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Biomechanics of the heel-raise test performed on an incline in two knee flexion positions
Clinical Biomechanics 28 (2013) 664–671
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Biomechanics of the heel-raise test performed on an incline in two knee flexion positions Kim Hébert-Losier ⁎, Hans-Christer Holmberg Swedish Winter Sports Research Centre, Department of Health Sciences, Mid Sweden University, Kunskapens väg 8, Hus D, 83125 Östersund, Sweden
a r t i c l e
i n f o
Article history: Received 21 April 2013 Accepted 6 June 2013 Keywords: Plantar-flexion Triceps surae muscles Endurance Clinical test Fatigue
a b s t r a c t Background: Although single-legged heel-raise cycles are often performed on an incline in different knee flexion positions to discriminate the relative contribution of the triceps surae muscles, detailed kinematic and kinetic analyses of this procedure are not available. Our study characterizes and compares the biomechanics and clinical outcomes of single-legged heel-raise cycles performed to volitional exhaustion on an incline with the knee straight (0°) and bent (45°), considering the effect of sex and age. Methods: Fifty-six male and female volunteers, with equal numbers of younger (20 to 40 years of age) and older (40 to 60 years of age) individuals, completed a maximal number of heel-raise cycles on an incline at both nominal knee angles. Kinematic and kinetic data were acquired during testing using a 3D motion capturing system and multi-axial force plate. The impact of fatigue on performance was quantified using changes in maximal voluntary isometric contraction force and biomechanical performance of cycles. Findings: Overall, participants completed three more cycles and maintained better biomechanical performance with 45° than 0° of knee flexion. More precisely, the decreases in maximal heel-raise heights, plantar-flexion angles at maximal height and ranges of ankle motion per cycle were all smaller with the knee bent. However, several outcomes indicated similar plantar-flexion fatigue at both knee angles. Males demonstrated a more rapid decline in peak ground reaction forces during testing; but otherwise, neither sex nor age significantly impacted outcomes. Interpretation: It is concluded that the differences discerned here in the biomechanics of single-legged heel-raise cycles performed at 0° and 45° of knee flexion to volitional exhaustion on an incline may be too small to identify in clinical settings or reflect substantial alterations in the relative contribution of the triceps surae muscles. © 2013 Elsevier Ltd. All rights reserved.
1. Introduction During the 1940s poliomyelitis epidemic, rehabilitation professionals observed that the traditional manual muscle test was limited in assessing the anti-gravitational function of the triceps surae (Florence et al., 1992). Many individuals were not able to stand or walk due to an underlying plantar-flexion weakness, yet the plantar-flexors were given the highest test score and classified as functionally normal (Lunsford and Perry, 1995). To provide a more accurate and valid representation of plantarflexion function, manual resistance was replaced with the performance of heel-raise cycles in weight-bearing on one leg. Nowadays, to specifically examine the endurance characteristics of the triceps surae, heel-raise cycles are performed to volitional exhaustion, a procedure referred to herein as the heel-raise test (HRT). To characterize the relative contribution of the gastrocnemius and/or soleus muscles to plantar-flexion, heel-raises are performed in differing degrees of knee flexion (KF) (Alfredson et al., 1998; Stasinopoulos and Manias, 2013), with the HRT in 0° suggested for ⁎ Corresponding author. E-mail address: [email protected] (K. Hébert-Losier). 0268-0033/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.clinbiomech.2013.06.004
gastrocnemius and 45° for soleus. However, with a straight and bent knee, the total number of cycles completed (Hébert-Losier et al., 2011) and surface electromyography indicators of fatigue for soleus and gastrocnemius (Hébert-Losier et al., 2012) are comparable. Consequently, the muscle-selective value of performing the HRT for endurance in several KF angles is questionable. The two investigations referred to above were carried out with the foot initially on the ground and their outcomes may not apply to permutations of the heel-raise task when the foot is positioned on an incline (Silbernagel et al., 2010) or step edge (Alfredson et al., 1998; Reid et al., 2012). Currently, no detailed kinematic or kinetic analyses of the HRT performed on an incline at two distinct KF angles have been reported. Such studies would provide important information concerning the usefulness of evaluating heel-raise performance at differing KF angles, thereby assisting clinicians and researchers in interpreting and/or monitoring individuals' outcomes. Furthermore, age and sex are important factors in both practical and experimental settings. Most studies report lower plantar-flexion strength and endurance in females than males and in older than younger individuals (Danneskiold-Samsøe et al., 2009; Fugl-Meyer et al., 1980); however, the impact of age and sex is task-dependent (Hunter, 2009). Accordingly,
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there is debate regarding the impact of age and sex on HRT outcomes (Hébert-Losier et al., 2012; Lunsford and Perry, 1995). Our study was designed to characterize and compare the biomechanics and clinical outcomes of the single-legged HRT performed on an incline with the knee straight (0°) and bent (45°), while considering age and sex as confounders. Our primary hypothesis was that KF angle would influence these outcomes, with a greater number of heel-raise cycles being performed with the knee bent, thereby supporting the continued use of several KF angles. Our secondary hypothesis was that younger individuals and males would exhibit greater resistance to fatigue than older individuals and females. 2. Methods 2.1. Participants The participants for this study were recruited from the local community with recruitment advertised using selected e-mail distribution lists, local newspapers, bulletin-boards, online forums and word-of-mouth. After providing written informed consent, 56 volunteers took part in this study (28 males [mean (SD); age: 38 (12) years; height: 181 (7) cm; mass: 82 (9) kg] and 28 females [age: 41 (11) years; height: 169 (8) cm; mass: 69 (9) kg]), with equal numbers of both sexes aged between 20 to 40 and 40 to 60 years. Inclusion criteria were good self-reported health with regular physical activity and no current or recent musculoskeletal injury or medical contraindications. The research protocol was pre-approved by the Regional Ethical Review Board and adhered to the Declaration of Helsinki. 2.2. Study design The repeated-measures design (Fig. 1) of this study required each participant to take part in a single experimental session that included familiarization. To eliminate the potential influence of testing order and fatigue, each individual was tested on the dominant leg at 0° and 45° of KF in a block-randomized order according to age and sex, with half of the males and half of the females in each age group beginning at 0° and the others at 45° of KF. The same investigator carried out all kinematic and kinetic assessments. 2.3. Procedures 2.3.1. Baseline measures Age, height and mass were recorded on the day of testing. Leg dominance (51 right: 5 left) was determined using the Dunedin Footedness Inventory (Schneiders et al., 2010). Standing on the dominant leg, the end-range of ankle dorsi-flexion motion was assessed on an incline at both 0° and 45° of KF. The incline was adjusted to match the end-range of ankle dorsi-flexion (Fig. 2) and ankle angles measured using a goniometer (Model 01135, Lafayette Instrument Company®, Loughborough, UK). The angles were 72 (6)° and 64 (7)° at 0° and 45° of KF, where 90° represents the neutral position (i.e., the 5th metatarsal bone perpendicular to the fibula) and more acute angles reflect greater dorsi-flexion. 2.3.2. Maximal voluntary isometric contractions Plantar-flexion maximal voluntary isometric contractions (MVICs) were performed standing on the dominant leg before (MVICpre) and after (MVICpost) each HRT, at both 0° and 45° of KF. Using previously described methods (Hébert-Losier and Holmberg, 2013), participants stood underneath a weightlifting stand (Eleiko Sport AB, Halmstad, SE) on a DBA force plate (New Development Technologies AB, Farsta, SE) that recorded vertical ground reaction forces during MVICs at a rate of 200-Hz using the DBA® Software v.3.2 (see Fig. 1 in the supplementary material). To promote appropriate and maximal effort, standardized
