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The Relationship of Anticipatory Gluteus Medius Activity to Pelvic and Knee Stability in the Transition to Single-Leg Stance
1 2 3 4 5 PM R XXX (2015) 1-7 www.pmrjournal.org 6 7 8 9 10 11 12 13 14 15 16 17 Q4 18 19 20 21 22 Abstract 23 24 25 Background: The knee abduction moment in a weight-bearing limb is an important risk factor of conditions such as patellofemoral 26 pain and knee osteoarthritis. Excessive pelvic drop in single-leg stance can increase the knee abduction moment. The gluteus 27 28 medius muscle is crucial to prevent pelvic drop and must be activated in anticipation of the transition from double-leg to single29 leg stance. 30 Objective: To examine the relationship of anticipatory activity of the gluteus medius to pelvic drop and knee abduction moment. 31 Design: Observational, cross-sectional correlational study. 32 33 Setting: Research laboratory. 34 Participants: Twenty female adults (mean age 22.6 years, standard deviation 2.5) were recruited and fully participated. 35 Participant selection was limited to healthy women who did not have a history of knee and ankle ligament injuries, any indication 36 37 of knee, hip, and/or low back pain, and/or knowledge of the proper squat technique. 38 Methods: Participants performed 16 single-leg mini squats on their nondominant leg. 39 Main Outcome Measures: The onset and magnitude of anticipatory gluteus medius activity were measured in relation to toe-off of 40 41 the dominant leg during the transition from double-leg to single-leg stance. Preplanned correlations between anticipatory gluteus 42 medius onset and its activation magnitude, pelvic obliquity, and knee abduction moment were examined. 43 Results: The magnitude of anticipatory gluteus medius activity was significantly correlated with the knee abduction moment 44 (rs (18) ¼ 0.303, P < .001) and pelvic obliquity (rs (18) ¼ 0.361, P < .001), whereas gluteus medius onset was not significantly 45 46 correlated with either knee abduction moment or pelvic obliquity. 47 Conclusions: The amount of gluteus medius activity is more important for controlling knee and pelvic stability in the frontal plane 48 than the onset of activation. 49 50 51 52 53 In addition, greater knee abduction moments during Introduction 54 55 walking have also been associated with the development 56 of knee OA [15,16], and poor alignment at the knee can Knee pain syndromes such as patellofemoral pain (PFP) 57 58 be considered an independent risk factor for the progresand knee osteoarthritis (OA) are of growing importance in 59 sion of knee OA [17]. the health care community [1-3], especially in women, 60 Frontal plane pelvic motion may play an important who have a higher incidence of these conditions compared 61 62 role in changing knee abduction moments in a weightwith men [4,5]. These knee pain conditions have a nega63 bearing limb [12,18,19]. Pelvic rotation (frontal plane) tive impact on the overall health-related quality of life, as 64 65 toward or away from a support limb can change the well as functional disability and associated health care 66 location of the center of mass (COM) relative to the knee costs [6-9]; therefore, preventing and treating these knee 67 68 joint [12,19,20], thereby altering the knee abduction pain syndromes is important for improving public health 69 moment. Indeed, young adult women with PFP have and decreasing health care costs [10,11]. 70 been shown to experience more pelvic drop (ie, tilt of Internal knee abduction moments play a critical role 71 72 the pelvis toward the unsupporting leg) when compared in the development of PFP and knee OA [12,13]. Past 73 with healthy persons [21]. It has also been suggested research has found that persons with PFP exhibited a 74 75 that knee OA could be accelerated by excessive pelvic significantly greater knee abduction moment in the frontal 76 drop [12]. To develop strategies for preventing excessive plane during walking than did healthy persons [14]. 77 78 79 1934-1482/$ - see front matter ª 2015 by the American Academy of Physical Medicine and Rehabilitation 80 http://dx.doi.org/10.1016/j.pmrj.2015.06.005
Original Research
The Relationship of Anticipatory Gluteus Medius Activity to Pelvic and Knee Stability in the Transition to Single-Leg Stance Daehan Kim, MSc, Janelle Unger, BSc, Joel L. Lanovaz, PhD, Alison Oates, PhD
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GMED Activity and Pelvic and Knee Stability
pelvic drop and subsequent increases of the knee abduction moment, previous research has focused on elucidating the role of the hip abductors in stabilizing frontal plane pelvic posture [22,23]. Because it has the largest physiological crosssectional area among the hip abductors, the gluteus medius (GMED) mainly provides frontal plane pelvic stability [22,24,25]. Several studies have shown that persons with PFP have delayed onset of GMED activation compared with healthy persons [26-29]. Importantly, the authors of one of these studies reported that subjects with PFP showed both delayed GMED onset and increased knee abduction moment compared with healthy subjects [26], but the relationship between the onset of GMED and the increased knee abduction moment was not investigated. Given that an inevitable delay exists between the onset of muscle activity and force development of a muscle group [30], anticipatory activation of GMED appears crucial to control pelvic drop for the transition from single-leg to double-leg stance. It is important to elucidate how anticipatory GMED activation, in terms of onset timing and activation magnitude during a double-leg to single-leg support transition, controls frontal plane pelvic motion and the knee abduction moment. Knee disease and pain may alter the way someone moves, which then confounds the understanding of whether a change in movements caused the pain or if pain caused the change in movement; therefore, it is important to first investigate the neural control of a healthy, disease- and pain-free population to establish a normal pattern of control. The aim of this study was to examine the relationship of anticipatory GMED activity with frontal plane pelvic motion and the knee abduction moment. This correlation was measured when participants transitioned from double-leg to single-leg support while performing a single-leg mini squat. Anticipatory GMED activity was defined as activity prior to toe-off of the nonsupporting leg. We hypothesized that an earlier onset and greater magnitude of the anticipatory GMED activity of the supporting leg would be significantly correlated with decreased pelvic drop and reduced knee abduction moment of the same leg.
Eligibility to participate was determined through a prescreening questionnaire. This research protocol was reviewed and approved by the institutional research ethics board. Informed consent was obtained before beginning the testing protocol for all participants. Instrumentation Leg dominance was identified using a Modified Waterloo Footedness Questionnaire [31]. Participants rated which leg they most often used for object manipulation tasks (ie, the dominant leg), as well as for providing support (the nondominant leg). Three-dimensional (3D) kinematic data from the pelvis and lower limbs were collected using a motion capture system (Vicon Nexus, Vicon Motion Systems, Los Angeles, CA), and ground reaction forces (GRFs) were measured using force platforms under each foot (OR6, Advanced Mechanical Technology, Inc, Watertown, MA) while the participants performed single-leg mini squats (SLMS). Kinematic data and GRF data were collected at a sampling rate of 100 and 2000 Hz, respectively. An SLMS is a commonly used clinical screening tool for assessing frontal plane pelvic and knee movement during weight bearing that is functionally similar to stair negotiation [32]. Furthermore, the quality of SLMS performance can reliably represent the functional quality of GMED activation [33]. To perform the SLMS, participants first transitioned from double-leg to singleleg standing, and then lowered their body by flexing their hip, knee, and ankle (Figure 1). Surface electromyography (EMG; 2400GT2, Noraxon Inc, Scottsdale, AZ), sampled at 2000 Hz, was used to record the muscle activity of the GMED [34,35] during the movement. Testing Protocol An initial 60-second quiet standing trial was collected to obtain baseline EMG values. Participants then performed a total of 32 SLMS. Movement speed was standardized using the beat of a metronome set at 80 beats per minute: At the first beat, the participant lifted her toe off the force platform to make the transition from
Methods Participants Participants in this study were 20 healthy women between the ages of 18 and 39 years (mean, 22.6 years; standard deviation [SD], 2.5). Because pain, injuries, and knowledge of movement mechanics may modify the movement pattern of the participants, participant selection was limited to healthy women who did not have a history of knee and ankle ligament injuries, any indication of current knee, hip, and/or low back pain, and/or knowledge of the proper squat technique.
