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Sex differences in semitendinosus muscle fiber‐type composition

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Sex differences in muscle fiber-type composition have been documented in several muscle groups while the hamstring muscle fiber-type composition has been poorly characterized. This study aimed to compare the semitendinosus muscle composition between men and women. Biopsy samples were obtained from the semitendinosus muscle of twelve men and twelve women during an anterior cruciate ligament reconstruction. SDH and ATPase activities as well as the size and the proportion of muscle fibers expressing myosin heavy chain (MyHC) isoforms were used to compare muscle composition between men and women. The proportion of SDH-positive muscle fibers was significantly lower (37.4 ± 11.2% vs. 49.3 ± 10.6%, p<0.05) and the percentage of fast muscle fibers (i.e., based on ATPase activity) was significantly higher (65.8 ± 10.1% vs. 54.8 ± 8.3%, p<0.05) in men versus women. Likewise, men muscles exhibited a lower percentage of the area occupied by MyHC-I labeling (35.6 ± 10.1% vs. 48.7 ± 8.9%; p < 0.05) and a higher percentage of the area occupied by MyHC-IIA (38.3 ± 6.7% vs. 32.5 ± 6.5%; p < 0.05) and MyHC-IIX labeling (26.1 ± 9.6% vs. 18.8 ± 8.5%; p = 0.06) as compared with women muscles. The cross-sectional area of MyHC-I, MyHC-IIA and MyHC-IIX muscle fibers was 31%, 43% and 50% larger in men as compared with women, respectively. We identified sex differences in semitendinosus muscle composition as illustrated by a faster phenotype and larger muscle size in men as compared with women. This sexual dimorphism might have functional consequences.
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Scand J Med Sci Sports. 2022;00:1–8.
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1
wileyonlinelibrary.com/journal/sms
Received: 8 September 2021
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Revised: 16 December 2021
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Accepted: 31 December 2021
DOI: 10.1111/sms.14127
ORIGINAL ARTICLE
Sex differences in semitendinosus muscle fiber- type
composition
GaspardFournier1
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ClaraBernard2
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MaximeCievet- Bonfils1
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RaymondKenney3
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MaximePingon1
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ElliotSappey- Marinier1
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BénédicteChazaud2
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JulienGondin2
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ElvireServien1,4
© 2022 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Gaspard Fournier, Clara Bernard, Julien Gondin, and Elvire Servien authors are equally contributed to this work.
1Department of Orthopedic Surgery
and Sport Medicine, FIFA medical
center of excellence, Hôpital de la
Croix- Rousse, University Lyon 1, Lyon,
France
2Institut NeuroMyoGène, CNRS UMR
5310, INSERM U1217, Université
Claude Bernard Lyon 1, Univ Lyon,
Lyon, France
3Department of Orthopaedics,
University of Rochester Medical Center,
Rochester, New York, USA
4EA 7424 - Inter- University Laboratory
of Human Movement Science, Univ
Lyon, Université Claude Bernard Lyon
1, Villeurbanne, France
Correspondence
Julien Gondin, Institut NeuroMyoGène
(INMG), CNRS 5310 – INSERM U1217
- UCBL1, Faculté de Médecine et de
Pharmacie, 8 Avenue Rockefeller, 69008
Lyon, France.
Email: julien.gondin@univ-lyon1.fr
Funding information
Antonin Poncet prize
Sex differences in muscle fiber- type composition have been documented in sev-
eral muscle groups while the hamstring muscle fiber- type composition has been
poorly characterized. This study aimed to compare the semitendinosus muscle
composition between men and women. Biopsy samples were obtained from the
semitendinosus muscle of twelve men and twelve women during an anterior cru-
ciate ligament reconstruction. SDH and ATPase activities as well as the size and
the proportion of muscle fibers expressing myosin heavy chain (MyHC) isoforms
were used to compare muscle composition between men and women. The pro-
portion of SDH- positive muscle fibers was significantly lower (37.4±11.2% vs.
