BJMB
Brazilian Journal of Motor Behavior
Special issue:
“Fatigue issue in the performance of motor skills”
!
Teruya et al.
2023
VOL.17
N.5
193 of 200
Fatigue effect on muscle coactivation during inversion movement in females with
chronic ankle instability
THIAGO T. TERUYA
1
| ALEX S. O. C. SOARES
2
| JULIO C. SERRÃO
1
| LUIS MOCHIZUKI
3
| ALBERTO C. AMADIO
1
1
School of Physical Education and Sport, University of São Paulo, São Paulo, SP, Brazil
2
Department of Physical Therapy, University of Taubaté, Taubaté, SP, Brazil
3
School of Arts, Sciences and Humanities, University of São Paulo, São Paulo, SP, Brazil
Correspondence to:!Thiago Toshi Teruya!
Laboratory of Biomechanics of School Physical Education and Sport, University of São Paulo, Av. Prof. Mello Moraes, 65 - Cidade Universitária, CEP: 05508-030 -
São Paulo SP.
email: thiago.teruya@alumni.usp.br
https://doi.org/10.20338/bjmb.v17i5.379
HIGHLIGHTS
Chronic ankle instability decreased muscle co-
activation in all muscle pairs.
Fatigue increased muscle co-activation in the FB- FL
muscle pair.
These results suggest that chronic ankle instability is an
unprotected factor to the ankle.
ABBREVIATIONS
ANOVA Analysis of variance
CAI Chronic ankle instability
CAIT Cumberland Ankle Instability Tool
EMG Electromyography
FB Fibularis brevis
FL Fibularis longus
GL Gastrocnemius lateralis
SENIAM Surface Electromyography for the Non-
Invasive Assessment of Muscles
TA Tibialis anterior
PUBLICATION DATA
Received 16 06 2023
Accepted 01 09 2023
Published 30 09 2023
BACKGROUND: An ankle sprain is a relevant public health issue. Fatigue changes the
neuromuscular response in people with chronic ankle instability (CAI).
AIM: To evaluate the muscle co-activation on people with chronic ankle instability using cross-
correlation analysis.
METHOD: Twenty-four healthy women were selected and divided into stability and instability
groups. Ankle sprain was simulated with a mechanical platform. Electrical muscle activity
(fibularis brevis, FB; fibularis longus, FL; gastrocnemius lateralis, GL; and tibialis anterior, TA)
and platform acceleration were recorded at 2KHz. Two sets of 8 right and eight left foot fall in
random order were performed before and after the fatigue protocol. Fatigue protocol ended
when the volunteer increased the test run time by 150% of the best round. Co-activation was
calculated with cross-correlation. Agonist-agonist (FB-FL, FB-GL, and FL-GL) and agonist-
antagonist (TA-GL, TA-FB, and TA-FL) pairs were evaluated. Statistical significance was
p<0.05.
RESULTS: Co-activation was lower for the instability group. Fatigue did not induce changes in
5 out of the 6 analyzed muscle pairs.
CONCLUSION: CAI is a factor of joint instability. Fatigue may not be relevant in altering joint
stability. Therefore, interventions should be focused on enhancing joint stability.
KEYWORDS: Biomechanics | Motor control | Electromyography | Sprain | Injury | Cross-
correlation
INTRODUCTION
Ankle sprains represent a significant public health concern. In the United State of America the incidence of ankle sprains is 2.1
per 1000 people per year
1
. Furthermore, one-fifth of the Australian population experiences chronic musculoskeletal ankle disorders
2
,
while 61% of soccer players suffer from recurrent ankle sprains
3
.
Ankle sprains lead to ankle instability due to impaired muscular strength, a limited range of dorsiflexion motion, and delayed
response of ankle muscles
4
. Persons with functional and mechanical ankle joint instability and history of two or more ankle sprains have
chronic ankle instability (CAI)
5
.
