Knee joint kinematics and neuromuscular responses in female athletes during and after multi-directional perturbations

Human Movement Science 70 (2020) 102596

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Full Length Article

Knee joint kinematics and neuromuscular responses in female athletes during and after multi-directional perturbations

T

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Mohsen Damavandia,b, , Lishani Mahendrarajaha, Philippe C. Dixonc, Richard DeMonta a

Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, QC, Canada Faculty of Sport Sciences, Hakim Sabzevari University, Sabzevar, Iran c Department of Environmental Health, T.H. Chan School of Public Health, Harvard University, Boston, MA, USA b

A R T IC LE I N F O

ABS TRA CT

Keywords: Joint stability EMG Kinematics Lower limb Anterior cruciate ligament (ACL)

The purpose of this study was to investigate weight-bearing knee joint kinematic and neuromuscular responses during lateral, posterior, rotational, and combination (simultaneous lateral, posterior, and rotational motions) perturbations and post-perturbations phases in 30° flexed-knee and straight-knee conditions. Thirteen healthy female athletes participated. Knee joint angles and muscle activity of vastus lateralis (VL), vastus medialis (VM), biceps femoris (BF), semitendinosus (ST), lateral gastrocnemius (LG), and medial gastrocnemius (MD) muscles were computed. Knee abducted during lateral perturbations, whereas it adducted during the other perturbations. It was internally rotated during flexed-knee and externally rotated during straight-knee perturbations and post-perturbations. VL and VM's mean and maximum activities during flexed-knee perturbations were greater than those of straight-knee condition. BF's mean activities were greater during flexed-knee perturbations compared with straight-knee condition, while its maximum activities observed during combination perturbations. ST's maximum activities during combination perturbations were greatest compared with the other perturbations. LG and MG's activities were greater during straight-knee conditions. Compared with the perturbation phase, the mean and maximum muscles' activities were significantly greater during post-perturbations. The time of onset of maximum muscle activity showed a distinctive pattern among the perturbations and phases. The perturbation direction is an important variable which induces individualized knee kinematic and neuromuscular response.

1. Introduction Constant alterations of the motion patterns and neuromuscular control of the lower extremity muscles are required to maintain knee joint dynamic stability during athletic performance. These alternations could potentially increase the stress on the knee articular surfaces and tissue that in turn may impact on the knee stabilization (Li et al., 1999; Markolf et al., 1995). In addition, the weightbearing condition, the knee flexion angle, and sex can alter joint muscular responses and stability (Hsieh & Walker, 1976; Markolf, Bargar, Shoemaker, & Amstutz, 1981; Rozzi, Lephart, Gear, & Fu, 1999; Wilk et al., 1996). Renstrom, Arms, Stanwick, Johnson, and Pope (1986) demonstrated at knee flexion angles less than 15–30°, the knee stability is declined owing to the ineffective hamstrings action in limiting anterior and rotary tibial translation. Shultz et al. (2001) observed earlier quadriceps activation in female athletes

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Corresponding author at: Department of Health, Kinesiology and Applied Physiology, Concordia University, Montreal, QC, Canada. E-mail addresses: [email protected], [email protected] (M. Damavandi).

https://doi.org/10.1016/j.humov.2020.102596 Received 23 September 2019; Received in revised form 7 January 2020; Accepted 19 February 2020 Available online 28 February 2020 0167-9457/ © 2020 Elsevier B.V. All rights reserved.

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compared with males during rotational perturbations while the knee was 35° flexed. This may diminish the ability of the hamstrings to adequately stabilize the knee joint. Therefore, kinematic and neuromuscular adaptations of the weight-bearing knee in female athletes during different sport activities, as important determinants in providing joint stabilization and potential injury prevention, need to be well identified. The knowledge of these adaptations could enable us to identify the underlying causes of lesser joint stability in female athletes, which lead to three to five times higher rates of the anterior cruciate ligament (ACL) injury among them, compared with their male counterparts. Furthermore, this information can be applied by sports therapists to establish more efficient preventive strategies (e.g., neuromuscular trainings, improving at risk movement patterns, etc.) to increase knee functional stability in female athletes during sports activities. Sudden perturbations of the support surface beneath a single weight-bearing-leg have commonly been used to study the knee biomechanical and neuromuscular adaptations during standing (Chen et al., 2014; Gage, Frank, Prentice, & Stevenson, 2007; Schmitz, Shultz, Kulas, Windley, & Perrin, 2004; Shultz et al., 2000). During sudden external and internal perturbations of the trunk and femur relative to the weight-bearing tibia while the knee was 30° flexed, Schmitz et al. (2004) observed external perturbations resulted in significant internal rotation of the tibia on the femur and greater knee valgus position, while internal perturbations resulted in significant external rotation of the tibia on the femur and greater knee varus position. In a similar testing conditions, Shultz et al. (2000) found the gastrocnemius fired significantly faster than the hamstring, which in turn fired significantly faster than the quadriceps. These authors also observed the lateral hamstring was significantly slower in reaction to both internal and external rotation perturbation conditions compared with the medial hamstring. However, these findings explain the kinematic and muscular responses of weight-bearing knee only while the joint is flexed and during the internal and external rotations. Malfait et al. (2015) reported that the dynamic neuromuscular control of the knee is more challenging during single-plane perturbations compared with the multi-planar perturbations. However, their single-plane perturbations included purely translations in the lateral direction. Since perturbations in the sagittal (e.g. high-velocity acceleration/deceleration during running, forward/backward pushes on the trunk and upper leg of the weight-bearing foot in soccer, etc.) and horizontal (e.g. pivoting trunk and thigh relative to weight-bearing lower leg in handball and basketball) planes are common in various movements, the neuromuscular control of the knee during posterior perturbations and rotation around the vertical axis of the lower extremity also need to be evaluated. Furthermore, since the previous researches have evaluated the motion patterns and neuromuscular responses of the flexed knee (up to 30°), it is unclear how the knee behaves to maintain its equilibrium if the joint is fully extended during perturbations. Understanding the impact of perturbation directions on efficient neuromuscular control required for a dynamic joint stabilization during different knee angles will increase knowledge about appropriate evaluation methods and training programs for knee injuries. Previous studies investigated knee joint kinematics and neuromuscular activation patterns during different types of perturbations (Chen et al., 2014;Malfait et al., 2015; Schmitz et al., 2004; Shultz et al., 2000). However, to our knowledge, the knee kinematic and neuromuscular responses following the completion of these perturbations (post-perturbations) have not been investigated. Previous researches have shown that the muscle activity from the onset of the perturbations to 350 ms after their onset are associated with latencies of balance corrections (40–120 ms) and balance correcting (120–340 ms), while the stabilizing reaction responses occur from 350 to 700 ms following the initiation of the perturbations (Allum, Huwiler, & Honegger, 1996; Carpenter, Allum, & Honegger, 1999; Diener, Bootz, Dichgans, & Bruzek, 1983). Since in the previous researches the knee kinematic and muscle activity were studied during the balance correcting time interval of perturbations (Malfait et al., 2015; Schmitz et al., 2004; Shultz et al., 2000), the stabilizing reaction responses of the knee are not quantified. Thus, it remains unclear whether there are fundamental differences in the kinematic and neuromuscular responses during and after the perturbations. Knowledge of the knee joint behavior during and after the multi-directional perturbations could provide some insight on the balance control and injury mechanisms in female athletes. Thus, the purpose of this study was to investigate the knee joint kinematic and neuromuscular responses of the weight-bearing lower limb in two knee conditions during four perturbations and the related post-perturbations. The knee positions used were 30° flexed-knee and straight-knee (fully extended), while the perturbations were lateral, posterior, rotational, and a simultaneous combination of these three motions. From this study, we can identify the related knee stability mechanisms, the perturbation direction(s) with greater risk of knee injuries, and the effect of knee angle during each perturbation on the kinematic and muscle activity of the weight-bearing lower extremity. 2. Methods 2.1. Participants Thirteen female athletes from varsity university soccer and basketball teams (20.2 ± 1.4 years, 165.6 ± 8.5 cm, and 75.7 ± 28.4 kg) participated. They were physically active at least 5 days a week with no history of: (1) lower extremity injuries, (2) regular use of knee and/or ankle braces or taping for stability during physical activity, and (3) previous enrollment in an injury prevention exercise intervention program. Prior to participating in the study, all the procedures were explained to each participant and they signed a consent form, approved by the Human Research Ethics Committee of Concordia University. 2.2. Experimental set-up We used a perturbation platform including two fixed AMTI force plates (model OR6-5-1000, Watertown, MA, USA). As illustrated in Fig. 1, the force plates were stabilised on the platform equipped with an engine enabling movements in different directions creating multi-directional perturbations, including lateral, posterior, rotational (external rotation about the vertical axis of the platform), and 2

