Sensorimotor function as a predictor of chronic ankle instability

Clinical Biomechanics 24 (2009) 451–458

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Sensorimotor function as a predictor of chronic ankle instability JoEllen M. Sefton a,*, Charlie A. Hicks-Little f, Tricia J. Hubbard b,d, Mark G. Clemens c,d, Christopher M. Yengo c,d, David M. Koceja e, Mitchell L. Cordova b,d a

Department of Kinesiology, Auburn University, Auburn, AL 36849-5323, USA Department of Kinesiology, The University of North Carolina at Charlotte, Charlotte, NC, USA c Department of Biology, The University of North Carolina at Charlotte, Charlotte, NC, USA d Center for Biomedical Engineering Systems, The University of North Carolina at Charlotte, Charlotte, NC, USA e Program in Neural Science and Motor Control Laboratory, Department of Kinesiology Indiana University, Bloomington, IN, USA f Department of Exercise and Sport Science, University of Utah, Salt Lake City, UT, USA b

a r t i c l e

i n f o

Article history: Received 7 August 2008 Accepted 8 March 2009

Keywords: Postural control H-reflex Joint proprioception Dynamic balance Ankle injury

a b s t r a c t Background: Recurrent ankle injury occurs in 70% of individuals experiencing a lateral ankle sprain. The cause of this high level of recurrence is currently unknown. Researchers have begun to investigate sensorimotor deficits as one possible cause with inconclusive and often conflicting results. The purpose of this study was to further the understanding of the role of sensorimotor deficits in the chronically unstable ankle by establishing which specific measures best distinguish between chronically unstable and healthy ankles. Methods: Twenty-two participants with chronic ankle instability and 21 healthy matched controls volunteered. Twenty-five variables were measured within four sensorimotor constructs: joint kinesthesia (isokinetic dynamometer), static balance (force plate), dynamic balance (Star Excursion Balance Test) and motoneuron pool excitability (electromyography). Findings: The above variables were evaluated using a discriminant function analysis [Wilks’ K = 0.536 v2(7, N = 43) = 22.118, P = 0.002; canonical correlation = 0.681]. The variables found to be significant were then used to assess group discrimination. This study revealed that seven separate variables from the static balance (anterior/posterior and medial/lateral displacement and velocity) and motoneuron pool excitability constructs (single-legged recurrent inhibition and single- and double-legged paired reflex depression) accurately classified over 86% of participants with unstable ankles. Interpretation: These results suggest that a multivariate approach may be necessary to understand the role of sensorimotor function in chronic ankle instability, and to the development of appropriate rehabilitation and prevention programs. Out of the four overall constructs, only two were needed to accurately classify the participants into two groups. This indicates that static balance and motoneuron pool excitability may be more clinically important in treatment and rehabilitation of chronic ankle instability than functional balance or joint kinesthesia. Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction Lateral ankle sprains comprised over 14% of all injuries recorded in National Collegiate Athletic Association athletes in the past 16 years (Hootman et al., 2007). It is the most common injury experienced by active individuals, with an incidence rate of approximately 23,000 per day in the United States (Gerber et al., 1998). This injury results in pain, disability, and time lost from work and activity resulting in an estimated 1.2 million physician visits per year, at a cost of $835–$1206 per patient with an annual cost of 3.8 billion dollars (Gerber et al., 1998). The recurrence rates

* Corresponding author. E-mail address: [email protected] (J.M. Sefton). 0268-0033/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.clinbiomech.2009.03.003

for lateral ankle sprains have been estimated to be as high as 70% (Yeung et al., 1994). Recent research has focused on understanding the contributing factors (Kaminski and Hartsell, 2002; Konradsen, 2002), the role of rehabilitation intervention programs (Denegar and Miller, 2002), and predisposing conditions (Kaminski and Hartsell, 2002; Beynnon et al., 2002) for this injury. Potentially, more important than the injury itself is the known predisposition to chronic disability and the early onset of degenerative ankle joint disease (Brown et al., 2006; Valderrabano et al., 2006). This tendency toward repeated lateral ankle sprains and the associated recurring symptoms is termed chronic ankle instability (CAI) (Janis et al., 1998; Safran et al., 1999a,b). The potential causes of CAI have commonly been separated into mechanical and functional components (Freeman et al., 1965); however, it is more likely that CAI is a result of the combination