Figure 1. Sequential movement events.
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double- to single-leg stance. At the next beat she descended her body to the lowest position of the SLMS. Naturally, each participant needed time to stabilize herself on one leg before initiating the descent. Such time between toe-off and initiation of descent was defined as the single-leg stance phase. As a result, the SLMS was broken down into 3 phases (Figure 1): (1) double-leg stance, (2) single-leg stance, and (3) descent. Participants were instructed to keep their arms crossed on their chest for the entire movement. Sixteen SLMS were performed on each leg, with the order of the supporting leg randomized but limited to a maximum of 4 in a row on the same leg. The participants were given instructions for the SLMS and allowed to practice the movement at least 5 times for familiarization before starting. If the participant needed more than 10 practices, at least 1 minute of rest was given after the 10 practices to prevent fatigue. She was also allowed to rest between trials to prevent fatigue. Data Analysis The analysis in this study focused on the transition from double-leg to single-leg stance to investigate anticipatory GMED control. The descent of the SLMS was not included in the analysis because it is well established that GMED activation is more involved in transverse rotation of the hip rather than frontal plane rotation of the pelvis when the hip is flexed [23,36]. All analyses focused on the nondominant leg because this leg is more likely than the dominant leg to be involved in stability-related tasks during daily activities [31,37]. Kinematic and kinetic data were processed using a 4th order Butterworth digital filter, Visual 3D (C-Motion, Inc., Kingston, Ontario, Canada) and custom MATLAB (R2006b for PC, MathWorks, Natick, MA) routines. The 3D marker trajectories and GRF data were low-pass filtered at a cutoff frequency of 8 and 250 Hz, respectively. Toe-off was identified using GRFs. Toe-off was defined as the point when the vertical force dropped below a threshold value defined as 2 SDs of the zero load force tracing. This toe-off timing defined the end of the double-leg stance and the start of the single-leg stance. A virtual pelvic center marker midway between the bilateral anterior superior iliac spine and posterior superior iliac spine was used for detecting when a participant initiated the descent phase. Descent start was defined as the first point when the vertical velocity of the pelvic center marker became negative. The hip and knee joint center were identified using the functional calibration data according to the method described by Schwartz and Rozumalski [38]. Standard 3D rigid body analyses were performed for the lower limb, with anatomic axes defined using joint centers [39] and segmental kinematics tracked with 4 marker rigid clusters on each segment.
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The frontal plane angle of the pelvis was defined by the vertical axis of the laboratory and the line connecting the hip joint center and midway between the left anterior superior iliac spine and posterior superior iliac spine. To quantify the pelvic obliquity occurring during single-leg stance, the net change of pelvic angle between toe-off and initiation of descent was calculated. An increase in the pelvic angle represented pelvic obliquity, whereas a decrease in the angle represented pelvic drop. Inverse dynamics were used to calculate the net resultant internal knee abduction moment. The principle moments of inertia, the segment masses, and the locations of the COM of each segment were obtained from anthropometric tables [40]. The joint moment was normalized to participants’ weight and height. The net change of the knee abduction moment during single-leg stance was included in the data analysis. EMG data was high-pass filtered at 10 Hz, fully rectified, and then low-pass filtered at 50 Hz [41]. The electromechanical delay between the GMED onset and the generation of force during an SLMS has not previously been reported; therefore, the GMED activity integrated over 60 msec prior to toe-off was chosen as a measure of anticipatory activation based on studies of other activities, including comfortable walking [42,43]. These EMG magnitudes were normalized to the EMG integrated over 30 msec around the largest peak burst of EMG throughout all trials [44]. GMED onset was calculated using a threshold of 1.5 times the mean amplitude value of the quiet standing trial. EMG amplitudes were required to exceed the threshold for a minimum of 65 msec. Statistical Analysis Data were analyzed using SPSS versions 19.0 and 22 (IBM Corp, Armonk, NY) with an a level set at 0.05. Normal distribution of the data was tested using the Shapiro-Wilk test, skewness, and kurtosis analyses. The mean of the normally distributed data and the median of the non-normal data were used as the representative samples. Correlation statistics were used to examine if the GMED activation timing and magnitude on the supporting leg were significantly related to the pelvic obliquity and knee abduction moment of the same leg. In addition, the relationship between pelvic obliquity and knee abduction moment was examined to confirm if pelvic motion contributes to the change of knee abduction moment. Spearman’s rho (two-tailed) was used to determine the correlation coefficients to better fit the nonlinear relationship between the variables [45]. Results All 20 participants showed onset of the GMED before toe-off of the nonsupporting leg (Figure 2). Table 1 shows the mean and SD of the outcome variables. The GMED onset occurred on average 330 133 msec before
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GMED Activity and Pelvic and Knee Stability
Figure 2. Gluteus medius (GMED) activation, pelvic motion, and knee kinetic patterns by movement phases. Data represent average values of all trials for a representative participant. Data from different trials were synchronized in reference to the percentage of total duration of each phase. The gray areas represent one standard deviation from the mean. The thick vertical line depicts 60 msec before toe-off. EMG ¼ electromyography.
toe-off, and the GMED remained activated until the completion of each trial. All participants demonstrated pelvic obliquity instead of pelvic drop at toe-off. Statistical analyses showed that the magnitude of GMED activity over 60 msec prior to toe-off was negatively correlated with net change of knee abduction moment (rs (18) ¼ 0.303, P < .001) and positively correlated with pelvic obliquity (rs (18) ¼ 0.361, P < .001) (Figure 3). This finding indicates that the participants who had greater activity levels of GMED more than 60 msec before toe-off experienced greater pelvic obliquity and less increase of knee abduction moment during the single-leg stance phase. On the other hand, the onset of GMED was not significantly correlated with net change of knee abduction moment (rs (18) ¼ 0.109, P ¼ .105) or pelvic obliquity (rs (18) ¼ 0.058, P ¼ .389). The net change of pelvic obliquity and knee abduction moment were not significantly correlated with each other; however, the P value was very close to being statistically significant (rs (18) ¼ 0.442, P ¼ .05).
Discussion The purpose of this study was to determine the relationship between anticipatory GMED activity and Table 1 Descriptive data of gluteus medius onset, pelvic obliquity, and knee abduction moment during the transition to single-leg stance Variables
Mean SD
GMED onset
330 133 msec before toe-off 0.23 0.11
Normalized GMED EMG magnitude over 60 msec before toe-off (ratio of integrated EMG over 60 msec before toe-off to integrated EMG over 60 msec around the peak burst) Net change of pelvic obliquity during single-leg stance Net change of knee abduction moment during single-leg stance
3.81 1.24 ( ) 0.049 0.06 (Nm/Kg $ m)
EMG ¼ electromyography; GMED ¼ gluteus medius; SD ¼ standard deviation.
