Sex Differences in Endurance Running

Sports Medicine (2022) 52:1235–1257
https://doi.org/10.1007/s40279-022-01651-w
REVIEW ARTICLE
Sex Differences in Endurance Running

Thibault Besson1 · Robin Macchi2 · Jeremy Rossi1 · Cédric Y. M. Morio3 · Yoko Kunimasa2 · Caroline Nicol2 ·
Fabrice Vercruyssen4 · Guillaume Y. Millet1,5
Accepted: 12 January 2022 / Published online: 5 February 2022

© The Author(s), under exclusive licence to Springer Nature Switzerland AG 2022
Abstract
In recent years, there has been a significant expansion in female participation in endurance (road and trail) running. The often
reported sex differences in maximal oxygen uptake (VO2max) are not the only differences between sexes during prolonged
running. The aim of this narrative review was thus to discuss sex differences in running biomechanics, economy (both in
fatigue and non-fatigue conditions), substrate utilization, muscle tissue characteristics (including ultrastructural muscle
damage), neuromuscular fatigue, thermoregulation and pacing strategies. Although males and females do not differ in terms
of running economy or endurance (i.e. percentage VO2max sustained), sex-specificities exist in running biomechanics (e.g.
females have greater non-sagittal hip and knee joint motion compared to males) that can be partly explained by anatomical
(e.g. wider pelvis, larger femur-tibia angle, shorter lower limb length relative to total height in females) differences. Compared
to males, females also show greater proportional area of type I fibres, are more able to use fatty acids and preserve carbo-
hydrates during prolonged exercise, demonstrate a more even pacing strategy and less fatigue following endurance running
exercise. These differences confer an advantage to females in ultra-endurance performance, but other factors (e.g. lower O2
carrying capacity, greater body fat percentage) counterbalance these potential advantages, making females outperforming
males a rare exception. The present literature review also highlights the lack of sex comparison in studies investigating run-
ning biomechanics in fatigue conditions and during the recovery process.
Key Points
Female participation in endurance running has increased

considerably over the last 20 years. Some physiological
factors are known to explain sex differences in ‘classic’
endurance running performance (e.g. V̇ O2max); this narra-
tive review discusses via a multidisciplinary approach—
physiological, biomechanical and neuromuscular factors
that differentiate sexes in prolonged running exercise.
* Guillaume Y. Millet Although males and females demonstrate differences in

[email protected] running biomechanics, they do not differ in terms of run-
ning economy. A greater proportion of type I fibres and
1
Univ Lyon, UJM-Saint-Etienne, Inter-University greater ability to use fatty acids in females could explain
Laboratory of Human Movement Biology, EA 7424,
42023 Saint‑Étienne, France the lower neuromuscular fatigue of the quadriceps and
2
triceps surae reported after prolonged running races
Institute of Movement Sciences (ISM), National Center
of Scientific Research (CNRS) and Aix Marseille Univ, compared to males, and could confer an advantage to
Marseille, France females over ultra-endurance competitions.
3
Decathlon SportsLab, Movement Sciences Department, Lille, More direct comparisons between males versus females
France in response to fatiguing running exercise are needed.
4
Impact of Physical Activity on Health (IAPS), University
of Toulon, Toulon, France
5
Institut Universitaire de France (IUF), Paris, France
Vol.:(0123456789)
1236 T. Besson et al.
1 Introduction [18] reported a ⁓ 10–13% gap when comparing the fastest

male and female runners ever of the 24-h ultra-marathon.
Running, one of the most popular recreational sports, is How do we explain the variability in sex differences in run-
associated with many health benefits [1–3]. Supported by ning performance between studies regarding events longer
major sports companies, running as a leisure activity has than the marathon? First, reported sex differences depend on
grown rapidly since the 1970s in North America and in how the question is framed, for example, comparing the top
Europe since the beginning of the 1980s [3]. During the last female and male runners or considering all participants. In
decade, female participation in running events has increased the latter case, sex differences seem to even decrease with
considerably. According to a recent survey (https://r unre increasing race distance and no differences were reported in
peat.c om/s tate-o f-r unnin g), covering more than 70,000 road races longer than 315 km (e.g. https://runrepeat.com/state-
races from 5 km to marathons all over the world, female par- of-ultra-running), whereas, based on unpublished data, the
ticipation had reached 50% in 2018. The International Trail sex difference in performance appears constant with increas-
Running Association recently reported an increase in female ing distance when considering the first males and the first
participation in trail running from 18% in 2013 to 26% in females. Second, the percentage of female participation in
2019 (https://itra.run/). In ultra-trail races, the participation these events is much lower than reported for males, being
rate of females is much lower, yet a sixfold increase has also as low as 10% in some events, which may confound the per-
been reported since the 1980s [4]. Despite the increasing formance differences in the very long-distance races [19].
female participation, the vast majority of scientific studies Third, many of the races above the marathon distance are
are still conducted on males. Indeed, based on data collected trail running events. These races are not as standardized as
from three major sport and exercise medicine journals, the road races, and consist of regular changes in terrain, techni-
average ratio of male to female participants per article is ⁓ cal difficulty, elevation gain and exact distance, and it is not
65:35 [5]. Part of this difference has been attributed to sex known if this has a greater impact on males than females, or
differences in willingness to participate in certain types of vice versa. Despite the substantially lower participation rate
research. In other words, a volunteer bias in female partici- of females, ultra-distance in running is one of the rare dis-
pation in running research may exist [6]. ciplines where females are able to outperform men. To cite
With the growth of the number of females engaged in only a few, Corinne Favre, Pamela Reed, Hiroko Okiyama
running events, their performance rapidly improved through and Jasmin Paris finished at first place overall at the ‘CCC’
the 1980s [7] and, from then, researchers started to compare in 2006 (86 km), ‘Badwater’ 2002 and 2003 (217 km), the
male and female running performance from sprint to mara- ‘Deutschland-lauf’ in 2007 (1,204 km), and the 268-mile
thon distances [8, 9]. In the 1990s, it was believed that there Montane Spine race, respectively. Jasmin Paris not only won
would be a reduction [10–12] or even disappearance [8] of the race, but also shattered the previous male record by 12 h.
sex differences in running performance. For instance, using It is, however, likely that these exceptional performances are
a regression analysis between running velocities over several not only due to the great mental and physical capacities of
distances and historical time in males and females, Whipp these runners but also to the fact that the best men were not
and Ward [8] reported in 1992 that females could outrun running in these particular events. In summary, although
males in marathon distance in 1998. However, the difference the question of the evolution of performance across race
in performance between sexes remains around 10–12% for distance according to sex is a complex one, largely due to a
running events from sprint to marathon [13–15]. The issue question of parity in trail and ultra-trail running participa-
of sex differences in performance as a function of distance tion, the sex gap in performance appears relatively constant
is complex. When using the world best times from 100 m with increasing distance when focusing on top level runners.
to 200 km, Coast et al. [14] reported that the difference in Long-distance running performance (up to the marathon)
performance increases with distance, particularly in events depends on the interaction between V̇ O2max, the fraction of
longer than the marathon. It has also been reported that the V̇ O2max sustained (F) on the covered distance that is closely
difference between sexes when comparing the best male and linked to lactate threshold (LT), and running economy (RE)
the best female runners was ~ 17% for the 100-km Lauf Biel (e.g. [20, 21]). Endurance factors such as F or LT do not
in Switzerland [16] and ~ 20% for the 161 km of various seem to be affected by sex (e.g. [22–25]). For instance,
north American ultra-marathons [7]. Additionally, da Fon- Davies and Thompson [22] reported that male and female
seca-Engelhardt et al. [17] observed the same tendency on athletes were able to sustain similar F over the marathon dis-
two of the hardest ultramarathons worldwide, i.e. the ‘Bad- tance (82 and 79%, respectively). The most obvious physi-
water’ in the USA and the ‘Spartathlon’ in Greece, with ological variable to explain running performance difference
performances being ⁓ 20% slower for females than for males is the maximal oxygen uptake (V̇ O2max). When expressed
(based on the top five finishers). On the contrary, Peter et al. in mlO2·min−1·kg−1 (of body mass), V̇ O2max is considered
as the main factors explaining sex differences in endurance
Sex Differences in Running 1237
running performance [20, 26], mainly due to greater per- speeds above 16 km h−1, female runners present shorter
centage of body fat and lower haematocrit levels in females absolute contact time, longer absolute flight time, shorter
[26, 27]. When V̇ O2max in males and females is adjusted to absolute stride length and higher stride frequency than males
fat-free mass, some controversy exists in the literature, with [36]. Because of shorter contact time and longer flight time,
some studies showing no sex differences [28–30] whereas females present a lower duty factor, i.e. percentage of stride
other report a higher V̇ O2max in males [31, 32]. Lower time spent on the ground, indicating that females are not
O2-carrying capacity is definitively one factor explaining a “scaled-down version of the male model” [36]. Interest-
the lower V̇ O2max in females [33]. As sex differences in V̇ ingly, these sex differences seem to disappear at slower
O2max have largely been reviewed elsewhere [26, 31, 32, 34], speeds (10–14 km h−1), with the exception of contact time
the present review focuses on the other factors that differ- as females still present shorter contact time than males
entiate males and females in endurance running. Thus, the when the speed decreases [35]. At high absolute speeds,
aim of the present narrative review was to examine whether females probably have to adjust their biomechanics, in par-
males and females differ in terms of running biomechanics, ticular through adopting a high stride frequency as they are
economy and physiological responses during short (< 1 h) closer than males to their maximal speed. Indeed, once nor-
and prolonged (i.e. several hours of running) running exer- malized to maximal velocity (from 60 to 90% of maximal
cises. This narrative review offers a novel comprehensive velocity), sex differences in contact time and in duty fac-
and multidisciplinary (i.e. psychological, physiological, neu- tor tend to disappear and step frequency is actually lower
romuscular and biomechanical aspects) overview of the sex in females [36]. Sex differences in body proportions might
differences in endurance running. Article databases of the also explain part of the sex differences in spatiotemporal
US National Library of Medicine (PubMed), ScienceDirect parameters. For instance, several studies reported shorter
and SPORTDiscuss were searched using the search general step length in females at various running speeds (from
(Gender or Sex differences) and specific terms (correspond- 7.5 to 24 km h−1), but these differences vanished or even
ing to the studied scientific area of each part). For instance, reversed once adjusted to stature or leg length [35, 36, 38,
article databases focusing on the “Running economy” part 39]. Furthermore, a significant positive association between
were searched as follows: Gender OR Sex differences AND contact time and body height, leg length and body mass has
Running economy OR oxygen demand OR Energy cost of been found [37], but the extent to which morphological dif-
running OR Oxygen cost of running OR oxygen uptake OR ferences contribute to the sex influence on spatiotemporal
metabolic efficiency. Any additional relevant literature was parameters is not yet clear.
obtained from the reference lists of the published papers.
This searching process has been applied for each part of the 2.2 Running Kinematics and Muscle
current review. Electromyographic Activity
The multitude of variables studied and the diversity of the

