820517
research-article2019
SPHXXX10.1177/1941738118820517Cristi-Sánchez et alSports Health
vol. 11 • no. 2 SPORTS HEALTH
Patellar and Achilles Tendon Stiffness
in Elite Soccer Players Assessed Using
Myotonometric Measurements
Iver Cristi-Sánchez, PT,*† Claudia Danes-Daetz, PT,‡ Alejandro Neira, PT,† Wilson Ferrada, PT,§
Roberto Yáñez Díaz, MD,§ and Rony Silvestre Aguirre, PT, MSc§
Background: Tendon overuse injuries are an issue in elite footballers (soccer players) and may affect tendon function.
Achilles and patellar tendinopathy are the most frequent pathologies. Tendon stiffness, the relationship between the force
applied to a tendon and the displacement exerted, may help represent tendon function. Stiffness is affected by training and
pathology. Nevertheless, information regarding this mechanical property is lacking for elite soccer athletes.
Hypothesis: Achilles and patellar tendon stiffness assessed using myotonometric measurements will be greater in elite
soccer athletes than in control participants.
Study Design: Cross-sectional study.
Level of Evidence: Level 4.
Methods: Forty-nine elite soccer athletes and 49 control participants were evaluated during the 2017 preseason. A
handheld device was used to measure Achilles and patellar tendon stiffness. Dominant and nondominant limbs were
assessed for both groups.
Results: A significantly stiffer patellar tendon was found for both the dominant and the nondominant limb in the elite soccer
athletes compared with the control group. Nevertheless, no differences were found in Achilles tendon stiffness between
groups. When comparing between playing positions in soccer athletes, no significant differences were found for both tendons.
Conclusion: Greater patellar tendon stiffness may be related to an improvement in force transmission during muscle
contraction. On the other hand, it seems that after years of professional training, Achilles tendon stiffness does not change,
conserving the storing-releasing function of elastic energy. The nonsignificant differences between positions may be
attributable to the years of homogeneous training that the players underwent.
Clinical Relevance: The present study shows another technique for measuring mechanical properties of tendons in soccer
athletes that could be used in clinical settings. In the future, this technique may help clinicians choose the best exercise
protocol to address impairments in tendon stiffness.
Keywords: tendon stiffness; elite soccer athletes; soccer; myotonometric measurements; patellar tendon; Achilles tendon
F
ootball (soccer) is the world’s most popular sport, with in soccer athletes, possibly resulting from the high demands on
approximately 265 million players worldwide.13 Injuries in speed and power for the leg extensors30; ankle and knee
soccer are common, with a rate of 2.6 injuries per match sprains and hamstrings strains show a higher prevalence (32.2%
being reported during international elite tournaments.23 and 18.1%, respectively).1 Patellar tendinopathy can result from
Particularly, overuse injuries are a major problem in soccer, long-standing absence from competition.5 On the other hand,
accounting for almost one-third of the injury incidence.37 A Achilles tendon (AT) injuries are also common, and it has been
prevalence of 13.5% for patellar tendinopathy has been reported shown that 96% of AT injuries correspond with
From †Escuela de Kinesiología, Facultad de Ciencias, Universidad Mayor, Santiago, Chile, ‡Laboratorio Integrativo de Biomecánica y Fisiología del Esfuerzo, Escuela de
Kinesiología, Facultad de Medicina, Universidad de los Andes, Santiago, Chile, and §Clínica MEDS, Santiago, Chile
*Address correspondence to Iver Cristi-Sánchez, PT, Universidad Mayor, Chile, Camino La Piramide 5750, Huechuraba, Santiago, Chile 8580000 (email: [email protected]).
The authors report no potential conflicts of interest in the development and publication of this article.
DOI: 10.1177/1941738118820517
© 2019 The Author(s)
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Cristi-Sánchez et al Mar • Apr 2019
Table 1. Demographic characteristics by groupa
Elite Soccer Players Control Group
(n = 49) (n = 49) P
Age, y 24.59 (5.22) 25.90 (3.86) 0.16
Mass, kg 73.94 (6.27) 74.04 (8.19) 0.94
Height, m 1.76 (0.06) 1.75 (0.08) 0.44
2
Body mass index, kg/m 23.67 (0.98) 24.01 (1.76) 0.24
a
Demographic characteristics by group are presented as mean (SD). No significant intergroup differences (P > 0.05) were observed.
