Serum androgen levels and their relation to performance in track and field: Mass spectrometry results from 2127 observations in male and female elite athletes

Abstract

Objective
To describe and characterise serum androgen levels and to study their possible influence on athletic performance in male and female elite athletes.

Methods
2127 observations of competition best performances and mass spectrometry-measured serum androgen concentrations, obtained during the 2011 and 2013 International Association of Athletics Federations World Championships, were analysed in male and female elite track and field athletes. To test the influence of serum androgen levels on performance, male and female athletes were classified in tertiles according to their free testosterone (fT) concentration and the best competition results achieved in the highest and lowest fT tertiles were then compared.

Results
The type of athletic event did not influence fT concentration among elite women, whereas male sprinters showed higher values for fT than male athletes in other events. Men involved in all throwing events showed significantly (p<0.05) lower testosterone and sex hormone binding globulin than men in other events. When compared with the lowest female fT tertile, women with the highest fT tertile performed significantly (p<0.05) better in 400 m, 400 m hurdles, 800 m, hammer throw, and pole vault with margins of 2.73%, 2.78%, 1.78%, 4.53%, and 2.94%, respectively. Such a pattern was not found in any of the male athletic events.

Conclusion
Female athletes with high fT levels have a significant competitive advantage over those with low fT in 400 m, 400 m hurdles, 800 m, hammer throw, and pole vault.

Full text

1
Bermon S, Garnier P-Y. Br J Sports Med 2017;0:1–7. doi:10.1136/bjsports-2017-097792
ABSTRACT
Objective To describe and characterise serum androgen
levels and to study their possible influence on athletic
performance in male and female elite athletes.
Methods 2127 observations of competition best
performances and mass spectrometry-measured serum
androgen concentrations, obtained during the 2011 and
2013 International Association of Athletics Federations
World Championships, were analysed in male and female
elite track and field athletes. To test the influence of
serum androgen levels on performance, male and female
athletes were classified in tertiles according to their free
testosterone (fT) concentration and the best competition
results achieved in the highest and lowest fT tertiles
were then compared.
Results The type of athletic event did not influence
fT concentration among elite women, whereas male
sprinters showed higher values for fT than male athletes
in other events. Men involved in all throwing events
showed significantly (p<0.05) lower testosterone and
sex hormone binding globulin than men in other events.
When compared with the lowest female fT tertile,
women with the highest fT tertile performed significantly
(p<0.05) better in 400 m, 400 m hurdles, 800 m,
hammer throw, and pole vault with margins of 2.73%,
2.78%, 1.78%, 4.53%, and 2.94%, respectively. Such a
pattern was not found in any of the male athletic events.
Conclusion Female athletes with high fT levels have a
significant competitive advantage over those with low
fT in 400 m, 400 m hurdles, 800 m, hammer throw, and
pole vault.
INTRODUCTION
Testosterone and its chemical derivatives, andro-
gens, have been abused by athletes since the 1950s.
These molecules produce improved performances
in both male and female athletes, sometimes in a
systematic way, as reported in the recently disclosed
documentation from experiments performed by
sports scientists in the former German Democratic
Republic.1 These scientists concluded after the
1972 Olympic Games in Munich that “the effects
of the treatment with androgenic hormones were so
spectacular, particular in female athletes in strength
dependent events, that few competitors not using
the drugs had a chance of winning”.
Although androgens have been widely abused by
female athletes during the last few decades, obvious
ethical and disciplinary limitations explain why
mechanisms underlying the performance-enhancing
effects of these androgens, as well as the magnitude
of their effects, have not been properly addressed.
However, the high incidence of such androgens in
adverse analytical findings from analysis of athletes’
samples suggests that the athletes at least perceive
they have a material impact on athletic perfor-
mance. For instance, among the 296 elite athletes
serving a doping ban under the rules of the Interna-
tional Association of Athletics Federations (IAAF)
as of 19 December 2016, 116 are females, of which
64 tested positive for androgens.2 These findings
confirm that these doping substances are the most
prevalent ones among female athletes, in spite of
continually improving analytical techniques and
strategies to detect their abuse.3 Additionally, the
highly increased endogenous productions of andro-
gens demonstrated by some female athletes, as well
as their virilised phenotype, have been highlighted
in sports and represent a subject of controversy
among the scientific community.4–9
To address this sensitive issue, the IAAF and
the International Olympic Committee respec-
tively published regulations and recommendations
governing the eligibility of women with hyper-
androgenism to compete in the female category
of competitions.10 11 An Indian athlete, Dutee
Chand, challenged the IAAF regulations before
the Court of Arbitration for Sports (CAS).12 The
CAS panel accepted that “possessing high levels
of testosterone, and thereby increased LBM (Lean
Body Mass), … creates a competitive advantage”,
and also that there was “evidence and opinion to
support the conclusion that endogenous and exog-
enous testosterone have identical physiological
effects”; however, the panel ruled that, in order to
justify the discriminatory effect the IAAF regula-
tions have on androgen-sensitive hyperandrogenic
athletes (requiring them to have treatment to lower
their endogenous testosterone levels in order to
continue to compete), the IAAF must also produce
“sufficient scientific evidence about the quantitative
relationship between enhanced testosterone levels
and improved athletic performance in hyperandro-
genic athletes”, such as evidence of a correlation
between testosterone levels and relative rankings
in competitive athletics events. It suspended the
IAAF regulations pending receipt of such further
evidence. The purpose of this article is therefore
to explore the possible relationship between serum
androgen concentration (particularly serum testos-
terone concentration) and athletic performance.
