Original Research
Lower Extremity Muscle Activation During Functional Exercises in Patients With and Without Chronic Ankle Instability Mark A. Feger, MEd, Luke Donovan, MEd, Joseph M. Hart, PhD, Jay Hertel, PhD Objective: To determine whether individuals with chronic ankle instability (CAI) exhibit altered neuromuscular control as demonstrated by surface electromyography (EMG) amplitudes compared with healthy controls during single-limb eyes-closed balance, Star Excursion Balance Test, forward lunge, and lateral hop exercises. Design: A cross-sectional laboratory study. Setting: A research laboratory. Participants: Fifteen young adults with CAI and 15 healthy controls. Interventions: The subjects performed functional exercises while surface EMG signals were recorded from the tibialis anterior, peroneus longus, lateral gastrocnemius, rectus femoris, biceps femoris, and gluteus medius. Main Outcome Measurements: Surface EMG amplitudes (root mean square area) for each muscle, muscles of the shank (distal 3 muscles), muscles of the thigh (proximal 3 muscles), and total muscle activity (all 6 muscles) of the lower extremity were analyzed and compared between the groups. Results: Individuals with CAI demonstrated significantly less EMG activity in the muscles of the lower extremity during all 4 functional exercises. Effect sizes for significant differences between groups ranged from 0.75 to 1.08, none of which had 95% confidence intervals that crossed zero, which indicates moderate to large decreases in muscle activity in patients with CAI compared with healthy controls. Conclusions: Patients with CAI demonstrated decreased muscle activity of ankle, knee, and hip musculature during common functional rehabilitative tasks. Clinicians may benefit from implementing functional exercises for patients with CAI that target both distal and proximal muscles of the lower extremity. PM R 2014;-:1-10
INTRODUCTION Ankle sprains account for 15%-23% of athletic injuries in the high school and collegiate settings [1,2]. Furthermore, ankle sprains are the most common site for recurrent injury and account for 25% of all recurrent injuries [3], and recurrent ankle sprains account for 15% of all ankle sprains [4]. Recurrent ankle sprains are often associated with residual symptoms such as pain, subjective instability, and decreased self-reported function [5,6]. A recent position statement indicates that a history of at least 1 significant ankle sprain, a subsequent history of the ankle “giving way,” and self-reported functional limitations are defining characteristics of a heterogeneous condition known as chronic ankle instability (CAI) [7]. Sensory, reflexive, and motor control deficits may contribute to CAI [8]. Visual inspection of motor control patterns in patients with CAI is difficult in practice; however, adaptations have been reported with laboratory measures. Patients with CAI have demonstrated altered motor control indicated by surface EMG (sEMG) during walking and drop landing [9-11]. During walking, patients with CAI activate their peroneus longus (PL) before initial contact (IC), whereas healthy controls do so after IC [9,10]. An opposite relationship exists during drop landing, in which patients with CAI have less anticipatory muscle activity compared with healthy individuals [12]. Altered motor control patterns also PM&R 1934-1482/13/$36.00 Printed in U.S.A.
M.A.F. Department of Kinesiology, 210 Emmet Street South Charlottesville, VA 22904. Address correspondence to M.A.F.; e-mail: [email protected] Disclosure: nothing to disclose L.D. Department of Kinesiology, University of Virginia, Charlottesville, VA Disclosure: nothing to disclose J.M.H. Department of Kinesiology, University of Virginia, Charlottesville, VA Disclosure: nothing to disclose J.H. Department of Kinesiology, University of Virginia, Charlottesville, VA Disclosure: nothing to disclose Submitted for publication August 26, 2013; accepted December 22, 2013.
ª 2014 by the American Academy of Physical Medicine and Rehabilitation Vol. -, 1-10, --- 2014 http://dx.doi.org/10.1016/j.pmrj.2013.12.013
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have been identified in proximal joint muscles, including decreased gluteus maximus muscle activity during a rotational squat exercise in patients with CAI [13]. During the transition from a bipedal to a unipedal stance, a slower onset of muscle activity and less anticipatory muscle activation in the ankle, knee, and hip muscles were seen in patients with CAI, which indicates a reliance on feedback, rather than feedforward, motor control to complete the postural transition [14]. Balance and coordination training are effective intervention strategies for reducing the risk of ankle sprains, especially in patients who have a history of ankle sprain but who have not developed CAI [15], but the efficacy of such exercises at reducing the risk of recurrent sprains in patients with CAI is uncertain [15]. Altered motor control patterns have been identified in muscles that act on the ankle, knee, and hip during gait [9-11] and isolated functional exercises [12-14,16] in patients with CAI; however, there has not previously been a comprehensive analysis of the EMG activity of both distal and proximal lower extremity muscles during common functional exercises used for rehabilitation in patients with CAI. An understanding of how patients with CAI activate muscles to complete functional rehabilitative exercises can give insight into how rehabilitation can be tailored to specifically target and improve patient outcomes. Our purpose was to compare the sEMG root mean square (RMS) area during common functional exercises, including lunges, single limb balance, the Star Excursion Balance Test (SEBT), and lateral hopping exercises to test the hypothesis that patients with CAI would have decreased sEMG amplitudes of ankle, knee, and hip musculature during all tasks compared with healthy counterparts.
METHODS
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Table 1. Subject demographics
Mean SD age, y Mean SD height, cm Mean SD mass, kg Men:women No. previous sprains, mean SD Mean SD time since last sprain, mo Godin score, mean SD FAAM ADL, mean SD FAAM Sport, mean SD
CAI Group
Control Group
23 4.2 173 10.8 72.4 14 5:10 4.5 3.2 15.2 9.3
22.9 3.4 173 9.4 70.8 18 5:10 N/A N/A
94 47 87.2 7.1 68.5 5.7
84 40 100 0 100 0
CAI ¼ chronic ankle instability; SD ¼ standard deviation; N/A ¼ not applicable; Godin score ¼ Godin Leisure-Time Exercise Questionnaire score; FAAM ADL ¼ Foot and Ankle Ability Measure Activities of Daily Living scale score; FAAM Sport ¼ Foot and Ankle Ability Measure Sport subscale score.
and the same cohorts have previously been reported in another article that investigated EMG differences during gait [9]. Briefly, the control group was self-reported to be healthy and to have no history of ankle sprain to either ankle. The CAI group had a history of more than 1 ankle sprain with the initial sprain occurring more than 1 year before the study onset and current self-reported functional deficits due to ankle symptoms. The subjects were allocated to groups based on their ankle health status (CAI or healthy), and healthy test limbs were side matched (right or left) to the involved CAI test limbs [9]. Subjects were excluded if they had an ankle sprain within the 6 weeks before the study onset, a history of lower extremity injury or surgery, balance disorders, neuropathies, diabetes, or other conditions known to affect balance. The subjects provided informed consent, and the study was approved by the university’s institutional review board.
Design We performed a cross-sectional laboratory study in which the independent variable was the group (CAI, healthy control) and the dependent variables were sEMG RMS area for the tibialis anterior (TA), PL, lateral gastrocnemius, rectus femoris (RF), biceps femoris, and gluteus medius during single-limb eyes-closed balance, SEBT reach directions (anterior, posterior medial, and posterior lateral), forward lunges, and lateral hops. We also summed the normalized sEMG amplitudes for individual muscles to analyze segmental muscle activity for the distal musculature (TA, PL, lateral gastrocnemius), proximal musculature (RF, biceps femoris, gluteus medius), and total lower extremity musculature (all 6 muscles) between groups.
Subjects Fifteen young adults with CAI and 15 healthy controls volunteered (Table 1). This study was part of a larger study,
Instruments The sEMG signals were collected from disposable, pregelled, 10-mm, round Silver-Silver Chloride (Ag-AgCl) electrodes and amplified with a high-gain, differential-input biopotential amplifier with a gain of 1000 and digitized with a 16-bit data acquisition system (MP 150, Biopac Systems Inc, Goleta, CA) at 2000 Hz with a common-mode rejection ratio of 110 dB, an input impedance of 1.0 MU, and a noise voltage of 0.2 mV. Acqknowledge software (v.4.0, Cambridge, England) was used for data collection and processing of EMG signals. The EMG data were collected by using real-time processing with a 10- to 500Hz band pass filter and a 10-sample moving average RMS algorithm. A foot switch (BIOPAC Systems, Santa Barbara, CA) was used to identify ground contact during the SEBT, forward lunge, and lateral hopping exercises. All the subjects wore standard athletic shoes for all exercises (X755WB; New Balance, Brighton, MA).