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supervised training was provided before and emphatic verbal encouragement was given during MVIC trials. 2.3.3. Heel-raise tests Each participant performed a maximal number of single-legged heel-raise cycles on an incline at 0° and 45° of KF (Fig. 3), separated by 1-hr of rest, following previously described HRT protocols (HébertLosier et al., 2011; Hébert-Losier et al., 2012). To avoid strain from repetitive contractions in an elongated position (Garrett, 1990), the incline was adjusted to ~5° less than the previously established end-range of ankle dorsi-flexion motion. To ensure that there was no residual fatigue, the peak force at a given KF angle during the single MVICpre completed immediately preceding the HRT was compared to that of the three others that were performed earlier (see Fig. 1). The rest period was prolonged if the difference was greater than 5%. No participant expressed residual fatigue or soreness from the procedures preceding heel-raise testing. To assist balance, individuals were permitted to apply up to 2% of their bodyweight on a horizontal bar suspended in front of them at shoulder height. This bar was connected to a 0 to 50 kg force sensor and MuscleLab 4010 Unit with relevant software (Ergotest Innovation AS, Porsgrunn, NO), enabling the monitoring of force in real-time. Prior to testing, each participant went through an individualized familiarization session during which the investigator provided corrective feedback designed to ensure that the task was performed in an appropriate manner. Since the heel can be lifted without vertical displacement of the center of mass through hip flexion, each participant was instructed to lift their entire body upwards using their ‘calf’ muscles to reach a maximal (heel-raise) height, while maintaining the knee at the designated angle. The HRT cycle cadence was controlled at 60 per minute by a metronome (TempoPerfect© v.2.02, NCH Software, Canberra, AUS). Verbal feedback designed to maintain the HRT parameters regulating the cadence, balance support, heel excursion, and especially the KF angle was provided at regular intervals during testing. The test was terminated when participants could no longer lift the stance heel from the incline and/or repeat another cycle. Since the purpose was to investigate the biomechanics of performance of the HRT to volitional exhaustion, the test was not terminated if the specified threshold height of heel-raise was not reached, the set pace or KF angle was momentarily lost, or the balance support was inadvertently used to assist performance. Participants were asked to rate their perceived (calf muscle) exertion on the 6–20 point Borg (1982) scale at exhaustion. 2.4. Equipment 2.4.1. Motion capture Whole-body motion was monitored during the HRT at a rate of 300 Hz using a 3D motion analysis system consisting of 8 Oqus 300 infrared cameras and QTM software v.2.7 (Qualisys AB, Gothenburg, SE). A total of 49 retro-reflective markers (9 mm) were taped to the skin over anatomical landmarks using a variation of the Conventional (Full-Body) Gait Model (Bell et al., 1989), selected Oxford-foot markers (Stebbins et al., 2006) and additional lower-extremity tracking markers (Fig. 3). Ground reaction forces were collected during the HRT by having participants stand on the incline in the middle of a calibrated multi-axial force plate (Kistler 9281EA, Kistler Instrumente AG, Winterthur, CH). The QTM software was configured for synchronous collection of kinematic (i.e., Oqus cameras) and kinetic (i.e., Kistler force plate) data. From the reference set of markers, a full-body rigid-link biomechanical model with 6-degrees-of-freedom and 15 segments for the feet, shanks, thighs, pelvis, trunk, head, upper arms, forearms, and hands was constructed in Visual3D Professional™ Software v.4.96.7 (C-Motion Inc., Germantown, MD, USA). For kinematic analysis, the distal end of one segment was linked to the proximal end of another, with all lower-extremity segments modeled as frusta of cones.
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Baseline measurements Age, height, mass, leg dominance, and end-range of ankle dorsi-flexion motion with 0° (straight) and 45° (bent) of KF
Familiarization with MVIC performance Standard instructions and supervised training of MVIC performed with 0° and 45° of KF
Warm-up 7-min of easy cycling on a stationary ergometer
MVICpre Recording of data from 3 MVICpre with 0° of KF and 3 MVICpre with 45° of KF, in a randomized order and with 2-min rest after each MVICpre Preparation for the 3D motion capture Positioning of 49 reflective markers
Familiarization with heel-raise cycle performance Standard instructions and supervised training of heel-raise cycles performed on an incline with 0° or 45° of KF, depending on the randomized order Repeated with Static calibration
the knee in the
Recording of data for 10-s in the appropriate anatomical position for static calibration
other position
Heel-raise test Recording of data from an MVIC pre + HRT + MVICpost with the knee at 0° or 45° of KF, depending on the randomized order and with 2-min rest after the MVICpre, rating of perceived (calf muscle) exertion after the HRT, and 60-min rest after the MVICpost
Fig. 1. Flow diagram illustrating the experimental procedure performed by each participant. Abbreviations: KF, knee flexion; MVIC, maximal voluntary isometric contraction.
Prior to each trial, the measurement volume was calibrated using a 750-mm wand and an L-frame that defined the Cartesian origins of the laboratory. Each participant then stood still in the appropriate anatomical position in the middle of this volume for 10-s to allow static calibration and case-specific model definition. The local coordinates of all body segments were derived from this static measurement and used as reference coordinates for the eminent HRT trial. 2.5. Data processing 2.5.1. Maximal voluntary isometric contractions The vertical ground reaction forces registered during each MVIC were downloaded in the ASCII format and low-pass filtered (Butterworth fourth order, zero-lag) at 10-Hz. The peak plantar-flexion force was normalized to bodyweight (BW), employing 9.82 m·s−1 as the gravitational constant. The highest MVICpre was subtracted from the highest MVICpost value to obtain the pre-to-post change in force at both 0° and 45° of KF. 2.5.2. Heel-raise tests The kinematic and kinetic data from all HRT trials were exported in the c3d format and processed in Visual3D. These data were low-pass filtered (Butterworth fourth order, zero-lag) at 10-Hz and 50-Hz, respectively. Each trial was divided into cycles based on the vertical position and velocity of the heel marker. Each cycle included two consecutive
heel-to-incline contacts and had an instance at maximal heel-raise height. To identify cycles, all maximal heights within a 100-frame (333-ms) window were located. Then, starting from each maximal vertical coordinate, the end-point of the corresponding cycle was defined when the vertical velocity of the heel attained −0.02 m·s−1; and the starting point of the consequent cycle, when this same curve attained +0.02 m·s−1. The number of maximal heights defined the total number of cycles completed, while the difference between the vertical position of the heel at maximal and minimal height defined the maximal height reached during each cycle. The count and maximal height measures are the most practical and useful in clinics (Silbernagel et al., 2010). Kinematic parameters were calculated using rigid-body analysis and the Euler angles obtained from the static calibration. Sagittal plane knee and ankle-joint angles were computed using an x–y–z Cardan sequence equivalent to the Joint Coordinate System (Grood and Suntay, 1983). The primary kinematic outcomes examined were the mean knee-joint angle; the knee and ankle-joint angles at the instance of heel-to-incline contact and maximal heel-raise height; and the range of ankle motion during cycles. The vertical displacement of the center of mass, estimated from each individual's full-body biomechanical model using standard procedures (Hanavan, 1964), exhibited strong correlation with the vertical displacement of the heel [mean (SD): 0.92 (0.05); range: 0.79 to 0.99]. In light of these similarities between the movement patterns of the heel and center of mass, only the former was treated.
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0° of KF
45° of KF
0° of KF
45° of KF
Fig. 2. The end-range of ankle dorsi-flexion motion of the dominant leg was established for each participant by determining the maximal slope at which the heel was still in contact with the adjustable incline. Ankle angles were measured using an extendable goniometer (bottom pictures) with positioning at 0° (left pictures) and 45° (right pictures) of KF. The 90° angle at the ankle represents the neutral position, with the 5th metatarsal bone perpendicular to the fibula. More acute angles than 90° reflect greater dorsi-flexion. To avoid muscle straining during the heel-raise test, the incline was adjusted to ~5° less than the one determined here. Abbreviation: KF, knee flexion.
Kinetic parameters were calculated after the addition of a force structure in Visual3D to consider that participants stood on an incline rather than on the force plate itself. The primary kinetic outcomes assessed were the normalized peak vertical ground reaction forces (expressed as %BW) and the range of anterior–posterior and medial–lateral displacements of the center of pressure (CoP) normalized to body height (expressed as %BH) during cycles. To quantify the influence of fatigue on the biomechanical performance of the HRT, the lines obtained through the linear regression of each parameter across the cycles of one HRT trial were extrapolated to the y-axis.
outcomes from testing under a known set of conditions. When there was a significant interaction effect, the data were reanalyzed utilizing the mixed-effects model with the main effects of KF (0° and 45°) and four different groups (younger males, younger females, older males and older females), with the younger males as the arbitrary reference group for comparison. A P-value ≤0.05 was defined as statistically significant prior to all analyses. All analyses took the repeated-measures design of this study into consideration and were performed using Stata/IC v.11.2 (StataCorp LP, College Station, TX, USA) and Microsoft Excel 2010 (Microsoft Corp., Redmond, WA, USA).