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of multiple factors representative of these components. (Kaminski and Hartsell, 2002; Konradsen, 2002; Monaghan et al., 2006) A recent study (Hubbard et al., 2007) examined a combination of mechanical and functional variables to assess which were most associated with CAI. In this work, a discriminant analysis revealed that the mechanical and functional variables investigated accounted for approximately 46% of the total variance between CAI and healthy participants. This work is important as it provides the first step toward understanding, from a multivariate perspective, which specific set of mechanical and functional factors are most associated with CAI. These results, however, also suggest that approximately 54% of the variance observed in the CAI group membership remains unexplained (Hubbard et al., 2007). The variance that was unaccounted for by the mechanical and functional factors tested may be a result of sensorimotor factors that are contributing to this complex ankle pathology. Past research examining CAI and sensorimotor function has utilized a univariate approach to examine multiple variables often with conflicting results. Specifically, the proprioceptive measures of joint motion detection (kinesthesia) (Gross, 1987; Konradsen, 2002) and joint position sense have been assessed in multiple studies. The work utilizing joint position sense has been more extensive and joint position sense was thus chosen as a variable for the current study. Several studies have indicated an increase in joint position sense absolute error in inversion with subjects with chronically unstable ankles as compared to stable ankles (Konradsen, 2002); and increased error in active and passive plantarflexion and inversion in functionally unstable ankles (Docherty et al., 1998). However, Brown et al. (2004) found no differences between subjects with functionally unstable and healthy ankles in joint position sense in passive dorsiflexion, plantar flexion, inversion, or eversion. Deficits and impairments in static balance (postural control) measures have consistently been found in participants with CAI (Riemann, 2002; McKeon and Hertel, 2008). However, balance variables are numerous and there seems to be no agreement on which measures provide the most information on CAI deficits. Variables include center of pressure (CoP) excursion (Nakagawa and Hoffman, 2004), excursion velocity, and range (McKeon et al., 2008) CoP mean and frequency amplitude (Palmieri et al., 2002a), variability of the mediolateral force signal (Goldie et al., 1994), root mean square velocity of center of pressure excursions (McKeon and Hertel, 2008), center of pressure velocity (Hale et al., 2007), mean CoP velocity, standard deviation of CoP, postural sway (Mitchell et al., 2008), mediolateral and fore-aft sway and displacement (Yaggie and McGregor, 2002), and others (Guskiewicz and Perrin, 1996; Riemann, 2002). Most often measures of CoP are utilized in the analysis of postural control. Once the CoP is determined, deviation from this point represents postural sway (Guskiewicz and Perrin, 1996). There are several ways to measure postural sway, for this study we chose the mean velocity and displacement from CoP; both total and in the medial/lateral and anterior/posterior directions. Shorter CoP displacement paths and slower CoP velocities indicate better postural control. Additionally, root mean square of these measures was calculated as an indicator of variability of the measure. These measures were chosen as they assessed point-to-point changes in CoP and enable the examination of differences between the anterior/posterior and medial/lateral directions. Dynamic measures of postural control such as the Star Excursion Balance Test are becoming more widely studied in those that suffer from CAI (Olmsted et al., 2002). Measures of functional balance provide a more clinical assessment of deficits that may be present after injury. One study found deficits in subjects with CAI as compared to subjects with healthy ankles (Gribble et al., 2007), while two studies have found functional balance and postural control improvements after balance training (Hale et al.,

2007; McKeon et al., 2008). Together, these studies suggest the value of measuring functional as well as static balance in the assessment of individuals with CAI. Finally, motoneuron pool excitability has been an area of interest (McVey et al., 2005; Sefton et al., 2007) because of the role spinal reflexes play in modulating muscle activation during gait (Schneider and Capaday, 2003) and its known influence on maintaining an upright static posture (Mynark and Koceja, 2002). Multiple questions exist concerning the possible role motoneuron pool excitability modulation may play in CAI. For example, are modulations of motoneuron pool excitability occurring pre- or post-synaptically, and do these changes vary depending on stance? Is there an interaction between changes in motoneuron pool excitability, postural control, and other sensorimotor measures? Sensorimotor research has contributed to a better understanding of the mechanisms that may cause CAI, however, the complexity of the sensorimotor system suggests that a multivariate approach is required to further the study of this condition. While the relationship between CAI and various sensorimotor measures has been investigated in the literature, it is not readily apparent which measure is most able to detect sensorimotor deficits in persons with CAI. It appears that the optimal approach to understanding the relationship between sensorimotor function and CAI is a multivariate, discriminative approach. Thus, the objective of this work was to determine the optimal combination of sensorimotor variables that would discriminate between CAI and healthy ankles. This knowledge will not only provide valuable information as to the combination of sensorimotor deficits involved in CAI; but also help to focus future research on variables known to distinguish between healthy and CAI ankles.

2. Methods 2.1. Experimental design This study utilized a case-control experimental design to study the effects of CAI on multiple sensorimotor measures within four central constructs: joint kinesthesia, static balance, dynamic balance and motoneuron pool excitability. The independent variable was ankle group with two levels (healthy and CAI). The dependent variables were: Static balance: center of pressure (CoP) medial/lateral average displacement (ML DISP), root mean square (RMS) of CoP medial/lateral average displacement (RMS CoP ML DISP), CoP anterior/posterior average displacement (AP DISP), RMS of CoP anterior/posterior average displacement (RMS CoP AP DISP), total CoP average displacement (total CoP DISP), RMS total CoP average displacement (RMS total CoP DISP), total CoP medial/lateral velocity (ML VEL), total CoP anterior/posterior velocity (AP VEL), total CoP average velocity (total CoP AVE VEL). Together, these commonly used variables provide information on total deviations from CoP, as well as defining deviations the medial/lateral and anterior/ posterior directions; the velocity of these deviations; and the variability of these deviations (root mean square) (Guskiewicz and Perrin, 1996). Dynamic balance: Star Excursion Balance Test measures were completed in the anterior medial direction, medial direction, and posterior medial directions. Star Excursion Balance Test values represent the directional reach distance normalized by leg length. The simplified Star Excursion Balance Test utilizing three test directions was utilized as it has been found to be sufficient to detect functional stability deficits (Hertel et al., 2006). Motoneuron pool excitability: Hoffmann-reflex protocols to elicit double-legged paired reflex depression (2PRD), double-legged recurrent inhibition (2RI), maximum H-reflex amplitude (Hmax), maximum M-wave amplitude (Mmax), Hmax/Mmax ratio, single-legged paired reflex depression (1PRD), and single-legged recurrent

