This article was downloaded by: [University of Nebraska, Lincoln] On: 06 April 2015, At: 12:18 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Journal of Sports Sciences Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/rjsp20
Relationship between Achilles tendon properties and foot strike patterns in long-distance runners a
b
b
b
b
Keitaro Kubo , Daisuke Miyazaki , Shigeharu Tanaka , Shozo Shimoju & Naoya Tsunoda a
Department of Life Science, The University of Tokyo, Meguro, Tokyo, Japan
b
Faculty of Physical Education, Kokushikan University, Tokyo, Japan Published online: 03 Oct 2014.
Click for updates To cite this article: Keitaro Kubo, Daisuke Miyazaki, Shigeharu Tanaka, Shozo Shimoju & Naoya Tsunoda (2015) Relationship between Achilles tendon properties and foot strike patterns in long-distance runners, Journal of Sports Sciences, 33:7, 665-669, DOI: 10.1080/02640414.2014.962576 To link to this article: http://dx.doi.org/10.1080/02640414.2014.962576
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Sports Sciences, 2015 Vol. 33, No. 7, 665–669, http://dx.doi.org/10.1080/02640414.2014.962576
Relationship between Achilles tendon properties and foot strike patterns in long-distance runners
KEITARO KUBO1, DAISUKE MIYAZAKI2, SHIGEHARU TANAKA2, SHOZO SHIMOJU2 & NAOYA TSUNODA2 1
Department of Life Science, The University of Tokyo, Meguro, Tokyo, Japan and 2Faculty of Physical Education, Kokushikan University, Tokyo, Japan
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
(Accepted 1 September 2014)
Abstract The purpose of this study was to investigate the relationship between Achilles tendon properties and foot strike patterns in long-distance runners. Forty-one highly trained male long-distance runners participated in this study. Elongation of the Achilles tendon and aponeurosis of the medial gastrocnemius muscle were measured using ultrasonography, while the participants performed ramp isometric plantar flexion up to the voluntary maximum. The relationship between the estimated muscle force and tendon elongation during the ascending phase was fit to a linear regression, the slope of which was defined as stiffness. In addition, the cross-sectional area of the Achilles tendon was measured using ultrasonography. Foot strike patterns (forefoot, midfoot and rearfoot) during running were determined at submaximal velocity (18 km · h−1) on a treadmill. The number of each foot strike runner was 12 for the forefoot (29.3%), 12 for the midfoot (29.3%) and 17 for the rearfoot (41.5%). No significant differences were observed in the variables measured for the Achilles tendon among the three groups. These results suggested that the foot strike pattern during running did not affect the morphological or mechanical properties of the Achilles tendon in long-distance runners. Keywords: plantar flexor, tendon stiffness, cross-sectional area, economy
Introduction Widespread interest has recently developed in the foot strike patterns of recreational and competitive endurance runners (e.g. Lieberman et al., 2010). Three patterns of foot striking have been commonly described in the literature (Hasegawa, Yamauchi, & Kraemer, 2007; Larson et al., 2011): (1) rearfoot strike, in which the heel contacts the ground first; (2) midfoot strike, in which the heel and ball of the foot contact the ground simultaneously; and (3) forefoot strike, in which the ball of the foot contacts the ground before the heel comes down. Based on the previous findings (Hasegawa et al., 2007; Hayes & Caplan, 2012; Larson et al., 2011), forefoot (and midfoot) strike runners may be faster than rearfoot strike runners as a result of the greater storage and release of elastic energy from the foot arch and Achilles tendon. Furthermore, previous cross-sectional and longitudinal studies demonstrated that more economical runners had more compliant tendon structures (Arampatzis et al., 2006; Kubo, Tabata, Ikebukuro, Igarashi, & Tsunoda, 2010).
Therefore, the elastic properties of the Achilles tendon for forefoot (and midfoot) strike runners may be suitable for storing elastic energy during running. However, other studies reported that the ankle joint moment was greater for forefoot strike runners than for rearfoot strike runners during the first half of the stance phase (Almonroeder, Willson, & Kernozek, 2013; Kulmala, Avela, Pasanen, & Parkkari, 2013; Rooney & Derrick, 2013; Williams, McClay, & Manal, 2000). Therefore, differences in the stress imposed on the Achilles tendon among these strike patterns may lead to differences in the size and elastic properties of the Achilles tendon in long-distance runners. The cross-sectional area of the Achilles tendon of long-distance runners was previously shown to be significantly greater than that of untrained subjects (e.g. Magnusson & Kjaer, 2003). Furthermore, mechanical stress was found to be important for changes in tendon stiffness (Arampatzis, Karamanidis, & Albracht, 2007; Kubo et al., 2006). For example, we previously reported that an isotonic training regimen using high loads
Correspondence: Keitaro Kubo, Department of Life Science (Sports Sciences), The University of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan. E-mail: [email protected] © 2014 Taylor & Francis
666
K. Kubo et al. Table I. The physical characteristics, duration of training experience, best official record of the three groups.
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
Age (years) Height (cm) Body mass (kg) Duration of training experience (years) Best official record in a 5000 m race (m:s)
Forefoot strike
Midfoot strike
Rearfoot strike
Mean (s)
Mean (s)
Mean (s)
20.4 169.8 57.1 6.5 14:58
(1.3) (5.2) (4.7) (1.9) (0:31)
increased tendon stiffness, whereas that using low loads with vascular occlusion did not (Kubo et al., 2006). Based on these findings, we hypothesised that the Achilles tendon of forefoot strike runners was larger and stiffer than that of rearfoot strike runners. As described earlier, two opposing hypotheses may exit. In any case, the strike pattern may be related to the morphological and elastic properties of the Achilles tendon. In the present study, we investigated the relationship between Achilles tendon properties (i.e. maximal strain, stiffness and cross-sectional area) and foot strike patterns in highly trained long-distance runners.