49.3±10.6%, p < 0.05), and the percentage of fast muscle fibers (i.e., based on
ATPase activity) was significantly higher (65.8±10.1% vs. 54.8±8.3%, p<0.05)
in men versus women. Likewise, men muscles exhibited a lower percentage of
the area that was occupied by MyHC- I labeling (35.6±10.1% vs. 48.7± 8.9%;
p<0.05) and a higher percentage of the area that was occupied by MyHC- IIA
(38.3± 6.7% vs. 32.5±6.5%; p<0.05) and MyHC- IIX labeling (26.1±9.6% vs.
18.8± 8.5%; p=0.06) as compared with women muscles. The cross- sectional
area of MyHC- I, MyHC- IIA, and MyHC- IIX muscle fibers was 31%, 43%, and 50%
larger in men as compared with women, respectively. We identified sex differ-
ences in semitendinosus muscle composition as illustrated by a faster phenotype
and larger muscle size in men as compared with women. This sexual dimorphism
might have functional consequences.
KEYWORDS
hamstrings, muscle biopsies, muscle composition, myosin heavy chain
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FOURNIER et al.
1
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INTRODUCTION
Skeletal muscle is the largest organ in the human body,
accounting for up to 40% of body weight, and is a very
heterogeneous tissue. One of the main characteristics of
skeletal muscle relies on its composition of different types
of muscle fibers that can be activated to perform various
functional tasks. Human skeletal muscle is composed of
three major fiber types that can be identified according to
either their ATPase activity or their expression of the my-
osin heavy chain (MyHC) isoforms.1 On that basis, mus-
cle fibers are usually classified as slow type 1 (expressing
MyHC- I), fast intermediate type 2A (expressing MyHC-
IIA), and fast type 2X (expressing MyHC- IIX). Each fiber
type possesses specific contractile responses (i.e., slow vs.
fast) and metabolic activities (i.e., aerobic vs. anaerobic)
that are required to perform a broad range of functional
activities ranging from short- duration and high- force
level contractions (e.g., explosive movements) to long-
lasting and low- intensity contractions (e.g., endurance
exercises).
Sex differences in muscle fiber- type composition have
been largely documented in humans.2 Several studies have
demonstrated that men possess a lower proportion of type
1 and a higher proportion of type 2A as compared with
women.3- 10 However, these observations mainly arose
from analysis of quadriceps muscle biopsy samples4,7 (i.e.,
vastus lateralis), while only a few investigations focused on
other muscle groups such as biceps brachii,10 lateral gas-
trocnemius,11 or tibialis anterior12 muscles. Surprisingly,
fiber- type composition of hamstring muscles (i.e., semi-
tendinosus, semimembranosus, and biceps femoris mus-
cles), which are the main knee flexors and are involved
in various explosive tasks such as sprinting and running,
have been poorly characterized. So far, hamstring mus-
cle fiber- type composition has been mainly examined in
men13- 15 and has never been directly compared between
men and women.16,17 The investigation of potential sex
differences in hamstring muscle fiber- type composition is
particularly relevant if we consider the higher incidence
of hamstring muscle strain injuries (HSI) in men vs.
women,18,19 the higher susceptibility to exercise- induced
muscle injury in the fast vs. slow muscle fibers,20,21 as well
as the higher fatigability observed in men as compared
with women.22
In the present study, we analyzed biopsy samples from
the semitendinosus obtained in men and women during an
anterior cruciate ligament (ACL) reconstruction. We com-
bined histochemical analyses with MyHC immunostain-
ing in order to characterize oxidative and ATPase activities
together with the size and the proportion of muscle fibers
expressing MyHC- I, MyHC- IIA, and MyHC- IIX isoforms.
2
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MATERIALS AND METHODS
2.1
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Population
Study enrollment began in March 2019. Inclusion crite-
ria were as follows: patients scheduled for an ACL recon-
struction using semitendinosus and gracilis autograft and
aged between 18 and 50years old. Exclusion criteria in-
cluded history of prior hamstring injuries, neuromuscular
diseases, or chronic use of corticosteroids. Demographics
information is summarized in Table1. Sport played and
activity level were recorded using Tegner Activity Scale23
before ACL injury (Table 1). The Tegner Activity Scale
aims at providing a standardized method of grading work
and sporting activities. The score varies from 0 to 10. A
score of 0 represents sick leave or disability pension be-
cause of knee problems, whereas a score of 10 corresponds
to participation in national and international elite com-
petitive sports. A score of 5– 6 corresponds to participa-
tion in recreational sports. No professional athletes were
included. Overall, twelve men and twelve women were
included. The delay between the ACL injury and surgery
as well as the Tegner activity score was not significantly
different between the two groups (Table1). Gender and
age- appropriate consent were obtained under a protocol
approved by Hospital's ethics committee (N°19– 52) and
by data protection committee (19– 083) of Lyon.
