Jumping and running have similar characteristics consisting of the flight and contact phases. During these both movements, the leg extensor muscles do lengthen and shorten in turns. These actions are well known as a typical stretch-shortening cycle (SSC) (1 ). The SSC has been recognized to enhance performance (2 ) and improve mechanical efficiency (3 ) as compared with isolated concentric action. McBride et al. (4 ) has suggested that repeated vertical jumping could also be used as an index of efficiency for distance runners. As a running is assumed to be a repetitive jumping in the forward direction, it is studied that running has similar tendon × muscular elasticity and movement efficiency characteristics as of repetitive jumping.
Efficiency during SSC exercises has been extensively studied (e.g., 2, 5). Kyröläinen and Komi (5 ) summarized these studies that mechanical efficiency during SSC exercises is improved correspond to increases in the prestretch intensity and decreases in coupling time between the eccentric (braking) and concentric (push-off) phases. However, mechanisms of SSC exercises to improve mechanical efficiency are not concluded yet, especially for whole body movement. Some studies have focused on the association between efficiency and muscle mechanisms. Abbott and Aubert (6 ) demonstrated that the isometric force followed by a stretch of an activated muscle was greater than the isometric force obtained from a purely isometric contraction at the same muscle length. This phenomenon is called “force enhancement” (7 ). Joumaa and Herzog (8 ) suggested that skeletal muscles become more efficient after the stretch, either by increasing the amount of force produced per cross-bridge or by engaging a passive element. However, these earlier studies concentrate only on narrow perspectives of human movement. To apply practical issues such as improving human performance, it is essential to relate motor control, that is, coordination of muscles and/or joints, and energy cost. Belli and Bosco (9 ) and Lamontagne and Kennedy (10 ) have suggested that angular displacement and velocity of the ankle joint plays an important role in movement efficiency. Similarly, Lamontagne and Kennedy (10 ) reported an importance of the knee joint since the knee joint generates large force while jumping as well as the ankle joint.
Biomechanical factors, affecting mechanical efficiency during a repetitive squat, countermovement, and drop jumps, have also been studied (11 ). It was suggested, however, that negative work and muscular activity during the eccentric phase could increase mechanical efficiency, but McCaulley et al. (11 ) failed to take into account the joints’ and/or muscles’ coordination. Thus, the authors have not calculated joint mechanical work but only external mechanical work (11 ). On the other hand, Farris and Sawicki (12 ) have stated that the distribution of mechanical work could explain the difference in efficiency. It can be speculated that the distribution of mechanical work at the lower limb joints could be explained as a difference in energy cost during whole body movement. Earlier studies (e.g., 12) have focused on only one joint work or external work where they might have overlooked this aspect. Utilizing changes in exercise conditions, lower limb joints kinetics and energy cost could also be changed. Therefore, the main purpose of the present study was to clarify the effects of the lower limb joint kinetics on energy cost during jumping. We hypothesized that changing surface inclination elicits SSC action of plantarflexors through enhancing prestretch. It might increase the contribution of the ankle joint, and improves the energy cost during repeated vertical jumping. Sawicki et al. (13 ) indicated that the lower limb joints have different mechanical efficiencies, especially the ankle joint has higher efficiency.
METHODS
Subjects
The subjects were eight male Japanese middle- and long-distance runners (age: 21.3 ± 0.8 yr; height: 1.73 ± 0.03 m; body mass: 62.6 ± 4.5 kg). They were recruited from a group of university track and field athletes and gave voluntary informed consent prior to participation. This experiment was approved by the ethical committee in the Faculty of Health and Sport Sciences, University of Tsukuba, Japan in accordance with the Declaration of Helsinki.
Procedures and measurements
The subjects were asked to perform repeated vertical jumps for 3 min on a force platform in the following three conditions: 1) Incline (+8°), 2) Level (0°), and 3) Decline (−8°). In the Incline and Decline experimental conditions with the fixed inclination of +8° and − 8°, the subjects were asked to jump vertically at the frequency of 2 Hz, guided by a metronome based on a previous study (14 ). In Level, the subjects repeated their jumps on a flat surface. Exercise duration of 3 min was selected for the purpose of reaching a steady-state level of oxygen consumption. The subjects were instructed to hold their arm on their hip. Prior to these measurements, the subjects maximal jump height of five vertical jumps was measured. Exercise intensities were 49.0% ± 6.4%, 49.5% ± 6.2%, and 47.1% ± 7.2% from the maximal jump height in Incline, Level, and Decline, respectively. All the subjects were familiarized with these exercises prior to assessment.
