Tendon transmits force from muscle to bone resulting in joint stabilization, motion, and function. The Achilles tendon (AT) is the strongest tendon in the human body and is exposed to high forces during daily activities and athletics. Force exposure ranges from 3 kN during maximal isometric contractions (23), 5 kN during unilateral hopping (21), and 9 kN during running, exceeding 12 times the body weight (17). To add perspective, the anterior cruciate ligament has an ultimate tensile strength near 1.7 kN (27), representing a fraction of the force encountered by the AT during demanding activities. The magnitude of AT loading during daily activity results in positive adaptation but excessive and repetitive forces are a precursor to degeneration and tendinopathy (11,33).
Adaptation to repetitive force occurs through alterations in tissue composition and biomechanical behavior of the tendon (32). The tendon cell (tenocyte) is responsible for maintaining tendon tissue through the remodeling and production of extracellular matrix (ECM) (15). Much of the stimulus required by the tenocyte to adapt to increased functional demand is derived from the mechanical signal inherent in the activity. Mechanical forces experienced in the tendon are transmitted through ECM to resident cells, resulting in increased production and remodeling of ECM components.
Evidence also exists that changes in the mechanical behavior of tendon occur in response to acute stimuli (16,24). Passive stretching decreases stiffness of the AT acutely (3,19) with women demonstrating a far greater increase in compliance (22.4%) compared with men (8.8%) after 5 minutes of a passive stretch (3). In fact, a woman's tendon is less stiff at baseline before intervention (18). An acute response to resistance activity has also been observed. Isometric plantarflexion yields an immediate decrease in stiffness that quickly plateaus with the addition of continued activity. Ten 4-second isometric plantarflexion contractions resulted in decreased tendon stiffness after the first 5 contractions but did not increase significantly thereafter in a sample of 6 men (22). Similarly, decreased tendon stiffness was observed after six 8-second maximum voluntary isometric contraction (MVIC) of the plantarflexors with no further decrease after an additional 180 seconds of static stretching in 8 men and women (14). Differences across sex were not compared. Of note, although muscle force and activity recovered 30 minutes after activity, tendon stiffness did not. Accumulated increase in tendon compliance in the presence of fully recovered force production is likely related to overuse injury.
The increasing incidence of connective tissue injuries in women has drawn considerable attention; however, the prevalence of AT pathology is disproportionally high in men (9,10,25). In fact, male sex is a proposed intrinsic risk for the development of Achilles pathology (20). Men accounted for 74% of 891 spontaneously ruptured tendons in the study conducted by Kannus and Jozsa (13), the preponderance of which involved the AT. Similar results were found in a large retrospective review of 7,375 Achilles ruptures in which 79% occurred in men (28).
Although baseline and post stretching differences in mechanical behavior exist across sex, acute response of the AT to high demand loading has not been compared prospectively in men and women. The purpose of this study is to compare AT mechanical characteristics (force, elongation, stiffness) and material properties (stress, strain, modulus) in men and women at baseline, and after a low and high demand bout of exercise. The mechanical behavior of tendon is linked to its susceptibility for injury. Identifying differential responses to loading will advance understanding of the markedly higher incidence of tendon pathology in men.
Experimental Approach to the Problem
Our ultrasound and dynamometry methodology has been described elsewhere in great detail (12). A subset of the subjects used in this study were used to determine reliability for our dynamometer and ultrasound measurements, found to be excellent with intrasession reliability for the dynamometer and excursion measures both 0.99 ICC (2, 1) (11). We examined mechanical properties of the AT acutely after a period of rest, light, and heavy loading.
