Kinematics and kinetics during walking in individuals with gluteal tendinopathy

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1 Accepted Manuscript Kinematics and kinetics during walking in individuals with gluteal tendinopathy Kim Allison, Tim V. Wrigley, Bill Vicenzino, Kim L. Bennell, Alison Grimaldi, Paul W. Hodges PII: S (16) DOI: doi: /j.clinbiomech Reference: JCLB 4107 To appear in: Clinical Biomechanics Received date: 17 September 2015 Accepted date: 7 January 2016 Please cite this article as: Allison, Kim, Wrigley, Tim V., Vicenzino, Bill, Bennell, Kim L., Grimaldi, Alison, Hodges, Paul W., Kinematics and kinetics during walking in individuals with gluteal tendinopathy, Clinical Biomechanics (2016), doi: /j.clinbiomech This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

2 Title Kinematics and Kinetics during walking in Individuals with Gluteal Tendinopathy Authors & Affiliations: Kim Allison a, Tim V Wrigley a, Bill Vicenzino b, Kim L Bennell a, Alison Grimaldi c and Paul W. Hodges b a The University of Melbourne, Department of Physiotherapy, 161 Barry St, Parkville, VIC 3010 Australia kallison1@student.unimelb.edu.au, timw@unimelb.edu.au, k.bennell@unimelb.edu.au b The University of Queensland, School of Health & Rehabilitation Sciences, Brisbane, QLD 4072, Australia b.vicenzino@uq.edu.au, p.hodges@uq.edu.au c Physiotec Physiotherapy, 23 Weller Rd, Tarragindi, QLD, 4121, Australia info@dralisongrimaldi.com Corresponding Author Kim Allison Department of Physiotherapy, University of Melbourne 161 Barry St Parkville, VIC 3010 Australia Ph: Fax: kallison1@student.unimelb.edu.au Word count abstract: 250 Word count main text: 4140 (proposed deletions tracked)

3 Abstract Background. Lateral hip pain during walking is a feature of gluteal tendinopathy but little is known how walking biomechanics differ in individuals with gluteal tendinopathy. This study aimed to compare walking kinematics and kinetics between individuals with and without gluteal tendinopathy. Methods. Three-dimensional walking-gait analysis was conducted on 40 individuals aged 35 to 70 years with unilateral gluteal tendinopathy and 40 pain-free controls. An analysis of covariance was used to compare kinematic and kinetic variables between groups. Linear regression was performed to investigate the relationship between kinematics and external hip adduction moment in the gluteal tendinopathy group. Findings. Individuals with gluteal tendinopathy demonstrated a greater hip adduction moment throughout stance than controls (standardized mean difference ranging from 0.60 (first peak moment) to 0.90 (second peak moment)). Contralateral trunk lean at the time of the first peak hip adduction moment was 1.2 degrees greater (P=0.04), and pelvic drop at the second peak hip adduction moment 1.4 degrees greater (P=0.04), in individuals with gluteal tendinopathy. Two opposite trunk and pelvic strategies were also identified within the gluteal tendinopathy group. Contralateral pelvic drop was significantly correlated with the first (R=0.35) and second peak (R=0.57) hip adduction moment, and hip adduction angle with the second peak hip adduction moment (R=-0.36) in those with gluteal tendinopathy. Interpretation. Individuals with gluteal tendinopathy exhibit greater hip adduction moments and alterations in trunk and pelvic kinematics during walking. Findings provide a basis to consider frontal plane pelvic control in the management of gluteal tendinopathy. Keywords

4 Gluteal tendinopathy; gait; kinetics; kinematics; external hip adduction moment; walking Highlights Hip adduction moment during walking is larger in those with gluteal tendinopathy Pelvic obliquity is associated with hip adduction moment in gluteal tendinopathy Two trunk and pelvic strategies are seen during walking in gluteal tendinopathy Addressing gait biomechanics may be relevant for gluteal tendinopathy management