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Testing Procedures By using methods previously described in detail [9], surface electrodes were placed 2 cm apart and oriented parallel to the muscle-fiber orientation over the midline of the muscle belly determined via manual palpation during a voluntary contraction. Before testing, the subjects performed a 5minute warm-up that consisted of walking at a self-selected pace, and then standardized maximal voluntary isometric contractions (MVIC) were recorded for each muscle against manual resistance for normalization of sEMG amplitudes.
Exercises The subjects completed at least 3 practice trials for each exercise before testing and additional practice trials until they self-reported to be comfortable with each task; however, no subject required more than 5 practice trials per task. For all tasks, failed trials were repeated until the desired number of repetitions was completed. Due to the submaximal nature of the tasks and the low volume of each exercise performed, we did not expect fatigue to affect our outcome measures. Thus, all the subjects completed the tasks in the order described below. Five consecutive lunges were performed and the lead leg was tested. A target line was placed to signal the appropriate heel strike position at a distance determined during practice trials. The target distance was selected to ensure that the test limb reached 90 of hip and knee flexion when the knee of the contralateral stance limb lightly contacted the ground [17]. The subjects were visually monitored and required to keep their hands on their hips, and failed trials included removing hands from the hips or missing the target line during heel strike. A single-limb eyes-closed balance trial was performed for 15 seconds with the stance limb tested. The subjects were required to place their hands on their hips with the contralateral limb comfortably elevated and not in contact with stance limb [18]. The SEBT was performed in the anterior, posteromedial, and posterolateral reach directions by using previously described methods (Figure 1A-C) [19]. Traditionally, the SEBT has been used as a functional assessment for dynamic balance deficits; however, Donovan and Hertel [20] highlighted the benefit of implementing the SEBT as a functional rehabilitation exercise in patients with CAI. Lateral hops were performed with the hopping limb tested. A modified side hop test was performed [21]. The subjects hopped laterally over a 1.5-inch line at a pace of 110 hops per minute for 20 seconds. A metronome was used to set the cadence. A foot switch was used to signal ground contact.
Data Processing Forward Lunge. The middle 3 lunges of the 5 consecutive lunge trials were analyzed. To gain an understanding of
Figure 1. (A) Star Excursion Balance Test, anterior reach. (B) Star Excursion Balance Test, posteromedial reach. (C) Star Excursion Balance Test, posterolateral reach.
preparatory muscle activation and reflexive activation of all muscles [22], a 50-millisecond epoch immediately before IC was used to calculate the pre-IC area under the RMS curve [22]. A 100-millisecond epoch immediately after IC was used to calculate the post-IC area under the RMS curve [22]. Lunge amplitudes were normalized to respective MVIC epochs. Single-limb Eyes-closed Balance. A 3-second epoch during the middle of the single-limb eyes-closed balance trial was analyzed. The area under the RMS curve was calculated and normalized to a 3-second MVIC epoch for each muscle. SEBT. A 500-millisecond epoch just before maximum excursion was averaged over 3 trials for each of the 3 directions. Maximum excursion was defined as the time at which the contralateral limb touched down. The average area under the RMS curve over the 3 trials was normalized to a 500millisecond MVIC epoch for each muscle. Lateral Hops. Six total consecutive hops (3 in each direction) were selected from the middle of the lateral hopping trial. To gain an understanding of preparatory and reflexive activation of all muscles, a 50-millisecond epoch immediately before IC was used to calculate the pre-IC area under the RMS curve [22]. A 100-millisecond epoch immediately
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Table 2. Muscle activation patterns with forward lunge Isolated Muscle Activation Muscles Anterior tibialis Pre-IC Post-IC Peroneus longus Pre-IC Post-IC Lateral gastrocnemius Pre-IC Post-IC Rectus femoris Pre-IC Post-IC Biceps femoris Pre-IC Post-IC Gluteus medius Pre-IC Post-IC
CAI, Mean ± SD
Control, Mean ± SD
ES (95% CI)*
Py
0.46 0.16 0.44 0.13
0.57 0.26 0.61 0.18
0.51 (1.24 to 0.22) 1.08 (1.85 to 0.32)
.21 .01
0.22 0.12 0.33 0.15
0.30 0.27 0.48 0.35
0.38 (1.11 to 0.34) 0.56 (1.29 to 0.17)
.33 .16
0.40 0.36 0.34 0.23
0.45 0.33 0.55 0.37
0.14 (0.86 to 0.57) 0.68 (1.42 to 0.05)
.67 .08
0.13 0.09 0.23 0.17
0.21 0.20 0.17 0.09
0.52 (1.24 to 0.21) 0.44 (0.28 to 1.17)
.21 .38
0.13 0.07 0.12 0.05
0.19 0.11 0.17 0.09
0.65 (1.39 to 0.08) 0.69 (1.42 to 0.05)
.14 .12
0.10 0.07 0.17 0.10
0.17 0.19 0.20 0.10
0.49 (1.22 to 0.24) 0.30 (1.02 to 0.42)
.18 .40
CAI ¼ chronic ankle instability; SD ¼ standard deviation; ES ¼ Cohen d effect size; CI ¼ confidence interval; Pre-IC ¼ 50ms pre-initial contact root mean square area; Post-IC ¼ 100ms post-initial contact root mean square area. *A negative ES indicates decreased muscle activity in the subjects with CAI; a positive ES indicates increased muscle activity in the subjects with CAI. y Independent t test statistical results; level of significance was set a priori at P .05.
after IC was used to calculate the post-IC area under the RMS curve [22]. Lateral hopping amplitudes were normalized to respective MVIC epochs. Distal, Proximal, and Total Muscle Activity. To gain a more comprehensive understanding of the EMG activity of the entire lower extremity during rehabilitative tasks, we summed the normalized muscle activity of the distal (TA, PL, and lateral gastrocnemius), proximal (RF, biceps femoris, and gluteus medius), and entire lower extremity (all 6 muscles). The summed values were analyzed as separate dependent variables for each task as described below.
Statistical Analysis The independent variable was group (CAI and healthy control), and the main outcome measures were sEMG
RMS areas for a predetermined epoch respective of each task for each individual muscle, the sum of the 3 distal muscles, the sum of the 3 proximal muscles, and the sum of all 6 muscles. We performed an independent t test for each dependent variable to compare the groups. The level of significance was set a priori at P .05 for all analyses. Per contemporary statistical recommendations [23], we did not control for multiple comparisons; instead, in addition to inferential statistical comparison, we calculated Cohen d effect sizes and associated 95% confidence intervals to estimate the magnitude and precision of group differences for each measure. Effect sizes were interpreted as 0.80, large; 0.50, moderate; and 0.20, small. Negative effect sizes indicated that CAI muscle activation was less than that of the control group. Positive effect sizes indicated that CAI muscle activation was greater than that of the control group. Data were analyzed by using the
Table 3. Muscle activation patterns with single-leg eyes-closed balance Isolated Muscle Activation Muscles Anterior tibialis Peroneus longus Lateral gastrocnemius Rectus femoris Biceps femoris Gluteus medius
CAI, Mean ± SD 0.35 0.45 0.25 0.09 0.07 0.16
0.18 0.22 0.11 0.10 0.07 0.11
Control, Mean ± SD 0.49 0.48 0.33 0.19 0.12 0.13
0.19 0.26 0.19 0.11 0.11 0.09
ES (95% CI)* 0.76 0.12 0.52 0.95 0.54 0.30
(1.5 to 0.02) (0.84 to 0.59) (1.24 to 0.21) (1.71 to 0.20) (1.27 to 0.19) (0.42 to 1.02)
Py .05 .74 .16 .02 .13 .55
CAI ¼ chronic ankle instability; SD ¼ standard deviation; ES ¼ Cohen d effect size; CI ¼ confidence interval. *A negative ES indicates decreased muscle activity in the subjects with CAI; a positive ES indicates increased muscle activity in the subjects with CAI. y Independent t test statistical results; level of significance was set a priori at P .05.
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Table 2. Continued Distal-Proximal Muscle Activation CAI, Mean ± SD Control, Mean ± SD
1.08 0.57 1.11 0.32
1.32 0.58 1.64 0.71
Total Muscle Activation P y CAI, Mean ± SD Control, Mean ± SD
ES (95% CI)*
0.56 0.32 0.67 0.37
Py
0.42 (1.14 to 0.31) .28 0.96 (1.72 to 0.21) .02 1.45 0.59 1.63 0.48
0.36 0.16 0.52 0.25
ES (95% CI)*
1.88 0.82 2.30 0.99
0.60 (1.33 to 0.13) .12 0.86 (1.61 to 0.11) .03
0.79 (1.53 to 0.05) .05 0.48 (1.20 to 0.25) .22
Statistical Package for the Social Sciences version 20.0 (SPSS Inc, Chicago, IL).