For this study, participants consisted of 17 men (age, 24.6 ± 2.4 years; height, 175.4 ± 7.5 cm; mass, 86.9 ± 13.3 kg) and 14 women (age, 23.6 ± 1.6 years; height, 166.3 ± 7.5 cm; mass, 67.2 ± 6.5 kg). All were classified as at least being moderately physically active as defined by the International Physical Activity Questionnaire (IPAQ) (6). Presence of Achilles tendinopathy, defined as a score less than 94 on the Victorian Institute of Sport Assessment-Achilles (VISA-A) Questionnaire, was an exclusion criteria for participation. The VISA-A is both a reliable and valid index of severity of Achilles tendinopathy (31). In addition, no subject had evidence of disorganized or hypoechoic regions on ultrasound. The study was approved by the University of Connecticut's institutional review board, and all subjects provided informed consent.
Subjects were instructed to refrain from exercise or unusual activity the day before testing. Subjects were seated on an isokinetic dynamometer (Biodex System 4, Shirley, NY, USA) set at 0° plantarflexion, 0° knee flexion and time synchronized with a B-wave diagnostic ultrasound device (Philips HD11 XE, 12-5 MHz Linear Array transducer, Royal Philips, Netherlands). The same experienced examiner obtained and digitized all images in 1 laboratory setting. The myotendinous junction (MTJ) of the soleus insertion into the AT was imaged and marked. Free AT length was calculated by obtaining the distance from the insertion of the Achilles on the calcaneal tubercle to the soleus MTJ. Five maximal isometric contractions were performed before testing to condition the tendon (22).
During testing, subjects performed a MVIC in plantarflexion with a 5-second ramp, held the contraction for 3 seconds and then gradually relaxed over 5 seconds. Force elongation data were obtained from torque on the dynamometer and fascicle excursion during simultaneous ultrasonographic video capture. A fascicle approximate to the soleus MTJ was used for measures of fascicle excursion (Figure 1).
Following baseline measures, subjects performed a light loading protocol, consisting of a 10-minute walk on a treadmill with 0° incline at a self-selected pace. Tendon force and elongation were again recorded. Finally, a fatigue protocol of 100 toe jumps was performed in a Smith machine, with a load equaling 20% of the subject's body mass (Figure 2). During the fatigue protocol, the subjects were instructed to land and jump on the balls of their feet, not allowing heel strike and limiting knee flexion to maximally load the Achilles. Constant verbal feedback was given during the protocol to insure correct form. All subjects were able to complete the fatigue protocol. The subjects were then positioned in the Biodex and a third force elongation curve was obtained.
Tendon force, tendon stress, tendon elongation, tendon stiffness, and Young's modulus values were calculated from data obtained from the dynamometer and ultrasound recordings. Muscular force (Fmus) was derived from plantarflexion torque (TQ) data obtained during plantarflexion contractions performed on the dynamometer and moment arm of the Achilles (MA) as follows:
Because tendon force is directly related to the contribution of the muscles to which the tendon is attached:
where k is the relative contribution of muscles contributing to total tendon force, which in our case equals 1 (100%). Thus,
because Fmus and Ft are Interchangeable
Tendon elongation (L) was measured as a value of proximal fascicle excursion during the plantarflexion MVIC. A force elongation curve was derived. Stiffness was calculated from the slope of the linear portion of the force/elongation curve (26,29).
Stress and strain are normalized values for force/elongation. To calculate stress, we divided tendon force by the tendon cross-sectional area (CSA). Thus,
Cross sectional area was measured from a transverse scan at a location approximate to the fascicle visualized and used to obtain tendon elongation.
Strain is the relative percentage of elongation in relation to resting length of the tendon and calculated as: Strain (ε) = ΔL/L0, where (L) is measured displacement; L0 is the reference (resting) length.
Young's modulus (E), a material property analogous to normalized stiffness, was determined by the slope of the linear portion of the stress/strain curve.
Tendon force, stress, elongation, stiffness, and modulus were analyzed separately with a 1 between (sex) 1 within (measurement time) mixed model analysis of variance with SPSS version 17; SPSS, Inc., Chicago, IL. These data were analyzed separately because they represent distinctly different performance and mechanical measures. An alpha level of 0.05 was set for statistical significance.