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inhibition (1RI) were utilized for this study. H-reflex measures are functionally dependent, thus all reflex tests were conducted on the soleus muscle as this muscle is an important contributor to the maintenance of upright stance; (Sefton et al., 2007). While the peroneus longus muscle is important during ankle inversion (Sefton et al., 2006), it would not be expected to be highly active while maintain upright stance. The combination of measures utilized in this study allows for the detection of pre- and post-synaptic modulations in motoneuron pool excitability (paired reflex depression and recurrent inhibition, respectively), as well as assessing differences in modulation due to changes in stance. Joint kinesthesia: assessment of plantar flexion constant error (PFCE), plantar flexion absolute error (PFAE), plantarflexion variable error (PFVE), inversion constant error (IVCE), inversion absolute error (IVAE), inversion variable error (IVVE) were completed. Active positioning in plantarflexion and inversion were chosen as they represent functional measures in the two directions most often involved in lateral ankle injury. Measures of constant, absolute and variable error are different ways of assessing the same measurement, and were included to determine if one method provides more information than the others (Konradsen, 2002; Gross, 1987). 2.2. Participants Twenty-two participants (5 males and 17 females) with chronic ankle instability (mean: age = 22.3 years, height = 167.6 cm, mass = 69.8 kg) and 21 healthy (5 males and 16 females) gender, side and age-matched controls (mean: age = 21.9 years, height = 166.0 cm, mass = 64.1 kg) volunteered. Results for orthopedic assessments, activity levels, and ankle disability scores are located in Table 1. Bilateral orthopedic ankle assessments (anterior drawer and talar tilt tests) were completed by one of two Certified Athletic Trainers each with over 6 years experience. These results further demonstrate the inability of the orthopedic tests to discriminate between the CAI and healthy groups, reinforcing the need for additional screen methods for CAI. Participants were screened for participation with the Ankle Injury History Questionnaire, the Functional Ankle Instability Index, and the Functional Ankle Instability Index – Sport assessment tool (Martin et al., 1999; Eechaute et al., 2007). This index is a measure of percent disability. The Functional Ankle Instability Index and Functional Ankle Instability Index – Sport scores demonstrated a wide range of disability levels among the participants. Participants with healthy ankles typically

Table 1 Subject demographics comparing orthopedic tests and activity levels by group (values are mean ± SD unless indicated as total positive tests). Fitness/orthopedic variable

Ankle sprains (previous year) Anterior drawer test Total positive tests * Talar tilt test Total positive tests * FADI + FADI sport score (%) Aerobic activity (h/week) Resistant training (h/week) Total exercise (h/week) Years competition *

Ankle group

P value

CAI

Healthy

3.3 (3.2) 1.32 (0.48) 7 1.45 (0.51) 10 136.10 (75.35) 4.6 (4.3) 1.5 (2.2) 6.2 (4.7) 7.8 (5.6)

0.0 1.01 (0.30) 2 1.19 (0.40) 4 0.95 (3.0) 3.3 (1.3) 2.2 (2.0) 5.5 (3.2) 4.4 (4.3)

0.003 0.075 0.067 <0.0001 0.83 0.12 0.33 0.67

Standard orthopedic tests, with a positive outcome indicating ligament and joint laxity typically found after ankle sprain. These are subjective tests, with the examiner comparing the CAI side to the healthy side. The positive tests found in the healthy subjects with no history of lateral ankle sprain most likely indicate individuals with greater overall joint laxity; and point out the problem of relying on orthopedic testing to determine group membership. The Functional Ankle Instability Index (FADI) and FADI Sport are scored as percent of total points (104 for the FADI, 32 for the FADI Sport), 100% represents no dysfunction.

