Running Shoes Increase Achilles Tendon Load in Walking: An Acoustic Propagation Study SCOTT C. WEARING1,2, LLOYD REED1, SUE L. HOOPER2, SIMON BARTOLD3, JAMES E. SMEATHERS1, and TORSTEN BRAUNER4 1
Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, AUSTRALIA; 2Centre of Excellence for Applied Sport Science Research, Queensland Academy of Sport, Brisbane, AUSTRALIA; 3School of Health Sciences, University of Melbourne, Melbourne, AUSTRALIA; and 4Faculty of Sports and Health Sciences, Technische Universita¨t Mu¨nchen, Munich, GERMANY
ABSTRACT WEARING, S. C., L. REED, S. L. HOOPER, S. BARTOLD, J. E. SMEATHERS, and T. BRAUNER. Running Shoes Increase Achilles Tendon Load in Walking: An Acoustic Propagation Study. Med. Sci. Sports Exerc., Vol. 46, No. 8, pp. 1604–1609, 2014. Background: Footwear remains a prime candidate for the prevention and rehabilitation of Achilles tendinopathy because it is thought to decrease tension in the tendon through elevation of the heel. However, evidence for this effect is equivocal. Purpose: This study used an acoustic transmission technique to investigate the effect of running shoes on Achilles tendon loading during barefoot and shod walking. Methods: Acoustic velocity was measured in the Achilles tendon of 12 recreationally active males (age, 31 T 9 yr; height, 1.78 T 0.06 m; weight, 81.0 T 16.9 kg) during barefoot and shod walking at matched self-selected speed (3.4 T 0.7 kmIhj1). Standard running shoes incorporating a 10-mm heel offset were used. Vertical ground reaction force and spatiotemporal parameters were determined with an instrumented treadmill. Axial acoustic velocity in the Achilles tendon was measured using a custom-built ultrasonic device. All data were acquired at a rate of 100 Hz during 10 s of steady-state walking. Statistical comparisons between barefoot and shod conditions were made using paired t-tests and repeated-measure ANOVA. Results: Acoustic velocity in the Achilles tendon was highly reproducible and was typified by two maxima (P1, P2) and minima (M1, M2) during walking. Footwear resulted in a significant increase in step length, stance duration, and peak vertical ground reaction force compared with barefoot walking. Peak acoustic velocity in the Achilles tendon (P1, P2) was significantly higher with running shoes. Conclusions: Peak acoustic velocity in the Achilles tendon was higher with footwear, suggesting that standard running shoes with a 10-mm heel offset increase tensile load in the Achilles tendon. Although further research is required, these findings question the therapeutic role of standard running shoes in Achilles tendinopathy. Key Words: SOFT TISSUE, QUANTITATIVE ULTRASOUND, SPEED OF SOUND, FOOTWEAR, ACHILLES TENDON, ACOUSTIC PROPAGATION
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the inherent heel offset in traditional running shoes elevates the heel, shortens the muscle–tendon unit, and thereby decreases the load in the Achilles tendon during gait (31). However, supporting evidence for this effect remains equivocal. Elevation of the heel, in the order of 15 to 18 mm, has been estimated to either increase (9), decrease (11), or have no effect (3,10,31) on peak tensile loading of the Achilles tendon during running. To date, the majority of studies evaluating the effect of footwear on Achilles tendon loading have focused on running gait and used inverse dynamic models to indirectly estimate tendon loads (9–11,31). Although insightful, indirect estimation of internal tendon loads using the inverse approach is not without limitations. As noted by Gregor et al. (13) in comparing direct and indirect estimates of Achilles tendon loading during cycling, inverse dynamic models may overestimate tendon loads by as much as 50%. Although studies investigating direct loading of the Achilles tendon in vivo during sports-related activities have been performed (12,18), such experiments are typically highly invasive and have not specifically evaluated the effects of footwear. Acoustic transmission techniques, in contrast, have the potential to provide direct noninvasive estimates of human
chilles tendinopathy is a common lower limb injury, which has a protracted clinical course that often requires lengthy and difficult clinical management plans (1). Footwear remains a prime candidate for the prevention of tendinopathy and is often used as a key therapeutic intervention in Achilles tendon rehabilitation postinjury (1). Inadequate heel offset (heel elevation) in running shoes has long been anecdotally implicated in the development of Achilles tendinopathy, and modification of footwear via heel lifts has been suggested to be an effective treatment for Achilles tendon disorders on the basis of selfreported clinical outcomes (14,23). It has been speculated that
Address for correspondence: Scott C. Wearing, PhD, Institute of Health and Biomedical Innovation, Queensland University of Technology, 60 Musk Avenue, Kelvin Grove, Qld 4059, Australia; E-mail: [email protected]. Submitted for publication August 2013. Accepted for publication December 2013. 0195-9131/14/4608-1604/0 MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ Copyright Ó 2014 by the American College of Sports Medicine DOI: 10.1249/MSS.0000000000000256
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tendon loading and have been widely used to evaluate the mechanical properties of human bone in vivo (38). Studies in animal tendon have also confirmed that the axial transmission of acoustic waves is governed by the bulk modulus and density of tendon and is proportional to the tensile load to which it is exposed (16,20,26,28). The aim of this study, therefore, was to explore the use of an acoustic transmission technique to investigate the effect of standard running shoes on Achilles tendon loading during walking. Because there is a positive correlation between acoustic velocity and tension in tendon (4,28), it was hypothesized that acoustic velocity in the Achilles tendon would be lower during walking in shoes with an inherent heel offset (elevation) compared with unshod gait.
MATERIALS AND METHODS
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FIGURE 1—Axial acoustic velocity was measured in the right Achilles tendon using a custom-built ultrasonic device (U), which was maintained in close contact with the skin using an acoustic coupling medium and elasticized straps. The end-blocks of a flexible twin-axis strain-gauge electrogoniometer (G) were fixed to the skin over the lateral aspect of fibula and calcaneus using double-sided adhesive tape and further fixed with surgical tape.
