Reliability of electromyographic methods used for assessing hip and knee neuromuscular activity in females diagnosed with patellofemoral pain syndrome

https://doi.org/10.1016/j.jelekin.2008.11.008Get rights and content

Abstract

Patellofemoral pain syndrome (PFPS) is one of the most common, yet misunderstood, knee pathologies. PFPS is thought to result from abnormal patella tracking caused from altered neuromuscular control. Researchers have investigated neuromuscular influences from the gluteus medius (GM), vastus medialis (VM), and vastus lateralis (VL) but with inconsistent findings. A reason for these discrepancies may be from varying methodology. The purpose of this study was to determine the reliability of electromyographic (EMG) methods used to assess amplitudes and timing differences of the GM, VM, and VL in subjects with PFPS. Seven females with PFPS participated. GM, VM, and VL activity was assessed during the stance phase of a stair descent task on two separate occasions. Amplitudes during the different intervals of stance were recorded and expressed as a percent of each muscle’s maximum voluntary isometric contraction. Muscle onsets at the beginning of stair descent were also determined. VM–GM, VL–GM, and VL–VM onset timing differences were quantified. Intraclass correlation coefficients (ICCs) and standard errors of measurement (SEMs) were calculated to assess between-day reliability. Most EMG measures had acceptable reliability (ICC3,5  0.70). Although some measures had moderate reliability (ICC < 0.70), they had low SEMs, which suggested high measurement precision. These findings support using these methods for examining neuromuscular activity in subjects with PFPS.

Introduction

Patellofemoral pain syndrome (PFPS) represents a commonly seen and clinically challenging pathology (Wilk et al., 1998). Dye et al. (1999) described PFPS as the “Black Hole of Orthopaedics” because of its misunderstood etiology. Fulkerson (2002) has described abnormal patella tracking within the femoral trochlea as a possible cause of PFPS. Abnormal tracking may result from reduced vastus medialis (VM) muscle activity relative to the vastus lateralis (VL) as well as delayed onset of the VM relative to the VL (Cowan et al., 2002, Grabiner et al., 1994). More recent investigations (Brindle et al., 2003, Ireland et al., 2003, Powers et al., 2003, Boling et al., 2006) have focused on the influence of the hip on knee function. Brindle et al. (2003) have reported a delay in gluteus medius (GM) activation relative to the VM and VL and concluded that altered GM activity may adversely affect knee function.

A current review of the literature has shown discrepancies regarding VM and VL amplitudes and onset timing differences in subjects with and without PFPS during stair descent. One reason for such discrepancies may result from the way that data were expressed or analyzed. Powers et al., 1996, Souza and Gross, 1991 determined the average amplitude of the VM and VL throughout the entire cycle of stair descent for subjects with and without PFPS and did not report group differences. Alternatively, Mohr et al. (2003) assessed amplitudes for each 2% interval of stair descent. They reported greater VM and VL amplitudes in subjects with PFPS from patella instability, especially during the loading response interval of stair descent. This finding suggested that assessing amplitudes over discrete intervals may represent a more sensitive manner for identifying differences (Salsich et al., 2002).

Others have determined either the peak (Sheehy et al., 1998) or average (Souza and Gross, 1991) VM and VL activity during stair descent and expressed these values as a VM to VL ratio. Subjects with and without PFPS in these studies had similar ratios. The potential for not detecting group differences could have existed as subjects with PFPS could have exhibited lower VM and VL amplitudes but still have similar VM to VL ratios as healthy subjects. Therefore, expressing amplitudes as absolute values (not a ratio) and analyzing them over discrete intervals of stair descent may provide more conclusive information regarding neuromuscular activity in patients with PFPS.

Most prior works have examined onset timing differences between the VM and VL. Researchers (Voight and Wieder, 1991, Witvrouw et al., 1996) have reported delayed reflex response times of the VM compared to the VL during a patellar tendon tap. A potential limitation of these studies was the assessment of afferent pathways. Karst and Willett (1995) examined both reflex response times and VM–VL onsets during non-weight bearing and weight bearing voluntary knee extension exercise. Although they reported similar differences with reflex responses (Voight and Wieder, 1991, Witvrouw et al., 1996), they did not find VM–VL onset timing differences during voluntary exercise. This finding suggested that reflex testing was a poor indicator of muscle activity onsets during voluntary knee extension.