RESULTS
from 0.05 (small) to 1.85 (large), which indicated moderate-to-large decreases in muscle activity in the CAI group (Table 2).
Single-limb Eyes-closed Balance
Forward Lunges There was significantly less proximal muscle activation before IC in the CAI group compared with healthy controls (Table 2). There was significantly less muscle activation for the TA in the CAI group compared with the healthy controls for post-IC amplitude. In addition, there were significantly less distal and total lower extremity post-IC amplitudes in the CAI group compared with the healthy control group. Effect sizes for significant findings during forward lunges ranged from 0.79 (moderate) to 1.08 (large), with 95% confidence intervals that ranged
There was significantly less muscle activity in the CAI group when compared with healthy controls for the TA and RF sEMG amplitudes during single-limb eyes-closed balance. For total lower extremity muscle activation, the CAI group had a significantly lower sEMG amplitude compared with the healthy control group. Effect-size point estimates for the significant findings during single-limb eyes-closed balance ranged from 0.76 (moderate) to 0.95 (large), with 95% confidence intervals that ranged from 0.02 (small) to 1.71 (large), which indicated moderate-to-large decreases in muscle activity in the CAI group (Table 3).
Table 3. Continued Distal-Proximal Muscle Activation CAI, Mean ± SD Control, Mean ± SD
ES (95% CI)*
Total Muscle Activation P y CAI, Mean ± SD Control, Mean ± SD
1.05 0.36
1.31 0.43
0.66 (1.39 to 0.08) .10
0.32 0.17
0.45 0.24
0.63 (1.36 to 0.11) .11
1.37 0.42
1.75 0.56
ES (95% CI)*
Py
0.77 (1.51 to 0.03) .05
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Table 4. Muscle activation patterns with Star Excursion Balance Test Isolated Muscle Activation Muscles
CAI, Mean ± SD
Control, Mean ± SD
ES (95% CI)*
Py
Anterior Posteromedial Posterolateral
0.40 0.22 0.50 0.19 0.75 0.28
0.71 0.45 0.68 0.28 0.89 0.31
0.88 (1.62 to 0.13) 0.75 (1.49 to 0.01) 0.47 (1.20 to 0.25)
.03 .05 .22
Anterior Posteromedial Posterolateral
0.48 0.20 0.34 0.12 0.35 0.12
0.44 0.29 0.38 0.18 0.40 0.24
0.16 (0.56 to 0.88) 0.26 (0.98 to 0.46) 0.26 (0.98 to 0.46)
.66 .61 .48
Anterior Posteromedial Posterolateral
0.39 0.28 0.18 0.11 0.22 0.10
0.51 0.39 0.25 0.18 0.29 0.20
0.35 (1.07 to 0.37) 0.47 (1.19 to 0.26) 0.44 (1.17 to 0.28)
.34 .23 .23
Anterior Posteromedial Posterolateral
0.42 0.23 0.54 0.28 0.54 0.31
0.44 0.30 0.70 0.41 0.73 0.47
0.07 (0.79 to 0.64) 0.46 (1.18 to 0.27) 0.48 (1.20 to 0.25)
.83 .24 .22
Anterior Posteromedial Posterolateral
0.17 0.07 0.11 0.06 0.16 0.08
0.18 0.10 0.13 0.06 0.16 0.07
0.12 (0.83 to 0.60) 0.33 (1.05 to 0.39) 0 (0.72 to 0.72)
.66 .62 .89
Anterior Posteromedial Posterolateral
0.17 0.12 0.25 0.14 0.24 0.15
0.13 0.09 0.23 0.18 0.20 0.14
0.38 (0.34 to 1.10) 0.12 (0.59 to 0.84) 0.50 (1.23 to 0.22)
.31 .70 .52
Reach Direction
Anterior tibialis
Peroneus longus
Lateral gastrocnemius
Rectus femoris
Biceps femoris
Gluteus medius
CAI ¼ chronic ankle instability; SD ¼ standard deviation; ES ¼ Cohen d effect size; CI ¼ confidence interval. *A negative ES indicates decreased muscle activity in the subjects with CAI; a positive ES indicates increased muscle activity in the subjects with CAI. y Independent t test statistical results; level of significance was set a priori at P .05.
Table 5. Muscle activation patterns with lateral hop Isolated Muscle Activation Muscles Anterior tibialis Pre-IC Post-IC Peroneus longus Pre- IC Post-IC Lateral gastrocnemius Pre-IC Post-IC Rectus femoris Pre-IC Post-IC Biceps femoris Pre-IC Post-IC Gluteus medius Pre-IC Post-IC
ES (95% CI)*
Py
CAI, Mean ± SD
Control, Mean ± SD
0.24 0.16 0.35 0.26
0.34 0.17 0.54 0.31
0.61 (1.34-0.13) 0.66 (1.40 to 0.07)
.13 .10
0.50 0.17 0.67 0.19
0.70 0.46 0.88 0.52
0.58 (1.31 to 0.15) 0.54 (1.26 to 0.19)
.16 .19
0.83 0.55 1.21 1.23
1.39 0.86 1.61 1.06
0.78 (1.52 to 0.03) 0.35 (1.07 to 0.37)
.06 .38
0.28 0.38 0.62 0.47
0.30 0.21 0.77 0.40
0.07 (0.78 to 0.65) 0.34 (1.06 to 0.38)
.88 .41
0.38 0.20 0.31 0.26
0.49 0.30 0.32 0.15
0.43 (1.16 to 0.29) 0.05 (0.76 to 0.67)
.28 .96
0.35 0.20 0.60 0.26
0.56 0.44 0.69 0.43
0.61 (1.35 to 0.12) 0.25 (0.97 to 0.47)
.13 .53
CAI ¼ chronic ankle instability; SD ¼ standard deviation; ES ¼ Cohen d effect size; CI ¼ confidence interval; Pre-IC ¼ 50 ms pre-initial contact root mean square area; Post-IC ¼ 100 ms post-initial contact root mean square area. *A negative ES indicates decreased muscle activity in the subjects with CAI; a positive ES indicates increased muscle activity in the subjects with CAI. y Independent t test statistical results; level of significance was set a priori at P .05.
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Table 4. Continued Distal-Proximal Muscle Activation CAI, Mean ± SD Control, Mean ± SD
1.26 0.44 1.02 0.25 1.32 0.33
1.66 0.82 1.30 0.49 1.58 0.61
ES (95% CI)*
Total Muscle Activation P y CAI, Mean ± SD Control, Mean ± SD
0.75 0.37 1.06 0.49 1.09 0.56
Py
0.61 (1.34 to 1.10) .12 0.72 (1.46 to 0.02) .06 0.53 (1.26 to 0.20) .16 2.02 0.64 1.93 0.52 2.25 0.53
0.76 0.38 0.91 0.37 0.94 0.45
ES (95% CI)*
2.4 1.13 2.36 0.75 2.67 1.05
0.41 (1.14 to 0.31) .27 0.67 (1.40 to 0.07) .09 0.50 (1.23 to 0.22) .19
0.03 (0.69 to 0.74) .97 0.35 (1.07 to 0.38) .37 0.30 (1.01 to 0.42) .42
Table 5. Continued Distal-Proximal Muscle Activation CAI, Mean ± SD Control, Mean ± SD
1.57 0.68 2.22 1.31
2.43 1.12 3.03 1.22
ES (95% CI)*
Total Muscle Activation P
y
CAI, Mean ± SD Control, Mean ± SD
1.34 0.65 1.78 0.81
Py
0.93 (1.68 to 0.17) .03 0.64 (1.37 to 0.09) .12 2.57 0.99 3.76 1.62
1.00 0.51 1.54 0.78
ES (95% CI)*
0.58 (1.31 to 0.15) 0.30 (1.02 to 0.42)
.15 .45
3.77 1.61 4.81 1.86
0.90 (1.65 to 0.15) .03 0.60 (1.33 to 0.13) .14
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SEBT Results for the SEBT in the anterior, posteromedial, and posterolateral direction are summarized in Table 4. There was significantly less muscle activity in the CAI group during the SEBT in the TA during the anterior and posteromedial reach directions. No other significant differences were identified between the groups during SEBT trials in any direction. Effect sizes for significant findings during SEBT trials ranged from 0.75 (moderate) to 0.88 (large), with 95% confidence intervals that ranged from 0.01 (small) to 1.62 (large), which indicated a moderate to large decrease in muscle activity in the CAI group compared with the control group.