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Figure 3. The relationship of anticipatory gluteus medius (GMED) activation magnitude to knee abduction moment and pelvic obliquity during single-leg stance. EMG ¼ electromyography.
frontal plane pelvic motion and knee moment during the single-leg stance phase of a SLMS. GMED activation prior to toe-off is critical to stabilize the pelvis when it loses the support from one leg. Our results indicated that increased anticipatory GMED activation magnitude was significantly correlated with increased pelvic obliquity and decreased knee abduction moment, whereas GMED onset timing was not significantly correlated with pelvic obliquity or knee abduction moment. These results suggest that the magnitude and not the timing of GMED activation is a more important factor for protecting against excessive pelvic drop and knee abduction moment when moving from double-leg to single-leg support in healthy persons. Importantly, these results provide insights regarding how training for neuromuscular control of the GMED could be provided in a rehabilitation setting: By emphasizing the magnitude of GMED contraction before transitioning from double- to single-leg stance, lower limb positioning may be improved and knee pain may be reduced. To our knowledge, this study is the first to investigate how GMED activation is related with both dynamic pelvic posture and knee abduction moment in a weightbearing limb. Aminaka et al [26] reported that patients with PFP had both delayed GMED onset and greater knee abduction moment compared with healthy participants during a stair descent. These authors suggested a need to investigate a possible association between the GMED onset and knee abduction moment; however, our study could not support the correlation between these 2 variables. It is important to note that Aminaka et al [26] used different reference events for calculating GMED onset: GMED onset was calculated relative to toecontact of the stance leg. The functional demands on
the GMED for preventing excessive knee abduction moment at toe-contact on stair descent can be fundamentally different from that at toe-off in a double-leg to single-leg transition. Toe-off during the SLMS in our study is a critical event at which pelvic drop could rapidly influence the knee abduction moment. GMED onset occurred on average 330 msec before toe-off, and all participants demonstrated pelvic obliquity; therefore, the GMED was likely activated voluntarily in anticipation of toe-off [45] with sufficient time to generate the force required to prevent pelvic drop and even counter with slight pelvic obliquity. Previous studies [12,18,19] have only theorized that frontal plane pelvic motion would affect the knee abduction moment in a stance leg; the relationship between the 2 variables have not been directly examined prior to our study, which provides the unique assessment of the relationship between the pelvis and knee frontal plane movement. Given that GMED activation directly affects the pelvic motion, the relationship between anticipatory GMED activation and knee abduction moment could have been mediated by frontal plane pelvic motion; however, our study could not confirm such a theory because there was no significant correlation between pelvic obliquity and knee abduction moment. Nevertheless, considering that the P value was very close to being statistically significant (P ¼ .05), it is difficult to rule out the possible relationship between the 2 variables. It is important to note that trunk leaning might have affected the location of COM position relative to the knee joint, thereby masking the effects of pelvic motion on the knee abduction moment [18,23]. Such a confounding factor was not controlled in
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GMED Activity and Pelvic and Knee Stability
our study. It is also important to note that other factors such as lateral trunk leaning [46] and activation of other muscles that are involved with lumbar stabilization, including quadratus lumborum, multifidus, and internal oblique [47], may contribute to pelvic obliquity during the transition from double-limb to single-limb support. It is necessary to conduct further research on how GMED activation, trunk leaning, and lumbar stability affect pelvic obliquity and knee abduction moment to truly understand what determines the knee abduction moment of a supporting leg. This study has several limitations. The metronome used as a cue to move through the SLMS was determined to be a comfortable pace during pilot testing but may have disrupted natural movements, making it difficult to generalize the results to other activities. In addition, we did not analyze the descent of the SLMS. Asking participants to perform the descent was important, however, because it prompted them to maintain good single leg balance before descending. Finally, the results here reflect the neuromuscular control of healthy persons who were free of knee pain and/or disease. Further research into a population with knee pain and/or disease is needed to determine if this anticipatory neuromuscular control is altered and to appropriately extrapolate these findings to such a clinical population. Conclusions This study offers important information on the neuromuscular control of knee stability in a healthy population, which provides the basis for a comparison to a population with knee pain and/or disease. The relationship between timing and magnitude of activation related to knee abduction moment has not previously been compared in the same participants, healthy or clinical, thereby making our findings novel and relevant to clinicians. We found that increasing the magnitude of anticipatory activity in the GMED is important for reducing knee abduction moment and preventing pelvic drop during the single-leg stance phase of a SLMS. The results suggest that anticipatory GMED timing does not seem to significantly contribute to the change of knee abduction moment or pelvic obliquity during single-leg stance. Anticipatory GMED activity may have contributed to decreased knee abduction moment via its control over pelvic obliquity. To confirm such a mechanism, more research on the relationship between pelvic obliquity and knee abduction moment is warranted, in particular with other functional movements such as walking and/or the transition between sitting and standing. These findings can help clinicians focus rehabilitative efforts on increasing the strength of the gluteus medius and emphasizing, perhaps through EMGbased biofeedback training, an increased level of contraction before transitioning from double-leg to single-leg support to help prevent knee pain. Future
research is necessary to determine if/how neuromuscular control of the GMED on the pelvis and knee change with knee pain and/or disease, as well as if a therapeutic intervention focused on increasing GMED activation would be helpful in improving lower limb positioning and knee pain in a clinical population. Acknowledgments We sincerely thank Guido Van Ryssegem, Dr Junggi Hong, Dr Jonathan Farthing, and Dr Sandra Webber for providing practical insights. References 1. Bennell K, Bartam S, Crossley K, Green S. Outcome measures in patellofemoral pain syndrome: Test retest reliability and interrelationships. Phys Ther Sport 2000;1:32-41. 2. Ellis R, Hing W, Reid D. Iliotibial band friction syndrome: A systematic review. Man Ther 2007;12:200-208. 3. Tveit M, Rosengren BE, Nilsson J-A, Karlsson MK. Former male elite athletes have a higher prevalence of osteoarthritis and arthroplasty in the hip and knee than expected. Am J Sports Med 2012;40:527-533. 4. Srikanth VK, Fryer JL, Zhai G, Winzenberg TM, Hosmer D, Jones G. A meta-analysis of sex differences prevalence, incidence and severity of osteoarthritis. Osteoarthr Cartil 2005;13:769-781. 5. Taunton JE, Ryan MB, Clement DB, McKenzie DC, Lloyd-Smith DR, Zumbo BD. A retrospective case-control analysis of 2002 running injuries. Br J Sports Med 2002;36:95-101. 6. Van Der Waal JM, Terwee CB, Van Der Windt DAWM, Bouter LM, Dekker J. The impact of non-traumatic hip and knee disorders on health-related quality of life as measured with the SF-36 or SF-12. A systematic review. Qual Life Res 2005;14:1141-1155. 7. Lawrence RC, Helmick CG, Arnett FC, et al. Estimates of the prevalence of arthritis and selected musculoskeletal disorders in the United States. Arthritis Rheum 1998;41:778-799. 8. Ruffin IV MT, Kiningham RB. Anterior knee pain: The challenge of patellofemoral syndrome. Am Fam Physician 1993;47:185-194. 9. Thomas MJ, Wood L, Selfe J, Peat G. Anterior knee pain in younger adults as a precursor to subsequent patellofemoral osteoarthritis: A systematic review. BMC Musculoskelet Disord 2010;11:201. 10. Arroll B, Ellis-Pegler E, Edwards A, Sutcliffe G. Patellofemoral pain syndrome: A critical review of the clinical trials on nonoperative therapy. Am J Sports Med 1997;25:207-212. 11. Kettunen JA, Harilainen A, Sandelin J, et al. Knee arthroscopy and exercise versus exercise only for chronic patellofemoral pain syndrome: 5-year follow-up. Br J Sports Med 2012;46:243-246. 12. Chang A, Hayes K, Dunlop D, et al. Hip abduction moment and protection against medial tibiofemoral osteoarthritis progression. Arthritis Rheum 2005;52:3515-3519. 13. Powers CM, Ward SR, Fredericson M, Guillet M, Shellock FG. Patellofemoral kinematics during weight-bearing and non-weight-bearing knee extension in persons with lateral subluxation of the patella: A preliminary study. J Orthop Sports Phys Ther 2003;33:677-685. 14. Paoloni M, Mangone M, Fratocchi G, Murgia M, Maria Saraceni V, Santilli V. Kinematic and kinetic features of normal level walking in patellofemoral pain syndrome: More than a sagittal plane alteration. J Biomech 2010;43:1794-1798. 15. Miyazaki T, Wada M, Kawahara H, Sato M, Baba H, Shimada S. Dynamic load at baseline can predict radiographic disease progression in medial compartment knee osteoarthritis. Ann Rheum Dis 2002;61:617-622. 16. Sharma L, Song J, Felson DT, Cahue S, Shamiyeh E, Dunlop DD. The role of knee alignment in disease progression and functional decline in knee osteoarthritis. JAMA 2001;286:188-195.