methods of running kinematics analysis make comparisons
2 Biomechanics of Running
between studies quite challenging. However, a shared obser-
vation across studies is that sex differences mostly existed at
Many studies have been conducted to compare the run-
the hip and knee level [40–51].
ning biomechanics of males and females (Table 1). Several
In recreational runners, females exhibited significantly
parameters such as the studied population, footwear, run-
greater hip adduction and internal rotation during the
ning surface and speed may contribute to the disparity in the
stance phase of running compared to males across a range
results observed between studies. In the absence of fatigue,
of speeds [40, 42, 43, 49] and surface inclinations [42].
differences in spatiotemporal, kinematic and kinetics param-
Sex differences in running kinematics at the hip level have
eters of the running pattern have been extensively studied,
been attributed to the fact that females have a wider pelvis
but primarily in experimental conditions at given absolute
[52] and possibly weaker hip abductor and external rotator
running speeds and for a short period of time rather than in
muscle strength compared to males [49, 53]. Despite mod-
endurance condition. The major sex differences are indicated
erate correlations between hip, pelvis and trunk kinemat-
in blue on Fig. 1.
ics and hip abductors or external rotator strength in both
males or females, hip strength parameters remain a sub-
2.1 Spatiotemporal Parameters stantial portion of the explained variance in running kin-
ematics for both sexes [45]. Females have also been shown
Sex differences in spatiotemporal parameters have been to present greater knee abduction during the stance phase
investigated over a large range of running velocities (from of running compared to males [43, 44, 47–50]. Greater
7.5 to 24 km h−1) [35–38]. For given absolute running knee abduction has been associated with smaller rearfoot
Table 1 Overview of sex differences in running biomechanics
1238
References n Footstrike Footwear Surface Speed (km h-1) and slope Spatiotemporal parameters Kinematics Kinetics
Almonroeder and Benson 14 M Rearfoot Std 14.4 Peak angles: MOMENT