Muscle co-activation is a variable extracted from the electromyographic signal that can be related to the ability to stabilize a
joint. DeMers, Hicks, & Delp
6
suggested that preparatory muscle co-activation could prevent injuries in individuals with chronic ankle
instability (CAI). Lin, Chen & Lin
7
proposed that the co-activation of tibialis anterior and fibularis longus decreases in individuals with CAI;
Conversely, Suda, Amorim, & Sacco
8
demonstrated similar co-activation patterns in ankle muscles of individuals both with and without
ankle functional instability. Muscle co-activation is typically studied within agonist-antagonist muscle pairs
9,10
; However, it is possible to
classify muscle co-activation into three groups
11
: 1) antagonist co-activation, involving simultaneous activation of agonist and antagonist
muscles at the same joint; 2) synergistic co-activation, referring to muscles activating at the same joint to perform the same movement;
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
Teruya et al.
2023
VOL.17
N.5
194 of 200
Special issue:
Fatigue issue in the performance of motor skills
and 3) intramuscular co-activation, involving activation of different regions within the same muscle.
Fatigue alters the neuromuscular response in individuals with CAI. Fatigue impairs both physical and cognitive functions
through interactions between performance and perceived fatigue
12
. According to Gribble, Hertel, Denegar, & Buckley
13
, fatigue induced
by lower limb isokinetic exercises impairs balance control in individuals with CAI, particularly when swaying in different directions. The
performance on the Star Excursion Balance Test is impaired after fatigue in individuals with CAI
13
. However, fatigue resulting from
strength training, proprioception training, or their combination does not significantly affect quiet standing postural control in individuals
with CAI
14
. Therefore, does fatigue impact muscle co-activation in individuals with chronic ankle instability? To address this question, the
purpose of this study is to assess the effects of fatigue on muscle co-activation in individuals with chronic ankle instability. The hypothesis
posits that individuals with chronic ankle instability will exhibit reduced muscle co-activation during ankle inversion motion, and this
reduction will be more pronounced under conditions of fatigue.
METHODS
This study is an observational study. The University Ethical Committee (nº 133.682) granted approval for this study. All
participants were informed about the study's objectives, and they provided written consent to participate. The results of the CAIT test
were utilized to categorize the participants into respective groups.
Subjects
The participants included twenty-four healthy women, who were divided into two groups: a stability group (n=12; 24.2±5.5 years
old, 62.4±9.3 kg mass, 1.64±0.10 m tall) and an instability group (n=12; 21.3±2.8 years old, 60.8±11.1 kg mass, 1.62±0.10 m tall). The
inclusion criteria for the instability group were as follows: pain resulting from ankle sprain, edema, or abnormalities during locomotion;
experiencing episodes of ankle 'giving way' during daily activities or sports; sensations of joint instability; and a CAIT (Cumberland Ankle
Instability Tool) score of <24 points
5
; 18-40 years old; and indoor football player for at least 3 years. The inclusion criteria for the
experimental group were as follows: individuals aged between 18 and 40 years; indoor football players with a minimum of 3 years of
experience. For the control group, inclusion criteria were: absence of pain resulting from ankle sprain, edema, or abnormalities during
locomotion; no reported episodes of ankle 'giving way' during daily activities or sports; no sensations of joint instability; CAIT
(Cumberland Ankle Instability Tool) score >24 points
5
; individuals aged between 18 and 40 years; indoor football players with a minimum
of 3 years of experience. Exclusion criteria for both groups included: recent fractures or lower limb surgeries within the last six months;
presence of any vestibular or nervous system conditions; musculoskeletal injuries and acute ankle sprains (<1 month) that would hinder
the subject's ability to perform the test. The inclusion and exclusion criteria followed by our study were suggested by the study conducted
by International Ankle Consortium
5
.
In Table 1, CAIT scores are presented. In the instability group, Student's t-test indicated a significant difference in CAIT scores
between limbs (p=0.002). In the control group, CAIT scores were similar for both limbs (p=0.84).
Table 1. Mean and standard deviation of CAIT Score in both legs and both groups, as well as mean and standard deviation of the number of ankle
sprains. In the Instability group, CAIT 1 pertains to the affected limb, while CAIT 2 pertains to the healthy limb. In the control group, CAIT 1 corresponds
to the dominant limb, and CAIT 2 corresponds to the contralateral limb.