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961 17. Tanamas S, Hanna FS, Cicuttini FM, Wluka AE, Berry P, 962 Urquhart DM. Does knee malalignment increase the risk of devel963 opment and progression of knee osteoarthritis? A systematic re964 view. Arthritis Care Res 2009;61:459-467. 965 18. Powers CM. The influence of abnormal hip mechanics on knee 966 injury: A biomechanical perspective. J Orthop Sports Phys Ther 967 968 2010;40:42-51. 969 19. Perry J. Gait Analysis: Normal and Pathological Function. vol. 970 Q2 12. 2010. 971 20. Rogers MW, Pai YC. Patterns of muscle activation accompanying 972 transitions in stance during rapid leg flexion. J Electromyogr 973 974 Kinesiol 1993;3:149-156. 975 21. Willson JD, Davis IS. Lower extremity mechanics of females with 976 and without patellofemoral pain across activities with progres977 sively greater task demands. Clin Biomech 2008;23:203-211. 978 22. Ward SR, Winters TM, Blemker SS. The architectural design of the 979 gluteal muscle group: Implications for movement and rehabilita980 981 tion. J Orthop Sports Phys Ther 2010;40:95-102. 982 23. Neumann DA. Kinesiology of the hip: A focus on muscular actions. 983 J Orthop Sports Phys Ther 2010;40:82-94. 984 24. Clark JM, Haynor DR. Anatomy of the abductor muscles of the hip 985 as studied by computed tomography. J Bone Joint Surg Am 1987; 986 69:1021-1031. 987 988 25. Kendall F, McCreary E, Kendall H. Muscles: Testing and Function. 989 3rd ed. Baltimore, MD: Williams and Wilkins; 1983. 990 26. Aminaka N, Pietrosimone BG, Armstrong CW, Meszaros A, 991 Gribble PA. Patellofemoral pain syndrome alters neuromuscular 992 control and kinetics during stair ambulation. J Electromyogr 993 994 Kinesiol 2011;21:645-651. 995 27. Brindle T, Mattacola C, McCrory J. Electromyographic changes in 996 the gluteus medius during stair ascent and descent in subjects with 997 anterior knee pain. Knee Surg Sports Traumatol Arthrosc 2003;11: 998 244-251. 999 28. Willson JD, Kernozek TW, Arndt RL, Reznichek DA, Scott Straker J. 1000 1001 Gluteal muscle activation during running in females with and with1002 out patellofemoral pain syndrome. Clin Biomech 2011;26:735-740. 1003 29. Cowan SM, Crossley KM, Bennell KL. Altered hip and trunk muscle 1004 function in individuals with patellofemoral pain. Br J Sports Med 1005 2009;43:584-588. 1006 30. Cavanagh PR, Komi PV. Electromechanical delay in human skeletal 1007 1008 muscle under concentric and eccentric contractions. Eur J Appl 1009 Physiol Occup Physiol 1979;42:159-163. 1010 31. Elias LJ, Bryden MP, Bulman-Fleming MB. Footedness is a better 1011 predictor than is handedness of emotional lateralization. Neuro1012 psychologia 1998;36:37-43. 1013 1014 32. Ageberg E, Bennell KL, Hunt MA, Simic M, Roos EM, Creaby MW. 1015 Validity and inter-rater reliability of medio-lateral knee motion 1016 1017 1018 1019 Disclosure 1020 1021 1022 D.K. College of Kinesiology, University of Saskatchewan, 87 Campus Drive, 1023 Saskatoon, Saskatchewan, S7N 5B2, Canada 1024 Disclosure: MSc program funding, College of Graduate Studies and Research and 1025 the College of Kinesiology, University of Saskatchewan 1026 1027 J.U. College of Kinesiology, University of Saskatchewan, 87 Campus Drive, 1028 Saskatoon, Saskatchewan, S7N 5B2, Canada 1029 Disclosure: nothing to disclose 1030 1031 1032 J.L.L. College of Kinesiology, University of Saskatchewan, 87 Campus Drive, 1033 Saskatoon, Saskatchewan, S7N 5B2, Canada 1034 Disclosures related to this publication: grant, Saskatchewan Health Research 1035 Foundation (money to institution); disclosures outside this publication: grants/ 1036 grants pending, Saskatchewan Health Research Foundation, Royal University 1037 Hospital Foundation (money to institution) 1038 1039 1040
33.
34.
35. 36. 37.
38. 39.
40. 41.
42. 43.
44.
45.
46.
47.
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1041 observed during a single-limb mini squat. BMC Musculoskelet 1042 Disord 2010;11:265. Crossley KM, Zhang W-J, Schache AG, Bryant A, Cowan SM. Per- 1043 1044 formance on the single-leg squat task indicates hip abductor 1045 muscle function. Am J Sports Med 2011;39:866-873. 1046 Hermens H, Freriks B, Disselhorst-Klug C, Rau G. The SENIAM 1047 project: Surface electromyography for non-invasive assessment of 1048 Q3 1049 muscle. ISEK Congress 2002. 1050 Criswell E. Cram’s Introduction to Surface Electromyography. 2nd 1051 ed. Sudbury, MA: Jones and Bartlett Publishers; 2010. 1052 Delp SL, Hess WE, Hungerford DS, Jones LC. Variation of rotation 1053 1054 moment arms with hip flexion. J Biomech 1999;32:493-501. Brophy R, Silvers HJ, Gonzales T, Mandelbaum BR. Gender in- 1055 fluences: The role of leg dominance in ACL injury among soccer 1056 1057 players. Br J Sports Med 2010;44:694-697. 1058 Schwartz MH, Rozumalski A. A new method for estimating joint 1059 parameters from motion data. J Biomech 2005;38:107-116. 1060 1061 Wu G, Siegler S, Allard P, et al. ISB recommendation on definitions of joint coordinate system of various joints for the reporting of 1062 human joint motiondpart I: Ankle, hip, and spine. International 1063 1064 Society of Biomechanics. J Biomech 2002;35:543-548. 1065 De Leva P. Adjustments to Zatsiorsky-Seluyanov’s segment inertia 1066 parameters. J Biomech 1996;29:1223-1230. 1067 Bolgla LA, Malone TR, Umberger BR, Uhl TL. Reliability of elec- 1068 tromyographic methods used for assessing hip and knee neuro- 1069 1070 muscular activity in females diagnosed with patellofemoral pain 1071 syndrome. J Electromyogr Kinesiol 2010;20:142-147. 1072 Kim JW, Kwon Y, Chung HY, et al. Age-sex differences in the hip 1073 1074 abductor muscle properties. Geriatr Gerontol Int 2011;11:333-340. 1075 Hirschfeld H, Forssberg H. Phase-dependent modulations of 1076 anticipatory postural activity during human locomotion. J Neuro1077 physiol 1991;66:12-19. 1078 Liu Y, Peng CH, Wei SH, Chi JC, Tsai FR, Chen JY. Active leg 1079 stiffness and energy stored in the muscles during maximal counter 1080 movement jump in the aged. J Electromyogr Kinesiol 2006;16: 1081 1082 342-351. Yao W, Fuglevand RJ, Enoka RM. Motor-unit synchronization 1083 1084 increases EMG amplitude and decreases force steadiness of simu- 1085 lated contractions. J Neurophysiol 2000;83:441-452. 1086 Hunt MA, Birmingham TB, Bryant D, et al. Lateral trunk lean 1087 explains variation in dynamic knee joint load in patients with 1088 medial compartment knee osteoarthritis. Osteoarthr Cartil 2008; 1089 1090 16:591-599. 1091 Cynn HS, Oh JS, Kwon OY, Yi CH. Effects of lumbar stabilization 1092 using a pressure biofeedback unit on muscle activity and lateral 1093 pelvic tilt during hip abduction in sidelying. Arch Phys Med Rehabil 1094 1095 2006;87:1454-1458.