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Fig. 1. The perturbation platform including two AMTI force plates to create multi-directional perturbations (posterior, lateral, rotational, and a combination of them).

combinational perturbations. The combinational perturbation combined lateral, posterior, and rotational motions simultaneously. These perturbations could mimic the conditions during physical activities in which the weight-bearing limb is fixed on the ground and the body moves to other directions, slip and trip while walking, step on slippery and irregular surfaces, and side-stepping tasks. The linear velocity of the platform in posterior and lateral directions was 200 mm/s, while its angular velocity during rotational perturbation was 20°/s. The duration of each perturbation was set for 500 ms. To prevent falls, the participants were fitted with an adjustable upper body harness which did not impede their balance response. The perturbations were performed in 2 knee conditions: flexed-knee (30°, measured prior to the perturbations by hand-held goniometer) and straight-knee. The 30° knee flexion was chosen because while the knee is slightly flexed, the femur is externally rotated. The external rotation of the femur at flexed-knee condition, accompanied by the knee varus/valgus during the perturbations, simulate a common mecahnism of ACL injury (Andrews, Mcleod, Ward, & Howard, 1977). Furthermore, the knee flexion angles in female handball and basketball players with ACL injury ranged from 11 to 30° at initial contact (Koga et al., 2010). The experiments were conducted with a counterbalanced testing order and participant single-blind. After familirization to the perturbations, the participants were asked to stand as quiet as possible on their shod non-dominant (stance) leg with their hands on the iliac crests and head and eyes directed forward, as the perturbation platform moved in different directions. The non-dominant leg was determined by asking the participants which leg they would not use to kick a ball (Gstöttner et al., 2009). During the perturbations the unsupported leg was flexed and not touching the stance leg. Four trials were performed in each perturbation direction and for each one of the knee conditions (32 trails in total).

2.3. Data collection Kinematic data were collected using an 8-camera Vicon™ system (Vicon, Los Angeles, USA) at a sampling rate of 100 Hz. The participants were fitted with 16 reflective markers (14 mm diameter) according to the Vicon Plug-in-Gait model (Kadaba, Ramakrishnan, & Wooten, 1990). In addition, 4 reflective markers were put at the corners of the perturbation platform to determine the initiation and termination times of the perturbations. The activity of the stance lower extremity muscles were recorded using a 16-channel wireless system with a sampling frequency of 1500 Hz (Noraxon TeleMyo DTS, Scottsdale, Arizona, USA). Silver‑silver chloride bipolar surface EMG electrodes were placed over the muscle belly and aligned with the longitudinal axis of the vastus lateralis (VL), vastus medialis (VM), biceps femoris (BF), semitendinosus (ST), lateral gastrocnemius (LG), and medial gastrocnemius (MD) muscles, according to the SENIAM recommendations (Hermens, Freriks, Disselhorst-Klug, & Rau, 2000). The skin was shaved, abraded, and cleaned with alcohol before electrode placement. The interelectrode distances were 10 mm to reduce the crosstalk (De Luca, Kuznetsov, Gilmore, & Roy, 2012). In addition, cross-correlation analyses of EMG signals were conducted for one participant to quantify the crosstalk (Lowery, Stoykov, & Kuiken, 2003). The cross-correlation values were less than 0.30 (ranged from 0.16 to 0.27) that indicates low association between the muscle activity signals (Marshall & Murphy, 2003). Thus, the activity of each lower extremity muscle can be considered as isolated signal free of crosstalk. The EMG unit was synchronised with the motion capture system. Prior to the perturbations, the kinematic and muscle activity data were recorded during a quiet standing trial (static trial) for a period of 5 s to calculate the related offset values.

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2.4. Data analysis All the data were processed using biomechZoo (Dixon, Loh, Michaud-Paquette, & Pearsall, 2017) and custom codes in Matlab® (v2016b, The Math works Inc., Natick, MA, USA). The initiation and termination of the perturbations were determined when the linear velocity of the markers located on the corners of the perturbation platform crossed a 5 mm/s threshold. The kinematic data were filtered with a 4th order zero-lag low-pass Butterworth filter having a cut-off frequency of 7 Hz. The kinematic variables of the knee joint were obtained from the Vicon Plug-in-Gait model outputs during the static and perturbation trials. The knee angles during static trial were used as an indicator of a correct anatomical calibration (Benedetti et al., 2017) and to remove an offset from the perturbation trials. This approach was implemented to reduce the inter-participant variability of the results. The dependent variables were the mean, maximum, and the timing of maximum occurrence during the perturbation phases (%perturbation) of the threedimensional (3D) knee angles during-perturbations and 250 ms post-perturbations. To extract the muscle activity variables, first, the averages of the muscle activity values from the static trial were used to remove offsets for the muscle activities during each perturbation. Then, the raw muscle activity signals were filtered using a 4th order zerolag high-pass and low-pass Butterworth filters at a cut-off frequency of 20 Hz and 500 Hz, respectively (Robertson & Dowling, 2003). Afterward, the muscle activity signals were rectified and their root mean squares (RMS) were calculated and normalized to the maximum RMS of the corresponding maximum voluntary isometric contractions (MVIC) for each muscle. Finally, the muscle activity signals were down-sampled to match the kinematic data through spline interpolation. The dependant variables were the ensemble mean and maximum (peak) amplitudes of each muscle activity values (%MVIC), and the time of onset of maximum muscle activity amplitude during-perturbation and post-perturbation phases (%perturbation). 2.5. Statistical analysis The 3D kinematic variables of the knee joint and the muscle activity values of the lower extremity muscles were averaged across all the trials per condition within participants during-perturbation and post-perturbation phases. These variables were analyzed using MANOVA for repeated measures (2 knee conditions × 4 perturbations) in SPSS for Windows Version 20 (SPSS Inc., Chicago, IL, USA) within each phase. A Bonferroni post hoc test was performed, if a statistical main effect for conditions was observed (α = 0.05). The related effect sizes were calculated using standardised measure of Cohen's effect. Paired t-test between the two phases was applied for all the kinematic and muscle activity variables (α = 0.05). 3. Results 3.1. Kinematic results The mean knee angles were significantly different during-perturbations and post-perturbations in different knee conditions and directions (Table 1). For the sagittal plane, while there was no difference between the perturbations within each specific knee condition, the mean knee angles during the flexed-knee perturbations at the both phases were significantly higher (≥27.1°) compared with those of straight-knee perturbations (≤5.3°) (in all cases, P < .001, effect size ≥ 0.74). At the flexed-knee condition, the mean knee flexion angles were significantly lesser during post-perturbation phase compared to the perturbation phase for all the perturbation directions (in all cases, P < .001, effect size ≥ 0.89). Significant main effect differences in the mean knee angles were found in the frontal plane between the perturbation directions, knee conditions, and the perturbation phases as presented in Table 1. Generally, the tibia was abducted in relation to the femur during perturbations in lateral direction at the both knee conditions, whereas it adducted during perturbations in the other directions and post-perturbations. During-perturbations while the tibia abducted in relation to the femur during lateral perturbations at flexedknee (4.2°) and straight-knee (0.3°) conditions, it showed an adduction up to 5.2° in the other directions (in all cases, P ≤ .001, effect size ≥ 0.54). During the lateral direction perturbations, the tibia abducted at the both knee conditions in perturbation phase while it was adducted (1.2° to 2.8°) during post-perturbations (P < .001, effect size ≥ 0.35). In the transverse plane, distinct patterns of motion were observed between the flexed- and straight-knee conditions (Table 1). More specifically, while the tibia was internally rotated with respect to the femur during all the perturbations at flexed-knee condition at the both perturbation phases (up to 4.5°), it externally rotated during the straight-knee perturbations (up to 4.3°) (P ≤ .012, effect size ≥ 0.28). The maximum knee angles during- and post-perturbations in different directions and knee conditions are given in Table 2. In the sagittal plane, no difference between the perturbations within each specific knee condition was observed. The maximum knee angles during the flexed-knee perturbations at the both phases were significantly higher (≥28.6°) compared with those of straight-knee perturbations (≤8.1°) (in all cases, P < .001, effect size ≥ 0.69). At the flexed-knee condition, the maximum knee flexion angles were significantly greater during-perturbation phase compared to those of the post-perturbation phase for all the directions (in all cases, P < .001, effect size ≥ 0.73). For the frontal plane, significant main effect differences in the maximum knee angles were found between the perturbation directions, knee conditions, and the perturbation phases (Table 2). During-perturbations the maximum tibia abduction in relation to the femur in lateral perturbations at flexed-knee (5.0°) and straight-knee (1.1°) conditions were significantly different from the tibial adductions (up to 7.1°) observed in the other directions (in all cases, P ≤ .001, effect size ≥ 0.64). While during-perturbations in the lateral direction the tibia reached to its maximum abduction at the both knee conditions, the knee was adducted (2.8° to 4.9°) during 4