Tendon Force and Stress
Tendon force and stress data are reported in Table 1. Tendon force was not significantly different between men and women at any time point (p = 0.24) as there were large SDs in measures. Both sexes demonstrated a decrease in force (p < 0.01) after the loaded jumping exercise. Similarly, no difference in tendon stress was found between sexes (p = 0.28); however, both groups exhibited significantly (p = 0.013) less stress after the loaded jumping exercise.
Tendon Elongation and Strain
Tendon elongation and strain data are reported in Table 2. Women exhibited greater tendon elongation across measures (p < 0.001), with much greater tendon elongation after jumping. Men exhibited significantly less strain at all 3 measurements times (p = 0.01), whereas women experienced a significant increase in tendon strain after jumping which was not observed in men (p < 0.01).
Tendon stiffness and Young's modulus data are depicted in Figures 3 and 4, respectively. Men demonstrated greater stiffness at each measurement time point (p < 0.01), whereas only women demonstrated a substantial decrease in stiffness after jumping (p < 0.01).
As one would expect, men had a significantly greater Young's modulus (p = 0.01) across measurements. There were only small differences (p > 0.05) in Young's modulus in men across the 3 measurements, whereas women demonstrated a marked decrease (p ≤ 0.05) in Young's modulus after jumping.
In summary, we found a similar sex interaction over time with respect to tendon elongation, stiffness, and Young's modulus in which women experienced a marked decrease in all measures after the jumping exercise bout, whereas men did not. Force and stress were not different between sexes; however, we observed decreases in each measure subsequent to the heavy load experienced during the jumping exercise bout.
Men and women both exhibited decreased tendon force and stress during isometric plantarflexion contractions after the jumping exercise. This is not surprising because of the fatiguing nature of the loading protocol. The fact that baseline measures of force and stress were not statistically different was unexpected; however, the limited literature in this area is inconclusive regarding isometric plantarflexion force in men and women with 1 study showing no difference in both force and stress (30) and another demonstrating men producing greater isometric plantarflexion torque (18).
We demonstrate a difference in tendon compliance between men and women which is in agreement with other studies (3,18); however, we are the first to show an interaction in which women respond to an acute loading protocol with a dramatic increase in tendon compliance, represented by an increase in deformation and a decrease in stiffness and modulus. Men remained fairly constant on these measures across loading schemes. Peltonen et al. (30) examined the effect of a single bout of hopping to fatigue and did not find a difference in tendon stiffness acutely. Their methodology differed in that there was no external load or comparison across sex. We did not measure or control for the hormone status of subjects in this study. Hormone fluctuation, however, has not been shown to substantially alter the mechanical properties of tendons (4,5).
Optimal tendon mechanical properties are likely activity specific. Compliant tendons store more energy during stretch, which is returned during recoil to maximize the contribution of elastic strain to movement (8,23). However, excessive tissue compliance results in inefficient energy transfer to the moving segment. Accumulated residual increases in tendon compliance may lead to subsequent injury when recovery is insufficient and large/repetitive forces are encountered. Our results along with others (3,18) indicate that a woman's tendon is more compliant and we have demonstrated a marked continual increase in compliance in women in response to an intense bout of loading. We believe an increase in compliance during intensive loading may represent a protective effect, which might in part explain the large discrepancy in tendon disorders and rupture rates between sexes. We did not measure time to return to baseline values in women, which would have been valuable. If the lower AT injury rates among women are, in fact, related to mechanical behavior of the tendon, it would be logical to assume increases in compliance are quicker to return to baseline values in women. This is a promising area of continued investigation.
Our comparison of acute responses to loading in healthy tendon is a logical first step to understanding mechanical characteristics predisposing injury. Arya (2) found an increase in CSA and decrease in stiffness and modulus in tendinopathic tendon in a study of 12 men with Achilles tendinopathy. This is not a surprise because of the structural changes that accompany tendinopathy and should not be misinterpreted as causal. Chronically increased compliance associated with tendinopathy is not equivalent to acute increases in compliance in response to heavy loading exercise. Additionally, increased compliance is not necessarily reflective of lower tensile strength of the tendon (14). An area for future research should further examine acute response to heavy loading along with time to return to baseline mechanical properties.