A.O. College of Kinesiology, University of Saskatchewan, 87 Campus Drive, Saskatoon, Saskatchewan, S7N 5B2, Canada. Address correspondence to: A.O.; e-mail: [email protected] Disclosures related to this publication: grant, New Faculty Graduate Student funding (money to institution); Disclosures outside this publication: grants/ grants pending, Saskatchewan Health Research Foundation, Rick Hansen Institute (money to institution) Submitted for publication January 2, 2015; accepted June 5, 2015.
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Original Research
The Relationship of Anticipatory Gluteus Medius Activity to Pelvic and Knee Stability in the Transition to Single-Leg Stance Daehan Kim, MSc, Janelle Unger, BSc, Joel L. Lanovaz, PhD, Alison Oates, PhD
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GMED Activity and Pelvic and Knee Stability
pelvic drop and subsequent increases of the knee abduction moment, previous research has focused on elucidating the role of the hip abductors in stabilizing frontal plane pelvic posture [22,23]. Because it has the largest physiological crosssectional area among the hip abductors, the gluteus medius (GMED) mainly provides frontal plane pelvic stability [22,24,25]. Several studies have shown that persons with PFP have delayed onset of GMED activation compared with healthy persons [26-29]. Importantly, the authors of one of these studies reported that subjects with PFP showed both delayed GMED onset and increased knee abduction moment compared with healthy subjects [26], but the relationship between the onset of GMED and the increased knee abduction moment was not investigated. Given that an inevitable delay exists between the onset of muscle activity and force development of a muscle group [30], anticipatory activation of GMED appears crucial to control pelvic drop for the transition from single-leg to double-leg stance. It is important to elucidate how anticipatory GMED activation, in terms of onset timing and activation magnitude during a double-leg to single-leg support transition, controls frontal plane pelvic motion and the knee abduction moment. Knee disease and pain may alter the way someone moves, which then confounds the understanding of whether a change in movements caused the pain or if pain caused the change in movement; therefore, it is important to first investigate the neural control of a healthy, disease- and pain-free population to establish a normal pattern of control. The aim of this study was to examine the relationship of anticipatory GMED activity with frontal plane pelvic motion and the knee abduction moment. This correlation was measured when participants transitioned from double-leg to single-leg support while performing a single-leg mini squat. Anticipatory GMED activity was defined as activity prior to toe-off of the nonsupporting leg. We hypothesized that an earlier onset and greater magnitude of the anticipatory GMED activity of the supporting leg would be significantly correlated with decreased pelvic drop and reduced knee abduction moment of the same leg.
Eligibility to participate was determined through a prescreening questionnaire. This research protocol was reviewed and approved by the institutional research ethics board. Informed consent was obtained before beginning the testing protocol for all participants. Instrumentation Leg dominance was identified using a Modified Waterloo Footedness Questionnaire [31]. Participants rated which leg they most often used for object manipulation tasks (ie, the dominant leg), as well as for providing support (the nondominant leg). Three-dimensional (3D) kinematic data from the pelvis and lower limbs were collected using a motion capture system (Vicon Nexus, Vicon Motion Systems, Los Angeles, CA), and ground reaction forces (GRFs) were measured using force platforms under each foot (OR6, Advanced Mechanical Technology, Inc, Watertown, MA) while the participants performed single-leg mini squats (SLMS). Kinematic data and GRF data were collected at a sampling rate of 100 and 2000 Hz, respectively. An SLMS is a commonly used clinical screening tool for assessing frontal plane pelvic and knee movement during weight bearing that is functionally similar to stair negotiation [32]. Furthermore, the quality of SLMS performance can reliably represent the functional quality of GMED activation [33]. To perform the SLMS, participants first transitioned from double-leg to singleleg standing, and then lowered their body by flexing their hip, knee, and ankle (Figure 1). Surface electromyography (EMG; 2400GT2, Noraxon Inc, Scottsdale, AZ), sampled at 2000 Hz, was used to record the muscle activity of the GMED [34,35] during the movement. Testing Protocol An initial 60-second quiet standing trial was collected to obtain baseline EMG values. Participants then performed a total of 32 SLMS. Movement speed was standardized using the beat of a metronome set at 80 beats per minute: At the first beat, the participant lifted her toe off the force platform to make the transition from
Methods Participants Participants in this study were 20 healthy women between the ages of 18 and 39 years (mean, 22.6 years; standard deviation [SD], 2.5). Because pain, injuries, and knowledge of movement mechanics may modify the movement pattern of the participants, participant selection was limited to healthy women who did not have a history of knee and ankle ligament injuries, any indication of current knee, hip, and/or low back pain, and/or knowledge of the proper squat technique.
Figure 1. Sequential movement events.
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double- to single-leg stance. At the next beat she descended her body to the lowest position of the SLMS. Naturally, each participant needed time to stabilize herself on one leg before initiating the descent. Such time between toe-off and initiation of descent was defined as the single-leg stance phase. As a result, the SLMS was broken down into 3 phases (Figure 1): (1) double-leg stance, (2) single-leg stance, and (3) descent. Participants were instructed to keep their arms crossed on their chest for the entire movement. Sixteen SLMS were performed on each leg, with the order of the supporting leg randomized but limited to a maximum of 4 in a row on the same leg. The participants were given instructions for the SLMS and allowed to practice the movement at least 5 times for familiarization before starting. If the participant needed more than 10 practices, at least 1 minute of rest was given after the 10 practices to prevent fatigue. She was also allowed to rest between trials to prevent fatigue. Data Analysis The analysis in this study focused on the transition from double-leg to single-leg stance to investigate anticipatory GMED control. The descent of the SLMS was not included in the analysis because it is well established that GMED activation is more involved in transverse rotation of the hip rather than frontal plane rotation of the pelvis when the hip is flexed [23,36]. All analyses focused on the nondominant leg because this leg is more likely than the dominant leg to be involved in stability-related tasks during daily activities [31,37]. Kinematic and kinetic data were processed using a 4th order Butterworth digital filter, Visual 3D (C-Motion, Inc., Kingston, Ontario, Canada) and custom MATLAB (R2006b for PC, MathWorks, Natick, MA) routines. The 3D marker trajectories and GRF data were low-pass filtered at a cutoff frequency of 8 and 250 Hz, respectively. Toe-off was identified using GRFs. Toe-off was defined as the point when the vertical force dropped below a threshold value defined as 2 SDs of the zero load force tracing. This toe-off timing defined the end of the double-leg stance and the start of the single-leg stance. A virtual pelvic center marker midway between the bilateral anterior superior iliac spine and posterior superior iliac spine was used for detecting when a participant initiated the descent phase. Descent start was defined as the first point when the vertical velocity of the pelvic center marker became negative. The hip and knee joint center were identified using the functional calibration data according to the method described by Schwartz and Rozumalski [38]. Standard 3D rigid body analyses were performed for the lower limb, with anatomic axes defined using joint centers [39] and segmental kinematics tracked with 4 marker rigid clusters on each segment.