[40] 18 F Knee flex : = Peak moment:
Knee add: = Knee ext moment: F−
Knee IR: = PFJ stress: F−
Hip add: F+ PFJ reaction Force: F−
Hip IR: F+
Bazuelo-Ruiz et al. [41] 28 M Rearfoot Std 11.9 Peak angles: GRF
27 F Knee flex: F+ Impact peak: =
Ankle dorsiflexion: F+ Active peak: F−
Loading rate: F+
Peak braking force: =
Peak propulsive force: F+
Chumanov et al. [42] 17 M NS NS 6.5, 9.7, 13 For all speed and incline:
17 F With 0, 10 and 15% uphill Peak angles:
incline Hip add: F+
Hip IR: F+
Lateral pelvic tilt: =
Amplitudes:
Hip add: F+
Hip rotation and lateral
pelvic tilt: =
Esculier et al. [193] 51 M NS Std Preferred running speed* Stride length: F− Peak angles: MOMENT
36 F M: 11.2 Step width: F− Knee flex: = Peak moment:
F: 10.1 Knee add: = Medial TFJ forces: F−
Knee abd: = External knee flex: F−
External knee add: =
Ferber et al. [43] 20 M Rearfoot NS 13.1 Contact time: = Peak angles: MOMENT
20 F Hip flex: = Peak moment:
Hip add: F+ Hip ext, add and IR: =
Hip IR: F+ Knee ext, abd and IR: =
Knee flex: = WORK
Knee abd: F+ Negative work:
Knee IR: = Hip sagittal plane: =
Hip frontal and trans planes:
F+
Knee sagittal, frontal and
trans planes: =
T. Besson et al.
Table 1 (continued)
Garcia-Pinillos et al. [35] 51 M NS NS 10, 11, 12, 13, 14, 15, 16 Contact time: F− at 10 to 16
46 F km h−1
Flight time: = at 10 to 16
km h−1
Stride length: = at 10 to 13
Sex Differences in Running
km h−1
F− at 14 to 16 km h−1
Stride length (norm.): = at
10 to 14 km h−1
F− at 15 and 16 km.h-1
Step frequency: = at 10 to
13 km h−1
F+ at 14 to 16 km h−1
Gehring et al. [44] 16 M Rearfoot Std 10.8, 14.4, 18 Contact time: F− Peak angles: MOMENT
16 F Hip add: F+ Peak moment:
Knee add: F− Hip add at Impact and Mid-
stance: F+
Knee add at Impact and Mid-
stance: =
WORK
Hip joint impulse: F+
Knee joint impulse: F+
Hannigan et al. [45] 37 M NS Std Self-selected “easy” run Amplitudes:
23 F pace* Hip ext: F+
M: 12.6 Hip add: =
F: 11.9 Hip IR: F+
Anterior pelvic tilt, Con-
tralateral pelvic drop and
Pelvic IR: =
Hennig [194] 17 M NS Std 11.9 Contact time: = GRF
15 F Impact peak: F−
Active peak: =
1239
Table 1 (continued)
1240
Isherwood et al. [60] 20 M Rearfoot Std 11.9 Contact time: F− Peak angles: GRF
20 F Hip flex and add: = Impact peak and active peak:
Hip IR: F+ =
Knee flex, add: = Loading rate: F+
Knee IR: F− Peak braking force and pro-
Ankle eversion: = pulsive force: =
Ankle add: = MOMENT
Peak moment:
In the sagittal plane, for Hip,
Knee and Ankle: F−
Keller et al. [63] 13 M NS Std From 12.6 to maximal speed GRF
10 F Active peak: F− at 18 km h −1
Loading rate: =
Malinzak et al. [46] 11 M NS Perso M: 18.8 Peak angles:
9F F: 18.4 Knee flex : F−
Nelson et al. [36] 24 M NS NS 16.5 to 24.1 Absolute speed:
21 F Stride length, contact time
and duty factor: F−
Step frequency and flight
time: F+
Stride length (normalized):
F+
Relative speed:
Stride length, step frequency
and duty factor: F−
Contact time: =
Flight time: F+
Stride length (normalized):
F−
Nigg et al. [47] 47 M Rearfoot Std 12 Amplitudes:
46 F Pelvic tilt: F+
Hip add: F+
Knee abd: F+
Phinyomark et al. [48] 220 M NS Std Self-selected speed Peak angles:
263 F 8 to 12.1 Hip add: F+
Knee abd and ER: F+
Knee flex: F−
Ankle eversion and dorsi-
flexion: F−
Roche-Seruendo et al. [37] 52 M NS Perso 12 Contact time: =
45 F Flight time: =
Step length: =
Step frequency: =
T. Besson et al.
Table 1 (continued)
Sakaguchi et al. [49] 11 M NS Std 12.6 Contact time: = Peak angles:

11 F Hip add and IR: F+
Knee IR: =
Knee abd: F+
Tibial IR: =
Sex Differences in Running
Rearfoot eversion: F−
Schache et al. [39] 22 M NS Perso 14.4 Stride time: F− Amplitudes:
22 F Stride frequency: F+ Pelvis (antero post tilt,
Stride length: F− obliquity and axial rota-
Stride length (normalized): tion): F+
= Hip flex-ext and IR-ER: =
Contact time: F− Hip Add-abd: F+
Flight time: F−
Sinclair et al. [50] 12 M NS Std 14.4 Contact time: = Only significant differences GRF
12 F are reported Vertical impact peak : =
Peak angles: Loading rate: =
Hip flex: F− Peak braking force and prop
Knee abd and IR: F+ force: =
Ankle eversion: F+ Peak medial force and lateral
force: =
Sinclair and Selfe [67] 15 M Rearfoot Std 14.4 MOMENT
15 F Peak moment:
Knee extensor and abd: F+
PTJ contact force: F+
PTJ load rate: F+
Sinclair and Taylor [55] 20 M NS Std 14.4 Peak angles:
20 F Ankle eversion: F+
Tibial IR: F+
Amplitudes:
Ankle eversion and Tibial
IR: =
1241
Table 1 (continued)
1242
Takabayashi et al. [38] 12 M Rearfoot Barefoot Individual transition speed Relative speed: Only significant differences
12 F from walking to running Step frequency: = are reported
on a treadmill* Step length: F− Peak angles:
M: 7.8 Step length (normalized): = Rearfoot plantarflexion: F+
F: 7.3 Midfoot dorsiflexion and
Abd: F+
Amplitudes:
Rearfoot sagittal plane: F+
Midfoot sagittal plane: F+
Willson et al. [51] 19 M NS Std Between 12.7 and 14 Amplitudes:
19 F Hip add and ER: =
Knee IR: F−
Knee add: =
Angle at mid stance:
Hip add: F+
Hip ER: =
Knee IR and add: =
For kinematic variables, only peak and amplitude joint angles were reported. The results reported are based on the p value according to the significant level set in each studies
M males, F females, overground, treadmill, GRF ground reaction forces, Std standardized footwear (i.e. all participants wore the same pair of shoes), Perso personal shoes, Flex flexion,
Ext extension, Abd abduction, Add adduction, IR internal rotation, ER external rotation, TFJ tibio-femoral joint, PFJ patello-femoral joint, NS not specified, * significant sex difference, F+ supe-
rior in females, F− inferior in females, = no sex difference
T. Besson et al.
Fig. 1 This schematic representation of a female runner is an over- ning performance are boxed in green and orange, respectively. >:
view of the main psychological, physiological, neuromuscular and superior in females, <: inferior in females, =: no sex difference, AT
biomechanical sex differences in endurance running. Parameters that Achilles tendon, O2 oxygen, V̇ O2max maximal oxygen uptake
could give an advantage to males and to females in endurance run-
eversion to compensate for larger hip adduction, as typi- to differences in body size and spatiotemporal parameters
cally seen in females [49], i.e. sex differences in kinemat- [38], as described in Sect. 2.1.
ics at the hip level can explain differences at the knee Given the identified sex differences in joint kinematics,
level. In other words, greater knee abduction in females research has been conducted to identify sex specificities in
could also be a plausible consequence of morphological lower limb muscle activities. Unfortunately, sex compari-
differences and especially the greater Q-angle (i.e. the sons have mostly been studied at given absolute running
acute angle formed by the vector for the combined pull speeds and for very short periods of time (about 10 s).
of the quadriceps femoris muscle and the patellar tendon The neuromuscular strategies adopted may thus differ from
[54]) reported in females [43, 50]. Smaller knee flexion those used in endurance running and racing conditions.
angles have been reported in females both at high running In these experimental running conditions, females had a
velocities (around 18 km h−1 [46]) and at preferred run- higher activation of the gluteus maximus [42, 51] than
ning speed among a very large sample of 483 (263 females males at all speed (from 9.7 to 14 km h−1) and incline (0,
and 220 males) recreational and competitive runners [48]. 10 and 15%) conditions and a larger increase in activity
However, previous investigations showed no sex differ- of the vastus lateralis than males as incline increased [42].
ence in knee sagittal plane motion between females and Females may thus use different neuromuscular strategies
males [43, 50]. These discrepancies could be explained than males in case of increased task demand, i.e. changes
by the imposed speed (13 and 14.4 km h−1) in previous in speed and incline [56]. At similar running speeds of
studies [43, 50], where running speeds varied from 8 to around 18 km h −1, Malinzak et al. [46] demonstrated a
12 km h−1 in Phinyomark et al. [48]. At the ankle level, higher activation of the quadriceps but a lower activation
one study found smaller rearfoot eversion in female run- of the hamstrings in recreational female athletes compared
ners [49], whereas two other studies found greater rearfoot to males, which potentially induced a higher anterior knee
eversion in females [50, 55]. In these studies, as males shear force (i.e. perpendicular force applied by the quadri-
and females ran at the same absolute speed, Takabayashi ceps muscles on the tibia) in female runners. In contrast, a
et al. [38] suggested that differences could be attributed higher medial hamstring pre-activation has been reported
in downhill running at a slow running speed (7.5 km h−1 reaction force and plantar pressure) between Western and
on a 15° declined treadmill) in female runners, which Chinese runners. Thus, the authors emphasized the fact that
may contribute to better stabilization of the knee joint in ethnicity should be considered when comparing running
this situation [57]. Similarly, an increased pre-activation biomechanics in males and females, in particular by run-
of the peroneal muscle group was found in female running shoe manufacturers. Another under-studied topic is the
ners during level running, and this was considered as a influence of females’ breasts on their running biomechanics.
strategy to stabilize and protect the ankle joint [58]. As A recent review [61] pointed out that, although there is some
these studies only considered a small number of muscles, information on breast motion during walking or running,
further analysis of the inter-muscular coordination in run- the previous breast-focused literature had “poor research
ning was limited. However, in a recent study conducted design and inadequate biomechanical methods used to quan-
in 60 females and 60 males [59], the concept of muscle tify complex three-dimensional breast motion”. Brown and
synergies could be used based on the electromyographic Scurr [62] found a slightly negative influence of breast mass
recording of 13 lower limb muscles at running speeds on the marathon finish-time; however, no studies have been
ranging from 7.2 to 13.7 km h−1. This study found sparse conducted so far to determine the influence of the biome-
sex-specific modulations of the relative muscle contribu- chanics of females’ breasts and trunk on their running per-
tion in running. During the stance phase, no sex differ- formance. This specificity of females’ morphology should
ences were found in the contribution of the hip extensors, also be considered in future studies examining sex difference
tensor fasciae latae and plantar flexors, yet females used in running biomechanics.
the vastus medialis less during the weight acceptance. In
this particular phase, the timing of the main peak of activ- 2.3 Running Kinetics and Muscle–Tendon Stiffness
ity was similar but the synergy was narrower in females, Regulation
implying a shorter time-duration of activation in females
than in males. The authors suggested that the neuromotor At given running speeds up to 21.6 km h−1, Keller et al. [63]
strategy showed by females could reduce their fatigabil- did not report any sex difference in the changes in maximal
ity during prolonged locomotion efforts. During the early vertical ground reaction force and loading rate (normalized
swing, females used the rectus femoris less but the gluteus by body weight) with speed. However, sex differences in the
medius more whereas during the late swing, females used normalized force data have been reported in a larger group
the tibialis anterior more compared to males. of recreational runners when running at the same absolute
Overall, despite sex-specificities of the running kinemat- running speed of 11.9 km h−1 [41]. Females exhibited a sig-
ics, the reported differences in muscle activities, such as the nificantly higher loading rate but a lower active peak force
female-specific protective joint strategies, are still contro- than males in both pre-fatigue and fatigue conditions. They
versial and unlikely to reduce the sex-related gap in perfor- also showed higher peak propulsive force (antero-posterior),
mance. Further studies should focus on the sex differences in but only before fatigue. Again, as this study was conducted
muscle synergies under endurance and competitive running at the same absolute running speed, greater peak propul-
conditions. sion force (measured on the antero-posterior axis) observed
Most of these studies investigated running mechanics at in females may have been due to the greater relative effort
the same absolute speed, putting female runners at a greater compared to males.
relative demand on their musculoskeletal system. Indeed, Joint moments and mechanical stress applied to lower
most of the previous literature on kinematics differences limb joints have been compared to better understand poten-
between male and female runners failed to establish a rela- tial sex differences in running-related injuries, rather than
