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ARTICLE IN PRESS

Manual Therapy 13 (2008) 411–418


www.elsevier.com/math

Original Article

Alterations of stiffness and resting position of the elbow joint


following flexors resistance training
Juliana M. Ocarinoa,, Sérgio T. Fonsecab, Paula L.P. Silvac, Marisa C. Mancinib,
Gabriela G.P. Gonc- alvesd
a
Centro Universitário de Belo Horizonte UNIBH, Doctor Student Rehabilitation Science Program, Federal University of Minas Gerais – UFMG, Brazil
b
School of Physical Education, Physical Therapy and Occupational Therapy – UFMG, Brazil
c
Doctor Student Center for the Ecological Studies of Perception and Action, University of Connecticut, USA
d
Master Student Rehabilitation Science Program – UFMG, Brazil
Received 6 November 2006; received in revised form 2 March 2007; accepted 14 March 2007

Abstract

Skeletal muscles adapt their length and stiffness according to the functional demands to which they are regularly submitted. The
modification of muscle stiffness and length induced by resistance training can alter joint stiffness and, theoretically, change joint
resting position.
Thirty subjects, randomly assigned to two groups, were submitted to a resistance training of the elbow flexor muscles of the non-
dominant arm. This training was performed in the inner range in group 1 and throughout the complete range of motion in group 2.
The dominant arm of each subject was considered the control. A biomechanical model of a hybrid mass–spring pendulum was used
to estimate the elbow joint stiffness and the elbow resting position was assessed using a standard goniometer.
There was a significant increase in joint stiffness of the experimental arm after complete range of motion training, which was not
observed after the training performed in inner range. The resting position of the experimental arm was modified to a significantly
greater flexion angle in both groups. No change was observed after resistance training in the control arm.
The results showed that modifications in joint stiffness seem to depend on the volume of work imposed to skeletal muscles.
In addition, both models of resistance training changed, through different mechanisms, the elbow joint resting position. These
findings suggest that posture and joint stability may be modified by specific strengthening protocols.
r 2007 Elsevier Ltd. All rights reserved.

Keywords: Stiffness; Muscular hypertrophy; Resting position; Equilibrium Point Hypothesis

1. Introduction dysfunctions (Gossman et al, 1982; Sahrmann, 2002).


However, it is still not clear how joint stiffness can be
Modifications in the structure and properties of the modified, and the influence of this modification in
skeletal muscles are proposed to result from adaptation postural alignment.
to particular demands imposed to them (Herbert, 1988). Muscle or joint stiffness represent the resistance
There is evidence that modifications in muscle length offered by these structures to their displacement or
and stiffness may be associated with joint instability and deformation (Latash and Zatsiorsky, 1993). Joint
postural deviations commonly observed in movement stiffness is given by the stiffness of the muscles and
passive tissues (capsule, ligaments) that cross the joint
Corresponding author. Rua Progresso 234/501. Padre Eustaquio, (Obusek et al, 1995). The relation between joint or
Belo Horizonte, Minas Gerais 30720320, Brazil.
muscle stiffness and joint position can be modeled
Tel.: +55 31 34138816. through the Equilibrium Point Hypotheses of movement
E-mail address: julianaocarino@terra.com.br (J.M. Ocarino). control (Feldman, 1986; Bizzi et al., 1992). These models

