JCLB-03739; No of Pages 7 Clinical Biomechanics xxx (2014) xxx–xxx

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Frontal and transverse plane hip kinematics and gluteus maximus recruitment correlate with frontal plane knee kinematics during single-leg squat tests in women John H. Hollman ⁎, Christy M. Galardi, I-Hsuan Lin, Brandon C. Voth, Crystal L. Whitmarsh Program in Physical Therapy, the Department of Physical Medicine & Rehabilitation and Sports Medicine Center, Mayo Clinic, Rochester, MN, USA

a r t i c l e

i n f o

Article history: Received 2 August 2013 Accepted 30 December 2013 Keywords: Lower extremity Hip Knee Biomechanics Electromyography Muscle strength

a b s t r a c t Background: Hip muscle dysfunction may be associated with knee valgus that contributes to problems like patellofemoral pain syndrome. The purpose of this study was to (1) compare knee and hip kinematics and hip muscle strength and recruitment between “good” and “poor” performers on a single-leg squat test developed to assess hip muscle dysfunction and (2) examine relationships between hip muscle strength, recruitment and frontal plane knee kinematics to see which variables correlated with knee valgus during the test. Methods: Forty-one active women classified via visual rating as “good” or “poor” performers on the test participated. Participants completed 5-repetition single-leg squat tests. Isometric hip extension and abduction strength, gluteus maximus and gluteus medius recruitment, and 3-dimensional hip and knee kinematics during the test were compared between groups and examined for their association with frontal plane knee motion. Findings: “Poor” performers completed the test with more hip adduction (mean difference = 7.6°) and flexion (mean difference = 6.3°) than “good” performers. No differences in knee kinematics, hip strength or hip muscle recruitment occurred. However, the secondary findings indicated that increased medial hip rotation (partial r = 0.94) and adduction (partial r = 0.42) and decreased gluteus maximus recruitment (partial r = 0.35) correlated with increased knee valgus. Interpretation: Whereas hip muscle function and knee kinematics did not differ between groups as we'd hypothesized, frontal plane knee motion correlated with transverse and frontal plane hip motions and with gluteus maximus recruitment. Gluteus maximus recruitment may modulate frontal plane knee kinematics during single-leg squats. © 2014 Elsevier Ltd. All rights reserved.

1. Introduction The prevalence of patellofemoral pain syndrome, characterized by peri- or retropatellar pain, in active adolescent and young adult women is approximately 15% (Boling et al., 2010; Myer et al., 2010). The condition is commonly aggravated by squatting, kneeling, traversing stairs and running and therefore affects one's ability to perform athletic activities (Dixit et al., 2007). Recent evidence suggests hip muscle function is impaired in individuals with patellofemoral pain syndrome and may be a risk factor for its development. Prins and Van Der Wurff (2009) reported that hip abduction, external rotation and extension strength are all diminished in women with patellofemoral pain syndrome compared with asymptomatic individuals. Impaired hip abduction and external rotation strength have also been identified as risk factors for the condition in adolescent female runners. If hip abduction and external rotation strength are impaired, excessive adduction and medial rotation during weightbearing activities may be induced ⁎ Corresponding author at: Mayo Clinic, Program in Physical Therapy, Siebens 11, 200 First Street SW, Rochester, MN 55905, USA. E-mail address: [email protected] (J.H. Hollman).

(Finnoff et al., 2011; Fredericson et al., 2000; Fulkerson, 2002; Fulkerson and Arendt, 2000; Ireland et al., 2003), which concomitantly increases knee valgus that is theorized to contribute to patellofemoral pain syndrome (Powers, 2003). Impaired neuromuscular control may also contribute to movements that trigger patellofemoral pain syndrome. Neuromuscular control– defined as the maintenance of functional joint stability through subconscious muscle recruitment in response to joint movements and loading conditions (Riemann and Lephart, 2002)–is reflected by electromyograms (EMG) that quantify neural input to muscles. Gluteus medius recruitment, for example, is delayed in women with patellofemoral pain syndrome during stair-stepping tasks compared with asymptomatic individuals (Brindle et al., 2003; Cowan et al., 2009). Moreover, peak gluteus maximus recruitment correlates negatively with knee valgus during single leg squats (Hollman et al., 2009). These relationships make sense because the gluteus medius abducts and the gluteus maximus extends and laterally rotates the hip. Recruiting these muscles during weightbearing tasks may limit hip adduction or medial rotation, thereby limiting knee valgus, implying that altered neuromuscular control at the hip may influence hip and knee kinematics and contribute to patellofemoral pain syndrome.

