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Original Research

Sex Differences in Mechanical Properties of the Achilles Tendon: Longitudinal Response to Repetitive Loading Exercise

Lepley, Adam S.; Joseph, Michael F.; Daigle, Nathan R.; Digiacomo, Jessica E.; Galer, John; Rock, Emily; Rosier, Samuel B.; Sureja, Parth B.

Author Information
Journal of Strength and Conditioning Research: November 2018 - Volume 32 - Issue 11 - p 3070-3079
doi: 10.1519/JSC.0000000000002386
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Abstract

Introduction

The Achilles is one of the most commonly injured tendons in the human body (10,11), manifesting clinically as a chronic overuse disorder (tendinopathy) or an acute disruption of the tissue after degenerative changes (rupture) (15). Those at the greatest risk of injury include athletes who engage in strenuous physical activities that overload the tendon; with runners, soccer, volleyball, and basketball players demonstrating the highest occurrence rates (22,23). The increased risk of Achilles tendon injuries is likely attributed to the higher exposure to tissue overload comparative with other tendons, which can reach between 70 and 110 MPa during athletic tasks (17).

Tendons are able to adapt to mechanical loading; however, injury occurs when the tendon is no longer able to withstand the increase in mechanical loading during exercise. Acutely, passive stretching (2,21), isometric plantar flexion contractions (16), and resisted plantar flexion exercises (13) have been shown to significantly affect mechanical properties of the Achilles tendon, including decreases in tendon stiffness and modulus (28). Interestingly, muscle force seems to recover 30 minutes after isometric contractions have been completed; however, tendon stiffness remains decreased at this time (16). The chronically impaired mechanical properties of the tendon to resist external forces, in combination with the restoration of muscle force production, have clinical implications for tendon injury.

Lacking from many previous investigations is the comparison between sexes. Men are identified as having a greater risk of Achilles tendon rupture compared with women (approximately 70–80% of all ruptures occur in men (4,27)), likely due to the increased number of sports participants, hormonal differences, and an ability to generate higher muscle and tendon forces (8,27). Previous investigations (2,13,20) have demonstrated sex differences in mechanical properties of the Achilles tendon, indicating that women generate less muscle and tendon force, exhibit shorter tendon length and smaller cross-sectional area (CSA), and demonstrate less tendon stiffness and modulus compared with men. Furthermore, it has been reported that women show significantly greater responses to static stretching than men, exhibiting greater decreases in tendon stiffness after passive stretching of the calf muscles (2). The differences in baseline mechanical properties of the Achilles tendon and distinctive response to stretching between men and women may help to elucidate the underlying disparity in injury risk between the sexes.

Although differences in tendon mechanical properties have been observed between the sexes at baseline and after passive stretching, the literature is lacking prospective investigations that aim to compare the acute response of the Achilles tendon with high demand loading compared between men and women. Joseph et al. (13) observed a sex-dependent response to acute exercise, where women exhibited greater declines in stiffness and modulus of the Achilles tendon after calf-raise exercises, similar to that found after passive stretching. However, acute decreases in tendon mechanical properties after exercise are not equivalent to chronic changes that are associated with tendon injury, and no data currently exist to elucidate the recovery of Achilles tendon mechanics after repetitive loading exercise. These data would provide an understanding of sex differences in tendon properties that may help to explain the disparity in injury risk. Therefore, the purpose of this investigation was to compare Achilles tendon mechanical properties between men and women before, immediately after, and 60 minutes after a repetitive loading exercise.

Methods

Experimental Approach to the Problem

We conducted a single-session study to evaluate the differences in Achilles tendon mechanical properties between sexes (male and female) and in response to a repetitive loading exercise over the course of 1 hour (baseline, immediately after, and 60 minutes after). The outcome measures of interest were Achilles tendon force, elongation, stiffness, stress, strain, and modulus obtained using diagnostic ultrasound images as previously reported (13,14). All outcomes were evaluated in the dominant limb of all participants at all 3 time points. An a priori power analysis using published data (13) indicated 15 participants per group to detect differences between sexes using an α level of 0.05 and power of 80%.

Subjects

Seventeen women (age: 24.0 ± 3.9 years [age range: 20-31 years old]; height: 167.4 ± 6.9 cm; and mass: 64.9 ± 8.5 kg) and 18 men (age: 23.9 ± 2.4 years [age range: 20-31 years old]; height: 179.2 ± 5.09 cm; and mass: 78.4 ± 8.7 kg), recruited from the university community, volunteered to complete this study. To be included, participants were required to report no history of Achilles tendon disease and a score of >94 on the Victorian Institute of Sport Assessment—Achilles questionnaire (33). In addition, all participants were classified as moderately active as defined by the International Physical Activity Questionnaire (5). The study was approved by the University of Connecticut's Institutional Review Board and informed written consent was obtained before enrollment.