5 1. Introduction Gluteal Tendinopathy (GT) is a prevalent, recalcitrant cause of hip pain (18, 54) and disability (19) most frequently affecting women aged years (19). Individuals with GT frequently report lateral hip pain during walking (7, 18), which can lead to a reduction in activity levels and subsequent detrimental effect on health and well-being (18). Although it is postulated that GT involves abnormal biomechanics during walking (7, 25, 28, 43), there has been little formal investigation to confirm or characterize abnormalities. Identification of biomechanics associated with GT may guide effective treatment of this chronic condition. GT involves tendinopathic change of the gluteus medius and/or gluteus minimus tendons (8, 33, 39), two primary hip abductors (1, 41). Previous research has identified hip abductor weakness in individuals with GT (2, 54), which may have relevance for walking. Force from the hip abductor muscles is required to control the position of the pelvis in the frontal plane on the stance leg during walking (1, 23, 55). This is particularly needed in order to balance the external hip adduction moment caused primarily by the path of the external ground reaction vector medial to the hip (53, 55). The medio-lateral position of the trunk, and to a lesser extent the pelvis, directly influences the medio-lateral position of the centre of mass in the frontal plane and the magnitude of the external hip adduction moment (Figure 1); thus trunk kinematics are an important variable for investigation during walking in individuals with GT. Pelvic position during walking in GT has been studied by visual observation in two studies with conflicting findings (8, 54). During the stance phase of walking, hip abductor muscle weakness has been shown to be associated with contralateral pelvic drop and lateral pelvic translation in the frontal plane (56), likely resulting in a shift of the body s center of mass away from the stance limb and a greater external hip adduction moment. The likely net effect of these biomechanical patterns is greater loads through

6 the gluteal tendons on the weight-bearing limb, which may contribute to the development or persistence of GT. The primary aim of this study was to compare trunk, pelvis and hip kinematics and kinetics during walking using three-dimensional motion analysis in individuals with GT and controls with no history of GT, lumbar spine or lower limb pain. We hypothesized that individuals with GT would demonstrate a greater external hip adduction moment, hip adduction angle, contralateral pelvic drop and lateral pelvic translation than controls during the stance phase of walking. 2. Methods 2.1 Participants Forty individuals aged years with clinical and radiological diagnosed GT, and 40 age- and sex-comparable controls were recruited via online and local newspaper advertising. The GT and control groups were comparable in age, height and number of males and females; however the GT group was significantly heavier, had greater BMI and inter-asis distances (i.e. greater pelvic width) (all P<0.05) (Table 1), consistent with previous descriptive studies. The median (Interquartile Range (IQR)) duration of lateral hip pain symptoms for GT participants was 28 (28) months. The median (IQR) values of average and worst pain experienced over the past week reported on the NRS were 5 (1) and 7 (1), respectively. Inclusion criteria for GT participants were a primary report of unilateral hip pain at the greater trochanter (20, 43, 54) for 3 months with an average intensity of 4 on an 11-point numeric pain rating scale (NRS) ( 0 no pain ; 10 worst pain imaginable). Physical assessment was performed by a qualified physiotherapist to confirm the clinical diagnosis of GT and exclude a

7 clinical diagnosis of intra-articular hip pathology; the latter defined by reproduction of groin pain during a passive hip quadrant test (38). Clinical diagnosis of GT was defined as reproduction of lateral hip pain 4/10 on the NRS with palpation of the greater trochanter (20, 54) plus at least one pain-provocative clinical test for GT (8, 20, 26, 35): (1) Hip FADER (14), (2) Hip FADER static de-rotation test (35), (3) Hip FABER (46), (4) Modified Ober s Test (31), (5) Static hip abduction at end range Ober s Test position (46) or (6) 30-second single-leg-stance test (35). Radiological inclusion criterion was a primary MRI diagnosis of GT defined as per Blakenbaker et al. (10). Exclusion criteria included radiological evidence of hip osteoarthritis (Kellegren Lawrence Grade 2 on plain X-ray (30)), BMI > 36 kg/m 2 (due to difficulties with skin marker placement for 3D gait analysis), previous lower limb surgery, any neurological or systemic diseases affecting the musculoskeletal system. Control participants underwent phone screening to ensure they met the following inclusion criteria: aged years, BMI 36kg/m 2, absence of any musculoskeletal injury, lower limb surgery, neurological or systemic diseases affecting the musculoskeletal system. Ethics approval was obtained from the institutional Human Research Ethics Committee and all participants provided written informed consent. 2.2 GT related lateral hip pain history In the GT group, lateral hip pain severity was measured using the NRS and reported as average and worst pain experienced over the past week. 2.3 Walking Analysis Participants underwent three-dimensional gait analysis while walking barefoot along a ten-metre walkway (such that each consecutive trial was in the opposite direction along the walkway), at their self-selected comfortable walking speed rating any pain experienced on the NRS.