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Please cite this article as: Hollman, J.H., et al., Frontal and transverse plane hip kinematics and gluteus maximus recruitment correlate with frontal plane knee kinematics during single-leg squat test..., Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2013.12.017

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To understand how hip muscle dysfunction may be associated with impaired movements that contribute to patellofemoral pain syndrome, Crossley et al. (2011) developed a rating system for assessing single-leg squat performance in healthy adults based on balance and perturbations as well as the trunk, pelvis, hip and knee posture (Table 1). Participants classified as “poor” performers with hip dysfunction had delayed gluteus medius onset and weaker hip abduction strength than those rated as “good” performers (Crossley et al., 2011). The investigators did not examine the magnitude of gluteus medius recruitment during the test. Furthermore, despite the potential influences of gluteus maximus function on hip and knee kinematics as described above, the investigators did not examine hip extension strength or gluteus maximus recruitment, nor did they examine 3-dimensional hip and knee kinematics to validate their rating system. The purposes of this study, therefore, were twofold. First, we compared hip and knee kinematics and hip muscle function–including hip extension and abduction strength and magnitudes of gluteus maximus and gluteus medius recruitment–between “good” and “poor” performers on the single-leg squat test. Second, we examined the relationships between hip strength, gluteus maximus and gluteus medius recruitment and hip and knee kinematics to see which variables most strongly predicted the magnitude of knee valgus during the test. We hypothesized that knee valgus, hip adduction and medial hip rotation would be greater– and hip extensor strength and gluteus maximus recruitment would be lower–in women who demonstrated poor performance during the single-leg squat test. Third, we hypothesized that reduced hip extension strength and gluteus maximus recruitment would be associated with increased knee valgus. 2. Methods 2.1. Participants Active, healthy active women 18 to 36 years old were recruited. Inclusion criteria included the ability to walk, run, jump, and squat without knee pain. Exclusion criteria included history of knee ligament injury, patella dislocation, knee pain within 6 months of testing, or any suspected pathology of the knee or hip that compromised safety during Table 1 Rating criteria for the single-leg squat test. Performance was operationally defined as “Good” when participants performed the test over 5 repetitions with 3 or fewer departures from the Crossley et al. (2011) criteria for good performance; as “Fair” performance with 4–7 departures from the criteria; and as “Poor” performance when participants performed the test with 7 or more departures from the criteria. Criterion Overall impression across 5 squats Ability to maintain balance Perturbations of the person Depth of the squat Speed of the squat Trunk posture Trunk/thoracic lateral deviation or shift Trunk/thoracic rotation Trunk/thoracic lateral flexion Trunk/thoracic forward flexion Pelvis posture Pelvic lateral deviation Pelvic rotation Pelvic tilt (take note of depth of squat) Hip joint Hip adduction Hip medial rotation Knee joint Apparent knee valgus Knee position relative to foot position

To be rated “Good” Participant does not lose balance Movement is performed smoothly Performed to at least 60° of knee flexion Performed at approximately 1 per 2 s No trunk/thoracic lateral deviation or shift No trunk/thoracic rotation No trunk/thoracic lateral flexion No trunk/thoracic forward flexion No pelvic lateral deviation No pelvic rotation No pelvic tilt No hip adduction No hip medial rotation No apparent knee valgus Center of knee remains over center of foot

Note: adapted from Crossley et al. (2011) with permission.

