circulating Testosterone as the Hormonal Basis of Sex Differences in Athletic Performance. Endocr Rev 2018;39(5):803-29.
3. Tannenbaum C, Barrett-Connor E, Laughlin GA, Platt RW. A longitudinal study of dehydroepiandrosterone sulphate (DHEAS) change in older men and women: the Rancho Bernardo Study. Eur J Endocrinol. 2004;151(6):717-25.
Competing interests: No competing interests
We respond to correct misstatements in the editorial “Sex, Gender and Sports” by Tannenbaum and Bekker1. Appraising this contentious and complex area requires expertise in sports medicine, exercise physiology and endocrinology for which a background in gender scholarship alone may not be sufficient.
Throughout sports competitions, men outperform women by 8-12% for timed events and up to 20% for jumping events2 while the winning margin (to get gold, get a medal or make finals) is consistently <1%. Furthermore, the best elite female times are surpassed by hundreds of men every year3 including by boys from 14-15 years of age and onwards. Women could never compete effectively to win fame and fortune without a protected category. For decades, therefore, sport and society have embraced the concept of a separate, protected competition and category for women (after the onset of puberty) at all levels from recreational to elite events. What has always been controversial, and has recently gained increased public attention, is the definition of female for eligibility purposes. This controversy involves both transgender athletes and athletes with Disorders/Differences of Sex Development (DSD, also known as intersex). Similar to how disability, age, weight, and other protected competition classes are defined in sports, the IAAF has the obligation to set eligibility rules for the protected category of female events that ensure fair competition in that category. It has chosen to condition eligibility for the female category on having circulating serum testosterone below 5 nmol/L, because circulating testosterone in distinct male vs female ranges is the most recognized factor to explain the sex difference in performance and is objective and minimally intrusive.
Confounding this discussion is the confusion of sex and gender. Sex is biologically determined, including chromosomal sex, gonadal sex, and phenotypic sex. When one or more domains of sex are discordant, the individual is said to have a DSD according to current nomenclature4. Gender, on the other hand, is subjective, dynamic and self-determined, including male, female, and various non-binary forms. For well over 99% of adults, sex and gender are concordant and unambiguous. The remaining individuals comprise the DSD, transgender, and gender non-binary individuals. Because sports competitions are dichotomous for male and female, whereas sex and gender may not always be, a logical and scientifically based objective approach to defining who belongs in the protected female category is necessary5.
The editorial fails to cite the comprehensive scientific basis for the IAAF’s case outlined in a major review in a top peer-reviewed endocrinology journal6. That review defines the case for defending fairness for the vast majority of elite female athletes in the eligibility criteria for competing in the protected category of female events. It establishes with detailed supportive evidence the following facts which are misstated in the editorial: (1) circulating testosterone has a non-overlapping bimodal distribution with widely separated male and female reference ranges5, (2) this sex difference originates from the time of puberty when testosterone production in males increases to 15-20 times that in children or in women of any age2, (3) the detailed quantitative justification for the serum testosterone criterion (5 nmol/L) aims to include all females with or without polycystic ovarian syndrome (which causes mild increases in endogenous testosterone) but to exclude androgen-sensitive 46XY individuals with a DSD, testes and male circulating testosterone concentrations9, (4) although many variables such as genetics, nutrition, training and resources contribute to athletic performance, all of these are equally available to males and females but only males have the advantage of post-pubertal male circulating testosterone concentrations which produce sexually dimorphic effects on muscle and haemoglobin from puberty onwards in men, and (5) there is excellent, reproducible evidence from well-designed studies6 showing that testosterone has dose-response effects on muscle mass and strength and on haemoglobin concentration, which are strong determinants of power and endurance, respectively. Such potent effects of testosterone on athletic performance make it unfair for athletes with adult male circulating testosterone to compete in female events. Not only are healthy men ineligible to compete in the female category. So too are untreated adult male-to-female transgender individuals, as well as androgen-sensitive 46XY DSD individuals who have testes that produce male testosterone levels (and sperm) rather than ovaries and uteri.
In DSD individuals, physical and genital examinations are elements of professional gynaecological and endocrinology practice to evaluate signs of virilisation including hirsutism, deepening of the voice, breast atrophy, and clitoromegaly. This is necessary to reach a diagnosis and should not be considered as an “invasion of personal privacy”. For example, athletes with primary amenorrhea by the age of 16 require proper medical review for diagnosis and appropriate care7.
