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PLOS ONE
RESEARCH ARTICLE
Neuromuscular characteristics of agonists

and antagonists during maximal eccentric
knee flexion in soccer players with a history of
hamstring muscle injuries
Ramona Ritzmann ID1*, Sarah Strütt2,3, Ignacio Torreno3, Janine Riesterer2,
Christoph Centner2, Luis Suarez-Arrones ID4,5
a1111111111 1 Department of Sports and Sport Science, University of Freiburg, Freiburg, Germany, 2 Praxisklinik
a1111111111 Rennbahn AG, Muttenz, Switzerland, 3 FC Basel, Basel, Switzerland, 4 FC Lugano, Lugano, Switzerland,
a1111111111 5 Department of Sports and Computer Science, Section of Physical Education and Sports, Universidad Pablo
a1111111111 de Olavide, Seville, Spain
a1111111111 * ramona.ritzmann@sport.uni-freiburg.de
Abstract
OPEN ACCESS
Citation: Ritzmann R, Strütt S, Torreno I, Riesterer

J, Centner C, Suarez-Arrones L (2022) Background
Neuromuscular characteristics of agonists and Muscle strain injuries (MSIs) in the hamstrings are among the most prevalent injuries in elite
antagonists during maximal eccentric knee flexion
in soccer players with a history of hamstring
soccer. We aimed to examine the relation between biomechanical maladaptation in eccen-
muscle injuries. PLoS ONE 17(12): e0277949. tric strength and neuromuscular factors separated by their time and frequency domains.
https://doi.org/10.1371/journal.pone.0277949
Editor: Sumiaki Maeo, Ritsumeikan University, Methods

JAPAN
20 elite soccer players with a previous history of unilateral MSI in the M. biceps femoris (BF)
Received: April 22, 2022 long head and 20 without MSI participated. Knee flexion torques, rate of torque development
Accepted: November 7, 2022 (RTD) and electromyographic signals (EMG) of the BF, the M. semitendinosus (SMT) and
Published: December 1, 2022 knee extensors were obtained during unilateral maximal eccentric knee flexions performed
at slow (30˚/s) and fast (120˚/s) angular speeds. Root mean squares and mean power fre-
Copyright: © 2022 Ritzmann et al. This is an open
access article distributed under the terms of the quency (MF) was calculated.
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
Results
author and source are credited. In the group with a history of MSI, reduced maximal eccentric flexion torque (slow eccentrics
Data Availability Statement: Data cannot be -8±11, p<0.05; fast eccentrics -18±13 N*m, p<0.05) and RTD (-33±28 N*m/s, p<0.05; -95
shared publicly because of the involvement of elite ±47 N*m/s, p<0.05) concomitantly occurred with diminished agonistic myoelectrical activi-
sportmen. Data are available from the ties (-4±5% of MVC, p<0.05; -10±7% of MVC, p<0.05) and MFs (-24±13 Hz, p<0.05; -24±18
Rennbahnklinik Institutional Data Access for
researchers who meet the criteria for access to
Hz, p<0.05) in the BF. Simultaneously, antagonistic myoelectric activity was elevated (+4
confidential data. The data underlying the results ±3% of MVC, p<0.05; +3±3% of MVC, p<0.05) in MSI affected legs as compared to unaf-
presented in the study are available from (Ramona fected legs for both eccentric contractions. Deficits in myoelectrical activity (r2 = 0.715,
Ritzmann, Ramona.ritzmann@sport.uni-freiburg.
p<0.05; r2 = 0.601, p<0.05) and MF (r2 = 0.484, p<0.05; r2 = 0.622, p<0.05) correlated with
de). Data are owned by a third-party organization
which is the FC Basle. Data can also be requested deficits in maximal torque in the affected leg in the MSI group. Analysis of SMT demon-
via mail to info@fcb.ch. strated no significant differences.
PLOS ONE | https://doi.org/10.1371/journal.pone.0277949 December 1, 2022 1 / 19

PLOS ONE Neuromuscular adaptations in soccer players with a history of hamstring muscle injuries
Funding: The author(s) received no specific Conclusion