2.6. Data analysis
3. Results
Mean and standard deviation [mean (SD)] values were computed for all variables. Mixed-effects models and stepwise regressions were applied to assess the main effects of KF (0° and 45°), sex (male and female) and age (20 to 40 years and 40 to 60 years) on all outcomes, as well as the interaction effect between sex and age. The model employed a Gaussian distribution, clustered measures within participants and applied exchangeable correlation matrices. For analysis of the total number of cycles, a Poisson distribution was used. Non-significant effects were removed from the original model during stepwise regression, starting with the interaction effect and then main effects. Thus, the final regressed model contained only significant effects and its coefficients (expressed as β [SE]) were used to compare
A descriptive summary of the data from the MVIC and HRT trials at both KF angles and corresponding results from analyses are reported in Table 1; and those specific to changes in biomechanical performance during the HRT, in Table 2. In all cases, the sex–age interaction was removed during stepwise regression, except for the instantaneous knee and ankle angles at maximal height and peak vertical ground reaction forces during cycles (see Table 1 in supplementary material). In comparison to the arbitrary reference group (i.e., younger males), younger females had more extensive ankle plantar-flexion angles at maximal height (P = 0.017) and vertical ground reaction forces during cycles (P = 0.041) and older females had larger KF angles at maximal height (P b 0.001). No other between-group differences were significant.
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Anterior view
Posterior view
Balance support
Balance support
Adjustable incline Adjustable incline
Kistler force plate
Kistler force plate
45° of KF
0° of KF
Fig. 3. Anterior (top left) and posterior (top right) views showing the 49 retro-reflective markers used to capture motion during the heel-raise test. The bottom left and right pictures depict the set-up for the heel-raise test at 0° and 45° of KF, respectively, involving an adjustable incline, Kistler force plate and balance support suspended from the ceiling. The markers used in the post-processing and analysis of data are circled in these bottom pictures (if visible). Abbreviation: KF, knee flexion.
At termination of the HRT, all participants perceived similar levels of (calf muscle) exertion, regardless of KF angle, sex and age (P ≥ 0.323, Table 1). The plantar-flexion force during MVICpost was −25.4 (25.9) %BW lower than during MVICpre, with no significant main effect of KF, sex or age (P ≥ 0.086). The total number of cycles and maximal heel-raise heights did not differ significantly between sexes or the two age groups (P ≥ 0.142, Table 1), but were dissimilar at the two KF angles (P ≥ 0.038, Table 1). Participants completed 37 (13) [range: 15 to 69] and 40 (17) [range: 9 to 86] cycles at 0° and 45° of KF, reaching 11.6 (2.3) [range: 7.4 to 16.9] and 10.7 (2.7) [range: 5.7 to 17.6] cm at maximal heel-raise height. The regression coefficients (β [SE]) indicate that KF was 3.4 [1.3]° and 3.2 [1.6]° greater throughout testing and upon heel-to-incline contact in older adults; and that the ranges of anterior–posterior and medial–lateral displacements of the CoP were 0.2 [0.1] and 0.08 [0.03] %BH smaller at 45° than 0° of KF. Although the instantaneous ankle joint angles at heel-to-incline contact and at maximal heel-raise height differed between KF angles, the range of ankle motion was similar (P = 0.252).
Neither sex nor age influenced the slope of the linearly regressed lines for the biomechanical parameters across cycles (Table 2), except for peak forces decreasing to a greater extent in males than females (P = 0.028). In contrast, the KF angle exerted a significant impact on several slope lines. The drop in maximal heights, plantar-flexion angles at maximal height, and ranges of ankle motion per cycle were all greater with the knee straight (P ≤ 0.025). As testing progressed, larger KF angles were observed at both 0° and 45° of nominal KF, except upon heel-to-incline contact where the slope of the linear regression suggests a slight decrease in the KF angle during testing at 45° [−1.6 (15.7)° × 10−2·cycle−1]. The ranges of anterior–posterior and medial–lateral displacements of the CoP also decreased as the number of cycles performed increased, with more pronounced attenuation in the anterior–posterior direction during testing at 0° (P = 0.030). 4. Discussion The present characterization and comparison of the biomechanics and clinical outcomes of the HRT performed to volitional exhaustion
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Table 1 Biomechanical and clinical parameters of heel-raise cycle performance at 0° and 45° of knee flexion for all of the participants combined (n = 56). The values in the second column are the means (standard deviations) for all of the cycles of the test. The results from the analyses using mixed-effects models and stepwise regressions are presented in the third and fourth columns. Main effecta β [SE], P-value
Knee flexion angle Mean (SD)
Parameter
Interaction P-value
0°
45°
KF
Sex
Age
Sex–age
−26.5 (23.6)
−24.4 (28.3)
ns, 0.644
ns, 0.716
ns, 0.086
0.710
37 (13) 11.6 (2.3) 16.6 (1.5)
40 (17) 10.7 (2.7) 16.4 (1.5)
3 [2], 0.038 0.9 [0.3], 0.001 ns, 0.323
ns, 0.907 ns, 0.142 ns, 0.429
ns, 0.605 ns, 0.896 ns, 0.355
0.958 0.237 0.312
Ankle angle (°) At heel-to-incline contact At maximal heel-raise height Range of motion
76.9 (13.6) 104.2 (15.9) 27.3 (7.0)
71.8 (12.7) 98.3 (15.6) 26.4 (7.8)
5.0 [0.6], b0.001 −6.0 [0.9], b0.001 ns, 0.252
ns, 0.159 na, 0.017 ns, 0.397
ns, 0.871 ns, 0.285 ns, 0.501
0.139 0.045 0.107
Knee angle (°) At heel-to-incline contact At maximal heel-raise height During a heel-raise cycle
7.8 (9.3) 12.7 (7.6) 10.1 (7.2)
44.5 (6.2) 46.5 (6.5) 45.4 (5.4)
36.7 [1.3], b0.001 33.8 [1.0], b0.001 35.3 [1.0], b0.001
ns, 0.767 ns, 0.557 ns, 0.544
3.2 [1.6], 0.046 ns, 0.795 3.4 [1.3], 0.007
0.556 0.015 0.093
3.0 (0.8) 1.2 (0.2)
2.8 (0.8) 1.1 (0.3)
−0.2 [0.1], 0.022 −0.08 [0.03], 0.011
ns, 0.222 ns, 0.133
ns, 0.460 ns, 0.236
0.914 0.185
−9.6 [1.4], b0.001
na, 0.041
ns, 0.317
0.049
MVIC (%BW) Change in forceb Outcomes Number of cycles (count) Maximal heel-raise height (cm) Rating of perceived exertion (6–20)
Center of pressure (%BH) Anterior–posterior Medial–lateral Force (%BW) Peak during heel-raise cycles
127.6 (13.3)
118.2 (9.3)
Abbreviations: KF, knee flexion; MVIC, maximal voluntary isometric contraction; BW, bodyweight; BH, body height; ns, not significant; na, not applicable. a The β [SE] values are provided when the main effect is significant and not influenced by a significant interaction effect. b Calculated by subtracting MVICpre from MVICpost.