Serum androgen levels and their relation to
performance in track and field: mass spectrometry
results from 2127 observations in male and female
eliteathletes
Stéphane Bermon,1 Pierre-Yves Garnier2
Original article
To cite: BermonS,
GarnierP-Y.
Br J Sports Med Published
Online First: [please include
Day Month Year]. doi:10.1136/
bjsports-2017-097792
►Additional material is
published online only. To view
please visit the journal online
(http:// dx. doi. org/ 10. 1136/
bjsports- 2017- 097792).
1Université Côte d'Azur,
LAMHESS Nice, France and
Monaco Institute of Sports
Medicine and Surgery, Monaco
2International Association of
Athletics Federations Health and
Science, Monaco, Monaco
Correspondence to
Stéphane Bermon, Stéphane
Bermon, Institut Monégasque
de Médecine et Chirurgie
du Sport, avenue d’Ostende;
bermon@ unice. fr
Received 14 March 2017
Revised 12 May 2017
Accepted 15 May 2017

2Bermon S, Garnier P-Y. Br J Sports Med 2017;0:1–7. doi:10.1136/bjsports-2017-097792
Original article
METHODS
Our aim was to describe and characterise serum androgen
levels in athletes taking part in the 2011 (Daegu, South Korea)
and 2013 (Moscow, Russia) IAAF World Championships. As a
second step, we studied the influence of serum androgen levels
and athletic performance in both male and female populations.
All logistical, methodological (including sampling, pre-analyt-
ical conditions and analytical methods), and ethical aspects of
this project have been extensively described and published else-
where.13–15 The project comprised a study of elite female athletes
taking part in the Daegu and the Moscow IAAF World Champi-
onships, and elite male athletes taking part in the Moscow IAAF
World Championships. The data obtained from male athletes
competing in Daegu were not selected for the purpose of this
study since the serum androgen levels were not measured by
mass spectrometry, but by immunological methods.
Subjects
The subjects were athletes competing at the highest level in
the different track and field events (of which there are 21 for
females and 22 for males). Athletes with missing blood data were
excluded from the study, as were athletes who did not start, did
not finish, were disqualified, or had no results. Athletes taking
part in relay races (but not taking part in individual races) were
also excluded. In the female athlete group, 17.3% of athletes
took part in both the 2011 and 2013 World Championships,
and all their results were included in our statistical analysis. As
a result, the present study relies on 1332 observations of elite
female athletes and 795 observations of elite male athletes—a
total of 2127 observations. A blood sample was taken from each
of these athletes.
Measures
Athletes were required to go to the doping-control station at any
time during their stay, provided it was at least 24 hours after their
arrival in Daegu or Moscow and at least 2 hours after intense
exercise. All pre-analytical conditions and analytical methods
have been extensively described in previous publications.13
14 In female athletes, samples were collected regardless their
menstrual status and phase. Whole blood samples and sera were
collected after 10 min of rest, in a non-fasting state, and sera
were frozen at −20°C until assay. Haemoglobin (Hb) concentra-
tion was measured as part of the athlete haematological passport,
as previously described.14 All analyses for endocrine parameters
were conducted in the Lausanne World Anti-Doping Agency
(WADA)-accredited laboratory. Serum sex hormone binding
globulin (SHBG) and luteinising hormone (LH) concentrations
were determined with an Immulite 2000 (Siemens Healthcare
Diagnostics SA, Zürich, Switzerland), whereas serum dehy-
droepiandrosterone sulfate (DHEAS) was determined with
an Immulite 2000 XPi (Siemens Healthcare Diagnostics SA,
Zürich, Switzerland). Measurement kits, reagents, equipments,
adjustors and protocols were provided by the manufacturer.
All samples, adjustors and quality controls (QC) were run with
the same batch lot numbers. Finally, serum testosterone (T) and
androstenedione (A4) were measured by LC-MS high resolution
(Q-Exactive, ThermoFisher Scientific, Reinach, Switzerland).