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Participants. Twelve healthy adult males were recruited from university faculty to participate in the study. The mean T SD age, height, body mass, and foot length of participants was 31 T 9 yr (range, 20–47 yr), 1.78 T 0.06 m, 81.0 T 16.9 kg, and 26.4 T 0.9 cm, respectively. Participants were nonsmokers, nonmedicated, and recreationally active on the basis of selfreport. No participant reported a medical history of diabetes, inflammatory joint disease, familial hypercholesterolemia, or Achilles tendon pain or pathology. No participants reported a history of Achilles tendon surgery. All participants gave written informed consent before participation in the research. The study received approval from the university human research ethics committee and was undertaken according to the principles outlined in the Declaration of Helsinki. Equipment. A flexible twin-axis strain-gauge electrogoniometer (SG110A, Penny and Giles; Biometrics, Gwent, UK) and accompanying angle display unit was used to estimate the change in ankle flexion with footwear during quiet bipedal standing. The end-blocks of the device were fixed to the skin overlying the lateral calcaneus and the distal aspect of the fibula of the right ankle using double-sided adhesive tape, and further secured with surgical tape (34). The electrogoniometer has a resolution of 1-, and the device has been shown to be accurate to within 1.5% over a 100- range (33). Vertical ground reaction force and temporospatial gait parameters were determined during barefoot and shod walking using an instrumented treadmill system (FDM-THM-S; Zebris Medical GmbH, Isny, Germany). The treadmill system is composed of a capacitance-based pressure platform housed within a variable speed treadmill. The pressure platform had a sensing area of 108.4 47.4 cm and incorporated 7168 sensors, each approximately 0.85 0.85 cm. The treadmill had a contact surface of 150 50 cm, and its belt speed could be adjusted between 0.2 and 22 kmIhj1, at intervals of 0.1 kmIhj1. The grade of the contact surface of the treadmill was maintained in a horizontal position (0%) throughout testing. Reported coefficients of variation for the majority of temporospatial gait parameters are typically below 10% for repeated measures (30).
Axial acoustic velocity was synchronously measured in the right Achilles tendon using a custom-built ultrasonic device and a five-element ultrasound probe similar to that described previously (28,29). The probe consisted of a 1-MHz broadband pulse emitter and four regularly spaced receivers (range, 33.0–40.5 mm) and was positioned over the midline of the posterior aspect of the Achilles tendon, with the emitter placed 1 cm above the calcaneal attachment. The probe was maintained in close contact with the skin using a coupling medium and elasticized straps (Fig. 1). The received ultrasonic signals were digitized at 10 MHz, and the time of flight of the first arriving transient signal between receivers was estimated using the first zero crossing criterion (2). Average acoustic velocity was subsequently calculated given the known distance between receivers and the measured time of flight. The reported error in predicting applied tensile force in tendon from direct measures of acoustic velocity is typically G2% (4). Protocol. Participants reported to the gait laboratory wearing lightweight, comfortable clothing and having abstained from vigorous physical activity on the day of testing. The skin overlying the posterior Achilles tendon and lateral aspect of the right shank was shaved and cleaned using standard alcohol abrading methods. After fixation of the probe and electrogoniometer to the right leg, participants were afforded a 10-min treadmill acclimatization session. During the acclimatization session, participants were instructed to adjust the speed of the treadmill to a ‘‘comfortable’’ walking pace using a previously outlined method (30). The defined gait speed was subsequently used to evaluate acoustic velocity in the Achilles tendon during shod and unshod (barefoot) gait conditions. The order of each gait condition was randomized between participants, and each gait condition was followed by a rest period in which ankle angle was measured during quiet bipedal stance.
A standard running shoe (Oregon; Adidas, Herzogenaurach, Germany) ranging in size between US 9.5 and 11.5 (length 29.4–30.9 cm) and mass between 359 and 396 g, with identical, flexible mesh uppers and incorporating a single density ethylene vinyl acetate (EVA) midsole and rubber outsole were used for the shod condition. The midsole and outsole hardness of the shoes was 60 T 1 and 88 T 1, respectively, as determined by a Shore A Durometer, which measures resistance to indentation on a dimensionless scale ranging from 0 to 100. All shoes were made by the same manufacturer and had a heel offset (elevation) of 10 mm (forefoot height, 17.0–19.5 mm; heel height, 27.0–29.5 mm). After 5 min of shod and unshod steady-state walking, acoustic velocity in the right Achilles tendon, vertical ground reaction force, and basic temporospatial gait data were sampled over a 10-s period and at a rate 100 Hz. Data reduction and statistical analysis. Proprietary software (Zebris Medical GmbH, Isny, Germany) was used to calculate mean temporospatial gait parameters including cadence, step and stride length, step width, foot rotation, stance and stride times and swing phase, and single and double support durations (Table 1). With the exception of stride and stance times, temporal data were expressed as a percentage of the gait cycle. Vertical ground reaction force data were exported in ASCII format, and custom computer code (Matlab R2012a; MathWorks, Natick, MA) was subsequently used to identify the magnitude (FZ1–FZ3) and timing (TFZ1–TFZ3) of conventional vertical ground reaction force peaks for each step (Fig. 2). The relative time to each force maxima and topic minima was expressed as a percentage of the stance phase duration. Peak force loading rate (PFLR), defined as the greatest rate of force change during the first 20 ms of the gait cycle, was calculated using previously outlined methods (32), whereas the total foot impulse was estimated by numerical integration of the vertical ground reaction force with respect to time (40). Topic maxima and minima in acoustic data were analyzed, and the peak rate of change in acoustic velocity during loading of the Achilles tendon was also calculated using custom computer code. Mean values were calculated for all steps recorded within the 10-s data capture period, which equated
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TABLE 1. Mean temporospatial (SD) gait parameters during barefoot and shod walking. Barefoot Global Velocity (kmIhj1) Cadence (stepsIminj1) Spatial Stride length (cm) Step width (cm) Step length (cm) Temporal Stride time (ms) Step time (ms) Stance phase (%) Swing phase (%) Single support (%) Double support (%)
Shod
3.4 (0.7) 101.6 (12.6)
3.4 (0.7) 96.7* (12.9)
110.1 (12.8) 10.7 (2.2) 54.8 (6.3)
115.2* (11.1) 10.6 (2.1) 57.2* (4.4)
1202 774 64 36 35 29
1268* 865* 68* 32* 32* 35*
(102) (158) (3) (3) (2) (5)
(92) (191) (3) (3) (3) (5)
*Indicates a statistically significant difference between barefoot and shod conditions (P G 0.05).