on an incline support our primary hypothesis that these outcomes would differ between knee straight (0°) and bent (45°) conditions. In general, our participants completed more cycles and showed better biomechanical maintenance of performance during the HRT at 45°, suggesting that performing the single-legged HRT on an incline while maintaining different KF angles may be of value in the assessment and training of triceps surae endurance. However, whether the differences detected here under experimental conditions are easy to discern in clinical settings, useful for conceptualizing individualized care and are
sufficient in magnitude to reflect specific responses in the soleus and gastrocnemius muscles require further examination. As one illustrative example, our participants completed on average 3 more cycles with the knee at 45° than 0°, which corresponds to a 7% difference in outcomes or a 0.2 standardized difference in mean. This standardized difference would be termed small and borderline trivial in practical settings by Hopkins et al. (2009) and may not reflect a substantial alteration in the relative contributions of, or respective fatigue in, the soleus and/or gastrocnemius muscles. The total amount of
Table 2 Alterations in the biomechanical parameters of heel-raise cycle performance at 0° and 45° of knee flexion for all of the participants combined (n = 56). The values in the second column are the means (standard deviations) of the slopes of the regression lines across all of the cycles of the test. The results from the analyses using mixed-effects models and stepwise regressions are presented in the third and fourth columns. Main effecta β [SE] × 10−2, P-value
Knee flexion angle Mean (SD) × 10−2
Parameter
0° Heel marker (cm·cycle−1) At maximal heel-raise height
45°
Interaction P-value
KF
Sex
Age
Sex–age
5.4 [0.8], b0.001
ns, 0.144
ns, 0.260
0.869
ns, 0.081 9.9 [3.4], 0.003 6.1 [2.7], 0.025
ns, 0.695 ns, 0.481 ns, 0.749
ns, 0.492 ns, 0.426 ns, 0.791
0.419 0.767 0.894
−15.1 (8.0)
−9.5 (6.7)
Ankle angle (°·cycle ) At heel-to-incline contact At maximal heel-raise height Range of motion
−0.7 (16.5) −41.3 (25.3) −42.0 (24.8)
−4.3 (10.8) −31.2 (20.1) −35.5 (20.9)
Knee angle (°·cycle−1) At heel-to-incline contact At maximal heel-raise height During heel-raise cycles
5.9 (20.4) 13.0 (19.3) 7.9 (12.5)
−1.6 (15.7) 9.8 (23.4) 4.3 (11.9)
−7.5 [3.1], 0.013 ns, 0.319 ns, 0.075
ns, 0.407 ns, 0.550 ns, 0.127
ns, 0.902 ns, 0.170 ns, 0.484
0.842 0.210 0.354
−1
Center of pressure (%BH∙cycle−1) Anterior–posterior Medial–lateral
−2.6 (2.5) −0.8 (1.4)
−1.5 (2.3) −0.9 (1.0)
1.1 [0.5], 0.030 ns, 0.777
ns, 0.322 ns, 0.762
ns, 0.893 ns, 0.510
0.566 0.771
Force (%BW·cycle−1) Peak during a heel-raise cycle
−0.9 (4.4)
−1.0 (2.2)
ns, 0.794
1.8 [0.8], 0.027
ns, 0.141
0.138
Abbreviations: KF, knee flexion; BH, body height; BW, body weight; ns, not significant. a The β [SE] values are provided when the main effect is significant and not influenced by a significant interaction effect.
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vertical (number of cycles × maximal height) and angular (number of cycles × ankle range of motion) displacements at the two KF angles did not differ by more than 2.5%, indicating that the mechanical work performed at these two angles was comparable for a given bodyweight. Our participants probably could complete more cycles at 45° because of the smaller ranges of motion at the heel and ankle. Most of the other outcomes (e.g., reduction in MVIC force, ratings of perceived exertion and decline in peak force) indicated that HRT-induced plantar-flexion fatigue was similar between angles. One biomechanical characteristic that was different between 0° and 45° was the nature of the ankle range of motion. With 45° of KF, dorsi-flexion upon heel-to-incline contact was greater, while plantarflexion at maximal heel-raise height was smaller. As gains from muscle training are specific to the range of motion (Morrissey et al., 1995), the choice of KF may be important when employing the HRT for individualized assessment and/or training. Moreover, together with alterations in knee-joint angles (Arndt et al., 1998), differential strains in the Achilles tendon and aponeuroses are associated with change in ankle-joint angles (Muramatsu et al., 2001). Although not quantified in this study; these tensile strains certainly differ under the two testing conditions, may result in differential adaptations to fatiguing heel-raise exercises, and could be examined using ultrasound. In fact, the contractile behaviors of the human gastrocnemius and soleus muscles change differently when walking at accelerating speeds and/or for a prolonged period of time (Cronin et al., 2013a). Although these latter experimental conditions differ from ours; both involve cyclic activities in an upright stance that rely on the triceps surae muscles. Therefore, the contractile behaviors of the soleus and gastrocnemius muscles probably also differ to a significant extent during the HRT as the KF angle and/or number of cycles completed increase. Since kinematics and kinetics do not always adequately reflect muscle function (Cronin et al., 2013b), studies designed to examine the individual behaviors of the soleus and gastrocnemius muscles are required to verify these assumptions, e.g., by using electromyography to detect muscle onset and offset or ultrasonography to monitor muscle lengthening and shortening. Increasing KF angles is one strategy for lowering the center of mass and maintaining balance (Nashner et al., 1979), possibly explaining why the KF angle increased as the HRT progressed (Table 2) and was greater in older participants (Table 1). Likewise, the anterior–posterior and medial–lateral displacements in the CoP were smaller with the knee at 45° versus 0°, likely due to the enhanced stability of the position. A more extensive displacement of the CoP towards the end of the HRT was expected as stabilization decreases with lower-extremity muscle fatigue (Reimer and Wikstrom, 2010). Interestingly, the negative slopes of the CoP regression lines indicate that the anterior–posterior and medial–lateral displacements of the CoP were smaller at the end of testing. This finding can be linked to the greater KF angles, smaller ranges of ankle motion and lower heel-raise heights observed with continued testing resulting in a lower center of mass and reduced area over which the body moves. Further, fatiguing the distal (e.g., ankle) musculature exerts a much smaller impact on one's stabilization than fatiguing the proximal (e.g., hip) leg musculature (Bisson et al., 2011). Corbeil et al. (2003) observed no significant change in the range of CoP motion following 100 bilateral heel-raise cycles and proposed that the postural control system can maintain CoP displacement despite fatigue of the plantar-flexors. Our secondary hypothesis that females and older individuals would demonstrate greater fatigue during testing must be rejected based on our study results. The only significant sex- or age-related difference detected here was the more rapid decline in the peak ground reaction forces in male than female participants during testing. This observation is consistent with Larsson et al. (2006) who reported a more pronounced decline in the plantar-flexion torque of males than females during an isokinetic fatiguing protocol that was correlated to the larger and greater proportion of fast-twitch fibers
in the male gastrocnemius muscle. Although the specific mechanisms explaining why our females showed slightly better maintenance of plantar-flexion force during the HRT remain unclear, these may involve sex-specific metabolic pathways, activation strategies, muscle masses and perfusion (Enoka and Duchateau, 2008). Three factors in the present investigation of clinical relevance are the maintenance of KF angles, the number of cycles completed and the cohort investigated. First, the ability of our participants to match a given KF angle in a weight-bearing situation agrees with earlier research (Stillman and McMeeken, 2001). Participants did, however, flex the knee by ~10° in the condition that required 0°, supporting previous findings that most individuals cannot keep the knee straight at 0° during plantar-flexion testing (Arndt et al., 1998) demonstrating that 10° of flexion is likely a more natural and functional position at the knee. Secondly, the total number of cycles completed was ~ 40 in all age and sex groups. By documenting performance of the single-legged HRT with 0° of KF in 203 individuals, Lunsford and Perry (1995) concluded that completing 25 cycles reflected normal plantar-flexion function in both males and females of similar age as our cohort. This criterion is still applied in research (Bennett et al., 2012) despite evidence that it appears to underestimate the maximal ability of individuals (Hébert-Losier et al., 2012; Silbernagel et al., 2010). Even 6-mth and 12-mth post Achilles tendon rupture, more than 25 cycles are performed (Silbernagel et al., 2010). Reference values for the singlelegged HRT should be up regulated to assist in the comparison, interpretation and use of outcomes. Finally, Reid and colleagues (2012) found greater activation of the triceps surae muscles during single-legged heel-raise cycles in individuals with Achilles tendinopathy, at both 0° and 45° of KF. Wyndow et al. (2013) also observed differential recruitment patterns of the soleus and gastrocnemius muscles of runners with Achilles tendinopathies, suggesting differences in the intra-tendinous loads. Accordingly, our results should not be applied directly to individuals with pathologies and further research in this area is indicated. 5. Conclusions In conclusion, although there were certain differences in the biomechanical performance and clinical outcomes of the single-legged HRT performed on an incline between 0° and 45° of KF, these differences may be difficult to detect and quantify in clinical practice. The lack of any major difference between 0° and 45° may be of significant interest to clinicians and researchers who use this test, especially over time since there may be no major concern regarding the exact knee angle of the individual being tested. Neither sex nor age exerted any pronounced impact on the outcomes of the HRT; all our participants completed ~ 40 cycles both with the knee straight and bent. Under pathological conditions, the differences detected here between the two KF angles may be amplified and this possibility warrants further investigation. Conflict of interest statement There are no relevant conflicts of interest to declare that relate to this research project. No specific source of funding was required during the preparation of this paper. Acknowledgments The authors would like to thank the team working at Qualisys AB, Sweden, for their technical assistance; in particular, from Patrik Almström during the set-up for this project and from Dr. Nils F. Betzler during the data processing and Visual3D scripting. The authors are also grateful for the research assistance from Sarah J. Willis, MSc, and Maria Hansson, PT, during data collection and the voluntary participation of all the participants.
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Appendix A. Supplementary data Supplementary data to this article can be found online at http:// dx.doi.org/10.1016/j.clinbiomech.2013.06.004.