During the repeated vertical jumps, ground reaction forces (GRF) were measured using a force platform (9287B, Kistler, Switzerland). In Incline and Decline, the center of pressure (COP) will be on a slope plane, and thus its vertical coordinate may not be zero. Normally, only horizontal coordinate of COP has been calculated but in this case, vertical coordinate of COP must also be calculated. The first horizontal coordinate of COP (a y ) was calculated by solving a static equilibrium of moment about x coordinate for a y (Eq. 1, see Fig. 1 ).
FIGURE 1: Calculation method of the COP for Incline and Decline conditions.
where a y is the y coordinate of COP, r is the distance between the origin and each sensor, F z 1 , F z 2 , F z 3 , and F z 4 are the vertical forces measured by each sensor, F z is the sum of the vertical component (F z1 , F z2 , F z3 , and F z4 ) of the GRF.
Then the vertical coordinate of COP (a z ) was calculated to be solved an equation of a tangent for a z in incline plane (Eq. 2).
where a z is the z coordinate of the COP, α is the horizontal coordinate of the intersection point between the incline and basal planes of the force platform, and &thetas; is the angle between the incline and vertical planes.
Respiratory gases were continuously analyzed by “breath-by-breath” method with a computerized standard open circuit technique (15 ) (AE301s, Minato Medical Science, Japan). EMG was recorded with active surface electrodes (SX-230, Biometrics, UK) at a sampling frequency of 1 kHz from the rectus femoris (RF), vastus lateralis (VL), gluteus maximus, biceps femoris long head (BF), tibialis anterior, gastrocnemius medial head (GA), and soleus (SO) muscles. The interelectrode distance was 20 mm. The electrodes were placed longitudinally over the muscle belly between the center of the innervation zone and the distal tendon of each muscle in accordance with the SENIAM guidelines (16 ). Sagittal plane kinematic data were obtained using a high-speed camera (Ex-100Pro; Casio Computer, Japan). The frame rate and shutter speed of the camera were set at 120 ft·s−1 and 1/2000 s, respectively. Kinematic data were synchronized with the GRF and EMG data based on a LED signal.
Analysis
The respiratory gases were analyzed during the last minute of each 3-min jumping period. Energy expenditure was calculated according to the energy equivalent of 20,202 J·L−1 of oxygen refers to the respiratory exchange ratio (R ) of 0.82 and a change of ±0.01 resulted in a respective ±50 J change in energy expenditure (17 ). We did not measure blood lactate values, because blood lactate values were less than 2 mmol·L−1 in our pilot study. Energy cost, which is an index of economy, was calculated as energy expenditure divided by the jumping frequency and vertical distance. Energy cost was expressed in joules per kilogram per meter. Given that energy cost is defined as energy to cover a unit work or distance (18 ), energy cost was defined as the energy needed to raise the body a unit of distance.
Two-dimensional coordinates were obtained by digitizing reflective markers placed on nine anatomical landmarks (toe, head of the fifth metatarsal bone, heel, lateral malleolus, lateral epicondyle, greater trochanter, anterior superior iliac spine, posterior superior iliac spine, and acromion) using a video analysis software (Frame-Dias IV; DKH, Japan). The coordinate data were smoothed using a Butterworth digital filter at 4.8 to 10.8 Hz after residual analysis of each point (19 ). The body segments’ center of mass and moment of inertia were obtained according to the estimations of Ae et al. (20 ). The vertical distance of the center of mass was defined as a difference between the highest and lowest points of the greater trochanter. Joint torques at the hip, knee, and ankle were calculated using an inverse dynamics method (21 ). Mechanical work was calculated by integrating the joint torque power, which was an inner product of the joint torque and joint angular velocity. Muscle–tendon complex (MTC) length of the GA muscle was calculated based on the equation reported by Grieve et al. (22 ), whereas MTC length of the VL and SO muscle was calculated according to Hawkins and Hull (23 ).
EMG data were high-pass filtered with a Butterworth digital filter at 10 Hz to eliminate the low-frequency motion artifact. EMG was rectified and low-pass filtered by using Butterworth digital filter at 15 Hz to obtain an envelope. EMG envelope was normalized to a maximum value during maximal jumping. Integrated EMG (iEMG) was calculated by integrating the EMG envelope during the contact phase.
Kinematics, kinetics, and iEMG were averaged during the contact phase of 10 jumps from each condition. These jumps were selected starting from 2.5 min after the beginning of the 3-min jumping period. For comparing energy costs in different conditions, mechanical work and iEMG were normalized by a vertical distance. Additionally, iEMG was presented as the relative value in Level referring to 100%. Time histories of segment angle, joint angular velocity, joint torque, and EMG envelope in each condition during the contact phase were normalized based on the contact time in Level.
Statistics
Parameters were expressed as the mean ± standard deviation (SD). Nonparametric statistical techniques were utilized in the present study. Some variables exhibited a nonnormal distribution caused by small sample size. Thus, nonparametric statistics were deemed the most appropriate approach. Friedman one-way ANOVA tested effects of conditions, and the Wilcoxon matched-pairs signed-rank test emulated the t -test with repeated measures. Statistical significance was set at 5%.