tendinopathy.17,22 Thus, tendon pathology appears to be of The main aims of this study were to describe the mechanical
importance in elite soccer athletes. properties (stiffness) of the PT and AT in elite soccer athletes
Tendons are responsible for transmitting force produced by using myotonometric measurements and to compare the results
muscles and for storing and releasing elastic energy during with a healthy control group. A second aim was to compare PT
movement.34 This double function is highly important during the and AT stiffness between playing positions among the soccer
muscle-tendon interaction, allowing for efficient functioning of athletes. Data regarding tendon stiffness could be used to
the muscle-tendon complex (MTC) in human movements.16,33 improve training program design, to create prevention strategies
Tendon function can be assessed mechanically through the use in overuse tendon injuries, and to optimize rehabilitation in
of dynamometry combined with ultrasonography, known as “in tendon pathology.
vivo” assessment.42 Stiffness, the relationship between the force
applied to a tissue and the displacement exerted, is one of the Methods
mechanical properties most reported in tendon function Participants
assessment in either passive15 or active conditions.25 Tendon
stiffness has been widely used to represent changes in the A total of 49 elite soccer athletes were recruited during the
mechanical properties of tendons after training or in the offseason from 3 different soccer clubs. Players underwent a
presence of pathology. Greater stiffness values have been found clinical interview to determine eligibility. Participant inclusion
in participants who underwent short-term–specific load-training criteria included the following: normal training regimen in the
programs.3,43 Moreover, stiffer tendons have been found in past 6 months, and no history or symptoms of PT and AT or
athletes who have been training for years (ie, long-term training), surgery. Exclusion criteria were as follows: history of quadriceps
highlighting that tendons adapt to short- or long-term training and triceps sural muscle strain in the past 6 months, and history
regimens.20 Alterations of mechanical properties have also been of knee or ankle surgery in the past year. A group of 49 healthy
found in pathological stages such as tendinopathy. Patellar participants was also recruited using the following inclusion
tendon (PT) and AT pathologies have shown lower stiffness criteria: not having been an elite athlete, and no history or
values than those for normal tendons, which affects the symptoms of PT and AT. The exclusion criteria for this second
transmission of force through the tendon.2,7 Although muscle group were as follows: history of quadriceps and triceps sural
force production may be normal, altered transmission may affect muscle strain in the past 6 months, and history of knee or ankle
motor output.40 Therefore, assessment of tendon stiffness is surgery in the past year. Anthropometric characteristics for each
needed to understand tendon function during training adaptation group are provided in Table 1. All participants provided their
and to optimize rehabilitation in pathological stages. signed informed consent before participating in this study, which
Although dynamometry combined with ultrasonography is the was approved by the bioethics committee of the university and
gold standard to measure passive tendon stiffness, it is an conducted in accordance with the Declaration of Helsinki.
expensive and operator-dependent technique that can only be
used in laboratory settings. Recently, another technique has Outcomes
been reported that evaluates the mechanical properties of The PT and AT were assessed using myotonometric
tendons.9,11 Myotonometric measurement is a noninvasive and measurements with the MyotonPRO device (Myoton Ltd). The
painless technique based on free oscillation theory where a measuring method of the device is based on the free oscillation
brief mechanical impulse is realized over the skin using a technique, where the following steps occur during a single
probe, and parameters, such as stiffness, can be obtained.12 measurement: (1) the device is placed perpendicular to the skin
Nevertheless, studies that used myotonometric measurements and a constant pre-pressure is applied for compressing the
have mainly measured muscle properties,19,36 and only a few subcutaneous tissue; (2) a brief mechanical impulse is applied,
have measured tendon stiffness.39 Hence, more studies assessing causing damped oscillation of the tissue; and (3) the
tendon stiffness by myotonometric measurements are needed. co-oscillation generated in the tissue is recorded by an
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vol. 11 • no. 2 SPORTS HEALTH
was repeated 3 times per extremity. Only measures that had a
coefficient of variation lower than 3% were considered;
otherwise, the measured was repeated. The dominant limb was
selected as the one used for kicking the ball.4
Statistical Analysis
Sample size was calculated based on a difference of 139 N/m in
PT stiffness between athletes and control participants from
previous studies that took place in our laboratory. This is
equivalent to a moderate effect size (0.75) using an α = 0.05
and β = 0.20, and a sample size of 30 participants per group
was required.38 Since estimates on this outcome were not
available in the literature, we decided to be conservative, and
thus we recruited 49 participants per group.