Lateral Hops There was significantly less pre-IC amplitude for distal and total lower extremity amplitudes in the CAI group during lateral hopping. Effect sizes for significant findings in pre-IC amplitude during lateral hops ranged from 0.90 (large) to 0.93 (large), with 95% confidence intervals that ranged from 0.15 (small) to 1.68 (large), which indicated large decreases in preparatory muscle activity with the CAI group relative to the control group (Table 5). There were no significant differences between the groups during lateral hopping for post-IC amplitude measures (Table 5).
DISCUSSION We identified group differences in sEMG activity during all 4 functional exercises. The CAI group exhibited less muscle activity in muscles that act on the ankle, knee, and hip when completing the rehabilitative exercises compared with healthy controls. Decreased preparatory muscle activity was demonstrated in the pre-IC analyses during lunges and lateral hopping exercises. Decreased reflexive muscle activity was seen after IC during lunges as well as during static and dynamic balance tasks. Previous studies have identified altered motor control patterns in patients with CAI compared with healthy counterparts during gait [9-11,24], drop landing [12], and various isolated functional tasks [13,14,16,25]. To our knowledge, however, this is the first study to identify altered motor control patterns in muscles that act on the ankle, knee, and hip during common rehabilitative tasks in patients with CAI. This same CAI cohort demonstrated earlier activation of ankle, knee, and hip musculature but not differences in measures of sEMG amplitude before or after IC during walking [9]. Specifically, there was a shift to a preactivation of the PL in those with CAI, which is hypothesized to be a mechanism to control the excessive inversion positioning of the rear foot observed during terminal swing [9]. The differences in the type of compensatory motor control pattern within the same cohort leads us to
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believe that alterations in motor control in patients with CAI are task dependent. Similar to our current study, patients with CAI demonstrate decreased soleus muscle activity during a time to stabilization task after a jump landing [25], and decreased gluteus maximus muscle activity during a rotational squat exercise [13]. Delahunt et al [16], however, found increased muscle activity before and after IC in a lateral hopping task in patients with CAI. This unidirectional lateral hop landing phase has been suggested to directly stress the stability of the lateral ankle [26] and to significantly increase the demand on the PL muscle as a dynamic stabilizer [27]. The increased demand on the lateral dynamic stabilizers in the presence of ankle instability may have selectively provided a stimulus for an increase in preparatory and responsive muscle activity in patients with CAI [16]. However, in the absence of a direct stimulus, such as instability induced during the unidirectional landing phase of the side hop test or an inverted foot position before ground contact during walking, patients with CAI demonstrated decreased muscle activation of the entire lower extremity. Clinically, there has traditionally been a rehabilitative focus on distal ankle musculature, specifically, the peroneals, for their ability to provide dynamic lateral ankle stability. Interestingly, we did not identify a deficit in the extent of peroneal activation during any of the rehabilitative tasks in our study. Gribble et al [28] analyzed dynamic postural control following open chain ankle and lunge fatiguing protocols, and found that deficits caused by motor control alterations in proximal joints could be exposed by functional fatiguing protocols. We were able to identify alterations in distal and proximal joint muscle activity without completing a fatiguing protocol. In addition, we identified segmental differences in distal, proximal, and total muscle activation between the groups When using total muscle activation per epoch used for analysis as an indication of task intensity, the magnitude of the group differences in our study was not exacerbated as the intensity of the rehabilitative tasks increased. Hubbard et al [29] found strong correlations between measures of strength and power of multiple lower extremity muscles, and they speculated that central mechanisms were involved in the global decreases in functional deficits associated with CAI [29]. Patients with CAI also have exhibited gait initiation strategies different from those of healthy counterparts, which have been attributed to altered supraspinal mechanisms of motor control [30]. These findings, along with ours, support that central nervous system mechanisms are likely playing a role in the functional deficits associated with CAI, and that a comprehensive approach to rehabilitation is required, which includes centrally mediated muscle function of distal and proximal muscles. Although centrally mediated deficits are likely playing an integral role in functional deficits in patients with CAI, many of the studies that identified decreases in muscle activity associated with CAI have been performed with tasks that allowed participants to self-select the intensity at which tasks
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were completed. We attempted to standardize subject effort on tasks when possible. For example, the subjects were required to reach as far as possible during SEBT trials. During lunging tasks, the distance was standardized to the individual person, but the rate of lunging was self-selected based on the associated comfort with the task. Similarly, in the lateral hopping task, the subjects were required to hop over a fixed width at a standardized pace; however, the height and maximal lateral excursion were not controlled nor recorded. Although the EMG RMS area does not provide great insight into the quality of the movement or the motor recruitment patterns adopted by each subject, it does provide insight into the extent of motor unit recruitment required to complete the designated exercise with respect to the maximal voluntary capacity of the muscle. Donovan and Hertel [20] developed a paradigm specifically designed for clinicians when targeting deficits associated with CAI. A key component of the paradigm includes an initial assessment of functional limitations so that interventions can be chosen to specifically target those deficits. In the rehabilitation setting, allowing patients to self-select the intensity of various tasks in the presence of ankle instability may result in an unconscious decrease in the intensity at which tasks are performed and may impair clinicians’ ability to improve deficits in muscle activation. However, setting a safe but specific objective goal that includes not only the quantity but also the quality of the movement pattern may require patients to stress the sensorimotor system beyond what they may have otherwise achieved.
Study Limitations Limitations of this study include the lack of kinematic and kinetic data to help support the aforementioned hypotheses of centrally mediated inhibition or unconscious protection via lower intensity or rate of task completion. In addition, the relatively small sample size used in this study, when coupled with the large standard deviations that are inherent with sEMG, collectively increase the potential risk of a type II error in comparisons when statistical significance was not found.
CONCLUSION We identified decreased muscle activation in patients with CAI during common functional rehabilitation exercises. Clinicians should be aware of distal and proximal alterations in motor control in patients with CAI. Identifying novel ways to increase muscle activity and motor recruitment beyond what is currently used for functional rehabilitation may improve patient outcomes.
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2. Nelson AJ, Collins CL, Yard EE, Fields SK, Comstock RD. Ankle injuries among United States high school sports athletes, 2005e2006. J Athl Train 2007;42:381. 3. Swenson DM, Yard EE, Fields SK, Comstock RD. Patterns of recurrent injuries among US high school athletes, 2005e2008. Am J Sports Med 2009;37:1586-1593. 4. Swenson DM, Collins CL, Fields SK, Comstock RD. Epidemiology of US high school sports-related ligamentous ankle injuries, 2005/062010/11. Clin J Sport Med 2013;23:190-196. 5. Anandacoomarasamy A, Barnsley L. Long term outcomes of inversion ankle injuries. Br J Sports Med 2005;39:e14; discussion e14. 6. van Rijn RM, van Os AG, Bernsen RM, Luijsterburg PA, Koes BW, Bierma-Zeinstra SM. What is the clinical course of acute ankle sprains? A systematic literature review. Am J Med 2008;121:324-331. 7. Gribble PA, Delahunt E, Bleakley C, et al. Selection criteria for patients with chronic ankle instability in controlled research: A position statement of the International Ankle Consortium. J Orthop Sports Phys Ther 2013;43:585-591. 8. Hertel J. Sensorimotor deficits with ankle sprains and chronic ankle instability. Clin Sports Med 2008;27:353-370. 9. Feger M, Donovan L, Hart J, Hertel J. Lower extremity muscle activation in patients with and without chronic ankle instability. J Athl Train. In press. 10. Delahunt E, Monaghan K, Caulfield B. Altered neuromuscular control and ankle joint kinematics during walking in subjects with functional instability of the ankle joint. Am J Sports Med 2006;34: 1970-1976. 11. Hopkins JT, Coglianese M, Glasgow P, Reese S, Seeley MK. Alterations in evertor/invertor muscle activation and center of pressure trajectory in participants with functional ankle instability. J Electromyogr Kinesiol 2012;22:280-285. 12. Delahunt E, Monaghan K, Caulfield B. Changes in lower limb kinematics, kinetics, and muscle activity in subjects with functional instability of the ankle joint during a single leg drop jump. J Orthop Res 2006;24:1991-2000. 13. Webster KA, Gribble PA. A comparison of electromyography of gluteus medius and maximus in subjects with and without chronic ankle instability during two functional exercises. Phys Ther Sport 2012;14: 17-22. 14. Van Deun S, Staes FF, Stappaerts KH, Janssens L, Levin O, Peers KK. Relationship of chronic ankle instability to muscle activation patterns during the transition from double-leg to single-leg stance. Am J Sports Med 2007;35:274-281. 15. McKeon PO, Hertel J. Systematic review of postural control and lateral ankle instability, part II: Is balance training clinically effective? J Athl Train 2008;43:305-315. 16. Delahunt E, Monaghan K, Caulfield B. Ankle function during hopping in subjects with functional instability of the ankle joint. Scand J Med Sci Sports 2007;17:641-648. 17. Farrokhi S, Pollard CD, Souza RB, Chen Y, Reischl S, Powers CM. Trunk position influences the kinematics, kinetics, and muscle activity of the lead lower extremity during the forward lunge exercise. J Orthop Sports Phys Ther 2008;38:403. 18. Finnoff JT, Peterson VJ, Hollman JH, Smith J. Intrarater and interrater reliability of the Balance Error Scoring System (BESS). PM R 2009;1: 50-54. 19. Gribble PA, Kelly SE, Refshauge KM, Hiller CE. Interrater reliability of the Star Excursion Balance Test. J Athl Train 2013;48:621-626. 20. Donovan L, Hertel J. A new paradigm for rehabilitation of patients with chronic ankle instability. Phys Sportsmed 2012;40:41-51. 21. Itoh H, Kurosaka M, Yoshiya S, Ichihashi N, Mizuno K. Evaluation of functional deficits determined by four different hop tests in patients with anterior cruciate ligament deficiency. Knee Surg Sports Traumatol Arthrosc 1998;6:241-245. 22. Jones GM, Watt D. Observations on the control of stepping and hopping movements in man. J Physiol (Lond) 1971;219:709-727.