1356-689X/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.math.2007.03.009
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propose that the angle of a joint depends on the resting The objective of this study was to investigate
length and stiffness of the muscles around the joint. As modifications in joint stiffness and resting position of
the stiffness of the muscles can influence the joint’s the elbow joint after progressive resistance training of
position, the Equilibrium Point Hypothesis could also the elbow flexor muscles performed in the inner range
be applied as a model to understand modifications in and throughout the complete range of elbow flexion.
postural alignment. However, changes in postural In addition, this study investigated if there was any
alignment through changes in muscle stiffness and difference between these two models of progressive
length still remain highly speculative, as it is not well resistance training in relation to the gains obtained in
known the type of clinical intervention needed to effect stiffness and resting position of the elbow joint after the
such changes. training period.
Modifications in muscle length and stiffness have
been experimentally induced through immobiliza-
tion, electrostimulation and voluntary contraction 2. Methods
imposed to different muscle lengths (Williams and
Goldspink, 1978; Lynn et al., 1998). Increases in muscle 2.1. Subjects
stiffness can be obtained through increases in activat-
ion level (Feldman, 1986; Obusek et al., 1995) and Thirty subjects were randomly assigned to two
or through tissue modifications (Kovanen et al, 1984). groups. The group 1 (13 women and 2 men; mean age
There is evidence that resistance training increases 22.173 years; and mean body weight, 59.9710.3 kg)
the stiffness of the joint, muscles and tendons due undertook progressive resistance training of the elbow
to a production of contractile and non-contractile flexor muscles in the inner range. The subjects in group 2
proteins in the muscle (Chleboun et al., 1997; Reeves (12 women and 3 men; mean age, 21.0671.4 years; and
et al., 2003). Hence, resistance training not only mean body weight, 58.68711.2 kg) undertook progres-
increases the tension-generating capacity of the muscle, sive resistance training performed throughout the
but it seems to increase the stiffness of muscles and complete range of motion. In both groups, the non-
joints. dominant arm of each subject was used in training
Reduction in fiber length occurs not only when a (experimental arm). The dominant arm of each subject
muscle is immobilized in a shortened position but also was not trained and was used as a control to verify the
when it is forced to work within a reduced range of stability of the outcome measures. All subjects should
motion (Williams et al., 1988). For example, Williams not have been involved in any type of strengthening
et al. (1988) observed a significant reduction in serial program within the last 12 months and they should not
sarcomere number and an increase in muscle stiffness in have upper extremities pain or history of injury. The
the diaphragm muscle of hamsters that were forced to procedures of the study were explained to the subjects
work in a reduced range. In addition, several studies and informed consent was obtained. The University’s
that investigated adaptations of stiffness and length of Institutional Ethics Review Committee approved
skeletal muscles after immobilization or muscle activa- this study.
tion in shortened position verified a displacement of the
peak of the length-tension curve to the left, indicating a 2.2. Procedure
reduction in muscle fiber length (Witzmann et al., 1982;
Williams et al., 1988). These modifications in length and Initially, the subjects were weighted using a balance
stiffness were more evident when the position in which scale and the length of the forearm (elbow axis to ulnar
the muscle was held was associated with muscular styloid) and hand (wrist axis to knuckle II middle finger)
contraction. were measured with a measuring tape. During elbow
Adaptive modifications in muscle stiffness and length stiffness evaluation, the electromyographic (EMG)
seem to happen as a consequence of the functional activity of the biceps and triceps brachium muscles were
demands to which the muscles are submitted (Herbert, recorded to guarantee that any modification in elbow
1988; Savelberg and Meijer, 2003). According to Goss- stiffness was not due to increases in muscular activation
man et al. (1982), the greater reduction in serial level, but a result of training. Active surface electrodes
sarcomere number with increase in muscle stiffness were placed over these muscles after skin preparation
occurs when muscles contract while in shortened (Cram and Kasman, 1998). Data were collected
position (inner range). Hence, a resistance training at a frequency of 1000 Hz by an electromyographer
performed in inner range would have a greater potential MP100WSW (Biopac System).
to induce adaptive changes in stiffness, muscle length,
and theoretically, in resting position of a joint when 2.2.1. Evaluation of joint stiffness
compared to training performed in the complete range Elbow joint stiffness was evaluated through rhythmic
of motion. oscillations of the forearm and hand segments about the
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elbow joint, assuming a behavior consistent with an 2.2.2. Evaluation of resting joint position
escapement driven hybrid mass–spring pendulum model The subjects were instructed to stay in the same
(Kugler and Turvey, 1987). In order to perform the position as before and place their arm as comfortable as
oscillations in the frontal plane, the subjects were seated possible, on the armrest. As soon as the subjects were
in the chair of an isokinetic dynamometer (Biodex completely relaxed, the elbow joint angle was measured
System 3 Pros). The arm of each subject was positioned using a standard goniometer (test–retest reliability ICC
in an armrest placed proximal to the elbow joint (Fig. 1). of 0.94, SEM of 0.71) and the value obtained was used
An electrogoniometer (TSD 130s Biopac System) was to represent the resting position of this joint. The mean
placed with adhesive tape on the upper limb of the of three measures was considered for analyses. The
subjects, crossing the elbow joint and calibrated follow- same examiner performed the pre- and post-training
ing the manufacturer’s instructions. This equipment evaluations.
recorded the cycles of oscillation performed during
stiffness evaluation. The subjects were instructed to 2.2.3. Evaluation of the maximum voluntary isometric
oscillate the forearm and hand about the elbow joint contraction (mvic)
simulating a pendulum movement. The oscillation was In order to evaluate the MVICs of the biceps and
performed in a smooth and comfortable manner without triceps brachium muscles, the subjects were seated in the
pauses and considered as the natural frequency of arm dynamometer with their arm supported in the same way
oscillation. The correct motion was demonstrated to the described for stiffness evaluation. The elbow joint was
subjects and a maximum of 5 min of training were positioned at 1201 and 151 of elbow flexion for biceps
allowed before data collection. and triceps brachium evaluation, respectively. The
The cycles of oscillation and EMG signals were subjects were instructed to perform three maximum
collected during 20 sec after natural frequency was isometric contractions of each muscle with duration of
achieved and minimal EMG activity and stability of 6 s. The EMG signals were recorded during the MVIC
the amplitude of oscillation cycle were observed. Pairs of tests and the 2 s of highest activity in each trial were
photoelectric cells were placed at each side of the processed. The highest value of the three trials was used
oscillating arm to guarantee that angular displacement to normalize the EMG activity.
during the swing task did not exceed 201. Oscillations
with amplitudes above this limit were not accepted to 2.2.4. Resistance training program
allow the use of a linearized equation of motion of the All subjects were submitted to a progressive resistance
pendulum. Five measures were obtained for each arm training program (Kraemer et al, 2002). The protocol
with one minute of rest between them. The highest and involved three sets of eight repetitions with an intensity
lowest frequency values were discarded and the mean of of 80% of one maximum repetition and two minutes of
the three remaining measures was considered for further rest between sets. This training was performed three
analyses. Test–retest reliability of this method was times a week for eight weeks. This protocol was chosen
assessed in 10 subjects, with a time interval between to guarantee a sufficient stimulus to produce muscle
test–retest of 24 h. An intra-class correlation coefficient hypertrophy (Kraemer et al, 2002). When each subject
(ICC) of 0.98 was obtained with a standard error of performed one repetition over the established number in
measurement (SEM) of 0.022. all sets and in two consecutive training sessions the load
was increased by approximately 10%. Group 1 was
submitted to a resistance training of the elbow flexor
muscles of the non-dominant arm in the last 401 of the
elbow flexion movement (part of the range in which the
muscles work in shortened position). During this
training, the subjects were seated with their trunk bent
forward and a support was used to guarantee that the
exercise was performed in the desired amplitude (Fig. 2).
The elbow flexor muscles of the non-dominant arm of
group 2 were submitted to resistance training in the
complete range of elbow flexion. This training was
performed with the subjects standing, leaning against a
wall, with their knees slightly bent (Fig. 3).
After eight weeks of training, all subjects were
submitted to stiffness, resting position and MVIC
evaluations following the same procedures described
before. The examiner was blinded in relation to group
Fig. 1. Positioning of the subjects during stiffness evaluation. and measures obtained in the pre-training evaluations.
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biomechanical model of an escapement driven hybrid