Procedures

Participants were instructed to refrain from exercise and any unusual activity the day before testing. For testing, participants were seated in an isokinetic dynamometer (Biodex System 4, Shirley, NY, USA) set at 0° plantar flexion and 0° knee flexion and synchronized using a diagnostic ultrasound unit (Terason t3200; Transducer 15L4; Terason, Burlington, MA, USA; Figure 1A). The same experienced examiner obtained all ultrasound images because these procedures have previously demonstrated excellent intrasession reliability (13,14).

F1
Figure 1.:
Participant set up in the isokinetic dynamometer (A) and ultrasound images of the Achilles tendon during testing. Resting Achilles tendon length was measured from the musculotendinous junction to insertion on the calcaneus (B), whereas tendon elongation (mm) was measured as the maximum change in tendon length from pre–maximal voluntary isometric contraction (C) to maximal voluntary isometric contraction (D).

Before testing, Achilles tendon length was calculated by obtaining the distance from the insertion of the tendon on the calcaneal tubercle to the soleus musculotendinous junction (Figure 1B) (14,24,25). Because the length of the Achilles tendon was larger than the transducer's field of view, the examiner used the TeraScape feature within the ultrasound unit's software (Terason), which allows for panoramic viewing. The examiner glided the transducer from the insertion of the tendon on the calcaneal tubercle to the soleus musculotendinous junction. In addition, tendon CSA was assessed by tracing the tendon outline using ultrasound imaging software (Terason t3200) from a transverse ultrasound scan at the level of the musculotendinous junction (14,18).

During testing, participants performed an 11-second maximal voluntary isometric contraction (MVIC) protocol in plantar flexion, where the participant began with a 3-second ramp-up, held the contraction for 5 seconds, and then gradually ramped down over another 3 seconds. Force elongation data were obtained from torque production on the dynamometer and fascicle excursion during simultaneous ultrasonic video analysis. Images were obtained of the soleus musculotendinous junction in the sagittal plane and a fascicle just distal to the MTJ was assessed for elongation measures as previously reported (14). After baseline measurements, participants performed a repetitive loading exercise of the Achilles tendon, consisting of 100 successive calf raises using a Smith machine (MG-PL62; Matrix, Cottage Grove, WI, USA) at a load of 20% of participant body mass. Calf raises were performed bilaterally in plantar flexion only, beginning from a standing position with their foot flat on the ground. During the loading protocol, participants were instructed to limit knee flexion (i.e., instructed to contract at the ankle like pressing down on a gas pedal, as opposed to bending at the knee) so that force was being produced using the calf muscles to maximally load the Achilles tendon. Verbal feedback and encouragement was provided to ensure maximal effort and correct form. All participants were able to complete the entire protocol in less than 3 minutes.

Immediately after calf raises, participants were seated in the dynamometer to undergo posttesting. Participants then remained seated for 60 minutes, and were instructed not to place any load on their tested limb. After 60 minutes of rest, another round of testing was completed.

Data Analysis

Achilles tendon force, elongation, stiffness, stress, strain, and Young's modulus were calculated from data obtained from the dynamometer and ultrasound assessments at each time point. Each of these calculations have been explained in detail in previous investigations (13,14,26,30). Briefly, tendon force (N) is calculated as the plantar flexion MVIC torque produced on the dynamometer multiplied by the moment arm of the Achilles tendon (average distance from medial and lateral malleoli to the tendon). Tendon elongation (mm) is measured as the maximum change in tendon length from pre-MVIC to MVIC (Figure 1C–D), whereas tendon stiffness (N·mm−1) is calculated as the tendon force divided by tendon elongation. Tendon stress (MPa) is evaluated by dividing the tendon force by CSA, and tendon strain (%) is calculated by dividing the tendon elongation value by resting Achilles tendon length. Finally, Young's modulus (MPa) serves as a material property analogous to normalized stiffness, where tendon stress is divided by tendon strain.

Statistical Analyses

We used 2 × 3 (sex by time) repeated-measures analyses of variances to assess differences in male participants and female participants on each mechanical property (tendon force, elongation, stiffness, stress, strain, and Young's modulus) of the Achilles tendon at 3 separate times of baseline, immediately after calf raises, and 60 minutes after calf raises. Bonferroni post hoc comparisons were performed in the presence of significant main and interaction effects a-prior significance was set at p ≤ 0.05.