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23. Hopkins W, Marshall S, Batterham A, Hanin J. Progressive statistics for studies in sports medicine and exercise science. Med Sci Sport Exerc 2009;41:3-13. 24. Santilli V, Frascarelli MA, Paoloni M, et al. Peroneus longus muscle activation pattern during gait cycle in athletes affected by functional ankle instability. A surface electromyographic study. Am J Sports Med 2005;33:1183-1187. 25. Brown C, Ross S, Mynark R, Guskiewicz K. Assessing functional ankle instability with joint position sense, time to stabilization, and electromyography. J Sport Rehabil 2004;13:122-124. 26. Docherty CL, Arnold BL, Gansneder BM, Hurwitz S, Gieck J. Functional-performance deficits in volunteers with functional ankle instability. J Athl Train 2005;40:30.
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27. Yoshida M, Taniguchi K, Katayose M. Analysis of muscle activity and ankle joint movement during the side-hop test. J Strength Cond Res 2011;25:2255-2264. 28. Gribble PA, Hertel J, Denegar CR. Chronic ankle instability and fatigue create proximal joint alterations during performance of the Star Excursion Balance Test. Int J Sports Med 2007;28:236-244. 29. Hubbard TJ, Kramer LC, Denegar CR, Hertel J. Correlations among multiple measures of functional and mechanical instability in subjects with chronic ankle instability. J Athl Train 2007;42: 361-366. 30. Hass CJ, Bishop MD, Doidge D, Wikstrom EA. Chronic ankle instability alters central organization of movement. Am J Sports Med 2010; 38:829-834.
Lower Extremity Muscle Activation During Functional Exercises in Patients With and Without Chronic Ankle Instability Mark A. Feger, MEd, Luke Donovan, MEd, Joseph M. Hart, PhD, Jay Hertel, PhD Objective: To determine whether individuals with chronic ankle instability (CAI) exhibit altered neuromuscular control as demonstrated by surface electromyography (EMG) amplitudes compared with healthy controls during single-limb eyes-closed balance, Star Excursion Balance Test, forward lunge, and lateral hop exercises. Design: A cross-sectional laboratory study. Setting: A research laboratory. Participants: Fifteen young adults with CAI and 15 healthy controls. Interventions: The subjects performed functional exercises while surface EMG signals were recorded from the tibialis anterior, peroneus longus, lateral gastrocnemius, rectus femoris, biceps femoris, and gluteus medius. Main Outcome Measurements: Surface EMG amplitudes (root mean square area) for each muscle, muscles of the shank (distal 3 muscles), muscles of the thigh (proximal 3 muscles), and total muscle activity (all 6 muscles) of the lower extremity were analyzed and compared between the groups. Results: Individuals with CAI demonstrated significantly less EMG activity in the muscles of the lower extremity during all 4 functional exercises. Effect sizes for significant differences between groups ranged from 0.75 to 1.08, none of which had 95% confidence intervals that crossed zero, which indicates moderate to large decreases in muscle activity in patients with CAI compared with healthy controls. Conclusions: Patients with CAI demonstrated decreased muscle activity of ankle, knee, and hip musculature during common functional rehabilitative tasks. Clinicians may benefit from implementing functional exercises for patients with CAI that target both distal and proximal muscles of the lower extremity. PM R 2014;-:1-10
INTRODUCTION Ankle sprains account for 15%-23% of athletic injuries in the high school and collegiate settings [1,2]. Furthermore, ankle sprains are the most common site for recurrent injury and account for 25% of all recurrent injuries [3], and recurrent ankle sprains account for 15% of all ankle sprains [4]. Recurrent ankle sprains are often associated with residual symptoms such as pain, subjective instability, and decreased self-reported function [5,6]. A recent position statement indicates that a history of at least 1 significant ankle sprain, a subsequent history of the ankle “giving way,” and self-reported functional limitations are defining characteristics of a heterogeneous condition known as chronic ankle instability (CAI) [7]. Sensory, reflexive, and motor control deficits may contribute to CAI [8]. Visual inspection of motor control patterns in patients with CAI is difficult in practice; however, adaptations have been reported with laboratory measures. Patients with CAI have demonstrated altered motor control indicated by surface EMG (sEMG) during walking and drop landing [9-11]. During walking, patients with CAI activate their peroneus longus (PL) before initial contact (IC), whereas healthy controls do so after IC [9,10]. An opposite relationship exists during drop landing, in which patients with CAI have less anticipatory muscle activity compared with healthy individuals [12]. Altered motor control patterns also PM&R 1934-1482/13/$36.00 Printed in U.S.A.
M.A.F. Department of Kinesiology, 210 Emmet Street South Charlottesville, VA 22904. Address correspondence to M.A.F.; e-mail: [email protected] Disclosure: nothing to disclose L.D. Department of Kinesiology, University of Virginia, Charlottesville, VA Disclosure: nothing to disclose J.M.H. Department of Kinesiology, University of Virginia, Charlottesville, VA Disclosure: nothing to disclose J.H. Department of Kinesiology, University of Virginia, Charlottesville, VA Disclosure: nothing to disclose Submitted for publication August 26, 2013; accepted December 22, 2013.
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have been identified in proximal joint muscles, including decreased gluteus maximus muscle activity during a rotational squat exercise in patients with CAI [13]. During the transition from a bipedal to a unipedal stance, a slower onset of muscle activity and less anticipatory muscle activation in the ankle, knee, and hip muscles were seen in patients with CAI, which indicates a reliance on feedback, rather than feedforward, motor control to complete the postural transition [14]. Balance and coordination training are effective intervention strategies for reducing the risk of ankle sprains, especially in patients who have a history of ankle sprain but who have not developed CAI [15], but the efficacy of such exercises at reducing the risk of recurrent sprains in patients with CAI is uncertain [15]. Altered motor control patterns have been identified in muscles that act on the ankle, knee, and hip during gait [9-11] and isolated functional exercises [12-14,16] in patients with CAI; however, there has not previously been a comprehensive analysis of the EMG activity of both distal and proximal lower extremity muscles during common functional exercises used for rehabilitation in patients with CAI. An understanding of how patients with CAI activate muscles to complete functional rehabilitative exercises can give insight into how rehabilitation can be tailored to specifically target and improve patient outcomes. Our purpose was to compare the sEMG root mean square (RMS) area during common functional exercises, including lunges, single limb balance, the Star Excursion Balance Test (SEBT), and lateral hopping exercises to test the hypothesis that patients with CAI would have decreased sEMG amplitudes of ankle, knee, and hip musculature during all tasks compared with healthy counterparts.