8 Twenty seven spherical retro-reflective markers were placed on the trunk (C7, T1, T12), pelvis (ASIS, PSIS), and lower limb (3-marker triad over the lateral thigh, 3-marker triad over the lateral tibial shank, lateral femoral condyles, lateral malleoli, calcaneus, second and fifth metatarsal bases, first and fifth metatarsal heads) in accordance with Besier et al (6). Kinematic data were recorded at 120 Hz using a twelve-camera (MX F20/F40) Vicon motion capture system (Vicon, Oxford, UK). Ground reaction force data were collected at 1200 Hz using two force plates (Advanced Mechanical Technology Inc., Watertown, MA) embedded in the movement laboratory floor. Walking speed was derived from photoelectric timing gates 4 meters apart. Each participant performed 6-15 walking trials in order to collect six trials (three in each direction) with single full contact foot strikes on the force plate (20N threshold) for the study limb. Knee joint center locations were derived from mean helical axes calculated from five consecutive squats to 45 degrees knee flexion (6). Hip joint centres were determined using regression equations by Harrington et al (27). Marker trajectory data and ground reaction force data were low-pass filtered at 6 Hz with a dualpass 2 nd order Butterworth filter. Hip joint, pelvis and trunk angles were calculated from the walking trials using Vicon BodyBuilder software (6). Pelvic angles were extracted using a rotation-obliquity-tilt Cardan angle sequence (4). Lateral pelvic translation in the frontal plane was represented by the distance of the calcaneal marker relative to the floor-projected midline, defined by a vertical line from the midpoint between the ASIS markers. This value was normalized to half the distance between the ASIS markers (to account for the likely wider base of support with greater pelvic width (53)) and expressed as a percentage, to provide simple relative quantification of the position of the calcaneus to the midline of the participant (0% representing

9 a position of the calcaneus directly under the midline and 100% under the ASIS). Lateral trunk lean was expressed by the frontal plane angle of the trunk segment (defined by the sternum, C7 and T10 markers) in relation to the laboratory coordinate system. Maximum values of hip adduction, contralateral pelvic drop (obliquity), contralateral trunk lean, and lateral pelvic translation, were determined at the time of the first hip adduction moment peak, minimum moment in mid-stance, and second moment peak for each of the six walking trials and averaged. Joint moments were calculated from the walking trials using inverse dynamics in Vicon Body Builder software (UWA model (6)) and normalized to body weight times height (Nm/BW.Ht%) to account for body size. The maximum external hip adduction moments for each trial were determined during 0-50% and % of stance, representing the first and second hip adduction moment peaks respectively, and the minimum value between the two peaks to represent the midstance moment. The values of the six trials were then averaged. 2.4 Data analysis For control participants, a test hip was designated in a random manner using a coin toss. Data analyses were performed using Statistical Package for the Social Sciences (SPSS), version 22 (IBM, New York, USA). Data were explored for normality and homogeneity of variance prior to analysis. Independent t-tests were used to compare descriptive data and spatiotemporal variables of walking between groups when normally distributed, and Mann-Whitney U tests for nonnormal data. Given the potential effect of speed on walking biomechanics, an analysis of covariance (ANCOVA) with walking speed (velocity, m/s) as a covariate, was used to compare kinematic and kinetic variables between the two groups. Linear regression was performed to investigate the relationship between kinematics and the magnitude of the hip adduction moment

10 in the GT group. Alpha was set at 0.05 for all analyses. The standardized mean difference (SMD) was calculated to estimate the effect sizes for statistically significant outcomes (13). Given that individuals can use different trunk and pelvic strategies to compensate for hip abductor muscle dysfunction, we performed additional exploratory analysis to elucidate subgroups within the GT group. We tested the hypothesis that different strategies were represented in the GT group (high contralateral trunk lean and high pelvic tilt; high ipsilateral trunk lean and reduced pelvic tilt (as recognized in hip osteoarthritis (50, 52, 56))) by identification of participants with largest and smallest trunk lean (greater or less than one SD from the mean) at the three moment time points and investigated the relationship between trunk and pelvic position with linear regression for these individuals. 3. Results Significant between-group differences were identified in all spatiotemporal variables of walking. Participants with GT had a shorter step length (mean difference 0.04 metres; 95% CI -0.08, , P=0.01, SMD=0.67) and walked at a slower velocity (mean difference -0.1 m/sec; 95% CI - 0.2, -0.05, P=0.001, SMD=0.75) than controls. Median (IQR) pain intensity reported during walking in the GT group was 2 (1) on the NRS. During the stance phase of walking, significant between-group differences were evident in both kinetic (Table 2 and Figure 2) and kinematic variables (Table 2 and Figure 2), with between group differences consistent if sexes were analysed separately. Individuals with GT demonstrated a greater first peak (0-50% stance) hip adduction moment (mean difference 0.56 Nm/BW.Ht%;