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reported 100% ability (with one person reporting 99% in the Functional Ankle Instability Index Sport index). CAI participants reported ability levels with a range of 31.7% on the Functional Ankle Instability Index and 56.2% on the Functional Ankle Instability Index Sport (Table 1). All participants self-reported no history or current incidence of neurological or lower extremity musculoskeletal pathology. Healthy participants reported no incidence of chronic or acute lower extremity injuries. CAI participants reporting a history of more than one ankle sprain 1 year prior to the start of this study, recurring symptoms, and indicating difficulty in more than two areas in the sport index or one area in the Functional Ankle Instability Index section were eligible. All participants provided written informed consent and this study was approved by the University’s Institutional Review Board. 2.3. Procedures Participants were tested in the afternoon to control for known diurnal changes in the H-reflex. The H-reflex measures were tested first to ensure participants had a testable reflex (two participants were dismissed prior to data collection, resulting in 43 total participants). A balanced Latin square design established the order of testing for all other measures. All tests were carried out on the CAI ankle side or the matched-control extremity. 2.3.1. Static balance A force platform (4060-NC Bertec Corporation, Columbus, Ohio, USA) interfaced to a Motion Monitor (Innovative Sports Training, Chicago, IL, USA) data collection system was utilized for measurement of center of pressure variables. Data was sampled at 500 Hz (gain set to 1.0) and digitally filtered using a second-order lowpass Butterworth digital filter with the cut-off frequency set at 6 Hz. Participants assumed an eyes-open single-legged stance with hands resting on their hips for 20 s per trial for a total of five trials, with a 45-s rest period between trials (Palmieri et al., 2002b). The nonstance extremity was held in approximately 30° of hip flexion and 45° of knee flexion. Total CoP average displacement (mm), medial/lateral and anterior/posterior CoP displacement (mm), velocity of total displacement (mm/s), and velocity of medial/lateral and anterior/posterior displacement (mm/s) were measured and root mean square values calculated. 2.3.2. Dynamic balance Dynamic balance was assessed using the Star Excursion Balance Test. Star Excursion Balance Test measurements (cm) were taken in the anterior medial, medial, and posterior medial reach directions (Hertel et al., 2006). The participants maintained a singleleg stance on the test leg while reaching with the reach leg as far as possible in the specified direction on a pre-measured grid after three practice trials, the average of six trials in each direction normalized to leg length was calculated (Olmsted et al., 2002). 2.3.3. Motoneuron pool excitability Soleus H-reflex measurements were recorded using a 16-channel biological signal data acquisition system (MP150 MSW; BIOPAC Systems, Santa Barbara, California, USA). A 4 mm shielded Ag/AgCl disc electrode (BIOPAC) was used to deliver a 200 V maximum square wave stimulus utilizing a stimulator module (STM100C, BIOPAC) and isolation adaptor unit (STMISOC, BIOPAC). Soleus electromyography signals were collected using a pair of disposable 10 mm Ag/AgCl surface disc electrodes (Ver Med, Bellows Falls, Vermont, USA). The raw signal was differentially amplified (gain set at 1000, Common Mode Rejection Ratio (CMRR) = 110 dB, input impedance = 1000 M X, signal/noise = 0.2) and digitally converted at 2000 Hz. The signal was bandpass filtered online (10–500 Hz) and collected for a 250 ms duration.

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Skin preparation and electrode placement was completed as previously described (Sefton et al., 2007). Recording lectrodes were placed over the soleus muscle above the musculotendenous junction. The stimulating electrode was secured over the posterior tibial nerve in the popliteal fossa and the dispersal pad placed on the ipsilateral suprapatellar region. The ground electrode was placed on the ipsilateral lateral malleolus. A series of 1.0 ms square wave stimuli were delivered at 10–20 s intervals to determine the standing soleus maximum Hoffmann-reflex (H-reflex) (Hmax), maximum M-wave (Mmax). The H-reflex was measured on the up-sloping portion of the recruitment curve (Mynark and Koceja, 2002). Seven repetitions were completed for each test condition (H-reflex and Mmax in double-legged stance; and paired reflex depression and recurrent inhibition in double-legged and single-legged stance). 2.3.4. Paired reflex depression protocol A paired reflex depression protocol was used to measure the influence of activation history on the H-reflex as previously described (Sefton et al., 2007). The conditioning stimuli was the first of a pair of equal intensity pulses separated by 80 ms. These were alternated with an unconditioned stimulus to eliminate any neural adaptation. The test stimulus was standardized at 35% of the soleus Mmax (Palmieri et al., 2004) paired reflex depression was measured as the percent depression of the conditioned H-reflex peak relative to the non-conditioned H-reflex peak (Trimble et al., 2000). A series of seven trials of double stimulations were completed in the double- and single-legged stance. The mean percent decrease of the conditioned soleus H-reflex (peak to peak measures) relative to the unconditioned H-reflex was utilized for data analysis. 2.3.5. Recurrent inhibition protocol A recurrent inhibition protocol was used to measure the postsynaptic modulation of the H-reflex. The electrodes and stimulation procedures are identical to those used in the paired reflex depression protocol. This protocol uses a conditioning stimulus of 25% of the soleus Mmax with a second stimulus set at Mmax (to evoke all of the MNs) 10 ms later. Recurrent inhibition is determined by calculating the percent difference between the amplitude of the H-reflex with the conditioning stimulus (H0 ) and the H-reflex without the conditioning stimulus (H1) (Bussel and Pierrot-Deseilligny, 1977; Earles et al., 2002; Palmieri et al., 2004). 2.3.6. Joint kinesthesia measurements Joint position sense was quantified using a Biodex System three exercise dynamometer (Biodex Medical Systems, Shirley, New York, USA). JPS was determined by the subject’s ability to actively replicate a passively placed joint reference angle (Konradsen and Magnusson, 2000). The subject was placed in a prone position with the treatment foot on the plantarflexion/dorsiflexion foot plate of the dynamometer and the knee of the same leg fully extended. The ankle and thigh were secured with straps. The test foot was placed in neutral position (designated as 0°). The treatment ankle was passively moved into 30° of plantarflexion where it remained for 10 s. The ankle was passively moved through two full range of motions. The subject then actively reproduced the original reference angle. Testing for 15° of inversion followed the same protocol. The blindfolded subject was seated with treatment ankle placed on the inversion/eversion foot plate and the ipsilateral knee in 45° of flexion. The ankle and thigh were secured with straps. The ankle was placed in a 0° neutral position. The treatment ankle was placed in 15° of inversion by the investigator, who moved the ankle through two full range of motions. The subject then reproduced the reference angle as closely as possible. Three practice trials followed by six test trials were performed at each reference position for both the inversion and plantarflexion testing. Constant error was calculated as the actual difference between the reference angle