Results

Tendon Force

There was no sex by time interaction (F2,66 = 0.62, p = 0.54) for tendon force; however, there were significant sex (F1,33 = 15.17, p < 0.001) and time (F2,66 = 5.25, p = 0.009) main effects observed. Regardless of time, women demonstrated lower Achilles tendon force compared with men (p < 0.001). Regardless of sex, all participants experienced an immediate decline in tendon force after the calf-raise exercises (p = 0.006), and was observed to be equal to baseline at 60-minute postexercise because tendon force at 60-minute postexercise was not different compared with baseline (p = 0.30) or immediately postexercise (p = 0.47) (Figure 2).

F2
Figure 2.:
Achilles tendon force depicted across time by sex. Data are presented as mean ± SD. *Indicates significant main effect for sex. Female participants demonstrated lower levels of tendon force regardless of time point (p < 0.001). †Indicates significant main effect for time. All participants, regardless of sex, experienced an immediate decline in tendon force, with significant differences between the baseline and immediate post time points (p = 0.006).

Tendon Elongation

There was no sex by time interaction (F2,66 = 0.07, p = 0.93), and no differences between sex (F1,33 = 2.45, p = 0.12) or differences over time (F2,66 = 0.08, p = 0.91) were observed for Achilles tendon elongation. (Figure 3).

F3
Figure 3.:
Achilles tendon elongation depicted across time by sex. Data are presented as mean ± SD. No significant differences were observed.

Tendon Stiffness

There was no sex by time interaction (F2,66 = 0.45, p = 0.64) for tendon stiffness; however, there were both sex (F1,33 = 4.22, p = 0.04) and time (F2,66 = 3.01, p = 0.05) main effects observed. Regardless of time, women demonstrated lower Achilles tendon stiffness compared with men (p = 0.04). Regardless of sex, all participants experienced an immediate decline in tendon stiffness after the calf-raise exercises (p = 0.05), and was observed to be equal to baseline at 60-minute postexercise because tendon stiffness at 60-minute postexercise was not different compared with baseline (p = 0.38) or immediately postexercise (p = 0.52) (Figure 4).

F4
Figure 4.:
Achilles tendon stiffness depicted across time by sex. Data are presented as mean ± SD. *Indicates significant main effect for sex. Female participants demonstrated lower levels of tendon stiffness regardless of time point (p = 0.04). †Indicates significant main effect for time. All participants, regardless of sex, experienced an immediate decline in tendon stiffness, with significant differences between the baseline and immediate post time points (p = 0.05).

Tendon Stress

There was no sex by time interaction effect (F2,66 = 0.17, p = 0.84) for tendon stress; however, there were both sex (F1,33 = 6.13, p = 0.01) and time (F2,66 = 4.86, p = 0.01) main effects observed. Regardless of time, women demonstrated lower Achilles tendon stress compared with men (p = 0.01). Regardless of sex, all participants experienced an immediate decline in tendon stress after the calf-raise exercises (p = 0.01), and was observed to be equal to baseline at 60-minute postexercise because tendon stress at 60-minute postexercise was not different compared with baseline (p = 0.25) or immediately postexercise (p = 0.34) (Figure 5).

F5
Figure 5.:
Achilles tendon stress depicted across time by sex. Data are presented as mean ± SD. *Indicates significant main effect for sex. Female participants demonstrated lower levels of tendon stress regardless of time point (p = 0.01). †Indicates significant main effect for time. All participants, regardless of sex, experienced an immediate decline in tendon stress, with significant differences between the baseline and immediate post time points (p = 0.01).

Tendon Strain

There was no sex by time interaction (F2,66 = 0.42, p = 0.65), and no differences between sex (F1,33 = 0.01, p = 0.98), or differences over time (F2,66 = 0.38, p = 0.68) were observed for Achilles tendon strain (Figure 6).

F6
Figure 6.:
Achilles tendon strain depicted across time by sex. Data are presented as mean ± SD. No significant differences were observed.

Young's Modulus

There was no sex by time interaction effect (F2,66 = 0.10, p = 0.89) for Young's modulus; however, there were both sex (F1,33 = 2.72, p = 0.05) and time (F2,66 = 2.65, p = 0.05) main effects observed. Regardless of time, women demonstrated lower Achilles tendon modulus compared with men (p = 0.01). Regardless of sex, all participants experienced an immediate decline in tendon modulus after the calf-raise exercises (p = 0.05), and was observed to be equal to baseline at 60-minute postexercise because tendon modulus at 60-minute postexercise was not different compared with baseline (p = 0.37) or immediately postexercise (p = 0.99) (Figure 7).