2.2
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Muscle samples
Muscle samples were obtained from semitendinosus of pa-
tients undergoing ACL reconstruction using a close- ended
tendon stripper (Figure1). Semitendinosus muscle biop-
sies were frozen in isopentane placed in liquid- nitrogen
and kept at −80°C until use. Cryosections (10µm) were
prepared for staining and immunohistochemical analyses
(all compounds from Sigma- Aldrich unless indicated).
TABLE  Patient's characteristics
Men
(n=12)
Women
(n=12) p value
Age (years) 34±8 35±8 p=0.9
BMI (kg/m²) 25.5±3.4 24.8±5.3 p=0.7
Tegner activity score 5.9±0.7 5.3±0.6 p=0.08
Delay between ACL
injury and surgery
(days)
73.4±9.6 79.6±13.1 p=0.4
Note: Data are presented as mean ±SD. ACL: anterior cruciate ligament;
BMI: Body mass index.
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FOURNIER et al.
2.3
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Succinate dehydrogenase
(SDH) staining
Succinate dehydrogenase activity was revealed histochemi-
cally as a marker of muscle fiber oxidative capacity. Briefly,
cryosections were dried at room temperature for 30min and
further incubated in a solution composed of nitroblue tetra-
zolium 1.5mM, EDTA 5mM, succinic acid 48mM, sodium
azide 0.75mM, methyl- phenylmethlyl sulfate 30mM, and
phosphate buffered to pH 7.6 for 45min at 37°C. Cryosections
were then washed in deionized water for 5min, dehydrated
in ethanol 50% for 2min, and mounted for viewing (Eukitt).
2.4
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ATPase staining
ATPase activity was revealed histochemically as a marker
of muscle fiber type. Cryosections were incubated in a solu-
tion composed of barbital acetate 0.1M and HCl 0.1M at pH
4.5– 4.6 for 5min at room temperature. Cryosections were
then washed in deionized water and incubated in a solution
with ATP, sodium barbital, and calcium chloride for 25min
at room temperature. Then, they were washed 3 times with
calcium chloride 1%, were incubated in cobalt chloride 2% for
10min, washed 5 times with sodium barbital 0.1M, incubated
with ammonium sulfide 2% for 30s, and finally rinsed with
tap water. Cryosections were then dehydrated in ascending
alcohols baths (50%, 70%, 80%, 95%, and 100%), cleared with
xylene, and mounted with Eukitt mounting medium.
2.5
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MyHC immunostaining
Cryosections were incubated with primary antibodies
overnight at 4°C, washed with PBS, and further incubated
with secondary antibody for 1 h at 37°C. The following
antibodies were used: anti- MyHC- I (mouse IgG2b, BA-
D5, 1/100), anti- MyHC- IIA (mouse IgG1, SC- 71, 1/100)
and anti- MyHC- IIX (mouse IgM, 6H1, 1/100) (all from
Developmental Studies Hybridoma Bank), and anti-
laminin (rabbit, L9393, 1/200, Sigma- Aldrich). Secondary
antibodies were Alexa Fluor 405- conjugated donkey
anti- mouse IgG2b (1/200), Alexa Fluor 488- conjugated
anti- mouse IgG1 (1/200), Alexa Fluor 546- conjugated
donkey anti- mouse IgM (1/200), and Cy- 5- conjugated
donkey anti- rabbit antibodies (1/200) (all from Jackson
Immunoresearch). Slides were washed with PBS and
mounted in Fluoromount- G medium.