Free T (fT) was calculated using the Sodergard formula, with
a standard average albumin concentration of 4.3 g/dL.16 For
purpose of comparison with previously published data, albumin
concentration was considered at 4.3 g/dL (and not 4.0 g/dL as
recommended by some authors) for fT calculation in females.
For each athlete, the best performance (heats or finals) achieved
during the corresponding World Championships was considered
for statistical analysis.
Statistical analyses
Data distributions were assessed for normality using visual
inspection, calculation of skewness and kurtosis, and the Kolm-
ogorov-Smirnov test. In order to test for the possible effects of
the type of athletic event on hormonal parameters, all athletes
were assigned to one of the seven following groups: throwing
events (discus throw, javelin throw, hammer throw, and shot put),
jumping events (high jump, long jump, triple jump, pole vault),
sprinting events (100 m, 110 m hurdles, 200 m, 400 m, 400 m
hurdles), combined events (heptathlon for females and decathlon
for males), middle distance running (800 m, 1500 m, and 3000
m steeple chase), long distance running (5000 m, 10 000 m, and
marathon), and race walking (20 km race walking in females and
20 km and 50 km race walking in males). The effects of the type
of athletic event were tested with a one-way analysis of variance
(ANOVA) on log-transformed age and endocrine parameters
across the considered groups and Tukey HSD (Spjotvoll/Stoline)
post hoc test when appropriate. In order to test the influence of
serum androgen levels on athletic performance, in each of the 21
female athletic events and 22 male athletic events, athletes were
classified in tertiles according to their fT concentration. Then, the
athletic performances and Hb concentrations of the highest and
lowest fT tertiles were compared by using non-paired Student's
t-test. These different athletic events were considered as distinct
independent analyses and adjustment for multiple comparisons
was not required. Classification in tertiles according to the T
(both genders) and Hb (female gender) concentrations were also
performed and appear online (see supplementary tables 6-13).
When appropriate, a χ2 test was used. Correlations were tested
by the Pearson correlation test. A value of p<0.05 was consid-
ered statistically significant. All data analyses were performed
using Statistica version 7.1 (StatSoft, France).
RESULTS
For the female group of athletes, their ages and concentrations
of serum T, A4, DHEAS, LH and SHBG, as well as the calculated
fT, are presented in table 1. Among the 1332 female observations,
44 showed an fT concentration >29.4 pmol/L.17 Twenty-four
female athletes showed a T concentration >3.08 nmol/L which
has been calculated to represent the 99th percentile in a previous
normative study in elite female athletes.13 Among these 24
individuals, nine were diagnosed with a condition of hyperan-
drogenic disorder of sex development (DSD), nine were later
found to have been doping, and six athletes were impossible to
classify. This also explains the high calculated standard deviation
for T and fT in some groups of athletic events (table 1). Long
distance runners showed lower A4 concentrations than sprinter
and middle distance runners, and lower DHEAS concentrations
than sprinters, race walkers and throwers.
For the male group of athletes, their ages and serum T, A4,
DHEAS, LH and SHBG concentrations, and the calculated fT, are
presented in table 2. Among the 795 male athletes, 101 showed
an fT value <0.23 nmol/L. Fourteen of them were sprinters, 14
were middle distance runners, 21 were long distance runners,
16 were race walkers, 20 were jumpers, 13 were throwers,
and two were combined events specialists. The male sprinters
showed a higher fT concentration than the other male athletes.
Interestingly, throwers showed significantly lower T and SHBG
concentrations than the other male athletes.

3
Bermon S, Garnier P-Y. Br J Sports Med 2017;0:1–7. doi:10.1136/bjsports-2017-097792
Original article
The comparison of the highest and lowest female fT tertiles
and their associated athletic performances in running events is
presented in table 3. When compared with the lowest fT tertile,
the highest fT tertile demonstrated significantly better perfor-
mances in 400 m, 400 m hurdles, and 800 m with calculated
differences of 2.73%, 2.78%, and 1.78%, respectively.
In other non-running events (table 4), hammer throwers and
pole vaulters with high fT concentrations performed better
(+4.53% and 2.94%, respectively) than their peers with low fT
concentrations.
In male elite athletes, no significant difference in performance
was noted when comparing the lowest and the highest fT tertiles.