testing. Participants were screened for eligibility with a knee pain history questionnaire; with Lachman, posterior drawer, valgus and varus stress tests for ligament stability; a patellar apprehension test for patellofemoral instability; and palpation for joint line tenderness indicative of meniscal injury. A single investigator performed the screening exam. All participants provided written informed consent. The study was approved by the Mayo Foundation Institutional Review Board. Since estimates of hip extension strength and variance are more readily available in the literature than are estimates of hip and knee kinematics or hip muscle recruitment during single-leg squats, we conducted a power analysis based on previously published hip strength data. Hip extension strength in healthy, adult women is approximately 43% body weight (% BW) (Hollman et al., 2012). Detecting a 10% BW difference in hip extension strength, assuming a standard deviation of 11% BW within groups, at a statistical power of 0.80 required a sample size of 42 participants (21 per group). 2.2. Instrumentation Data collected included participants' physical activity levels, hip extension and abduction muscle strength, gluteus maximus and gluteus medius recruitment and hip and knee kinematics during single-leg squats. Since physical activity may influence dynamic performance, participants completed a 7-question form of the International Physical Activity Questionnaire (Craig et al., 2003). Performance of single-leg squats during an initial screening exam was recorded with a Kodak Zi8 digital video camera (Eastman Kodak Company, Rochester, New York, USA). Hip extension and abduction strength were measured with a MicroFET2 dynamometer (Hoggan Health Industries, Inc., West Jordan, Utah, USA). EMGs were acquired at 1000 Hz through a 16-bit NI-DAQ PCI-6220 analog-to-digital card (National Instruments Corporation, Austin, Texas, USA) with Bagnoli DE-3.1 double-differential bipolar surface electrodes and a Bagnoli-16 amplifier (Delsys Inc., Boston, Massachusetts, USA) having a common mode rejection ratio of 92 dB at 60 Hz, input impedance N 1015 ohms, estimated noise ≤ 1.2 μV and overall amplification of 100–10,000 V/V. Electrodes were constructed of 10-mm × 1-mm silver bars, spaced 10-mm apart within preamplifiers having a gain of 10 V/V. Kinematic data were acquired at 100 Hz with a Vicon MX system and five MX20 + cameras (Vicon Motion Systems, Oxford, United Kingdom). Vicon Nexus software was used to quantify lower extremity kinematics. 2.3. Procedures Following a physical exam to assess eligibility for enrolling in the study, the single-leg squat test was demonstrated. Participants crossed their arms in front of their chest and performed single-leg squats with their dominant leg (preferred kicking leg) five times consecutively from a 20-cm high platform at a rate of approximately 1 squat per 2 s, as described by Crossley et al. (2011). Participants performed 3 practice squats to familiarize themselves with the task before their performance was formally tested. In contrast to methods used by Crossley et al. (2011), who used standardized footwear, our participants performed the test with bare feet to eliminate potential effects of footwear on lower extremity mechanics. Test performance was recorded with the digital video camera placed on a tripod 3-m anterior to the participant and downloaded onto a Dell Optiplex 755 desktop computer. Four investigators independently reviewed the video footage and rated each participant's performance as “good,” “fair” or “poor” based on Crossley et al.'s (2011) criteria (Table 1). Agreement by three or more raters was required to categorize performance as “good” or “poor.” On analysis of the investigators' ratings, overall agreement was 70% and the kappa coefficient for multiple raters was equal to 0.55, slightly lower than kappa coefficients from 0.60 to 0.80 reported by Crossley et al. (2011).

Please cite this article as: Hollman, J.H., et al., Frontal and transverse plane hip kinematics and gluteus maximus recruitment correlate with frontal plane knee kinematics during single-leg squat test..., Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2013.12.017

J.H. Hollman et al. / Clinical Biomechanics xxx (2014) xxx–xxx

Fig. 1. Markers were placed on anatomic landmarks in accordance with Vicon's Plug-in Gait marker set at the posterior and anterior superior iliac spines, the lateral midline and lateral epicondyle of the thighs, the lateral midline and lateral malleoli of the shanks, posterior aspect of the calcanei and dorsum of the 2nd metatarsophalangeal joints.