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Biomechanics of the heel-raise test performed on an incline in two knee flexion positions Kim Hébert-Losier ⁎, Hans-Christer Holmberg Swedish Winter Sports Research Centre, Department of Health Sciences, Mid Sweden University, Kunskapens väg 8, Hus D, 83125 Östersund, Sweden
a r t i c l e
i n f o
Article history: Received 21 April 2013 Accepted 6 June 2013 Keywords: Plantar-flexion Triceps surae muscles Endurance Clinical test Fatigue
a b s t r a c t Background: Although single-legged heel-raise cycles are often performed on an incline in different knee flexion positions to discriminate the relative contribution of the triceps surae muscles, detailed kinematic and kinetic analyses of this procedure are not available. Our study characterizes and compares the biomechanics and clinical outcomes of single-legged heel-raise cycles performed to volitional exhaustion on an incline with the knee straight (0°) and bent (45°), considering the effect of sex and age. Methods: Fifty-six male and female volunteers, with equal numbers of younger (20 to 40 years of age) and older (40 to 60 years of age) individuals, completed a maximal number of heel-raise cycles on an incline at both nominal knee angles. Kinematic and kinetic data were acquired during testing using a 3D motion capturing system and multi-axial force plate. The impact of fatigue on performance was quantified using changes in maximal voluntary isometric contraction force and biomechanical performance of cycles. Findings: Overall, participants completed three more cycles and maintained better biomechanical performance with 45° than 0° of knee flexion. More precisely, the decreases in maximal heel-raise heights, plantar-flexion angles at maximal height and ranges of ankle motion per cycle were all smaller with the knee bent. However, several outcomes indicated similar plantar-flexion fatigue at both knee angles. Males demonstrated a more rapid decline in peak ground reaction forces during testing; but otherwise, neither sex nor age significantly impacted outcomes. Interpretation: It is concluded that the differences discerned here in the biomechanics of single-legged heel-raise cycles performed at 0° and 45° of knee flexion to volitional exhaustion on an incline may be too small to identify in clinical settings or reflect substantial alterations in the relative contribution of the triceps surae muscles. © 2013 Elsevier Ltd. All rights reserved.
1. Introduction During the 1940s poliomyelitis epidemic, rehabilitation professionals observed that the traditional manual muscle test was limited in assessing the anti-gravitational function of the triceps surae (Florence et al., 1992). Many individuals were not able to stand or walk due to an underlying plantar-flexion weakness, yet the plantar-flexors were given the highest test score and classified as functionally normal (Lunsford and Perry, 1995). To provide a more accurate and valid representation of plantarflexion function, manual resistance was replaced with the performance of heel-raise cycles in weight-bearing on one leg. Nowadays, to specifically examine the endurance characteristics of the triceps surae, heel-raise cycles are performed to volitional exhaustion, a procedure referred to herein as the heel-raise test (HRT). To characterize the relative contribution of the gastrocnemius and/or soleus muscles to plantar-flexion, heel-raises are performed in differing degrees of knee flexion (KF) (Alfredson et al., 1998; Stasinopoulos and Manias, 2013), with the HRT in 0° suggested for ⁎ Corresponding author. E-mail address: [email protected] (K. Hébert-Losier). 0268-0033/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.clinbiomech.2013.06.004
gastrocnemius and 45° for soleus. However, with a straight and bent knee, the total number of cycles completed (Hébert-Losier et al., 2011) and surface electromyography indicators of fatigue for soleus and gastrocnemius (Hébert-Losier et al., 2012) are comparable. Consequently, the muscle-selective value of performing the HRT for endurance in several KF angles is questionable. The two investigations referred to above were carried out with the foot initially on the ground and their outcomes may not apply to permutations of the heel-raise task when the foot is positioned on an incline (Silbernagel et al., 2010) or step edge (Alfredson et al., 1998; Reid et al., 2012). Currently, no detailed kinematic or kinetic analyses of the HRT performed on an incline at two distinct KF angles have been reported. Such studies would provide important information concerning the usefulness of evaluating heel-raise performance at differing KF angles, thereby assisting clinicians and researchers in interpreting and/or monitoring individuals' outcomes. Furthermore, age and sex are important factors in both practical and experimental settings. Most studies report lower plantar-flexion strength and endurance in females than males and in older than younger individuals (Danneskiold-Samsøe et al., 2009; Fugl-Meyer et al., 1980); however, the impact of age and sex is task-dependent (Hunter, 2009). Accordingly,
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there is debate regarding the impact of age and sex on HRT outcomes (Hébert-Losier et al., 2012; Lunsford and Perry, 1995). Our study was designed to characterize and compare the biomechanics and clinical outcomes of the single-legged HRT performed on an incline with the knee straight (0°) and bent (45°), while considering age and sex as confounders. Our primary hypothesis was that KF angle would influence these outcomes, with a greater number of heel-raise cycles being performed with the knee bent, thereby supporting the continued use of several KF angles. Our secondary hypothesis was that younger individuals and males would exhibit greater resistance to fatigue than older individuals and females. 2. Methods 2.1. Participants The participants for this study were recruited from the local community with recruitment advertised using selected e-mail distribution lists, local newspapers, bulletin-boards, online forums and word-of-mouth. After providing written informed consent, 56 volunteers took part in this study (28 males [mean (SD); age: 38 (12) years; height: 181 (7) cm; mass: 82 (9) kg] and 28 females [age: 41 (11) years; height: 169 (8) cm; mass: 69 (9) kg]), with equal numbers of both sexes aged between 20 to 40 and 40 to 60 years. Inclusion criteria were good self-reported health with regular physical activity and no current or recent musculoskeletal injury or medical contraindications. The research protocol was pre-approved by the Regional Ethical Review Board and adhered to the Declaration of Helsinki. 2.2. Study design The repeated-measures design (Fig. 1) of this study required each participant to take part in a single experimental session that included familiarization. To eliminate the potential influence of testing order and fatigue, each individual was tested on the dominant leg at 0° and 45° of KF in a block-randomized order according to age and sex, with half of the males and half of the females in each age group beginning at 0° and the others at 45° of KF. The same investigator carried out all kinematic and kinetic assessments. 2.3. Procedures 2.3.1. Baseline measures Age, height and mass were recorded on the day of testing. Leg dominance (51 right: 5 left) was determined using the Dunedin Footedness Inventory (Schneiders et al., 2010). Standing on the dominant leg, the end-range of ankle dorsi-flexion motion was assessed on an incline at both 0° and 45° of KF. The incline was adjusted to match the end-range of ankle dorsi-flexion (Fig. 2) and ankle angles measured using a goniometer (Model 01135, Lafayette Instrument Company®, Loughborough, UK). The angles were 72 (6)° and 64 (7)° at 0° and 45° of KF, where 90° represents the neutral position (i.e., the 5th metatarsal bone perpendicular to the fibula) and more acute angles reflect greater dorsi-flexion. 2.3.2. Maximal voluntary isometric contractions Plantar-flexion maximal voluntary isometric contractions (MVICs) were performed standing on the dominant leg before (MVICpre) and after (MVICpost) each HRT, at both 0° and 45° of KF. Using previously described methods (Hébert-Losier and Holmberg, 2013), participants stood underneath a weightlifting stand (Eleiko Sport AB, Halmstad, SE) on a DBA force plate (New Development Technologies AB, Farsta, SE) that recorded vertical ground reaction forces during MVICs at a rate of 200-Hz using the DBA® Software v.3.2 (see Fig. 1 in the supplementary material). To promote appropriate and maximal effort, standardized