mass–spring pendulum (Kugler and Turvey, 1987). The
calculation of elbow stiffness was performed using the
resonant equation (1) that describes the relationship
between the parameters of the model and its frequency
of oscillation (Kugler and Turvey, 1987)
Kb2 ¼ ðmL2e Þo2  mLe g, (1)
2
where Kb represents the elastic torque produced by the
muscles and connective tissue around the elbow joint, o
is the angular frequency of oscillation, m is the total
mass, Le is the length of the simple pendulum equivalent
to the pendulum composed by the forearm and hand,
and (g) gravitational acceleration. Any modification
in the elastic torque represents modifications in stiff-
ness (K).
Fig. 2. Positioning of the subjects during training performed in the
Estimates of forearm and hand masses, location of the
inner range of motion.
center of mass and radius of gyration of each segment
were calculated using Dempster’s anthropometrical
table (Winter, 1990). These estimates were used to
calculate the simple pendulum equivalent length using
the parallel axis theorem (Kugler and Turvey, 1987).
Mass and length of the pendulum were used to calculate
the gravitational torque (mLeg) for each subject. The
time to perform 10 cycles of oscillation during the
stiffness test was used to obtain the natural frequency of
oscillation of the simple pendulum equivalent.
Since joint stiffness is not independent of the mass
and length of the segments (Obusek et al., 1995), to
avoid the effects of anthropometrical differences, elastic
torque was divided by gravitational torque to obtain a
normalized stiffness variable, allowing comparison of
the experimental arms of subjects from different groups.
EMG data processing was performed using the
software (Biopac System, USA). The signals obtained
from the biceps and triceps brachium muscles during
stiffness and MVIC tests were low-pass and high-pass
filtered with cut-off frequencies of 500 and 10 Hz,
respectively, and full wave rectified. Root mean square
(RMS) value was calculated for each muscle. In order to
normalize the EMG signals, the RMS value of each
muscle recorded during the stiffness test was divided by
the highest RMS value obtained during the MVIC test
of same muscle and subject. Biceps and triceps muscles
EMG activities were added to obtain total EMG activity
variable.
Fig. 3. Positioning of the subjects during training performed in the
complete range of motion.
2.4. Data analysis

