ACHILLES TENDON BIOMECHANICS ACUTE INTENSE EXERCISE
IN
RESPONSE
TO
MICHAEL F. JOSEPH,1,2,3 KURTIS R. LILLIE,1,2 DANIEL J. BERGERON,1,2 KEVIN C. COTA,1,2 JOSEPH S. YOON,1,2 WILLIAM J. KRAEMER,1,3 AND CRAIG R. DENEGAR1,2,3 1
Department of Kinesiology; 2Physical Therapy Program; and 3Human Performance Laboratory, University of Connecticut, Storrs, Connecticut ABSTRACT
Joseph, MF, Lillie, KR, Bergeron, DJ, Cota, KC, Yoon, JS, Kraemer, WJ, and Denegar, CR. Achilles tendon biomechanics in response to acute intense exercise. J Strength Cond Res 28(5): 1181– 1186, 2014—Achilles tendinopathy is a common disorder and is more prevalent in men. Although differences in tendon mechanics between men and women have been reported, understanding of tendon mechanics in young active people is limited. Moreover, there is limited understanding of changes in tendon mechanics in response to acute exercise. Our purpose was to compare Achilles tendon mechanics in active young adult men and women at rest and after light and strenuous activity in the form of repeated jumping with an added load. Participants consisted of 17 men and 14 women (18–30 years) who were classified as being at least moderately physically active as defined by the International Physical Activity Questionnaire. Tendon force/elongation measures were obtained during an isometric plantarflexion contraction on an isokinetic dynamometer with simultaneous ultrasound imaging of the Achilles tendon approximate to the soleus myotendinous junction. Data were collected at rest, after a 10-minute treadmill walk, and after a fatigue protocol of 100 toe jumps performed in a Smith machine, with a load equaling 20% of body mass. We found greater tendon elongation, decreased stiffness, and lower Young’s modulus only in women after the jumping exercise. Force and stress were not different between groups but decreased subsequent to the jumping exercise bout. In general, women had greater elongation and strain, less stiffness, and a lower Young’s modulus during plantarflexor contraction. These data demonstrate differences in tendon mechanics between men and women and suggest a potential protective mechanism explaining the lower incidence of Achilles tendinopathy in women.
KEY WORDS stress, tendon, adaptation, material properties, stiffness, tendinopathy
Address correspondence to Michael F. Joseph, [email protected]. 28(5)/1181–1186 Journal of Strength and Conditioning Research Ó 2014 National Strength and Conditioning Association
INTRODUCTION
T
endon 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 VOLUME 28 | NUMBER 5 | MAY 2014 |
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Achilles Tendon Mechanics (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.
METHODS 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. Subjects
For this study, participants consisted of 17 men (age, 24.6 6 2.4 years; height, 175.4 6 7.5 cm; mass, 86.9 6 13.3 kg) and 14 women (age, 23.6 6 1.6 years; height, 166.3 6 7.5 cm; mass, 67.2 6 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
Figure 1. Ultrasound image of the soleus myotendinous junction during an isometric plantarflexion contraction. Proximal excursion is measured, and a force/ elongation curve is generated. Calculations are derived from the linear portion of the curve between 50 (A) and 100% (B) of a MVIC. MVIC = maximum voluntary isometric contraction.
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Figure 2. One hundred toe jumps with 20% body mass were performed to load the Achilles tendon.
was approved by the University of Connecticut’s institutional review board, and all subjects provided informed consent. Procedures
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 08 plantarflexion, 08 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
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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 08 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:
Fmus ¼ TQ3MA21 : Because tendon force is directly related to the contribution of the muscles to which the tendon is attached:
Fmus ¼ k3Ft; TABLE 1. Force (N) and stress (MPa) 6 SD.
Baseline Walk Jump
Sex
Force (N)
SD
Stress (MPa)
SD
Men Women Men Women Men* Women*
3451.6 3207.2 3615.2 3203.6 3093.5 2797.8
897.9 703.9 769.7 643.4 861.8 374.9
38.2 32.9 38.8 32.9 32.4 29.8
17.5 9.3 15.6 7.9 10.4 7.2
where k is the relative contribution of muscles contributing to total tendon force, which in our case equals 1 (100%). Thus,
Fmus ¼ Ft And
Ft ¼ TQ3MA21
*Significant decline in force and stress for both sexes after toe jumping.
because Fmus and Ft are Interchangeable VOLUME 28 | NUMBER 5 | MAY 2014 |
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Achilles Tendon Mechanics
TABLE 2. Tendon elongation (mm) and strain (%).*
Baseline Walk Jump
Sex
Elongation (mm)
SD
Strain (%)
SD
Men Women† Men Women† Men Women†z
4.6 5.9 4.7 5.9 4.1 7.8
0.7 1.2 0.8 1.2 1.0 1.5
9.4 11.0 10.0 11.0 8.4 15.0
3.1 2.9 3.2 2.8 3.4 3.5
*Greater compliance in women across all conditions. †Significant difference between sex. zSignificant difference between loading condition.