Methods Participants Forty-one highly trained male long-distance runners participated in this study. The duration of training experience was 7.3 ± 2.7 years. The best official record in a 5000 m race within 1 year prior to these tests ranged from 14:11 to 16:15 (14:56 ± 0:28) (min:s). Throughout one year, the participants of this study ran from 150 to 200 km per week on average (at least 6 days · week−1, up to 4 h · day−1). We confirmed that all participants did not change foot strike patterns during running at the beginning of this study. The participants were fully informed of the procedures to be utilised as well as the purpose of this study. Written informed consent was obtained from all participants. This study was approved by the office of the Department of Sports Sciences, University of Tokyo, and complied with their requirements for human experimentation.
Foot strike pattern during running The foot strike pattern during shod running was determined at submaximal velocity (18 km · h−1) on a treadmill (AR-100, Minato Medical Science, Osaka, Japan). After a warm-up period of 4 min at a running velocity of 10 km · h−1, the subjects ran at three submaximal velocities (14, 16 and 18 km · h−1) for 4 min. At the final phase (approximately 30 s) at
20.6 170.7 56.7 8.4 14:59
(1.3) (4.9) (4.0) (2.0) (0:31)
20.6 170.9 58.5 7.3 14:52
(1.0) (5.6) (4.2) (3.3) (0:24)
P values
Effect size
0.932 0.868 0.507 0.222 0.807
0.167 0.210 0.419 0.792 0.222
a speed of 18 km · h−1, a sagittal image of the entire stance phase of the foot of runners was obtained using a high-speed video camera (sampling rate 250 Hz; VCC-H1600C, Digimo, Tokyo, Japan) placed on the right side of the treadmill. We confirmed that all steps were the same foot strike pattern in each participant. Following the criteria of Hasegawa et al. (2007), participants were divided into three groups according to their foot strike patterns: forefoot, midfoot and rearfoot strike runners. Forefoot strike was defined as a foot strike in which the ball of the foot contacts the ground before the heel comes down. Midfoot strike was defined as a foot strike in which the heel and ball of the foot contact the ground simultaneously. Rearfoot strike was defined as a foot strike in which the heel contacts the ground first. The physical characteristics of the three groups are summarised in Table I.
Elastic properties of the Achilles tendon The maximal voluntary isometric strength (MVC) of plantar flexor muscles was determined using a specially designed dynamometer (Applied Office, Tokyo, Japan). The participant lay prone on a test bench, and the waist and shoulders were secured by adjustable lap belts and held in position. In the present study, we measured the right lower limb due to the limitation of used equipment. According to our previous studies (e.g. Kubo et al., 2007, 2009), there were no differences in the tendon properties between the right and left limbs for untrained subjects. We considered that there were also no differences in the tendon properties between the both sides for longdistance runners, since they used the lower limbs of both side in the same way. The right ankle joint was set at 90° (anatomical position) with the knee joint at full extension, and the foot was securely strapped to a foot plate connected to the lever arm of the dynamometer. Prior to the test, the participant performed a standardised warm-up and submaximal contractions to become accustomed to the test procedure. The centre of rotation of the dynamometer was visually aligned with the centre of rotation of the ankle joint
667
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
Foot strike pattern and tendon property in runner
Fm¼k _TQ _MA
1
where k is the relative contribution of the physiological cross-sectional area of the medial gastrocnemius muscle within plantar flexor muscles (Fukunaga, Roy, Shellock, Hodgson, & Edgerton, 1996) and MA is the moment arm length of the triceps surae muscles at 90° of the ankle joint, which is estimated from the lower leg length of each subject (Grieve, Pheasant, & Cavagna, 1978). Figure 1 presents a typical example of the relationship between Fm and L. The Fm–L relation in the tendon structure was curvilinear consisting of an initial region (toe-region) characterised by a large increase in L with increasing force and a linear region immediately after the toe-region. In this study, Fm and L above 50% of MVC were fitted to a linear regression equation, the slope of which was adopted as stiffness (Kubo et al., 2006, 2010).
400
100%MVC
300
Fm (N)
under submaximal isometric plantar flexion. The participant was instructed to develop a gradually increasing force from a relaxed state to MVC within 5 s. The task was repeated two times per participant with at least 3 min between trials. A real-time ultrasonic apparatus (SSD-6500, Aloka, Japan) was used to obtain a longitudinal ultrasonic image of the medial gastrocnemius muscle at a level of 30% of the lower leg length, from the popliteal crease to the centre of the lateral malleolus. Ultrasonic images were recorded on videotape at 30 Hz and synchronised with recordings of a clock timer for subsequent analyses. The point at which one fascicle was attached to the aponeurosis was visualised on these images. The displacement of this point was considered to indicate the lengthening of tendon structures (deep aponeurosis and distal tendon). Additional measurements were taken under passive conditions to correct measurements taken for the tendon and aponeurosis elongation. The displacement of each site obtained from the ultrasound images could be corrected for that attributed to joint rotation alone for each participant. Only values corrected for angular rotation were reported in the present study. To calculate strain values from the measured elongation (L), we measured the initial length of tendon structures, from the measured site (position of the probe) to the insertion of the Achilles tendon at 90° of the ankle angle. The torque (TQ) measured by the dynamometer during isometric plantar flexion was converted to muscle force (Fm) using the following equation:
Stiffness (N · mm–1)
200
50%MVC
100
0 0
5
10
15
20
L (mm) Figure 1. Typical example of estimated muscle force (Fm)–tendon elongation (L) relation in medial gastrocnemius muscle.