funding for this work.
Positive relationships between neuromuscular deficits and the reduced eccentric strength
Competing interests: The authors have declared
profile underpin neuronal inhibition after MSI. This persistent involvement of dysfunctional
that no competing interests exist.
synergist and antagonist neural hamstring function in strength weakness is of clinical rele-
vance in sports medicine for prevention and rehabilitation.
Background
Muscle strain injuries (MSIs) in the hamstrings are among the most prevalent non-contact
injuries in soccer [1]. The biceps femoris long head (BF) is the most commonly injured muscle
accounting for 60–85% of all muscle injuries [2]. A typical MSI is characterized by sudden
pain in the posterior thigh which is elicited by a mechanical disruption of sarcomeres induced
by an external eccentric strain exceeding tissue strain capacity [1]. MSI severity is classified
into three grades: minor microscopic tearing and some loss of function (grade I), extensive
damage, with numerous muscle fibers torn (grade II) and a full (grade III). MSIs among grades
I- III in elite sports cause a remarkable time loss of three to 20 weeks from training and compe-
tition [3] which results in a diminished athletic performance [4] and subsequently, in financial
loss. In the English premier soccer league, the projected loss of output due to such injuries
amounted up to 100 Mio $ per season [5].
Despite extensive research to identify risk factors predisposing athletes to MSIs, epidemio-
logical data obtained from team sports across 20 years of research indicates that rates and
recurrences of MSIs have not declined in the last decade [6]. Despite the awareness for impor-
tant risk factors (e.g., previous MSI, short fascicles) [7], the recurrence rates in MSIs are not
regressing which highlights that current approaches aiming at the prevention MSIs require
further scientific investigation [6–9].
Whilst it is commonly accepted that the etiology of MSIs and its recurrencies are multifac-
torial in nature, the potential role of the nervous system (NS) has been overlooked and moved
into the fore just in the most recent years. The NS regulates muscle length and controls for tol-
erable changes in myo-elongation with contraction forces achieved by electromechanical cou-
pling [10, 11]. Sensory feedback from myoreceptors collect information about the actual
muscle tensions and thus, can protect the muscle from experiencing excessive strain [12].
Some studies point out relevant neuromuscular aspects such deteriorated contributions of
biceps femoris and its synergists [13] and chronic activation deficits of hamstrings with a for-
mer MSI during contractions. In addition, previously injured hamstrings were reported to be
weaker and BF myoelectrical activity lower as compared to the contralateral uninjured ham-
string [14, 15]. Pathophysiologically, this is particularly interesting as a previous MSI has been
consistently identified as a primary risk factor which predisposes athletes to a secondary MSI
[10].
Within a sport specific context, clinicians and trainers integrate eccentric muscle strength
as a measure of neuromuscular integrity as a key criterion to determine if an athlete is ready
for return to sport or competition after MSI [7, 9]. Measurement paradigms encompass (sub)
maximal eccentric isokinetic, leg curls and Nordic hamstring exercises at various speeds (30˚/
s– 240˚/s) [16]. Isokinetic dynamometry is in the top three tests for player screening in elite
sport. Joint torques and impulses are commonly compared between the injured and the unin-
jured legs to detect (a)symmetries. Although there is currently no uniform cut-off for a safe
return to sport, an inter-limb difference (injured vs- uninjured) of 10% is frequently used as a
consensus [17] without consideration of the neuromuscular factors [18].

Therefore, this cross-sectional study examines the relation between maladaptation in bio-
mechanics and neuromuscular control of eccentric knee flexion separated by their time and
frequency domains in a cohort of elite soccer players a previous MSI in the BF long head as
compared to healthy controls. Understanding these factors may interact based on myoelectri-
cal and torque-time data, we also propose a tentative hypothesis as to how previous MSIs may
lead to neuronal maladaptation of the BF which may dysregulate the force generating capacity.
Methods
Experimental design
We executed a cohort study with elite soccer players in a cross-sectional repeated measures
design. Players with a previous unilateral MSI in the BF long head were compared to healthy
players without MSI. We experimentally evaluated the effect of eccentric loading of the active
hamstring muscle tendon unit induced by isokinetic measures on neuromuscular correlates
and joint torque among the active range of motion.
The study had been approved by Swiss Ethics for Ethics in Human Experimentation (No
EKNZ 2017–01825). The study is registered with the German Register of Clinical Studies (No
DRKS00020210).
Participants
Eighty-seven elite male soccer athletes volunteered to participate in the study. All subjects gave
their written informed consent for these experiments.
Inclusion criteria were i) an age > 17y, ii) a former traumatic MSI in the BF long head expe-
rienced during soccer training or competition certified to be grade I or II by an MRI or MRI/
ultrasonography, iii) clinically released, fully participating in regular trainings and matches
and elite athletes. Elite refers as a minimum to national selection actively participating in
national and international championships. Exclusion criteria were sickness, inflammation,
flue, neurologic diseases, acute orthopedic or muscle injuries of the lower extremities, vestibu-
lar or proprioceptive dysfunctions, previous cartilage or ligamentous surgeries on the knee
joint, neuro-degenerative diseases or single events associated with neural dysfunctions. Partici-
pants underwent a medical screening to verify eligibility for the experiment. In this context,
subjects were screened for previous hamstring strain injuries [19] and assigned into one of two
groups: CONTROL group and MSI group. For the MSI group, subjects were only included if
the injury was one-sided and occurred within the last year. A total of n = 20 participants were
enrolled in the MSI group and n = 20 participants were enrolled in the CONTROL group
(Fig 1).
A priori, the sample size was estimated by means of a power analysis based on a previously
executed pilot study including 7 subjects (f = 0.90; alpha = 0.05; power = 0.90).
Clinical data
The history of muscle strain injuries was addressed by the following items: the affected leg (left
or right) and topographic location differentiated by the damaged muscles. The injury event
was described by the date, season (pre or competitive season), the activity during which the
injury occurred (run, sprint, cut, shot, jump; with or without ball; opponent contact or no
opponent contact). Injury severity was addressed by the duration of time loss until full partici-
pation in training and competition [20] and the number of competitive games missed. Infor-
mation about the players‘position, training, and match exposure prior to injury were collected.