2.6
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Image analysis
All images were recorded and analyzed in a blinded fash-
ion. For both SDH and ATPase staining, 4 randomized
images were recorded from each section with a Axioskop
Zeiss microscope at 20X magnification connected to an
AxioCam ICc Zeiss camera.
SDH- positive fibers were stained dark blue (high ox-
idative enzymatic activity) while SDH- negative fibers
were stained light blue (low oxidative enzymatic activity).
ATPase- positive fibers (sensitive to pH 4.6, i.e., fast mus-
cle fibers) were stained light blue while ATPase- negative
fibers (not sensitive to pH 4.6, i.e., slow muscle fibers)
were stained dark blue. For both stainings, the number of
positive and negative fibers was quantified with Imaging
Software (Image J, NIH) and normalized to the total num-
ber of fibers (i.e., ~450 fibers per sample).
For MyHC immunostaining, 4 randomized images were
recorded from each section with an Imager Z1 Zeiss mi-
croscope at 20X magnification connected to a CoolSNAP
MYO camera. Using the combination of antibodies de-
scribed above, MyHC- I was labeled by a blue staining,
MyHC- IIA by a green staining, MyHC- IIX by a red stain-
ing, and laminin by far red staining that was converted
into false white for a clear visible delineation of muscle
fibers. Muscle fiber cross- sectional area was quantified for
each MyHC isoform with ICY software (version 2.1.4.0;
http://icy.bioim agean alysis.com). The percentage of each
MyHC was then expressed relative to whole muscle cross-
sectional area (i.e., % total area representing ~320 fibers
per sample).7 The number of fibers expressing each MyHC
isoform was also quantified with Imaging Software (Image
J, NIH) and was normalized to the total number of fibers
(i.e., % total number representing ~500 fibers per sample).
2.7
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Statistical analysis
Statistical analysis was performed using GraphPad Prism
Software (version 7.00). Data distribution was initially
FIGURE  (A) Tendon and (B) semitendinosus muscle samples
obtained during anterior cruciate ligament reconstruction. The
panel A illustrates the insertion of the semitendinosus muscle on
the distal tendon while the panel B shows the amount of muscle
tissue obtained during the surgery
(A)
(B)
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FOURNIER et al.
investigated using Kolmogorov- Smirnov test. Student's t
test was performed for demographic variables. Student's
t test with Welch correction was used to test differences
between men and women for other variables. Cohen's d
values were calculated with G*Power software (Version
3.1.9.6).24 Small, moderate, and large effects were con-
sidered for d 0.2, 0.5, and 0.8, respectively. Data are
presented as mean ±SD with significance set at p<0.05.
3
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RESULTS
3.1
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SDH staining
SDH staining was used to compare the proportion of
muscle fibers showing high oxidative enzymatic activ-
ity between men and women (Figure2A- B). Men had a
significantly lower proportion of oxidative muscle fibers
(37.4±11.2%) as compared with women (49.3 ± 10.6%;
p<0.05; d=1.10; Figure2C).
3.2
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ATP staining
ATPase staining was performed to compare the propor-
tion of slow and fast muscle fibers between men and
women (Figure2D- E) A significant higher proportion of
fast muscle fibers was observed in men (65.8±10.1%) as
compared with women (54.8±8.3%, p< 0.05, d = 1.19;
Figure2F).
3.3
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MyHC immunostaining
MyHC immunostaining was performed to compare
the size and the proportion of muscle fibers expressing
MyHC- I, MyHC- IIA, and MyHC- IIX isoforms between
men and women (Figure3A- B) The cross- sectional area
of MyHC- I, MyHC- IIA, and MyHC- IIX muscle fibers
was 31%, 43%, and 50% larger in men as compared with
women, respectively (p<0.05; Table2). Considering the
variation in the size of both type 1 and type 2muscle fibers
between men and women, we first quantified the propor-
tion of muscle fibers expressing MyHC- I, MyHC- IIA, and
MyHC- IIX isoforms with regard to the area occupied by
each MyHC isoform. Men had a significantly lower per-
centage of MyHC- I positive- muscle fibers (35.6 ± 10.1%
vs. 48.7±8.9%; p<0.05; d=1.38; Figure3C) and a higher
percentage of MyHC- IIA (38.3 ± 6.7% vs. 32.5 ± 6.5%;
p<0.05; d=0.87; Figure3D) as compared with women.