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FIGURE 2—Illustration of vertical ground reaction force parameters calculated from the instrumented treadmill system. The force–time integral, or total foot impulse, is represented by the area under the curve, whereas the PFLR was the maximum rate of force change within the first 20 ms of the gait cycle. Note that time to force maxima (TFZ1 and TFZ3) and topic minima (TFZ2) was expressed as a percentage of the stance phase duration.
to an average of 12.1 T 1.6 steps during barefoot walking and 11.3 T 1.7 steps during shod walking. The Statistical Package for the Social Sciences (SPSS Inc., Chicago, IL) was used for all statistical procedures. Kolmogorov–Smirnov tests were used to evaluate data for underlying assumptions of normality. Outcome variables were determined to be normally distributed, so means and SD were used as summary statistics. Paired t-tests were used to evaluate potential differences in acoustic parameters, cadence, stride length, step width, double support, and gait cycle duration. For all other variables, differences between shod and unshod conditions were assessed using repeatedmeasures ANOVA within a generalized linear modeling framework. In each case, condition (shod and barefoot) and limb (left and right) were treated as within-subject factors. Underlying assumptions regarding the uniformity of the variance–covariance matrix were assessed using Mauchly test of sphericity. When the assumption of uniformity was violated, an adjustment to the degrees of freedom of the F-ratio was made using Greenhouse–Geisser Epsilon, thereby making the F-test more conservative. Because there were no statistically significant main effects for limb, only data for the right limb have been presented. An alpha level of 0.05 was used for all tests of significance.
RESULTS Running shoes increased mean ankle plantarflexion by 4- T 2- during quiet bipedal stance and resulted in a significant decrease in cadence and duration of single support and an increase in step length, stance duration, double support, peak vertical ground reaction force, and PFLR during treadmill walking when compared with barefoot walking (Tables 1 and 2).
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TABLE 2. Mean (SD) vertical ground reaction forces during barefoot and shod walking. Barefoot FZ1 (N) FZ2 (N) FZ3 (N) TFZ1 (%) TFZ2 (%) TFZ3 (%) PFLR (BWIsj1) FTI (NIs)
842 (132) 714 (151) 856 (113) 29 (4) 50 (3) 74 (4) 174 (51) 476 (103)
Shod 890* 745* 890* 30 49 72* 108* 521*
(123) (146) (104) (4) (3) (5) (46) (104)
*Indicates a statistically significant difference between barefoot and shod conditions (P G 0.05). BW, body weight; FTI, total foot impulse.
Acoustic velocity in the Achilles tendon was highly reproducible during heel–toe walking and was characterized by two maxima (P1, P2) and two topic minima (M1, M2) (Fig. 3). The mean–within-subject coefficient of variation for acoustic maxima and minima during steady-state walking ranged between 0.2% T 0.1% and 1.0% T 0.6%. Although there was no significant difference in minimum acoustic velocity (M1, M2) with footwear (Table 3), peak acoustic velocity in the right Achilles tendon (P1, P2) was significantly higher with running shoes with a 10-mm heel offset. There was no significant difference in the peak rate of change in acoustic velocity in the Achilles tendon during loading in barefoot and shod conditions.
DISCUSSION Peak acoustic velocity of the Achilles tendon in the current study was comparable with that reported previously for human tendon (,1900–2050 mIsj1) (28,29) and was of a similar pattern to the force in the Achilles tendon measured directly with implanted force transducers during walking (12,18). As described by Komi (18), force in the Achilles tendon is typically reduced after heel contact and is followed by a second steep rise in tendon load during the stance. In the current study, both the first and second peaks in acoustic
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Acoustic Velocity
Barefoot
P1 (mIsj1) P2 (mIsj1) M1 (mIsj1) M2 (mIsj1) Rate of acoustic velocity (mIsj2)
1920 2022 1860 1814 13,112
(67) (92) (85) (89) (3353)
Shod 1943* 2047* 1865 1852 13,923
(55) (71) (58) (54) (3925)
*Indicates a statistically significant difference between barefoot and shod conditions (P G 0.05).
velocity (P1, P2) were highly reproducible during steadystate walking (mean within-subject coefficient of variation G1%), which is consistent with earlier observations that the peak-to-peak amplitude of Achilles tendon force is invariant across a range of walking speeds (1.1–1.8 mIsj1) (12). In contrast to our hypothesis, however, peak acoustic velocity in the Achilles tendon was significantly higher during shod compared with barefoot, treadmill walking, suggesting that standard running shoes with a 10-mm heel elevation increase tensile load in the Achilles tendon during walking. Although the present experimental setup did not allow for a mechanistic explanation for the increase in acoustic velocity of the Achilles tendon observed during shod gait, previous research has highlighted the potential influence of heel elevation, through high-heeled shoes (8.5–10 cm), to increase muscular activity and cocontraction of several lower limb muscles during overground walking (25,37). However, consistent effects of high-heeled shoes on lower leg muscular activity, particularly of the triceps surae, are not universally reported, and the electromyographic effects of heel offsets commonly used in traditional running shoes are even less clear (37). Although Scott et al. (35) detected a small but statistically significant increase in peak EMG activity of only the medial gastrocnemius between walking barefoot and with standard running shoes (heel offset, 20 mm), others have found no significant differences during running with heel offsets of 18 mm (11). Although the effects of standard running shoes on muscle activity may be mediated, in part, by midsole properties (39), quantification of tensile force based on the surface EMG remains elusive, particularly during dynamic activities such as gait (8). It is noteworthy that the shoes used in this study resulted in significant changes in several basic gait parameters. Consistent with previous research investigating footwear effects in running (3,7,17), shod walking in the current study was characterized by a lower cadence (j5 steps per minute), greater stride (5%) and step length (5%), and longer step duration (12%) than barefoot, despite walking at identical speeds. When expressed as a percentage of the gait cycle, participants adopted a relatively longer stance phase duration (4%) and shorter swing phase (j4%) during shod walking when compared with barefoot gait. The footwear used in this study also increased ankle plantarflexion by approximately 4- during quiet bipedal stance. Although changes in static ankle angle with footwear may not reflect dynamic changes during gait, comparable changes in peak ankle plantarflexion have been reported previously during walking with elevation of the heel (18 mm) and with standard running shoes (11). Farris et al. (11) proposed that the
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FIGURE 3—Typical acoustic velocity recorded in the right Achilles tendon during barefoot (dashed line) and shod (solid line) walking at a matched gait speed. Shaded bands indicate stance phase. Note that the acoustic velocity in the Achilles tendon was characterized by two maxima (P1, P2) and two minima (M1, M2) during each gait cycle.