Fig 1. CONSORT flow chart diagram. Enrollment procedures and sample size.
https://doi.org/10.1371/journal.pone.0277949.g001
Isokinetic dynamometry
Maximal eccentric knee flexion torque was measured using an isokinetic dynamometer
(Humac1/NormTM, CSMi, Stoughton, Massachusetts, US) [21]. Measurements were per-
formed in the Praxisklinik Rennbahn AG, (Muttenz, Switzerland) either 10 am– 11:30 am,
3pm - 6pm during the week except for days before and after the matches.
Reliability and validity of this dynamometer for isokinetic concentric knee flexion and pro-
cedure are described elsewhere [16, 22]. Subjects were seated in a rigid chair and firmly
strapped at the hip, the torso and distal thigh at 90˚ [23]. The rotational axis of the dynamome-
ter was aligned to the lateral femoral epicondyle, and the lower leg was attached to the dyna-
mometer lever arm above the medial malleolus, with no fixation of the ankle joint. Both legs
were tested separately and in a random order; maintaining complete randomness of trials was
achieved by flipping a coin. The measurements were preceded by 10 min of warm-up at a sta-
tionary cycle ergometer (50W), followed by six submaximal familiarization trials with instruc-
tions for maximal contractions and moment cycles in the dynamometer.
Maximum voluntary concentric and eccentric hamstring contractions were randomly per-
formed during slow and fast knee movements with visual feedback for the contraction cycle

on a screen in front of the athlete. Counting backwards 3-2-1-0 indicated the beginning of the
contraction. According to literature we used knee joint angular velocities at 30˚/s and 120˚/s,
respectively [7, 9, 16]. Encouragement was done verbally for each athlete and each of the repe-
titions in the same way.
Knee joint excursion was from full extension 0˚ to 90˚ flexion [24]. Two successive trials
were performed, separated by a rest period of at least 30 s to a maximum of 1 min. All recorded
torque signals were corrected for the effect of gravity by calibration prior to each trial [25].
Synchronous sampling of the dynamometer strain gauge signal, lever arm position, and
EMG signals was performed at 2 kHz analogue-to-digital conversion rate using an external A/
D converter. Torque curves were smoothed by using a Butterworth fourth-order zero-lag low-
pass filter with a 10 Hz cut-off frequency.
Peak torque and peak torque index were assessed [24]. The index is the time (ms) between
onset until the peak torque has been reached. Peak torques were further extracted for the time
intervals 0–50 ms, 50–100 ms and 100–200 ms after onset [9] and for the interval 20˚ - 0˚ knee
extension (full extension, the BF muscle tendon unit and fascicles are most elongated) [23, 26].
Rate of torque development (RTD, Nm/s) was measured as the slope of the MVC torque-time-
curve in the time intervals 0–50 ms, 0–100 ms and 0–200 ms [22, 27, 28]. Impulses (Nm� s)
were calculated as the area below the MVC torque-time-curve among the entire ROM and in
the time intervals 0–50 ms, 0–100 ms and 0–200 ms.
Electromyographic (EMG) recordings

Bipolar Ag/AgCl surface electrodes (Ambu Blue Sensor P, Ballerup, Denmark; diameter 9 mm,
center-to-center distance 34 mm) were placed over the Musculus (M.) biceps femoris long head
(BFLH), the M. semitendinosus (ST), the vastus medialis (VM) and the M. rectus femoris (RF) of
the right and left leg according to SENIAM [29]. The longitudinal axes of the electrodes were in
line with the direction of the underlying muscle fibers. Inter electrode resistance was kept below
2.5 kO by means of shaving, light abrasion, degreasing, and disinfection of the skin. Electrodes
and preamplifiers were carefully taped to the skin and the upper and lower leg was covered with a
surgical net to avoid electrode movement. EMG Signals were transmitted wireless (Myon,
Schwarzenberg, Switzerland), recorded with 2 kHz, amplified, and filtered (band-pass filter 10
Hz– 1 kHz, 1000). Electromyographic data recording was synchronized to isokinetic data.
The trial with highest impulse (i.e., largest torque-angle curve area) was identified in each
subject and selected for further analysis [22]. Fig 2 shows representative torque-time curves
and the EMG-time curve of one subject. Data processing was performed according to the gold
standard for eccentric torque and EMG as follows:
EMG signals were smoothed by using a linear envelope, which consisted of digital high-
pass filtering at a 5-Hz cut-off frequency followed by full-wave rectification and subsequent
low-pass filtering at a 10-Hz cut-off frequency [22]. For between group comparison with refer-
ence to the MSI history, the BF and SMT root mean squares (RMS) were calculated for equiva-
lent time intervals as for torque measures. For VM and RF, the RMS procedure was applied for
90˚ - 0˚ and for 20˚ - 0˚.
vffi0
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi1
ffiffiffiffi
u ZT
u
u 1
RMS ¼ t@ x2 ðtÞdt A
T
0
where x(t) is the EMG signal and T is the acquisition time. Data were normalized to RMS val-
ues obtained during isometric MVC for BF at 20˚, SMT at 100˚ [30], VM and RF at 100˚ [31]
over a period of 500ms.

A Slow eccentric contraction, 30°/s
Unaffected leg without previous MSI history Affected leg with previous MSI
100Nm Torque
90°
0Nm Position 0°
2mV
EMG BF
-2mV
3mV
EMG ST
-3mV
1mV
EMG VM
-1mV
1mV
EMG RF
-1mV
t(s) t(s)
0 1 2 3 0 1 2 3
t
t
d
d
ar
ar
En
En
St
St
B Fast eccentric contraction, 120°/s
Unaffected leg without previous MSI history Affected leg with previous MSI
100Nm Torque
90°
0Nm Position 0°
2mV
EMG BF
-2mV
3mV
EMG ST
-3mV
1mV
EMG VM
-1mV
1mV
EMG RF
-1mV
t(s) t(s)
0 0.25 0.50 0.75 0 0.25 0.5 0.75
Fig 2. Raw tracings of isokinetic knee torque and electromyogram (EMG). They obtained in a male elite soccer player in the paradigm of
maximal eccentric knee flexion contraction during joint movements performed at slow (A) and fast (B) joint angular speeds (30˚/s and 120˚/
s, respectively) illustrated for the unaffected leg (left) and the affected leg with a history of MSI. Range of joint motion was from 90˚ to 0˚ (0˚ =
full knee extension). Upper tracings display the joint torque and position signal. Lower tracings display raw EMG signals recorded from the
biceps femoris (BF), semitendinosus (ST), vastus medialis (VM), and rectus femoris (RF) muscles. EMG was lower in the MSI affected
compared with the unaffected leg, suggesting significant neural inhibition after MSI. Note the appearance of large EMG amplitude spikes
separated by short inter spike periods of high neuromuscular activity in the BF and SMT of the unaffected leg as compared to the affected leg.
Furthermore, torque and EMG amplitudes were diminished on the MSI affected side, especially during eccentric and fast concentric
contractions (B).