Men also showed a trend toward a higher percentage of
MyHC- IIX (26.1±9.6% vs. 18.8±8.5%; p=0.06; d=0.81)
FIGURE  (A- B) Representative SDH staining of semitendinosus muscle obtained in men (panel A) and women (panel B). SDH- positive
fibers are stained dark blue (high oxidative enzymatic activity as shown by symbol “+”) while SDH- negative fibers are stained light blue
(low oxidative enzymatic activity as shown by symbol “- ”). Scale bar: 50μm. (C) Quantification of the proportion of oxidative fibers in men
(n=12) and women (n=12). (D- E) Representative ATPase staining of semitendinosus muscle obtained in men (panel D) and women (panel
E). ATPase- positive fibers (sensitive to pH 4.6, ie, fast muscle fibers) are stained light blue (as shown by symbol “+”) while ATPase- negative
fibers (not sensitive to pH 4.6, ie, slow muscle fibers) are stained dark blue (as shown by symbol “- ”). Scale bar: 50μm. (F) Quantification
of the proportion of fast fibers in men (n=12) and women (n=12). Significantly different from men: *p<0.05; **p<0.01. Results are
mean±SD
(A) (B)
(D) (E)
(C)
(F)
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FOURNIER et al.
expressing muscle fibers as compared with women
(Figure3E).
When expressed as a relative number of fibers, men
also had a significantly lower percentage of MyHC- I
positive- muscle fibers and higher percentage of MyHC- IIX
expressing muscle fibers as compared with women
(p<0.05; Table2). No significant difference was observed
for the expression of MyHC- IIA between the two groups
(Table2).
4
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DISCUSSION
In the present study, we combined histochemical and
immunostaining analyses to compare hamstring muscle
fiber- type composition between adult men and women.
The most important finding of this study was the iden-
tification of sex differences in muscle composition as il-
lustrated by a faster muscle phenotype and larger muscle
fiber size in men as compared with women.
4.1
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Semitendinosus muscle fiber- type
composition
Human skeletal muscle is a very heterogenous tissue fea-
turing a composition of various muscle fiber types. Recent
evidence illustrated that muscle fiber- type composition is
FIGURE  (A- B) Representative MyHC immunostaining of semitendinosus muscle obtained in men (panel A) and women (panel B).
MyHC- I is labeled by a blue staining, MyHC- IIA by a green staining, MyHC- IIX by a red staining, and laminin by far red staining that is
converted into false white for a clear visible delineation of muscle fibers. Regions of interest for the quantification of muscle fiber cross-
sectional area are drawn. Scale bar: 50μm. (C- E) Proportion of MyHC- I (panel C), MyHC- IIA (panel D), and MyHC- IIX (panel E) expressed
in percentage of the whole muscle cross- sectional area (ie, % total area) in men (n=12) and women (n=12), respectively. Significantly
different from men: *p<0.05; **p<0.01. Results are mean±SD
(A) MEN
WOMEN
MyHC-1/MyHC-IIA/MyHC-IIX
(B)
(C) (D)(E)
TABLE  Semitendinosus muscle fiber size and composition in
men and women
Men Women D
Fiber size (µm2)
MyHC- I 4905±1873 3396±1053*0.99
MyHC- IIA 5256±1616 3011±1099*** 1.62
MyHC- IIX 4622±2199 2327±1039** 1.33
Fiber- type composition
(% total number)
MyHC- I 32.3±8.2 42.0±8.7*1.14
MyHC- IIA 33.8±5.7 31.3±8.0 0.36
MyHC- IIX 33.9±7.4 27.4±7.6*0.87
Note: Cohen's d values are reported in the right column. Significantly
different from men: *p<0.05; **p<0.01; ***p<0.001. Data are presented as
mean±SD.
