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Journal of Science and Medicine in Sport 13 (2010) 106111

Original paper

Differences in lower extremity stiffness between endurance-trained athletes and untrained subjects
Hiroaki Hobara a,b, , Kozo Kimura c , Kohei Omuro d , Kouki Gomi d , Tetsuro Muraoka e , Masanori Sakamoto c , Kazuyuki Kanosue a,c,d,e
b a Graduate School of Human Sciences, Waseda University, Japan Motor Control Section, Department of Rehabilitation for the Movement Functions, Research Institute, National Rehabilitation Center for Persons with Disabilities, Japan c Faculty of Sport Sciences, Waseda University, Japan d Graduate School of Sport Sciences, Waseda University, Japan e Consolidated Research Institute for Advanced Science and Medical Care, Waseda University, Japan

Received 24 April 2008; received in revised form 14 August 2008; accepted 22 August 2008

Abstract An understanding of lower extremity stiffness is important for evaluation of sports performance and injury prevention. The aim of this study was to investigate whether stiffness regulation during hopping differed between endurance-trained athletes and untrained subjects. Eight endurance-trained athletes and eight untrained subjects performed two-legged hopping at 2.2 Hz. We determined leg and joint stiffness of hip, knee and ankle from kinetic and kinematics data. The endurance-trained athletes demonstrated signicantly higher leg stiffness than untrained subjects. Further, the differences in leg stiffness were attributable to differences in ankle and knee joint stiffness. This study demonstrates a possibility that endurance training, like power training, increases leg and joint stiffness. 2008 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
Keywords: Biomechanics; Training adaptation; Stiffness; Athlete

1. Introduction Because legs exhibit spring like characteristics during jumping, a spring-mass model is frequently used to represent the musculoskeletal system.1 This model consists of a body mass and a linear leg spring supporting the body mass. Leg stiffness, dened as the ratio of maximal ground reaction force to maximum leg compression at the middle of the stance phase, has been shown to augment with an increase in hopping height.24 The degree of stiffness is a factor in injuries; high stiffness can cause bony injuries, while low stiffness is associated with soft tissue injuries.5,6 An increased understanding of how training regimes affect leg stiffness would be expected to aid in the development of more effective train Corresponding author at: Motor Control Section, Department of Rehabilitation for the Movement Functions, Research Institute, National Rehabilitation Center for Persons with Disabilities, Japan. E-mail address: hobara@rehab.go.jp (H. Hobara).

ing methods and the subsequent reduction of injuries during sports activities. Previous studies suggested that power training improves leg stiffness through the adaptation of musculotendinous stiffness.79 Indeed, cross-sectional studies have reported that power-trained athletes show higher leg stiffness than endurance-trained athletes or untrained subjects.10,11 However, little is known about the effect of endurance training on leg stiffness. The purpose of this study was to investigate whether endurance training alters leg stiffness. We compared stiffness regulation of endurance-trained athletes and untrained subjects in a cross-sectional manner utilising two-legged hopping that facilitates quantication of the components of the spring-mass model. Overall leg stiffness depends on the joint stiffness, which is dened as the ratio of the maximal joint moment to the maximum joint exion at the middle of the stance phase.6 Previous studies demonstrated that joint stiffness regulation is modulated by joint angles at touchdown because it changes

1440-2440/$ see front matter 2008 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jsams.2008.08.002

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the distance of the moment arm of the ground reaction force at each joint.12,13 Further, intrinsic stiffness of the muscle and tendon also inuences to joint stiffness.6 A recent study suggested that the difference in joint stiffness between endurance- and power-trained athletes was best attributed to the difference in the intrinsic stiffness of the tendinous tissues rather than to touchdown joint angle.11 Since stiffness of the triceps surae tendon and aponeurosis did not differ between endurance runners and subjects not active in sports14 we hypothesised that leg and joint stiffness during hopping would not differ between two groups.

marker was digitised by movement-analysis software (FrameDias II, DKH Inc., Japan). Kinematic data were low-pass ltered by a fourth-order zero-lag Butterworth lter with a cut-off frequency of 8 Hz, from which joint angular displacements were determined. Because the peaks of ground reaction force and leg compression coincide in the middle of the ground contact phase, the vertical component of stiffness (Kleg ) can be calculated from force plate data as Kleg (N/m) = Fpeak L (1)