F7
Figure 7.:
Achilles tendon modulus depicted across time by sex. Data are presented as mean ± SD. *Indicates significant main effect for sex. Female participants demonstrated lower levels of tendon modulus regardless of time point (p = 0.05). †Indicates significant main effect for time. All participants, regardless of sex, experienced an immediate decline in tendon stress, with significant differences between the baseline and immediate post time points (p = 0.05).

Discussion

The results of our study suggest that women demonstrate less Achilles tendon force, stiffness, stress, and modulus compared with men; however, both sexes demonstrate similar tendon elongation and strain measures. The Achilles tendon of both men and women responded to repetitive loading exercise in the same manner, with decrease in mechanical properties from baseline to immediately after exercise, and recovery toward baseline at 60-minute postexercise. This is the first investigation to examine sex-dependent tendon responses to repetitive loading along with longitudinal assessment of return to baseline.

The immediate changes we observed in mechanical properties of the Achilles tendon after exercise are in agreement with other published findings. In particular, 5 minutes of passive dorsiflexion stretching (2,21), and isometric dorsiflexion contractions result in reductions in tendon stiffness and modulus, which occur in combination with reductions in triceps surae muscle force production and electromyographic activity (16). Although acute changes in the Achilles tendon have been observed after stretching and MVICs, less is known regarding the acute response of tendon to repetitive loading exercise. Because higher exposure to tissue overload in athletes such as runners, soccer, volleyball, and basketball players is thought to increase risk of Achilles tendon injury (22,23), it is important to also understand how the tendon responds to these repetitive loading exercises. We used the same experimental setup and repetitive loading exercise protocol as Joseph et al., (13) who reported immediate reductions in tendon force, stress, elongation stiffness, and modulus outcomes after calf-raise exercises. However, others have examined tendon responses after more sport-specific exercises, such as prolonged running (6,29) and bilateral hopping (31), with minimal change in tendon stiffness immediately after the interventions (28). The protocol used in the current investigation (100 successive calf raises performed at a load of 20% body weight) imposes repetitive loads on the Achilles tendon that may not mimic those imposed during running or hopping. In addition, tendon properties were assessed in a single joint position using isometric muscle contractions, and it remains unclear how different joint positions, or nonstatic testing, would influence the results found in this study. Future research would benefit from assessing mechanical properties of the Achilles tendon in a more functional position, as well as before and after actual or simulated athletic events.

After isometric plantar flexion contractions, previous data indicate that the immediate reductions in Achilles tendon stiffness lasts up to 30 minutes after contraction; however, muscle force seems to recover at this time (16). Unfortunately, there are limited data regarding the recovery of tendon properties after exercise, and the current investigation is the first to assess longitudinal assessment of tendon properties specifically after repetitive loading exercise. Although we did not observe statistically significant differences between 60-minute postexercise and baseline values, we also did not observe statistically significant differences between the immediate postexercise and 60-minute postexercise time points. Therefore, participants may have experienced slight, prolonged deficits in Achilles tendon properties even at 60-minute postexercise. This finding is clinically important because chronic impairments in the mechanical properties of the Achilles tendon can lead to tissue injury, especially if plantar flexion muscle force production is restored. Essentially, this creates more, or equal force production on a weakened tendon. We did not assess tendon properties longer than 60-minute postexercise, and we do not have serial data between the immediate and 60-minute postexercise time points. Future investigations would benefit from additional time points, both before and after 60 minutes.

The sex differences we observed in baseline Achilles tendon properties were expected because our results are in agreement with other studies (2,13,20). However, we had anticipated that men and women would respond differently to the repetitive loading exercise. Burgess et al. (2), concluded that women demonstrated greater decreases in Achilles tendon stiffness and modulus after passive stretching when compared with men. In addition, the results from Kubo et al. (20), indicate that women exhibit greater tendon elongation and tendon strain, and less tendon stiffness and modulus after plantar flexion MVICs compared with men. Baseline differences in the mechanical properties of the tendon, in combination with these previously published results, indicate a sex-specific response of the Achilles tendon to acute exercise, whereas the Achilles tendon of women demonstrate exaggerated responses compared with men.