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FOURNIER et al.
dependent on species,25 anatomical location,26 and sex.2
Despite the critical role of hamstring muscles in human
locomotion and sprint- based activities, their fiber- type
composition has been poorly characterized,13- 17 with most
studies being performed with samples obtained mainly via
autopsy from men13,14,16 and only a few investigations fo-
cusing on the semitendinosus muscle.16,17
When considering our data obtained in men only,
we found that the semitendinosus muscle had a larger
distribution of fast muscle fibers (i.e., ~66% of ATPase-
positive fibers and ~64– 68% of MyHC- II) as compared
with slow muscle fibers. This fast phenotype associated
with the semitendinosus muscle is in accordance with
that previously observed in ten (including 7 men) ca-
davers16 (i.e., ~60% of type 2 fibers) but differs with the
balanced fiber- type distribution reported in a previous
study of sixteen adult patients (including 14men) who
underwent ACL reconstruction17 (i.e., 50% of type 2 fi-
bers). Considering that we also analyzed biopsy sam-
ples from patients with the same pathology (i.e., ACL
reconstruction), this discrepancy is hard to explain. It is
noteworthy that the histochemical and immunostaining
investigations performed here are more thorough than
those performed by Eriksson et al.,17 our quantitative
analyses involving a larger number of fibers (i.e., ~500
fibers vs. ~200 fibers, respectively).
Our results obtained in men also underline that the sem-
itendinosus muscle displays the fastest phenotype among
the hamstrings as illustrated by the higher proportion of
fast fibers (> 60%) as compared with that reported in the
biceps femoris (i.e., ~51– 53% of MyHC- II)14,15 and in the
semimembranosus (i.e., ~50% of type 2 fibers)16muscles.
We showed that men semitendinosus muscle exhib-
ited a faster muscle fiber- type composition as compared
with women as illustrated by a smaller proportion of
SDH- positive fibers (i.e., Figure2A- C), a higher percent-
age of ATPase- positive fibers sensitive to specific acid
pH (i.e., Figure 2D- F), as well as a lower percentage of
area occupied by MyHC- I positive- muscle fibers (i.e.,
Figure3C) together with a higher percentage of area oc-
cupied by MyHC- IIA (i.e., Figure3D) and MyHC- IIX (i.e.,
p=0.06; Figure3E) positive- muscle fibers. These results
are in accordance with the sexual dimorphism previously
described in the quadriceps muscle (i.e., vastus latera-
lis), with men having a lower proportion of type 1 fibers
and higher percentage of type 2 fibers as compared with
women. Taken together, muscle fiber- type composition
differs between men and women in both vastus lateralis
and semitendinosus muscles, therefore independently of
the functional role of the considered muscle (i.e., knee ex-
tension vs. knee flexion, respectively).
Finally, we demonstrated that the cross- sectional area
of MyHC- I, MyHC- IIA, and MyHC- IIX muscle fibers
was larger in men as compared with women, the differ-
ence being higher for type 2 (+43– 50%) than for type 1
(+31%) muscle fibers. These results are similar with those
reported in the vastus lateralis,4,7 tibialis anterior,12 and bi-
ceps brachii10muscles. They indicate that sex differences
in muscle fiber size are consistently found among human
skeletal muscles in both upper and lower limbs and inde-
pendently of the subject characteristics (e.g., healthy vol-
unteers, patients undergoing ACL reconstruction).