DISCUSSION
To the best of our knowledge, this study is the first to report serum
androgen concentrations in such a large number of elite male
and female athletes. In the female athlete group, the statistical
analysis on performance and androgen levels, conducted using
only the 2013 Moscow data, confirmed the statistical findings
obtained from the 2011 Daegu dataset. This is why both female
datasets (from 2011 and 2013) were merged and as a conse-
quence some duplicate observations at the 2-year interval were
included. This oversampling bias is negligible, since androgen
level outliers from the 2011 Daegu dataset did not appear in
the 2013 Moscow dataset as a consequence of either IAAF anti-
doping or hyperandrogenism regulations enforcement.10
Our study design cannot provide evidence for causality
between androgen levels and athletic performance, but can indi-
cate associations between androgen concentrations and athletic
performance. Thus, we deliberately decided not to exclude
performances achieved by females with biological hyperandro-
genism and males with biological hypoandrogenism whatever
the cause of their condition (oral contraceptives, polycystic
ovaries syndrome, disorder of sex development, doping, over-
training). As a consequence, the calculated mean fT value in
the present study is higher than the 8.06 pmol/L median value
previously reported in a similar female population.13 Oral
contraceptive intake had not been registered during the 2013
Table 1 Age and androgenic parameters in the female population
n Age(years) fT(pmol/L) T(nmol/L) A4(nmol/L) DHEAS(µmol/L) LH(IU/L) SHBG(nmol/L)
Sprinting 390 25
(22–27)
9.5
(6.0–13.0)
0.73
(0.52–0.99)
3.38
(2.50–4.34)*
6.18
(4.13–9.40)*
3.35
(1.75–5.86)
56.5
(40.7–79.4)
Middle distance 186 25
(23–28)
8.1
(5.0–12.0)
0.64
(0.46–0.92)
3.26
(2.39–4.50)*
5.99
(3.72–8.86)
3.72
(1.78–6.74)
56.5
(42.8–75.3)
Long distance 165 28
(24–31)
7.2
(4.8–9.6)
0.55
(0.43–0.78)
2.80
(2.10–3.80)
4.61
(2.77–7.15)
2.86
(1.60–5.09)
55.8
(41.2–73.7)
Walking 97 25
(23–29)
7.5
(5.0–11.0)
0.58
(0.44–0.82)
3.20
(2.27–4.21)
7.06
(4.10–10.80)**
3.05
(1.36–4.38)
52.5
(35.1–70.9)
Jumping 220 27
(23.5–29)
7.9
(5.0–11.0)
0.68
(0.48–0.92)
2.32
(2.47–4.60)
5.69
(3.79–8.46)
3.78
(2.11–6.52)
60.0
(44.10–78.9)
Throwing 211 27
(23–29)
10.5
(7.1–15.1)
0.72
(0.56–0.98)
3.24
(2.32–5.40)
6.61
(4.34–9.37)**
3.38
(2.07–5.24)
44.2
(29.0–66.8)
Combined events 53 26
(23–28)
6.5
(4.8–9.5)
0.62
(0.42–0.79)
3.00
(2.01–3.42)
5.51
(3.75–8.86)
3.67
(1.84–5.81)
61.6
(46.7–87.7)
All 1332 26
(23–29)
8.5
(5.7–12.3)
0.67
(0.48–0.90)
3.22
(2.34–4.33)
5.92
(3.82–9.05)
3.41
(1.80–5.77)
55.3
(38.9–74.0)
Data are presented as median (25th percentile–75th percentile].
Different from Long distance: *p<0.05, **p<0.01.
A4, androstenedione; DHEAS, dehydroepiandrosterone sulfate;fT, free testosterone; LH, luteinising hormone; SHBG, sex hormone binding globulin;T, testosterone.
Table 2 Age and androgenic parameters in the male population
n Age(years) fT(nmol/L) T(nmol/L) A4(nmol/L) DHEAS(µmol/L) LH(IU/L) SHBG(nmol/L)
Sprinting 229
25
(22–27)
0.39
(0.31–0.48)
17.6
(13.8–22.0) ††
2.02
(1.64–2.60)
8.28
(5.99–10.88)
2.94
(2.06–4.04)
31.2
(24.9–38.0) ††
Middle distance 117 24
(22–28)
0.36
(0.28–0.42) *
15.91
(13.0–21.0) ††
2.15
(1.74–2.90)
8.48
(6.26–10.91) ‡‡
2.64
(2.06–3.62)
32.6
(26.4–41.7) ††
Long distance 102 27
(23–30)
0.31
(0.25–0.38) **
15.4
(11.6–19.0) †
1.91
(1.55–2.40)
6.20
(4.55–10.03)
2.74
(2.04–3.54)
34.5
(26.8–42.4) ††
Walking 94 26.5
(25–30)
0.34
(0.26–0.40) **
15.0
(11.8–18.2) †
2.14
(1.59–2.69)
7.57
(4.92–10.25)
2.77
(2.16–4.06)
28.6
(24.5–37.0) ††
Jumping 113 26
(23–29)
0.34
(0.26–0.42) **
15.7
(12.0–19.2) ††
2.13
(1.69–2.67)
8.86
(6.17–11.83) ‡
2.74
(1.96–3.91)
32.2
(26.6–37.5) ††
Throwing 115 28
(24–31)
0.30
(0.26–0.36) **
12.4
(9.8–15.4)
2.07
(1.59–2.88)
8.72
(6.05–13.66) ‡‡
3.45
(2.41–5.01)
21.6
(17.0–27.0)
Combined events 25 25
(23–27)
0.37
(0.31–0.42)
16.1
(13.7–21.5)
2.28
(1.87–2.67)
9.58
(6.76–11.12)
3.06
(2.26–4.41)
31.5
(24.7–41.9) ††
All 795
25
(23–29)
0.34
(0.27–0.43)
15.6
(12.1–19.8)
2.06
(1.65–2.65)
8.20
(5.72–11.99)
2.94
(2.11–4.10)
30.6
(23.5–37.9)
Data are presented as median (25th percentile–75th percentile).