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Table 1 Mean knee angles (°) during posterior, lateral, rotational, and combination perturbations at flexed-knee (30°) and straight-knee conditions duringperturbations and post-perturbations. Plane

Knee condition

Perturbation direction

During-perturbation (SD)

Post-perturbation (SD)

Sagittal

Flexed

Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination

31.5 (5.1) 32.1 (5.1) 30.2 (4.4) 30.1 (4.4) 5.3 (5.0)a,b,c,d 3.4 (4.1)a,b,c,d 2.1 (5.1)a,b,c,d 5.0 (3.8)a,b,c,d −4.2 (2.6) 2.5 (5.0)a 5.2 (6.9)a 4.1 (6.1)a −0.3 (1.8)a,c,d 2.3 (3.2)a 2.1 (3.3)a 2.0 (3.2)a 4.4 (5.2) 4.5 (6.3) 0.6 (5.7) 1.6 (5.5) −2.9 (6.3)a,b,c,d −4.8 (6.6)a,b,c,d −3.9 (5.2)a,b,c,d −2.7 (5.7)a,b,c,d

29.2 (4.8)⁎ 29.4 (4.8)⁎ 27.8 (4.3)⁎ 27.1 (3.6)⁎ 4.1 (6.7)a,b,c,d 3.7 (4.9)a,b,c,d 2.1 (6.5)a,b,c,d 4.7 (6.8)a,b,c,d 2.8 (5.9)⁎ 3.2 (3.9) 4.0 (4.6) 2.2 (3.3) 1.2 (3.3)⁎ 2.4 (3.2) 1.4 (2.8) 2.0 (3.3) 4.6 (8.7) 3.6 (9.2) 1.7 (4.7) 2.2 (6.6) −1.2 (4.8)a,b,c,d −4.3 (7.3)a,b,c,d −4.2 (5.4)a,b,c,d −2.8 (7.7)a,b,c,d

Straight

Frontal

Flexed

Straight

Transverse

Flexed

Straight

−: abduction and external rotation of tibia with respect to the femur. +: adduction and internal rotation of tibia with respect to the femur. a Flexed-knee, lateral perturbation vs. other conditions (P < .05). b Flexed-knee, posterior perturbation vs. other conditions (P < .05). c Flexed-knee, rotational perturbation vs. other conditions (P < .05). d Flexed-knee, combination perturbation vs. other conditions (P < .05). ⁎ Significant differences between during-perturbation and post-perturbation phases.

post-perturbations in the lateral direction (P < .001, effect size ≥ 0.26). In the transverse plane, distinct knee motion patterns were observed between the flexed- and straight-knee conditions (Table 2). While the maximum tibial internal rotations with respect to the femur were observed during all the perturbations at flexed-knee condition during the both perturbation phases (up to 7.9°), maximum relative tibia external rotation occurred during the straightknee condition perturbations (up to 6.8°) (P ≤ .002, effect size ≥ 0.47). Table 3 presents time of maximum knee angles occurrence. The maximum knee flexion during the perturbations in different directions at flexed-knee condition occurred at the first half of the perturbation duration that were significantly earlier than those of the straight-knee condition (P ≤ .010, effect size ≥ 0.29). During post-perturbation phase, the maximum knee flexion during the perturbations in different directions at flexed-knee condition occurred at the first 25% of the perturbation duration that were significantly earlier than those of the straight-knee condition (P ≤ .001, effect size ≥ 0.51). Compared with the perturbation phase, the maximum knee flexion angles occurred significantly earlier during post-perturbations of all the directions and the knee conditions (P ≤ .007, effect size ≥ 0.49). Significant main effect differences in the timing of maximum knee angles were found in the frontal plane between the perturbation directions, knee conditions, and perturbation phases (Table 3). During-perturbation phase the earliest maximum angles occurred during lateral perturbations (before 30% of perturbation duration), the latest peak angles occurred during rotational perturbations (after 61% of perturbation duration) (P ≤ .030, effect size ≥ 0.29), whereas the related timing of the posterior and combination perturbations were between 30 and 60%. An inversed trend was observed in the post-perturbation phase; the earliest maximum angles occurred during rotational perturbations (before 45% of perturbation duration), and the latest peak angles occurred during lateral perturbations (after 56% of perturbation duration) (P ≤ .011, effect size ≥ 0.38). In the transverse plane and during-perturbation phase, the maximum knee angles occurred significantly later in lateral perturbations at the both knee conditions (after 76% of perturbation duration) (P ≤ .004, effect size ≥ 0.47). The maximum knee flexion angles occurred significantly earlier during post-perturbations in all the directions and the knee conditions (P ≤ .015, effect size ≥ 0.33), compared with the perturbation phase. 3.2. Muscle activity results Table 4 presents the mean muscle activity (%MVIC) of the knee muscles. The mean normalized activity of VL and VM muscles during- and post-perturbations in different directions at flexed-knee condition (ranging from 6.4 to 8.6%MVIC) were significantly 5

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Table 2 Maximum knee angles (°) during posterior, lateral, rotational, and combination perturbations at flexed-knee (30°) and straight-knee conditions during-perturbations and post-perturbations. Plane

Knee condition

Perturbation direction

During-perturbation (SD)

Post-perturbation (SD)

Sagittal

Flexed

Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination

32.7 (4.5) 33.3 (5.0) 32.5 (4.2) 32.0 (4.9) 8.1 (4.5)a,b,c,d 7.5 (3.4)a,b,c,d 5.0 (5.3)a,b,c,d 6.6 (5.6)a,b,c,d −5.0 (3.6) 5.0 (6.1)a 7.1 (6.1)a 5.2 (4.9)a −1.1 (1.6)a,b,c,d 2.9 (3.1)a,c,d 2.8 (2.9)a,c,d 2.6 (3.0)a,c,d 6.3 (8.3) 7.9 (8.7) 4.1 (8.8) 3.7 (9.8) −5.9 (7.3)a,b,c,d −6.6 (7.2)a,b,c,d −6.7 (10.5)a,b,c,d −5.2 (8.5)a,b,c,d

31.6 (4.5)⁎ 30.2 (4.9)⁎ 29.4 (4.6)⁎ 28.6 (4.0)⁎ 6.1 (5.5)a,b,c,d 5.9 (4.3)a,b,c,d 5.2 (4.3)a,b,c,d 7.8 (3.6)a,b,c,d 4.9 (4.9)⁎ 5.0 (5.8) 4.8 (5.4) 3.4 (2.5) 2.8 (3.3) ⁎ 2.7 (3.1)d 2.6 (2.5)d 2.7 (2.8)d 8.3 (9.4) 6.7 (9.2) 4.0 (7.3) 5.6 (8.6) −3.9 (9.4)a,b,c,d −6.5 (7.9)a,b,c,d −6.7 (10.7)a,b,c,d −6.8 (11.3)a,b,c,d