tionship with sex, often because of the lack of control for running performance [64]. Specifically, females appeared
confounding factors such as running speed and participants’ to be at greater prevalence [65] and incidence [66] to sus-
height and body mass. It is therefore necessary to conduct tain patellofemoral joint pain compared to males. Conflict-
more studies with larger sample sizes allowing consideration ing results exist on sex differences in patellofemoral joint
of confounding factors in order to obtain a clearer picture of mechanical stress (PFJS) [40, 67, 68], probably due to dif-
the real influence of sex on running biomechanics. ferent methods used to calculate it. In addition, contradictory
A recent study assessed sex differences in running bio- results exist in sex differences when considering peak knee
mechanics in a population of Chinese males and females extension moment (normalized by body mass) in running
[60]. The authors report similarities with sex differences since no difference [43], greater [67] or lower [40] moment
in Western populations (e.g. increased hip and knee range in females have been reported. In the frontal plane, females
of motion in females), but also differences in biomechan- have been shown to display greater normalized hip and knee
ics (e.g. knee and ankle joint kinematics, vertical ground adduction moment compared to males [44]. Similar to sex
differences in running kinematics, sex differences in kinetics 3 Substrate Utilization and Running
have mainly been attributed to – yet not measured—morpho- Economy
logical sex differences.
Running is a stretch–shortening cycle type activity in 3.1 Substrate Utilization
which higher Achilles tendon (AT) stiffness is expected to
affect the storage of elastic energy during the braking phase, Numerous original studies and review studies have analyzed
followed by its recoil during the subsequent push-off phase. sex differences in substrate utilization during exercise last-
Therefore AT stiffness is expected to affect RE [69–73]. Ten- ing from 60 to 120 min (e.g. [81–86]) at different intensi-
don structural quality and resistance to deformation, tendon ties (from 35 to 75% V̇ O2max). Comparing sexes in substrate
collagen synthesis rate and hypertrophic effect of regular use is methodologically challenging since this parameter is
running exercise on the patellar and AT have been reported influenced by several factors such as training status, men-
to be lower in females than in males [74, 75]. In particular, strual cycle phase, diet, age, etc. Controlling for age, diet
no significant hypertrophic effect on the patellar and AT was and physical activity level (i.e. using V̇ O2max expressed rela-
found in young and regularly trained female runners (at least tive to fat-free mass) would allow avoiding heterogeneity
40 km of running mileage per week for the previous 5 years) in the results when comparing exercise-induced metabolic
as compared to untrained ones, whereas a significant gain responses between males and females [82]. Menstrual cycle
was found in similarly trained males [75]. Both non-athletic phase has been reported to have a small impact on sex differ-
[71] and trained female runners [73] have been reported with ence in substrate utilization [86]. Oral contraceptives have a
lower stiffness and hysteresis of AT than their male counter- slightly greater impact on substrate oxidation [86]. Together
parts. Despite this AT difference, trained female and male this implies that when the variance of these two factors is
runners had a similar RE (see Sect. 2.2), but this remains not controlled, sex differences in substrate utilization may
the only study on such a sex comparison. Other confounding be biased.
factors should be considered, such as AT length and moment When considering only the studies that presented as well
arm, but these factors were studied primarily in elite male controlled with regard to these factors, the overall conclu-
runners [76]. Thus, further work is needed to determine in sion is that females oxidize more lipid and less carbohydrate
females the exact influence of a less stiff AT on their RE and (CHO) and protein than males during prolonged exercise
running performance. (at least until 120 min of exercise duration). Females have
In addition to their effects on tendons, oestrogens are also greater metabolic flexibility since substrate oxidation is
reported to reduce ligament stiffness. Although suggested readily adjusted according to the availability of nutrients. In
as a potential risk factor for anterior cruciate ligament (ACL) this regard, the respiratory exchange ratio (RER) has been
injuries for female participants during sports activity [77], reported to be lower in females during low-intensity, pro-
a causal link is refuted by other studies reporting no asso- longed exercises, supporting a lower reliance on whole-body
ciated decrease in anterior knee stiffness [78]. ACL laxity CHO oxidation (e.g. [86]). For instance, lower RER values
also appears to be affected by the menstrual cycle, as evi- were found for females (0.87) than for males (0.94) dur-
denced by its increase reported in the late follicular phase, ing a 15.5 km treadmill run at 65% VO2max [84]. During an
i.e. when the serum level of estradiol peaks and progesterone incremental treadmill run test to exhaustion performed in a
is low (e.g. [78, 79]). Once again, no associated change was large cohort of 157 males and 143 females, Venables et al.
found in anterior knee stiffness [78]. Within this framework, [87] showed that females displayed higher maximal rates
muscle stiffness being an important component of joint sta- of fat oxidation. In addition, females exercised at a higher
bility, it is noteworthy that Khowailed et al. [80] revealed %VO2max, for which a CHO as dominant fuel is observed.
different muscle activation strategies in running during dif- Although less used than CHO and fat, protein provides
ferent phases of the menstrual cycle. During the follicular approximately 5–8% of total energy in both sexes [29] dur-
phase, when oestrogen levels are low, females placed greater ing prolonged exercise. However, it should be noted that the
reliance on the quadriceps than on the hamstrings. During protein catabolism seems to be lower in females, potentially
ovulation, when oestrogen level and knee laxity are high, due to the higher fatty acid oxidation [29, 30, 84, 88, 89].
increased hamstring pre-activation and co-activation during Theoretically, this may constitute an advantage for females
the braking phase have been observed. Thus, as oestrogen during ultra-endurance exercises (Fig. 1).
levels seem to influence the stretch–shortening cycle and The higher metabolic flexibility observed in females
potentially RE, running performance could possibly vary constitutes a sex-specific difference that depends on sev-
across the menstrual cycle. eral factors (and their interaction), including higher skeletal
muscle insulin sensitivity as well as high levels of circulat-
ing and intramuscular fatty acids required for the oxidation
process (for a review, see [83]). Some authors have reported 3.2 Running Economy
the crucial role of female sex steroid hormones (e.g. oestro-
gens) in the regulation of whole-body insulin sensitivity and RE is known to be the most predictive variable of running
substrate metabolism (e.g. [83, 86, 90]) at rest and during performance within homogeneous groups of trained athletes
endurance exercise. Within the endogenous forms of oes- (i.e. similar VO2max values) (e.g. [21]). RE depends on sev-
trogens, 17-ß-estradiol and associated oestrogen receptors eral physiological, biomechanical, anatomical and neuro-
α are important in the regulation of substrate metabolism in muscular (NM) attributes, supporting the importance of a
skeletal muscle. Higher levels of 17-ß-estradiol are reported holistic approach in RE determination (for reviews, see [103,
to spare glycogen stores and decrease liver glucose output 104]). Oxygen cost in mlO2 kg−1 km−1 is derived from the
and muscle uptake by shifting metabolism toward free fatty mass-specific VO2, dividing the steady-state VO2 the resting
acids at certain (low to moderate) exercise intensities [28, value by the running speed. Given that substrate metabolized
86, 91–93]. This metabolic hormonal action might thus to provide energy may vary with exercise constraints such
contribute to enhanced performance capabilities of females as intensity [105], duration [106], training and sex (e.g. [97,
compared to males for ultra-endurance exercise. Although 107]), it has been proposed to express RE as gross energy
lower RER values have been reported at submaximal run- cost [105] in J.kg−1.m−1 or kcal.kg−1.km−1. An enhanced/
ning intensities (30–60% VO2max) in the luteal phase of the improved RE is associated with a decrease in this value.
menstrual cycle [94, 95], other studies reported no signifi- During submaximal running tests (< 10 min), no sci-
cant differences throughout the menstrual cycle (e.g. [96]). entific consensus exists on the differences in RE between
Part of this discrepancy has been attributed to the complex trained or recreational male and female runners, with con-
balance between oestrogen and progesterone concentra- flicting results strongly related to differences in methodo-
tions and their fluctuations during the menstrual cycle [82]. logical setting [73, 108–114]. VO2max values, training back-
According to D'Eon et al. [92], the ratio of oestrogen/pro- ground, running performance, body fat and quantification of
gesterone would be sufficiently elevated to lead to metabolic RE have probably contributed to the lack of consensus on
changes between the menstrual phases. this issue. In this regard, sex-specific differences have often