The subjects were not informed about the study’s Repeated measures analyses of variance (ANOVA)
hypothesis. with one between-subject effect (group: models of
training) and two within-subject effect (arm: control
2.3. Data reduction and experimental; condition: pre- and post-training)
were used to evaluate differences between the means of
The oscillatory movement of the forearm and hand normalized stiffness, resting position of the elbow joint,
segments around the elbow joint was represented by a and total EMG activity. This procedure allowed the
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testing of the main effects group, arm and condition, as 3.2. Resting position of the elbow joint
well as interaction effects, with a level set at 0.05. Four
pre-planned focused contrasts were performed to locate The ANOVA demonstrated significant differences in
significant differences between control arm in pre- and elbow resting position only in the condition effect
post training conditions and between experimental arm (p ¼ 0.0001) and in the arm  condition interaction
in pre and post training conditions, in both groups. (p ¼ 0.0001). Contrasts analyses revealed a significant
Bonferroni corrections were performed to adjust the difference in elbow resting position of the experimental
level of significance to the number of focused contrasts. arm in groups 1 (p ¼ 0.0001) and 2 (p ¼ 0.0001). After
This procedure changed the a level to 0.0125. Indepen- both resistance training programs, the resting position
dent t-tests were used to test for significant differences of the elbow joint was modified to a significantly greater
between groups in the gain obtained in normalized flexion angle. There was no difference in the control arm
stiffness and in elbow resting position after resistance in group 1 (p ¼ 0.6318) or in group 2 (p ¼ 0.9990)
training. when pre- and post-training condition were compared.
The means, standard deviations and CI are illustrated in
Table 1.
The independent t-test did not show difference in
3. Results relation to the gain obtained in elbow resting position
variable (t ¼ 0.001, p ¼ 0.9719) when groups 1 (mean ¼
3.1. Normalized elbow stiffness (kb2/mlg) 8.731; SD ¼ 1.33) and 2 (mean ¼ 8.801; SD ¼ 1.90) were
compared.
The ANOVA demonstrated significant differences in
normalized elbow stiffness only between arms
(p ¼ 0.0001) and in the arm  condition interaction 3.3. Total electromyographic activity
(p ¼ 0.0178). Pre-planned contrast analyses showed a
significant increase in elbow stiffness of the experimental The ANOVA demonstrated significant differences
arm after complete range of motion training (group 2) only in condition effect (p ¼ 0.0020). The pre-planned
(p ¼ 0.0019). However, no difference was observed in contrast analyses showed a significant decrease in
elbow stiffness of the experimental arm after training activation level only in the experimental arm of the
performed in inner range of motion (group 1) group 2 (p ¼ 0.0009). No other difference in total
(p ¼ 0.1264). There was no difference in normalized electromyographic activity was observed (p40.0274).
stiffness of the control arm between pre- and post- The means, standard deviations and CI are illustrated in
training condition, in group 1 (p ¼ 0.9222) and in group Table 1.
2 (p ¼ 0.9443). The means, standard deviations and
confidence intervals (CI) are illustrated in Table 1. 4. Discussion
The independent t-test did not show any difference in
relation to the gain obtained in elbow stiffness after The results of the present study demonstrated that
the resistance training (t ¼ 1.099, p ¼ 0.3035) when elbow joint stiffness could be modified through resis-
groups 1 (mean ¼ 0.07; SD ¼ 0.07) and 2 (mean ¼ 0.15; tance training of elbow flexor muscles. Increase in elbow
SD ¼ 0.08) were compared. stiffness related to the pre-training condition was