Statistical analyses were performed using SPSS v 20.0 software
(IBM Corp). The Shapiro-Wilk test was applied to determine the
normality of data. Means and SDs were used to describe the
obtained data. Unpaired t tests were used for between-group
comparisons, and paired t tests were used for within-group
Figure 1. Obtained filtered acceleration curve. Displacement comparisons. A 1-way analysis of variance was performed to
and velocity curves are obtained by double integrating the compare AT and PT stiffness between playing positions of the
acceleration curve. (Reproduced with permission from soccer athletes. The Bartlett test was applied to analyze the
MyotonPRO User Manual.) equality of the variance. Goalkeepers were excluded from this
analysis because of the small sample size. The level of
significance was set at α = 0.05.
accelerometer. The raw signal is then processed to filter the
Results
frequencies that are not characteristic of the tissue’s natural
oscillation, and finally, the filtered acceleration curve is used to PT Stiffness
calculate the mechanical and viscoelastic properties of the PT stiffness in elite soccer athletes was 1138.0 ± 215.5 and
tissue.18 Further information regarding the free oscillation theory 1118.0 ± 199.1 N/m for the dominant and nondominant limbs,
can be found in the study by Ditroilo et al.12 respectively (Figure 3). PT stiffness for healthy controls was
From the obtained filtered signal, stiffness can be 897.7 ± 190.1 and 871.1 ± 178.5 N/m for the dominant and
mathematically inferred from the filtered curve. Stiffness was nondominant limbs, respectively (Figure 3). Significant
obtained as follows: differences were found between groups for the dominant (P =
0.0001) and nondominant limbs (P = 0.0001). No significant
a0 × mProbe ;
Stiffness = differences were found for the within-limb comparison in each
∆l group (elite soccer athletes, P = 0.336; healthy controls, P =
where a0 is the maximal acceleration of the curve (first 0.210).
negative peak), mProbe is the mass of the measurement
mechanism (probe), and ∆l is the maximal displacement of the AT Stiffness
tissue (Figure 1), obtained by double integration of the AT stiffness in elite soccer athletes was 1075.0 ± 100.8 and
acceleration curve. The MyotonPRO has good to excellent 1031.0 ± 115.9 N/m for the dominant and nondominant limbs,
test-retest reliability and has been established in previous respectively (Figure 3). AT stiffness for healthy controls was
literature.8,29 1098.0 ± 139.5 and 1072.0 ± 112.3 N/m for the dominant and
nondominant limbs, respectively (Figure 3). No significant
Design and Procedures differences were found in the between-group comparison for
Measures were performed during the preseason (January- the dominant (P = 0.220) and nondominant limbs (P = 0.054)
February 2017), and all measurements were conducted at the (Figure 3). Additionally, no significant differences were found in
MEDS Clinic. The anatomical landmark for the PT stiffness the within-limb comparison in each group (elite soccer athletes,
assessment was 3 cm below the inferior pole of the patella. The P = 0.051; healthy controls, P = 0.096).
participants sat with their knees flexed to 90° (Figure 2A). For
AT, the measure point was 4 cm above the distal insertion of the AT and PT Stiffness by Position
tendon (ie, calcaneal tuberosity). The participants lay prone No significant differences were found for PT and AT stiffness
with their ankles in a neutral position (approximately 90°) values between playing positions of the soccer players
(Figure 2B). For both tendons, the myotonometric evaluation (Table 2).
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Cristi-Sánchez et al Mar • Apr 2019
Figure 2. Patellar tendon and Achilles tendon assessment. (a) Position of the participant during stiffness assessment of the patellar
tendon. Players were relaxed and sat with their knees in 90° of flexion. (b) Position of the participant during stiffness assessment of the
Achilles tendon. Players were relaxed and lay on a stretcher with their ankles in neutral position (approximately 90°).
Figure 3. Patellar tendon and Achilles tendon stiffness for both groups, football (soccer athlete) and control. Significant intergroup
differences (*P < 0.05) can be observed.
Table 2. Patellar tendon and Achilles tendon stiffness by positiona
Goalkeepers Defenders Midfielders Strikers
Tendon Dominance (n = 4) (n = 17) (n = 16) (n = 12) F P
Patellar tendon Dominant 1349 (163.2) 1143 (241.3) 1051 (179.9) 1179 (193.4) 1.46 0.24
stiffness (N/m)
Nondominant 1120 (130.3) 1128 (189.4) 1074 (226.7) 1163 (201.9) 0.67 0.51
Achilles tendon Dominant 1136 (76.7) 1107 (117.5) 1043 (87.27) 1052 (84.8) 2.01 0.14
stiffness (N/m)
Nondominant 1086 (99.7) 1042 (126.9) 1000 (114.2) 1039 (109.2) 0.62 0.54
a
All values are presented as mean (SD). No significant differences (P > 0.05) can be observed for the comparison between playing positions.