Straight

Frontal

Flexed

Straight

Transverse

Flexed

Straight

−: abduction and external rotation of tibia with respect to the femur. +: adduction and internal rotation of tibia with respect to the femur. a Flexed-knee, lateral perturbation vs. other conditions (P < .05). b Flexed-knee, posterior perturbation vs. other conditions (P < .05). c Flexed-knee, rotational perturbation vs. other conditions (P < .05). d Flexed-knee, combination perturbation vs. other conditions (P < .05). ⁎ Significant differences between during-perturbation and post-perturbation phases.

greater than those of the straight-knee condition (ranging from 2.5 to 4.1%MVIC) (P ≤ .037, effect size ≥ 0.48). Compared with the perturbation phase, the mean activity of VL and VM muscles were greater during post-perturbations in all the directions and knee conditions (P ≤ .027, effect size ≥ 0.29). Generally, the mean normalized activity of BF during the flexed-knee perturbations were significantly greater (ranging from 2.0 to 10.5%MVIC) than those of the perturbations at straight-knee condition (ranging from 1.3 to 7.9%MVIC) during- and post-perturbations (P ≤ .023, effect size ≥ 0.23) (Table 4). There was no significant difference in the mean normalized of ST's activity (P > .05). The mean activities of BF and ST muscles were between 2 and 4.7 times greater during post-perturbations in all the directions and knee conditions in comparison with those of the perturbation phase (P ≤ .006, effect size ≥ 0.61). For the LG, the greatest mean normalized activities were observed during the straight-knee combination perturbations duringand post-perturbations (9.9 and 24.8%MVIC, respectively) that were significantly different from those of the other perturbations (P ≤ .041, effect size ≥ 0.19) (Table 4). The mean activity values of MG were significantly greater during the perturbations at straight-knee condition for the both perturbation phases (P ≤ .001, effect size ≥ 0.33), as presented in Table 4. Similar to the other knee muscles, the mean activities of LG and MG muscles were greater during post-perturbations in all the directions and knee conditions compared with those of the perturbation phase (P ≤ .012, effect size ≥ 0.40) (Table 4). The maximum muscle activities (%MVIC) of the knee muscles are given in Table 5. The maximum activities of VL and VM muscles during- and post-perturbations in different directions at flexed-knee condition were significantly greater (ranging from 10.4 to 18.1% MVIC) than those of the straight-knee condition (ranging from 4.6 to 14.3%MVIC) (P ≤ .023, effect size ≥ 0.51). Compared with the perturbation phase, the maximum muscle activity values were greater during post-perturbations in all the directions and knee conditions (P ≤ .009, effect size ≥ 0.40), except for the VM muscle at flexed-knee posterior and combination perturbations. For the BF and ST muscles during-perturbation phase at the both knee conditions, generally the maximum normalized muscle activities were significantly smaller in rotational perturbations (ranging from 2.5 to 4.5%MVIC), and greater in combination perturbations (8.9–13.3%MVIC) than those of the other perturbation directions (P ≤ .028, effect size ≥ 0.24) (Table 5). During postperturbation phase the maximum normalized activities of the BF and ST muscles were significantly greater during combination perturbations at the both knee conditions (≥20.9% MVIC) (P ≤ .009, effect size ≥ 0.45). The BF and ST's maximum activities were significantly greater during post-perturbations than those of the perturbation phase in all the directions and knee conditions (P ≤ .003, effect size ≥ 0.61). Within the perturbation phase the maximum activity values of the LG and MG muscles were significantly smaller during lateral and rotational perturbations (ranging from 9.1 to 24.1%MVIC) compared with the posterior and combination perturbations (ranging 6

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Table 3 Time of maximum knee angles occurrence at flexed-knee (30°) and straight-knee conditions during-perturbations and post-perturbations. Plane

Knee condition

Perturbation direction

During-perturbation (SD)

Post-perturbation (SD)

Sagittal

Flexed

Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination

48.1 43.8 45.2 41.0 80.3 65.9 63.5 65.8 26.4 45.3 64.1 54.6 29.7 43.7 61.4 47.8 76.7 57.3 53.0 54.6 87.2 70.0 69.3 71.1

18.2 18.8 18.5 19.3 40.9 38.0 46.8 43.9 56.3 41.0 30.0 45.7 65.2 53.5 44.5 52.4 45.4 31.0 32.6 42.1 48.3 35.9 46.3 47.8

Straight

Frontal

Flexed

Straight

Transverse

Flexed

Straight

(22.8) (23.3) (33.6) (22.9) (15.6)a,b,c,d (25.6)a,b,c,d (34.5)a,b,c,d (31.1)a,b,c,d (32.3) (24.8)a (16.1)a,b (24.0)a (34.6)c,d (36.7)c (20.2)a,e (33.4)a,e (25.4) (23.4)a (36.8)a (33.1)a (20.0)b,c,d (31.9) (38.3) (31.5)

(30.3)⁎ (32.6)⁎ (30.0)⁎ (32.5)⁎ (32.6)a,b,c,d,⁎ (33.8)a,b,c,d,⁎ (26.3)a,b,c,d,⁎ (35.3)a,b,c,d,⁎ (46.3)⁎ (28.9) (36.0)⁎ (38.7) (36.6)c,⁎ (44.9)c (30.4)⁎ (39.2) (44.0)⁎ (37.5)⁎ (39.7)⁎ (36.6)⁎ (33.8)⁎ (37.4)⁎ (42.7)⁎ (31.9)⁎

−: abduction and external rotation of tibia with respect to the femur. +: adduction and internal rotation of tibia with respect to the femur. All time are presented as a % of perturbation and post-perturbation durations. a Flexed-knee, lateral perturbation vs. other conditions (P < .05). b Flexed-knee, posterior perturbation vs. other conditions (P < .05). c Flexed-knee, rotational perturbation vs. other conditions (P < .05). d Flexed-knee, combination perturbation vs. other conditions (P < .05). e Straight-knee, lateral perturbations vs. other conditions (P < .05). ⁎ Significant differences between during-perturbation and post-perturbation phases.

from 21.8 to 56.5%MVIC) at the both knee conditions (P ≤ .014, effect size ≥ 0.47) (Table 5). Within the post-perturbation phase greater LG muscle's peak tensions were observed during rotational and combination perturbations at the straight-knee condition (P ≤ .001, effect size ≥ 0.77), whereas the maximum activity values of the MG muscle were significantly lesser during the lateral perturbations at the both knee conditions (≥27.2%MVIC, P ≤ .001, effect size ≥ 0.81). Generally, the maximum activities of LG and MG were greater during post-perturbations in all the directions and knee conditions compared with the perturbation phase, (P ≤ .007, effect size ≥ 0.60). The relative time of onset of maximum muscle activity amplitudes (as a % of during-perturbation and post-perturbation durations) are presented in Table 6. During-perturbation phase the peak activities of VL at flexed-knee combination perturbation, and straight-knee posterior and combination perturbations were completed at 70.9%, 81.2%, and 81.4% of the perturbations, respectively, which were significantly later than those of the other perturbations (in all cases P ≤ .015, effect size ≥ 0.29). In the postperturbation phase, the time of onset of VL's peak activities during rotational perturbations at the both knee conditions were significantly later (≥82.5% of the phase) compared with the other perturbations (in all cases, P ≤ .005, effect size ≥ 0.38). Compared with the perturbation phases, the time of onset of maximum muscle activity amplitudes were earlier during the posterior and combination perturbations, and later during the rotational perturbations of the post-perturbations at the both knee conditions (P ≤ .001, effect size ≥ 0.69). The VM's time of onset of the peak activity in the perturbation phase was completed later (76.8% of the phase) during straightknee combination perturbations (P ≤ .002, effect size ≥ 0.39), whereas it occurred later during rotational perturbations at the both knee conditions within the post-perturbation phase (≥76.9% of the phase, P ≤ .010, effect size ≥ 0.31) (Table 6). Compared with the perturbation phases, the VM's time of onset of maximum peak activities were earlier during the flexed-knee combination and straight-knee posterior and combination perturbations (39.2–49.9% of the phase, P ≤ .001, effect size ≥ 0.70), and later during the rotational perturbations of the post-perturbations at the both knee conditions (76.9–87.1%, P ≤ .001, effect size ≥ 0.66). Within the perturbation phase, the time of onset of BF's maximum activities were completed later (78.9–94.1% of the phase) during the combination perturbations at the both knee conditions than those of other perturbation directions, more specifically the rotational perturbations (before 56.0% of the phase, P ≤ .009, effect size ≥ 0.26) (Table 6). Generally, in the post-perturbation phase, the time of onset of BF's peak activities during posterior and combination perturbations at the both knee conditions were significantly earlier (before 48.5% of phase) compared with the lateral and rotational perturbations (in all cases, P ≤ .012, effect size ≥ 0.33). Compared with the perturbation phases, the BF's time of onset of maximum activities were earlier during the posterior 7