earlier. The cross-sectional area of the Achilles tendon was measured by an ultrasonic apparatus (SSD6500, Aloka, Japan) at the height of the lateral malleolus of the Achilles tendon. An outline of the tendon was traced from the cross-sectional image, and the traced image was transferred to a computer to calculate the cross-sectional area of the tendon using an open-source image analysis software (Image J, NIH, Bethesda, MD). Statistics Descriptive data represent mean ± s. Any significant differences in the measured variables (maximal elongation, strain and stiffness of tendon structures, and cross-sectional area of the Achilles tendon) among the three groups were tested using a one-way ANOVA. Effects size was calculated for relevant variables. The level of significance was set at P < 0.05. Results The number of each foot strike runner was 12 for forefoot (29.3%), 12 for midfoot (29.3%) and 17 for rearfoot (41.5%). No significant differences were observed in the physical characteristics, duration of training experience or best official record in a 5000 m race among the three groups (Table I). No significant differences were also noted in the measured variables of the Achilles tendon among the three groups (Table II). Discussion
Tendon cross-sectional area The participant’s posture was the same as that for the measurement of tendon properties described
This study demonstrated that there were no significant differences in the cross-sectional area or stiffness of the Achilles tendon among forefoot, midfoot
668
K. Kubo et al. Table II. The measured variables of Achilles tendon of the three groups.
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
Maximal tendon elongation (mm) Maximal tendon strain (%) Stiffness of tendon structures (N · mm−1) Cross-sectional area of tendon (mm2)
Forefoot strike
Midfoot strike
Rearfoot strike
Mean (s)
Mean (s)
Mean (s)
18.1 6.8 30.6 74.8
(3.6) (1.3) (9.6) (10.6)
and rearfoot runners. To the best of our knowledge, this is the first study to investigate the relationship between Achilles tendon properties and foot strike patterns. Although over 85% of recreational runners (Kasmer, Liu, Roberts, & Valadao, 2013; Larson et al., 2011) make initial contact with the heel first, a higher percentage of both midfoot and forefoot strike runners was observed among elite long-distance runners (Hasegawa et al., 2007; Kasmer et al., 2013). In the present study, the distribution of foot strike patterns was different from that of recreational runners, because the participants in this study were highly trained long-distance runners. As one of the reasons for this phenomenon, it has been suggested that the forefoot strike pattern may be faster than the rearfoot strike pattern as a result of greater storage and release of elastic energy from the foot arch and Achilles tendon (Hasegawa et al., 2007; Hayes & Caplan, 2012; Larson et al., 2011). Based on the findings of cross-sectional and longitudinal studies (Arampatzis et al., 2006; Kubo et al., 2010), more economical runners were found to have more compliant tendon structures. Therefore, we hypothesised at the beginning of this study that the Achilles tendon of forefoot and midfoot strike runners may be more compliant than that of rearfoot strike runners. However, this hypothesis was rejected. Except for the Achilles tendon, the elastic property of the arch is another factor that may contribute to differences in running performance and economy between forefoot (and midfoot) and rearfoot strike runners. Ker, Bennet, Bibby, Kester, and Alexander (1987) stated that 17% or slightly more of the total energy turnover per step was stored as strain energy in the compliant elements of the arch of the foot. The forefoot strike may permit more elastic energy storage and recoil in the longitudinal arch, whereas rearfoot strike runners experience little or no arch compression at impact (Perl, Daoud, & Lieberman, 2012). However, to the best of our knowledge, there is no experimental evidence of this advantage for running performance and economy for forefoot strike runners. In future studies, we need to investigate the relationship between foot strike patterns and mechanical properties of the arch.
18.2 6.6 29.8 75.7
(2.7) (1.1) (6.7) (11.7)
17.7 6.4 32.5 76.2
(2.4) (0.9) (8.9) (12.6)
P values
Effect size
0.898 0.612 0.801 0.873
0.172 0.364 0.321 0.120
A previous study reported that elite long-distance runners generally run 90–150 km a week (Holmich, Darre, Jahnsen, & Hartvig-Jensen, 1988). Hence, it is likely that the Achilles tendon of highly trained long-distance runner is imposed the great mechanical stress during running training. Recent studies showed that ankle joint moment was greater in forefoot strike runners than in rearfoot strike runners during the first half of the stance phase (Almonroeder et al., 2013; Kulmala et al., 2013; Rooney & Derrick, 2013; Williams et al., 2000). Therefore, we may say that the Achilles tendon of forefoot strike runners was imposed a greater mechanical stress than that of rearfoot strike runners. In the last decade, several studies have used ultrasonography to investigate the effects of resistance training on the elastic properties of human tendons in vivo (Arampatzis et al., 2007; Kubo et al., 2006). Among these, mechanical stress was found to be important for changes in the elastic properties of human tendons, that is, stiffness. Accordingly, we hypothesised that the Achilles tendon of forefoot strike runners was larger and stiffer than that of rearfoot strike runners. In the present study, however, there were no differences in cross-sectional area or stiffness of the Achilles tendon among the three different strike pattern runners. De Zee, BojsenMoller, and Voigt (2000) showed using in vitro experiments that the tendon properties of pigs hardly changed during 1600 cycles of dynamic loading used as an input of a model to predict dynamic creep in the human Achilles tendon during running of a marathon. Furthermore, Peltonen, Cronin, Avela, and Finni (2010) reported that the mechanical properties of the human Achilles tendon did not change after two-legged hopping exercise consisting of 1150–2600 high impacts until exhaustion. The finding of a cross-sectional study (Kubo, Tabata, Ikebukuro, Igarashi, Yata, et al., 2010) indicated that the tendons of long-distance runners were less extensible than those of untrained subjects for knee extensors, but not for plantar flexors. Taking these previous findings into account together with the present results, the morphological and elastic properties of the Achilles tendon may not be affected by repetitive exercise such as endurance running.