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,
Stress ðsÞ ¼ Force=CSA: 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 (e) = DL/L0, where (L) is measured displace-
ment; 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. Statistical Analyses
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.
RESULTS 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
Figure 3. Achilles tendon stiffness across sex and activity. Women were significantly less stiff after toe jumping. †significantly different from males. zsignificantly different from males and within loading conditions.
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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
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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 Figure 4. Young’s modulus across sex and activity. Women had a significantly lower modulus after toe jumping. substantially alter the mechanical properties of tendons (4,5). demonstrated a substantial decrease in stiffness after jumpOptimal tendon mechanical properties are likely activity ing (p , 0.01). specific. Compliant tendons store more energy during As one would expect, men had a significantly greater stretch, which is returned during recoil to maximize the Young’s modulus (p = 0.01) across measurements. There contribution of elastic strain to movement (8,23). However, were only small differences (p . 0.05) in Young’s modulus excessive tissue compliance results in inefficient energy in men across the 3 measurements, whereas women demontransfer to the moving segment. Accumulated residual instrated a marked decrease (p # 0.05) in Young’s modulus creases in tendon compliance may lead to subsequent injury after jumping. when recovery is insufficient and large/repetitive forces are encountered. Our results along with others (3,18) indicate Results Summary that a woman’s tendon is more compliant and we have In summary, we found a similar sex interaction over time demonstrated a marked continual increase in compliance with respect to tendon elongation, stiffness, and Young’s in women in response to an intense bout of loading. We modulus in which women experienced a marked decrease believe an increase in compliance during intensive loading in all measures after the jumping exercise bout, whereas men may represent a protective effect, which might in part did not. Force and stress were not different between sexes; explain the large discrepancy in tendon disorders and ruphowever, we observed decreases in each measure subsequent ture rates between sexes. We did not measure time to return to the heavy load experienced during the jumping exercise to baseline values in women, which would have been valubout. able. If the lower AT injury rates among women are, in fact, related to mechanical behavior of the tendon, it would be DISCUSSION logical to assume increases in compliance are quicker to return to baseline values in women. This is a promising area Men and women both exhibited decreased tendon force and of continued investigation. stress during isometric plantarflexion contractions after the Our comparison of acute responses to loading in healthy jumping exercise. This is not surprising because of the tendon is a logical first step to understanding mechanical fatiguing nature of the loading protocol. The fact that characteristics predisposing injury. Arya (2) found an increase baseline measures of force and stress were not statistically in CSA and decrease in stiffness and modulus in tendinopathic different was unexpected; however, the limited literature in tendon in a study of 12 men with Achilles tendinopathy. This this area is inconclusive regarding isometric plantarflexion is not a surprise because of the structural changes that accomforce in men and women with 1 study showing no difference pany tendinopathy and should not be misinterpreted as in both force and stress (30) and another demonstrating men causal. Chronically increased compliance associated with tenproducing greater isometric plantarflexion torque (18). dinopathy is not equivalent to acute increases in compliance We demonstrate a difference in tendon compliance between in response to heavy loading exercise. Additionally, increased men and women which is in agreement with other studies compliance is not necessarily reflective of lower tensile (3,18); however, we are the first to show an interaction in which VOLUME 28 | NUMBER 5 | MAY 2014 |
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Achilles Tendon Mechanics 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.
PRACTICAL APPLICATIONS 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 and Lorentzon, R. Chronic Achilles tendinosis: Recommendations for treatment and prevention. Sports Med 29: 135–146, 2000. 2. Arya, S and 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, and 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, and Onambe´le´, 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, and Onambe´le´, GL. Patellar tendon properties with fluctuating menstrual cycle hormones. J Strength Cond Res 24: 2088–2095, 2010. 6. Craig, CL, Marshall, AL, Sjo¨stro¨m, M, Bauman, AE, Booth, ML, Ainsworth, BE, Pratt, M, Ekelund, U, Yngve, A, Sallis, JF, and 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, and 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, and 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, and Blair, SN. Epidemiology of musculoskeletal injuries among sedentary and physically active adults. Med Sci Sports Exerc 34: 838– 844, 2002. 11. Ja¨rvinen, M, Jo´zsa, L, Kannus, P, Ja¨rvinen, TL, Kvist, M, and Leadbetter, W. Histopathological findings in chronic tendon disorders. Scand J Med Sci Sports 7: 86–95, 1997. 12. Joseph, MF, Lillie, K, Bergeron, D, and Denegar, CR. Measuring Achilles tendon mechanical properties: A reliable, non-invasive method. J Strength Cond Res 26: 2017–2020, 2012. the
14. Kay, AD and 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 of tendon and skeletal muscle to mechanical loading. Physiol Rev 84: 649–698, 2004. 16. Knobloch, K, Schreibmueller, L, Kraemer, R, Jagodzinski, M, Vogt, PM, and 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, and Jarvinen, M. Biomechanical loading of Achilles tendon during normal locomotion. Clin Sports Med 11: 521–531, 1992. 18. Kubo, K, Kanehisa, H, and 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, and 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.