TABLE 3. Mean (SD) acoustic velocity in the right Achilles tendon during shod and unshod walking.
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resultant ankle plantarflexion with heel elevation (18 mm) effectively lengthened the Achilles tendon moment arm and thereby reduced loading in the Achilles tendon. The results of the current study, however, tend not to support this concept, because the increase in static ankle plantarflexion observed with footwear in the current study was accompanied by an increase in acoustic velocity of the Achilles tendon during gait. Interestingly, although studies using 2D imaging-based estimates have suggested that the Achilles tendon moment arm is increased with ankle plantarflexion (24), more recent estimates using 3D imaging techniques have shown the opposite effect, with Achilles tendon moment arm either unchanged or even decreased with ankle plantarflexion (15,36). It should be noted that measures of acoustic velocity, as used in the current study, neither are predicated on estimates of the tendon moment arm nor require assumptions regarding the contribution of agonist and antagonist muscles to the net ankle joint moment, both of which have been shown to induce substantial errors in estimates of tendon loading (13,36). Shod walking in the current study was characterized by higher active vertical ground reaction forces (5%–7%) and a lower external PFLR (38%–44%) when compared with the barefoot walking. Although running shoes have been previously reported to lower peak external force loading rates during running (7,17), we observed no significant difference in the peak rate of acoustic transmission in the Achilles tendon between shod and barefoot conditions. Thus, peak external force loading rates as defined in the current study do not necessarily correspond with internal loading rates of the Achilles tendon during walking. Moreover, although standard running shoes acted to increase the magnitude of tensile load in the Achilles tendon during walking, they would seem to have a negligible influence on the rate of Achilles tendon loading. The use of acoustic transmission techniques to investigate the effect of running shoes on Achilles tendon loading is not without limitation. The propagation of acoustic waves in soft tissue media is influenced by several factors, including the density, temperature, hydration, and bulk modulus of the tissue through which it passes (26). Although tendon hydration and temperature may reasonably be assumed to be stable during shod and barefoot gait conditions in the current study, there is evidence, albeit in animal models, that the composition of the Achilles tendon may vary along its length (6). Thus, it is unknown whether the effects of footwear observed in the current study are applicable to the entire tendon structure. Similarly, the mechanical properties and response of the Achilles tendon to load may differ between sexes and over the lifespan (19,22). Although gender differences in tendon properties are not universally reported (27), it is important to note that this study was
limited to evaluating the effects of a standard running shoe in a small sample of healthy adult males walking at a single (preferred) gait speed and on the same day. The effect of footwear observed in the current study, therefore, may have represented a transient response and may not be directly transferable to Achilles tendon loading with habitual use in children, females, older cohorts, or at markedly faster or slower gait speeds. Similarly, although the ‘‘cushioning’’ properties and bending stiffness of running shoes have been suggested to influence muscle activity and gearing at the ankle joint (3,39), this study evaluated only a single shoe design that incorporated a hard midsole material (Shore A Durometer, 60 T 1) and a 10-mm heel offset. Consequently, the effects of individual components of the shoe, such as midsole cushioning and effective heel offset, on tendon loading could not be elucidated. Moreover, treadmill systems are known to induce both spatial and temporal constraints on gait and have been shown by some to alter neuromuscular coordination and subsequent lower extremity joint moments and powers during walking (21). Although other research has shown treadmill walking has negligible effect on fascicle behavior of the triceps surae when compared with overground walking (5), the findings of this study may not necessarily be representative of unconstrained walking in ‘‘real-world’’ settings outside of the laboratory. Nonetheless, the findings of the current study suggest that, in comparison to barefoot walking, standard running shoes with a 10-mm heel offset induce global changes in vertical ground reaction force and temporospatial gait parameters in healthy adults that act to increase tensile load in the Achilles tendon. Although further research elucidating potential mechanisms underpinning the observed effect is required, the results of this study raise questions as to the potential preventative and therapeutic effects of standard running shoes in the management of Achilles tendinopathy.
CONCLUSIONS This study is the first to show that standard running shoes increase Achilles tendon loading, as defined by an increase in acoustic velocity, during treadmill walking. These findings question the potential role of standard running shoes in the prevention and therapeutic management of Achilles tendinopathy and suggest that footwear with a 10-mm heel offset may increase loading in the Achilles tendon during gait. This research received financial support from the Queensland Academy of Sport and the Australian Institute of Sport. The authors declare no conflicts of interest, financial or otherwise. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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3. Braunstein B, Arampatzis A, Eysel P, Bru¨ggemann GP. Footwear affects the gearing at the ankle and knee joints during running. J Biomech. 2010;43(11):2120–5. 4. Crevier-Denoix N, Ravary-Plumio¨en B, Evrard D, Pourcelot P. Reproducibility of a non-invasive ultrasonic technique of tendon force measurement determined in vitro in equine superficial digital flexor tendons. J Biomech. 2009;42:2210–3. 5. Cronin NJ, Finni T. Treadmill versus overground and barefoot versus shod comparisons of triceps surae fascicle behaviour in human walking and running. Gait Posture. 2013;38(3):528–33. 6. Curwin SL, Roy RR, Vailas AC. Regional and age variations in growing tendon. J Morphol. 1994;221(3):309–20. 7. De Wit B, De Clercq D, Aerts P. Biomechanical analysis of the stance phase during barefoot and shod running. J Biomech. 2000;33(3): 269–78. 8. Disselhorst-Klug C, Schmitz-Rode T, Rau G. Surface electromyography and muscle force: Limits in sEMG–force relationship and new approaches for applications. Clin Biomech. 2009;24(3):225–35. 9. Dixon SJ, Kerwin DG. The influence of heel lift manipulation on Achilles tendon forces in running. J Appl Biomech. 1998;14:374–89. 10. Dixon SJ, Kerwin DG. Variations in Achilles tendon loading with heel lift intervention in heel-toe runners. J Appl Biomech. 2002;18: 321–31. 11. Farris DJ, Buckeridge E, Trewartha G, McGuigan MP. The effects of orthotic heel lifts on Achilles tendon force and strain during running. J Appl Biomech. 2012;28:511–9. 12. Finni T, Komi PV, Lukkariniemi J. Achilles tendon loading during walking: application of a novel optic fiber technique. Eur J Appl Physiol Occup Physiol. 1998;77:289–91. 13. Gregor RJ, Komi PV, Browning RC, Ja¨rvinen M. A comparison of the triceps surae and residual muscle moments at the ankle during cycling. J Biomech. 1991;24(5):287–97. 14. Grisogono V. Physiotherapy treatment for Achilles tendon injuries. Physiotherapy. 1989;75:562–72. 15. Hashizume S, Iwanuma S, Akagi R, Kanehisa H, Kawakami Y, Yanai T. In vivo determination of the Achilles tendon moment arm in three-dimensions. J Biomech. 2012;45(2):409–13. 16. Hoffmeister BK, Verdonk ED, Wickline SA, Miller JG. Effect of collagen on the anisotropy of quasi-longitudinal mode ultrasonic velocity in fibrous soft tissues: a comparison of fixed tendon and fixed myocardium. J Acoust Soc Am. 1994;96(4):1957–64. 17. Kerrigan DC, Franz JR, Keenan GS, Dicharry J, Della Croce U, Wilder R. The effect of running shoes on lower extremity joint torques. PM R. 2009;1(12):1058–63. 18. Komi PV. Relevance of in vivo force measurements to human biomechanics. J Biomech. 1990;23(1 Suppl):23–34. 19. Kubo K, Kanehisa H, Fukunaga T. Gender differences in the viscoelastic properties of tendon structures. Eur J Appl Physiol. 2003;88:520–6. 20. Kuo PL, Li PC, Li ML. Elastic properties of tendon measured by two different approaches. Ultrasound Med Biol. 2001;27(9):1275–84. 21. Lee SJ, Hidler J. Biomechanics of overground vs. treadmill walking in healthy individuals. J Appl Physiol. 2008;104(3):747–55. 22. Lewis G, Shaw KM. Tensile properties of human tendo Achillis: effect of donor age and strain rate. J Foot Ankle Surg. 1997;36(6): 435–45.
Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, AUSTRALIA; 2Centre of Excellence for Applied Sport Science Research, Queensland Academy of Sport, Brisbane, AUSTRALIA; 3School of Health Sciences, University of Melbourne, Melbourne, AUSTRALIA; and 4Faculty of Sports and Health Sciences, Technische Universita¨t Mu¨nchen, Munich, GERMANY
ABSTRACT WEARING, S. C., L. REED, S. L. HOOPER, S. BARTOLD, J. E. SMEATHERS, and T. BRAUNER. Running Shoes Increase Achilles Tendon Load in Walking: An Acoustic Propagation Study. Med. Sci. Sports Exerc., Vol. 46, No. 8, pp. 1604–1609, 2014. Background: Footwear remains a prime candidate for the prevention and rehabilitation of Achilles tendinopathy because it is thought to decrease tension in the tendon through elevation of the heel. However, evidence for this effect is equivocal. Purpose: This study used an acoustic transmission technique to investigate the effect of running shoes on Achilles tendon loading during barefoot and shod walking. Methods: Acoustic velocity was measured in the Achilles tendon of 12 recreationally active males (age, 31 T 9 yr; height, 1.78 T 0.06 m; weight, 81.0 T 16.9 kg) during barefoot and shod walking at matched self-selected speed (3.4 T 0.7 kmIhj1). Standard running shoes incorporating a 10-mm heel offset were used. Vertical ground reaction force and spatiotemporal parameters were determined with an instrumented treadmill. Axial acoustic velocity in the Achilles tendon was measured using a custom-built ultrasonic device. All data were acquired at a rate of 100 Hz during 10 s of steady-state walking. Statistical comparisons between barefoot and shod conditions were made using paired t-tests and repeated-measure ANOVA. Results: Acoustic velocity in the Achilles tendon was highly reproducible and was typified by two maxima (P1, P2) and minima (M1, M2) during walking. Footwear resulted in a significant increase in step length, stance duration, and peak vertical ground reaction force compared with barefoot walking. Peak acoustic velocity in the Achilles tendon (P1, P2) was significantly higher with running shoes. Conclusions: Peak acoustic velocity in the Achilles tendon was higher with footwear, suggesting that standard running shoes with a 10-mm heel offset increase tensile load in the Achilles tendon. Although further research is required, these findings question the therapeutic role of standard running shoes in Achilles tendinopathy. Key Words: SOFT TISSUE, QUANTITATIVE ULTRASOUND, SPEED OF SOUND, FOOTWEAR, ACHILLES TENDON, ACOUSTIC PROPAGATION
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A
the inherent heel offset in traditional running shoes elevates the heel, shortens the muscle–tendon unit, and thereby decreases the load in the Achilles tendon during gait (31). However, supporting evidence for this effect remains equivocal. Elevation of the heel, in the order of 15 to 18 mm, has been estimated to either increase (9), decrease (11), or have no effect (3,10,31) on peak tensile loading of the Achilles tendon during running. To date, the majority of studies evaluating the effect of footwear on Achilles tendon loading have focused on running gait and used inverse dynamic models to indirectly estimate tendon loads (9–11,31). Although insightful, indirect estimation of internal tendon loads using the inverse approach is not without limitations. As noted by Gregor et al. (13) in comparing direct and indirect estimates of Achilles tendon loading during cycling, inverse dynamic models may overestimate tendon loads by as much as 50%. Although studies investigating direct loading of the Achilles tendon in vivo during sports-related activities have been performed (12,18), such experiments are typically highly invasive and have not specifically evaluated the effects of footwear. Acoustic transmission techniques, in contrast, have the potential to provide direct noninvasive estimates of human
chilles tendinopathy is a common lower limb injury, which has a protracted clinical course that often requires lengthy and difficult clinical management plans (1). Footwear remains a prime candidate for the prevention of tendinopathy and is often used as a key therapeutic intervention in Achilles tendon rehabilitation postinjury (1). Inadequate heel offset (heel elevation) in running shoes has long been anecdotally implicated in the development of Achilles tendinopathy, and modification of footwear via heel lifts has been suggested to be an effective treatment for Achilles tendon disorders on the basis of selfreported clinical outcomes (14,23). It has been speculated that
Address for correspondence: Scott C. Wearing, PhD, Institute of Health and Biomedical Innovation, Queensland University of Technology, 60 Musk Avenue, Kelvin Grove, Qld 4059, Australia; E-mail: [email protected]. Submitted for publication August 2013. Accepted for publication December 2013. 0195-9131/14/4608-1604/0 MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ Copyright Ó 2014 by the American College of Sports Medicine DOI: 10.1249/MSS.0000000000000256
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tendon loading and have been widely used to evaluate the mechanical properties of human bone in vivo (38). Studies in animal tendon have also confirmed that the axial transmission of acoustic waves is governed by the bulk modulus and density of tendon and is proportional to the tensile load to which it is exposed (16,20,26,28). The aim of this study, therefore, was to explore the use of an acoustic transmission technique to investigate the effect of standard running shoes on Achilles tendon loading during walking. Because there is a positive correlation between acoustic velocity and tension in tendon (4,28), it was hypothesized that acoustic velocity in the Achilles tendon would be lower during walking in shoes with an inherent heel offset (elevation) compared with unshod gait.