Foot strike pattern and tendon property in runner In conclusion, the results of this study indicated that foot strike patterns were not related to the crosssectional area and stiffness of the Achilles tendon in highly trained long-distance runners. Further investigations are needed to clarify the relationship between foot strike patterns and other factors, that is, mechanical properties of the arch. Funding This study was supported by a Grant-in-Aid for Young Scientists (A) (21680047 to K. Kubo) from Japan Society for the Promotion of Science.
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
References Almonroeder, T., Willson, J. D., & Kernozek, T. W. (2013). The effect of foot strike pattern on Achilles tendon load during running. Annals Biomedical Engineering, 41, 1758–1766. Arampatzis, A., DeMonte, G., Karamanidis, K., Morey-Klapsing, G., Stafilidis, S., & Bruggemann, G. P. (2006). Influence of the muscle-tendon unit’s mechanical and morphological properties on running economy. Journal of Experimental Biology, 209, 3345–3357. Arampatzis, A., Karamanidis, K., & Albracht, K. (2007). Adaptational responses of the human Achilles tendon by modulation of the applied cyclic strain magnitude. Journal of Experimental Biology, 210, 2743–2753. De Zee, M., Bojsen-Moller, F., & Voigt, M. (2000). Dynamic viscoelastic behavior of lower extremity tendons during simulated running. Journal of Applied Physiology, 89, 1352–1359. Fukunaga, T., Roy, R. R., Shellock, F. G., Hodgson, J. A., & Edgerton, V. R. (1996). Specific tension of human plantar flexors and dorsiflexors. Journal of Applied Physiology, 80, 158– 165. Grieve, D. W., Pheasant, S., & Cavagna, P. R. (1978). Prediction of gastrocnemius length from knee and ankle joint posture. In E. Asmussen & K. Jorgensen (Eds.), Biomechanics VI: Proceeding of the sixth international congress of biomechanics, Copenhagen, Denmark (pp. 405–412). Baltimore, MD: University Park. Hasegawa, H., Yamauchi, T., & Kraemer, W. J. (2007). Foot strike patterns of runners at the 15-km point during an elitelevel half marathon. Journal of Strength and Conditioning Research, 21, 888–893. Hayes, P., & Caplan, N. (2012). Foot strike patterns and ground contact times during high-calibre middle-distance races. Journal of Sports Sciences, 30, 1275–1283. Holmich, P., Darre, E., Jahnsen, F., & Hartvig-Jensen, T. (1988). The elite marathon runner: Problems during and after competition. British Journal of Sports Medicine, 22, 19–21. Kasmer, M. E., Liu, X. C., Roberts, K. G., & Valadao, J. M. (2013). Foot-strike pattern and performance in a marathon.
669
International Journal of Sports Physiology and Performance, 8, 286–292. Ker, R. F., Bennet, M. B., Bibby, S. R., Kester, R. C., & Alexander, R. M. (1987). The spring in the arch of the human foot. Nature, 325, 147–149. Kubo, K., Ikebukuro, T., Yaeshima, K., Yata, H., Tsunoda, N., & Kanehisa, H. (2009). Effects of static and dynamic training on the stiffness and blood volume of tendon in vivo. Journal of Applied Physiology, 106, 412–417. Kubo, K., Komuro, T., Ishiguro, N., Tunoda, N., Sato, Y., Ishii, N., & Fukunaga, T. (2006). Effects of low load resistance training with vascular occlusion on the mechanical properties of muscle and tendon. Journal of Applied Biomechanics, 22, 112– 119. Kubo, K., Morimoto, M., Komuro, T., Yata, H., Tsunoda, N., Kanehisa, H., & Fukunaga, T. (2007). Effects of plyometric and weight training on muscle-tendon complex and jump performance. Medicine and Science in Sports and Exercise, 39, 1801– 1810. Kubo, K., Tabata, T., Ikebukuro, T., Igarashi, K., & Tsunoda, N. (2010). A longitudinal assessment of running economy and tendon properties in long distance runners. Journal of Strength and Conditioning Research, 24, 1724–1731. Kubo, K., Tabata, T., Ikebukuro, T., Igarashi, K., Yata, H., & Tsunoda, N. (2010). Effects of mechanical properties of muscle and tendon on performance in long distance runners. European Journal of Applied Physiology, 110, 507–514. Kulmala, J.-P., Avela, J., Pasanen, K., & Parkkari, J. (2013). Forefoot strikers exhibit lower running-induced knee loading than rearfoot strikers. Medicine and Science in Sports and Exercise, 45, 2306–2313. Larson, P., Higgins, E., Kaminski, J., Decker, T., Preble, J., Lyons, D., … Normile, A. (2011). Foot strike patterns of recreational and sub-elite runners in a long-distance road race. Journal of Sports Sciences, 29, 1665–1673. Lieberman, D. E., Venkadesan, M., Werbel, W. A., Daoud, A. I., D’Andrea, S., Davis, I. S., … Pitsiladis, Y. (2010). Foot strike patterns and collision forces in habitually barefoot versus shod runners. Nature, 463, 531–535. Magnusson, S. P., & Kjaer, M. (2003). Region-specific differences in Achilles tendon cross-sectional area in runners and non-runners. European Journal of Applied Physiology, 90, 549– 553. Peltonen, J., Cronin, N. J., Avela, J., & Finni, T. (2010). In vivo mechanical response of human Achilles tendon to a single bout of hopping exercise. Journal of Experimental Biology, 213, 1259– 1265. Perl, D. P., Daoud, A. I., & Lieberman, D. E. (2012). Effects of footwear and strike type on running economy. Medicine and Science in Sports and Exercise, 44, 1335–1343. Rooney, B. D., & Derrick, T. R. (2013). Joint contact loading in forefoot and rearfoot strike patterns during running. Journal of Biomechanics, 46, 2201–2206. Williams, D. S., McClay, I. S., & Manal, K. T. (2000). Lower extremity mechanics in runners with a converted forefoot strike pattern. Journal of Applied Biomechanics, 16, 210–218.