4.2
|
Potential consequences of sex
differences in semitendinosus muscle
composition
The functional consequences of the sexual dimorphism
in semitendinosus muscle fiber- type composition are un-
clear. On the basis of isolated and single muscle fiber ex-
periments, it was reported that MyHC composition is a
key determinant of muscle fiber contractile velocity27 and
fatigue resistance.28 One could therefore speculate that
the faster phenotype in men might be beneficial for rapid/
ballistic movements while the slower muscle typology in
women might provide an advantage in terms of fatigue re-
sistance. However, it has been recently reported that the
biceps femoris MyHC distribution was unrelated to any
measure of maximal or explosive strength in a cohort of
adult healthy men.15
Although sex differences in fatigue resistance have
been documented, illustrating a greater fatigue resistance
in women than in men,29,30 it should be kept in mind that
the etiology of fatigue is multifactorial and involves factors
other than muscle typology (e.g., impairment of the cen-
tral nervous system, alterations in excitation- contraction
coupling).28,31
Hamstring muscles play a key role in several explo-
sive muscle activities and are frequently injured. Indeed,
HSI is the most prevalent non- contact injury in various
sports such as soccer32 and sprinting.33 Interestingly,
evidence of a higher incidence of HSI in men than in
women is emerging.18,19 Considering the higher suscep-
tibility to exercise- induced muscle injury of fast muscle
fibers than the slow ones,20,21 one could speculate that
the faster hamstring muscle fiber- type composition in
men might be a predisposing factor to HSI. Although the
present study does not aim at addressing this issue, a di-
rect link between HSI and fiber- type distribution seems
questionable. Indeed, the semitendinosus is the fastest
muscle among the hamstrings but is also the less injured
muscle as it is involved in less than 10% of soccer- related
HSI while the biceps femoris accounting for more than
80% of HSI.34 One could, therefore, assume that fac-
tors other than muscle fiber- type composition (e.g.,
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FOURNIER et al.
anatomical and/or biomechanical factors35- 37) may play
a key role in the incidence of HSI.
4.3
|
Limitations
There are several limitations in our study. Muscle samples
were obtained from semitendinosus of patients undergoing
ACL reconstruction. It remains to demonstrate whether a
similar sex difference exists in both healthy subjects and
professional athletes. The surgical procedure of ACL re-
construction precluded any functional measurements at
the time of the biopsy. In addition, our study focused on
the semitendinosus muscle which accounts only for ~25%
of the total hamstring muscle volume, whereas hamstring
functional performance is influenced by both the biceps
femoris and the semimembranosus muscles. Finally, sem-
itendinosus muscle was obtained in patients aged from 22
to 49years in men and from 24 to 49years in women. Our
sample size was too small to consider subgroup of patients
according to their age (e.g., <30years vs. 30– 40 years vs.
>40 years). Further studies are warranted to determine
the influence of age on semitendinosus muscle fiber- type
composition in men and women.
5
|
CONCLUSION
The present study is the first to compare hamstring
muscle fiber- type composition between adult men and
women. Thanks to the combination of histochemical and
immunostaining analyses, we showed sex differences in
semitendinosus muscle fiber- type composition as illus-
trated by the faster phenotype and larger muscle fiber size
in men as compared with women.
6
|
PERSPECTIVE
The impact of this sexual dimorphism on explosive per-
formance, resistance to fatigue, and/or incidence of injury
is still unknown. Further studies are needed to determine
whether and to what extent sex differences in semiten-
dinosus muscle fiber- type composition influence muscle
performance in vivo.
ACKNOWLEDGMENT
This work was funded by the “Antonin Poncet” prize.
CONFLICT OF INTEREST
GF, CB, MCV, RK, MP, ESM, BC, and JG have nothing
to disclose. ES reports non- financial support from Corin,
non- financial support from Smith and Nephew, outside
the submitted work.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are avail-
able on request from the corresponding author. The
data are not publicly available due to privacy or ethical
restrictions.
ORCID
Julien Gondin https://orcid.org/0000-0002-3108-605X
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How to cite this article: Fournier G, Bernard C,
Cievet- Bonfils M, et al. Sex differences in
semitendinosus muscle fiber- type composition.
Scand J Med Sci Sports. 2022;00:1– 8. doi:10.1111/
sms.14127
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Age-related muscle loss (sarcopenia) is a major clinical problem affecting both men and women - accompanied by muscle weakness, dysfunction, disability, and impaired quality of life. Current definitions of sarcopenia do not fully encompass the age-related changes in skeletal muscle. We therefore examined the influence of aging and sex on elements of skeletal muscle health using a thorough histopathological analysis of myocellular aging and assessments of neuromuscular performance. Two-hundred and twenty-one untrained males and females were separated into four age cohorts [mean age 25 y (n = 47), 37 y (n = 79), 61 y (n = 51), and 72 y (n = 44)]. Total (-12%), leg (-17%), and arm (-21%) lean mass were lower in both 61 y and 72 y than in 25 y or 37 y (P < 0.05). Knee extensor strength (-34%) and power (-43%) were lower (P < 0.05) in the older two groups, and explosive sit-to-stand power was lower by 37 y (P < 0.05). At the histological/myocellular level, type IIx atrophy was noted by 37 y and type IIa atrophy by 61 y (P < 0.05). These effects were driven by females, noted by substantial and progressive type IIa and IIx atrophy across age. Aged female muscle displayed greater within-type myofiber size heterogeneity and marked type I myofiber grouping (~5-fold greater) compared to males. These findings suggest the predominant mechanisms leading to whole muscle atrophy differ between aging males and females: myofiber atrophy in females vs. myofiber loss in males. Future studies will be important to better understand the mechanisms underlying sex differences in myocellular aging and optimize exercise prescriptions and adjunctive treatments to mitigate or reverse age-related changes.