Although females and males do not differ in their glyco- been observed when authors expressed RE from oxygen cost
gen stores and capacity for storage of glucose into glycogen or submaximal VO2 (e.g. [23, 108, 112, 115]). Moreover,
[83, 84], females have a higher plasma fatty acid availability the majority of studies investigating sex differences in RE
due to a greater number of intramyocellular lipid (IMCL) have used small sample sizes (e.g. n < 30) and/or compari-
droplets (and not larger droplets) [97]. Moreover, female sons across absolute speeds (rarely with relative intensities).
skeletal muscle is reported to be better able to store lipids In a study comparing RE between trained female and male
and oxidize fatty acids during exercise, which would con- runners, Fletcher et al. [73] did not show any sex differ-
tribute to maintaining a high level of IMCL turnover [83]. ence at similar relative intensities (75, 85 and 95% of the
During exercise, this dependence on lipid substrate to cover speed at LT) when expressed in either energy cost or oxygen
energy expenditure in females might be explained by a cost, or when using of an allometric scaling factor in order
greater relative area of type I muscle fibers (see next section) to take into account sex differences in body mass. These
characterized by higher oxidative capacity, capillary density findings have been confirmed by the same research group
and higher insulin sensitivity [98]. Indeed, Essén et al. [99] with the inclusion of elite and trained male and female run-
previously reported that IMCL content was 2.8-fold higher ners [113]. In addition, using a larger sample size (n = 95),
in type I fibers compared to type II fibers. Despite inconsist- Black et al. [109] recently reported no sex differences in
encies in the literature [82], higher IMCL use during sub- RE in kcal.kg−1.km−1 at similar relative and absolute run-
maximal exercise has been reported in females as compared ning speeds among females and males of equivalent stand-
to males, irrespective of training status [100–102]. ard. Considering these findings, no clear difference in RE
The majority of studies focusing on sex differences in responses exists between male and female runners even
substrate oxidation have been conducted on a cycle ergom- when applying different RE units.
eter rather than in running (see Table 1 in Tarnopolsky [86]). In most of the articles focusing on RE responses in
The differences in substrate oxidation observed between females, a qualitative analysis of menstrual cycle is lacking,
sexes highlights the importance of quantifying the cycle and this might constitute an important methodological bias
menstrual phase, oral contraception, training level and diet in RE evaluation. During endurance exercises, females gen-
in females. erally use less CHO and have lower RER values [107, 116,
117]. These metabolic changes may depend on the phases of
the menstrual cycle as well as short-term oral contraceptives
and, in turn, affect the RE response in females. RE may also
be naturally influenced by the specificity of each phase (e.g.
early, late follicular and mid-luteal phases), and, therefore, relative intensity [129]. However, sex differences in fatiga-
circulating hormone levels (i.e. oestrogen and progesterone). bility are less clear following dynamic tasks as females have
For instance, investigating three different times during the been reported to be either less than or as fatigable as males
menstrual cycle in females taking oral contraceptives (i.e. (see Fig. 1 in Hunter [128]). Among these studies, a lower
constant doses of oestrogen and progestogen for 21 days), fatigue index (i.e. smaller decline in each isokinetic variable)
Giacomoni and Falgairette [118] reported an improved RE was found in females compared to males after a series of 30
at low intensities (7–9 km h−1) only during the late period maximal dynamic knee extension [130]. This finding could
of oral contraceptive use (i.e. days 19–21). In this regard, be of importance given that in a recent paper, Ehrstrom
Dokumacı and Hazır [119] recently reported an improved et al. [131] showed local endurance of the knee extensors
RE (i.e. in terms of energy or oxygen cost) in the luteal was a good predictor of performance on a short trail run-
phase compared to the follicular phase in female competitive ning exercise (27 km with 1400 m of positive elevation) in
athletes with no oral contraceptives. Conversely, two stud- trained male runners. On a fatiguing cycling task, Ansdell
ies have indicated that the mid-luteal phase (high levels of et al. [132] compared males and females after normalizing
oestrogen and progesterone) was associated with worse RE exercise intensity to critical intensity, and found that females
responses compared to early and late follicular phases [120, displayed a greater relative critical intensity compared to
121]. More work is needed to better understand the effects males, yet contrary to their hypothesis, females had a longer
of the menstrual phase in RE, but these findings suggest that time to task failure than males above critical power [132].
those effects must be considered. Females also exhibited lower strength loss and peripheral
fatigue at exhaustion. However, sex differences in fatigabil-
ity following prolonged running exercise is not well docu-
4 Fatigue Resistance mented. After 2 h of laboratory treadmill running at a speed
corresponding to their first ventilatory threshold, Glace et al.
NM function, RE and biomechanics are often measured in [133] reported that knee extensor/flexor strength measured
a non-fatigued state. However, our group and others have in isokinetic conditions (60° s−1) decreased in males only,
consistently shown in the last two decades using labora- while decreased hip strength was independent of sex.
tory or field experiments (e.g. marathon, trail/ultra-trails), Under real endurance racing conditions on short distances
that fatiguing endurance running exercise drastically affects (< 40 km), Boccia et al. [134] reported no sex difference in
maximal strength, RE and running patterns. Some sex differ- the decrease in knee extension force after a half-marathon
ences exist at these levels and are discussed below. performed by moderately trained runners under real rac-
ing conditions. These authors also found that the origin of
4.1 Neuromuscular Fatigue fatigue was independent of sex. After a graded 20-km race
(± 350 m) in recreational males and female runners, sex
NM fatigue has traditionally been defined as an exercise- differences were found in both the acute and delayed (up
induced reduction of maximal strength or power [122]. The to 4 days) recovery period [135]. Females showed smaller
causes can be peripheral (i.e., within the muscle) and/or functional decrements within the first 2 h and earlier full
central (i.e., proximal to the neuromuscular junction), and recovery than males. Indeed, only males showed decreases
NM fatigue etiology in running depends on many factors in maximal isometric knee extension force and maximal
such as exercise duration, intensity, altitude, and positive power in drop jump up to 4 days after the race. However,
and negative slope [123]. Central fatigue reflects an inability regarding the relative decrements (normalized by pre-val-
to voluntarily activate muscles, and has been described as ues), no sex difference was found, so that the lower fatigue
a protective mechanism acting to limit peripheral perturba- effects observed in females may be partly attributed to their
tions [124, 125]. In contrast to central fatigue, which occurs lower initial strength levels.
predominantly after very long and low intensity exercise, Over a much longer distance, Temesi et al. [136] assessed
peripheral fatigue is greater at higher intensities, shorter NM fatigue in experienced male and female ultra-endurance
duration exercise [126] including downhill running [127], trail runners matched by relative level of performance (i.e.
and could impair (1) action potential transmission along the same average percentage of performance as the winner of
sarcolemma, (2) excitation–contraction coupling, and (3) each sex) after a 110-km ultra-trail-running. In the ultra-trail
actin–myosin interaction [123]. study, female runners had (1) less peripheral fatigue in the
Sex differences in fatigability have been mostly inves- plantar flexors and (2) a lower decrease in maximal force in
tigated in laboratory conditions (for a review, see [128]). the knee extensors when compared to their male counter-
While females are less strong and less powerful than males, parts. The authors suggested that females were more fatigue
they were found to be less fatigable than males for sustained resistant following ultra-endurance running effort, which
or intermittent isometric contractions performed at a similar could partly explain why they manage to outperform males
in races of this format. A recent study from our group inves- females than in males [143]. Overall, these results explain
tigated sex differences in NM fatigue in trail running races why females show attenuated impairments in contractile
of various distances (from 40 to 170 km) [137]. Male and function compared to males [144], and are able to recover
female participants were matched by a relative level of per- at a faster rate from repeated fatiguing exercise [145].
formance using the same criteria as in Temesi et al. [136]. In addition to directly explaining the sex-related differ-
Greater knee extensor strength loss was found in males com- ence in fatigability at the muscle level, the attenuated meta-
pared to females and, contrary to our hypothesis, this sex dif- bolic disturbance related to the greater proportional area of