11 95%CI 0.1, 1.1, P=0.02, SMD=0.60), mid-stance (minimum between peaks) hip adduction moment (mean difference 1.3 Nm/BW.Ht%; 95% CI 0.4, 1.7, P=0.002, SMD=0.69) and second peak (50-100% stance) hip adduction moment (mean difference 1.8 Nm/BW.Ht%; 95% CI 0.8, 2.7, P<0.001, SMD=0.90). With respect to walking kinematics (Table 2 and Figure 2), individuals with GT demonstrated greater contralateral trunk lean at the time of the first peak hip adduction moment (mean difference 1.2 degrees; 95% CI 0.04, 2.4, P=0.04, SMD=0.49) and greater contralateral pelvic drop at the time of the second peak hip adduction moment (mean difference 1.4 degrees; 95%CI 0.04, 2.8, P=0.04, SMD=0.47). No significant between-group differences were identified with respect to hip adduction angle, internal rotation angle, or lateral translation of the pelvis. Relationships between the magnitude of the external hip adduction moment and kinematic and spatiotemporal variables in the GT group are presented in Table 3. There was a small but significant positive correlation between the first peak hip adduction moment and both pelvic drop (R=0.354, R 2 =0.126, P=0.03) and step length (R=0.362, R 2 =0.063, P=0.03). Although no kinematic variables were significantly correlated with the magnitude of the mid-stance moment, velocity (R=0.145, R 2 =0.104, P=0.04) and step length (R=0.250, R 2 =0.063, P=0.03) explained 10.4% and 6.3% of the variation, respectively. Contralateral pelvic drop was positively correlated, and hip adduction negatively correlated, with the magnitude of the second peak hip adduction moment; pelvic obliquity explained 32.8% (R=0.573, R 2 =0.328, P=0.000) and hip adduction explained 13.1% (R=0.362, R 2 =0.131, P=0.02) of the variation.

12 As it was expected that individuals may present with several different strategies of interaction between pelvic and trunk motion, data were also considered with respect to possible subgroups planned a priori. Individuals with contralateral and ipsilateral trunk lean greater than 1 SD from the mean were identified in the GT group (Figure 3). Descriptive characteristics of these individuals and ratio of males to females were comparable in both subgroups and to the group as a whole (Supplementary material Table 1.). Consistent with our hypothesis, when the relationship between trunk lean and pelvic obliquity was evaluated for these outlier individuals, trunk position was negatively correlated with pelvic position during stance (higher ipsilateral trunk lean corresponded to lower pelvic obliquity, and higher contralateral lean corresponded to higher pelvic obliquity). The correlation was significant at the time of first peak hip adduction moment (R=-0.619, R 2 =0.383, P=0.03) which corresponds to the period of weight acceptance. 4. Discussion This is the first study to evaluate walking biomechanics using 3-dimensional gait analyses in individuals with GT and to contrast these data with observations for pain-free controls. The principal finding of the present study is that individuals with GT demonstrated a greater external hip adduction moment throughout the stance phase of walking than healthy controls. There were also small, but significant, between-group differences in trunk lean during early stance and contralateral pelvic drop during late stance. The small size of these differences was not surprising considering our observation that there are subgroups within the GT group (comparable in age and gender to each other and to the group (Supplementary Table 1.)) with opposite patterns of trunk and pelvic motion during walking, presumably an indicator of poor control by the hip abductor muscles. Of potential clinical importance for interpretation of the kinetic findings, contralateral