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13. Kannus, P and 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.
21. Lichtwark, GA and 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, and Maffulli, N. Biomechanics of the Achilles tendon. Disabil Rehabil 30: 1542–1547, 2008. 24. Magnusson, SP, Hansen, P, and 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, and 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, and 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 and 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, and 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, and 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, and 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, and 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, and 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, and Fu, FH. Biomechanical basis for tendinopathy. Clin Orthop Relat Res 443: 320–332, 2006.
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IN
RESPONSE
TO
MICHAEL F. JOSEPH,1,2,3 KURTIS R. LILLIE,1,2 DANIEL J. BERGERON,1,2 KEVIN C. COTA,1,2 JOSEPH S. YOON,1,2 WILLIAM J. KRAEMER,1,3 AND CRAIG R. DENEGAR1,2,3 1
Department of Kinesiology; 2Physical Therapy Program; and 3Human Performance Laboratory, University of Connecticut, Storrs, Connecticut ABSTRACT
Joseph, MF, Lillie, KR, Bergeron, DJ, Cota, KC, Yoon, JS, Kraemer, WJ, and Denegar, CR. Achilles tendon biomechanics in response to acute intense exercise. J Strength Cond Res 28(5): 1181– 1186, 2014—Achilles tendinopathy is a common disorder and is more prevalent in men. Although differences in tendon mechanics between men and women have been reported, understanding of tendon mechanics in young active people is limited. Moreover, there is limited understanding of changes in tendon mechanics in response to acute exercise. Our purpose was to compare Achilles tendon mechanics in active young adult men and women at rest and after light and strenuous activity in the form of repeated jumping with an added load. Participants consisted of 17 men and 14 women (18–30 years) who were classified as being at least moderately physically active as defined by the International Physical Activity Questionnaire. Tendon force/elongation measures were obtained during an isometric plantarflexion contraction on an isokinetic dynamometer with simultaneous ultrasound imaging of the Achilles tendon approximate to the soleus myotendinous junction. Data were collected at rest, after a 10-minute treadmill walk, and after a fatigue protocol of 100 toe jumps performed in a Smith machine, with a load equaling 20% of body mass. We found greater tendon elongation, decreased stiffness, and lower Young’s modulus only in women after the jumping exercise. Force and stress were not different between groups but decreased subsequent to the jumping exercise bout. In general, women had greater elongation and strain, less stiffness, and a lower Young’s modulus during plantarflexor contraction. These data demonstrate differences in tendon mechanics between men and women and suggest a potential protective mechanism explaining the lower incidence of Achilles tendinopathy in women.
KEY WORDS stress, tendon, adaptation, material properties, stiffness, tendinopathy
Address correspondence to Michael F. Joseph, [email protected]. 28(5)/1181–1186 Journal of Strength and Conditioning Research Ó 2014 National Strength and Conditioning Association
INTRODUCTION
T
endon 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 VOLUME 28 | NUMBER 5 | MAY 2014 |
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Achilles Tendon Mechanics (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.
METHODS 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. Subjects
For this study, participants consisted of 17 men (age, 24.6 6 2.4 years; height, 175.4 6 7.5 cm; mass, 86.9 6 13.3 kg) and 14 women (age, 23.6 6 1.6 years; height, 166.3 6 7.5 cm; mass, 67.2 6 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
Figure 1. Ultrasound image of the soleus myotendinous junction during an isometric plantarflexion contraction. Proximal excursion is measured, and a force/ elongation curve is generated. Calculations are derived from the linear portion of the curve between 50 (A) and 100% (B) of a MVIC. MVIC = maximum voluntary isometric contraction.
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Figure 2. One hundred toe jumps with 20% body mass were performed to load the Achilles tendon.
was approved by the University of Connecticut’s institutional review board, and all subjects provided informed consent. Procedures
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 08 plantarflexion, 08 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
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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 08 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:
Fmus ¼ TQ3MA21 : Because tendon force is directly related to the contribution of the muscles to which the tendon is attached:
Fmus ¼ k3Ft; TABLE 1. Force (N) and stress (MPa) 6 SD.