Participants classified as “good” and “poor” performers returned within one week for repeat testing. Since there is evidence functional lower extremity performance tests like the single-leg squat test are performed reliably from week to week, participants were not re-classified at the second visit (Levinger et al., 2007; Whatman et al., 2011). At that visit, hip extension and abduction strength were measured with the MicroFET2™ dynamometer during isometric tests in which participants exerted maximum force against externally applied resistance. Hip extension strength was tested with participants in prone and the knee flexed to approximately 90° and abduction strength was tested with participants in side-lying, which are standardized positions for assessing extension and abduction strength, respectively (Hislop and Montgomery, 2007). The dynamometer was stabilized at the distal thigh by a strapping belt and an examiner's hand. Two repetitions were performed and the maximum force was recorded and expressed as a percentage of the participant's body weight (% BW). Each contraction was maintained for 5 s and approximately 30 s of rest between repetitions was provided. EMG data were acquired simultaneously to establish the amplitude of maximum voluntary isometric contractions (MVIC) to which subsequent data were normalized. Prior to collecting EMGs, the participant's skin was cleansed with alcohol. Electrodes were affixed at standardized locations in parallel with the muscles' respective lines of action (Criswell, 2011). One electrode pair was placed over the gluteus maximus at one-half the distance between the sacrum and greater trochanter. The second electrode pair was placed over the gluteus medius at one-third the distance between the iliac crest and greater trochanter. The reference electrode was placed on the tibial crest. Sixteen retroreflective markers were then placed on anatomic landmarks to generate the model from which kinematic data were obtained (Fig. 1). Additional measurements taken to facilitate kinematic measurements with Vicon's Plug-in-Gait model included participant height, leg lengths (ASIS to medial malleolus), inter-ASIS distance, inter-epicondylar distance at the distal thighs and intermalleolar distance at the distal shanks. Participants then performed the 5-repetition single-leg squat test while kinematic and EMG data were acquired.

Volunteers for study (n = 64) Excluded (n = 7) • Reported hip or knee pain in previous 6 months during at least two of the following activities: running, jumping, cutting, ascending or descending stairs, squatting or prolonged sitting (n=4) • Reported history of ligament injury, patella dislocation, knee surgery or other significant trauma to lower extremity (n = 3) Met inclusion criteria, screened for singleleg squat performance (n = 57)

Classified as “Good” performer (n = 21)

Classified as “Fair” performer (n = 15)

Classified as “Poor” performer (n = 21) Excluded (n = 1) • Missing marker data during kinematic analysis

Completed testing (n = 21)

3

Completed testing (n = 20) Fig. 2. Flow chart of recruitment.

Please cite this article as: Hollman, J.H., et al., Frontal and transverse plane hip kinematics and gluteus maximus recruitment correlate with frontal plane knee kinematics during single-leg squat test..., Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2013.12.017

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Table 2 Descriptive data in the “good” and “poor” performance groups.

Demographic/anthropometric Age (years) Height (cm) Mass (kg) Body mass index (kg · m−2) Physical activity (MET · min · wk−1) Low activity (b600) Moderate activity (600–3000) High activity (N3000) Hip strength (% body weight) Abduction Extension Hip kinematics (°) Flexion Adduction Medial rotation Knee kinematics (°) Flexion Varus Medial rotation EMG magnitude (% MVIC) Gluteus maximus Gluteus medius

“Good” group n = 21

“Poor” group n = 20

23.8 (1.8) 168.2 (7.1) 61.3 (8.2) 21.6 (2.0)

24.4 (2.9) 167.1 (7.1) 61.3 (9.6) 21.9 (2.3)

95% CI of the difference

P

−1.0 to 2.0 −5.6 to 3.4 −5.7 to 5.6 −1.1 to 1.6

0.473 0.624 0.989 0.690

0 (0%) 15 (71%) 6 (29%)

0 (0%) 14 (67%) 6 (33%)

52.6 (11.9) 40.8 (10.8)

54.0 (11.3) 43.6 (9.9)

−5.9 to 8.7 −3.7 to 9.4

0.389 0.706

42.6 (12.6) 13.4 (4.6) 2.0 (14.1)

50.1 (8.5) 19.7 (5.3) 9.0 (9.2)

0.8 to 14.4 3.2 to 9.4 −0.6 to 14.6

0.030⁎ b0.001⁎ 0.068

64.0 (8.3) 4.2 (12.2) 6.6 (12.9)

64.0 (10.3) 8.6 (7.2) 7.7 (12.0)

−6.0 to 9.0 −2.1 to 10.7 −6.8 to 9.0

0.985 0.181 0.774

23.8 (11.7) 28.3 (17.8)

20.9 (10.7) 26.0 (16.1)

0.920

−10.0 to 4.2 −13.0 to 8.4

0.413 0.666

Continuous variables are presented as mean (SD); ordinal data are presented as discrete numbers in each category (%). ⁎ Statistically significant difference between groups (P b 0.05).

We then computed mean joint angles and mean EMG amplitudes for each individual across the five repetitions of the single-leg squat test.