13 pelvic drop explained a significant amount of the variability in the peak hip adduction moments, and more than any other kinematic or spatiotemporal variable. Given the cross-sectional study design, we are unable to establish whether the higher hip adduction moments and kinematic differences between groups are a consequence and/or cause of GT. The external hip adduction moment, as measured during laboratory gait analysis in this study, must be balanced by an internal hip abduction moment. Thus a greater external adduction moment requires a greater internal hip abduction moment which involves greater active and passive loading of the hip abductors (12, 55); most obviously the primary hip abductor muscles gluteus medius and minimus (1, 23), the overlying tensor fascia lata (TFL) and upper gluteus maximus (UGM) muscles, and the iliotibial band (ITB) that arises from these two latter muscles (1, 41). In addition, greater contralateral pelvic drop observed in late stance, and in a subgroup of GT participants (4 females, 1 male) throughout stance, might increase gluteal tendon tensile load as the muscle-tendon units lengthen to the point where their length-tension relationship relies more on passive tensile loading (including tendon) than active cross-bridge overlap; and/or result in compression of the gluteal tendons against the greater trochanter. Further longitudinal studies are required to determine whether the greater external hip adduction moments and kinematic patterns identified here in individuals with GT might precede the development of GT, resulting in cumulative overload of the gluteal tendons and thus contributing to the development and/or perpetuation of GT. In the presence of greater external hip adduction moments during walking, it is likely that individuals with GT require greater activation of the hip abductor muscles, in order to control the position of the pelvis in the frontal plane. The gluteus medius and minimus muscles are the

14 primary hip abductors (1, 23) and contribute an estimated 70% of the hip abductor force required to maintain level alignment of the pelvis in single leg stance, with the remaining 30% from the TFL and UGM muscles via their insertion into the ITB (34). As walking requires only submaximal activation of the hip abductor muscles (42, 44, 45), it is not surprising that maximal isometric strength has not been shown to be directly related to the external hip adduction moment in disease-free controls (42). This relationship is likely to be altered in the presence of hip abductor weakness or pathology. We have recently shown maximal hip abductor strength deficits of 32% on the affected hip in those with GT when compared to controls (2). Interestingly, in the present study, individuals with GT exhibited: (1) 33% greater mid-stance hip adduction moments, representing the period of single leg support; (2) 25% greater hip adduction moments during late stance; and (3) 9% greater moments during early stance. Taken together these data imply that individuals with GT have a greater requirement for hip abductor moment development (to balance the larger external adduction moment) but lower hip abductor strength reserve to achieve it (2). Consequently there would be greater tensile demand on active and passive structures of the hip abductor muscles during walking in GT, with several implications. Tensile loading, within safe limits, is thought to provide an anabolic stimulus for tendon integrity in healthy tendon (15, 37), whereas the cumulative effects of excessive (32, 36) or reduced (49) tensile load are detrimental to tendon health. The gluteus medius and minimus muscles are the primary hip abductors (1), hence if increased external load pre-dated tendon pathology, they would theoretically be the first muscles recruited for abductor force generation with potential for tensile tendon overload. However, radiological studies have identified atrophic changes of the gluteus minimus and medius muscles in those with GT (40, 47, 54) from which it is tempting to speculate that these muscles (and tendons) are experiencing a reduction, rather than an increase

15 in, contractile load. Although the present study design does not permit interpretation of the relative contribution of each of the hip abductor muscles during walking, it is plausible that greater demand for hip abductor force would drive supplementary recruitment of the TFL and UGM muscles that exert their abductor force through the ITB (41, 51). This would lead to tension in the ITB, known to increase compressive forces against the greater trochanter into which the gluteal tendons insert (9). Given the relationship between activation of these muscles and ITB tension and compression forces at the greater trochanter, further electromyographic investigation of the hip abductor muscles during walking in individuals with GT is justified. Compressive forces are known to alter tenocyte cell structure, collagen type production and expression of large proteoglycans resulting in pathological tendon changes [see (16) for review]. Compression of the gluteal tendons against the greater trochanter as a result of ITB tension and/or increased hip adduction is thought to be a primary aetiological factor in the development of GT (11, 17, 25). ITB stiffness in standing, as measured by shear wave elastography, increases in parallel with external hip adduction moments in healthy individuals (48). Tateuchi et al. showed a 27% increase in the magnitude of the external hip adduction moment, manipulated by pelvic drop and contralateral trunk lean, resulted in a 25% increase in the shear elastic modulus of the ITB in a group of 14 healthy individuals. The present study showed 33% greater external hip adduction moments during mid-stance and 25% greater moments during late stance in individuals with GT than healthy controls. Taken together with the data from Tateuchi et al, this could increase stiffness of the ITB, with a potential to induce greater compressive forces against the gluteal tendons at their insertion into the greater trochanter, and it is plausible that this might contribute to development of GT.