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The frontal plane angle of the pelvis was defined by the vertical axis of the laboratory and the line connecting the hip joint center and midway between the left anterior superior iliac spine and posterior superior iliac spine. To quantify the pelvic obliquity occurring during single-leg stance, the net change of pelvic angle between toe-off and initiation of descent was calculated. An increase in the pelvic angle represented pelvic obliquity, whereas a decrease in the angle represented pelvic drop. Inverse dynamics were used to calculate the net resultant internal knee abduction moment. The principle moments of inertia, the segment masses, and the locations of the COM of each segment were obtained from anthropometric tables [40]. The joint moment was normalized to participants’ weight and height. The net change of the knee abduction moment during single-leg stance was included in the data analysis. EMG data was high-pass filtered at 10 Hz, fully rectified, and then low-pass filtered at 50 Hz [41]. The electromechanical delay between the GMED onset and the generation of force during an SLMS has not previously been reported; therefore, the GMED activity integrated over 60 msec prior to toe-off was chosen as a measure of anticipatory activation based on studies of other activities, including comfortable walking [42,43]. These EMG magnitudes were normalized to the EMG integrated over 30 msec around the largest peak burst of EMG throughout all trials [44]. GMED onset was calculated using a threshold of 1.5 times the mean amplitude value of the quiet standing trial. EMG amplitudes were required to exceed the threshold for a minimum of 65 msec. Statistical Analysis Data were analyzed using SPSS versions 19.0 and 22 (IBM Corp, Armonk, NY) with an a level set at 0.05. Normal distribution of the data was tested using the Shapiro-Wilk test, skewness, and kurtosis analyses. The mean of the normally distributed data and the median of the non-normal data were used as the representative samples. Correlation statistics were used to examine if the GMED activation timing and magnitude on the supporting leg were significantly related to the pelvic obliquity and knee abduction moment of the same leg. In addition, the relationship between pelvic obliquity and knee abduction moment was examined to confirm if pelvic motion contributes to the change of knee abduction moment. Spearman’s rho (two-tailed) was used to determine the correlation coefficients to better fit the nonlinear relationship between the variables [45]. Results All 20 participants showed onset of the GMED before toe-off of the nonsupporting leg (Figure 2). Table 1 shows the mean and SD of the outcome variables. The GMED onset occurred on average 330 133 msec before
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GMED Activity and Pelvic and Knee Stability
Figure 2. Gluteus medius (GMED) activation, pelvic motion, and knee kinetic patterns by movement phases. Data represent average values of all trials for a representative participant. Data from different trials were synchronized in reference to the percentage of total duration of each phase. The gray areas represent one standard deviation from the mean. The thick vertical line depicts 60 msec before toe-off. EMG ¼ electromyography.
toe-off, and the GMED remained activated until the completion of each trial. All participants demonstrated pelvic obliquity instead of pelvic drop at toe-off. Statistical analyses showed that the magnitude of GMED activity over 60 msec prior to toe-off was negatively correlated with net change of knee abduction moment (rs (18) ¼ 0.303, P < .001) and positively correlated with pelvic obliquity (rs (18) ¼ 0.361, P < .001) (Figure 3). This finding indicates that the participants who had greater activity levels of GMED more than 60 msec before toe-off experienced greater pelvic obliquity and less increase of knee abduction moment during the single-leg stance phase. On the other hand, the onset of GMED was not significantly correlated with net change of knee abduction moment (rs (18) ¼ 0.109, P ¼ .105) or pelvic obliquity (rs (18) ¼ 0.058, P ¼ .389). The net change of pelvic obliquity and knee abduction moment were not significantly correlated with each other; however, the P value was very close to being statistically significant (rs (18) ¼ 0.442, P ¼ .05).
Discussion The purpose of this study was to determine the relationship between anticipatory GMED activity and Table 1 Descriptive data of gluteus medius onset, pelvic obliquity, and knee abduction moment during the transition to single-leg stance Variables
Mean SD
GMED onset
330 133 msec before toe-off 0.23 0.11
Normalized GMED EMG magnitude over 60 msec before toe-off (ratio of integrated EMG over 60 msec before toe-off to integrated EMG over 60 msec around the peak burst) Net change of pelvic obliquity during single-leg stance Net change of knee abduction moment during single-leg stance
3.81 1.24 ( ) 0.049 0.06 (Nm/Kg $ m)
EMG ¼ electromyography; GMED ¼ gluteus medius; SD ¼ standard deviation.
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Figure 3. The relationship of anticipatory gluteus medius (GMED) activation magnitude to knee abduction moment and pelvic obliquity during single-leg stance. EMG ¼ electromyography.
frontal plane pelvic motion and knee moment during the single-leg stance phase of a SLMS. GMED activation prior to toe-off is critical to stabilize the pelvis when it loses the support from one leg. Our results indicated that increased anticipatory GMED activation magnitude was significantly correlated with increased pelvic obliquity and decreased knee abduction moment, whereas GMED onset timing was not significantly correlated with pelvic obliquity or knee abduction moment. These results suggest that the magnitude and not the timing of GMED activation is a more important factor for protecting against excessive pelvic drop and knee abduction moment when moving from double-leg to single-leg support in healthy persons. Importantly, these results provide insights regarding how training for neuromuscular control of the GMED could be provided in a rehabilitation setting: By emphasizing the magnitude of GMED contraction before transitioning from double- to single-leg stance, lower limb positioning may be improved and knee pain may be reduced. To our knowledge, this study is the first to investigate how GMED activation is related with both dynamic pelvic posture and knee abduction moment in a weightbearing limb. Aminaka et al [26] reported that patients with PFP had both delayed GMED onset and greater knee abduction moment compared with healthy participants during a stair descent. These authors suggested a need to investigate a possible association between the GMED onset and knee abduction moment; however, our study could not support the correlation between these 2 variables. It is important to note that Aminaka et al [26] used different reference events for calculating GMED onset: GMED onset was calculated relative to toecontact of the stance leg. The functional demands on