The spectral parameters were evaluated by standard Fast Fourier Transformation and the
median frequency (MF) calculated as follows:
Z
fmed Z1 Z1
1
MF ¼ Pðf Þdf ¼ Pðf Þdf ¼ Pðf Þdf
2
0 fmed 0
Where P(f) is the power spectrum density. The MDF, which is the frequency value that
divides the spectrum into two regions of equal power, is determined by the overall action
potential conduction velocity of the muscle. Analyses were performed using Matlab version
7.12 software (MathWorks, R2011a, Natick, MA, USA).
Statistics
The legs of the control group were grouped by left and right. The effect of a previous BF MSI on the
variables torque, RTD, impulse, the EMG activity (integrals and median frequency) of BF, ST, VM
and RF as well as VM/BF co-activation was evaluated using a two-factor analysis of variance
(ANOVA): group [CONTROL vs. MSI] and leg [affected vs. unaffected]. The normality of the data
was evaluated using Kolmogorov-Smirnov test and all data followed a normal distribution. If the
assumption of sphericity, as measured via Mauchly’s test, was violated, the Greenhouse-Geisser cor-
rection was used. To correct for multiple testing, the false discovery rate was controlled according to
the Benjamini–Hochberg–Yekutieli method. Benjamini–Hochberg–Yekutieli conceptualizes the
rate of type I errors [32]. Partial Eta squared (η2p) was used as an estimate of the effect size for the
ANOVA (η2p � 0.06 small, 0.06 < η2p < 0.14 medium, η2p � 0.14 large effect size) [33].
A linear regression was calculated for differences between the unaffected leg and the
affected leg with MSI history for neuromuscular and biomechanical parameters. Data were
illustrated as scatter plots with regression lines.
All analyses were executed using SPSS 27.0 (SPSS, Inc., Chicago, IL, USA). The values are
presented as mean ± standard deviations (M ± SD).
Results
In the MSI group, all hamstring MSIs were traumatic with an acute onset. 95% of MSIs
occurred in noncontact situations, only 5% were induced during foul play while in physical
contact with opponents. Athletes experienced 55% of MSIs during high-speed running or
sprinting, 30% during the change of direction and 15% during jumps. Days of absence from
training after MSIs were 48 ± 53 and amounted up 64 ± 81 for absence from competition
which resulted in 7 ± 3 missed games. The event of MSI dated back 201 ± 96 days. Anthropo-
metrics, age attributes, training or match exposure are illustrated in Table 1.
Knee flexion torque

Grand means and statistics are illustrated in S1 and S2 Tables.
For the slow eccentric contraction, the ANOVA revealed a significant interaction
(group × leg) effect for the peak torque, peak torque index, peak torque100ms and peak tor-
que200ms. Eccentric knee flexor torques were reduced and the peak torque index was increased
in the leg with a history of MSI (Fig 3). For RTD100, RTD200 and Impulse50, the analysis
showed a significant interaction of group × leg. These parameters were significantly reduced
in the leg with an MSI history in the MSI group. Effect sizes ranged from medium to large.
Likewise, for the fast eccentric contraction, the ANOVA revealed a significant interaction
(group × leg) effect for each of the parameters collected knee flexor torques and RTD. The impulse

Table 1. Cohort characteristics, anthropometric data, and athletic specification.

Groups MSI group CONTROL group
Number n = 20 n = 20
UEFA Europe League n = 12 n=7
National elite level n=8 n = 13
Position, training, and match exposure
Striker n=4 n=5
Midfielder n=3 n=4
Winger n=7 n=5
Defender n=5 n=4
Goalkeeper n=1 n=2
Total exposure h/player/season (M ± SD) 258±89 256±90
Training exposure, h/player/season (M ± SD) 218±78 211±81
Match exposure, h/player/season (M ± SD) 37±23 39±21
Anthropometrics
Age (years, M ± SD) 24±5 24±3
Body mass (kg, M ± SD) 75±7 74±8
Stature (cm, M ± SD) 179±6 178±6
Injured leg eq. dominant leg n=9 n.a.
https://doi.org/10.1371/journal.pone.0277949.t001
and Impulse200ms showed a significant interaction of group × leg. All parameters were reduced in
the leg with an MSI history in the MSI group despite peak torque index. Effect sizes were large.
EMG activity
Grand means and statistics are illustrated in Tables 2 and 3. Graphics are illustrated in Fig 4.
The ANOVA revealed a significant interaction (group × leg) effect for BF EMGrms for both
eccentric contraction speeds which indicates a reduced myoelectrical activation in the leg with
a history of MSI (Fig 4). For all time intervals, the ANOVA revealed statistical significance
despite for 100–200 ms after contraction onset in the slow contraction. ANOVA results for
SMT EMGrms revealed no significant differences. Effect sizes were medium to large.
For the antagonistic knee extensors VM and RF, the ANOVA revealed a significant interac-
tion (group × leg) effect for both contraction speed in all time intervals (Tables 2 and 3).
EMG frequency
The ANOVA revealed a significant interaction (group × leg) effect for BF MF in the slow and
fast eccentric condition (Tables 2 and 3). Results for SMT MF revealed no significant differ-
ences. Effect sizes were large.
Co-contraction RF/BF-ratio and VM/BF-ratio