Journal of Sports Sciences Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/rjsp20
Relationship between Achilles tendon properties and foot strike patterns in long-distance runners a
b
b
b
b
Keitaro Kubo , Daisuke Miyazaki , Shigeharu Tanaka , Shozo Shimoju & Naoya Tsunoda a
Department of Life Science, The University of Tokyo, Meguro, Tokyo, Japan
b
Faculty of Physical Education, Kokushikan University, Tokyo, Japan Published online: 03 Oct 2014.
Click for updates To cite this article: Keitaro Kubo, Daisuke Miyazaki, Shigeharu Tanaka, Shozo Shimoju & Naoya Tsunoda (2015) Relationship between Achilles tendon properties and foot strike patterns in long-distance runners, Journal of Sports Sciences, 33:7, 665-669, DOI: 10.1080/02640414.2014.962576 To link to this article: http://dx.doi.org/10.1080/02640414.2014.962576
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Sports Sciences, 2015 Vol. 33, No. 7, 665–669, http://dx.doi.org/10.1080/02640414.2014.962576
Relationship between Achilles tendon properties and foot strike patterns in long-distance runners
KEITARO KUBO1, DAISUKE MIYAZAKI2, SHIGEHARU TANAKA2, SHOZO SHIMOJU2 & NAOYA TSUNODA2 1
Department of Life Science, The University of Tokyo, Meguro, Tokyo, Japan and 2Faculty of Physical Education, Kokushikan University, Tokyo, Japan
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
(Accepted 1 September 2014)
Abstract The purpose of this study was to investigate the relationship between Achilles tendon properties and foot strike patterns in long-distance runners. Forty-one highly trained male long-distance runners participated in this study. Elongation of the Achilles tendon and aponeurosis of the medial gastrocnemius muscle were measured using ultrasonography, while the participants performed ramp isometric plantar flexion up to the voluntary maximum. The relationship between the estimated muscle force and tendon elongation during the ascending phase was fit to a linear regression, the slope of which was defined as stiffness. In addition, the cross-sectional area of the Achilles tendon was measured using ultrasonography. Foot strike patterns (forefoot, midfoot and rearfoot) during running were determined at submaximal velocity (18 km · h−1) on a treadmill. The number of each foot strike runner was 12 for the forefoot (29.3%), 12 for the midfoot (29.3%) and 17 for the rearfoot (41.5%). No significant differences were observed in the variables measured for the Achilles tendon among the three groups. These results suggested that the foot strike pattern during running did not affect the morphological or mechanical properties of the Achilles tendon in long-distance runners. Keywords: plantar flexor, tendon stiffness, cross-sectional area, economy
Introduction Widespread interest has recently developed in the foot strike patterns of recreational and competitive endurance runners (e.g. Lieberman et al., 2010). Three patterns of foot striking have been commonly described in the literature (Hasegawa, Yamauchi, & Kraemer, 2007; Larson et al., 2011): (1) rearfoot strike, in which the heel contacts the ground first; (2) midfoot strike, in which the heel and ball of the foot contact the ground simultaneously; and (3) forefoot strike, in which the ball of the foot contacts the ground before the heel comes down. Based on the previous findings (Hasegawa et al., 2007; Hayes & Caplan, 2012; Larson et al., 2011), forefoot (and midfoot) strike runners may be faster than rearfoot strike runners as a result of the greater storage and release of elastic energy from the foot arch and Achilles tendon. Furthermore, previous cross-sectional and longitudinal studies demonstrated that more economical runners had more compliant tendon structures (Arampatzis et al., 2006; Kubo, Tabata, Ikebukuro, Igarashi, & Tsunoda, 2010).
Therefore, the elastic properties of the Achilles tendon for forefoot (and midfoot) strike runners may be suitable for storing elastic energy during running. However, other studies reported that the ankle joint moment was greater for forefoot strike runners than for rearfoot strike runners during the first half of the stance phase (Almonroeder, Willson, & Kernozek, 2013; Kulmala, Avela, Pasanen, & Parkkari, 2013; Rooney & Derrick, 2013; Williams, McClay, & Manal, 2000). Therefore, differences in the stress imposed on the Achilles tendon among these strike patterns may lead to differences in the size and elastic properties of the Achilles tendon in long-distance runners. The cross-sectional area of the Achilles tendon of long-distance runners was previously shown to be significantly greater than that of untrained subjects (e.g. Magnusson & Kjaer, 2003). Furthermore, mechanical stress was found to be important for changes in tendon stiffness (Arampatzis, Karamanidis, & Albracht, 2007; Kubo et al., 2006). For example, we previously reported that an isotonic training regimen using high loads
Correspondence: Keitaro Kubo, Department of Life Science (Sports Sciences), The University of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan. E-mail: [email protected] © 2014 Taylor & Francis
666
K. Kubo et al. Table I. The physical characteristics, duration of training experience, best official record of the three groups.
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
Age (years) Height (cm) Body mass (kg) Duration of training experience (years) Best official record in a 5000 m race (m:s)
Forefoot strike
Midfoot strike
Rearfoot strike
Mean (s)
Mean (s)
Mean (s)
20.4 169.8 57.1 6.5 14:58
(1.3) (5.2) (4.7) (1.9) (0:31)
increased tendon stiffness, whereas that using low loads with vascular occlusion did not (Kubo et al., 2006). Based on these findings, we hypothesised that the Achilles tendon of forefoot strike runners was larger and stiffer than that of rearfoot strike runners. As described earlier, two opposing hypotheses may exit. In any case, the strike pattern may be related to the morphological and elastic properties of the Achilles tendon. In the present study, we investigated the relationship between Achilles tendon properties (i.e. maximal strain, stiffness and cross-sectional area) and foot strike patterns in highly trained long-distance runners.