The editorial misleadingly cites a paper that relies on substandard testosterone measurements8 (immunoassay, inaccurate in females) without reference to a rebuttal9 or to a paper using state-of-the-art liquid chromatography-mass spectrometry10. It also confuses the discussion of sex differences in circulating testosterone by failing to recognize the impact of athletic exertion on serum testosterone. It would be equally misleading to try characterizing menstrual cycle length in athletes, many of whom experience exercise-induced menstrual disturbance for similar physiological reasons.
If the IAAF’s challenge to maintain fairness for the vast majority of elite female athletes is viewed as a form of discrimination, then, in this circumstance, it is fair, reasonable and proportionate to the need to preserve equal opportunities in the sport for male and female athletes. In stark contrast to other historical forms of discrimination, the IAAF regulations do not reinforce unfair disadvantages in a majority but rather aim to reduce an unfair advantage experienced by a tiny minority to the detriment of the large majority.
1. Tannenbaum C, Bekker S. Sex, gender, and sports. BMJ 2019;364:l1120. doi: 10.1136/bmj.l1120 [published Online First: 2019/03/22]
2. Handelsman DJ. Sex differences in athletic performance emerge coinciding with the onset of male puberty. Clin Endocrinol (Oxf) 2017;87(1):68-72. doi: 10.1111/cen.13350 [published Online First: 2017/04/12]
3. Coleman DL. Sex in Sport. Law and Contemporary Problems 2017;80(4):63-126.
4. Hughes IA. Biology of fetal sex development. In, The legal status of intersex persons. Eds. Scherpe JM, Dutta A, Helms T. Intersentia, Cambridge, UK. 2018, pp 25-44.
5. Auchus RJ. Endocrinology and women’s sports: the diagnosis matters. Law and Contemporary Problems 2017;80(4): 127-138.
6. Handelsman DJ, Hirschberg AL, Bermon S. Circulating Testosterone as the Hormonal Basis of Sex Differences in Athletic Performance. Endocr Rev 2018;39(5):803-29. doi: 10.1210/er.2018-00020 [published Online First: 2018/07/17]
7. Marsh CA, Grimstad FW. Primary amenorrhea: diagnosis and management. Obstet Gynecol Surv 2014;69(10):603-12. doi: 10.1097/OGX.0000000000000111.
8. Healy ML, Gibney J, Pentecost C, et al. Endocrine profiles in 693 elite athletes in the postcompetition setting. Clin Endocrinol (Oxf) 2014;81(2):294-305. doi: 10.1111/cen.12445
9. Ritzen M, Ljungqvist A, Budgett R, et al. The regulations about eligibility for women with hyperandrogenism to compete in women's category are well founded. A rebuttal to the conclusions by Healy et al. Clin Endocrinol (Oxf) 2015;82(2):307-8. doi: 10.1111/cen.12531 [published Online First: 2014/06/24]
10. Bermon S, Garnier PY, Hirschberg AL, et al. Serum androgen levels in elite female athletes. J Clin Endocrinol Metab 2014;99(11):4328-35. doi: 10.1210/jc.2014-1391
Competing interests: No competing interests
As a BMA member, GP and woman who competes in sport I am concerned at the BMJ publishing only one side of this very important issue for female sport.
I think that if the current IAAF threshold of 5 for female sport is waived for women with naturally high levels of testosterone (who are usually intersex athletes with a Y chromosome) this will be hugely disadvantageous to the 99% of women with testosterone levels well under 5.
If Caster Semenya really believed that her high endogenous testosterone level didn't improve her sporting performance then why is she so opposed to reducing it to get below the limit? The fairness to the other competitors should outweigh her reluctance to take testosterone reducing medication.
Intersex people or people with Disorders of Sexual Development (DSD) are a tiny proportion of the population (0.1% BBC More or Less) but are much more common in women's elite sport. The 3 medal winners in the 800m final at the last olympics are widely believed to have a DSD although public information on these private medical matters is hard to come by.
Male records for nearly all sports are "better" than the female equivalents.
If we want female sport to continue to exist and women with no Y chromosomes to continue to feel they have a fair chance of winning women's races then insisting all female athletes reduce their testosterone down to below 5nmol/L is fair. The greatest good of the greatest number principle has to be applied here.
There are other advantages people with Y chromosomes who have had male levels of testosterone since puberty have over XX people even if the testosterone levels are later suppressed but the IAAF is not currently considering those.
If Caster Semenya wins her case I think it will be a very sad and disappointing day for female sport.
Competing interests: No competing interests