METHODS
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Table 1. Subject demographics
Mean SD age, y Mean SD height, cm Mean SD mass, kg Men:women No. previous sprains, mean SD Mean SD time since last sprain, mo Godin score, mean SD FAAM ADL, mean SD FAAM Sport, mean SD
CAI Group
Control Group
23 4.2 173 10.8 72.4 14 5:10 4.5 3.2 15.2 9.3
22.9 3.4 173 9.4 70.8 18 5:10 N/A N/A
94 47 87.2 7.1 68.5 5.7
84 40 100 0 100 0
CAI ¼ chronic ankle instability; SD ¼ standard deviation; N/A ¼ not applicable; Godin score ¼ Godin Leisure-Time Exercise Questionnaire score; FAAM ADL ¼ Foot and Ankle Ability Measure Activities of Daily Living scale score; FAAM Sport ¼ Foot and Ankle Ability Measure Sport subscale score.
and the same cohorts have previously been reported in another article that investigated EMG differences during gait [9]. Briefly, the control group was self-reported to be healthy and to have no history of ankle sprain to either ankle. The CAI group had a history of more than 1 ankle sprain with the initial sprain occurring more than 1 year before the study onset and current self-reported functional deficits due to ankle symptoms. The subjects were allocated to groups based on their ankle health status (CAI or healthy), and healthy test limbs were side matched (right or left) to the involved CAI test limbs [9]. Subjects were excluded if they had an ankle sprain within the 6 weeks before the study onset, a history of lower extremity injury or surgery, balance disorders, neuropathies, diabetes, or other conditions known to affect balance. The subjects provided informed consent, and the study was approved by the university’s institutional review board.
Design We performed a cross-sectional laboratory study in which the independent variable was the group (CAI, healthy control) and the dependent variables were sEMG RMS area for the tibialis anterior (TA), PL, lateral gastrocnemius, rectus femoris (RF), biceps femoris, and gluteus medius during single-limb eyes-closed balance, SEBT reach directions (anterior, posterior medial, and posterior lateral), forward lunges, and lateral hops. We also summed the normalized sEMG amplitudes for individual muscles to analyze segmental muscle activity for the distal musculature (TA, PL, lateral gastrocnemius), proximal musculature (RF, biceps femoris, gluteus medius), and total lower extremity musculature (all 6 muscles) between groups.
Subjects Fifteen young adults with CAI and 15 healthy controls volunteered (Table 1). This study was part of a larger study,
Instruments The sEMG signals were collected from disposable, pregelled, 10-mm, round Silver-Silver Chloride (Ag-AgCl) electrodes and amplified with a high-gain, differential-input biopotential amplifier with a gain of 1000 and digitized with a 16-bit data acquisition system (MP 150, Biopac Systems Inc, Goleta, CA) at 2000 Hz with a common-mode rejection ratio of 110 dB, an input impedance of 1.0 MU, and a noise voltage of 0.2 mV. Acqknowledge software (v.4.0, Cambridge, England) was used for data collection and processing of EMG signals. The EMG data were collected by using real-time processing with a 10- to 500Hz band pass filter and a 10-sample moving average RMS algorithm. A foot switch (BIOPAC Systems, Santa Barbara, CA) was used to identify ground contact during the SEBT, forward lunge, and lateral hopping exercises. All the subjects wore standard athletic shoes for all exercises (X755WB; New Balance, Brighton, MA).
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Testing Procedures By using methods previously described in detail [9], surface electrodes were placed 2 cm apart and oriented parallel to the muscle-fiber orientation over the midline of the muscle belly determined via manual palpation during a voluntary contraction. Before testing, the subjects performed a 5minute warm-up that consisted of walking at a self-selected pace, and then standardized maximal voluntary isometric contractions (MVIC) were recorded for each muscle against manual resistance for normalization of sEMG amplitudes.
Exercises The subjects completed at least 3 practice trials for each exercise before testing and additional practice trials until they self-reported to be comfortable with each task; however, no subject required more than 5 practice trials per task. For all tasks, failed trials were repeated until the desired number of repetitions was completed. Due to the submaximal nature of the tasks and the low volume of each exercise performed, we did not expect fatigue to affect our outcome measures. Thus, all the subjects completed the tasks in the order described below. Five consecutive lunges were performed and the lead leg was tested. A target line was placed to signal the appropriate heel strike position at a distance determined during practice trials. The target distance was selected to ensure that the test limb reached 90 of hip and knee flexion when the knee of the contralateral stance limb lightly contacted the ground [17]. The subjects were visually monitored and required to keep their hands on their hips, and failed trials included removing hands from the hips or missing the target line during heel strike. A single-limb eyes-closed balance trial was performed for 15 seconds with the stance limb tested. The subjects were required to place their hands on their hips with the contralateral limb comfortably elevated and not in contact with stance limb [18]. The SEBT was performed in the anterior, posteromedial, and posterolateral reach directions by using previously described methods (Figure 1A-C) [19]. Traditionally, the SEBT has been used as a functional assessment for dynamic balance deficits; however, Donovan and Hertel [20] highlighted the benefit of implementing the SEBT as a functional rehabilitation exercise in patients with CAI. Lateral hops were performed with the hopping limb tested. A modified side hop test was performed [21]. The subjects hopped laterally over a 1.5-inch line at a pace of 110 hops per minute for 20 seconds. A metronome was used to set the cadence. A foot switch was used to signal ground contact.
Data Processing Forward Lunge. The middle 3 lunges of the 5 consecutive lunge trials were analyzed. To gain an understanding of
Figure 1. (A) Star Excursion Balance Test, anterior reach. (B) Star Excursion Balance Test, posteromedial reach. (C) Star Excursion Balance Test, posterolateral reach.
preparatory muscle activation and reflexive activation of all muscles [22], a 50-millisecond epoch immediately before IC was used to calculate the pre-IC area under the RMS curve [22]. A 100-millisecond epoch immediately after IC was used to calculate the post-IC area under the RMS curve [22]. Lunge amplitudes were normalized to respective MVIC epochs. Single-limb Eyes-closed Balance. A 3-second epoch during the middle of the single-limb eyes-closed balance trial was analyzed. The area under the RMS curve was calculated and normalized to a 3-second MVIC epoch for each muscle. SEBT. A 500-millisecond epoch just before maximum excursion was averaged over 3 trials for each of the 3 directions. Maximum excursion was defined as the time at which the contralateral limb touched down. The average area under the RMS curve over the 3 trials was normalized to a 500millisecond MVIC epoch for each muscle. Lateral Hops. Six total consecutive hops (3 in each direction) were selected from the middle of the lateral hopping trial. To gain an understanding of preparatory and reflexive activation of all muscles, a 50-millisecond epoch immediately before IC was used to calculate the pre-IC area under the RMS curve [22]. A 100-millisecond epoch immediately
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Table 2. Muscle activation patterns with forward lunge Isolated Muscle Activation Muscles Anterior tibialis Pre-IC Post-IC Peroneus longus Pre-IC Post-IC Lateral gastrocnemius Pre-IC Post-IC Rectus femoris Pre-IC Post-IC Biceps femoris Pre-IC Post-IC Gluteus medius Pre-IC Post-IC
CAI, Mean ± SD
Control, Mean ± SD
ES (95% CI)*
Py
0.46 0.16 0.44 0.13
0.57 0.26 0.61 0.18
0.51 (1.24 to 0.22) 1.08 (1.85 to 0.32)
.21 .01
0.22 0.12 0.33 0.15
0.30 0.27 0.48 0.35
0.38 (1.11 to 0.34) 0.56 (1.29 to 0.17)
.33 .16
0.40 0.36 0.34 0.23
0.45 0.33 0.55 0.37
0.14 (0.86 to 0.57) 0.68 (1.42 to 0.05)
.67 .08
0.13 0.09 0.23 0.17
0.21 0.20 0.17 0.09
0.52 (1.24 to 0.21) 0.44 (0.28 to 1.17)
.21 .38
0.13 0.07 0.12 0.05
0.19 0.11 0.17 0.09
0.65 (1.39 to 0.08) 0.69 (1.42 to 0.05)
.14 .12
0.10 0.07 0.17 0.10
0.17 0.19 0.20 0.10
0.49 (1.22 to 0.24) 0.30 (1.02 to 0.42)
.18 .40
CAI ¼ chronic ankle instability; SD ¼ standard deviation; ES ¼ Cohen d effect size; CI ¼ confidence interval; Pre-IC ¼ 50ms pre-initial contact root mean square area; Post-IC ¼ 100ms post-initial contact root mean square area. *A negative ES indicates decreased muscle activity in the subjects with CAI; a positive ES indicates increased muscle activity in the subjects with CAI. y Independent t test statistical results; level of significance was set a priori at P .05.
after IC was used to calculate the post-IC area under the RMS curve [22]. Lateral hopping amplitudes were normalized to respective MVIC epochs. Distal, Proximal, and Total Muscle Activity. To gain a more comprehensive understanding of the EMG activity of the entire lower extremity during rehabilitative tasks, we summed the normalized muscle activity of the distal (TA, PL, and lateral gastrocnemius), proximal (RF, biceps femoris, and gluteus medius), and entire lower extremity (all 6 muscles). The summed values were analyzed as separate dependent variables for each task as described below.