Table 1
Means (standard deviation), mean differences (confidence intervals of 99%) of normalized stiffness, resting position of the elbow joint, and total
EMG activity variables for control and experimental arms in groups 1 and 2

Arm Variable Group Pre Post Mean differences (CI)

Experimental Normalized 1 0.402 (0.274) 0.472 (0.224) 0.07 (0.17 to 0.03)


Stiffness 2 0.397 (0.321) 0.549 (0.286) 0.15 (0.36 to 0.06)
Resting 1 54.1 (5.6) 62.8 (4.2) 8.73 (12.2 to 5.23)
Position (1) 2 52.7 (8.4) 61.5 (5.0) 8.8 (13.15 to 4.45)
Total EMG 1 0.032 (0.017) 0.024 (0.013) 0.008 (0.001 to 0.02)
Activity 2 0.034 (0.029) 0.019 (0.01) 0.015 (0.01 to 0.04)
Control Normalized 1 0.368 (0.272) 0.363 (0.280) 0.004 (-0.14 to 0.15)
Stiffness 2 0.327 (0.250) 0.330 (0.233) 0.003 (0.14 to 0.14)
Resting 1 56.7 (5.2) 57.1 (4.9) 0.47 (3.61 to 2.67)
Position (1) 2 55.5 (7.7) 55.5 (5.0) 0.000 (3.52 to 3.52)
Total EMG 1 0.028 (0.022) 0.019 (0.010) 0.009 (0.01 to 0.03)
Activity 2 0.031 (0.025) 0.023 (0.019) 0.008 (0.001 to 0.02)
 significant difference (po0.0125).
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observed only when the training was performed post-training conditions were compared. Although
throughout the complete range of motion, although significant increases in joint stiffness were observed only
there was no difference between groups. In addition, the after complete range of motion training, there was no
results demonstrated that resistance training, indepen- significant difference between the two resistance training
dent of work range, modified the resting position of the models in relation to the gain in joint stiffness.
elbow joint. The results of this study indicated that the resting
The increase in elbow joint stiffness observed in the position of the elbow joint was modified to a greater
experimental arm after complete range of motion flexion angle after both resistance training models. In
training is in agreement with evidences of increased the experimental arm of group 2, the modification in
stiffness in individuals submitted to muscular training elbow resting position was possibly caused by increases
(Chleboun et al., 1997). The greater volume of work in muscle stiffness. Applying the equilibrium point
induced by the complete range of motion training has model, increases in the stiffness of flexor muscles,
probably been sufficient to promote an increase in showed by an increase in the slope of the line
muscle mass and, consequently, in muscle stiffness. representing its torque–angle relationship, changes the
Although muscular volume was not measured in this location of the crossing point between the two slopes
study, there is evidence that resistance training per- (resting joint position) to a greater flexion angle
formed during six weeks is enough to promote (Fig. 4a). The experimental arm of the group trained
significant increases in the muscles’ cross sectional area in inner range also presented a modification in the
(Kraemer et al., 2002). The increase in joint stiffness resting position. However, in this group, there was no
observed in the experimental arm of group 2 cannot be increase in joint stiffness, which suggests that another
explained by modifications in activation level of the mechanism might have been responsible for the mod-
assessed muscles, since there was a significant decrease ification observed in elbow resting position. There is
in total EMG activity in this arm. In addition, the lack evidence that when muscles contract in a shortened
of differences in elbow stiffness in the control arm position there is a reduction in their number of
between pre- and post-training conditions reinforced the sarcomeres in series with consequent displacement of
idea that the increase in joint stiffness observed in the the length-tension curve to the left (Williams et al.,
experimental arm of group 2 was produced by the flexor 1998). According to the equilibrium point model, a
muscles resistance training. decrease in muscle length, represented by displacement
The increase in elbow stiffness observed after resis- of the line to the left also has the potential to modify the
tance training performed in the inner range was not location of the crossing between the slopes (Fig. 4b).
significant. Several studies have investigated the effect of Hence, a possible mechanism that could explain the
muscular contraction in a shortened position and change in elbow resting position to greater flexion angle
demonstrated increases in muscle stiffness (Williams would be a reduction in the number of sarcomeres in
et al., 1998; Gunst and Wu, 2001). However, these series. While the equilibrium point hypothesis was
studies were carried out with animals and did not proposed to investigate the control of voluntary move-
measure joint stiffness. In the present study, the lack of ments, the present study demonstrated that it is possible
significant differences in elbow joint stiffness in the to use this concept to explain modifications in the
experimental arm after training suggests that the volume resting position of a joint due to modifications in
of muscular work imposed in inner range training did the passive characteristics of a muscle, such as stiffness
not promote the hypertrophy necessary to modify joint and length.
stiffness. However, as the group 1 presented smaller The studies that have investigated adaptations in
effect size than group 2, the sample size might not have muscle length and number of sarcomeres in series,
been enough to allow the identification of significant resulting from immobilization or electrostimulation,
differences in joint stiffness in group 1 when pre- and showed that when muscle length decreases, there is a