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supervised training was provided before and emphatic verbal encouragement was given during MVIC trials. 2.3.3. Heel-raise tests Each participant performed a maximal number of single-legged heel-raise cycles on an incline at 0° and 45° of KF (Fig. 3), separated by 1-hr of rest, following previously described HRT protocols (HébertLosier et al., 2011; Hébert-Losier et al., 2012). To avoid strain from repetitive contractions in an elongated position (Garrett, 1990), the incline was adjusted to ~5° less than the previously established end-range of ankle dorsi-flexion motion. To ensure that there was no residual fatigue, the peak force at a given KF angle during the single MVICpre completed immediately preceding the HRT was compared to that of the three others that were performed earlier (see Fig. 1). The rest period was prolonged if the difference was greater than 5%. No participant expressed residual fatigue or soreness from the procedures preceding heel-raise testing. To assist balance, individuals were permitted to apply up to 2% of their bodyweight on a horizontal bar suspended in front of them at shoulder height. This bar was connected to a 0 to 50 kg force sensor and MuscleLab 4010 Unit with relevant software (Ergotest Innovation AS, Porsgrunn, NO), enabling the monitoring of force in real-time. Prior to testing, each participant went through an individualized familiarization session during which the investigator provided corrective feedback designed to ensure that the task was performed in an appropriate manner. Since the heel can be lifted without vertical displacement of the center of mass through hip flexion, each participant was instructed to lift their entire body upwards using their ‘calf’ muscles to reach a maximal (heel-raise) height, while maintaining the knee at the designated angle. The HRT cycle cadence was controlled at 60 per minute by a metronome (TempoPerfect© v.2.02, NCH Software, Canberra, AUS). Verbal feedback designed to maintain the HRT parameters regulating the cadence, balance support, heel excursion, and especially the KF angle was provided at regular intervals during testing. The test was terminated when participants could no longer lift the stance heel from the incline and/or repeat another cycle. Since the purpose was to investigate the biomechanics of performance of the HRT to volitional exhaustion, the test was not terminated if the specified threshold height of heel-raise was not reached, the set pace or KF angle was momentarily lost, or the balance support was inadvertently used to assist performance. Participants were asked to rate their perceived (calf muscle) exertion on the 6–20 point Borg (1982) scale at exhaustion. 2.4. Equipment 2.4.1. Motion capture Whole-body motion was monitored during the HRT at a rate of 300 Hz using a 3D motion analysis system consisting of 8 Oqus 300 infrared cameras and QTM software v.2.7 (Qualisys AB, Gothenburg, SE). A total of 49 retro-reflective markers (9 mm) were taped to the skin over anatomical landmarks using a variation of the Conventional (Full-Body) Gait Model (Bell et al., 1989), selected Oxford-foot markers (Stebbins et al., 2006) and additional lower-extremity tracking markers (Fig. 3). Ground reaction forces were collected during the HRT by having participants stand on the incline in the middle of a calibrated multi-axial force plate (Kistler 9281EA, Kistler Instrumente AG, Winterthur, CH). The QTM software was configured for synchronous collection of kinematic (i.e., Oqus cameras) and kinetic (i.e., Kistler force plate) data. From the reference set of markers, a full-body rigid-link biomechanical model with 6-degrees-of-freedom and 15 segments for the feet, shanks, thighs, pelvis, trunk, head, upper arms, forearms, and hands was constructed in Visual3D Professional™ Software v.4.96.7 (C-Motion Inc., Germantown, MD, USA). For kinematic analysis, the distal end of one segment was linked to the proximal end of another, with all lower-extremity segments modeled as frusta of cones.
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Baseline measurements Age, height, mass, leg dominance, and end-range of ankle dorsi-flexion motion with 0° (straight) and 45° (bent) of KF
Familiarization with MVIC performance Standard instructions and supervised training of MVIC performed with 0° and 45° of KF
Warm-up 7-min of easy cycling on a stationary ergometer
MVICpre Recording of data from 3 MVICpre with 0° of KF and 3 MVICpre with 45° of KF, in a randomized order and with 2-min rest after each MVICpre Preparation for the 3D motion capture Positioning of 49 reflective markers
Familiarization with heel-raise cycle performance Standard instructions and supervised training of heel-raise cycles performed on an incline with 0° or 45° of KF, depending on the randomized order Repeated with Static calibration
the knee in the
Recording of data for 10-s in the appropriate anatomical position for static calibration
other position
Heel-raise test Recording of data from an MVIC pre + HRT + MVICpost with the knee at 0° or 45° of KF, depending on the randomized order and with 2-min rest after the MVICpre, rating of perceived (calf muscle) exertion after the HRT, and 60-min rest after the MVICpost
Fig. 1. Flow diagram illustrating the experimental procedure performed by each participant. Abbreviations: KF, knee flexion; MVIC, maximal voluntary isometric contraction.
Prior to each trial, the measurement volume was calibrated using a 750-mm wand and an L-frame that defined the Cartesian origins of the laboratory. Each participant then stood still in the appropriate anatomical position in the middle of this volume for 10-s to allow static calibration and case-specific model definition. The local coordinates of all body segments were derived from this static measurement and used as reference coordinates for the eminent HRT trial. 2.5. Data processing 2.5.1. Maximal voluntary isometric contractions The vertical ground reaction forces registered during each MVIC were downloaded in the ASCII format and low-pass filtered (Butterworth fourth order, zero-lag) at 10-Hz. The peak plantar-flexion force was normalized to bodyweight (BW), employing 9.82 m·s−1 as the gravitational constant. The highest MVICpre was subtracted from the highest MVICpost value to obtain the pre-to-post change in force at both 0° and 45° of KF. 2.5.2. Heel-raise tests The kinematic and kinetic data from all HRT trials were exported in the c3d format and processed in Visual3D. These data were low-pass filtered (Butterworth fourth order, zero-lag) at 10-Hz and 50-Hz, respectively. Each trial was divided into cycles based on the vertical position and velocity of the heel marker. Each cycle included two consecutive
heel-to-incline contacts and had an instance at maximal heel-raise height. To identify cycles, all maximal heights within a 100-frame (333-ms) window were located. Then, starting from each maximal vertical coordinate, the end-point of the corresponding cycle was defined when the vertical velocity of the heel attained −0.02 m·s−1; and the starting point of the consequent cycle, when this same curve attained +0.02 m·s−1. The number of maximal heights defined the total number of cycles completed, while the difference between the vertical position of the heel at maximal and minimal height defined the maximal height reached during each cycle. The count and maximal height measures are the most practical and useful in clinics (Silbernagel et al., 2010). Kinematic parameters were calculated using rigid-body analysis and the Euler angles obtained from the static calibration. Sagittal plane knee and ankle-joint angles were computed using an x–y–z Cardan sequence equivalent to the Joint Coordinate System (Grood and Suntay, 1983). The primary kinematic outcomes examined were the mean knee-joint angle; the knee and ankle-joint angles at the instance of heel-to-incline contact and maximal heel-raise height; and the range of ankle motion during cycles. The vertical displacement of the center of mass, estimated from each individual's full-body biomechanical model using standard procedures (Hanavan, 1964), exhibited strong correlation with the vertical displacement of the heel [mean (SD): 0.92 (0.05); range: 0.79 to 0.99]. In light of these similarities between the movement patterns of the heel and center of mass, only the former was treated.
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0° of KF
45° of KF
0° of KF
45° of KF
Fig. 2. The end-range of ankle dorsi-flexion motion of the dominant leg was established for each participant by determining the maximal slope at which the heel was still in contact with the adjustable incline. Ankle angles were measured using an extendable goniometer (bottom pictures) with positioning at 0° (left pictures) and 45° (right pictures) of KF. The 90° angle at the ankle represents the neutral position, with the 5th metatarsal bone perpendicular to the fibula. More acute angles than 90° reflect greater dorsi-flexion. To avoid muscle straining during the heel-raise test, the incline was adjusted to ~5° less than the one determined here. Abbreviation: KF, knee flexion.
Kinetic parameters were calculated after the addition of a force structure in Visual3D to consider that participants stood on an incline rather than on the force plate itself. The primary kinetic outcomes assessed were the normalized peak vertical ground reaction forces (expressed as %BW) and the range of anterior–posterior and medial–lateral displacements of the center of pressure (CoP) normalized to body height (expressed as %BH) during cycles. To quantify the influence of fatigue on the biomechanical performance of the HRT, the lines obtained through the linear regression of each parameter across the cycles of one HRT trial were extrapolated to the y-axis.
outcomes from testing under a known set of conditions. When there was a significant interaction effect, the data were reanalyzed utilizing the mixed-effects model with the main effects of KF (0° and 45°) and four different groups (younger males, younger females, older males and older females), with the younger males as the arbitrary reference group for comparison. A P-value ≤0.05 was defined as statistically significant prior to all analyses. All analyses took the repeated-measures design of this study into consideration and were performed using Stata/IC v.11.2 (StataCorp LP, College Station, TX, USA) and Microsoft Excel 2010 (Microsoft Corp., Redmond, WA, USA).