Different from Sprinting: *p<0.05, **p<0.01. Different from Throwing: †p<0.05, ††p<0.01. Different from Long distance: ‡p<0.05, ‡‡p<0.01.
A4, androstenedione; DHEAS, dehydroepiandrosterone sulfate;fT, free testosterone; LH, luteinising hormone; SHBG, sex hormone binding globulin;T, testosterone.

4Bermon S, Garnier P-Y. Br J Sports Med 2017;0:1–7. doi:10.1136/bjsports-2017-097792
Original article
World Championships, but these medicines were reported to be
used by approximately 15% of elite female athletes.13
Key findings
As oral contraceptives increase SHBG concentration and T
bioavailability, we performed the main statistical analysis on
fT. Given criticism of the inaccuracy of the Sodergard formula,
we calculated fT by using the Sartorius formula and confirmed
our statistical findings.18 19 We also confirmed that the type
of athletic event does not influence T and fT concentrations
in elite females.13 Moreover, we found that female endurance
runners showed decreased A4 and DHEAS concentrations when
compared with other athletes. This finding can be explained by
the suppressive effect of endurance training on adrenocortico-
tropic hormone and the adrenal production of T.20 As far as male
athletes are concerned, sprinters showed higher values for fT,
but not for T, than other athletes.
No result including fT has been published on this matter so
far; the only available source is the article by Cardinale and
Stone who also reported, on a small number of subjects, higher
Table 3 Comparison of the lowest and highest fT tertiles and their
associated athletic performances in female running events
Event n All athletes
Lowest fT
tertile
Highest fT
tertile
100 m
Time s 112 11.88 (0.88) 11.78 (0.83) 12.09 (0.97)
fT pmol/L (1.4–32.8) (1.4–8.2) (12.1–32.8)
T nmol/L 0.90 (0.52) 0.53 (0.18) 1.32 (0.63)
100 m H
Time s  73 13.15 (0.48) 13.02 (0.46) 13.24 (0.54)
fT pmol/L (1.0–29.6) (1.0–6.6) (9.9–29.6)
T nmol/L 0.75 (0.33) 0.52 (0.20) 0.92 (0.34)
200 m
Time s 71 23.43 (0.90) 23.28 (0.74) 23.65 (1.11)
fT pmol/L (1.0–28.2) (1.0–6.3) (11.1–28.2)
T nmol/L 0.78 (0.48) 0.47 (0.15) 1.11 (0.62)
400 m
Time s 67 52.23 (2.56) 52.60 (3.30) 51.16 (1.06)*
fT pmol/L (1.2–124.4) (1.2–6.5) (13.0–124.4)
T nmol/L 2.82 (7.41) 0.45 (0.21) 7.08 (11.64)
400 m H
Time s 67 56.34 (2.65) 57.38 (3.53) 55.78 (1.60)*
fT pmol/L (1.4–174.5) (1.4–7.9) (12.4–174.5)
T nmol/L 1.03 (1.13) 0.54 (0.26) 1.68 (1.63)
800 m
Time s 64 121.80 (5.42) 122.68 (3.71) 120.50 (2.90)*
fT pmol/L (1.1–469.3) (1.1–7.0) (12.2–469.3)
T nmol/L 1.47 (4.03) 0.40 (0.14) 3.26 (6.60)
1500 m
Time s 66 250.16 (6.42) 250.00 (3.23) 250.65 (7.10)
fT pmol/L (0.6–48.7) (0.6–7.0) (10.8–48.7)
T nmol/L 0.79 (0.49) 0.50 (0.27) 1.12 (0.62)
3000 m SC
Time s 56 581.61 (17.39) 579.81 (17.74) 581.03 (18.70)
fT pmol/L (2.0–43.2) (2.0–4.9) (8.0–43.2)
T nmol/L 0.73 (0.54) 0.39 (0.15) 1.20 (0.66)
5000 m
Time s 40 932.67 (39.73) 932.80 (32.4) 935.80 (48.30)
fT pmol/L (2.8–51.8) (2.8–6.1) (8.0–51.8)
T nmol/L 0.73 (0.59) 0.41 (0.14) 1.07 (0.84)
10 000 m
Time s 33 1912.6 (55.6) 1903.6 (61.8) 1913.8 (50.6)
fT pmol/L (2.7–26.4) (2.7–4.5) (9.0–26.4)
T nmol/L 0.59 (0.27) 0.33 (0.13) 0.85 (0.21)
Marathon
Time s 92 9726.6 (790.9) 9921.3 (1018.9) 9620.1 (736.5)
fT pmol/L (2.1–363.6) (2.1–5.6) (9.0–363.6)
T nmol/L 0.97 (2.55) 0.41 (0.14) 1.85 (4.23)
Data are presented as mean (SD) or (min–max).