Methods Participants Forty-one highly trained male long-distance runners participated in this study. The duration of training experience was 7.3 ± 2.7 years. The best official record in a 5000 m race within 1 year prior to these tests ranged from 14:11 to 16:15 (14:56 ± 0:28) (min:s). Throughout one year, the participants of this study ran from 150 to 200 km per week on average (at least 6 days · week−1, up to 4 h · day−1). We confirmed that all participants did not change foot strike patterns during running at the beginning of this study. The participants were fully informed of the procedures to be utilised as well as the purpose of this study. Written informed consent was obtained from all participants. This study was approved by the office of the Department of Sports Sciences, University of Tokyo, and complied with their requirements for human experimentation.
Foot strike pattern during running The foot strike pattern during shod running was determined at submaximal velocity (18 km · h−1) on a treadmill (AR-100, Minato Medical Science, Osaka, Japan). After a warm-up period of 4 min at a running velocity of 10 km · h−1, the subjects ran at three submaximal velocities (14, 16 and 18 km · h−1) for 4 min. At the final phase (approximately 30 s) at
20.6 170.7 56.7 8.4 14:59
(1.3) (4.9) (4.0) (2.0) (0:31)
20.6 170.9 58.5 7.3 14:52
(1.0) (5.6) (4.2) (3.3) (0:24)
P values
Effect size
0.932 0.868 0.507 0.222 0.807
0.167 0.210 0.419 0.792 0.222
a speed of 18 km · h−1, a sagittal image of the entire stance phase of the foot of runners was obtained using a high-speed video camera (sampling rate 250 Hz; VCC-H1600C, Digimo, Tokyo, Japan) placed on the right side of the treadmill. We confirmed that all steps were the same foot strike pattern in each participant. Following the criteria of Hasegawa et al. (2007), participants were divided into three groups according to their foot strike patterns: forefoot, midfoot and rearfoot strike runners. Forefoot strike was defined as a foot strike in which the ball of the foot contacts the ground before the heel comes down. Midfoot strike was defined as a foot strike in which the heel and ball of the foot contact the ground simultaneously. Rearfoot strike was defined as a foot strike in which the heel contacts the ground first. The physical characteristics of the three groups are summarised in Table I.
Elastic properties of the Achilles tendon The maximal voluntary isometric strength (MVC) of plantar flexor muscles was determined using a specially designed dynamometer (Applied Office, Tokyo, Japan). The participant lay prone on a test bench, and the waist and shoulders were secured by adjustable lap belts and held in position. In the present study, we measured the right lower limb due to the limitation of used equipment. According to our previous studies (e.g. Kubo et al., 2007, 2009), there were no differences in the tendon properties between the right and left limbs for untrained subjects. We considered that there were also no differences in the tendon properties between the both sides for longdistance runners, since they used the lower limbs of both side in the same way. The right ankle joint was set at 90° (anatomical position) with the knee joint at full extension, and the foot was securely strapped to a foot plate connected to the lever arm of the dynamometer. Prior to the test, the participant performed a standardised warm-up and submaximal contractions to become accustomed to the test procedure. The centre of rotation of the dynamometer was visually aligned with the centre of rotation of the ankle joint
667
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
Foot strike pattern and tendon property in runner
Fm¼k _TQ _MA
1
where k is the relative contribution of the physiological cross-sectional area of the medial gastrocnemius muscle within plantar flexor muscles (Fukunaga, Roy, Shellock, Hodgson, & Edgerton, 1996) and MA is the moment arm length of the triceps surae muscles at 90° of the ankle joint, which is estimated from the lower leg length of each subject (Grieve, Pheasant, & Cavagna, 1978). Figure 1 presents a typical example of the relationship between Fm and L. The Fm–L relation in the tendon structure was curvilinear consisting of an initial region (toe-region) characterised by a large increase in L with increasing force and a linear region immediately after the toe-region. In this study, Fm and L above 50% of MVC were fitted to a linear regression equation, the slope of which was adopted as stiffness (Kubo et al., 2006, 2010).
400
100%MVC
300
Fm (N)
under submaximal isometric plantar flexion. The participant was instructed to develop a gradually increasing force from a relaxed state to MVC within 5 s. The task was repeated two times per participant with at least 3 min between trials. A real-time ultrasonic apparatus (SSD-6500, Aloka, Japan) was used to obtain a longitudinal ultrasonic image of the medial gastrocnemius muscle at a level of 30% of the lower leg length, from the popliteal crease to the centre of the lateral malleolus. Ultrasonic images were recorded on videotape at 30 Hz and synchronised with recordings of a clock timer for subsequent analyses. The point at which one fascicle was attached to the aponeurosis was visualised on these images. The displacement of this point was considered to indicate the lengthening of tendon structures (deep aponeurosis and distal tendon). Additional measurements were taken under passive conditions to correct measurements taken for the tendon and aponeurosis elongation. The displacement of each site obtained from the ultrasound images could be corrected for that attributed to joint rotation alone for each participant. Only values corrected for angular rotation were reported in the present study. To calculate strain values from the measured elongation (L), we measured the initial length of tendon structures, from the measured site (position of the probe) to the insertion of the Achilles tendon at 90° of the ankle angle. The torque (TQ) measured by the dynamometer during isometric plantar flexion was converted to muscle force (Fm) using the following equation:
Stiffness (N · mm–1)
200
50%MVC
100
0 0
5
10
15
20
L (mm) Figure 1. Typical example of estimated muscle force (Fm)–tendon elongation (L) relation in medial gastrocnemius muscle.