2.6. Data analysis
3. Results
Mean and standard deviation [mean (SD)] values were computed for all variables. Mixed-effects models and stepwise regressions were applied to assess the main effects of KF (0° and 45°), sex (male and female) and age (20 to 40 years and 40 to 60 years) on all outcomes, as well as the interaction effect between sex and age. The model employed a Gaussian distribution, clustered measures within participants and applied exchangeable correlation matrices. For analysis of the total number of cycles, a Poisson distribution was used. Non-significant effects were removed from the original model during stepwise regression, starting with the interaction effect and then main effects. Thus, the final regressed model contained only significant effects and its coefficients (expressed as β [SE]) were used to compare
A descriptive summary of the data from the MVIC and HRT trials at both KF angles and corresponding results from analyses are reported in Table 1; and those specific to changes in biomechanical performance during the HRT, in Table 2. In all cases, the sex–age interaction was removed during stepwise regression, except for the instantaneous knee and ankle angles at maximal height and peak vertical ground reaction forces during cycles (see Table 1 in supplementary material). In comparison to the arbitrary reference group (i.e., younger males), younger females had more extensive ankle plantar-flexion angles at maximal height (P = 0.017) and vertical ground reaction forces during cycles (P = 0.041) and older females had larger KF angles at maximal height (P b 0.001). No other between-group differences were significant.
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Anterior view
Posterior view
Balance support
Balance support
Adjustable incline Adjustable incline
Kistler force plate
Kistler force plate
45° of KF
0° of KF
Fig. 3. Anterior (top left) and posterior (top right) views showing the 49 retro-reflective markers used to capture motion during the heel-raise test. The bottom left and right pictures depict the set-up for the heel-raise test at 0° and 45° of KF, respectively, involving an adjustable incline, Kistler force plate and balance support suspended from the ceiling. The markers used in the post-processing and analysis of data are circled in these bottom pictures (if visible). Abbreviation: KF, knee flexion.
At termination of the HRT, all participants perceived similar levels of (calf muscle) exertion, regardless of KF angle, sex and age (P ≥ 0.323, Table 1). The plantar-flexion force during MVICpost was −25.4 (25.9) %BW lower than during MVICpre, with no significant main effect of KF, sex or age (P ≥ 0.086). The total number of cycles and maximal heel-raise heights did not differ significantly between sexes or the two age groups (P ≥ 0.142, Table 1), but were dissimilar at the two KF angles (P ≥ 0.038, Table 1). Participants completed 37 (13) [range: 15 to 69] and 40 (17) [range: 9 to 86] cycles at 0° and 45° of KF, reaching 11.6 (2.3) [range: 7.4 to 16.9] and 10.7 (2.7) [range: 5.7 to 17.6] cm at maximal heel-raise height. The regression coefficients (β [SE]) indicate that KF was 3.4 [1.3]° and 3.2 [1.6]° greater throughout testing and upon heel-to-incline contact in older adults; and that the ranges of anterior–posterior and medial–lateral displacements of the CoP were 0.2 [0.1] and 0.08 [0.03] %BH smaller at 45° than 0° of KF. Although the instantaneous ankle joint angles at heel-to-incline contact and at maximal heel-raise height differed between KF angles, the range of ankle motion was similar (P = 0.252).
Neither sex nor age influenced the slope of the linearly regressed lines for the biomechanical parameters across cycles (Table 2), except for peak forces decreasing to a greater extent in males than females (P = 0.028). In contrast, the KF angle exerted a significant impact on several slope lines. The drop in maximal heights, plantar-flexion angles at maximal height, and ranges of ankle motion per cycle were all greater with the knee straight (P ≤ 0.025). As testing progressed, larger KF angles were observed at both 0° and 45° of nominal KF, except upon heel-to-incline contact where the slope of the linear regression suggests a slight decrease in the KF angle during testing at 45° [−1.6 (15.7)° × 10−2·cycle−1]. The ranges of anterior–posterior and medial–lateral displacements of the CoP also decreased as the number of cycles performed increased, with more pronounced attenuation in the anterior–posterior direction during testing at 0° (P = 0.030). 4. Discussion The present characterization and comparison of the biomechanics and clinical outcomes of the HRT performed to volitional exhaustion
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Table 1 Biomechanical and clinical parameters of heel-raise cycle performance at 0° and 45° of knee flexion for all of the participants combined (n = 56). The values in the second column are the means (standard deviations) for all of the cycles of the test. The results from the analyses using mixed-effects models and stepwise regressions are presented in the third and fourth columns. Main effecta β [SE], P-value
Knee flexion angle Mean (SD)
Parameter
Interaction P-value
0°
45°
KF
Sex
Age
Sex–age
−26.5 (23.6)
−24.4 (28.3)
ns, 0.644
ns, 0.716
ns, 0.086
0.710
37 (13) 11.6 (2.3) 16.6 (1.5)
40 (17) 10.7 (2.7) 16.4 (1.5)
3 [2], 0.038 0.9 [0.3], 0.001 ns, 0.323
ns, 0.907 ns, 0.142 ns, 0.429
ns, 0.605 ns, 0.896 ns, 0.355
0.958 0.237 0.312
Ankle angle (°) At heel-to-incline contact At maximal heel-raise height Range of motion
76.9 (13.6) 104.2 (15.9) 27.3 (7.0)
71.8 (12.7) 98.3 (15.6) 26.4 (7.8)
5.0 [0.6], b0.001 −6.0 [0.9], b0.001 ns, 0.252
ns, 0.159 na, 0.017 ns, 0.397
ns, 0.871 ns, 0.285 ns, 0.501
0.139 0.045 0.107
Knee angle (°) At heel-to-incline contact At maximal heel-raise height During a heel-raise cycle
7.8 (9.3) 12.7 (7.6) 10.1 (7.2)
44.5 (6.2) 46.5 (6.5) 45.4 (5.4)
36.7 [1.3], b0.001 33.8 [1.0], b0.001 35.3 [1.0], b0.001
ns, 0.767 ns, 0.557 ns, 0.544
3.2 [1.6], 0.046 ns, 0.795 3.4 [1.3], 0.007
0.556 0.015 0.093
3.0 (0.8) 1.2 (0.2)
2.8 (0.8) 1.1 (0.3)
−0.2 [0.1], 0.022 −0.08 [0.03], 0.011
ns, 0.222 ns, 0.133
ns, 0.460 ns, 0.236
0.914 0.185
−9.6 [1.4], b0.001
na, 0.041
ns, 0.317
0.049
MVIC (%BW) Change in forceb Outcomes Number of cycles (count) Maximal heel-raise height (cm) Rating of perceived exertion (6–20)
Center of pressure (%BH) Anterior–posterior Medial–lateral Force (%BW) Peak during heel-raise cycles
127.6 (13.3)
118.2 (9.3)
Abbreviations: KF, knee flexion; MVIC, maximal voluntary isometric contraction; BW, bodyweight; BH, body height; ns, not significant; na, not applicable. a The β [SE] values are provided when the main effect is significant and not influenced by a significant interaction effect. b Calculated by subtracting MVICpre from MVICpost.