2. Methods Eight endurance-trained athletes (19.9 1.1 years, body mass 58.9 4.4 kg, height 1.72 0.04 m) and eight untrained subjects (24.3 1.9 years, body mass 62.9 2.9 kg, height 1.70 0.05 m, respectively) participated in this study. All of the endurance-trained athletes belonged to Waseda University Track and Field team as long distance runners who specialised in the 5000 or 10,000 m races. They had performed regular endurance running training between 4 and 6 days per week, for more than 9 years. All of these the subjects had competed at the regional or inter-collegiate level within the preceding year, and their best recorded times in the 5000 m race ranged from 14.0 to 15.5 min. Throughout the year, the endurance-trained athletes ran approximately 160 km a week. Around 90% of the entire endurance training was long slow distance running and about 10% was speed type training. The untrained subjects had not experienced regular exercise training. Informed consent approved by the Human Ethics Committee, Faculty of Sport Sciences, Waseda University, was obtained from all subjects before the experiment. We asked the subjects to hop in place with their hands on their hips. Hopping was performed on a force plate (60 cm 120 cm, Power Max-1500, Bertec Inc., Japan); the vertical ground contact force was recorded at 1 kHz. We set hopping frequency at 2.2 Hz with a digital metronome beat. Since different contact time instructions can affect stiffness regulation during hopping at a given hopping frequency,4 the subjects were asked to hop with as short a contact time as possible. Before data collection, subjects were instructed to practice for as long as was needed until they felt comfortable with the task. Five consecutive hops, from the sixth to the tenth of the 15 hops, were used for the analysis. From the measurement of ground reaction force, actual hopping frequency, ground contact time and aerial time were determined. Each subject was videotaped in the sagittal plane at 250 elds per second using a high-speed video camera (HSV500C3, NAC Inc., Japan). We placed six retroreective markers on the subjects in the following locations: the tip of the rst toe, the fth metatarsophalangeal joint, the lateral malleolus, the lateral epicondyle of the femur, the greater trochanter, and the acromion scapulae. The position of each

where Fpeak is the peak vertical ground reaction force, and L is the maximum vertical displacement of the center of mass (COM) during ground contact, which is obtained by integrating the vertical acceleration twice with respect to time.3 Joint stiffness can be calculated with the torsional spring model. In this model, it was assumed that four rigid segments (foot, shank, thigh and headarmtrunk) are interconnected with torsional joint springs of the hip, knee and ankle. Joints of the lower extremity ex in the period from the instance of touch down to the middle of the ground contact phase. Therefore, joint stiffness of the hip, knee and ankle (Khip , Kknee and Kankle , respectively) is calculated as Kjoint (Nm/rad) = Mjoint joint (2)

where Mjoint and joint are the changes in joint moment and the angular displacement at each joint during the rst half of the stance phase, respectively.3 We determined the net joint moment by inverse dynamics analysis using anthropomorphic data.15 Since a subjects body size inuences the stiffness value,16 both leg and joint stiffnesses were divided by the subjects body mass. It was recently demonstrated17 that the stiffness assessment utilising hopping was as valid and reliable as the oscillation technique commonly used in previous studies.1820 The comparison between the endurance-trained athletes and untrained subjects was made using the Student t-test. Statistical signicance was set at P < 0.05. All data are presented as mean values with standard errors of the mean (S.D.).

3. Results Hopping frequency, contact time and aerial time for both groups are shown in Table 1. There was no signicant difference in actual hopping frequency between the two groups. However, ground contact time was signicantly shorter in the endurance-trained athletes than in the untrained subjects, and ight time was signicantly longer in the endurance-trained athletes than in the untrained subjects. Fig. 1A shows a typical example of the relationship between force and COM displacement in single cycles of hopping, recorded from one endurance-trained subject.

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Table 1 Comparison of temporal, kinetic and kinematic characteristics between endurance-trained athletes and untrained subjects Endurance Hopping frequency (Hz) Contact time (ms) Aerial time (ms) Peak reaction force (N/BW) COM displacement (cm) Peak ankle moment (Nm/BW) Peak knee moment (Nm/BW) Peak hip moment (Nm/BW) Ankle angular displacement (rad) Knee angular displacement (rad) Hip angular displacement (rad) Ankle touchdown angle (rad) Knee touchdown angle (rad) Hip touchdown angle (rad) 2.21 (0.05) 183 (19) 270 (26) 51.3 (6.8) 8.4 (0.9) 4.35 (0.45) 4.62 (0.60) 0.91 (0.39) 0.43 (0.08) 0.18 (0.06) 0.07 (0.03) 2.09 (0.15) 2.60 (0.09) 2.92 (0.10) Untrained 2.14 (0.06) 243 (43) 225 (39)* 39.2 (7.3) 11.2 (1.2) 3.16 (0.67) 4.71 (0.98) 1.18 (1.06) 0.56 (0.09) 0.32 (0.09) 0.15 (0.07)* 2.18 (0.11) 2.68 (0.10) 2.96 (0.09)