the GMED for preventing excessive knee abduction moment at toe-contact on stair descent can be fundamentally different from that at toe-off in a double-leg to single-leg transition. Toe-off during the SLMS in our study is a critical event at which pelvic drop could rapidly influence the knee abduction moment. GMED onset occurred on average 330 msec before toe-off, and all participants demonstrated pelvic obliquity; therefore, the GMED was likely activated voluntarily in anticipation of toe-off [45] with sufficient time to generate the force required to prevent pelvic drop and even counter with slight pelvic obliquity. Previous studies [12,18,19] have only theorized that frontal plane pelvic motion would affect the knee abduction moment in a stance leg; the relationship between the 2 variables have not been directly examined prior to our study, which provides the unique assessment of the relationship between the pelvis and knee frontal plane movement. Given that GMED activation directly affects the pelvic motion, the relationship between anticipatory GMED activation and knee abduction moment could have been mediated by frontal plane pelvic motion; however, our study could not confirm such a theory because there was no significant correlation between pelvic obliquity and knee abduction moment. Nevertheless, considering that the P value was very close to being statistically significant (P ¼ .05), it is difficult to rule out the possible relationship between the 2 variables. It is important to note that trunk leaning might have affected the location of COM position relative to the knee joint, thereby masking the effects of pelvic motion on the knee abduction moment [18,23]. Such a confounding factor was not controlled in
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GMED Activity and Pelvic and Knee Stability
our study. It is also important to note that other factors such as lateral trunk leaning [46] and activation of other muscles that are involved with lumbar stabilization, including quadratus lumborum, multifidus, and internal oblique [47], may contribute to pelvic obliquity during the transition from double-limb to single-limb support. It is necessary to conduct further research on how GMED activation, trunk leaning, and lumbar stability affect pelvic obliquity and knee abduction moment to truly understand what determines the knee abduction moment of a supporting leg. This study has several limitations. The metronome used as a cue to move through the SLMS was determined to be a comfortable pace during pilot testing but may have disrupted natural movements, making it difficult to generalize the results to other activities. In addition, we did not analyze the descent of the SLMS. Asking participants to perform the descent was important, however, because it prompted them to maintain good single leg balance before descending. Finally, the results here reflect the neuromuscular control of healthy persons who were free of knee pain and/or disease. Further research into a population with knee pain and/or disease is needed to determine if this anticipatory neuromuscular control is altered and to appropriately extrapolate these findings to such a clinical population. Conclusions This study offers important information on the neuromuscular control of knee stability in a healthy population, which provides the basis for a comparison to a population with knee pain and/or disease. The relationship between timing and magnitude of activation related to knee abduction moment has not previously been compared in the same participants, healthy or clinical, thereby making our findings novel and relevant to clinicians. We found that increasing the magnitude of anticipatory activity in the GMED is important for reducing knee abduction moment and preventing pelvic drop during the single-leg stance phase of a SLMS. The results suggest that anticipatory GMED timing does not seem to significantly contribute to the change of knee abduction moment or pelvic obliquity during single-leg stance. Anticipatory GMED activity may have contributed to decreased knee abduction moment via its control over pelvic obliquity. To confirm such a mechanism, more research on the relationship between pelvic obliquity and knee abduction moment is warranted, in particular with other functional movements such as walking and/or the transition between sitting and standing. These findings can help clinicians focus rehabilitative efforts on increasing the strength of the gluteus medius and emphasizing, perhaps through EMGbased biofeedback training, an increased level of contraction before transitioning from double-leg to single-leg support to help prevent knee pain. Future
research is necessary to determine if/how neuromuscular control of the GMED on the pelvis and knee change with knee pain and/or disease, as well as if a therapeutic intervention focused on increasing GMED activation would be helpful in improving lower limb positioning and knee pain in a clinical population. Acknowledgments We sincerely thank Guido Van Ryssegem, Dr Junggi Hong, Dr Jonathan Farthing, and Dr Sandra Webber for providing practical insights. References 1. Bennell K, Bartam S, Crossley K, Green S. Outcome measures in patellofemoral pain syndrome: Test retest reliability and interrelationships. Phys Ther Sport 2000;1:32-41. 2. Ellis R, Hing W, Reid D. Iliotibial band friction syndrome: A systematic review. Man Ther 2007;12:200-208. 3. Tveit M, Rosengren BE, Nilsson J-A, Karlsson MK. Former male elite athletes have a higher prevalence of osteoarthritis and arthroplasty in the hip and knee than expected. Am J Sports Med 2012;40:527-533. 4. Srikanth VK, Fryer JL, Zhai G, Winzenberg TM, Hosmer D, Jones G. A meta-analysis of sex differences prevalence, incidence and severity of osteoarthritis. Osteoarthr Cartil 2005;13:769-781. 5. Taunton JE, Ryan MB, Clement DB, McKenzie DC, Lloyd-Smith DR, Zumbo BD. A retrospective case-control analysis of 2002 running injuries. Br J Sports Med 2002;36:95-101. 6. Van Der Waal JM, Terwee CB, Van Der Windt DAWM, Bouter LM, Dekker J. The impact of non-traumatic hip and knee disorders on health-related quality of life as measured with the SF-36 or SF-12. A systematic review. Qual Life Res 2005;14:1141-1155. 7. Lawrence RC, Helmick CG, Arnett FC, et al. Estimates of the prevalence of arthritis and selected musculoskeletal disorders in the United States. Arthritis Rheum 1998;41:778-799. 8. Ruffin IV MT, Kiningham RB. Anterior knee pain: The challenge of patellofemoral syndrome. Am Fam Physician 1993;47:185-194. 9. Thomas MJ, Wood L, Selfe J, Peat G. Anterior knee pain in younger adults as a precursor to subsequent patellofemoral osteoarthritis: A systematic review. BMC Musculoskelet Disord 2010;11:201. 10. Arroll B, Ellis-Pegler E, Edwards A, Sutcliffe G. Patellofemoral pain syndrome: A critical review of the clinical trials on nonoperative therapy. Am J Sports Med 1997;25:207-212. 11. Kettunen JA, Harilainen A, Sandelin J, et al. Knee arthroscopy and exercise versus exercise only for chronic patellofemoral pain syndrome: 5-year follow-up. Br J Sports Med 2012;46:243-246. 12. Chang A, Hayes K, Dunlop D, et al. Hip abduction moment and protection against medial tibiofemoral osteoarthritis progression. Arthritis Rheum 2005;52:3515-3519. 13. Powers CM, Ward SR, Fredericson M, Guillet M, Shellock FG. Patellofemoral kinematics during weight-bearing and non-weight-bearing knee extension in persons with lateral subluxation of the patella: A preliminary study. J Orthop Sports Phys Ther 2003;33:677-685. 14. Paoloni M, Mangone M, Fratocchi G, Murgia M, Maria Saraceni V, Santilli V. Kinematic and kinetic features of normal level walking in patellofemoral pain syndrome: More than a sagittal plane alteration. J Biomech 2010;43:1794-1798. 15. Miyazaki T, Wada M, Kawahara H, Sato M, Baba H, Shimada S. Dynamic load at baseline can predict radiographic disease progression in medial compartment knee osteoarthritis. Ann Rheum Dis 2002;61:617-622. 16. Sharma L, Song J, Felson DT, Cahue S, Shamiyeh E, Dunlop DD. The role of knee alignment in disease progression and functional decline in knee osteoarthritis. JAMA 2001;286:188-195.