MATERIALS AND METHODS
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FIGURE 1—Axial acoustic velocity was measured in the right Achilles tendon using a custom-built ultrasonic device (U), which was maintained in close contact with the skin using an acoustic coupling medium and elasticized straps. The end-blocks of a flexible twin-axis strain-gauge electrogoniometer (G) were fixed to the skin over the lateral aspect of fibula and calcaneus using double-sided adhesive tape and further fixed with surgical tape.
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Participants. Twelve healthy adult males were recruited from university faculty to participate in the study. The mean T SD age, height, body mass, and foot length of participants was 31 T 9 yr (range, 20–47 yr), 1.78 T 0.06 m, 81.0 T 16.9 kg, and 26.4 T 0.9 cm, respectively. Participants were nonsmokers, nonmedicated, and recreationally active on the basis of selfreport. No participant reported a medical history of diabetes, inflammatory joint disease, familial hypercholesterolemia, or Achilles tendon pain or pathology. No participants reported a history of Achilles tendon surgery. All participants gave written informed consent before participation in the research. The study received approval from the university human research ethics committee and was undertaken according to the principles outlined in the Declaration of Helsinki. Equipment. A flexible twin-axis strain-gauge electrogoniometer (SG110A, Penny and Giles; Biometrics, Gwent, UK) and accompanying angle display unit was used to estimate the change in ankle flexion with footwear during quiet bipedal standing. The end-blocks of the device were fixed to the skin overlying the lateral calcaneus and the distal aspect of the fibula of the right ankle using double-sided adhesive tape, and further secured with surgical tape (34). The electrogoniometer has a resolution of 1-, and the device has been shown to be accurate to within 1.5% over a 100- range (33). Vertical ground reaction force and temporospatial gait parameters were determined during barefoot and shod walking using an instrumented treadmill system (FDM-THM-S; Zebris Medical GmbH, Isny, Germany). The treadmill system is composed of a capacitance-based pressure platform housed within a variable speed treadmill. The pressure platform had a sensing area of 108.4 47.4 cm and incorporated 7168 sensors, each approximately 0.85 0.85 cm. The treadmill had a contact surface of 150 50 cm, and its belt speed could be adjusted between 0.2 and 22 kmIhj1, at intervals of 0.1 kmIhj1. The grade of the contact surface of the treadmill was maintained in a horizontal position (0%) throughout testing. Reported coefficients of variation for the majority of temporospatial gait parameters are typically below 10% for repeated measures (30).
Axial acoustic velocity was synchronously measured in the right Achilles tendon using a custom-built ultrasonic device and a five-element ultrasound probe similar to that described previously (28,29). The probe consisted of a 1-MHz broadband pulse emitter and four regularly spaced receivers (range, 33.0–40.5 mm) and was positioned over the midline of the posterior aspect of the Achilles tendon, with the emitter placed 1 cm above the calcaneal attachment. The probe was maintained in close contact with the skin using a coupling medium and elasticized straps (Fig. 1). The received ultrasonic signals were digitized at 10 MHz, and the time of flight of the first arriving transient signal between receivers was estimated using the first zero crossing criterion (2). Average acoustic velocity was subsequently calculated given the known distance between receivers and the measured time of flight. The reported error in predicting applied tensile force in tendon from direct measures of acoustic velocity is typically G2% (4). Protocol. Participants reported to the gait laboratory wearing lightweight, comfortable clothing and having abstained from vigorous physical activity on the day of testing. The skin overlying the posterior Achilles tendon and lateral aspect of the right shank was shaved and cleaned using standard alcohol abrading methods. After fixation of the probe and electrogoniometer to the right leg, participants were afforded a 10-min treadmill acclimatization session. During the acclimatization session, participants were instructed to adjust the speed of the treadmill to a ‘‘comfortable’’ walking pace using a previously outlined method (30). The defined gait speed was subsequently used to evaluate acoustic velocity in the Achilles tendon during shod and unshod (barefoot) gait conditions. The order of each gait condition was randomized between participants, and each gait condition was followed by a rest period in which ankle angle was measured during quiet bipedal stance.
A standard running shoe (Oregon; Adidas, Herzogenaurach, Germany) ranging in size between US 9.5 and 11.5 (length 29.4–30.9 cm) and mass between 359 and 396 g, with identical, flexible mesh uppers and incorporating a single density ethylene vinyl acetate (EVA) midsole and rubber outsole were used for the shod condition. The midsole and outsole hardness of the shoes was 60 T 1 and 88 T 1, respectively, as determined by a Shore A Durometer, which measures resistance to indentation on a dimensionless scale ranging from 0 to 100. All shoes were made by the same manufacturer and had a heel offset (elevation) of 10 mm (forefoot height, 17.0–19.5 mm; heel height, 27.0–29.5 mm). After 5 min of shod and unshod steady-state walking, acoustic velocity in the right Achilles tendon, vertical ground reaction force, and basic temporospatial gait data were sampled over a 10-s period and at a rate 100 Hz. Data reduction and statistical analysis. Proprietary software (Zebris Medical GmbH, Isny, Germany) was used to calculate mean temporospatial gait parameters including cadence, step and stride length, step width, foot rotation, stance and stride times and swing phase, and single and double support durations (Table 1). With the exception of stride and stance times, temporal data were expressed as a percentage of the gait cycle. Vertical ground reaction force data were exported in ASCII format, and custom computer code (Matlab R2012a; MathWorks, Natick, MA) was subsequently used to identify the magnitude (FZ1–FZ3) and timing (TFZ1–TFZ3) of conventional vertical ground reaction force peaks for each step (Fig. 2). The relative time to each force maxima and topic minima was expressed as a percentage of the stance phase duration. Peak force loading rate (PFLR), defined as the greatest rate of force change during the first 20 ms of the gait cycle, was calculated using previously outlined methods (32), whereas the total foot impulse was estimated by numerical integration of the vertical ground reaction force with respect to time (40). Topic maxima and minima in acoustic data were analyzed, and the peak rate of change in acoustic velocity during loading of the Achilles tendon was also calculated using custom computer code. Mean values were calculated for all steps recorded within the 10-s data capture period, which equated
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TABLE 1. Mean temporospatial (SD) gait parameters during barefoot and shod walking. Barefoot Global Velocity (kmIhj1) Cadence (stepsIminj1) Spatial Stride length (cm) Step width (cm) Step length (cm) Temporal Stride time (ms) Step time (ms) Stance phase (%) Swing phase (%) Single support (%) Double support (%)
Shod
3.4 (0.7) 101.6 (12.6)
3.4 (0.7) 96.7* (12.9)
110.1 (12.8) 10.7 (2.2) 54.8 (6.3)
115.2* (11.1) 10.6 (2.1) 57.2* (4.4)
1202 774 64 36 35 29
1268* 865* 68* 32* 32* 35*
(102) (158) (3) (3) (2) (5)
(92) (191) (3) (3) (3) (5)
*Indicates a statistically significant difference between barefoot and shod conditions (P G 0.05).