16 Contrary to our hypothesis, the only kinematic variables that differed systematically between groups during walking were contralateral trunk lean during early stance and contralateral pelvic drop during late stance. One consideration with respect to our findings was that differences were in the range of a few degrees and might not be detectable clinically. However, our analysis shows that within the GT group there are individuals with a degree of pelvic obliquity and trunk lean that would be clinically detectable above that of the control average. Consistent with our prediction, individuals in the GT group with the greatest contralateral lean typically exhibited greater pelvic drop than those with the greatest ipsilateral trunk lean (Figure 3). Similar patterns have been shown to represent time dependent adaptations to the presence of hip abductor weakness or pain in hip OA (50, 52). In early stage of hip osteoarthritis there is increased contralateral pelvic drop in the frontal plane during walking (52), whereas over time patients often develop an ipsilateral trunk lean to reduce the demand on the hip abductors to control the position of the pelvis in the frontal plane (50). Although we found similar kinematic patterns and subgroups, post hoc analysis showed that contralateral trunk lean at the three moment time points was not related to GT-symptom duration (R=0.74, R 2 =0.01, P=0.66; R = 0.21, R 2 =0.00, P =0.90; R=0.13, R 2 =0.02, P =0.45). Identification of GT subgroups in the present study may explain the conflicting findings of the previous studies evaluating pelvic position during walking (8, 54) and support evaluation of trunk and pelvic position during clinical observation of gait in order to identify specific maladaptive gait patterns in those with GT. With respect to interpretation of the kinematic data, the significant positive relationship between contralateral pelvic drop and the magnitude of the peak hip adduction moments has potential clinical relevance. Contralateral pelvic drop explained more variation in the magnitude of the peak hip adduction moments (R 2 =12.6% and R 2 =32.8% respectively) than any spatiotemporal or

17 kinematic variable, contrasting the strong relationship between walking velocity and peak hip adduction moment in healthy controls (42).Trunk angles did not correlate well with the hip adduction moment, likely due to the spectrum of kinematic patterns seen in the GT group (as highlighted by subgroup analysis), and/or the trunk segment used in the present study not representing the primary contributor to the centre of mass. Increased central adiposity has been identified in those with GT (21) and the GT group in the present study had a larger BMI and pelvic width than those in the control group. Taken together, this data might suggest that the pelvic segment represents a greater contribution to the position of the centre of mass in individuals with GT when compared to controls. Although causality cannot be confirmed it is reasonable to speculate that greater contralateral pelvic drop contributes to greater peak hip adduction moments during walking in individuals with GT, potentially due to the associated increased distance of the centre of mass from the hip joint centre in the medio-lateral direction (Figure 1). In contrast, hip adduction was negatively correlated with the magnitude of the second hip adduction moment explaining 13.1% of the variation. Although lower moments (associated with increasing hip adduction) likely represent a reduction in hip abductor muscle (and tendon) loading, hip adduction may also be associated with greater compressive force of the gluteal tendons against the greater trochanter; both factors mechanistic for tendon injury (3). The relationship between both hip adduction and pelvic obliquity and the magnitude of the external hip adduction moment supports the contemporary clinical notion that frontal plane hip and pelvic control has relevance for development and persistence of GT (5, 24).

18 This study has several key strengths. First, strict inclusion and exclusion criteria ensured that participants within the GT group had a primary clinical and radiological diagnosis of GT in the absence of intra-articular disease. This is unlike previous studies that relied on physical characteristics of those with GT diagnosed by retrospective radiographs and/or radiological diagnosis without clinical assessment to define GT pathology. Second, post hoc analysis of kinematic variables underpinning the magnitude of the external hip adduction moment aids clinically-helpful interpretation of the kinetics recorded in participants with GT. Consistent with previous studies, this study consisted of predominantly females and groups were matched for numbers of females and males. A limitation is that we did not investigate the controls with MRI to exclude tendinopathy, although they were free of any complaints of hip or lower limb pain. Second, differences between groups in pelvic width might have influenced the magnitude of the external hip adduction moment (by influencing the distance of the centre of mass from the hip joint centre), but we did not find a relationship between our measure of pelvic width (inter-asis distance) and the hip adduction moment. Third, individuals in the GT group were heavier and had a BMI that fell within the pre-obese range which infers higher levels of adipose, a risk factor for tendinopathy (22). Although individuals in the GT group were heavier, we normalized moments to body weight and height to account for body size. The cross-sectional design means we are unable to establish a cause and effect relationship between GT pathology and the kinematic and kinetic differences between groups, but provides a strong foundation for future longitudinal studies. Specifically, randomized clinical trials are required to establish whether modification of these biomechanical issues reduce symptoms and improve function in individuals with GT. Furthermore, EMG studies are necessary to evaluate the neuromuscular control of the hip abductor muscles during walking.