ference was independent of the race distance. Interestingly, type I may also lead to attenuated afferent feedback (groups
we observed greater peripheral fatigue on plantar flexor mus- III and IV). This may induce less inhibitory inputs to the
cles in males compared to females in races under 60 km motoneuronal pool, and thereby less central fatigue. Indeed,
but no sex difference in races above 100 km. This result greater levels of fatigue observed in males have been asso-
could be partly due to sex differences in the “competition ciated with greater central deficits, but these studies were
intentions” of the participants: with races < 60 km females using maximal efforts and it is not known if this is also true
reported that they performed the race in a more “pleasure for submaximal contractions [128].
mode” whereas males were more competitively oriented. In conclusion, as generally reported following single-joint
This possibility should be considered when concluding on fatiguing tasks, females appear less fatigued following trail
fatigability. In other words, less fatigue post-exercise does and ultra-trail races. A greater proportion of type I muscle
not necessarily mean a better resistance to fatigue, at least fibres and higher muscle capillarization (i.e. less muscle
in non-elite runners. de-oxygenation) in females compared to males are possible
explanations for lower fatigability in females, and could be
4.2 Muscle Tissue Characteristics of advantage for females over ultra-endurance running per-
formance (Fig. 1). Although the results obtained with the
Among the underlying mechanisms, males and females scale on “the competitive intention” of the runners must be
have distinct muscle properties. An obvious difference that treated with caution (i.e. the scale has not undergone a vali-
mainly explains the difference in maximal strength is muscle dation process), the fact that females (non-elite) have been
mass, due to larger diameter muscle fibers in males rather showed to be less competition oriented than males could also
than the number of fibers [138], this larger size being due to at least partly explain sex differences in fatigability follow-
sex-related differences in human skeletal muscle gene (e.g. ing such trail running races.
GRB10 and ACVR2B) expression [139]. This factor has
been presented as partly explaining the sex differences in 4.3 Muscle Fiber Damage, Inflammation
fatigability in most of the studies using single-joint exercise and Delayed‑Onset Muscle Soreness
since stronger muscles tend to be less perfused because of
higher blood flow occlusion resulting from higher intramus- Endurance running races induce metabolic stress and include
cular pressure. In order to overcome the occlusion effect, thousands of ground impacts and subsequent eccentric mus-
Ansdell et al. [140] compared NM fatigue in males and cle actions that are likely to induce very focal and limited
females across submaximal and short duration intermittent ultrastructural muscle damage. In the most severe case, less
isometric contractions (i.e. they used a 3-s contraction dura- than 10% of the sarcomeres appeared damaged [146], which
tion with a duty cycle allowing to negate the influence of clearly differ from those induced by pure eccentric mus-
occlusion). After normalizing the intermittent exercise inten- cle actions [147]. The subsequent ultrastructural recovery
sity by maximal force, lower force reduction and longer time process involves oedema, remodelling/inflammation, and
to task failure was still found in females compared to males. delayed-onset muscle soreness (DOMS) [148, 149]. The
However, this is not the only factor explaining the fatiga- ultrastructural damage is expected to be less or even absent
bility. Despite no sex differences in peak force, in power in trained runners [150, 151]. Importantly, (1) neither the
and shortening velocity of single fibers when normalized to degree nor the timing of exercise-induced muscle damage
muscle cell size (e.g. [141]), there is considerable evidence (EIMD) per se correlates well with the DOMS sensation
that females have a greater proportional area of type I fibers [152, 153], and (2) the timing of DOMS disappearance
in several key muscles for locomotion and daily function usually occurs prior to complete structural and functional
[128]. Females also have greater capillarization [100] and recoveries [149]. The only study that has directly addressed
lower glycolytic enzyme activity [142] when compared to in humans (via muscle biopsies) the effect of sex on ultras-
males. Related to these important features, a better vasodila- tructural muscle damage and/or inflammation up to 6 days
tory response to exercise has been reported for females. For after an eccentric exercise reported no sex difference in
example, vasodilatory responses of the femoral artery during muscle damage, yet an attenuated inflammatory response
dynamic knee extensor exercise were found to be greater in in females as compared to males [154]. In our own study
of the sex differences after a graded 20-km running race sex. Compared with males, females showed earlier restora-
[135], DOMS were recorded for the major lower limb mus- tion of the pre-run CK activity level (at 48 vs. 72 h) but
cles. Independently of sex, DOMS was reported at day 2 for longer-lasting DOMS (up to 72 vs. 48 h).
the quadriceps muscle group, but only in female runners for In conclusion, despite the lack of direct assessment of
the hamstrings, suggesting that possible sex differences are sex differences in the running-induced ultrastructural mus-
muscle-group dependent. At day 4, despite the disappear- cle damage, the reported time-evolution of indirect markers
ance of DOMS, males still had functional deficits in MVC of muscle inflammation (such as plasmatic CK activity and
and drop jump test. Female runners also had functional defi- DOMS) during the recovery period suggest less damage or
cits in DJ, but no longer reported DOMS and had already at least earlier structural recovery in female runners.
recovered in MVC.
Sorichter et al. [155] have summarized the literature on 4.4 Change in Running Biomechanics and Economy
the identification, usefulness and limits of indirect mark- with Fatigue
ers of ultrastructural muscle damage widely used in males
and females. Aside from DOMS, the most reported indi- An altered RE has been repeatedly reported after prolonged
rect indicators include myoglobin (Mb) and lactate dehy- road and trail exercises in male runners (e.g. [166–170]),
drogenase (LDH) plasma levels as well as serum creatine but only a few studies have been conducted in trained or
kinase (CK) activity [156]. According to Goodman et al. recreational female runners [133]. After a 2-h treadmill
[157], the increased serum levels of CK and Mb after an run session at a given relative intensity, Glace et al. [133]
endurance run might result from free radical-induced cell showed an increase in oxygen cost in male but not in female
membrane damage and/or transiently increased permeabil- distance runners. In male athletes, the exacerbated increase
ity rather than from mechanical ultrastructural damage. Part in oxygen cost was related to their greater muscle fatigue
of these perturbations are likely to decrease with training characterized by the larger strength decrement of the knee
(e.g. Margaritis et al. [158]). However, owing to high inter- extensors (see Sect. 4.1). To the best of our knowledge, only
individual variability none of these indirect markers accu- two other studies have examined sex differences with regard
rately reflect the magnitude of muscle damage. This appears to RE change with fatigue, albeit with shorter running bouts.
clearly in the extremely large range of CK concentration Similar changes in RE were found for males and females fol-
values (1500–264,300 IU L−1) reported among finishers of lowing (1) a 1-h run at marathon pace [171] and (2) a 5-km
ultra-trail running events, but no differences between sexes run at 80–85% of V̇ O2max [172]. These three experiments
have been reported [136, 159]. These methodological limits were conducted on a treadmill in laboratory conditions. A
apply to the serum CK [160], which is still widely used as a recent study from our group reported an increase in RE fol-
marker of the sex difference in the exercise-induced muscle lowing trail running races from 40 to 170 km; however, no
damage [161]. significant sex difference were observed in the changes in
As reviewed by Enns and Tiidus [162], sex and oestrogen RE measured on both flat (+ 3.1 vs. + 8.7% in females vs.
are reported as potentially attenuating indices of exercise- males, respectively) and uphill (+ 1.4 vs. + 6.9% in females
induced skeletal muscle damage by influencing the inflam- vs. males, respectively) conditions [137]. Further investiga-
mation and repair processes. Although the underlying mech- tions are warranted to further examine sex differences in RE
anisms are not yet fully elucidated in humans, oestrogens in the ecological context using models of prolonged road and
are thought to exert their protective effects by: (1) acting as trail run exercises.
an antioxidant, thus limiting oxidative damage; (2) acting While many studies have investigated sex differences
as a membrane stabilizer by intercalating within membrane in running biomechanics under acute conditions (see
phospholipids; and (3) binding to oestrogen receptors, thus Sect. 2.2), the literature is very limited on sex differences in
governing downstream muscle repair processes, including the alteration of running biomechanics following a fatigu-
the activation and proliferation of muscle satellite cells. ing task. Bazuelo-Ruiz et al. [41] reported a reduced ankle