and the matching angle, with + or  indicating the direction of the error. The variable error was calculated as the standard deviation of the constant error, indicating the error occurring when matching the reference angle. The absolute error was calculated as the absolute value of the difference between the matching and reference angle, indicating the composite of both the systematic and random error (Brown et al., 2004; Konradsen, 2002). 2.4. Statistical analysis 2.4.1. Data reduction Multiple trials were completed for each measure (see Section 2.3) and the trial mean for each dependent variable was used for statistical analysis. A multiple analysis of variance was performed on each sensorimotor construct to assess the effects of group on the linear combination of dependent variables: postural control (ML DISP, RMS CoP ML DISP, AP DISP, RMS CoP AP DISP, total CoP DISP, RMS total CoP DISP, ML VEL, AP VEL, total CoP AVE VEL); dynamic balance (anterior medial, medial, and posterior medial); and motoneuron pool excitability (2PRD, 2RI, Hmax/Mmax, 1 PRD, and 1RI); joint position sense (PFCE, PFAE, PFVE, IVCE, IVAE, IVVE). The first model determined group effect of the linear combination of the dependent variables for each construct. Follow-up univariate F tests were then used to identify which specific dependent variables were influenced by CAI. 2.4.2. Discriminant function analysis The multiple analysis of variance tests revealed that seven variables were significantly different between the CAI and healthy groups. These dependent variables were then used as factors in a discriminant function analysis where the criterion variable (group) was dichotomous (CAI and healthy ankles). The seven factors were entered into the equation using a hierarchical modeling approach to establish the best set of indicators of group membership. Because this was an exploratory study, two regularly tested static balance variables that closely approached statistical significance (CoP AP DISP, P = 0.056 and CoP AP VEL, 0.051) were included in the discriminant function analysis (Hubbard et al., 2007). Standardized canonical function coefficients and a structural matrix were used to investigate the contribution of each individual indicator on the determination of group membership. The level of significance was established a priori at P 6 0.05. Statistical Package for the Social Sciences (SPSS) for Windows (v14, SPSS, Inc., Chicago, IL, USA) was used for all analyses.

3. Results 3.1. Preliminary analysis The means, standard deviations, 95% confidence intervals, and P values for all dependent variables for each construct by group are presented in Tables 2–5. The multiple analysis of variance tests were followed by univariate F-tests to assess specific group differences on each separate dependent variable. Seven separate dependent variables were found to be significantly different between CAI and the healthy groups. These variables were then entered into the discriminant function analysis to determine which variables best classified CAI and healthy ankles. 3.1.1. Static balance Overall we found significant differences in static balance between the CAI and healthy groups on the linear combination of static balance dependent measures: [F(8, 31) = 2.73, P = 0.021]. Follow-up univariate F-tests revealed CAI participants had significantly more displacement in both the medial/lateral and ante-

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J.M. Sefton et al. / Clinical Biomechanics 24 (2009) 451–458 Table 2 Postural control variables by group (mean ± SD and 95% confidence intervals). Variablea

CAI

95% CI

Healthy

95% CI

P value

CoP CoP CoP CoP CoP CoP CoP CoP CoP

0.081 (0.021) 0.075 (0.018) 897.87 (230.90) 0.0001 (0.00003) 44.89 (11.55) 3.22 (2.6) 0.88 (7.33) 0.16 (0.13) 0.038 (0.37)

0.072–0.090 0.068–0.082 801.38–994.36 0.000009–0.00011 40.07–49.71 4.30 to 2.14 2.18–3.94 0.21 to 0.11 0.12–0.19

0.77 (0.017) 0.068 (0.016) 830.80 (187.08) 0.0001 (0.00002) 41.54 (9.36) 0.78 (4.71) 3.14 (5.43) 0.036 (0.24) 0.170 (0.27)

0.76–0.78 0.061–0.075 750.73–910.87 0.000091–0.00011 1.56–81.52 1.23–2.79 5.47 to 0.81 0.067–0.14 0.29–0.054

0.50 0.18 0.32 0.19 0.32 0.002b 0.056b 0.003b 0.05b

RMS ML DISP RMS AP DISP total DISP RMS DISP total VEL ML DISP AP DISP ML VEL AP VEL

ML: + value is medial,  value is lateral; AP: + value is anterior ,  value is posterior. See Section 2.3 for definition of variables. a Average displacement (mm), and velocity (mm/s). b Variables entered into the discriminant analysis.

Table 3 Dynamic balance variable by group (mean ± SD and 95% confidence intervals). Variablea

CAI (cm)

95% CI

Healthy

95% CI

P value

Anterior medial Medial Posterior medial

88.67 ± 6.73 89.11 ± 6.78 90.49 ± 7.35

85.87–91.47 86.27–91.95 87.41–93.57

88.90 ± 6.10 91.10 ± 7.08 95.12 ± 8.24

86.29–91.51 88.06–94.14 91.59–98.65

0.91 0.35 0.14

a

Reach distance (cm) normalized to subject leg length.