earlier. The cross-sectional area of the Achilles tendon was measured by an ultrasonic apparatus (SSD6500, Aloka, Japan) at the height of the lateral malleolus of the Achilles tendon. An outline of the tendon was traced from the cross-sectional image, and the traced image was transferred to a computer to calculate the cross-sectional area of the tendon using an open-source image analysis software (Image J, NIH, Bethesda, MD). Statistics Descriptive data represent mean ± s. Any significant differences in the measured variables (maximal elongation, strain and stiffness of tendon structures, and cross-sectional area of the Achilles tendon) among the three groups were tested using a one-way ANOVA. Effects size was calculated for relevant variables. The level of significance was set at P < 0.05. Results The number of each foot strike runner was 12 for forefoot (29.3%), 12 for midfoot (29.3%) and 17 for rearfoot (41.5%). No significant differences were observed in the physical characteristics, duration of training experience or best official record in a 5000 m race among the three groups (Table I). No significant differences were also noted in the measured variables of the Achilles tendon among the three groups (Table II). Discussion
Tendon cross-sectional area The participant’s posture was the same as that for the measurement of tendon properties described
This study demonstrated that there were no significant differences in the cross-sectional area or stiffness of the Achilles tendon among forefoot, midfoot
668
K. Kubo et al. Table II. The measured variables of Achilles tendon of the three groups.
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
Maximal tendon elongation (mm) Maximal tendon strain (%) Stiffness of tendon structures (N · mm−1) Cross-sectional area of tendon (mm2)
Forefoot strike
Midfoot strike
Rearfoot strike
Mean (s)
Mean (s)
Mean (s)
18.1 6.8 30.6 74.8
(3.6) (1.3) (9.6) (10.6)
and rearfoot runners. To the best of our knowledge, this is the first study to investigate the relationship between Achilles tendon properties and foot strike patterns. Although over 85% of recreational runners (Kasmer, Liu, Roberts, & Valadao, 2013; Larson et al., 2011) make initial contact with the heel first, a higher percentage of both midfoot and forefoot strike runners was observed among elite long-distance runners (Hasegawa et al., 2007; Kasmer et al., 2013). In the present study, the distribution of foot strike patterns was different from that of recreational runners, because the participants in this study were highly trained long-distance runners. As one of the reasons for this phenomenon, it has been suggested that the forefoot strike pattern may be faster than the rearfoot strike pattern as a result of greater storage and release of elastic energy from the foot arch and Achilles tendon (Hasegawa et al., 2007; Hayes & Caplan, 2012; Larson et al., 2011). Based on the findings of cross-sectional and longitudinal studies (Arampatzis et al., 2006; Kubo et al., 2010), more economical runners were found to have more compliant tendon structures. Therefore, we hypothesised at the beginning of this study that the Achilles tendon of forefoot and midfoot strike runners may be more compliant than that of rearfoot strike runners. However, this hypothesis was rejected. Except for the Achilles tendon, the elastic property of the arch is another factor that may contribute to differences in running performance and economy between forefoot (and midfoot) and rearfoot strike runners. Ker, Bennet, Bibby, Kester, and Alexander (1987) stated that 17% or slightly more of the total energy turnover per step was stored as strain energy in the compliant elements of the arch of the foot. The forefoot strike may permit more elastic energy storage and recoil in the longitudinal arch, whereas rearfoot strike runners experience little or no arch compression at impact (Perl, Daoud, & Lieberman, 2012). However, to the best of our knowledge, there is no experimental evidence of this advantage for running performance and economy for forefoot strike runners. In future studies, we need to investigate the relationship between foot strike patterns and mechanical properties of the arch.
18.2 6.6 29.8 75.7
(2.7) (1.1) (6.7) (11.7)
17.7 6.4 32.5 76.2
(2.4) (0.9) (8.9) (12.6)
P values
Effect size
0.898 0.612 0.801 0.873
0.172 0.364 0.321 0.120
A previous study reported that elite long-distance runners generally run 90–150 km a week (Holmich, Darre, Jahnsen, & Hartvig-Jensen, 1988). Hence, it is likely that the Achilles tendon of highly trained long-distance runner is imposed the great mechanical stress during running training. Recent studies showed that ankle joint moment was greater in forefoot strike runners than in rearfoot strike runners during the first half of the stance phase (Almonroeder et al., 2013; Kulmala et al., 2013; Rooney & Derrick, 2013; Williams et al., 2000). Therefore, we may say that the Achilles tendon of forefoot strike runners was imposed a greater mechanical stress than that of rearfoot strike runners. In the last decade, several studies have used ultrasonography to investigate the effects of resistance training on the elastic properties of human tendons in vivo (Arampatzis et al., 2007; Kubo et al., 2006). Among these, mechanical stress was found to be important for changes in the elastic properties of human tendons, that is, stiffness. Accordingly, we hypothesised that the Achilles tendon of forefoot strike runners was larger and stiffer than that of rearfoot strike runners. In the present study, however, there were no differences in cross-sectional area or stiffness of the Achilles tendon among the three different strike pattern runners. De Zee, BojsenMoller, and Voigt (2000) showed using in vitro experiments that the tendon properties of pigs hardly changed during 1600 cycles of dynamic loading used as an input of a model to predict dynamic creep in the human Achilles tendon during running of a marathon. Furthermore, Peltonen, Cronin, Avela, and Finni (2010) reported that the mechanical properties of the human Achilles tendon did not change after two-legged hopping exercise consisting of 1150–2600 high impacts until exhaustion. The finding of a cross-sectional study (Kubo, Tabata, Ikebukuro, Igarashi, Yata, et al., 2010) indicated that the tendons of long-distance runners were less extensible than those of untrained subjects for knee extensors, but not for plantar flexors. Taking these previous findings into account together with the present results, the morphological and elastic properties of the Achilles tendon may not be affected by repetitive exercise such as endurance running.
Foot strike pattern and tendon property in runner In conclusion, the results of this study indicated that foot strike patterns were not related to the crosssectional area and stiffness of the Achilles tendon in highly trained long-distance runners. Further investigations are needed to clarify the relationship between foot strike patterns and other factors, that is, mechanical properties of the arch. Funding This study was supported by a Grant-in-Aid for Young Scientists (A) (21680047 to K. Kubo) from Japan Society for the Promotion of Science.