19 5. Conclusion This study showed that individuals with GT had higher external hip adduction moments and alterations in trunk and pelvic kinematics during walking. Although present study design cannot inform whether these patterns are a cause or effect of GT, our data provide evidence to suggest that consideration of walking biomechanics may be relevant for the management of GT. 6. Acknowledgements The study was supported by the National Health Research and Medical Research Council of Australia (Program Grant: ID631717; Research Fellowships to KB: APP PH: APP ) and the Physiotherapy Research Fund (PRF Seeding Grant to KA: S14-012). The authors would like to acknowledge the work of Ms Pippa Nicholson in recruiting case participants for the present study.

20 Table 1. Participant characteristics (mean (SD) unless otherwise stated) Gluteal Tendinopathy (n=40) Control (n=40) Mean Difference (95% CI) Age, years 54 (9) 54 (9) -0.3 (-4.3, 3.8) Height, m 1.67 (0.09) 1.66 (0.09) 0.00 (-0.04, 0.04) Mass, kg 74 (14) 67 (12) 6.4 (0.6, 12.3) Body mass index, kg/m (4.2) 24.0 (2.6) 2.3 (0.7, 3.8) Inter ASIS width, mm 263 (25) 230 (21) 33 Sex, n (%) (22, 44) Female 31 (78%) 31 (78%) - - Male 9 (22%) 9 (22%) - - Symptomatic (test) hip* Left = 26, Symptom duration, Right = 14 Left = 17, Right = 23 months, median (IQR) 28 (28) 0 (0) Lateral hip pain severity, (0-10), median (IQR) P value * 0.01* <0.001* Average over past 5 (1) week Worst over past week 7 (1) During normal 3 (3.5) paced walking During fast paced 4 (4) walking

21 Data not normally distributed, * Test hip for controls designated using a coin toss

22 Table 2. Group biomechanical data (mean (SD)) Gluteal Controls Mean Difference P value Tendinopathy (n=40) (n=40) (95% CI) Spatiotemporal variables Velocity (m/sec) 1.3 (0.16) 1.4 (0.16) (-0.19, -0.05) 0.001* Step length (m) 0.66 (0.08) 0.71 (0.07) (-0.07, -0.01) 0.01* External Hip Adduction Moment (Nm/BW.Ht (%)) 1 st peak 6.2 (1.0) 5.6 (1.0) 0.56 (0.1, 1.1) 0.02* Mid-stance dip 4.0 (1.6) 2.9 (1.6) 1.3 (0.4, 1.7) 0.002* 2 nd peak 7.1 (2.0) 5.3 (2.1) 1.8 (0.8, 2.7) <0.001* Hip Adduction Angle, degrees At 1 st peak HAM 7.9 (4.0) 7.4 (4.2) 0.5 (-1.4, 2.5) 0.60 At Mid-stance 9.0 (3.8) 8.3 (3.8) 0.7 (-1.1, 2.4) 0.46 HAM At 2 nd peak HAM 6.0 (3.8) 6.4 (4.0) -0.4 (-1.9, 1.5) 0.64 Hip Internal Rotation Angle, degrees At 1 st peak HAM -1.3 (8.6) -1.2 (8.6) 0.06 (-3.9, 4.3) 0.97 At Mid-stance -2.0 (8.4) -2.5 (8.7) 0.5 (-3.3, 4.4) 0.78 HAM At 2 nd peak HAM 4.7 (9.1) 4.1 (9.0) 0.6 (-3.3, 4.5) 0.78 Contralateral Pelvic Drop (pelvic obliquity) Angle a, degrees At 1 st peak HAM 4.0 (2.3) 4.2 (2.3) -0.3 (-1.3, 0.8) 0.59 At Mid-stance 3.5 (2.5) 3.7 (2.5) -0.2 (-1.3, 0.9) 0.71 HAM At 2 nd peak HAM 4.2 (3.0) 2.8 (3.0) 1.4 (0.04, 2.8) 0.04* Lateral Translation of Pelvis (%Inter ASIS distance/2) b At 1 st peak HAM 21.7 (7.2) 21.6 (7.6) 0.04 (-3.4, 3.3) 0.98 At Mid-stance 15.6 (8.0) 13.5 (8.5) 2.1 (-1.6, 5.9) 0.26 HAM At 2 nd peak HAM 16.6 (8.6) 14.2 (9.1) 2.3 (-1.7, 6.4) 0.25 Trunk Angle c, degrees At 1 st peak HAM 0.50 (2.4) 1.7 (2.5) -1.2 (-2.4, -0.04) 0.04* At Mid-stance 0.83 (2.5) 1.8 (2.4) (-2.0, -0.24) 0.12 HAM At 2 nd peak HAM -1.0 (2.7) 0.16 (2.6) -1.3 (-2.4, -0.2) 0.06