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FIGURE 2—Illustration of vertical ground reaction force parameters calculated from the instrumented treadmill system. The force–time integral, or total foot impulse, is represented by the area under the curve, whereas the PFLR was the maximum rate of force change within the first 20 ms of the gait cycle. Note that time to force maxima (TFZ1 and TFZ3) and topic minima (TFZ2) was expressed as a percentage of the stance phase duration.
to an average of 12.1 T 1.6 steps during barefoot walking and 11.3 T 1.7 steps during shod walking. The Statistical Package for the Social Sciences (SPSS Inc., Chicago, IL) was used for all statistical procedures. Kolmogorov–Smirnov tests were used to evaluate data for underlying assumptions of normality. Outcome variables were determined to be normally distributed, so means and SD were used as summary statistics. Paired t-tests were used to evaluate potential differences in acoustic parameters, cadence, stride length, step width, double support, and gait cycle duration. For all other variables, differences between shod and unshod conditions were assessed using repeatedmeasures ANOVA within a generalized linear modeling framework. In each case, condition (shod and barefoot) and limb (left and right) were treated as within-subject factors. Underlying assumptions regarding the uniformity of the variance–covariance matrix were assessed using Mauchly test of sphericity. When the assumption of uniformity was violated, an adjustment to the degrees of freedom of the F-ratio was made using Greenhouse–Geisser Epsilon, thereby making the F-test more conservative. Because there were no statistically significant main effects for limb, only data for the right limb have been presented. An alpha level of 0.05 was used for all tests of significance.
RESULTS Running shoes increased mean ankle plantarflexion by 4- T 2- during quiet bipedal stance and resulted in a significant decrease in cadence and duration of single support and an increase in step length, stance duration, double support, peak vertical ground reaction force, and PFLR during treadmill walking when compared with barefoot walking (Tables 1 and 2).
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TABLE 2. Mean (SD) vertical ground reaction forces during barefoot and shod walking. Barefoot FZ1 (N) FZ2 (N) FZ3 (N) TFZ1 (%) TFZ2 (%) TFZ3 (%) PFLR (BWIsj1) FTI (NIs)
842 (132) 714 (151) 856 (113) 29 (4) 50 (3) 74 (4) 174 (51) 476 (103)
Shod 890* 745* 890* 30 49 72* 108* 521*
(123) (146) (104) (4) (3) (5) (46) (104)
*Indicates a statistically significant difference between barefoot and shod conditions (P G 0.05). BW, body weight; FTI, total foot impulse.
Acoustic velocity in the Achilles tendon was highly reproducible during heel–toe walking and was characterized by two maxima (P1, P2) and two topic minima (M1, M2) (Fig. 3). The mean–within-subject coefficient of variation for acoustic maxima and minima during steady-state walking ranged between 0.2% T 0.1% and 1.0% T 0.6%. Although there was no significant difference in minimum acoustic velocity (M1, M2) with footwear (Table 3), peak acoustic velocity in the right Achilles tendon (P1, P2) was significantly higher with running shoes with a 10-mm heel offset. There was no significant difference in the peak rate of change in acoustic velocity in the Achilles tendon during loading in barefoot and shod conditions.
DISCUSSION Peak acoustic velocity of the Achilles tendon in the current study was comparable with that reported previously for human tendon (,1900–2050 mIsj1) (28,29) and was of a similar pattern to the force in the Achilles tendon measured directly with implanted force transducers during walking (12,18). As described by Komi (18), force in the Achilles tendon is typically reduced after heel contact and is followed by a second steep rise in tendon load during the stance. In the current study, both the first and second peaks in acoustic
FOOTWEAR INCREASES ACHILLES TENDON LOADING
Acoustic Velocity
Barefoot
P1 (mIsj1) P2 (mIsj1) M1 (mIsj1) M2 (mIsj1) Rate of acoustic velocity (mIsj2)
1920 2022 1860 1814 13,112
(67) (92) (85) (89) (3353)
Shod 1943* 2047* 1865 1852 13,923
(55) (71) (58) (54) (3925)
*Indicates a statistically significant difference between barefoot and shod conditions (P G 0.05).