Grand means are illustrated in Table 4. The ANOVA revealed a significant interaction
(group × leg) effect for the co-contraction ratios in the slow eccentric contraction and the fast
eccentric indicating an increase in antagonistic co-contraction in the affected leg with MSI his-
tory as compared to the unaffected leg. Effect sizes ranged from medium to large.
Regressions
Scatter plots with regression lines are illustrated in Fig 5. The statistical analysis revealed posi-
tive regressions for normalized BF EMGrms and maximal knee flexion torque (slow eccentrics

Fig 3. A illustrates the MSI group with previous unilateral hamstring strain injuries experienced in the M. biceps long head
(left) and the healthy CONTROL group with bilateral healthy legs. Graphs B–E illustrate changes in joint torques and
impulses: B displays differences in the peak knee flexion joint torque (ordinate) and the corresponding knee flexion angle as
well as the joint torques at 30ms, 50ms 100ms and 200ms after the movement onset of the lever arm at 30˚/s speed for both
groups. Graph C displays differences in the total impulse and impulses calculated for the intervals 0–50ms, 0–100ms and

0–200ms after movement onset of the lever arm at 30˚/s speed. Joint torques at 120˚/s are illustrated in graph D. Joint
Impulses at 120˚/s are illustrated in graph E. Values are means ± SD; § indicates significant group � leg interaction effects; �
symbolizes significant pairwise differences.
F = 48.648, p<0.001, r2 = 0.715 and fast eccentrics F = 29.566, p<0.001, r2 = 0.601). BF

EMGrms and maximal knee flexion torque 0–200 ms after contraction onset and for BF MF
(slow eccentrics F = 18.833, p<0.001, r2 = 0.484 and fast eccentrics F = 38.196, p<0.001, r2 =
0.622) and maximal knee flexion torque revealed a positive interrelationship for both contrac-
tion speeds (slow eccentrics F = 20.843, p<0.001, r2 = 0.511 and fast eccentrics F = 34.724,
p<0.001, r2 = 0.641), as well.
Discussion
The current study permits major insights into the neuromuscular mechanisms underlying per-
sistently reduced eccentric force generating capacity of athletes with a history of MSI in the
BF. A reduced maximal eccentric knee flexion torque, rate of torque development and impulse
during eccentric knee flexion concomitantly occurred with diminished myoelectrical activities
and MFs in the BF while antagonistic myoelectric activity was elevated in affected legs with a
Table 2. Neuromuscular activity.

Eccentric contraction MSI group CONTROL group Statistics
unaffected MSI affected unaffected unaffected ANOVA η2p
M. biceps femoris
EMGRMS 95±4 91±5� 96±4 96±4 F = 7.014, p = 0.01 0.084
EMGRMS (0–50 ms) 15±4 10±5� 14±5 15±6 F = 6.010, p = 0.017 0.073
EMGRMS (50–100 ms) 29±7 21±7 29±8 30±8 F = 4.973, p = 0.029 0.061
EMGRMS (100–200 ms) 83±11 75±9� 81±8 83±9 F = 3.246, p = 0.076 0.041
EMGRMS (20˚–0˚) 90±8 81±5� 89±6 89±6 F = 9.696, p = 0.003 0.113
MF (Hz) 118±14 94±16� 120±15 123±15 F = 12.600, p = 0.001 0.142
M. semitendinosus
EMGRMS 94±5 93±5 94±4 95±4 F = 1.090, p = 0.30 0.014
EMGRMS (0–50 ms) 19±5 18±4 19±3 19±5 F = 0.358, p = 0.551 0.005
EMGRMS (50–100 ms) 27±6 26±6 27±7 27±5 F = 0.167, p = 0.684 0.002
EMGRMS (100–200 ms) 83±8 82±12 83±11 84±9 F = 3.246, p = 0.076 0.041
EMGRMS (20˚–0˚) 87±6 87±6 88±5 89±7 F = 0.102, p = 0.750 0.001
MF (Hz) 83±10 84±9 82±9 84±9 F = 0.210, p = 0.648 0.003
M. vastus medialis
EMGRMS 3±2 7±2� 3±1 4±2 F = 31.320, p<0.001 0.292
EMGRMS (20˚–0˚) 3±3 6±2� 4±1 3±2 F = 18.751, p<0.001 0.198
M rectus femoris
EMGRMS 3±3 7±2� 3±1 3±3 F = 15.251, p<0.001 0.167
�
EMGRMS (20˚–0˚) 4±4 7±2 3±2 4±2 F = 14.088, p = 0.007 0.093
Neuromuscular activation [electromyographic activity (root mean square normalized to MVC, EMGRMS) and median power frequency (MF)] obtained of knee flexor
and extensor muscles during slow (30˚/s) eccentric hamstring contractions. Differences in normalized EMGRMS are illustrated for the M. biceps femoris, M.
semitendinosus, M. vastus lateralis and M. rectus femoris for the entire range of motion and the interval 20˚–0˚ extension. BF and SMT is displayed for 0–50 ms, 50–100
ms and 100–200 ms intervals as well.
Values are means ± SE.
�
indicates a significant difference between legs. P values, F values and effect sizes (η2p) are given for significant group� leg interaction effects.