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Table 4 Mean activity of the knee muscles during posterior, lateral, rotational, and combination perturbations at flexed-knee (30°) and straight-knee conditions during-perturbations and post-perturbations. Muscle

Knee condition

Perturbation direction

During-perturbation (SD)

Post-perturbation (SD)

VL

Flexed

Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination

7.4 (3.0) 7.8 (3.0) 7.2 (2.9) 6.4 (0.9) 2.9 (0.9)a,b,c,d 3.3 (1.1)a,b,c,d 4.1 (2.1)a,b,c,d 3.0 (0.9)a,b,c,d 7.7 (2.6) 8.6 (3.2) 7.8 (3.3) 8.0 (2.5) 2.7 (1.2)a,b,c,d 2.5 (0.9)a,b,c,d 2.9 (1.4)a,b,c,d 2.8 (1.2)a,b,c,d 2.3 (1.0) 2.3 (0.8) 2.0 (0.8) 2.2 (0.9) 1.5 (0.6)a,b 1.3 (0.5)a,b,d 1.4 (0.7)a,b,d 1.5 (0.5)a,b 2.4 (0.9) 2.8 (1.1) 2.8 (1.2) 2.6 (0.9) 3.4 (1.1) 2.8 (1.1) 2.7 (1.2) 2.9 (1.4) 5.2 (1.8) 6.5 (2.4) 4.7 (1.3) 5.9 (1.9) 7.4 (2.9)c 6.7 (2.5) 5.7 (2.2) 9.9 (4.8)a,b,c,d,e,f,g 5.0 (1.9) 7.9 (3.2)a 5.3 (1.9) 7.0 (2.1) 10.5 (4.6)a,c,d 14.4 (4.2)a,b,c,d,e 11.3 (4.2)a,b,c,d 14.1 (2.9)a,b,c,d,e

10.2 (4.3)⁎ 9.0 (3.8)⁎ 9.1 (3.2)⁎ 9.7 (2.2)⁎ 6.5 (2.8)a,d,⁎ 6.5 (2.9)a,⁎ 6.3 (2.9)a,b,c,d,⁎ 7.4 (3.9)a,⁎ 10.0 (4.3)⁎ 10.2 (3.7)⁎ 8.8 (3.6)⁎ 9.7 (3.2)⁎ 5.0 (2.1)a,b,c,d,⁎ 4.5 (1.9)a,b,c,d,⁎ 4.3 (1.7)a,b,c,d,⁎ 6.2 (2.5)a,c,⁎ 5.5 (2.9)⁎ 6.3 (3.4)⁎ 5.1 (1.9)b,⁎ 10.5 (4.5)a,b,c,⁎ 3.9 (1.9)b,d,⁎ 4.9 (1.8)d,⁎ 3.0 (1.1)a,b,d,⁎ 7.9 (3.0)a,c,d,e,f,g,⁎ 5.7 (2.5)⁎ 7.5 (2.4)⁎ 5.1 (2.7)b,⁎ 9.6 (2.6)a,c,⁎ 6.9 (2.9)d,⁎ 7.5 (3.2)c,⁎ 5.2 (1.8)b,d,f,⁎ 8.7 (3.3)a,c,e,g,⁎ 12.8 (4.8)⁎ 16.3 (5.3)⁎ 11.7 (3.8)b,⁎ 18.3 (8.9)a,c,⁎ 17.0 (7.1)c,⁎ 17.8 (5.9)a,c,⁎ 15.4 (5.3)⁎ 24.8 (6.4)a,b,c,d,e,f,g,⁎ 9.0 (3.6)⁎ 21.1 (9.0)a,⁎ 20.9 (8.6)a,⁎ 19.0 (6.8)a,⁎ 12.6 (4.7)b,c,⁎ 26.2 (6.4)a,e,⁎ 25.2 (9.5)a,e,⁎ 34.7 (12.5)a,b,c,d,e,f,g,⁎

Straight

VM

Flexed

Straight

BF

Flexed

Straight

ST

Flexed

Straight

LG

Flexed

Straight

MG

Flexed

Straight

VL: vastus lateralis; VM: vastus medialis; BF: biceps femoris; ST: semitendinosus; LG: lateral gastrocnemius; MG: medial gastrocnemius. Muscle activities are presented as a % of maximum voluntary isometric contraction. a Flexed-knee, lateral perturbation vs. other conditions (P < .05). b Flexed-knee, posterior perturbation vs. other conditions (P < .05). c Flexed-knee, rotational perturbation vs. other conditions (P < .05). d Flexed-knee, combination perturbation vs. other conditions (P < .05). e Straight-knee, lateral perturbations vs. other conditions (P < .05). f Straight-knee, posterior perturbation vs. other conditions (P < .05). g Straight-knee, rotational perturbation vs. other conditions (P < .05). ⁎ Significant differences between during-perturbation and post-perturbation phases.

and combination perturbations, and later during the rotational perturbations of the post-perturbations at the both knee conditions (P ≤ .001, effect size ≥ 0.69). The ST's time of onset of maximum activities were earlier during the lateral and rotational perturbations (50.2–59.5% of the phase) at the both knee conditions than those of other perturbation directions (after 76.6% of the perturbations duration, P ≤ .001, effect size ≥ 0.74) within the perturbation phase (Table 6). This pattern was reversed in the post-perturbation phase in which later 8

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Table 5 Maximum activity of the knee muscles during posterior, lateral, rotational, and combination perturbations at flexed-knee (30°) and straight-knee conditions during-perturbations and post-perturbations. Muscle

Knee condition

Perturbationdirection

During-perturbation (SD)

Post-perturbation (SD)

VL

Flexed

Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination

11.4 (3.4) 12.5 (3.9) 10.4 (3.7) 11.7 (3.1) 5.7 (1.8)a,b,c,d 7.4 (3.2)a,b,d 5.5 (2.6)a,b,c,d 7.1 (4.7)a,b,d 13.9 (4.3) 14.8 (5.8) 12.6 (4.6) 14.8 (5.7) 5.1 (2.0)a,b,c,d 4.9 (1.8)a,b,c,d 4.6 (1.8)a,b,c,d 6.8 (3.6)a,b,c,d 4.5 (1.7) 5.9 (1.6) 3.6 (1.4)b 8.9 (2.7)a,b,c 3.9 (1.7)b,d 3.2 (1.2)b,d 2.5 (1.1)a,b,d 8.9 (2.4)a,b,c,e,f,g 4.7 (1.6) 7.0 (2.3)a 4.4 (1.1)b 12.4 (3.7)a,b,c 6.9 (1.9)c,d 7.1 (2.9)c,d 4.5 (1.8)b,d 13.3 (3.3)a,b,c,e,f,g 13.9 (7.4) 22.0 (8.0)a 9.1 (3.5)b 24.9 (9.7)a,c 18.9 (7.9)a,c 21.8 (8.7)a,c 13.0 (6.8)b,d,f 29.8 (14.1)a,c,e,g 15.0 (6.4) 44.0 (9.7)a 12.8 (5.5)b 50.3 (18.2)a,c 24.1 (8.8)b,c,d 50.9 (11.3)a,c,e 22.2 (7.4)b,d,c,f 56.5 (10.4)a,b,c,e,g