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vol. 11 • no. 2 SPORTS HEALTH
Discussion observed along with elongation of the AT.21,24 Also, during the
stance phase of running and a squat-jump task, shortening of
The aim of this study was to describe PT and AT stiffness in elite the gastrocnemius fascicles (ie, concentric contraction) and AT
soccer athletes and to compare these results with a control elongation have been observed.31,32 These behaviors optimize
group. The results indicate that elite soccer athletes have stiffer the mechanical function of the triceps surae MTC by 2
PTs than controls in both limbs—dominant and nondominant. mechanisms: (1) AT elongation allows efficient storage and
However, AT stiffness seems to be similar for both groups. release of elastic energy, and (2) no elongation of muscular
Previous studies have evaluated AT stiffness in karate fascicles enables them to work in the most efficient zone of the
competitors and reported lower AT stiffness values than those force-velocity curve.16 Hence, no changes in AT stiffness for the
obtained in the present study.39 A possible reason for this may elite soccer athletes compared with controls may mean that this
be the different mechanical demands exerted in karate and mechanism of interaction is maintained between fascicles and
soccer. Thus, mechanical adaptation of tendons may be different. tendinous tissue. Thus, other adaptations (eg, neuromuscular
adaptations) may play a key role in the maintenance of this
PT Stiffness mechanism.
Elite soccer athletes showed greater PT stiffness values than the
AT and PT Stiffness by Position
control group. This could be explained by the well-documented
phenomenon of tendon adaptation to training.3,43 Previous Statistical analysis showed no significant differences in AT and PT
studies using in vivo assessment have shown stiffer PT values stiffness between playing positions among the soccer athletes.
after short-term training regimens (12 weeks).26,35 Similar results Physical demands and position characteristics have been reported
have been reported in long-term training.20 Although there is no to be different from one another. It has been shown that midfield
clear training modality (eg, resistance, plyometric, or endurance) players cover significantly greater distances and display higher
that contributes less/more to this stiffening process, it seems to work rates than players in other positions.10 Although players in
be a homogeneous adaptation over time. Moreover, the PT has other positions may display different physical demands, the loads
been described as a transmission force tendon rather than an and the training dosage that they were subjected to during years
elastic energy store-release tendon.6 Elite soccer athletes are of professional training would be the same. This means that, from
subjected to long-term training, including the aforementioned a purely mechanical perspective, it can be hypothesized that both
different training modalities. Thus, PT stiffening seems to be an tendons adapted to similar mechanical demands after long-term
adaptation process that may enhance force transmission and training.20 Therefore, the observed stiffness values may be
sports performance. Therefore, myotonometric measuring seems enough to fulfill the physical demands of soccer, even if there are
to show a sensitivity to changes in PT stiffness, and the differences in work rates between playing positions. Overall, the
presented adaptations were similar to those reported in the differences in physical demands of each position (ie, different
literature. loads and workrates) may not influence the stiffness of both
tendons, resulting in similar tendon stiffness throughout the
AT Stiffness different playing positions.
No differences were found in AT stiffness between groups.
Evidence related to AT adaptation after training (short term or Strengths and Limitations
long term) and its relationship with performance in different Nowadays, the widely accepted methods for measuring tendon
disciplines is controversial. A few studies have reported that mechanical properties are dynamometry and ultrasonography.42
long-distance runners with the best records in a 5000-m race The present study shows another technique that could be used
presented lower AT stiffness values than those with the worst in the clinical setting and may help clinicians in deciding the
records.27,28 Nevertheless, other studies have shown that middle- best exercise protocol to address impairments in tendon
and long-distance runners with the best running economy or stiffness. Moreover, the obtained AT and PT stiffness values
the best records had stiffer ATs.14,41 Thus, there is no clear could be used as normative values, especially to compare
relationship between AT stiffness and performance. Because of pathological stages (ie, tendinopathy).
the nature of the triceps sural MTC and its function in the There are 2 main limitations to the present study. First, the
storing and releasing of elastic energy, no difference in AT cross-sectional study design did not allow measurement of PT
stiffness may facilitate this function, and it could be explained and AT adaptation to training and changes associated with
by the interaction between muscle and tendon during pathology. Prospective studies using this method are needed for
movement. a better understanding of the mechanical properties of the
The interaction of muscle and tendon during human tendon. Second, the estimated sample size may influence the
movement is complex. To understand the nature of the MTC it results of the present study. No previous study has measured PT
is necessary to distinguish the changes in the fascicle and or AT stiffness in elite soccer athletes; thus, the estimated
tendon length through different movements.16 In particular, the sample size may influence the obtained nonsignificant
triceps sural MTC has been widely studied in different tasks, differences for the within-limb comparisons as well as those
such as gait, running, and jumping. During the stance phase of between playing positions. Future studies should use a larger
gait, an isometric contraction of the gastrocnemius fascicle was sample size.
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Cristi-Sánchez et al Mar • Apr 2019
Conclusion early return to play: an 11-year follow-up of the UEFA Champions League injury
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