23 Kinematic values denote angles at the time of the external hip adduction moment (HAM) first peak, mid-stance minimum and second peak. a Positive pelvic obliquity indicates the contralateral pelvis is dropped relative to the stance limb b 0% = position of the calcaneus directly under the midline, 100% = position of the calcaneus directly under the ASIS c Ipsilateral trunk lean is positive, * significant between group difference.

24 Table 3. Linear regression of frontal plane kinematic and spatiotemporal variables and external hip adduction moment (HAM) during stance in individuals with gluteal tendinopathy 1 st Peak (Nm/BW. Ht(%)) Mid-stance (Nm/BW. Ht(%)) 2 nd Peak (Nm/BW. Ht(%)) Hip adduction angle, degrees At 1 st peak HAM R= R 2 =0.004 P=0.71 At mid-stance HAM - R=0.125 R 2 =0.016 P=0.44 At 2 nd peak HAM - - R= R 2 =0.131 P=0.02* Pelvic Obliquity, degrees At 1 st peak HAM R= R 2 =0.126 P=0.03* At mid-stance HAM - R= R 2 =0.067 P =0.68 At 2 nd peak HAM - - R=0.573 R 2 =0.328 P=0.000* Lateral Translation of Pelvis, Minimum Foot Placement: ½ Inter ASIS (%) At 1 st peak HAM R= R 2 =0.077 P=0.08 At mid-stance HAM - R= R 2 =0.000 P=0.92 At 2 nd peak HAM - - R=0.105 Trunk Lean, degrees R 2 =0.011 P=0.520 At 1 st peak HAM R= R 2 = P=0.18 At mid-stance HAM - R= R 2 = P=0.89 At 2 nd peak HAM - - R=0.064

25 Spatiotemporal variables Velocity Step length * P<0.05 R=0.145 R 2 =0.021 P=0.20 R=0.250 R 2 =0.063 P=0.03* R=0.322 R 2 =0.104 P=0.004* R=0.285 R 2 =0.08 P=0.01* R 2 = P=0.71 R=0.123 R 2 =0.015 P=0.28 R=0.073 R 2 =0.005 P=0.52

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29 54. Woodley S, Nicholson H, Livingstone V, et al. Lateral Hip Pain: Findings From Magnetic Resonance Imaging and Clinical Examination. Journal of Orthopaedic & Sports Physical Therapy. 2008;38(6): Yoon YS, Mansour JM. The passive elastic moment at the hip. J Biomech. 1982;15(12): Zeni J, Jr., Pozzi F, Abujaber S, Miller L. Relationship between physical impairments and movement patterns during gait in patients with end-stage hip osteoarthritis. J Orthop Res. 2015;33(3): Figure captions. Figure 1. The external hip adduction moment represented as the resultant force derived from the distance (D) of the centre of mass from the hip joint centre and the ground reaction force vector. Increasing pelvic obliquity is associated with an increased distance of the centre of mass from the hip joint centre, which can be compensated by ipsilateral trunk lean (compensated Trendelenburg). Contralateral trunk lean should be accompanied by greater pelvic obliquity (uncompensated Trendelenburg) Figure 2. Group ensemble averages for kinematic and kinetic variables. Data are shown for GT (red) and control (black) participants as mean (solid line) and standard deviation (dashed line). Figure 2 caption (below figure) FP:1/2 inter-asis(%) indicates the position relative position of foot placement (calcaneus marker) to the midline of the participant (where 0% represented a position of the calcaneus directly under the midline and 100% directly under the ASIS) Figure 3. Evaluation of relationship between trunk lean and pelvic angle. Data are plotted for the three hip adduction moment time-points (peaks and intervening minimum). GT participants with trunk lean > 1 SD (as above or below the dashed lines on the y axis corresponding with the GT group mean + 1 SD and 1SD respectively) are plotted against pelvic obliquity in the lower panels. Outliers in the GT group with ipsilateral trunk lean have less pelvic obliquity, and those with contralateral trunk lean have greater pelvic obliquity as demonstrated by the stick figure.

30 Fig. 1

31 Fig. 2

32 Fig. 3