Table 4 Motoneuron pool excitability variables by group (mean ± SD and 95% confidence intervals). Variable

CAI

95% CI

Healthy

95% CI

P value

Hmax/Mmax ratio Double-legged PRD (%) Double-legged RI (%) Single-legged PRD (%) Single-legged RI (%)

0.54 ± 0.053 84.10 ± 11.81 90.75 ± 5.32 83.1 ± 1.08 89.80 ± 3.90

0.52–0.56 79.16–89.04 86.12–95.38 78.55–87.81 88.17–91.42

0.56 ± 0.13 85.20 ± 11.80 83.40 ± 12.02 70.79 ± 15.50 83.91 ± 8.76

0.51–0.61 80.14–90.26 78.26–88.54 64.17–77.41 80.17–87.65

0.58 0.76 0.013a 0.004a 0.006a

a

Variables entered into the discriminant analysis. See Section 2.3 for definition of variables.

Table 5 Joint position sense variables by group (mean ± SD and 95% confidence intervals). Variable

CAI (°)

95% CI

Healthy (°)

95% CI

P value

Plantarflexion: CE Plantarflexion: AE Plantarflexion: VE Inversion: CE Inversion: AE Inversion: VE

2.28 ± 3.45 4.62 ± 1.7 3.46 ± 1.86 1.70 ± 3.53 4.20 ± 2.22 3.5 ± 1.65

3.73–0.83 3.91–5.33 2.68–4.24 0.23–3.17 3.28–5.12 2.88–4.26

0.70 ± 5.35 4.61 ± 2.04 2.97 ± 0.95 0.64 ± 2.22 3.48 ± 1.58 3.32 ± 1.37

2.99–1.59 3.73–5.49 2.55–3.38 0.30–1.58 2.81–4.15 2.73–3.91

0.25 0.98 0.29 0.25 0.23 0.59

See Section 2.3 for definition of variables.

rior/posterior directions. Additionally, this movement occurred at an increased velocity (Table 2). Increases in displacement or velocity represent a less stable stance; medial/lateral CoP average displacement [t(38) = 11.07, P = 0.002] and velocity [t(41) = 10.33, P = 0.003]; anterior/posterior CoP average displacement [t(38) = 3.88, P = 0.056] and velocity [t(38) = 4.05, P = 0.051]. There were significant differences between the two groups on the remaining static balance variables {RMS ML DISP [t(38) = 0.462], RMS AP DISP [t(38) = 1.91], RMS total DISP [t(38) = 1.02], RMS DISP [t(38) = 1.81], Total VEL [t(38) = 1.02]}. 3.1.2. Dynamic balance There were no significant differences found between the two groups on the linear combination of the Star Excursion Balance Test dependent measures [F(3, 39) = 1.32, P = 0.092]. Univariate Ftests revealed no differences in the distance the CAI and healthy

groups could reach in any of the three directions tested (Table 3): anterior medial [t(41) = 0.014], medial [t(41) = 0.89], posterior medial [t(41) = 2.33]. 3.1.3. Motoneuron pool excitability Overall significant differences were found between the two groups (Table 5) on the linear combination of all H-reflex measures: [F(5, 37) = 4.909, P = 0.002]. Follow-up univariate F-tests revealed significant differences in the way the motoneuron pool is modulated in CAI and healthy participants (Table 4). Three variables were found to be significant and were entered into the discriminant function analysis: recurrent inhibition (post-synaptic) in double-legged stance [t(41) = 6.82, P = 0.013] and single-legged stance [t(41) = 8.25, P = 0.006], and paired reflex depression (presynaptic) in a single-legged stance [t(41) = 9.15, P = 0.004]. Univariate F-tests also revealed no differences between the two groups on

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the remaining H-reflex variables: H/M 2 legged [t(41) = 0.31] and paired reflex depression in a double-legged stance [t(41) = 0.094]. 3.1.4. Joint kinesthesia No differences between CAI and healthy participants were found on the linear combination of all joint position sense measures [F(6, 37) = .998]. Moreover, the univariate F-tests also revealed no significant difference between the two groups on any of the joint position sense variables (Table 5): plantarflexion constant error [t(41) = 1.34], plantarflexion absolute error [t(41) = 0.001], plantarflexion variable error [t(41) = 1.17], inversion constant error [t(41) = 1.37], inversion absolute error [t(41) = 1.49], inversion variable error [t(41) = 0.89]. Thus, the two groups were equally able to replicate the inversion and plantarflexion joint angles indicating a satisfactory awareness of the ankle position. 3.2. Discriminant function analysis The discriminant function analysis data identifying the variables most related to CAI group membership can be found in Table 6. The seven dependent variables found to be significant during data reduction (medial/lateral displacement and velocity, anterior/posterior displacement and velocity, double- and singlelegged recurrent inhibition, and single-legged paired reflex depression) were used as indicators in the discriminant function analysis to assess the ability of these variables to best classify participants by group (CAI and healthy). Utilizing these seven variables as indicators, the overall discriminant analysis model revealed a significant differentiation between the CAI and healthy ankle groups [Wilks’ K = 0.536 v2(7, N = 43) = 22.118, P = 0.002; canonical correlation = 0.681]. The canonical discriminant function coefficients and classification function coefficients (Table 6) indicate that the medial/lateral and anterior/posterior velocity variables were the strongest contributors to the model, followed by medial/lateral and anterior/ posterior displacement. The resulting model correctly classified 76% of the healthy participants and 86% of the CAI participants. Overall, the discriminant analysis correctly classified group membership in 81% of the total cases. 4. Discussion Multiple measurements and techniques are currently being used to study factors contributing to chronic ankle instability. The objective of this work was to determine the optimal combination of sensorimotor variables within four sensorimotor constructs (static balance, dynamic balance, motoneuron pool excitability, and joint kinesthesia) that would discriminate between CAI and healthy ankles. This study revealed a combination of seven variables that were able to classify over 86% of CAI participants. These seven variables represent two constructs, static balance and motorneuron pool excitability, possibly indicating that these factors may be more important to consider in the development of CAI research and rehabilitation and prevention protocols.