RESULTS
The mean (±SD) oxygen consumptions (V˙O2 ) were 29.6 ± 2.6, 32.6 ± 2.2 mL·kg−1 ·min−1 , and 33.1 ± 1.7 mL·kg−1 ·min−1 in Incline, Level, and Decline, respectively. V˙O2 and energy cost were significantly smaller in Incline than Decline (P < 0.05, Table 1 ). Table 1 further demonstrates that averaged MTC length of the GA and SO muscles differed significantly between the conditions, being the longest in Incline and shortest in Decline. The maximal angular velocity of the ankle joint was significantly smaller in Decline than in Level (P < 0.01) and Incline (P < 0.05). The minimal angular velocity of the ankle joint was significantly smaller in Incline and Level than in Decline (P < 0.05).
TABLE 1: Mean (±SD) of selected parameters and results of ANOVA.
Figure 2 demonstrates the positive and negative mechanical work of the ankle, knee, and hip joints as well as the total mechanical work values of the lower limb joints. Total positive mechanical works of the lower limb joints in Incline, Level, and Decline were 3.86 ± 0.45 J·kg−1 ·m−1 , 3.91 ± 0.56 J·kg−1 ·m−1 , and 3.86 ± 0.39 J·kg−1 ·m−1 , respectively. Total negative mechanical works of the lower limb joints in Incline, Level, and Decline were −3.58 ± 0.44 J·kg−1 ·m−1 , −3.69 ± 0.48 J·kg−1 ·m−1 , and −3.44 ± 0.48 J·kg−1 ·m−1 , respectively. When comparing different experimental conditions, no significant differences in the total positive and negative mechanical work of the lower limb joints were obtained. Negative mechanical work of the ankle joint was the greatest in Incline, and it differed significantly between the conditions (Fig. 2 ). The positive and negative mechanical work of the knee joint was significantly smaller in Incline than in the Level and Decline conditions. Figure 3 demonstrates that energy cost was correlated with total mechanical work of the ankle (r = −0.648, P < 0.001) and knee joints (r = 0.577, P < 0.01).
FIGURE 2: Mean (±SD) mechanical work of the lower limb joints during the contact phase in each condition. Mechanical work was normalized to vertical distance.
FIGURE 3: Relationship between energy cost and mechanical work of the ankle and knee joints.
Figure 4 shows the MTC length of the VL, GA, and SO muscles during the contact phase. These muscles stretched during the first half of the contact phase and then shortened during the last half of the contact phase. The VL muscle was lengthening the longer time in Decline than in Incline and Level. The GA muscle showed a flatter pattern in Decline than in the Incline and Level conditions during the middle of the contact phase.
FIGURE 4: Average patterns of muscle–tendon complex length of the VL, GA and SO muscles during the contact phase. Time was normalized by the ground contact time of Level condition. Broken, solid, and dotted lines show Incline, Level, and Decline conditions, respectively.
The iEMG of the RF muscle was significantly smaller in Incline than in Level (P < 0.05) and Decline (P < 0.05). No significant differences in the other muscles were observed between the conditions. Figure 5 demonstrates the EMG envelopes of the VL, GA, and SO muscles. The GA muscle showed different activity pattern in Decline as compared to the Incline and Level conditions.
FIGURE 5: Average patterns of EMG envelopes of VL, GA, and SO muscles during contact phase. Broken, solid, and dotted lines show Incline, Level, and Decline conditions, respectively.
DISCUSSION
The major findings of the present study were as follows: 1) the energy cost was significantly smaller in Incline than in Decline, 2) energy cost correlated positively with the total mechanical work of the knee joint in all conditions while it correlated negatively with the total mechanical work of the ankle joint, 3) iEMG of the RF muscle was smaller in Incline than in the Level and Decline conditions. These findings are well in line with our hypotheses.
Earlier studies (1,11,24,25 ) have regulated jumping height and compared V˙O2 , although this approach may lead to unnatural movement. The present study regulated jumping frequency instead of jump height while maintaining natural movement of jumping in different conditions. In addition, energy cost was calculated to compare economy between different conditions because jumping height may differ between the conditions. Energy cost is defined as energy expenditure per unit vertical distance, and thus this variable could be used to compare between different jumping heights. In fact, even if V˙O2 was used to compare conditions, it would have no influence on the conclusion.