FLA 5.2.0 DTD PMRJ1515_proof 30 June 2015 10:32 pm ce
881 882 883 884 885 886 887 888 889 890 891 892 893 894 895 896 897 898 899 900 901 902 903 904 905 906 907 908 909 910 911 912 913 914 915 916 917 918 919 920 921 922 923 924 925 926 927 928 929 930 931 932 933 934 935 936 937 938 939 940 941 942 943 944 945 946 947 948 949 950 951 952 953 954 955 956 957 958 959 960
D. Kim et al. / PM R XXX (2015) 1-7
961 17. Tanamas S, Hanna FS, Cicuttini FM, Wluka AE, Berry P, 962 Urquhart DM. Does knee malalignment increase the risk of devel963 opment and progression of knee osteoarthritis? A systematic re964 view. Arthritis Care Res 2009;61:459-467. 965 18. Powers CM. The influence of abnormal hip mechanics on knee 966 injury: A biomechanical perspective. J Orthop Sports Phys Ther 967 968 2010;40:42-51. 969 19. Perry J. Gait Analysis: Normal and Pathological Function. vol. 970 Q2 12. 2010. 971 20. Rogers MW, Pai YC. Patterns of muscle activation accompanying 972 transitions in stance during rapid leg flexion. J Electromyogr 973 974 Kinesiol 1993;3:149-156. 975 21. Willson JD, Davis IS. Lower extremity mechanics of females with 976 and without patellofemoral pain across activities with progres977 sively greater task demands. Clin Biomech 2008;23:203-211. 978 22. Ward SR, Winters TM, Blemker SS. The architectural design of the 979 gluteal muscle group: Implications for movement and rehabilita980 981 tion. J Orthop Sports Phys Ther 2010;40:95-102. 982 23. Neumann DA. Kinesiology of the hip: A focus on muscular actions. 983 J Orthop Sports Phys Ther 2010;40:82-94. 984 24. Clark JM, Haynor DR. Anatomy of the abductor muscles of the hip 985 as studied by computed tomography. J Bone Joint Surg Am 1987; 986 69:1021-1031. 987 988 25. Kendall F, McCreary E, Kendall H. Muscles: Testing and Function. 989 3rd ed. Baltimore, MD: Williams and Wilkins; 1983. 990 26. Aminaka N, Pietrosimone BG, Armstrong CW, Meszaros A, 991 Gribble PA. Patellofemoral pain syndrome alters neuromuscular 992 control and kinetics during stair ambulation. J Electromyogr 993 994 Kinesiol 2011;21:645-651. 995 27. Brindle T, Mattacola C, McCrory J. Electromyographic changes in 996 the gluteus medius during stair ascent and descent in subjects with 997 anterior knee pain. Knee Surg Sports Traumatol Arthrosc 2003;11: 998 244-251. 999 28. Willson JD, Kernozek TW, Arndt RL, Reznichek DA, Scott Straker J. 1000 1001 Gluteal muscle activation during running in females with and with1002 out patellofemoral pain syndrome. Clin Biomech 2011;26:735-740. 1003 29. Cowan SM, Crossley KM, Bennell KL. Altered hip and trunk muscle 1004 function in individuals with patellofemoral pain. Br J Sports Med 1005 2009;43:584-588. 1006 30. Cavanagh PR, Komi PV. Electromechanical delay in human skeletal 1007 1008 muscle under concentric and eccentric contractions. Eur J Appl 1009 Physiol Occup Physiol 1979;42:159-163. 1010 31. Elias LJ, Bryden MP, Bulman-Fleming MB. Footedness is a better 1011 predictor than is handedness of emotional lateralization. Neuro1012 psychologia 1998;36:37-43. 1013 1014 32. Ageberg E, Bennell KL, Hunt MA, Simic M, Roos EM, Creaby MW. 1015 Validity and inter-rater reliability of medio-lateral knee motion 1016 1017 1018 1019 Disclosure 1020 1021 1022 D.K. College of Kinesiology, University of Saskatchewan, 87 Campus Drive, 1023 Saskatoon, Saskatchewan, S7N 5B2, Canada 1024 Disclosure: MSc program funding, College of Graduate Studies and Research and 1025 the College of Kinesiology, University of Saskatchewan 1026 1027 J.U. College of Kinesiology, University of Saskatchewan, 87 Campus Drive, 1028 Saskatoon, Saskatchewan, S7N 5B2, Canada 1029 Disclosure: nothing to disclose 1030 1031 1032 J.L.L. College of Kinesiology, University of Saskatchewan, 87 Campus Drive, 1033 Saskatoon, Saskatchewan, S7N 5B2, Canada 1034 Disclosures related to this publication: grant, Saskatchewan Health Research 1035 Foundation (money to institution); disclosures outside this publication: grants/ 1036 grants pending, Saskatchewan Health Research Foundation, Royal University 1037 Hospital Foundation (money to institution) 1038 1039 1040
33.
34.
35. 36. 37.
38. 39.
40. 41.
42. 43.
44.
45.
46.
47.
7
1041 observed during a single-limb mini squat. BMC Musculoskelet 1042 Disord 2010;11:265. Crossley KM, Zhang W-J, Schache AG, Bryant A, Cowan SM. Per- 1043 1044 formance on the single-leg squat task indicates hip abductor 1045 muscle function. Am J Sports Med 2011;39:866-873. 1046 Hermens H, Freriks B, Disselhorst-Klug C, Rau G. The SENIAM 1047 project: Surface electromyography for non-invasive assessment of 1048 Q3 1049 muscle. ISEK Congress 2002. 1050 Criswell E. Cram’s Introduction to Surface Electromyography. 2nd 1051 ed. Sudbury, MA: Jones and Bartlett Publishers; 2010. 1052 Delp SL, Hess WE, Hungerford DS, Jones LC. Variation of rotation 1053 1054 moment arms with hip flexion. J Biomech 1999;32:493-501. Brophy R, Silvers HJ, Gonzales T, Mandelbaum BR. Gender in- 1055 fluences: The role of leg dominance in ACL injury among soccer 1056 1057 players. Br J Sports Med 2010;44:694-697. 1058 Schwartz MH, Rozumalski A. A new method for estimating joint 1059 parameters from motion data. J Biomech 2005;38:107-116. 1060 1061 Wu G, Siegler S, Allard P, et al. ISB recommendation on definitions of joint coordinate system of various joints for the reporting of 1062 human joint motiondpart I: Ankle, hip, and spine. International 1063 1064 Society of Biomechanics. J Biomech 2002;35:543-548. 1065 De Leva P. Adjustments to Zatsiorsky-Seluyanov’s segment inertia 1066 parameters. J Biomech 1996;29:1223-1230. 1067 Bolgla LA, Malone TR, Umberger BR, Uhl TL. Reliability of elec- 1068 tromyographic methods used for assessing hip and knee neuro- 1069 1070 muscular activity in females diagnosed with patellofemoral pain 1071 syndrome. J Electromyogr Kinesiol 2010;20:142-147. 1072 Kim JW, Kwon Y, Chung HY, et al. Age-sex differences in the hip 1073 1074 abductor muscle properties. Geriatr Gerontol Int 2011;11:333-340. 1075 Hirschfeld H, Forssberg H. Phase-dependent modulations of 1076 anticipatory postural activity during human locomotion. J Neuro1077 physiol 1991;66:12-19. 1078 Liu Y, Peng CH, Wei SH, Chi JC, Tsai FR, Chen JY. Active leg 1079 stiffness and energy stored in the muscles during maximal counter 1080 movement jump in the aged. J Electromyogr Kinesiol 2006;16: 1081 1082 342-351. Yao W, Fuglevand RJ, Enoka RM. Motor-unit synchronization 1083 1084 increases EMG amplitude and decreases force steadiness of simu- 1085 lated contractions. J Neurophysiol 2000;83:441-452. 1086 Hunt MA, Birmingham TB, Bryant D, et al. Lateral trunk lean 1087 explains variation in dynamic knee joint load in patients with 1088 medial compartment knee osteoarthritis. Osteoarthr Cartil 2008; 1089 1090 16:591-599. 1091 Cynn HS, Oh JS, Kwon OY, Yi CH. Effects of lumbar stabilization 1092 using a pressure biofeedback unit on muscle activity and lateral 1093 pelvic tilt during hip abduction in sidelying. Arch Phys Med Rehabil 1094 1095 2006;87:1454-1458.
A.O. College of Kinesiology, University of Saskatchewan, 87 Campus Drive, Saskatoon, Saskatchewan, S7N 5B2, Canada. Address correspondence to: A.O.; e-mail: [email protected] Disclosures related to this publication: grant, New Faculty Graduate Student funding (money to institution); Disclosures outside this publication: grants/ grants pending, Saskatchewan Health Research Foundation, Rick Hansen Institute (money to institution) Submitted for publication January 2, 2015; accepted June 5, 2015.
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