Supporting the oestrogen protective effect in runners, lower dorsiflexion angle at touchdown in females only after a
resting serum CK values are reported in female compared succession of three consecutive tasks at high intensities
to male athletes [161] and in eumenorrheic compared to (shuttle-run, running up and downstairs, and jumps), this
amenorrhoeic female athletes [163], whereas no sex effect parameter being associated with a decrease in loading rate
was found in the peak values after a marathon [164] in mod- and vertical impact peak force. These authors suggested a
erately trained runners. Illustrating the limitations of using potential adaptative strategy to optimize shock attenuation
indirect markers of muscle damage and inflammation, the and thus prevent running injuries. However, these results
downhill running study of Oosthuyse and Bosch [165] found should be interpreted with caution since the fatiguing pro-
that DOMS peaked after 24 h in males and females, but the tocol was quite unusual. After a 110-km trail running race,
time to disappearance of CK and DOMS then differed by Giandolini et al. [173] reported that males adopted a flatter
pattern (i.e. a decreased foot/ground angle) and increased Medicine does not provide specific guidelines or strate-
step frequency contrary to females, who landed with a more gies for the female athlete. However, it has been argued
dorsiflexed ankle accentuating their rear-foot strike pat- that a sex difference in thermoregulation may depend on
tern. Changes in males were considered as a compensatory the percentage of humidity and exercise intensity [178].
adjustment to possibly greater decreased muscle capacity Indeed, Shapiro et al. [179] found that core temperature
compared to females [173]. Although female adaptations to increased less in females than in males for hot/humid envi-
fatigue observed in the studies of Bazuelo-Ruiz et al. [41] ronments (due to larger surface area to body mass ratio and
and Giandolini et al. [173] seem to go in opposite directions more efficient sweating suppression), whereas the opposite
(concerning the alteration of ankle angle with fatigue), the was true in hot/dry climates (due to lower overall sweat-
fatiguing tasks differed considerably between the two stud- ing capacity in females despite a higher density of sweat
ies and could explain the discrepancies in the results. As glands). Although thermoregulatory responses vary over
also suggested by the sex-dependent DOMS sensations per the cycle, Notley et al. [175] suggested that there was no
muscle after a graded running race [135] (see Sect. 4.3), additional thermoregulatory concern for female athletes
it appears that males and females adjust their running pat- if an oral contraceptive was used or at any phase of the
tern differently, which suggests sex-relative biomechanical menstrual cycle phase. It is not known if potential sex dif-
adaptations. Under laboratory conditions, no sex differences ferences exist in the time-course of acclimation.
were reported in running biomechanical parameters previ- It has also been suggested that performance was less
ously associated with the aetiology or exacerbation of patel- affected by warm weather in females than in males during
lofemoral joint pain after a run on a treadmill at 3.5 m s−1 a 161-km ultra-marathon [180], although no sex difference
until reaching a RPE of 17 out of 20 [68]. These studies was found in marathons. The opposite may actually be true
compared males and females following different modalities since performance is more negatively affected for slower
of exercise and under different methodological approaches. populations of runners on that distance [181]. Importantly,
Further studies are needed to better investigate potential sex because of their smaller body size, lower heat generation,
differences in biomechanical alterations following prolonged and less sweat loss (i.e. better efficiency in sweating that
running exercise. may decrease the total amount of so-called “wasted sweat-
ing” in a humid environment), the water intake required
to maintain hydration and thermal balance is attenuated in
5 Other Factors Influencing Running females. Since hydration guidelines have been developed
Performance using data mainly collected in studies with males, they
should be interpreted with caution when applied to females
5.1 Thermoregulation [176]. This is particularly important in ultra-endurance
exercises since over-hydration may induce gastro-intestinal
Whether sex differences exist in thermoregulation was distress.
uncertain until recently [174], i.e. it was not known if
thermoregulatory differences between males and females 5.2 Pacing
were due to sex per se or to other differences such as body
size or aerobic fitness. Indeed, a correlation between V̇ Several studies, including a large study with data from 14
O2max (lower in females) and the ability to maintain lower US marathons encompassing ~ 92,000 performances [182],
core temperatures during exercise in the heat has been have shown that females tend to have a more even pacing
found, potentially related to skin blood flow. Females strategy in marathon races [183]. A similar finding has been
may generate less heat in high ambient temperatures found in half-marathons [184], 10-km races (at least in fast
because of lower muscle mass and smaller body size but runners [185]) or even shorter races such as 5-km cross-
may be disadvantaged as their lower V̇ O2max can result in country race when males and females have similar relative
faster increases in body temperature. Notley et al. [175] performance [186]. It has been suggested that sex difference
concluded that, contrary to popular belief, sex does not in pacing partly reflects a sex difference in decision making
significantly impact exercise thermoregulation [175]. A [185] rather than greater susceptibility to glycogen depletion
review by Yanovich et al. [176] confirmed the lack of sex [186]. Interestingly, the sex differences in pacing were also
differences and concluded that females were not at greater found to be true for top runners. A study collected finishing
risk of heat illness, provided the usual risk-management and split times in 673 males and 549 females across nine
techniques are in place (pacing, clothing, hydration, accli- Olympic and World Championship marathons and found that
mation). It has been reported that female athletes used females slowed less and were more likely to run a negative
more heat illness prevention strategies than male athletes split than males [187]. In addition, in a study from Trubee
[177]. It is noteworthy that the American College of Sports et al. [188], the more even pacing strategy in females was
found to be an even greater advantage during warm weather biomechanics and economy. Sex differences in a fatigued
conditions. condition are a clearly under-investigated research area and
The number of studies on sex differences in pacing strat- further direct physiological and biomechanical comparisons
egy related to ultramarathon is low and there is no clear between males and females following prolonged running are
consistency among the results. Indeed, females showed warranted. Considering that females used different pacing
lower relative starting speeds and higher finishing speeds (i.e. more even) strategies than males, other psychological
than males on a 100-km race [189], yet no sex differences and/or sociological parameters that could affect performance
in pacing strategy [190] or even better preservation of mean or help to understand sex differences in running participation
speed throughout the race have been found in males [191] also need to be explored.
on 24-h races. It has been advised that, given the possibility
of a “herd principle”, comparison of competition dynamics Acknowledgements The authors sincerely thank Callum Brownstein
for English editing.
between sexes must be further explored in ultra-marathon.
The level of performance and age may be confounding
factors in pacing strategies although, again, the results are
Declarations
not that clear. As stated in the present section, sex differences Author contributions TB, RM, CN, FV and GYM drafted the manu-
in pacing on 10-k races were mostly found in good runners script; JR, CM and YK provided additional comments and contribu-
[185], whereas they occurred across all finishing time groups tions; all authors approved the final version.
in the marathon [182]. Deaner et al. [182] also showed that
Funding No sources of funding were used to assist in the preparation
sex differences in pacing occurred across age groups. On of this article.
the contrary, it has been found that females showed no dif-
ferences in pace variability across ages, whereas younger Conflict of interest Thibault Besson, Robin Macchi, Jérémy Rossi,
(< 30 years) and older (> 60 years) males showed a greater Cédric Morio, Yoko Kunimasa, Caroline Nicol, Fabrice Vercruyssen
variability in pacing than other age groups [192]. and Guillaume Millet declare that they have no conflicts of interest
relevant to the content of this review.
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Sports Medicine (2022) 52:1235–1257

Sex Differences in Endurance Running

Accepted: 12 January 2022 / Published online: 5 February 2022

Female participation in endurance running has increased

* Guillaume Y. Millet Although males and females demonstrate differences in

1 Introduction [18] reported a ⁓ 10–13% gap when comparing the fastest

The multitude of variables studied and the diversity of the

Almonroeder and Benson 14 M Rearfoot Std 14.4 Peak angles: MOMENT

Sakaguchi et al. [49] 11 M NS Std 12.6 Contact time: = Peak angles:

Through this narrative review, we have identified a num- References

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