17.9 (6.8)⁎ 16.8 (6.2)⁎ 18.1 (7.0)⁎ 17.5 (7.9)⁎ 11.5 (4.6)a,b,c,d,⁎ 11.4 (3.5)a,b,c,d,⁎ 14.0 (6.4)⁎ 14.3 (5.9)⁎ 17.6 (7.9)⁎ 14.0 (6.5) 16.9 (7.6)⁎ 15.9 (6.8) 8.5 (4.1)a,b,c,d,⁎ 7.8 (3.3)a,b,c,d,⁎ 9.2 (4.2)a,b,c,d,⁎ 10.9 (4.4)a,c,d,⁎ 10.2 (4.4)⁎ 11.8 (5.5)⁎ 13.5 (5.1)⁎ 21.6 (9.4)a,b,c,⁎ 9.1 (4.3)d,⁎ 12.1 (5.5)d,⁎ 11.4 (5.1)d,⁎ 20.9 (9.1)a,b,c,e,f,g,⁎ 12.3 (4.8)⁎ 15.5 (5.9)⁎ 16.9 (6.9)⁎ 22.4 (8.7)a,b,c,⁎ 14.4 (6.4)d,⁎ 17.3 (4.1)⁎ 17.7 (6.0)⁎ 23.8 (9.3)a,b,c,e,f,g,⁎ 25.5 (9.8)⁎ 32.3 (10.8)⁎ 30.1 (10.4)⁎ 37.1 (8.6)a,⁎ 28.9 (11.5)⁎ 34.0 (11.7)⁎ 41.2 (17.4)a,b,c,e,⁎ 50.0 (15.3)a,b,c,d,e,f,⁎ 21.6 (7.4)⁎ 54.5 (17.0)a,⁎ 57.3 (16.3)a,⁎ 58.3 (17.2)a,⁎ 27.2 (10.2)b,c,d 57.6 (17.3)a,e 65.9 (14.5)a,b,e,⁎ 68.2 (18.1)a,b,e,⁎

Straight

VM

Flexed

Straight

BF

Flexed

Straight

ST

Flexed

Straight

LG

Flexed

Straight

MG

Flexed

Straight

VL: vastus lateralis; VM: vastus medialis; BF: biceps femoris; ST: semitendinosus; LG: lateral gastrocnemius; MG: medial gastrocnemius. Muscle activities are presented as a % of maximum voluntary isometric contraction. a Flexed-knee, lateral perturbation vs. other conditions (P < .05). b Flexed-knee, posterior perturbation vs. other conditions (P < .05). c Flexed-knee, rotational perturbation vs. other conditions (P < .05). d Flexed-knee, combination perturbation vs. other conditions (P < .05). e Straight-knee, lateral perturbations vs. other conditions (P < .05). f Straight-knee, posterior perturbation vs. other conditions (P < .05). g Straight-knee, rotational perturbation vs. other conditions (P < .05). ⁎ Significant differences between during-perturbation and post-perturbation phases.

time of onset of the maximum muscle activities were observed during the lateral and rotational perturbations (55.9–85.2% of the phase) compared with the other perturbations (P ≤ .003, effect size ≥ 0.72). In comparison with the perturbation phase, the onset of maximum muscle activity amplitudes were earlier during the posterior and combination perturbations, and later during the rotational perturbations at the both knee conditions of the post-perturbations (P ≤ .006, effect size ≥ 0.62). Within the perturbation phase, the time of onset of the LG and MG muscles' maximum activities were earlier during the lateral and 9

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Table 6 Time of onset of the maximum muscle activity amplitudes at flexed-knee (30°) and straight-knee conditions during-perturbations and post-perturbations. Muscle

Knee condition

Perturbation direction

During-perturbation (SD)

Post-perturbation (SD)

VL

Flexed

Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination Lateral Posterior Rotational Combination

47.2 58.2 56.5 70.9 59.3 81.2 51.1 81.4 53.1 56.0 53.7 58.4 56.3 66.6 59.6 76.8 64.0 65.5 55.9 78.9 61.1 75.1 54.4 94.1 59.5 76.6 56.1 88.0 59.0 76.8 50.2 92.5 59.6 89.9 57.1 90.7 71.8 89.0 52.7 93.9 52.5 92.7 56.3 95.4 38.3 89.7 49.5 95.1

56.6 43.9 82.5 39.2 53.3 43.8 87.5 48.3 47.7 57.1 76.9 39.5 55.9 49.9 87.1 39.2 58.3 38.7 82.7 39.0 50.5 48.5 86.9 42.7 59.9 40.6 83.6 32.4 55.9 41.1 85.2 37.8 61.8 26.8 76.9 58.2 64.1 36.6 82.9 39.8 62.3 21.4 82.1 32.1 58.3 24.7 80.1 26.9

Straight

VM

Flexed

Straight

BF

Flexed

Straight

ST

Flexed

Straight

LG

Flexed

Straight

MG

Flexed

Straight

(32.9) (38.0) (22.1) (31.1)a (22.3) (25.1)a,b,c,e (29.2)d,f (36.4)a,b,c,e,g (33.1) (31.1) (27.5) (33.9) (32.3) (35.2) (30.3) (32.1)a,b,c,d,e,f,g (33.6) (35.9) (29.5) (30.5)c (36.5) (31.6) (28.9)d,f (15.0)a,b,c,e,g (33.6) (32.3) (32.8)b (25.4)a,c (30.9)d (31.1)c (33.8)b,d,f (19.6)a,c,e,g (38.0) (24.2)a (30.3)b (23.2)a,c (32.2)b,d (22.8)a,c (31.8)b,d,e,f (13.9)a,c,e,g (33.3) (20.1)a (30.0)b (15.7)a,c (25.6)b,c,d (24.9)a,c,e (31.5)b,d,f (11.8)a,c,e,g

(22.8) (33.4)⁎ (16.8)a,b,⁎ (35.5)c,⁎ (19.7)c (29.9)c,⁎ (14.9)a,b,d,e,f,⁎ (31.9)c,g,⁎ (27.3) (33.3) (24.1)a,b,⁎ (37.6)c,⁎ (26.4)c (29.7)c,⁎ (16.6)a,b,d,e,f,⁎ (35.5)c,g,⁎ (24.1) (26.3)a,⁎ (19.4)a,b,⁎ (26.6)a,c,⁎ (23.9)c (27.2)c,⁎ (17.8)a,b,d,e,f,⁎ (31.4)c,g,⁎ (23.2) (28.2)a,⁎ (18.1)a,b,⁎ (25.3)a,c,⁎ (26.1)b,c,d (27.1)a,c,⁎ (13.9)a,b,d,e,f,⁎ (29.8)a,c,e,f,⁎ (29.3) (27.7)a,⁎ (19.2)b,⁎ (35.3)b,⁎ (31.0)b,⁎ (30.2)a,c,e,⁎ (15.7)a,b,d,e,f,⁎ (36.7)a,c,e,g,⁎ (26.8) (21.4)a,⁎ (11.2)a,b,⁎ (36.4)a,c,⁎ (29.3)b,c,d,⁎ (25.8)a,c,e,⁎ (14.9)a,b,d,e,f,⁎ (29.7)a,c,e,g,⁎

VL: vastus lateralis; VM: vastus medialis; BF: biceps femoris; ST: semitendinosus; LG: lateral gastrocnemius; MG: medial gastrocnemius. All time are presented as a % of perturbation and post-perturbation durations. a Flexed-knee, lateral perturbation vs. other conditions (P < .05). b Flexed-knee, posterior perturbation vs. other conditions (P < .05). c Flexed-knee, rotational perturbation vs. other conditions (P < .05). d Flexed-knee, combination perturbation vs. other conditions (P < .05). e Straight-knee, lateral perturbations vs. other conditions (P < .05). f Straight-knee, posterior perturbation vs. other conditions (P < .05). g Straight-knee, rotational perturbation vs. other conditions (P < .05). ⁎ Significant differences between during-perturbation and post-perturbation phases.