The lowest energy cost, among three conditions, was shown in Incline. No significant differences between these conditions were found in the total mechanical work of the lower limb joints. Holt et al. (26 ) has suggested that the reduction in mechanical work may not necessarily decrease energy cost in isolated muscles. However, mechanical works of the knee and ankle joints were correlated with the simultaneous energy costs, although with an opposite trend. Although the role of the ankle joint is emphasized during repetitive jumping, the mechanical work of the knee joint may be related to an increase in energy cost. Mechanical work of the ankle joint was greater in Incline as compared to Level and Decline. In Decline condition, the ankle joint did insufficient mechanical work to raise the body due to a limitation of the movement of the ankle joint. The knee joint did the smallest mechanical work in Incline. On the other hand, in the Decline condition, where the ankle joint did the least mechanical work in all conditions, the knee joint did the greatest amount of mechanical work. These trade-offs of mechanical work between the ankle and knee joints might be one of the key factors for the difference in energy cost. These facts suggest that the knee joint might compensate for a lack of mechanical work of the ankle joint and increase energy cost.
Sawicki et al. (13 ) indicated that the lower limb joints have different mechanical efficiencies, because of the architectural differences in the muscle–tendon structure described as the proximodistal gradient (27 ). They reported that the mechanical efficiency of the ankle joint was better than the knee joint (13 ). Therefore, if the ankle joint has done sufficient mechanical work, the knee joint would do less mechanical work and energy cost would be small.
In the present study, the findings of the plantarflexors were in line with previous findings (5,24 ). As mentioned earlier, greater efficiency of SSC action was often explained by the storage and release of elastic energy (9,24,28 ). However, van Ingen Schenau et al. (29 ) stated that clarifying energy saving mechanisms through elastic energy utilization is difficult. In the present study, it was impossible to find evidence for elastic energy re-utilization. On the other hand, it is reported that muscles will produce greater force (30 ) and require less energy expenditure (31 ) when the muscle is lengthened while active. Holt et al. (26 ) reported that the energy cost of SSC action in isolated muscle without tendon was smaller than that of shortening and almost the same as isometric. Herzog (7 ) also reported that force enhancement occurs in immediate contraction following the stretch of an activated muscle. Joumaa and Herzog (8 ) suggested that skeletal muscles become more efficient after the stretch by force enhancement. The present study obtained the joint angular velocity which is closely related to muscle stretching or shortening velocities. However, muscular and/or fascicle length during dynamic actions of different angular velocities cannot be assumed solely from the joint angle (32 ). Moreover, function of the biarticular muscles also contributes to reducing energy cost (33 ). Therefore, SSC action and biarticular function of muscles might reduce energy cost, although its mechanisms have not yet been fully elucidated.
However, the mechanical work of the ankle and knee joints correlated with energy cost, and these correlations have an opposite tendency. The present study revealed that energy cost of whole body movement could be changed by coordination between muscles through changes in the length of the plantarflexors by manipulating jumping surface inclinations. Manipulating exercise conditions could naturally lead to altering human movement. McCaulley et al. (11 ) have reported that mechanical efficiency and energy cost differed between squat jump, countermovement jump and drop jump, and they did not refer to mechanisms of changing mechanical efficiency and energy cost from the perspective of muscle coordination (11 ). On the other hand, the present study focused on muscles’ coordination using a kinetic approach to explain changes in energy cost. Focusing on muscles’ coordination provides new insights to determine factors affecting energy cost during endurance exercises.
The present study utilized a changing exercise condition, for example, changing jumping surface inclinations. This approach could alter movement and energy cost naturally and could lead to some clarification of the biomechanical factors affecting energy cost during endurance exercises such as running. During running, work done to support the body weight was reported to be the primary determinant of energy cost (34 ). However, the biomechanical factors affecting energy cost during the support phase are still not completely understood. Given that, repeated vertical jumping is similar to the vertical movement during running, the findings of the present study may serve to elucidate how biomechanical factors affect energy cost in natural human locomotion. However, there is a potential difference between running and vertical jumping from the viewpoint of surface inclination . Inclined surface during jumping altered posture of the lower limbs without changing vertical mechanical work, but inclined surface during running may change vertical mechanical work as well as the posture of the lower limbs even at the same running speed. Considering these different effects of surface inclination , future work would provide new insights on biomechanical factor to improve running economy by a similar approach.
CONCLUSIONS
The present study revealed that muscles’ coordination correlates with energy cost during repeated vertical jumping. If the plantarflexors could not do sufficient mechanical work, the knee extensor would contribute to greater mechanical work to raise the body. In conclusion, the lower limb joints have different efficiencies to generate the same total mechanical work in repeated vertical jumping on different surface inclination . When mechanical work is mainly done by the ankle joint, energy cost would be smaller. On the other hand, when less mechanical work is done by the ankle joint, the knee and/or hip joint compensate for lack of mechanical work of the ankle joint and the energy cost increases.
This study was unfunded, and the authors declare no conflicts of interest. The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation, and a statement that results of the present study do not constitute endorsement by American College of Sports Medicine.
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