Fig. 4. Graphic representation of modification in joint resting position according to Equilibrium Point Model where: FT: flexor torque; ET: extensor
torque; EP1: equilibrium point of the joint. (a) EP2: new equilibrium point of the joint due to increase of the flexors muscles stiffness (slope); (b) EP2:
new equilibrium point of the joint due to reduction of the flexors muscles length (displacement of the line to the left). Adapted from Bizzi et al. (1992).
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consequent increase in muscle stiffness (Williams and resting position of the elbow joint observed in the present
Goldspink, 1978). Although the modification in elbow study can be used in interventions with the objective of
resting position in individuals trained in the inner range producing or maintaining the adaptive remodeling
of motion suggested a change in flexors muscles length, process of the muscle to promote gains in joint stability
there was no significant increase in stiffness in this group. and postural modifications. However, more clinically
A limitation of the present study is related to the oriented studies are still needed to verify the effect of
biomechanical model used to estimate joint stiffness. changes in muscle stiffness and length on joint stability
This model involved oscillations of the forearm and hand and on corrections of postural disorders.
segments in short amplitudes, which allowed the assess-
ment of the stiffness only in the initial toe region of the
passive torque–angle curve. In this portion of the curve,
5. Conclusion
relatively low torques are required to move a joint. In the
passive torque–angle curve, there is another region
The present study demonstrated that elbow joint
named linear portion. In this region, joint stiffness
stiffness increased after muscular resistance training
rapidly increases with joint movement. Chleboun et al.
performed in complete range of motion, which was not
(1997) demonstrated that muscle volume influenced
observed after training performed in inner range.
elbow joint stiffness in the linear portion of the torque–
However, both resistance training models modified the
angle curve. Despite the documented association be-
resting position of the elbow joint to a greater flexion
tween muscle volume and stiffness in the linear portion
angle. In the group trained in the complete range of
of the curve, there is no evidence to support the motion, the elbow resting position was possibly changed
argument that changes in stiffness due to modifications
by increases in joint stiffness. The lack of significant
in muscle length are more evident in the toe region or in
increase in stiffness in the group trained in the inner
the linear portion of the torque–angle curve. Hence, if
range suggests that another mechanism, possibly a
increases in elbow stiffness caused by reduction in muscle
decrease in the number of sarcomeres in series, could
length were more expressive in the linear portion of
be responsible for the modification in resting position of
the torque–angle curve, these increases would not be
the elbow joint.
detected by the methodology used in the present study.
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