The increased prevalence of AT disorders and rupture in men suggests a differential response to loading across sex. The increase in compliance of a woman's tendon at baseline and in response to intense loading may be advantageous. Currently, the most effective treatment for Achilles tendinopathy is eccentric exercise (1). The primary mean to prevent AT rupture is to avoid the degenerative changes that occur (13). The often asymptomatic nature of tendinopathy and the potential for related rupture makes avoidance a vexing dilemma. The current noninvasive methods to study mechanical properties of tendon in response to exercise will increase the understanding of advantageous adaptation to training and optimal intervention.
1. Alfredson H, Lorentzon R. Chronic Achilles tendinosis: Recommendations for treatment and prevention. Sports Med 29: 135–146, 2000.
2. Arya S, Kulig K. Tendinopathy
alters mechanical and material properties
of the Achilles tendon
. J Appl Physiol (1985) 108: 670–675, 2010.
3. Burgess KE, Graham-smith P, Pearson SJ. Effect of acute tensile loading on sex-specific tendon
structural and mechanical properties. J Orthop Res 27: 510–516, 2009.
4. Burgess KE, Pearson SJ, Onambélé GL. Menstrual cycle variations in oestradiol and progesterone have no impact on in vivo medial gastrocnemius tendon
mechanical properties. Clin Biomech (Bristol, Avon) 24: 504–509, 2009.
5. Burgess KE, Pearson SJ, Onambélé GL. Patellar tendon
properties with fluctuating menstrual cycle hormones. J Strength Cond Res 24: 2088–2095, 2010.
6. Craig CL, Marshall AL, Sjöström M, Bauman AE, Booth ML, Ainsworth BE, Pratt M, Ekelund U, Yngve A, Sallis JF, Oja P. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35: 1381–1395, 2003.
7. Gaida JE, Alfredson H, Kiss ZS, Bass SL, Cook JL. Asymptomatic Achilles tendon
pathology is associated with a central fat distribution in men and a peripheral fat distribution in women: A cross sectional study of 298 individuals. BMC Musculoskelet Disord 2: 11–41, 2010.
8. Hess GP, Cappiello WL, Poole RM, Hunter SC. Prevention and treatment of overuse tendon
injuries. Sports Med 8: 371–384, 1989.
9. Hess GW. Achilles tendon
rupture: A review of etiology, population, risk factors, and injury prevention. Foot Ankle Spec 3: 29–32, 2010.
10. Hootman JM, Macera CA, Ainsworth BE, Addy CL, Martin M, Blair SN. Epidemiology of musculoskeletal injuries among sedentary and physically active adults. Med Sci Sports Exerc 34: 838–844, 2002.
11. Järvinen M, Józsa L, Kannus P, Järvinen TL, Kvist M, Leadbetter W. Histopathological findings in chronic tendon
disorders. Scand J Med Sci Sports 7: 86–95, 1997.
12. Joseph MF, Lillie K, Bergeron D, Denegar CR. Measuring Achilles tendon
mechanical properties: A reliable, non-invasive method. J Strength Cond Res 26: 2017–2020, 2012.
13. Kannus P, Jozsa L. Histopathological changes preceding spontaneous rupture of a tendon
. A controlled study of 891 patients. J Bone Joint Surg Am 73: 1507–1525, 1991.
14. Kay AD, Blazevich AJ. Isometric contractions reduce plantar flexor moment, Achilles tendon stiffness
, and neuromuscular activity but remove the subsequent effects of stretch. J Appl Physiol (1985) 107: 1181–1189, 2009.