Baseline Walk Jump
Sex
Force (N)
SD
Stress (MPa)
SD
Men Women Men Women Men* Women*
3451.6 3207.2 3615.2 3203.6 3093.5 2797.8
897.9 703.9 769.7 643.4 861.8 374.9
38.2 32.9 38.8 32.9 32.4 29.8
17.5 9.3 15.6 7.9 10.4 7.2
where k is the relative contribution of muscles contributing to total tendon force, which in our case equals 1 (100%). Thus,
Fmus ¼ Ft And
Ft ¼ TQ3MA21
*Significant decline in force and stress for both sexes after toe jumping.
because Fmus and Ft are Interchangeable VOLUME 28 | NUMBER 5 | MAY 2014 |
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Achilles Tendon Mechanics
TABLE 2. Tendon elongation (mm) and strain (%).*
Baseline Walk Jump
Sex
Elongation (mm)
SD
Strain (%)
SD
Men Women† Men Women† Men Women†z
4.6 5.9 4.7 5.9 4.1 7.8
0.7 1.2 0.8 1.2 1.0 1.5
9.4 11.0 10.0 11.0 8.4 15.0
3.1 2.9 3.2 2.8 3.4 3.5
*Greater compliance in women across all conditions. †Significant difference between sex. zSignificant difference between loading condition.
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,
Stress ðsÞ ¼ Force=CSA: 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 (e) = DL/L0, where (L) is measured displace-
ment; 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. Statistical Analyses
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.
RESULTS 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
Figure 3. Achilles tendon stiffness across sex and activity. Women were significantly less stiff after toe jumping. †significantly different from males. zsignificantly different from males and within loading conditions.
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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
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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 Figure 4. Young’s modulus across sex and activity. Women had a significantly lower modulus after toe jumping. substantially alter the mechanical properties of tendons (4,5). demonstrated a substantial decrease in stiffness after jumpOptimal tendon mechanical properties are likely activity ing (p , 0.01). specific. Compliant tendons store more energy during As one would expect, men had a significantly greater stretch, which is returned during recoil to maximize the Young’s modulus (p = 0.01) across measurements. There contribution of elastic strain to movement (8,23). However, were only small differences (p . 0.05) in Young’s modulus excessive tissue compliance results in inefficient energy in men across the 3 measurements, whereas women demontransfer to the moving segment. Accumulated residual instrated a marked decrease (p # 0.05) in Young’s modulus creases in tendon compliance may lead to subsequent injury after jumping. when recovery is insufficient and large/repetitive forces are encountered. Our results along with others (3,18) indicate Results Summary that a woman’s tendon is more compliant and we have In summary, we found a similar sex interaction over time demonstrated a marked continual increase in compliance with respect to tendon elongation, stiffness, and Young’s in women in response to an intense bout of loading. We modulus in which women experienced a marked decrease believe an increase in compliance during intensive loading in all measures after the jumping exercise bout, whereas men may represent a protective effect, which might in part did not. Force and stress were not different between sexes; explain the large discrepancy in tendon disorders and ruphowever, we observed decreases in each measure subsequent ture rates between sexes. We did not measure time to return to the heavy load experienced during the jumping exercise to baseline values in women, which would have been valubout. able. If the lower AT injury rates among women are, in fact, related to mechanical behavior of the tendon, it would be DISCUSSION logical to assume increases in compliance are quicker to return to baseline values in women. This is a promising area Men and women both exhibited decreased tendon force and of continued investigation. stress during isometric plantarflexion contractions after the Our comparison of acute responses to loading in healthy jumping exercise. This is not surprising because of the tendon is a logical first step to understanding mechanical fatiguing nature of the loading protocol. The fact that characteristics predisposing injury. Arya (2) found an increase baseline measures of force and stress were not statistically in CSA and decrease in stiffness and modulus in tendinopathic different was unexpected; however, the limited literature in tendon in a study of 12 men with Achilles tendinopathy. This this area is inconclusive regarding isometric plantarflexion is not a surprise because of the structural changes that accomforce in men and women with 1 study showing no difference pany tendinopathy and should not be misinterpreted as in both force and stress (30) and another demonstrating men causal. Chronically increased compliance associated with tenproducing greater isometric plantarflexion torque (18). dinopathy is not equivalent to acute increases in compliance We demonstrate a difference in tendon compliance between in response to heavy loading exercise. Additionally, increased men and women which is in agreement with other studies compliance is not necessarily reflective of lower tensile (3,18); however, we are the first to show an interaction in which VOLUME 28 | NUMBER 5 | MAY 2014 |
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Achilles Tendon Mechanics 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.
PRACTICAL APPLICATIONS 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.
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