Statistical Analysis The independent variable was group (CAI and healthy control), and the main outcome measures were sEMG
RMS areas for a predetermined epoch respective of each task for each individual muscle, the sum of the 3 distal muscles, the sum of the 3 proximal muscles, and the sum of all 6 muscles. We performed an independent t test for each dependent variable to compare the groups. The level of significance was set a priori at P .05 for all analyses. Per contemporary statistical recommendations [23], we did not control for multiple comparisons; instead, in addition to inferential statistical comparison, we calculated Cohen d effect sizes and associated 95% confidence intervals to estimate the magnitude and precision of group differences for each measure. Effect sizes were interpreted as 0.80, large; 0.50, moderate; and 0.20, small. Negative effect sizes indicated that CAI muscle activation was less than that of the control group. Positive effect sizes indicated that CAI muscle activation was greater than that of the control group. Data were analyzed by using the
Table 3. Muscle activation patterns with single-leg eyes-closed balance Isolated Muscle Activation Muscles Anterior tibialis Peroneus longus Lateral gastrocnemius Rectus femoris Biceps femoris Gluteus medius
CAI, Mean ± SD 0.35 0.45 0.25 0.09 0.07 0.16
0.18 0.22 0.11 0.10 0.07 0.11
Control, Mean ± SD 0.49 0.48 0.33 0.19 0.12 0.13
0.19 0.26 0.19 0.11 0.11 0.09
ES (95% CI)* 0.76 0.12 0.52 0.95 0.54 0.30
(1.5 to 0.02) (0.84 to 0.59) (1.24 to 0.21) (1.71 to 0.20) (1.27 to 0.19) (0.42 to 1.02)
Py .05 .74 .16 .02 .13 .55
CAI ¼ chronic ankle instability; SD ¼ standard deviation; ES ¼ Cohen d effect size; CI ¼ confidence interval. *A negative ES indicates decreased muscle activity in the subjects with CAI; a positive ES indicates increased muscle activity in the subjects with CAI. y Independent t test statistical results; level of significance was set a priori at P .05.
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Table 2. Continued Distal-Proximal Muscle Activation CAI, Mean ± SD Control, Mean ± SD
1.08 0.57 1.11 0.32
1.32 0.58 1.64 0.71
Total Muscle Activation P y CAI, Mean ± SD Control, Mean ± SD
ES (95% CI)*
0.56 0.32 0.67 0.37
Py
0.42 (1.14 to 0.31) .28 0.96 (1.72 to 0.21) .02 1.45 0.59 1.63 0.48
0.36 0.16 0.52 0.25
ES (95% CI)*
1.88 0.82 2.30 0.99
0.60 (1.33 to 0.13) .12 0.86 (1.61 to 0.11) .03
0.79 (1.53 to 0.05) .05 0.48 (1.20 to 0.25) .22
Statistical Package for the Social Sciences version 20.0 (SPSS Inc, Chicago, IL).
RESULTS
from 0.05 (small) to 1.85 (large), which indicated moderate-to-large decreases in muscle activity in the CAI group (Table 2).
Single-limb Eyes-closed Balance
Forward Lunges There was significantly less proximal muscle activation before IC in the CAI group compared with healthy controls (Table 2). There was significantly less muscle activation for the TA in the CAI group compared with the healthy controls for post-IC amplitude. In addition, there were significantly less distal and total lower extremity post-IC amplitudes in the CAI group compared with the healthy control group. Effect sizes for significant findings during forward lunges ranged from 0.79 (moderate) to 1.08 (large), with 95% confidence intervals that ranged
There was significantly less muscle activity in the CAI group when compared with healthy controls for the TA and RF sEMG amplitudes during single-limb eyes-closed balance. For total lower extremity muscle activation, the CAI group had a significantly lower sEMG amplitude compared with the healthy control group. Effect-size point estimates for the significant findings during single-limb eyes-closed balance ranged from 0.76 (moderate) to 0.95 (large), with 95% confidence intervals that ranged from 0.02 (small) to 1.71 (large), which indicated moderate-to-large decreases in muscle activity in the CAI group (Table 3).
Table 3. Continued Distal-Proximal Muscle Activation CAI, Mean ± SD Control, Mean ± SD
ES (95% CI)*
Total Muscle Activation P y CAI, Mean ± SD Control, Mean ± SD
1.05 0.36
1.31 0.43
0.66 (1.39 to 0.08) .10
0.32 0.17
0.45 0.24
0.63 (1.36 to 0.11) .11
1.37 0.42
1.75 0.56
ES (95% CI)*
Py
0.77 (1.51 to 0.03) .05
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Table 4. Muscle activation patterns with Star Excursion Balance Test Isolated Muscle Activation Muscles
CAI, Mean ± SD
Control, Mean ± SD
ES (95% CI)*
Py
Anterior Posteromedial Posterolateral
0.40 0.22 0.50 0.19 0.75 0.28
0.71 0.45 0.68 0.28 0.89 0.31
0.88 (1.62 to 0.13) 0.75 (1.49 to 0.01) 0.47 (1.20 to 0.25)
.03 .05 .22
Anterior Posteromedial Posterolateral
0.48 0.20 0.34 0.12 0.35 0.12
0.44 0.29 0.38 0.18 0.40 0.24
0.16 (0.56 to 0.88) 0.26 (0.98 to 0.46) 0.26 (0.98 to 0.46)
.66 .61 .48
Anterior Posteromedial Posterolateral
0.39 0.28 0.18 0.11 0.22 0.10
0.51 0.39 0.25 0.18 0.29 0.20
0.35 (1.07 to 0.37) 0.47 (1.19 to 0.26) 0.44 (1.17 to 0.28)
.34 .23 .23
Anterior Posteromedial Posterolateral
0.42 0.23 0.54 0.28 0.54 0.31
0.44 0.30 0.70 0.41 0.73 0.47
0.07 (0.79 to 0.64) 0.46 (1.18 to 0.27) 0.48 (1.20 to 0.25)
.83 .24 .22
Anterior Posteromedial Posterolateral
0.17 0.07 0.11 0.06 0.16 0.08
0.18 0.10 0.13 0.06 0.16 0.07
0.12 (0.83 to 0.60) 0.33 (1.05 to 0.39) 0 (0.72 to 0.72)
.66 .62 .89
Anterior Posteromedial Posterolateral
0.17 0.12 0.25 0.14 0.24 0.15
0.13 0.09 0.23 0.18 0.20 0.14
0.38 (0.34 to 1.10) 0.12 (0.59 to 0.84) 0.50 (1.23 to 0.22)
.31 .70 .52
Reach Direction
Anterior tibialis
Peroneus longus
Lateral gastrocnemius
Rectus femoris
Biceps femoris
Gluteus medius
CAI ¼ chronic ankle instability; SD ¼ standard deviation; ES ¼ Cohen d effect size; CI ¼ confidence interval. *A negative ES indicates decreased muscle activity in the subjects with CAI; a positive ES indicates increased muscle activity in the subjects with CAI. y Independent t test statistical results; level of significance was set a priori at P .05.
Table 5. Muscle activation patterns with lateral hop Isolated Muscle Activation Muscles Anterior tibialis Pre-IC Post-IC Peroneus longus Pre- IC Post-IC Lateral gastrocnemius Pre-IC Post-IC Rectus femoris Pre-IC Post-IC Biceps femoris Pre-IC Post-IC Gluteus medius Pre-IC Post-IC
ES (95% CI)*
Py
CAI, Mean ± SD
Control, Mean ± SD
0.24 0.16 0.35 0.26
0.34 0.17 0.54 0.31
0.61 (1.34-0.13) 0.66 (1.40 to 0.07)
.13 .10
0.50 0.17 0.67 0.19
0.70 0.46 0.88 0.52
0.58 (1.31 to 0.15) 0.54 (1.26 to 0.19)
.16 .19
0.83 0.55 1.21 1.23
1.39 0.86 1.61 1.06
0.78 (1.52 to 0.03) 0.35 (1.07 to 0.37)
.06 .38
0.28 0.38 0.62 0.47
0.30 0.21 0.77 0.40
0.07 (0.78 to 0.65) 0.34 (1.06 to 0.38)
.88 .41
0.38 0.20 0.31 0.26
0.49 0.30 0.32 0.15
0.43 (1.16 to 0.29) 0.05 (0.76 to 0.67)
.28 .96
0.35 0.20 0.60 0.26
0.56 0.44 0.69 0.43
0.61 (1.35 to 0.12) 0.25 (0.97 to 0.47)
.13 .53
CAI ¼ chronic ankle instability; SD ¼ standard deviation; ES ¼ Cohen d effect size; CI ¼ confidence interval; Pre-IC ¼ 50 ms pre-initial contact root mean square area; Post-IC ¼ 100 ms post-initial contact root mean square area. *A negative ES indicates decreased muscle activity in the subjects with CAI; a positive ES indicates increased muscle activity in the subjects with CAI. y Independent t test statistical results; level of significance was set a priori at P .05.