We are aware of only one study that has investigated sex-dependent responses to repetitive loading exercise (13), which this current study was modeled after. Joseph et al. (13), concluded that women exhibited greater declines in stiffness and modulus of the Achilles tendon after the calf-raise exercises, whereas the mechanical properties of the Achilles tendon in men remained constant, and did not adapt immediately after calf raises. It is important to note that this previous investigation (13) used heavily resistance-trained men, who generated much greater tendon force (3,451.6 ± 897.9 N) and stiffness (835.4 ± 233.8 N·mm−1) compared with the recreationally active participants included in our study (force: 1661.8 ± 699.1 N; stiffness 206.5 ± 113.4 N·mm−1). It is likely that the increased stiffness and force production in these participants, which are hallmark changes of resistance training (19), made male tendons of the resistance-trained men more resistant to change after the calf-raise exercises (1). Furthermore, other studies are in agreement with our findings and have also observed no sex differences in tendon response to exercise (3), and recent evidence has indicated that male and female tendons have similar mechanical properties and biochemical composition (34). These conflicting data demonstrate the need for further investigation into the sex-specific adaptations occurring in the mechanical properties of the Achilles tendon.

In addition to the inclusion of multiple time points and more sport-specific activities, future research would benefit from the inclusion of Achilles tendon–injured populations. The evidence behind the Achilles tendon response to exercise in healthy populations is growing; however, it is important for clinicians to understand how these changes in mechanical properties influence tendon injury, so that clinicians can develop effective preventative strategies. Furthermore, it is also important to understand how these mechanical properties are altered in Achilles tendon–injured populations, so that clinicians can direct evidence based rehabilitation programs to improve outcomes in these patients. Ultimately, the data from our investigation demonstrate that repetitive loading exercise creates immediate changes in Achilles tendon mechanical properties that may have further implications for acute or chronic tendon injury for men and women. Athletes participating in sports with repetitive exposure to Achilles tendon tissue overload (i.e., running, soccer, volleyball, and basketball) and clinicians who work directly with these athletes should be aware of these risks and understand appropriate interventions. The current evidence suggests that the eccentric exercise may be the most beneficial intervention for both the prevention (allowing tendon to maximizes stresses it can withstand) and treatment (stimulation of tenocytes and anabolic activity) of tendon injuries, and may be included in preventative and rehabilitation protocols in high-risk athletes (7,12).

It is important to note that others have demonstrated no changes in the mechanical properties of the Achilles tendon after repeated loading exercises, such as recreational (6), marathon (32), and shuttle running (9). These authors suggest that single bouts of running, or natural loading over time, may not overstress the Achilles tendon, and that overuse-induced changes in tendon properties are not supported. The difference between these studies and the current investigation is the type of exercise performed. Although running and natural loading of the tendon over prolonged duration may not cause alterations in tendon properties, resistance exercise and repetitive loading, such as the calf-raise exercises used in this study, may induce tendon changes that may predispose individuals to tendon injury. Furthermore, duration of loading may also play a critical factor in these discrepancies because the period in which the tendon is loaded (i.e., ground contact) is of short duration during running (0.1–0.5 seconds) (6). These data together suggest that Achilles tendon properties are more stable under common locomotor tasks with short loading duration, and are more susceptible to alterations when load and load duration increase.

Practical Applications

Our data suggest that baseline differences in Achilles tendon properties may help to explain the disparity in injury risk between men and women because both sexes responded to and recovered from exercise similarly. Clinically, women may be less likely to sustain Achilles tendon injury due to the lower levels of tendon force, stress, and stiffness compared with men because the increase in compliance of female tendons at baseline may be advantageous for tendon health. In addition, our data indicate that male and female tendons respond similarly to exercise, with each sex experiencing increases in tendon compliance after repetitive loading exercise. Although mechanical properties of the tendon were equal to baseline at 60-minute postexercise, we are unable to conclude whether these outcomes fully recovered to baseline levels. Finally, our data indicate that repetitive loading resistance exercise, as opposed to repetitive loading (i.e., running), induce changes in the mechanical properties of the tendon that may increase injury risk. Clinicians should be aware of the prolonged changes (>60 minutes) in the mechanical properties of tendons after exercise, and future research is needed to understand how these changes influence injury risk.

This investigation examined sex- dependent tendon responses immediately and 60 minutes after repetitive loading exercises. Consistent with previous evidence, women exhibited less Achilles tendon force, stiffness, stress, and modulus compared with men. Both sexes responded to repetitive loading exercise similarly, with immediate decreases in mechanical properties of the Achilles tendon from baseline to immediately postexercise. Tendon properties were observed to be equal to baseline values at 60-minute postexercise. Future research should aim to include additional time points (both leading up to and after 60 minutes), and assess tendon responses to more sport-specific activities, while also including patients diagnosed with Achilles tendon injuries.

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Keywords:

ankle; tendinopathy; Young's modulus; strain; stiffness

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