Table 3. Neuromuscular activity.

M. biceps femoris
EMGRMS 86±8 76±5 86±5 85±5 F = 12.750, p = 0.01 0.144
EMGRMS (0–50 ms) 11±2 8±3 13±4 12±3 F = 4.177, p = 0.044 0.052
EMGRMS (50–100 ms) 23±5 18±4 24±4 22±5 F = 6.277, p = 0.014 0.076
EMGRMS (100–200 ms) 67±9 55±10 65±9 67±10 F = 132.654, p<0.001 0.636
EMGRMS (20˚– 0˚) 75±7 64±8 75±8 74±7 F = 9.050, p = 0.006 0.096
MF 103±26� 79±13 109±15 108±15 F = 61.097, p<0.001 0.46
M. semitendinosus
EMGRMS 85±4 86±5 85±4 86±4 F = 0.193, p = 0.662 0.003
EMGRMS (0–50 ms) 15±5 13±5 14±3 16±4 F = 0.654, p = 0.421 0.009
EMGRMS (50–100 ms) 23±6 22±8 17±6 19±6 F = 0.167, p = 0.684 0.002
EMGRMS (100–200 ms) 72±10 69±13 71±9 71±10 F = 0.182, p = 0.671 0.002
EMGRMS (20˚– 0˚) 76±8 75±7 75±9 77±8 F = 0.073, p = 0.788 0.001
MF 75±10� 76±9 76±9 77±8 F = 27.070, p = 828 0.001
M. vastus medialis
EMGRMS 4±4 7±2 3±2 4±3 F = 8.227, p = 0.008 0.106
EMGRMS (20˚– 0˚) 4±4 8±4 4±3 4±2 F = 5.143, p = 026 0.063
M rectus femoris
EMGRMS 4±4 7±2 3±2 4±2 F = 1.550, p = 0.061 0.041
EMGRMS (20˚– 0˚) 3±5 7±3 3±2 2±2 F = 10.127, p = 0.016 0.099
Neuromuscular activation [electromyographic activity (root mean square normalized to MVC, EMGRMS) and median power frequency (MF)] obtained during fast
(120˚/s) eccentric hamstring contractions. Differences in normalized EMGRMS are illustrated for the M. biceps femoris, M. semitendinosus, M. vastus lateralis and M.
rectus femoris for the entire range of motion and the interval 20˚–0˚ extension. BF and SMT is displayed for 0–50 ms, 50–100 ms and 100–200 ms intervals as well.
Values are means ± SE.
�
indicates a significant difference between legs. P values, F values and effect sizes (η2p) are given for significant group� leg interaction effects.
history of MSI as compared to the unaffected legs. Myoelectric deficits correlated with deficits
in torque profiles in the MSI affected leg. Importantly, no differences for the contralateral,
non-injured leg of the MSI group and the healthy control group have been observed. These
outcomes provide evidence for the interrelationship between neuromuscular parameters and
muscle function when sustaining supramaximal eccentric loads.
Eccentric knee flexion torque

A left shift of the torque-angle-curve derived from slow concentric and fast eccentric knee flex-
ion dynamometry [34] concomitant with a reduced torque generating capacity to sustain
supramaximal external forces was observed in legs with a history of a healed previous MSI in
the BF long head (Figs 2 and 3). That knee flexors of the affected leg generate their peak tor-
ques at shorter muscle lengths than unaffected contralateral knee flexors is in line with previ-
ous results obtained in recreational athletes [24]. But it is new and remarkable finding for the
population of elite soccer players in the active stage of their careers. Eccentric knee flexion tor-
que was reduced by 5–15% in the leg with a previous MSI. With reference to a bilateral deficit
of 10% to allow a safe return to sport after MSI [17], the results are particularly delicate at high
angular speeds. Besides maximal torque and impulse (S1 and S2 Tables), the rate of torque
development at the beginning of the eccentric movement was diminished. The rate of torque
development refers to the ability of the neuromuscular system to increase contractile forces

§
*
§
*
Fig 4. Grand means of myoelectrical activities. A illustrates Biceps femoris myoelectrical activity as the root mean
square normalized to MVC and B the median frequency at 30˚/s during the eccentric knee flexion for the MSI and
CONTROL group. Grands means for myograms are illustrated across the entire range of motion and the intervals
0–50ms, 0–100ms and 0–200ms after movement onset of the lever arm at 30˚/s speed. C illustrates Biceps femoris
myoelectrical activity and D the median frequency at 120˚/s during the eccentric knee flexion for the MSI and
CONTROL group. Not the reduced myoelectrical activities and frequencies for the affected leg of the MSI groups as
compared to the healthy contralateral side or the CONTROL group. Values are means ± SD; § indicates significant
group � leg interaction effects; � symbolizes significant pairwise differences.
from a resting level as fast as possible [21]. Causal relationships with neuromuscular deficits
and the reduced eccentric strength profile underpin dysfunctional synergist and antagonist
neural hamstring function [18] as the underlying mechanism as highlighted in detail below.
Neuromuscular responses
Long-term weakness after musculoskeletal injury can be mediated by both muscular and neu-
ral adaptations [1]. Whilst myo-structural maladaptation have been reported previously [24],
the impact of a prior hamstring strain injury on neural function has been less understood [13–