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Performance fatigability differs between men and women for a range of fatiguing tasks. Women are usually less fatigable than men and this is most widely described for isometric fatiguing contractions, and some dynamic tasks. The sex difference in fatigability is specific to the task demands so that one mechanism is not universal, including any sex differences in skeletal muscle physiology, muscle perfusion and voluntary activation. However, there are substantial knowledge gaps about the task dependency of the sex differences in fatigability, the involved mechanisms and the relevance to clinical populations and with advanced age. The knowledge gaps are in part due to the significant deficits in the number of women included in performance fatigability studies despite a gradual increase in the inclusion of women over the last 20 years. Therefore, this review 1) provides a rationale for the limited knowledge about sex differences in performance fatigability, 2) summarizes the current knowledge on sex differences in fatigability and the potential mechanisms across a range of tasks, 3) highlights emerging areas of opportunity in clinical populations, and 4) suggests strategies to close the knowledge gap and understanding the relevance of sex differences in performance fatigability. The limited understanding about sex differences in fatigability in healthy and clinical population presents as a field ripe with opportunity for high impact studies. Such studies will inform on the limitations of men and women during athletic endeavors, ergonomic tasks and daily activities. Because fatigability is required for effective neuromuscular adaptation, sex difference in fatigability studies will also inform on optimal strategies for training and rehabilitation in both men and women.
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Background During top-level international athletics championships, muscle injuries are frequent. Objective To analyse the incidence and characteristics of muscle injuries and hamstring muscle injuries (hamstring injuries) occurring during top-level international athletics championships. Methods During 16 international championships held between 2007 and 2015, national medical team and local organising committee physicians reported daily all injuries on a standardised injury report form. Only muscle injuries (muscle tears and muscle cramps) and hamstring injuries have been analysed. Results 40.9% of all recorded injuries (n=720) were muscle injuries, with 57.5% of them resulting in time loss. The overall incidence of muscle injuries was higher in male athletes than female athletes (51.9±6.0 vs 30.3±5.0 injuries per 1000 registered athletes, respectively; RR=1.71; 95% CI 1.45 to 2.01). Muscle injuries mainly affected the thigh (52.9%) and lower leg (20.1%), and were mostly caused by overuse with sudden onset (38.2%) and non-contact trauma (24.6%). Muscle injury risk varied according to the event groups. Hamstring injuries represented 17.1% of all injuries, with a higher risk in male compared to female athletes (22.4±3.4 vs 11.5±2.6 injuries per 1000 registered athletes, respectively; RR=1.94; 95% CI 1.42 to 2.66). Conclusions During international athletics championships, muscle injury is the principal type of injury, and among those, the hamstring is the most commonly affected, with a two times higher risk in male than female athletes. Athletes in explosive power events, male athletes and older male athletes, in specific were more at risk of muscle injuries and hamstring injuries. Injury prevention strategies should be sex-specific.
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Previous studies have identified over 3,000 genes that are differentially expressed in male and female skeletal muscle. Here, we review the sex-based differences in skeletal muscle fiber composition, myosin heavy chain expression, contractile function, and the regulation of these physiological differences by thyroid hormone, estrogen, and testosterone. The findings presented lay the basis for the continued work needed to fully understand the skeletal muscle differences between males and females. ©2015 Int. Union Physiol. Sci./Am. Physiol. Soc.