2.4. Data processing Marker trajectories were filtered with a Woltring quintic spline filter (20-mm mean square error). Hip and knee joint angles were calculated with Cardan angles using Vicon's Nexus software, whereby rotations about orthogonal local axes derived from a neutral standing trial corresponded to flexion/extension in the sagittal plane, adduction/ abduction (varus/valgus) in the frontal plane and medial/lateral rotation in the transverse plane, respectively. Raw EMGs were band-pass filtered between 20 and 450 Hz with a 4th order Butterworth filter and analyzed with Delsys EMGworks 3.7.2.0 software. We processed EMGs with a root mean square algorithm over 250-ms time constants with sliding windows and normalized data from the gluteus maximus and gluteus medius to their respective MVIC trials. We analyzed 3-dimensional hip and knee angles at the completion of the eccentric phase of each squat, defined as the point at which maximum knee flexion was reached. For EMG data, we examined mean amplitudes over 500-ms epochs preceding maximum knee flexion.

2.5. Statistical analysis Descriptive data were calculated for anthropometric and demographic characteristics (height, weight, body mass index, and age), hip extension and abduction strength, hip and knee joint angles and gluteus maximus and gluteus medius recruitment during the test. Differences between “good” and “poor” performers were examined with independent t-tests for parametric data and χ2 tests for ordinal data. Second, we used multiple regression to examine relationships among frontal plane knee angles and 3-dimensional hip angles; gluteus maximus and gluteus medius recruitment; and isometric hip extension and abduction strength. We analyzed R2 values and partial correlation coefficients to examine the relationship among each predictor variable with frontal plane knee motion, controlling for other variables in the analysis.

Table 3 Summary of hierarchical regression analysis on the frontal plane knee angle. Variable Constant Hip angles (°) Frontal plane Sagittal plane Transverse plane Hip strength (% BW) Extension Abduction Muscle recruitment (% MVIC) Gluteus maximus Gluteus medius

R2

ΔR2

β

r

partial r

−0.17 0.07 0.99

0.03 −0.10 0.92

−0.42 0.18 0.94

0.07 (−0.07 to 0.22) 0.14 (−0.03 to 0.31)

0.07 0.16

−0.01 −0.17

0.17 0.28

0.13 (0.01 to 0.26) 0.08 (−0.01 to 0.17)

0.15 0.13

−0.06 0.21

0.35 0.29

B (95% CI)

P

−11.86 0.865

0.865 −0.29 (−0.52 to −0.07) 0.06 (−0.05 to 0.17) 0.83 (0.72 to 0.93)

0.873

0.895

0.007

0.022

b0.01 0.01 0.29 b0.01 0.39 0.32 0.10 0.04 0.04 0.09

Notes: R2 = cumulative proportion of variance in the frontal plane knee angle accounted for by variance in the independent variable; ΔR2 = change in R2; B = unstandardized regression coefficient (with 95% confidence interval); β = standardized regression coefficient; r = zero-order Pearson product-moment correlation coefficient between the independent variable and frontal plane knee angle; partial r = partial correlation between the independent variable and frontal plane knee angle, controlling for other independent variables; P = significance of ΔR2 or of B or β or the partial r. Using unstandardized regression coefficients, the regression equation is represented as: Frontal plane knee angle (°) = −11.86°–0.29 (frontal plane hip angle [°]) + 0.83 (transverse plane hip angle [°]) + 0.13 (gluteus maximus recruitment [% MVIC]).

Please cite this article as: Hollman, J.H., et al., Frontal and transverse plane hip kinematics and gluteus maximus recruitment correlate with frontal plane knee kinematics during single-leg squat test..., Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2013.12.017

J.H. Hollman et al. / Clinical Biomechanics xxx (2014) xxx–xxx

4. Discussion We compared hip and knee kinematics as well as gluteus maximus and gluteus medius function between “good” and “poor” performers on a single-leg squat test. Findings partially supported our hypothesis that kinematic performance would differ between groups. “Poor” performers completed the task with more hip adduction than “good” performers, which supports the concept that frontal plane hip and pelvis control are key elements of performing a single-leg squat. In contrast to our hypothesis, knee angles at the termination of the squat did not differ between groups, which may imply the performance indicators of the single-leg squat test do not adequately cue the rater to assess knee motions. Alternatively, that finding may simply reflect the comprehensive nature of the rating scale. Assessing performance during the single-leg squat test involves the assessment of the trunk and pelvis posture in addition to a general assessment of balance and smoothness of movement. Participants who were rated poorly on those components of the test did not necessarily perform the test with increased magnitudes of knee valgus. Moreover, no differences in hip muscle performance occurred between “good” and “poor” performers. Neither extension nor abduction strength differed between groups, nor did gluteus maximus or gluteus medius recruitment. These findings contrast with findings that hip abduction strength was diminished and gluteus medius recruitment was delayed in “poor” performers (Crossley et al.,