Table 4. Co-contraction.
Slow angular speed (30°/s)
RF/BF-ratio 0.02±0.01 0.05±0.03 0.01±0.01 0.02±0.01 F = 4.550, p = 0.04 0.144
VM/BF-ratio 0.03±0.02 0.06±0.05 0.03±0.02 0.04±0.02 F = 10.026, p = 0.02 0.179
Fast angular speed (120°/s)
RF/BF-ratio 0.03±0.02 0.07±0.03 0.02±0.03 0.03±0.03 F = 7.991, p = 0.013 0.082
VM/BF-ratio 0.03±0.02 0.06±0.05 0.03±0.02 0.04±0.02 F = 12.718, p = 0.003 0.198
15]. Particularly, neuromuscular adaptation of elite athletes has been scarcely studied, yet [13].
In the current study with reference to healthy controls, between limb comparisons of normal-
ized neuromuscular factors revealed differences in neural hamstring function between the
affected and unaffected limbs (both time and frequency domain, Fig 4). Our current findings
manifest a 5% to 30% reduction of myoelectrical activity and frequency during slow and fast
eccentric contractions (Table 2 and S1 Table).
With reference to the time domain, the muscles’ EMG activity is related to the extent of the
muscle fibers’ recruitment [35] and firing rate [35, 36]. A high EMG activity results from a
high number of recruited muscle fibers and high motor unit discharge rates [37] and is accom-
panied by high forces generated by the musculature [37]. Based on these relations, the EMG
activity is the primary indicator for the activation intensity of the BF muscle at least within cer-
tain limits such as synergistic cross talk and nonlinearity [38]. A high EMGRMS, therefore, is
indicative of an increased muscle excitation allowing athletes to maintain myofibrillar linkages
and thus active force production during eccentric loading without being excessively stretched
or (micro)damaged [22]. A reduced EMGRMS, most critical in conditions of maximal muscle
lengthening during fast eccentric loading (i.e. at 20˚ at 120˚/s flexion approx. -15%), is indica-
tive of neuronal inhibition, reduced activation intensities and diminished forces [37] leading
to an increased risk of unphysiological muscle lengthening during the eccentric loading [18].
This close relationship between myoelectric activity and knee flexion torque is further
highlighted by the findings from our regression analysis, which indicate that deficits in EMG
amplitude predict 60–71% of the variance in deficits in maximal eccentric knee flexion torques
for slow and fast angular velocities, respectively (Fig 5). Although our findings within the labo-
ratory cannot easily be transferred into situation on the field, it should be noted that during
sprinting and changes of direction (as primary injury movements), the muscle undergoes pre-
cisely this eccentric stretching and an instantaneous high tensile force at high speed [11].
With reference to the frequency domain, the power spectrum of the EMG in the affected
BF shifted towards lower frequencies (approx. 25%) for the cohort of elite soccer players with a
history of MSI (Tables 2 and 3). Such lower frequency shifting has been associated with
changes in firing properties towards diminished motor unit action potential [39], increased
activation of slow motor units and a concomitant decrease in activation of fast units [40].
Interestingly, the observed responses confirm persistent neuromuscular deficits when the
opposite would be needed to protect the muscle from structural damage.
With reference to the augmented antagonistic co-activation on the side with a history of
an MSI it becomes apparent that not only the neuronal pattern synergistic but also the antago-
nistic muscles are affected. One of the direct mechanical effects of agonist-antagonistic coacti-
vation is a reduction in the resultant forces and moments [41]. Thus, the increased
myoelectrical activity of the quadriceps femoris during eccentric knee flexion (S2 Table)

Fig 5. Scatter plots with regression lines. They are illustrated for differences (Δ) between the unaffected leg and the
affected leg with MSI history in the biceps femoris long head (BF) muscles of the MSI group (n = 20) for the slow (30˚/
s, black) and fast (120˚/s, grey) eccentric contraction. A illustrates the plot for maximal torque and BF EMGRMS
(normalized to MVC) for the entire range of motion. B illustrates maximal torque and BF EMGRMS for the interval
0–200ms after contraction onset. Graph C illustrates the plot for maximal torque and the corresponding the medium
frequency. Regressions A–C are significantly positive.

indicates that antagonist muscles provide more opposing force to the contracting hamstrings.
Beside the BF, the ST and M. semimembranosus also belongs to the synergic hamstrings.
While myoelectrical signals cannot be derived from the M. semimembranosus, ST shows no
changes among the entire protocol (Tables 3 and 4). As the rectus femoris and vasti oppose the
action of the BF, the eccentric net torque is diminished [42]. A high antagonist coactivation is
associated with a protective stabilization throughout voluntary joint stiffening [41] while less
antagonist coactivation is associated with a high skill level, fine coordination or familiarity
with a movement pattern [42]. Both aspects are important for the clinical implication as the
protective safety is an important deliberate neural control strategy in terms of injury avoid-
ance. No differences for the contralateral, non-injured leg of the MSI group and the healthy
control group have been observed. This indicates that a neuromuscular and biomechanical
maladaptation’s in the leg with a history of MSI is certainly due to the previously strained mus-
cle and not individual-specific.
Limitations
For a conclusive statement, it is crucial to consider the limitations of the study. Two aspects
are of substantial importance: First, we identified the parameters such as myoelectrical ampli-
tude and frequency of the agonists and the ratio of antagonist-agonist myoelectrical activity to
affect the eccentric torque produced by the knee flexors. But the extent to which these factors
are responsible for the reduction in force cannot be determined with this study protocol. Sec-
ond, a follow-up describing the long-term effects of reduced neuromuscular capacity and its
association with recurrences was not included in the present study. Thus, we cannot make any
statement about the extent to which the neuromuscular adaptations are of long-term
relevance.
Clinical consequences
The positive regressions (Fig 5) between maximal torques and BF EMGRMS or MF underpin
prolonged neuronal deficits during maximal concentric muscle activation associated with a
reduced eccentric strength. Importantly, the athletes of the MSI cohort had already been clini-
cally released and fully participating in regular training and match operations for weeks. Thus,
despite the full recovery of the injury, neuronal deficits are still present. The causative between
maladaptation in muscle mechanics and neuromuscular risk factors separated by their time
and frequency domains (Fig 5) in the cohort of elite soccer players is a notable scientific insight
and noteworthy being implemented into sports medical diagnostics and therapy to support
advances in recovery. There is an ongoing debate about neuromuscular screening of elite ath-
letes [1, 43], combining dynamometry and electromyography for criteria-based return to sport
or return to competition after injury to prevent recurrence due to chronic weakness. Individ-
ual intervention-relevant weaknesses could thus be detected and clinically prioritized.
Conclusion
Since neuronal mediated hamstring weakness appears to be a long-lasting consequence of MSI
with reference to our results and a primary predictor for recurrences [44], neuromuscular fac-
tors represent important deficits which needs to be considered in clinic and rehabilitation
[18]. There is strong evidence to suggest that muscle injuries typically occurs when the muscle
is subjected to strain during high tension [45]. Activation deficits require more attention in
RTS diagnostics. Further, late rehabilitation including eccentric exercises seems appropriate
for this purpose because of its positive effects on muscle activation [46]. Further work is