A dagger () and an asterisk (*) indicate signicant differences between the two groups; P < 0.01 and 0.05, respectively.

The leg was compressed from the moment of landing, and ground reaction force increased with COM displacement. Ground reaction force peaked at the moment of maximum leg compression, and subsequently, the force decreased with extension of the leg until take-off. Leg stiffness is represented by the slope of the forcedisplacement curve in the leg compression phase. As shown in Fig. 1E, leg stiffness was signicantly greater in the endurance-trained athletes than in the untrained subjects. Fig. 1BD depict typical examples of the relationship between joint moment and angular displacement in ankle, knee and hip, respectively. These data were obtained from the same subject and the same hopping cycle as in Fig. 1A. From the moment of touch down, the joints were exed, and joint moments increased. The joint moment peaked at the maximum joint exion, after which the joint began to extend with a decrease in joint moment until take-off. Fig. 1F depicts joint stiffness, the slope of these momentangular displacement curves. Both ankle and knee stiffnesses were signicantly greater in the endurance-trained athletes than in the untrained subjects. Hip stiffness did not differ between the two groups. Table 1 shows the joint angle of hip, knee and ankle at touchdown for both groups. There was no signicant difference in touchdown angle between the endurance-trained athletes and untrained subjects.

4. Discussion The purpose of this study was to investigate whether endurance training alters leg stiffness in a cross-sectional manner. We compared leg and joint stiffness between the endurance-trained athletes and untrained subjects. The endurance-trained athletes demonstrated higher leg stiffness than the untrained subjects (Fig. 1E). This result contrasts with our hypothesis that leg stiffness during hopping would not differ between the two groups. Past ndings have shown

that power-trained athletes demonstrate higher leg stiffness than endurance-trained athletes or untrained subjects,10,11 indicating that power training, including weight training and/or plyometrics, improves the leg stiffness. Thus, the present study suggests that not only the power training but also endurance training increases leg stiffness. In our study, observed differences in leg stiffness between the endurance-trained athletes and untrained subjects were accompanied by a difference in ankle and in knee stiffness (Fig. 1F). Joint stiffness is composed of many mechanical elements, which include muscles and tendons, as well as other connective tissues.6,12 A recent nding11 reported that the difference in joint stiffness between groups with a different training background may be attributed to a difference in the intrinsic stiffness of the tendinous tissues. However, past ndings suggested that endurance running had no effect on the mechanical properties of triceps surae tendon and aponeurosis.14,21,22 Since touchdown joint angles in the present study also did not differ between the two groups (Table 1), the difference in joint stiffness between the two groups probably depends upon something other than tendinous tissues. A logical choice would be the intrinsic properties of the muscles. It has been demonstrated that endurance training results in an increase in muscle stiffness associated with a decrease in type II bers of rat soleus muscles.23 Further, although we did not measure muscle ber composition in the present study, it is reasonable to assume that the endurancetrained athletes possess more slow-twitch muscle bers than the untrained subjects.24 It is known that slow-twitch muscle bers possess a greater dynamic stiffness than do fast-twitch muscle bers.25 Moreover, the pennation angles of the medial gastrocnemius muscle and vastus lateralis muscle are greater in the endurance-runners group as compared with the nonactive individuals.26,27 Considering that joint stiffness is partly inuenced by joint moment, differences in the pennation angle of muscles also seem to produce differences in joint stiffness. Indeed, in the present study, the endurancetrained athletes demonstrated a higher ankle moment than the untrained subjects (Table 1). Hence, it could be speculated that the difference in joint stiffness between the two groups was due to the intrinsic stiffness of the muscle bers, rather than to tendon stiffness. Suppose that endurance-trained athletes possess more slow-twitch muscle bers than the untrained subjects, our results that the endurance-trained athletes hopped higher than the control subjects may seem paradoxical. However, force generating capacity depends on not only muscle ber composition but also muscle volume, pennation angles and muscle activation level. Thus, it is not always the case that the amount of type II ber is directly linked to force generating capacities. Indeed, Skurvydas et al.28 demonstrated that the height of jumps performed by long distance runners in drop jumps (from the height of 0.4 m) were higher than those of untrained subjects. Therefore, even if endurance-trained athletes had less type II ber than untrained subjects, endurance-trained