velocity (P1, P2) were highly reproducible during steadystate walking (mean within-subject coefficient of variation G1%), which is consistent with earlier observations that the peak-to-peak amplitude of Achilles tendon force is invariant across a range of walking speeds (1.1–1.8 mIsj1) (12). In contrast to our hypothesis, however, peak acoustic velocity in the Achilles tendon was significantly higher during shod compared with barefoot, treadmill walking, suggesting that standard running shoes with a 10-mm heel elevation increase tensile load in the Achilles tendon during walking. Although the present experimental setup did not allow for a mechanistic explanation for the increase in acoustic velocity of the Achilles tendon observed during shod gait, previous research has highlighted the potential influence of heel elevation, through high-heeled shoes (8.5–10 cm), to increase muscular activity and cocontraction of several lower limb muscles during overground walking (25,37). However, consistent effects of high-heeled shoes on lower leg muscular activity, particularly of the triceps surae, are not universally reported, and the electromyographic effects of heel offsets commonly used in traditional running shoes are even less clear (37). Although Scott et al. (35) detected a small but statistically significant increase in peak EMG activity of only the medial gastrocnemius between walking barefoot and with standard running shoes (heel offset, 20 mm), others have found no significant differences during running with heel offsets of 18 mm (11). Although the effects of standard running shoes on muscle activity may be mediated, in part, by midsole properties (39), quantification of tensile force based on the surface EMG remains elusive, particularly during dynamic activities such as gait (8). It is noteworthy that the shoes used in this study resulted in significant changes in several basic gait parameters. Consistent with previous research investigating footwear effects in running (3,7,17), shod walking in the current study was characterized by a lower cadence (j5 steps per minute), greater stride (5%) and step length (5%), and longer step duration (12%) than barefoot, despite walking at identical speeds. When expressed as a percentage of the gait cycle, participants adopted a relatively longer stance phase duration (4%) and shorter swing phase (j4%) during shod walking when compared with barefoot gait. The footwear used in this study also increased ankle plantarflexion by approximately 4- during quiet bipedal stance. Although changes in static ankle angle with footwear may not reflect dynamic changes during gait, comparable changes in peak ankle plantarflexion have been reported previously during walking with elevation of the heel (18 mm) and with standard running shoes (11). Farris et al. (11) proposed that the
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FIGURE 3—Typical acoustic velocity recorded in the right Achilles tendon during barefoot (dashed line) and shod (solid line) walking at a matched gait speed. Shaded bands indicate stance phase. Note that the acoustic velocity in the Achilles tendon was characterized by two maxima (P1, P2) and two minima (M1, M2) during each gait cycle.
TABLE 3. Mean (SD) acoustic velocity in the right Achilles tendon during shod and unshod walking.
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resultant ankle plantarflexion with heel elevation (18 mm) effectively lengthened the Achilles tendon moment arm and thereby reduced loading in the Achilles tendon. The results of the current study, however, tend not to support this concept, because the increase in static ankle plantarflexion observed with footwear in the current study was accompanied by an increase in acoustic velocity of the Achilles tendon during gait. Interestingly, although studies using 2D imaging-based estimates have suggested that the Achilles tendon moment arm is increased with ankle plantarflexion (24), more recent estimates using 3D imaging techniques have shown the opposite effect, with Achilles tendon moment arm either unchanged or even decreased with ankle plantarflexion (15,36). It should be noted that measures of acoustic velocity, as used in the current study, neither are predicated on estimates of the tendon moment arm nor require assumptions regarding the contribution of agonist and antagonist muscles to the net ankle joint moment, both of which have been shown to induce substantial errors in estimates of tendon loading (13,36). Shod walking in the current study was characterized by higher active vertical ground reaction forces (5%–7%) and a lower external PFLR (38%–44%) when compared with the barefoot walking. Although running shoes have been previously reported to lower peak external force loading rates during running (7,17), we observed no significant difference in the peak rate of acoustic transmission in the Achilles tendon between shod and barefoot conditions. Thus, peak external force loading rates as defined in the current study do not necessarily correspond with internal loading rates of the Achilles tendon during walking. Moreover, although standard running shoes acted to increase the magnitude of tensile load in the Achilles tendon during walking, they would seem to have a negligible influence on the rate of Achilles tendon loading. The use of acoustic transmission techniques to investigate the effect of running shoes on Achilles tendon loading is not without limitation. The propagation of acoustic waves in soft tissue media is influenced by several factors, including the density, temperature, hydration, and bulk modulus of the tissue through which it passes (26). Although tendon hydration and temperature may reasonably be assumed to be stable during shod and barefoot gait conditions in the current study, there is evidence, albeit in animal models, that the composition of the Achilles tendon may vary along its length (6). Thus, it is unknown whether the effects of footwear observed in the current study are applicable to the entire tendon structure. Similarly, the mechanical properties and response of the Achilles tendon to load may differ between sexes and over the lifespan (19,22). Although gender differences in tendon properties are not universally reported (27), it is important to note that this study was
limited to evaluating the effects of a standard running shoe in a small sample of healthy adult males walking at a single (preferred) gait speed and on the same day. The effect of footwear observed in the current study, therefore, may have represented a transient response and may not be directly transferable to Achilles tendon loading with habitual use in children, females, older cohorts, or at markedly faster or slower gait speeds. Similarly, although the ‘‘cushioning’’ properties and bending stiffness of running shoes have been suggested to influence muscle activity and gearing at the ankle joint (3,39), this study evaluated only a single shoe design that incorporated a hard midsole material (Shore A Durometer, 60 T 1) and a 10-mm heel offset. Consequently, the effects of individual components of the shoe, such as midsole cushioning and effective heel offset, on tendon loading could not be elucidated. Moreover, treadmill systems are known to induce both spatial and temporal constraints on gait and have been shown by some to alter neuromuscular coordination and subsequent lower extremity joint moments and powers during walking (21). Although other research has shown treadmill walking has negligible effect on fascicle behavior of the triceps surae when compared with overground walking (5), the findings of this study may not necessarily be representative of unconstrained walking in ‘‘real-world’’ settings outside of the laboratory. Nonetheless, the findings of the current study suggest that, in comparison to barefoot walking, standard running shoes with a 10-mm heel offset induce global changes in vertical ground reaction force and temporospatial gait parameters in healthy adults that act to increase tensile load in the Achilles tendon. Although further research elucidating potential mechanisms underpinning the observed effect is required, the results of this study raise questions as to the potential preventative and therapeutic effects of standard running shoes in the management of Achilles tendinopathy.
CONCLUSIONS This study is the first to show that standard running shoes increase Achilles tendon loading, as defined by an increase in acoustic velocity, during treadmill walking. These findings question the potential role of standard running shoes in the prevention and therapeutic management of Achilles tendinopathy and suggest that footwear with a 10-mm heel offset may increase loading in the Achilles tendon during gait. This research received financial support from the Queensland Academy of Sport and the Australian Institute of Sport. The authors declare no conflicts of interest, financial or otherwise. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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2. Bossy E, Talmant M, Laugier P. Effect of bone cortical thickness on velocity measurements using ultrasonic axial transmission: a 2-D simulation study. J Acoust Soc Am. 2002;112:297–307.
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FOOTWEAR INCREASES ACHILLES TENDON LOADING
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