needed to clarify the potential contribution of neuromuscular inhibition to MSI recurrences

and to examine the efficacy of rehabilitation protocols on voluntary hamstring activation.
Supporting information
S1 Table. Knee joint torques (N� m), rate of torque development (N� m/s) and contractile
impulse (N� m� s) during the slow eccentric contraction (speed 30˚/s) illustrated as
means ± standard deviations (M ± SD). RTD (Δ moment / Δ time) was calculated in time
intervals 0–50, 0–100, and 0–200ms (Δ time) from the onset of contraction. Contractile
R
impulse, defined as the area covered by the moment-time curve ( moment dt), was calculated
in the same time intervals. Values are means ± SE. � indicates a significant difference between
legs. P values and effect sizes partial eta square (η2p) are given for significant group� leg interac-
tion effects. Bolt numbers refer to significant pairwise differences between the affected and
non-affected leg.
(DOCX)
S2 Table. Knee joint torques (N� m), rate of torque development (N� m/s) and contractile
impulse (N� m� s) during the fast eccentric contraction (speed 120˚/s) illustrated as
means ± standard deviations (M ± SD). RFD (Δ moment / Δ time) was calculated in time
intervals of 0–50, 0–100, and 0-200ms (Δ time) from the onset of contraction. Contractile
R
impulse, defined as the area covered by the moment-time curve ( moment dt), was calculated
in the same time intervals. Values are means ± SE. � indicates a significant difference between
legs. P values and effect sizes partial eta square (η2p) are given for significant group� leg interac-
tion effects. Bolt numbers refer to significant pairwise differences between the affected and
non-affected leg.
(DOCX)
Acknowledgments
We would like to thank the athletes for their participation. We acknowledge support by the
Open Access Publication Fund of the University of Freiburg.
Author Contributions
Conceptualization: Ramona Ritzmann, Sarah Strütt, Ignacio Torreno, Luis Suarez-Arrones.
Data curation: Ramona Ritzmann, Sarah Strütt, Ignacio Torreno, Luis Suarez-Arrones.
Formal analysis: Ramona Ritzmann.
Investigation: Ramona Ritzmann, Sarah Strütt, Ignacio Torreno, Janine Riesterer, Luis Sua-
rez-Arrones.
Methodology: Ramona Ritzmann, Sarah Strütt, Ignacio Torreno, Janine Riesterer, Luis Sua-
rez-Arrones.
Project administration: Ignacio Torreno, Luis Suarez-Arrones.
Software: Ramona Ritzmann, Luis Suarez-Arrones.
Supervision: Ramona Ritzmann, Ignacio Torreno.
Visualization: Janine Riesterer, Luis Suarez-Arrones.
Writing – original draft: Ramona Ritzmann, Christoph Centner, Luis Suarez-Arrones.

Writing – review & editing: Ramona Ritzmann, Sarah Strütt, Ignacio Torreno, Janine Ries-
terer, Luis Suarez-Arrones.
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PLOS ONE

Neuromuscular characteristics of agonists

Citation: Ritzmann R, Strütt S, Torreno I, Riesterer

Editor: Sumiaki Maeo, Ritsumeikan University, Methods

PLOS ONE | https://doi.org/10.1371/journal.pone.0277949 December 1, 2022 1 / 19

Funding: The author(s) received no specific Conclusion

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PLOS ONE | https://doi.org/10.1371/journal.pone.0277949 December 1, 2022 3 / 19

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Electromyographic (EMG) recordings

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A Slow eccentric contraction, 30°/s

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Knee flexion torque

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Table 1. Cohort characteristics, anthropometric data, and athletic specification.

Co-contraction RF/BF-ratio and VM/BF-ratio

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F = 48.648, p<0.001, r2 = 0.715 and fast eccentrics F = 29.566, p<0.001, r2 = 0.601). BF

Table 2. Neuromuscular activity.

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Table 3. Neuromuscular activity.

Eccentric knee flexion torque

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needed to clarify the potential contribution of neuromuscular inhibition to MSI recurrences

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