Table 6 Discriminant analysis classification results: predicted group membership. Group

Healthy

CAI

Healthy CAI

Number of participants correctly classified 16 5 3 19

21 22

Healthy CAI

Percentage of participants correctly classified 76.2 23.8 13.6 86.4

100 100

81.4% of original grouped cases correctly classified.

Total

4.1. Static balance Multiple studies examining CAI participants have found deficits in static balance measures (Gribble et al., 2004; Riemann, 2002). Thus, out of the seven variables found to be significant it is not surprising that four (medial/lateral average displacement, medial/ lateral average velocity, anterior/posterior average displacement, anterior/posterior average velocity) were postural control measures. Examination of both the canonical and classification coefficients in Table 6 reveals that the static balance measures exhibited the most influence on the group classification. Medial/ lateral velocity displayed the strongest effect, followed by anterior/posterior velocity, medial/lateral average displacement and anterior/posterior average displacement. The results in the current study are in agreement with previously published work in this area suggesting that participants with CAI exhibit increased static balance instability (Riemann, 2002; Hertel and Olmsted-Kramer, 2007). Results indicating the strong influence of CAI on postural control measures have important clinical implications. Balance training is typically a component of rehabilitation programs designed for individuals with CAI. As postural control measures are the strongest indicators of CAI group, rehabilitation programs can be modified to focus on this deficit. Moreover, several works (Tropp et al., 1985; Eils and Rosenbaum, 2001; Ross et al., 2007) reinforces the prophylactic use of balance training in the prevention of future ankle sprains in individuals with acute ankle sprains and the improvement of balance measures in participants with CAI stability. 4.2. Dynamic balance In the current study the modified version of the Star Excursion Balance Test was utilized by testing in only the anteromedial, medial and posteromedial directions (Hertel et al., 2006). The dynamic balance measures revealed no differences between the CAI and healthy groups. A great deal of variability was found within subject groups. Additionally, confidence intervals were wider than other variables indicating a somewhat less precise measurement, as would be expected in a more functional measure. Past research has found CAI participants to have a deficit in reach length during dynamic balance tests as compared to participants with healthy ankles. (Hertel et al., 2006; Olmsted et al., 2002) Dynamic postural control tests must by definition involve several neuromuscular systems. Factors such as muscle strength, flexibility and activity level are probable contributors to Star Excursion Balance Test results. The variety of activity and disability levels in our test groups (Table 1) may have been a confounding factor in this test. The mean disability level for the CAI participants was 81% with a standard deviation of 13.1%. This is a wide variability in disability level, and further demonstrates the seven variables that were added into the discriminant function analysis were robust for a range in disability. Testing on very homogeneous populations may be more likely to produce significant differences between CAI and healthy groups. The activity levels of the participants were not significantly different between the CAI and healthy groups. Interestingly, there was a trend towards a greater number of years of sport competition in the CAI group. The high level of activity maintained by many of the CAI subjects indicates these participants are developing coping mechanisms to deal with their disability, and except in the most extreme cases, are continuing to maintain an active lifestyle. However, participants reported changing the type of activities (i.e. from running to swimming) in which they participate in response to their CAI. Future work should examine if the Star Excursion Balance Test can be used to differentiate between different levels of CAI disability; and if this measure can discriminate between those successfully coping with this disability and those who have not developed these adaptive mechanisms.