15. Kjaer M. Role of extracellular matrix in adaptation
and skeletal muscle to mechanical loading. Physiol Rev 84: 649–698, 2004.
16. Knobloch K, Schreibmueller L, Kraemer R, Jagodzinski M, Vogt PM, Redeker J. Sex and eccentric training in Achilles mid-portion tendinopathy
. Knee Surg Sports Traumatol Arthrosc 18: 648–655, 2010.
17. Komi PV, Fukashiro S, Jarvinen M. Biomechanical loading of Achilles tendon
during normal locomotion. Clin Sports Med 11: 521–531, 1992.
18. Kubo K, Kanehisa H, Fukunaga T. Sex differences in the viscoelastic properties of tendon
structures. Eur J Appl Physiol 88: 520–526, 2003.
19. Kubo K, Kanehisa H, Kawakami Y, Fukunaga T. Influence of static stretching on viscoelastic properties of human tendon
structures in vivo. J Appl Physiol (1985) 90: 520–527, 2001.
20. Kvist M. Achilles tendon
injuries in athletes. Ann Chir Gynaecol 80: 188–201, 1991.
21. Lichtwark GA, Wilson AM. Is Achilles tendon
compliance optimised for maximum muscle efficiency during locomotion? J Biomech 40: 1768–1775, 2007.
22. Maganaris CN. Tendon
conditioning: Artefact or property? Proc Biol Sci 270(Suppl. 1): S39–S42, 2007.
23. Maganaris CN, Narici MV, Maffulli N. Biomechanics of the Achilles tendon
. Disabil Rehabil 30: 1542–1547, 2008.
24. Magnusson SP, Hansen P, Kjaer M. Tendon
properties in relation to muscular activity and physical training. Scand J Med Sci Sports 13: 211–223, 2003.
25. Magnusson SP, Hansen M, Langberg H, Miller B, Haraldsson B, Westh EK, Koskinen S, Aagard P, Kjaer M. The adaptability of tendon
to loading differs in men and women. Int J Exp Pathol 88: 237–240, 2007.
26. Muraoka T, Muramatsu T, Fukunaga T, Kanehisa H. Geometric and elastic properties of in vivo human Achilles tendon
in young adults. Cells Tissues Organs 178: 197–203, 2004.
27. Noyes FR, Grood ES. The strength of the anterior cruciate ligament in humans and Rhesus monkeys. J Bone Joint Surg Am 58: 1074–1082, 1976.
28. Nyyssonen T, Luthje P, Kroger H. The increasing incidence and difference in sex distribution of Achilles tendon
rupture in Findland in 1987–1999. Scand J Surg 97: 272–275, 2008.
29. Pearson SJ, Burgess K, Onambele GN. Creep and the in vivo assessment of human patellar tendon
mechanical properties. Clin Biomech (Bristol, Avon) 22: 712–717, 2007.
30. Peltonen J, Cronin NJ, Avela J, Finni T. In vivo mechanical response of human Achilles tendon
to a single bout of hopping exercise. J Exp Biol 213: 1259–1265, 2010.
31. Robinson JM, Cook JL, Purdam C, Visentini PJ, Ross J, Maffulli N, Taunton JE, Khan KM; and Victorian Institute of Sport Tendon
Study Group. The VISA-A questionnaire: A valid and reliable index of the clinical severity of Achilles tendinopathy
. Br J Sports Med 35: 335–341, 2001.
32. Rosager S, Aagaard P, Dyhre-Poulsen P, Neergaard K, Kjaer M, Magnusson SP. Load-displacement properties of the human triceps surae aponeurosis and tendon
in runners and non-runners. Scand J Med Sci Sports 12: 90–98, 2002.
33. Wang JH, Iosifidis MI, Fu FH. Biomechanical basis for tendinopathy
. Clin Orthop Relat Res 443: 320–332, 2006.
Keywords:Copyright © 2014 by the National Strength & Conditioning Association.
stress; tendon; adaptation; material properties; stiffness; tendinopathy