on an incline support our primary hypothesis that these outcomes would differ between knee straight (0°) and bent (45°) conditions. In general, our participants completed more cycles and showed better biomechanical maintenance of performance during the HRT at 45°, suggesting that performing the single-legged HRT on an incline while maintaining different KF angles may be of value in the assessment and training of triceps surae endurance. However, whether the differences detected here under experimental conditions are easy to discern in clinical settings, useful for conceptualizing individualized care and are
sufficient in magnitude to reflect specific responses in the soleus and gastrocnemius muscles require further examination. As one illustrative example, our participants completed on average 3 more cycles with the knee at 45° than 0°, which corresponds to a 7% difference in outcomes or a 0.2 standardized difference in mean. This standardized difference would be termed small and borderline trivial in practical settings by Hopkins et al. (2009) and may not reflect a substantial alteration in the relative contributions of, or respective fatigue in, the soleus and/or gastrocnemius muscles. The total amount of
Table 2 Alterations in the biomechanical parameters of heel-raise cycle performance at 0° and 45° of knee flexion for all of the participants combined (n = 56). The values in the second column are the means (standard deviations) of the slopes of the regression lines across all of the cycles of the test. The results from the analyses using mixed-effects models and stepwise regressions are presented in the third and fourth columns. Main effecta β [SE] × 10−2, P-value
Knee flexion angle Mean (SD) × 10−2
Parameter
0° Heel marker (cm·cycle−1) At maximal heel-raise height
45°
Interaction P-value
KF
Sex
Age
Sex–age
5.4 [0.8], b0.001
ns, 0.144
ns, 0.260
0.869
ns, 0.081 9.9 [3.4], 0.003 6.1 [2.7], 0.025
ns, 0.695 ns, 0.481 ns, 0.749
ns, 0.492 ns, 0.426 ns, 0.791
0.419 0.767 0.894
−15.1 (8.0)
−9.5 (6.7)
Ankle angle (°·cycle ) At heel-to-incline contact At maximal heel-raise height Range of motion
−0.7 (16.5) −41.3 (25.3) −42.0 (24.8)
−4.3 (10.8) −31.2 (20.1) −35.5 (20.9)
Knee angle (°·cycle−1) At heel-to-incline contact At maximal heel-raise height During heel-raise cycles
5.9 (20.4) 13.0 (19.3) 7.9 (12.5)
−1.6 (15.7) 9.8 (23.4) 4.3 (11.9)
−7.5 [3.1], 0.013 ns, 0.319 ns, 0.075
ns, 0.407 ns, 0.550 ns, 0.127
ns, 0.902 ns, 0.170 ns, 0.484
0.842 0.210 0.354
−1
Center of pressure (%BH∙cycle−1) Anterior–posterior Medial–lateral
−2.6 (2.5) −0.8 (1.4)
−1.5 (2.3) −0.9 (1.0)
1.1 [0.5], 0.030 ns, 0.777
ns, 0.322 ns, 0.762
ns, 0.893 ns, 0.510
0.566 0.771
Force (%BW·cycle−1) Peak during a heel-raise cycle
−0.9 (4.4)
−1.0 (2.2)
ns, 0.794
1.8 [0.8], 0.027
ns, 0.141
0.138
Abbreviations: KF, knee flexion; BH, body height; BW, body weight; ns, not significant. a The β [SE] values are provided when the main effect is significant and not influenced by a significant interaction effect.
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vertical (number of cycles × maximal height) and angular (number of cycles × ankle range of motion) displacements at the two KF angles did not differ by more than 2.5%, indicating that the mechanical work performed at these two angles was comparable for a given bodyweight. Our participants probably could complete more cycles at 45° because of the smaller ranges of motion at the heel and ankle. Most of the other outcomes (e.g., reduction in MVIC force, ratings of perceived exertion and decline in peak force) indicated that HRT-induced plantar-flexion fatigue was similar between angles. One biomechanical characteristic that was different between 0° and 45° was the nature of the ankle range of motion. With 45° of KF, dorsi-flexion upon heel-to-incline contact was greater, while plantarflexion at maximal heel-raise height was smaller. As gains from muscle training are specific to the range of motion (Morrissey et al., 1995), the choice of KF may be important when employing the HRT for individualized assessment and/or training. Moreover, together with alterations in knee-joint angles (Arndt et al., 1998), differential strains in the Achilles tendon and aponeuroses are associated with change in ankle-joint angles (Muramatsu et al., 2001). Although not quantified in this study; these tensile strains certainly differ under the two testing conditions, may result in differential adaptations to fatiguing heel-raise exercises, and could be examined using ultrasound. In fact, the contractile behaviors of the human gastrocnemius and soleus muscles change differently when walking at accelerating speeds and/or for a prolonged period of time (Cronin et al., 2013a). Although these latter experimental conditions differ from ours; both involve cyclic activities in an upright stance that rely on the triceps surae muscles. Therefore, the contractile behaviors of the soleus and gastrocnemius muscles probably also differ to a significant extent during the HRT as the KF angle and/or number of cycles completed increase. Since kinematics and kinetics do not always adequately reflect muscle function (Cronin et al., 2013b), studies designed to examine the individual behaviors of the soleus and gastrocnemius muscles are required to verify these assumptions, e.g., by using electromyography to detect muscle onset and offset or ultrasonography to monitor muscle lengthening and shortening. Increasing KF angles is one strategy for lowering the center of mass and maintaining balance (Nashner et al., 1979), possibly explaining why the KF angle increased as the HRT progressed (Table 2) and was greater in older participants (Table 1). Likewise, the anterior–posterior and medial–lateral displacements in the CoP were smaller with the knee at 45° versus 0°, likely due to the enhanced stability of the position. A more extensive displacement of the CoP towards the end of the HRT was expected as stabilization decreases with lower-extremity muscle fatigue (Reimer and Wikstrom, 2010). Interestingly, the negative slopes of the CoP regression lines indicate that the anterior–posterior and medial–lateral displacements of the CoP were smaller at the end of testing. This finding can be linked to the greater KF angles, smaller ranges of ankle motion and lower heel-raise heights observed with continued testing resulting in a lower center of mass and reduced area over which the body moves. Further, fatiguing the distal (e.g., ankle) musculature exerts a much smaller impact on one's stabilization than fatiguing the proximal (e.g., hip) leg musculature (Bisson et al., 2011). Corbeil et al. (2003) observed no significant change in the range of CoP motion following 100 bilateral heel-raise cycles and proposed that the postural control system can maintain CoP displacement despite fatigue of the plantar-flexors. Our secondary hypothesis that females and older individuals would demonstrate greater fatigue during testing must be rejected based on our study results. The only significant sex- or age-related difference detected here was the more rapid decline in the peak ground reaction forces in male than female participants during testing. This observation is consistent with Larsson et al. (2006) who reported a more pronounced decline in the plantar-flexion torque of males than females during an isokinetic fatiguing protocol that was correlated to the larger and greater proportion of fast-twitch fibers
in the male gastrocnemius muscle. Although the specific mechanisms explaining why our females showed slightly better maintenance of plantar-flexion force during the HRT remain unclear, these may involve sex-specific metabolic pathways, activation strategies, muscle masses and perfusion (Enoka and Duchateau, 2008). Three factors in the present investigation of clinical relevance are the maintenance of KF angles, the number of cycles completed and the cohort investigated. First, the ability of our participants to match a given KF angle in a weight-bearing situation agrees with earlier research (Stillman and McMeeken, 2001). Participants did, however, flex the knee by ~10° in the condition that required 0°, supporting previous findings that most individuals cannot keep the knee straight at 0° during plantar-flexion testing (Arndt et al., 1998) demonstrating that 10° of flexion is likely a more natural and functional position at the knee. Secondly, the total number of cycles completed was ~ 40 in all age and sex groups. By documenting performance of the single-legged HRT with 0° of KF in 203 individuals, Lunsford and Perry (1995) concluded that completing 25 cycles reflected normal plantar-flexion function in both males and females of similar age as our cohort. This criterion is still applied in research (Bennett et al., 2012) despite evidence that it appears to underestimate the maximal ability of individuals (Hébert-Losier et al., 2012; Silbernagel et al., 2010). Even 6-mth and 12-mth post Achilles tendon rupture, more than 25 cycles are performed (Silbernagel et al., 2010). Reference values for the singlelegged HRT should be up regulated to assist in the comparison, interpretation and use of outcomes. Finally, Reid and colleagues (2012) found greater activation of the triceps surae muscles during single-legged heel-raise cycles in individuals with Achilles tendinopathy, at both 0° and 45° of KF. Wyndow et al. (2013) also observed differential recruitment patterns of the soleus and gastrocnemius muscles of runners with Achilles tendinopathies, suggesting differences in the intra-tendinous loads. Accordingly, our results should not be applied directly to individuals with pathologies and further research in this area is indicated. 5. Conclusions In conclusion, although there were certain differences in the biomechanical performance and clinical outcomes of the single-legged HRT performed on an incline between 0° and 45° of KF, these differences may be difficult to detect and quantify in clinical practice. The lack of any major difference between 0° and 45° may be of significant interest to clinicians and researchers who use this test, especially over time since there may be no major concern regarding the exact knee angle of the individual being tested. Neither sex nor age exerted any pronounced impact on the outcomes of the HRT; all our participants completed ~ 40 cycles both with the knee straight and bent. Under pathological conditions, the differences detected here between the two KF angles may be amplified and this possibility warrants further investigation. Conflict of interest statement There are no relevant conflicts of interest to declare that relate to this research project. No specific source of funding was required during the preparation of this paper. Acknowledgments The authors would like to thank the team working at Qualisys AB, Sweden, for their technical assistance; in particular, from Patrik Almström during the set-up for this project and from Dr. Nils F. Betzler during the data processing and Visual3D scripting. The authors are also grateful for the research assistance from Sarah J. Willis, MSc, and Maria Hansson, PT, during data collection and the voluntary participation of all the participants.
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Appendix A. Supplementary data Supplementary data to this article can be found online at http:// dx.doi.org/10.1016/j.clinbiomech.2013.06.004.
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