rotational perturbations (38.3–71.8% of the phase) than those of other perturbations (89.0–95.4% of that phase) at the both knee conditions (P ≤ .001, effect size ≥ 0.77), as presented in Table 6. However, in the post-perturbation phase later time of onset of the peak muscle activities were observed during the lateral and rotational perturbations (58.3–82.9% of the phase) compared with the other perturbations (P ≤ .023, effect size ≥ 0.24). Compared with the perturbation phases, the onset of maximum muscle activity amplitudes were earlier during the posterior and combination perturbations, and later during the lateral (except for the flexed-knee 10

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condition) and rotational perturbations of the post-perturbations at the both knee conditions (P ≤ .005, effect size ≥ 0.55). 4. Discussion The purpose of this study was to investigate the knee joint kinematic and neuromuscular responses of the weight-bearing lower limb during-perturbations and post-perturbations in various directions, and in 30° of flexed-knee and straight-knee conditions. Since knee flexion angle influences the joint muscle activity and stability (Wilk et al., 1996), its motion patterns and neuromuscular changes in response to external perturbations, as knee is moving from full-extension to flexion, need to be identified. Given that in knee flexion angles ≤30° knee is less stable owing to the limited effectiveness of the hamstrings (Hirokawa, Solomonow, Luo, & D'Ambrosia, 1991), these information are important to understand the dynamic stability and injury mechanisms of the knee in moderate flexion angles. Overall, our results revealed significant differences in the 3D kinematic adaptations of the knee joint as well as the neuromuscular responses of its muscles during- and post-perturbations in different directions and knee conditions. As our participants were healthy females, it is likely that these responses occurred to augment knee joint stability, and balance control in general, during various perturbations. While the significant differences in the knee flexion angles between the two knee conditions were linked to the initial position of the joint prior to the perturbations (flexed- and straight-knee), these angles, along with the timing of the maximum angles (% perturbation), were similar during various perturbations within each specific knee condition. Even though the knee flexion angles were not affected by the direction of the perturbations in each knee condition, the knee initial flexion position could be a determinant to its behavior in the frontal and transverse planes. For instance, McLean, Neal, Myers, and Walters (1999) found up to 10° of external tibial rotation and knee abduction during the stance phase of a side-step maneuver (which is similar to a lateral perturbation) when the knee flexion ranged from 18 to 35°. Therefore, the knee joint kinematic adaptions during various perturbations could be better understood, if its initial position in the sagittal plane is taken into account. This has also functional relevance for exercise training settings using instability devices, in which the feet are instable and a bottom-up perturbation is generated. Such a bottom-up perturbations increase knee flexion angle during training (Narin, Sutherland, & Drake, 2017), which in turn, could change the knee coupling motions in the frontal and horizontal planes of motion. However, the significant reduction of knee flexion angles during post-perturbations in comparison with those of perturbation phases at flexed-knee condition in this study, indicated that a “predetermined” knee flexion angle at the initiation of perturbations would change throughout the course of perturbations and postperturbations. Accordingly, the coupling motions of tibia with respect to the femur in the frontal and transverse planes would be modified. The maximum timing of the knee flexions at the flexed-knee condition occurred before 50% and 20% of the perturbations duration during-perturbations and post-perturbations, respectively, while it happened considerably later during the straight-knee perturbations (after 63.5% during-perturbations and 38.0% of the post-perturbation phases). Presumably, in flexed-knee condition, the flexion motion reached its peak quickly to facilitate the knee motions in the frontal and transverse planes. During-perturbations in the lateral direction the knee was abducted in the both knee conditions, owing to the lateral quick movement of the foot and leg with respect to the femur. The greater tibial abduction at the flexed-knee condition (4.2°), compared with the straight-knee (0.3°), could be related to accompanying abduction and knee flexion motions (Patel et al., 2004; Saari, Carlsson, Karlsson, & Karrholm, 2005). In addition, the tibia was internally rotated with respect to the femur (≥4.4°) during- and post-perturbations in lateral direction at the flexed-knee condition. The combination of tibial internal rotation and knee abduction is a kinematic pattern associated with the pivot shift clinical test to assess the ACL strain/integrity (Kanamori et al., 2000). Slight flexion of the knee (≈30°) accompanied by internal tibial rotation and knee abduction together during sport activities is a serious risk factor leading to knee destabilization and ACL rupture (Boden, Dean, Feagin Jr, & Garrett Jr., 2000; DeMorat, Weinhold, Blackburn, Chudik, & Garrett, 2004; Krosshaug et al., 2007; Silvers & Mandelbaum, 2011). Moreover, our observed consistent pattern during straight-knee lateral perturbation that included knee abduction while the joint was close to full extension combined with external tibial rotation, has been suggested as the ACL injury mechanism in female athletes (Olsen, Myklebust, Engebretsen, & Bahr, 2004). Conversely, the tibia adduction excursions with respect to the femur during the both phases of posterior, rotational, and combination perturbations at the flexed- and straight-knee conditions could be considered a beneficial kinematic response to increase the knee dynamic stability through reducing the strain of the knee joint soft tissues. Furthermore, the external rotation of the tibia accompanied with the knee adduction during these three perturbations at the straight-knee condition could potentially minimize the ACL strain. A study to assess the ACL stain during these knee excursions is warranted to verify this interpretation. The maximum knee joint angles during-perturbations in lateral direction occurred earlier (prior to 30% of the phase) in the frontal plane, and later in the transverse plane (after 76% of the phase) compared with the other perturbation directions. These findings could generally indicate that the temporal aspects of the knee joint kinematic adaptations during posterior, rotational, and combination perturbations are more consistent than those of the lateral perturbations, regardless of the knee condition (flexed-knee vs straight-knee). Therefore, the perturbation direction is a crucial variable which induces a distinct kinematic response of the knee joint. The results of this study showed that the muscular activity of the selected quadriceps, hamstring, and gastrocnemius muscles were significantly different during-perturbations and post-perturbations in different knee conditions and directions. While the mean and maximum muscle activity values of VL and VM were comparable during the multi-directional perturbations within each specific knee condition, they were by far higher at the flexed-knee condition. This indicates that the activity levels of VL and VM are more a function of knee initial position than the perturbation directions. Since contraction of the quadriceps increases ACL strain between 15° and 30° of knee flexion (Beynnon et al., 1995; Beynnon et al., 1997), the greater activity of VL and VM is suspected as a contributing neuromuscular risk factor for ACL injury during the multi-directional perturbations in the bent knee position. These 11