Group
CAIT 1
CAIT 2
nº of ankle sprains
Instability
18.5 ± 4.0
24.8±4.2
3.8±3.3
Control
28.1±1.6
27.9±2.6
0.6±0.7
Experimental setup
Participants stood on an inversion platform to undergo ankle inversion, constituting the inversion test. The participants were
unaware of which foot would be subjected to inversion, and the order of falls was randomized. The individual responsible for operating
the inversion platform was blinded to the groups. Surface electromyography (EMG) was used to measure the electrical activity of ankle
muscles, while a triaxial accelerometer recorded platform motion. The inversion test was conducted both before and after the fatigue
protocol.
Instruments
A mechanical platform (Figure 1) was employed to induce ankle inversion motion and simulate the motion associated with
ankle sprain. The setup of the inversion platform was designed based on the works of Myers, Riemann, Hwang, Fu, and Lephart
15
as
well as Karlsson, Peterson, Andreasson, and Högfors
16
. It consisted of two rectangular boards measuring 320 mm x 220 mm, mounted
on a foundation measuring 452 mm x 380 mm. These boards were linked by a hinge joint that facilitated a lateral inclination of 30º and
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
Teruya et al.
2023
VOL.17
N.5
195 of 200
Special issue:
Fatigue issue in the performance of motor skills
This is a safe angle that does not present any harm to the ankle joint
15,16
. An attached pedal drive for each board was utilized to initiate
this rotation.
Figure 1. Inversion platform simulating the ankle sprain movement.
Surface electromyography and accelerometry data were collected using a 16-bit 8-channel signal acquisition system (EMG-
800C, EMG System Brasil Ltda). Each channel was equipped with a common rejection module (>100 dB) and had an input impedance of
109 Ω. Acceleration and EMG signals were sampled at a rate of 2 kHz. For electromyography, disposable surface Ag/AgCl electrodes
were positioned 20 mm apart on each muscle (fibularis brevis, FB; fibularis longus, FL; gastrocnemius lateralis, GL; and tibialis anterior,
TA) as per the recommendations outlined by the Surface Electromyography for the Non-Invasive Assessment of Muscles (SENIAM)
protocol
17
. We collected data only from the dominant limb (control group) and the limb affected by CAI (instability group); however, the
electrodes were placed on both legs.
The data were processed using Matlab scripts (Matlab version R2015a). Raw EMG signals underwent initial filtering through a
20-500 Hz analog band-pass filter and were then pre-amplified by a factor of 100. The digitalized raw EMG signals were first demeaned,
followed by filtering through a 200 Hz 4th order low-pass Butterworth filter, and a notch filter (60 Hz and harmonics) Butterworth filter. The
rectified EMG signals were then normalized to 95% of the maximum signal amplitude. To determine the initiation and cessation of
platform motion, the platform's acceleration data was utilized. The accelerometer was affixed to the inversion platform, and the
acceleration signals were subjected to low-pass filtering (20 Hz 4th order Butterworth filter).
Procedures
Inversion test
Participants stood on the inversion platform and executed preliminary falls to acclimate to the equipment. To eliminate sensory
feedback, their eyes and ears were covered. Subsequently, a total of 16 randomized falls were executed for each lower limb.
Fatigue protocol
Participants engaged in the Modified Southeast Missouri Agility Drill
18
to induce muscular fatigue. This test entails a sequence
of forward sprints, lateral shifts, and reverse running. The course, measuring 3.6 x 5.7 m in a rectangular shape, included the following
sequence: a forward sprint, lateral shuffle to the right and then back, diagonal reverse running, followed by another forward sprint, lateral
shuffle to the left and then back, and a final diagonal reverse run to the opposite side where the circuit originated. After completing the
circuit, participants performed ten rapid countermovement jumps, as depicted in Figure 2.
Participants underwent this circuit three times to acquaint themselves with the routine and determine their preferred pace. Each
round was timed. Participants aimed to complete as many rounds as possible until the round time reached 150% of their best round
19
.
The time between rounds was 10 seconds, as determined by participants' subjective perception of exertion. Immediately after the fatigue
protocol (within a maximum of 1 minute), participants repeated the inversion test. The second inversion test was completed within 5
minutes to mitigate any potential fatigue recovery effects. These intervals are suggested to prevent significant recovery of the effects of
muscular fatigue
20
.