Different fromthe lowest fT tertile: *p<0.05.
fT, free testosterone; H, hurdles; SC, Steeple Chase; T, testosterone.
Table 4 Comparison of the lowest and highest fT tertiles and their
associated athletic performances in female non-running events
Event n All athletes
Lowest fT
tertile
Highest fT
tertile
Discus
Distance m 48 60.18 (4.24) 59.58 (4.97) 60.69 (4.34)
fT pmol/L (2.1–33.4) (2.1–7.5) (12.7–33.4)
T nmol/L 0.82 (0.44) 0.60 (0.24) 1.16 (0.53)
Hammer throw
Distance m 54 69.31 (4.34) 67.76 (2.75) 70.83 (5.16)*
fT pmol/L (1.0–50.4) (1.0–8.5) (13.1–50.4)
T nmol/L 0.82 (0.40) 0.62 (0.31) 1.13 (0.36)
Shot put
Distance m 54 18.21 (1.33) 17.94 (1.58) 18.54 (1.23)
fT pmol/L (1.8–319.9) (1.8–10.0) (16.8–319.9)
T nmol/L 1.03 (1.57) 0.57 (0.22) 1.72 (2.45)
Javelin
Distance m 55 60.40 (4.35) 61.9 (4.64) 60.37 (4.40)
fT pmol/L (2.2–26.8) (2.2–7.3) (9.9–26.8)
T nmol/L 0.73 (0.27) 0.59 (0.21) 0.90 (0.16)
Long jump
Distance m 62 6.46 (0.28) 6.39 (0.34) 6.47 (0.30)
fT pmol/L (2.1–24.2) (2.1–6.9) (10.4–24.2)
T nmol/L 0.80 (0.43) 0.53 (0.23) 1.00 (0.26)
Triple jump
Distance m 54 14.00 (0.49) 14.05 (0.52) 13.95 (0.43)
fT pmol/L (1.4–242.8) (1.4–6.4) (9.2–242.8)
T nmol/L 0.92 (1.59) 0.42 (0.16) 1.66 (2.54)
High jump
Distance m 56 1.91 (0.07) 1.89 (0.06) 1.90 (0.06)
fT pmol/L (3.6–23.4) (3.6–6.0) (8.9–23.4)
T nmol/L 0.74 (0.42) 0.48 (0.21) 1.07 (0.51)
Pole vault
Distance m 48 4.51 (0.18) 4.41 (0.18) 4.54 (0.17)*
fT pmol/L (2.0–22.9) (2.0–6.3) (8.7–22.9)
T nmol/L 0.78 (0.31) 0.63 (0.28) 0.98 (0.31)
20 km RW
Time s 97 5600 (617) 5680 (235) 5647 (232)
fT pmol/L (1.8–31.9) (1.8–5.9) (9.7–31.9)
T nmol/L 0.62 (0.29) 0.43 (0.16) 0.87 (0.30)
Heptathlon
Point 53 6121 (309) 6095 (353) 6096 (263)
fTpmol/L (1.8–30.4) (1.8–5.7) (8.9–30.4)
T nmol/L 0.69 (0.36) 0.47 (0.12) 1.02 (0.43)
Data are presented as mean (SD) or (min–max).
Different fromthe lowest fT tertile: *p<0.05.
fT, free testosterone; RW, race walking;T, testosterone.

5
Bermon S, Garnier P-Y. Br J Sports Med 2017;0:1–7. doi:10.1136/bjsports-2017-097792
Original article
T concentrations in male sprinters when compared with hand-
ball and soccer players.21 The observed low T concentration in
male throwers is an unexpected result. This trend is observed in
all throwing events: mean T concentrations were 14.1 nmol/L,
12.6 nmol/L, 11.2 nmol/L, and 14.5 nmol/L in discus, hammer
throw, shot put, and javelin, respectively. All these results are
below the T concentration measured in male race walkers and
marathon runners which are athletic events where hypoandro-
genism is a commonly reported condition.22 Male throwers not
only showed low T but also low SHBG concentrations. These
differences are not explained by age or ethnic background in our
subgroup of male throwers.