Knee Valgus (degrees) Knee Varus

Fifty-seven individuals were screened before 21 were classified as “good” and 21 as “poor” performers on the test (Fig. 2). Secondary to technical issues, kinematic data from one participant classified as “poor” were not acquired so the final sample included 21 “good” and 20 “poor” performers. Participant height, weight, BMI, age and physical activity levels did not differ between “good” and “poor” performers (Table 2). Hip kinematics during the test differed between groups. “Poor” performers completed the task with more hip flexion (mean difference = 7.6°, 95% CI = 0.8° to 14.4°, P = 0.03) and adduction (mean difference = 6.3°, 95% CI = 3.2° to 9.4°, P b 0.01) and tended to have more medial hip rotation than “good” performers, though the difference was not statistically significant (mean difference = 7.0°, 95% CI = − 0.6° to 14.6°, P = 0.07). In contrast, knee kinematics, hip extension and abduction strength and gluteus maximus and gluteus medius recruitment did not differ between groups (Table 2). Variance in hip kinematics, hip strength and hip muscle recruitment accounted for nearly 90% of the variance in frontal plane knee kinematics (Table 3; R2 = 0.895, F7,33 = 40.20, P b 0.01). Three variables contributed significantly to that variance: transverse (partial r = 0.94, 95% CI = 0.89 to 0.97, P b 0.01) and frontal plane hip motion (partial r = − 0.42, 95% CI = − 0.13 to − 0.64, p = 0.03) and gluteus maximus recruitment (partial r = 0.35, 95% CI = 0.05 to 0.59, P = 0.04). Holding other variables constant, increased knee valgus correlated with increased medial hip rotation and adduction and with decreased gluteus maximus recruitment (Figs. 3 & 4).

30

A

20 10 0 -10

partial r = 0.939 p < 0.001

-20 -30 -25

-20

-15

-10

-5

0

5

10

15

20

25

Medial Hip Rotation (degrees) Lateral Hip Rotation Knee Valgus (degrees) Knee Varus

3. Results

2011). Methodological differences may potentially account for our contrasting results. We examined the magnitude of EMG recruitment in the gluteus maximus and gluteus medius, for example, whereas Crossley et al. (2011) only examined gluteus medius onset timing. Furthermore, differences in our use of the rating scale during the single-leg squat test may have influenced how participants were categorized. Crossley et al. (2011) used a consensus panel to categorize participants and did not assign points for specific components of the test but instead evaluated the performance as a whole. Their definition of a poor rating reflected a situation in which intervention would be necessary to address the hip muscle dysfunction. We believed using the number of movements that departed from a good standard of performance would be more objective, but it is possible our threshold for defining poor performance differed from the Crossley's threshold. We also examined relationships between frontal plane knee kinematics and hip muscle strength and neuromuscular control. Findings supported our hypothesis that variance in gluteus maximus function would be associated with variance in knee valgus during the test.

30

B

20 10 0 -10

partial r = -0.417 p = 0.013

-20 -30 5

10

15

20

25

Hip Adduction (degrees) Knee Valgus (degrees) Knee Varus

We analyzed data with SPSS 21.0 software (IBM Corporation, Armonk, New York, USA). The threshold for statistical significance for all statistical tests was α = 0.05. Diagnostic capabilities were used to assess whether assumptions of linearity, normality and homoscedasticity in the regression analysis were violated. Frontal plane knee data were linearly associated with the variables included in the regression. Kolmogorov–Smirnov tests indicated that the variables' distributions did not depart significantly from normal distributions. Plots of standardized residuals and standardized predicted values indicated the assumptions of homoscedasticity were not violated. Variance inflation factors were less than 3.0, suggesting that multicollinearity was not problematic.

5

30

C

20 10 0 -10

partial r = 0.345 p = 0.043

-20 -30 10

15

20

25

30

35

Gluteus Maximus Recruitment (% MVIC) Fig. 3. Partial correlations between frontal plane knee kinematics and transverse plane hip kinematics (A), frontal plane hip kinematics (B) and gluteus maximus recruitment (C) during the single-leg squat test.