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Fig. 1. Typical examples of forceCOM displacement (A) and momentangular displacement curves of the ankle (B), knee (C), and hip (D) and comparison of leg stiffness (E) and joint stiffness (F) between the two groups. A dagger () indicates signicant differences between the groups; P < 0.01.

athletes could still be more explosive than the control subjects. Our interpretations about intrinsic adaptation to training and the effect on leg stiffness were in accordance with some recent ndings29 but not others.17,30 The cause of this discrepancy could involve methodological differences. Because there was no signicant relationship between ankle joint stiffness and tendon stiffness during the drop jump, Kubo et al.29 suggested that ankle stiffness was related to the properties of muscle but not to the properties of the tendon. On the other hand, both McLachlan et al.17 and Rabita et al.30 demonstrated the absence of a signicant relationship between leg stiffness and musculotendinous stiffness. Kubo et al.29 calculated ankle stiffness as the change in joint torque divided by the change in joint angle during the eccentric phase of the drop jump, in which the subjects were instructed to jump

to a maximal height. However, both McLachlan et al.17 and Rabita et al.30 used a quick release test and/or a sinusoidal perturbation test for the musculotendinous stiffness calculation. In this case the subject was instructed to maintain a constant (submaximal) level of isometric plantar exion. The present study is similar to Kubos in that we instructed the subjects to perform jumping with maximal effort and used the same stiffness calculation. Thus, it seems likely that the above methodological differences led to the discrepancies in the results. An increased understanding of how training regimes affect leg stiffness will provide us with a basis for better evaluating injury prevention during sports activities. In the current study, we observed differences in lower extremity stiffness between endurance-trained athletes and untrained subjects. Previous studies suggested that high stiffness can cause bony injuries,

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while low stiffness is associated with soft tissue injuries.5,6 Further, recent ndings indicate that runners with a history of tibial stress fractures, a serious overuse injury, have higher stiffness than control subjects during running.31,32 Thus, the results of the present study indicate that longterm endurance training enhances leg spring stiffness through changes of intrinsic muscle properties which, unfortunately, may increase the risk of bony injuries. There are several concerns on the interpretation of the ndings. First, the hopping frequency was set identical but there is a signicant difference in contact time between endurance athletes and untrained subjects. If the contact time could inuence the stiffness by itself, the potential effect of the difference in contact time should be considered as a confounding factor in interpreting the difference in stiffness between groups. Indeed, a recent study has shown that compared to the frequency, the effects of contact time variations appears to be a stronger and more direct determinant of Kleg .33 It concerns running activity, but there is no reason to think that the ndings cannot be transferred to hopping tasks. Secondly, we could only report limited specics of the training of the endurance-trained subjects. Because the endurance athletes in the present study performed both long slow distance and speed type training, we could not determine which training inuenced the leg spring stiffness. Thirdly, our results were based on cross-sectional, not longitudinal, observations. Therefore, the current data cannot determine whether the higher leg and joint stiffness in the endurance-trained athletes was due to training or had a genetic origin. Further research is needed on how, and whether, leg stiffness can be altered by endurance training. 5. Conclusions The results of the present study suggest that, as evaluated in a two-legged hopping task, endurance-trained athletes have stiffer leg springs than do untrained subjects. Differences in leg stiffness between the two groups are due to an increased joint stiffness, which is most likely attributed to intrinsic muscle properties. Practical implications Evaluation of lower extremity stiffness while performing sport is an important for assessing musculoskeletal performance and injury. Not only power training but also endurance training may increase the lower extremity stiffness through changing muscle properties. Detraining may decrease the lower extremity stiffness. Conict of interest None.

Acknowledgements This study received grant support from the Institute of Top Performance, Waseda University (#10). The authors thank the members of the Sport Neuroscience Laboratory, Faculty of Sport Sciences, Waseda University for data collections. Finally, we thank Dr. Larry Crawshaw for his careful reviews of earlier drafts. References
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