One explanation could be the higher prevalence of doping
with exogenous androgens in this subgroup. Indeed, it has been
reported that oral administration of androgens decreases both T
(a well-known withdrawal phenomenon experienced when the
athletes are approaching competitions and associated urinary
anti-doping tests) and SHBG concentrations.23 24 Recently,
Rasmussen et al showed that a significant proportion of former
androgen abusers exhibit moderately or notably lowered testos-
terone levels years after cessation of androgen abuse.25 However,
our male throwers did not show decreased LH concentrations
(a reported consequence of doping with androgens via the
negative feedback loop of the hypothalamic-pituitary-gonadal
axis).26 Although it has not been measured in the present study,
throwers are also likely to be athletes with the highest body mass
index and fat mass. Hence, the known negative influence of fat
mass on SHBG concentration and T bioavailability may possibly
account for the low T and SHBG concentrations reported in
male throwers in our study.27
In female athletes, a high fT concentration appears to confer a
1.8–2.8% competitive advantage in long sprint and 800 m races.
Taking into account a linear dose–response relationship between
serum androgen levels and athletic capacity, it is possible that the
magnitude of this advantage will be even greater for an andro-
gen-sensitive female athlete with T or fT concentrations within
the normal male range.28 A possible explanation for these findings
is the important contribution of oxidative metabolism in the total
energy spent to run a 400 or 800 m race. Duffield et al calculated
that in females the aerobic/anaerobic energy system contribution
is 45%/55% for 400 m and 70%/30% for 800 m.29 As androgens
are erythropoietic hormones, it is tempting to hypothesise that
female athletes with high T and fT levels show high Hb concen-
trations which in turn increase the oxygen-carrying capacity and
(non-bicarbonate) extracellular buffering capacity30—both of
which are crucial when running 400 m, 400 m hurdles or 800 m
races. For each of these three running events, fT concentration
significantly (p<0.05) positively correlated with Hb concentra-
tion, and within these groups, athletes with the highest fT levels
showed higher Hb concentrations than athletes with the lowest
fT levels (table 5). This average difference in Hb concentration is
approximately 0.6 g/100 mL. However, in these three events,
we found no significant correlation between Hb concentration
and performance (table 5), and when athletes were clustered in
tertiles according to their Hb concentrations, no difference was
noted in performances between the high and low Hb (see online
supplementary results).
Taken together, these results show that whereas fT positively
influences Hb, fT concentration is a stronger determinant of
performance in the 400 m, 400 m hurdles and 800 m than
Hb concentration. Increased lean body mass, mental drive and
aggressiveness, which are also known to be influenced by andro-
gens, provide alternative explanations, but these parameters
have not been measured in the present study.31
Free testosterone concentration and throwing events
The relationship between high fT concentration and better
performances by female athletes in hammer throw and pole vault
(+4.5% and +2.9%, respectively) is a finding reported for the first
time. In order to perform at elite level in these two events, athletes
must achieve a high level of power and strength, supported by an
increased lean body mass. Although an effect of high androgen
levels on these functional and anthropometric characteristics is
likely, performance in other strength and power events like shot
put, javelin or long jump does not seem to be influenced by the
fT concentration in our study. Pole vault and hammer throw are
the athletic events which require the highest spatial abilities. For
instance, hammer throw requires three final high speed turns
(more than 720°/s), inside a 7-foot diameter ring, to release a 4 kg
hammer at a terminal speed of 27 m/s with an optimal release angle
between 43° and 44° to the horizontal plan and within a cage sector
of only 34.9°. There are well known sex differences in spatial abili-
ties as measured with the mental rotation task (MRT), where males
have an advantage over females.32 This difference is of critical
importance, since the performance at the MRT is associated with
the type of sports practised and the level of expertise. In a recent
study, including non-athletes, orienteers, gymnasts and endurance
runners, Schmidt et al showed that athletes outperformed non-ath-
letes at the MRT. Interestingly, athletes with high mental rotation
demand, like gymnasts (egocentric transformation) and orien-
teers (allocentric transformation), showed the best results at the
MRT. 33 By using functional MRI assessment, two research groups
showed a female-like activation pattern in mental rotation-related
brain areas in individuals with complete androgen insensitivity
syndrome, indicating that the sexual differentiation of visuospatial
neural activation is not directly influenced by sex chromosomal
composition, but is determined by exposure to androgens.34 35
Speculation as to mechanisms underpinning our findings
Our hypothesis is that, in addition to their recognised effect on
aggressiveness and risk-taking behaviours, androgens exert their
ergogenic effects on some sportswomen through better visuo-
spatial neural activation. This assumption, which may be of
critical importance in acrobatic, team or racket sports, warrants
Table 5 Comparison of the haemoglobin concentrations in the
lowest and highest fT tertiles and correlation between haemoglobin
concentration and free testosterone or athletic performance in female
400 m, 400 m hurdles and 800 m
400 m Hb
Lowest fT tertile 13.41 (0.90)
Highest fT tertile 14.03 (1.03) *
Correlation fT vs Hb r=0.26 †
Correlation performance vs Hb r=−0.12
400 m H Hb
Lowest fT tertile 13.25 (0.88)
Highest fT tertile 13.88 (0.99) *
Correlation fT vs Hb r=0.29 †
Correlation performance vs Hb r=0.04
800 m Hb
Lowest fT tertile 13.47 (0.78)
Highest fT tertile 14.16 (1.09) *
Correlation fT vs Hb r=0.26 †
Correlation performance vs Hb r=0.03
Data are presented as mean (SD).