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Table 4. Continued Distal-Proximal Muscle Activation CAI, Mean ± SD Control, Mean ± SD
1.26 0.44 1.02 0.25 1.32 0.33
1.66 0.82 1.30 0.49 1.58 0.61
ES (95% CI)*
Total Muscle Activation P y CAI, Mean ± SD Control, Mean ± SD
0.75 0.37 1.06 0.49 1.09 0.56
Py
0.61 (1.34 to 1.10) .12 0.72 (1.46 to 0.02) .06 0.53 (1.26 to 0.20) .16 2.02 0.64 1.93 0.52 2.25 0.53
0.76 0.38 0.91 0.37 0.94 0.45
ES (95% CI)*
2.4 1.13 2.36 0.75 2.67 1.05
0.41 (1.14 to 0.31) .27 0.67 (1.40 to 0.07) .09 0.50 (1.23 to 0.22) .19
0.03 (0.69 to 0.74) .97 0.35 (1.07 to 0.38) .37 0.30 (1.01 to 0.42) .42
Table 5. Continued Distal-Proximal Muscle Activation CAI, Mean ± SD Control, Mean ± SD
1.57 0.68 2.22 1.31
2.43 1.12 3.03 1.22
ES (95% CI)*
Total Muscle Activation P
y
CAI, Mean ± SD Control, Mean ± SD
1.34 0.65 1.78 0.81
Py
0.93 (1.68 to 0.17) .03 0.64 (1.37 to 0.09) .12 2.57 0.99 3.76 1.62
1.00 0.51 1.54 0.78
ES (95% CI)*
0.58 (1.31 to 0.15) 0.30 (1.02 to 0.42)
.15 .45
3.77 1.61 4.81 1.86
0.90 (1.65 to 0.15) .03 0.60 (1.33 to 0.13) .14
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SEBT Results for the SEBT in the anterior, posteromedial, and posterolateral direction are summarized in Table 4. There was significantly less muscle activity in the CAI group during the SEBT in the TA during the anterior and posteromedial reach directions. No other significant differences were identified between the groups during SEBT trials in any direction. Effect sizes for significant findings during SEBT trials ranged from 0.75 (moderate) to 0.88 (large), with 95% confidence intervals that ranged from 0.01 (small) to 1.62 (large), which indicated a moderate to large decrease in muscle activity in the CAI group compared with the control group.
Lateral Hops There was significantly less pre-IC amplitude for distal and total lower extremity amplitudes in the CAI group during lateral hopping. Effect sizes for significant findings in pre-IC amplitude during lateral hops ranged from 0.90 (large) to 0.93 (large), with 95% confidence intervals that ranged from 0.15 (small) to 1.68 (large), which indicated large decreases in preparatory muscle activity with the CAI group relative to the control group (Table 5). There were no significant differences between the groups during lateral hopping for post-IC amplitude measures (Table 5).
DISCUSSION We identified group differences in sEMG activity during all 4 functional exercises. The CAI group exhibited less muscle activity in muscles that act on the ankle, knee, and hip when completing the rehabilitative exercises compared with healthy controls. Decreased preparatory muscle activity was demonstrated in the pre-IC analyses during lunges and lateral hopping exercises. Decreased reflexive muscle activity was seen after IC during lunges as well as during static and dynamic balance tasks. Previous studies have identified altered motor control patterns in patients with CAI compared with healthy counterparts during gait [9-11,24], drop landing [12], and various isolated functional tasks [13,14,16,25]. To our knowledge, however, this is the first study to identify altered motor control patterns in muscles that act on the ankle, knee, and hip during common rehabilitative tasks in patients with CAI. This same CAI cohort demonstrated earlier activation of ankle, knee, and hip musculature but not differences in measures of sEMG amplitude before or after IC during walking [9]. Specifically, there was a shift to a preactivation of the PL in those with CAI, which is hypothesized to be a mechanism to control the excessive inversion positioning of the rear foot observed during terminal swing [9]. The differences in the type of compensatory motor control pattern within the same cohort leads us to
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believe that alterations in motor control in patients with CAI are task dependent. Similar to our current study, patients with CAI demonstrate decreased soleus muscle activity during a time to stabilization task after a jump landing [25], and decreased gluteus maximus muscle activity during a rotational squat exercise [13]. Delahunt et al [16], however, found increased muscle activity before and after IC in a lateral hopping task in patients with CAI. This unidirectional lateral hop landing phase has been suggested to directly stress the stability of the lateral ankle [26] and to significantly increase the demand on the PL muscle as a dynamic stabilizer [27]. The increased demand on the lateral dynamic stabilizers in the presence of ankle instability may have selectively provided a stimulus for an increase in preparatory and responsive muscle activity in patients with CAI [16]. However, in the absence of a direct stimulus, such as instability induced during the unidirectional landing phase of the side hop test or an inverted foot position before ground contact during walking, patients with CAI demonstrated decreased muscle activation of the entire lower extremity. Clinically, there has traditionally been a rehabilitative focus on distal ankle musculature, specifically, the peroneals, for their ability to provide dynamic lateral ankle stability. Interestingly, we did not identify a deficit in the extent of peroneal activation during any of the rehabilitative tasks in our study. Gribble et al [28] analyzed dynamic postural control following open chain ankle and lunge fatiguing protocols, and found that deficits caused by motor control alterations in proximal joints could be exposed by functional fatiguing protocols. We were able to identify alterations in distal and proximal joint muscle activity without completing a fatiguing protocol. In addition, we identified segmental differences in distal, proximal, and total muscle activation between the groups When using total muscle activation per epoch used for analysis as an indication of task intensity, the magnitude of the group differences in our study was not exacerbated as the intensity of the rehabilitative tasks increased. Hubbard et al [29] found strong correlations between measures of strength and power of multiple lower extremity muscles, and they speculated that central mechanisms were involved in the global decreases in functional deficits associated with CAI [29]. Patients with CAI also have exhibited gait initiation strategies different from those of healthy counterparts, which have been attributed to altered supraspinal mechanisms of motor control [30]. These findings, along with ours, support that central nervous system mechanisms are likely playing a role in the functional deficits associated with CAI, and that a comprehensive approach to rehabilitation is required, which includes centrally mediated muscle function of distal and proximal muscles. Although centrally mediated deficits are likely playing an integral role in functional deficits in patients with CAI, many of the studies that identified decreases in muscle activity associated with CAI have been performed with tasks that allowed participants to self-select the intensity at which tasks
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were completed. We attempted to standardize subject effort on tasks when possible. For example, the subjects were required to reach as far as possible during SEBT trials. During lunging tasks, the distance was standardized to the individual person, but the rate of lunging was self-selected based on the associated comfort with the task. Similarly, in the lateral hopping task, the subjects were required to hop over a fixed width at a standardized pace; however, the height and maximal lateral excursion were not controlled nor recorded. Although the EMG RMS area does not provide great insight into the quality of the movement or the motor recruitment patterns adopted by each subject, it does provide insight into the extent of motor unit recruitment required to complete the designated exercise with respect to the maximal voluntary capacity of the muscle. Donovan and Hertel [20] developed a paradigm specifically designed for clinicians when targeting deficits associated with CAI. A key component of the paradigm includes an initial assessment of functional limitations so that interventions can be chosen to specifically target those deficits. In the rehabilitation setting, allowing patients to self-select the intensity of various tasks in the presence of ankle instability may result in an unconscious decrease in the intensity at which tasks are performed and may impair clinicians’ ability to improve deficits in muscle activation. However, setting a safe but specific objective goal that includes not only the quantity but also the quality of the movement pattern may require patients to stress the sensorimotor system beyond what they may have otherwise achieved.
Study Limitations Limitations of this study include the lack of kinematic and kinetic data to help support the aforementioned hypotheses of centrally mediated inhibition or unconscious protection via lower intensity or rate of task completion. In addition, the relatively small sample size used in this study, when coupled with the large standard deviations that are inherent with sEMG, collectively increase the potential risk of a type II error in comparisons when statistical significance was not found.
CONCLUSION We identified decreased muscle activation in patients with CAI during common functional rehabilitation exercises. Clinicians should be aware of distal and proximal alterations in motor control in patients with CAI. Identifying novel ways to increase muscle activity and motor recruitment beyond what is currently used for functional rehabilitation may improve patient outcomes.
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