Please cite this article as: Hollman, J.H., et al., Frontal and transverse plane hip kinematics and gluteus maximus recruitment correlate with frontal plane knee kinematics during single-leg squat test..., Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2013.12.017

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syndrome have shown generally positive outcomes (Khayambashi et al., 2012; Nakagawa et al., 2008), we hypothesize that promoting gluteus maximus function may be more relevant to limiting hip adduction, medial rotation and knee valgus during weightbearing tasks than promoting abduction strengthening. The second theoretical foundation is that muscle strength and neuromuscular control are distinct elements of physiologic function that influence motor performance. The motor task in our study was the single-leg squat. Performance was represented by the lower extremity kinematics. We sought to understand the extent to which hip extensor and abductor strength and neuromuscular control are associated with knee kinematics. The question is relevant because, while many investigators have reported hip strength deficits among individuals with patellofemoral pain syndrome (Bolgla et al., 2008; Finnoff et al., 2011; Fulkerson, 2002; Fulkerson and Arendt, 2000; Ireland et al., 2003), it is evident that hip strengthening in isolation is insufficient to induce changes in frontal plane knee motion (Herman et al., 2008; Mizner et al., 2008; Snyder et al., 2009). Mizner et al. (2008), for example, reported that instruction on jump-landing techniques produced changes in jump-landing performance among collegiate female athletes, but that hip abduction and extension strength were not associated with those improvements. Further, while hip strengthening produces stronger hip muscles, they affect frontal plane hip and knee kinematics minimally during running or jump-landing activities (Herman et al., 2008; Snyder et al., 2009). Feedback on motor performance induces greater changes in frontal plane kinematics than hip strengthening alone (Herman et al., 2009). Our finding that gluteus maximus recruitment during single-leg squats is associated with frontal plane knee motion supports conclusions that neuromuscular control rather than strength provides insight into how individuals perform dynamic lower extremity weightbearing motor tasks (Hollman et al.,

While transverse and frontal plane hip motions correlated most strongly with frontal plane knee motion, increased knee valgus also correlated with reduced gluteus maximus recruitment (Fig. 3C). The regression equation (Table 3) indicates that when other variables are held constant, a 1.2° increase in medial hip rotation, a 3.4° increase in hip adduction or a 7.7% MVIC reduction in gluteus maximus recruitment is associated with a 1° increase in knee valgus during the single-leg squat test. Assuming the magnitude of muscle recruitment represents an element of neuromuscular control (Pullman et al., 2000), an implication is that gluteus maximus neuromuscular control may modulate frontal plane knee motion during single-leg squats, though the findings may not generalize to all single-leg tasks. Two theoretical foundations support our findings. First, the gluteus maximus and gluteus medius may have distinct relationships with frontal plane knee kinematics. While Claiborne et al. (2006) reported an association between hip abduction strength and knee valgus and asserted that abduction strength controls frontal plane knee motion, our findings contradict that assertion. We believe there are plausible kinesiologic explanations for our findings. One may suggest that greater abduction strength can restrict hip adduction and knee valgus motions because the muscle stabilizes frontal plane hip motion (Khayambashi et al., 2012; Nakagawa et al., 2008). The pathomechanics about which clinicians are concerned, however, represents multi-planar phenomena in which excessive movements occur not only in the frontal but also in the transverse plane of motion. The gluteus medius is primarily a hip abductor but secondarily assists medial rotation. Its medial rotation moment arm increases as the hip flexes, particularly beyond 30° (Delp et al., 1999). Per our findings, the hip flexes at 40–50° during the single-leg squat. An excessively strong or overly-recruited gluteus medius may act not to prevent hip adduction but rather to exacerbate medial hip rotation that is coupled to adduction. Even though trials of hip abduction strengthening for patellofemoral pain

Knee Flexion (°)

80 70 60

50 40

30 20

30 20

10 0

10 0

15 10

2

4

6

8

10

12

14

16

2

4

6

8

10

12

14

2

4

6

8

10

12

14

2

4

6

8

10

12

14

E

10 5

0

0

-5

-5

-10

-10

-15

-15 0

Gluteus Maximus EMG (% MVIC)

0 15

B

5

40

D

70 60

50 40

0

Knee Valgus (°) Knee Varus

80

A

2

4

6

8

10

12

14

0

16 40

C

30

30

20

20

10

10

0

F

0 0

2

4

6

8

10

Time (s)

12

14

16

0

Time (s)

Fig. 4. Representative data from a participant who performed the single-leg squat test with neutral to varus frontal plane knee motion (A–C) and a participant with valgus frontal plane knee motion (D–F). Note the contrast in gluteus maximus recruitment between the two participants. The vertical dashed line segments indicate the times at which peak knee flexion occurred.