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higher VL and VM muscular activities when accompanied by a knee abduction position and tibia internal rotation may cause impingement of the ACL on the femoral condyle; a possible mechanism of ACL rupture (Ebstrup & Bojsen-Moller, 2000; Olsen et al., 2004). The time of onset of peak VL and VM activities were related to both perturbation directions and knee conditions. In general, these muscles reached to their maximum activities significantly later during posterior and combination perturbations within the perturbation phase, and earlier during post-perturbations, more often at the straight-knee condition. This neuromuscular response could reflect the lesser contributions of VL and VM to dynamic stability of the knee during the perturbation phase while the perturbation direction does not elongate them (i.e., posterior perturbation) or different knee muscles contract simultaneously (i.e., combination perturbation), whereas they respond quickly to recover knee stability after the perturbations are completed. This assumption needs to be addressed in future research, perhaps retrospectively. Greater mean and maximum muscle activity values were observed for BF during all perturbations at flexed-knee condition compared with the straight-knee perturbations in the both perturbation phases, while its maximum activities were considerably greater during combination perturbations during the both knee conditions, more specifically in post-perturbation phase. In addition, BF and ST muscles showed substantially less muscular activity than VL and VM during all perturbations at the flexed-knee condition within the perturbation phase. Thus, BF and ST might not be able to effectively limit the anterior tibial translation during multidirectional perturbations at flexed-knee condition. This finding is in agreement with cadaveric studies that have demonstrated the ineffectiveness of the hamstrings in limiting anterior and rotary tibial translation while the knee is flexed 15–30° (Renstrom et al., 1986; Wilk et al., 1996). Simonsen et al. (2000) reported that elite female handball players during side-cutting movements (i.e., similar to the lateral and combination perturbations in this study) with maximal hamstrings' contraction were not able to reduce the forces on the ACL. Colby et al. (2000) found the same results during deceleration motion (i.e., eccentric motion) associated with sidestep cutting, cross-cutting, stopping, and landing in healthy collegiate and recreational athletes. This low level of hamstrings activity and low knee flexion angle during deceleration, coupled with relatively high level of quadriceps activity could produce significant anterior tibial motion, contributing to ACL injury (Colby et al., 2000). However, the active tensions of BF and ST muscles were considerably increased during post-perturbation phase (2 to more than 5 times compared with those of during-perturbation phase). That indicates a delay in the contribution of the hamstrings to the knee stability. Furthermore, the time of onset of maximum activities of BF and ST muscles showed that ST is possibly more involved in the knee stability than BF during the perturbation phases at the both knee conditions. While they reached to their peak activity earlier during rotational perturbations (prior to 56.2% of the phase), and later during combination perturbations (after 78.8% of the phase) within the perturbation phase, the time of onset of maximum activity of ST was earlier during the lateral perturbations (prior to 59.6% of the perturbations duration), as well. This quicker and more consistent response of ST could be considered as a preventive strategy to minimize the knee abduction motion during-perturbations in the lateral direction in healthy athletes. In post-perturbation phases, while the time of onset of peak activity of these muscles were later during rotational perturbations (after 82.7% of the phase) and earlier during posterior and combination perturbations (prior to 48.5% of the phase), the earlier time of onset of ST's maximum activity during the combination perturbations might indicate its faster adaptations to the post-perturbations. Therefore, it seems ST is contributing to the knee joint stability during the both phases of the multi-directional perturbations more than BF muscle. Mean and maximum activity values of LG and MG muscles were significantly greater during all the perturbations at straight-knee condition compared with the flexed-knee perturbations during- and post-perturbations. Since the foot was stationary on the perturbation platform surface during the perturbations (i.e., closed kinetic chain), the LG and MG would likely have a strong posterior pull in the femur, specifically at the straight-knee condition. Therefore, the participants were able to stand upright with the minimal contraction of VL and VM muscles during straight-knee perturbations, as illustrated in Fig. 2. While the reduced quadriceps muscle activity could be considered as a compensator mechanism for decreasing tibial anterior translation (i.e., less ACL strain), the increased gastrocnemius muscle activity secured the knee stability during straight-knee perturbations at the both perturbation phases. In addition, tension reduction of the VL, VM, BF, and ST muscles during straight-knee perturbations could be postulated as a

Quadriceps - Gastrocnemius Activities during Perturbations 30

(% MVIC)

25 20 15 10 5 0 Lateral

Posterior

Rotational Combination

Lateral

Flexed Knee

Posterior

Rotational Combination

Straight Knee

VL+VM

LG+MG

Fig. 2. Net muscle activation of vastus lateralis and vastus medialis (VL + VM), and lateral gastrocnemius and medial gastrocnemius (LG + MD) muscles during-perturbations at the both knee conditions and different perturbations. 12

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preventive neuromuscular strategy against the higher activity levels of LG and MG muscles, which in turn might lead to a reduction of the cumulative load on the knee. This hypothesis, however, needs to be tested by comparing the muscular activities between healthy and pathologic populations (e.g., athletes with reconstructed ACL and osteoarthritis patients). The time of onset of maximum activity of LG and MG were generally earlier during the lateral and rotational perturbations (prior to 71.8% of the perturbations duration) compared with the posterior and combination perturbations (after 89.0% of the perturbations duration) at the both knee conditions. Arguably, to overcome the destabilization of the knee joint during the lateral and rotational perturbations, faster responses of the gastrocnemius muscle is required. The reverse trend in the time of onset of maximum activity of these muscles during post-perturbations (i.e. later peak muscle activity occurrences during the lateral and rotational perturbations) might demonstrate a neuromuscular adaptation in which the gastrocnemius muscles' active tension is prolonged to enhance the dynamic stability of the knee joint during lateral and rotational perturbations. Compared with the muscular activities during perturbation phases, the mean and maximum activities of the lower extremity muscles were significantly greater during post-perturbations. This is in agreement with the findings of previous research that showed late reflex responses to compensate for unpredicted perturbations to recover body equilibrium (Ritzmann, Lee, Krause, Gollhofer, & Freyler, 2018). Generally, the time of onset of maximum amplitudes of the muscles followed a similar trend during-perturbations and post-perturbations; earlier time of peak occurrence during-perturbation phase in lateral and rotational perturbations, and later time of peak occurrence during post-perturbation phase in lateral and rotational perturbations. For the posterior and combination perturbations, the onset of maximum muscle activities happened later during-perturbations, and earlier in post-perturbations. Though a greater lower extremity muscular activity is needed to maintain the knee joint stability during multi-directional perturbations, the lateral and rotational perturbations seem to be more demanding as a faster muscular response was observed. This indicates that the perturbation direction is an important variable which induces an individual neuromuscular response. This study provides insight into the knee joint's kinematic and neuromuscular responses during multi-directional perturbations at flexed- and straight-knee conditions. However, a few limitations of the study remain. The non-sagittal planes knee kinematic data calculated using Plug-in-Gait model need to be interpreted with caution. Poor consistency was found in the knee abduction/adduction obtained from this model in comparison with four well-known methods during swing-phase of walking (Ferrari et al., 2008). Compared with a dynamic stereo radiography system, Li, Zheng, Tashman, and Zhang (2012) reported Plug-in-Gait model gave mean RMS differences of 2° and 6.4° for the abduction/adduction and internal/external rotation of the tibiofemoral kinematics, respectively, during running. These inaccuracies might be owing to incorrect identification of anatomical landmarks, which in turn would lead to interpreting knee flexion as abduction (crosstalk) (Benedetti et al., 2017). In this study experienced personnel performed the markers placement, the knee angles during static posture were used to verify the anatomical calibration, the lower extremity was in quiet standing during perturbations, and the knee flexion was limited to 30° (compared with about 45° to 90° flexion during walking and running). Thus, it can be assumed that the frontal and transverse planes knee angles were less prone to inaccuracies than previously reported. To verify the consistency of our data, the knee angles in the sagittal, frontal, and transverse planes during combination perturbations at the both knee conditions were plotted (Fig. 3). Another limitation is related to the absence of kinetic analysis of the knee during perturbations. In order to fully understand the mechanisms of knee stability and injury during multidirectional perturbations, shear forces, compressive forces and the 3D moments of force of the joint should be quantified. Furthermore, the co-activation of the quadriceps, hamstrings, and gastrocnemius muscles should be determined in future studies.

5. Conclusion The knee kinematic adaptations and neuromuscular responses suggest that compared to straight-knee condition, the multi-directional perturbations at 30° knee flexion could reduce the dynamic stability of the knee joint and potentially increase the risk of knee injuries. Knee abduction accompanied with internal/external rotations observed during the lateral perturbations in both flexedand straight-knee conditions may increase the joint soft tissue strain. Furthermore, the higher activities of quadriceps in comparison

Fig. 3. The weight-bearing knee angles in sagittal, frontal, and transverse planes during combination perturbations at the flexed (mean, solid blue line; SD, gray line) and straight (mean, dotted red line; SD, gray line) knee conditions. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) 13

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with the hamstrings, more specifically during the flexed-knee perturbations, may contribute to destabilization of the knee in young healthy female athletes. The gastrocnemius muscles seem to be the main stabilizers of the knee during perturbation phases at the straight-knee condition. Compared with the posterior and combination perturbations, a faster lower extremity muscular activity is needed to enhance the knee stability during lateral and rotational perturbations. Declaration of competing interest None. References Allum, J. H. J., Huwiler, M., & Honegger, F. (1996). Prior intention to mimic a balance disorder: Does central set influence normal balance-correcting responses. Gait & Posture, 4, 39–51. Andrews, J., Mcleod, W. D., Ward, T., & Howard, K. (1977). The cutting mechanism. American Orthopaedic Society for Sports Medicine, 5(3), 111–121. Benedetti, M. G., Beghi, E., De Tanti, A., Cappozzo, A., Basaglia, N., Cutti, A. G., ... Ferrarin, M. (2017). 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