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4.3. Motoneuron pool excitability The current investigation found three motoneuron pool excitability measures (double-legged and single-legged RI, and singlelegged paired reflex depression) to be significant indicators of group membership (Table 6), although they contributed less to the model. These findings demonstrate that motoneuron pool excitability varied between the healthy and CAI subject groups. While several groups have investigated neuromuscular factors related to CAI the assessment of motoneuron pool excitability is just beginning to be investigated in CAI research. (McVey et al., 2005; Sefton et al., 2008) Recent work in this area examining the influence of CAI on spinal reflex measures found differences in Hmax/ Mmax ratio between CAI and healthy ankles (McVey et al., 2005). Interestingly, in the current study the Hmax/Mmax ratio was the least significant and most variable of all the motor neuron excitability measures, and thus not included in the discriminant function analysis. Assessment of activation history and post-synaptic inhibition were included in this study as these measures have been found to be modulated in the spinal cord in response to changes in surface stability and ankle bracing (Sefton et al., 2006, 2007). Thus, these measures may be important in elucidating the mechanisms behind how these two groups differ in their response to environmental challenges such as responding to unstable surfaces a maintaining an upright stance. Although the H-reflex measures were found to be of less importance than the static balance measures in determining group membership, the importance of these measures in the overall classification is intriguing. A recent review (Hertel, 2008) summarizing current research on the relationship between the sensorimotor system and CAI concluded changes in motoneuron pool excitability may be involved in muscle activation deficits and dysfunction in muscles that cross the ankle joint and in the proximal leg muscles. Results of the current study support this conclusion. Additionally, the delayed reaction times in stretch reflexes (Konradsen and Ravn, 1990; Lofvenberg et al., 1995; Vaes et al., 2002) often reported in CAI subjects may also be related to changes in spinal level responses. Thus, many factors likely contribute to the sensorimotor involvement in CAI (i.e. cutaneous, muscle/tendon and articular receptors, gamma motoneurons, descending input). However, it may be that changes in motoneuron pool excitability, through pre- or post-synaptic modulation, act as a central mechanism to modify the overall spinal cord response to the combination of these afferent inputs. Finally, research has found that individuals unable to modulate segmental spinal reflexes also had poor static balance measures (Koceja et al., 1995; Mynark and Koceja, 2002). After participation in a reflex training program, the individuals demonstrated improved static balance measures (Trimble and Koceja, 1994). This and other studies have demonstrated that reflexes can be trained (Wolpaw and Tennissen, 2001; Granacher et al., 2006), and that this training can result in changes in other sensorimotor measures. Current research in our laboratory is investigating the link between changes in segmental spinal reflex modulation and current clinical rehabilitation protocols. As we learn more about how reflex modulation influences these other measures we may be able to develop improved clinical rehabilitation and prevention programs for CAI and other disabilities. 4.4. Joint kinesthesia The exclusion of any joint position sense variables as indicators in the discriminant analysis is not completely unexpected, as previous work in this area has reported conflicting results (Boyle and Negus, 1998; Konradsen and Beynnon, 2000; Konradsen, 2002; Brown et al., 2004). The current study utilized active reproduction of a passively presented joint angle to stimulate both joint recep-

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tors and muscle receptors. Damage to mechanoreceptors or ligaments after a lateral ankle sprain are thought to result in a pathogenic deficit in position sense and an increased risk of stumbling and ankle re-injury. (Freeman et al., 1965; Konradsen, 2002) Both CAI and healthy participants tended to underestimate the plantarflexion position angle and overestimate the inversion position angle (Table 5). The width of the confidence intervals for the joint position sense measures is consistent and relatively small, indicating good precision and consistency of the measurements. However, expected changes in joint position sense due to CAI have been noted to be on the order of only a few degrees and may have been masked by within-group variability. Decreased accuracy in detecting active and passive joint position sense at a position close to maximal inversion in participants with chronically unstable ankles has been found (Willems et al., 2002). However, no differences were found when comparing chronically unstable and stable ankles in passive and active replication of eversion and inversion (Konradsen, 2002). 5. Summary To our knowledge, this was the first study to investigate the relationship between CAI and sensorimotor function using a multivariate approach. This study evaluated a wide range of common sensorimotor measures in their ability to distinguish between healthy and CAI participants. The combination of variables found to determine group membership represented two of the four sensorimotor constructs examined. Seven of the 25 variables tested correctly categorize over 86% of CAI participants. The necessity of utilizing a combination of two different aspects of sensorimotor function demonstrates the complexity of the CAI. These results further suggest that these seven measures can classify CAI participants across a wide range of disability levels. Specifically, of these constructs, postural control measures were found to be the most influential component of classification. Interestingly, H-reflex measures comprised three of the seven total indicators that were found to significantly classify group membership. These results suggest that future studies should continue to focus on postural control and motoneuron pool excitability measures in furthering our understanding of the relationship between sensorimotor function deficits and CAI. This will ultimately aid in further enhancing prevention techniques and rehabilitation interventions in managing this common ankle pathology. Conflict of interest There are no conflicts of interest. Acknowledgement No financial support was received for the completion of this project. References Beynnon, B.D., Murphy, D.F., Alosa, D.M., 2002. Predictive factors for lateral ankle sprains: a literature review. J. Athl. Train. 37, 376–380. Boyle, J., Negus, V., 1998. Joint position sense in the recurrently sprained ankle. Aust. J. Physiother. 44, 159–163. Brown, C., Ross, S., Mynark, R.G., Guskiewicz, K., 2004. Assessing functional ankle instability with joint position sense, time to stabilization, and electromyography. J. Sport Rehabil. 13, 122–134. Brown, T.D., Johnston, R.C., Saltzman, C.L., Marsh, J.L., Buckwalter, J.A., 2006. Posttraumatic osteoarthritis: a first estimate of incidence, prevalence, and burden of disease. J. Orthop. Trauma 20, 739–744. Bussel, B., Pierrot-Deseilligny, E., 1977. Inhibition of human motoneurons, probably of Renshaw origin, elicited by an orthodromic motor discharge. J. Physiol. 269, 319–339.

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