Please cite this article as: Hollman, J.H., et al., Frontal and transverse plane hip kinematics and gluteus maximus recruitment correlate with frontal plane knee kinematics during single-leg squat test..., Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2013.12.017

J.H. Hollman et al. / Clinical Biomechanics xxx (2014) xxx–xxx

2009, 2012; Zazulak et al., 2005). In healthy individuals, one's recruitment of a muscle during a motor task may be more relevant to physiologic function and task performance than is absolute muscle strength. We acknowledge several limitations in this study. Our inter-rater agreement for classifying performance on the single-leg squat test was moderately strong (kappa = 0.55) though lower than comparable coefficients reported by developers of the rating system (Crossley et al., 2011). If participants were misclassified as “good” or “poor” performers on the test or if they performed differently during the testing session, that may potentially account for the lack of group differences we'd hypothesized may occur. Second, it's possible that our measurements were not most representative of hip muscle function. Muscle strength, for example, is greatest during eccentric contractions. We analyzed eccentric phases of the single-leg squat. Eccentric strength tests may have provided greater insight about relationships between knee kinematics and hip extension and abduction strength. Similarly, other measures of neuromuscular control such as EMG onset, peak recruitment or timing of peak recruitment may have provided different insights than examining mean recruitment through 500-ms epochs leading to termination of the squat. Third, participants were healthy, asymptomatic women. Women with patellofemoral pain syndrome exhibit lower isometric strength than asymptomatic controls (Bolgla et al., 2008; Ireland et al., 2003). The extent to which gluteus maximus recruitment is associated with frontal plane knee motion may differ in participants with impaired strength. Fourth, surface EMG constrained us from examining relationships between deep hip external rotators and knee kinematics. Since minimizing medial hip rotation may be an important component of limiting knee valgus during single-leg squats, it may be important to understand how recruitment of the deep hip external rotators is associated with frontal plane knee motion. In-dwelling EMG could be used to address that question. Last, it is important to recognize that our study design does not permit causal inferences. Similarly, while the regression analysis permits one to examine associations between variables, it does not imply a cause-and-effect relationship. While reduced gluteus maximus recruitment as well as increased medial hip rotation and hip adduction may be associated with increased knee valgus, one should not interpret that finding to imply that reduced gluteus maximus recruitment causes knee valgus to increase during a single-leg squat. Despite these limitations, our finding that increased medial hip rotation and hip adduction and reduced gluteus maximus recruitment are correlated with increased knee valgus during a single-leg squat test is clinically relevant. The finding provides a plausible linkage between gluteus maximus function and frontal plane knee kinematics. Future studies should examine how gluteus maximus recruitment can be enhanced and whether that influences lower extremity kinematics during dynamic weightbearing tasks. 5. Conclusion The single-leg squat test used in this study was developed to identify individuals who may have impaired hip muscle function. In our study, hip flexion and adduction were increased in female participants identified as “poor” performers during the test compared to “good” performers. However, no differences in knee kinematics, hip extension or abduction strength or in gluteus maximus or gluteus medius recruitment were identified between the groups. Nevertheless, controlling for hip kinematics, gluteus maximus recruitment was correlated with frontal plane knee motion. This finding implies that gluteus maximus neuromuscular control may modulate frontal plane knee kinematics during single-leg squats. References Bolgla, L.A., Malone, T.R., Umberger, B.R., Uhl, T.L., 2008. Hip strength and hip and knee kinematics during stair descent in females with and without patellofemoral pain syndrome. J. Orthop. Sports Phys. Ther. 38, 12–18.

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Please cite this article as: Hollman, J.H., et al., Frontal and transverse plane hip kinematics and gluteus maximus recruitment correlate with frontal plane knee kinematics during single-leg squat test..., Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2013.12.017