Downloaded by [University of Nebraska, Lincoln] at 12:18 06 April 2015
References Almonroeder, T., Willson, J. D., & Kernozek, T. W. (2013). The effect of foot strike pattern on Achilles tendon load during running. Annals Biomedical Engineering, 41, 1758–1766. Arampatzis, A., DeMonte, G., Karamanidis, K., Morey-Klapsing, G., Stafilidis, S., & Bruggemann, G. P. (2006). Influence of the muscle-tendon unit’s mechanical and morphological properties on running economy. Journal of Experimental Biology, 209, 3345–3357. Arampatzis, A., Karamanidis, K., & Albracht, K. (2007). Adaptational responses of the human Achilles tendon by modulation of the applied cyclic strain magnitude. Journal of Experimental Biology, 210, 2743–2753. De Zee, M., Bojsen-Moller, F., & Voigt, M. (2000). Dynamic viscoelastic behavior of lower extremity tendons during simulated running. Journal of Applied Physiology, 89, 1352–1359. Fukunaga, T., Roy, R. R., Shellock, F. G., Hodgson, J. A., & Edgerton, V. R. (1996). Specific tension of human plantar flexors and dorsiflexors. Journal of Applied Physiology, 80, 158– 165. Grieve, D. W., Pheasant, S., & Cavagna, P. R. (1978). Prediction of gastrocnemius length from knee and ankle joint posture. In E. Asmussen & K. Jorgensen (Eds.), Biomechanics VI: Proceeding of the sixth international congress of biomechanics, Copenhagen, Denmark (pp. 405–412). Baltimore, MD: University Park. Hasegawa, H., Yamauchi, T., & Kraemer, W. J. (2007). Foot strike patterns of runners at the 15-km point during an elitelevel half marathon. Journal of Strength and Conditioning Research, 21, 888–893. Hayes, P., & Caplan, N. (2012). Foot strike patterns and ground contact times during high-calibre middle-distance races. Journal of Sports Sciences, 30, 1275–1283. Holmich, P., Darre, E., Jahnsen, F., & Hartvig-Jensen, T. (1988). The elite marathon runner: Problems during and after competition. British Journal of Sports Medicine, 22, 19–21. Kasmer, M. E., Liu, X. C., Roberts, K. G., & Valadao, J. M. (2013). Foot-strike pattern and performance in a marathon.
669
International Journal of Sports Physiology and Performance, 8, 286–292. Ker, R. F., Bennet, M. B., Bibby, S. R., Kester, R. C., & Alexander, R. M. (1987). The spring in the arch of the human foot. Nature, 325, 147–149. Kubo, K., Ikebukuro, T., Yaeshima, K., Yata, H., Tsunoda, N., & Kanehisa, H. (2009). Effects of static and dynamic training on the stiffness and blood volume of tendon in vivo. Journal of Applied Physiology, 106, 412–417. Kubo, K., Komuro, T., Ishiguro, N., Tunoda, N., Sato, Y., Ishii, N., & Fukunaga, T. (2006). Effects of low load resistance training with vascular occlusion on the mechanical properties of muscle and tendon. Journal of Applied Biomechanics, 22, 112– 119. Kubo, K., Morimoto, M., Komuro, T., Yata, H., Tsunoda, N., Kanehisa, H., & Fukunaga, T. (2007). Effects of plyometric and weight training on muscle-tendon complex and jump performance. Medicine and Science in Sports and Exercise, 39, 1801– 1810. Kubo, K., Tabata, T., Ikebukuro, T., Igarashi, K., & Tsunoda, N. (2010). A longitudinal assessment of running economy and tendon properties in long distance runners. Journal of Strength and Conditioning Research, 24, 1724–1731. Kubo, K., Tabata, T., Ikebukuro, T., Igarashi, K., Yata, H., & Tsunoda, N. (2010). Effects of mechanical properties of muscle and tendon on performance in long distance runners. European Journal of Applied Physiology, 110, 507–514. Kulmala, J.-P., Avela, J., Pasanen, K., & Parkkari, J. (2013). Forefoot strikers exhibit lower running-induced knee loading than rearfoot strikers. Medicine and Science in Sports and Exercise, 45, 2306–2313. Larson, P., Higgins, E., Kaminski, J., Decker, T., Preble, J., Lyons, D., … Normile, A. (2011). Foot strike patterns of recreational and sub-elite runners in a long-distance road race. Journal of Sports Sciences, 29, 1665–1673. Lieberman, D. E., Venkadesan, M., Werbel, W. A., Daoud, A. I., D’Andrea, S., Davis, I. S., … Pitsiladis, Y. (2010). Foot strike patterns and collision forces in habitually barefoot versus shod runners. Nature, 463, 531–535. Magnusson, S. P., & Kjaer, M. (2003). Region-specific differences in Achilles tendon cross-sectional area in runners and non-runners. European Journal of Applied Physiology, 90, 549– 553. Peltonen, J., Cronin, N. J., Avela, J., & Finni, T. (2010). In vivo mechanical response of human Achilles tendon to a single bout of hopping exercise. Journal of Experimental Biology, 213, 1259– 1265. Perl, D. P., Daoud, A. I., & Lieberman, D. E. (2012). Effects of footwear and strike type on running economy. Medicine and Science in Sports and Exercise, 44, 1335–1343. Rooney, B. D., & Derrick, T. R. (2013). Joint contact loading in forefoot and rearfoot strike patterns during running. Journal of Biomechanics, 46, 2201–2206. Williams, D. S., McClay, I. S., & Manal, K. T. (2000). Lower extremity mechanics in runners with a converted forefoot strike pattern. Journal of Applied Biomechanics, 16, 210–218.