Different fromthe lowest tertile *p<0.05. Significant correlation †p<0.05.
fT, free testosterone; H, hurdles; Hb, haemoglobin concentration in g/100 mL.

6Bermon S, Garnier P-Y. Br J Sports Med 2017;0:1–7. doi:10.1136/bjsports-2017-097792
Original article
further research. Unlike female athletes, males with the highest
fT concentration did not outperform those with the lower fT
concentration in any of the events. Our results obtained in
both sexes could confirm the recent hypothesis from Bird et al,
suggesting that in terms of gains in muscle mass and strength,
females have the capacity to gain a greater relative increase
from androgen use than males.36 Hence, when the results from
male and female athletes are pooled, the relationship linking T
concentration to athletic performance would look more like a
sigmoid curve, with the steepest portion found between above
the female range upper limit and below the male lower limit.
In conclusion, our original work confirmed the weak influ-
ence of particular athletic events on circulating androgens levels
in females, whereas male throwers showed low T and SHBG
concentrations but normal fT levels. Such a finding might be a
consequence of either a higher prevalence of doping with andro-
gens or a higher adiposity in this group of athletic events. In
female 400 m, 400 m hurdles, 800 m, hammer throw and pole
vault, high fT concentration is associated with a higher (from
1.8% to 4.5%) level of athletic performance when compared
with competitors with low fT. In addition to the well-known
performance-enhancing effects of androgens on lean body mass,
erythropoiesis, mental drive and aggressiveness, the results
obtained in pole vaulters and hammer throwers seem to confirm
that females with high levels of androgens may also benefit from
a competitive advantage through improved visuospatial abilities.
What are the findings?
►In females, theserum testosteronelevel is not influenced by
the type of athletic events, whereas androstenedioneand
DHEAS are decreased in endurance runners.
►Male throwers have lower testosteroneand SHBG
concentrations than other elite male athletes.
►In 400 m, 400 m hurdles, 800 m, hammer throw and pole
vault, female athletes with high testosterone levels benefit
from a 1.8% to 4.5% competitive advantage over other
female competitors with normal androgen levels.
How might it impact on clinical practice in the future?
►The quantitative relationship between enhanced
testosteronelevels and improved athletic performance
should be taken into account when the eligibility of women
with hyperandrogenism to compete in the female category
of competition is discussed.
Acknowledgements The authors wish to acknowledge the organisational and
logistical support provided by the Local Organising Committee of both theDaegu
and Moscow IAAF World Championships. The authors would like to acknowledge
theSwiss Laboratory for Doping Analyses, Siemens Healthcare Diagnostics SA
(Zürich, Switzerland) for providing hormone tests, and Ms Jane Davies and Ms
Susanna Verdesca for processing the data and checking the manuscript.
Contributors SB was involved in the study design, statistical analysis and
manuscript drafting. PYG was involved in the study design, data collection, and
manuscript drafting.
Funding This study was supported by the International Association of Athletics
Federations, the World Anti-Doping Agency.
Disclaimer SB is a medical and scientific consultant for the IAAF and a member
of the IAAF and IOC working groups on hyperandrogenic female athletes and
transgender athletes and for that purpose appeared as a witness in the Dutee Chand
vs IAAF CAS case. PYG is the director of the IAAF Health and Science Department
and has no other relevant financial involvement with any organization or entity with
a financial interest with the subject matter or materials discussed in the manuscript.
Competing interests None declared.
Patient consent Obtained.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement The endocrine part of the data can be shared on an
anonymous basis. However, the performance part of the data which is linked to the
endocrine part cannot be shared since it could allow individuals to be identified and
constitutes a breach of confidentiality.
© Article author(s) (or their employer(s) unless otherwise stated in the text of the
article) 2017. All rights reserved. No commercial use is permitted unless otherwise
expressly granted.
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