Conflicting results exist regarding VM and VL onsets during volitional tasks. Some investigators (Brindle et al., 2003, Powers et al., 1996, Sheehy et al., 1998) have reported simultaneous VM and VL activation whereas others (Cowan et al., 2002, Boling et al., 2006, Cowan et al., 2001) have found delayed VM activation. Reasons for discrepancies may result from differences with task performance, muscle onset identification, and signal processing (Cowan et al., 2000). Subjects in studies that did not find onset differences completed stair descent at a self-selected pace (Brindle et al., 2003, Powers et al., 1996, Sheehy et al., 1998) and the investigators identified muscle onsets using either visual analysis (Sheehy et al., 1998) or a computer algorithm (Brindle et al., 2003, Powers et al., 1996). Variations in signal processing also occurred as some researchers applied a 15 Hz low pass filter (Brindle et al., 2003) while others applied a 150–1000 Hz band pass filter (Powers et al., 1996).

Hodges and Bui (1996) recommended identifying muscle onsets using both visual inspection and a computer algorithm. They also recommended applying a low pass filter at 50 Hz because excessive signal smoothing can hinder proper determination of onsets. Based on these recommendations, Cowan et al. (2000) determined the reliability of a protocol to identify muscle onsets. In this study, healthy subjects completed a stair descent task at a standardized rate of 96 beats per minute. Electromyographic (EMG) signals were full wave rectified and low pass filtered at 50 Hz. They used an algorithm that defined an onset as the point in which a signal deviated by more than three standard deviations, for a minimum of 25 ms, over a baseline level taken 200 ms before a trial began. All muscle onsets were also visually confirmed. Using these procedures, Cowan et al. reported an intraclass correlation coefficient (ICC) equal to 0.96. More important, results from subsequent studies (Cowan et al., 2002, Boling et al., 2006, Cowan et al., 2001) that have incorporated these procedures have shown delayed VM onset relative to the VL during stair descent in subjects with PFPS. Therefore, these refinements may better identify differences in VM and VL onsets.

Recent attention has focused on the influence of the hip on PFPS (Ireland et al., 2003, Bolgla et al., 2008); however, limited information exists regarding neuromuscular activity of the hip in this patient population. To date, no study has examined hip muscle amplitudes and only two investigations (Brindle et al., 2003, Boling et al., 2006) have compared GM onsets to that of the VM and VL during stair descent. While Brindle et al. (2003) reported a greater delay in GM activation relative to the VM and VL in subjects with PFPS, Boling et al. (2006) did not corroborate this finding. Methodological difference most likely accounted for these discrepancies.

Inconclusive study results from prior research may reflect varying methodology instead of true differences in the observed parameter (Portney and Watkins, 2000). A limitation of prior works has been limited attention to measurement reliability. To our knowledge, no study has established measurement reliability for determining amplitudes during stair descent. Only Cowan et al. (2000) have specifically examined measurement reliability for identifying VM and VL onsets. Although they reported excellent measurement reliability in healthy subjects during stair descent, it has remained elusive if these methods would be equally reliable when assessing subjects with pathology. The identification and systematic use of reliable measures is paramount to better understand hip and knee neuromuscular activity for patients with PFPS.

Therefore, the purpose of this study was to establish measurement reliability for procedures designed to assess neuromuscular activity of the GM, VM, and VL during stair descent in subjects with PFPS. Specifically, we wanted to determine the reliability for quantifying amplitudes over discrete intervals of stair descent (Mohr et al., 2003) and identifying muscle onsets based on recommendations from Hodges and Bui, 1996, Cowan et al., 2000. We hypothesized that all measures would have an ICC greater than or equal to 0.70 (Portney and Watkins, 2000).

Section snippets

Subjects

Only female subjects participated since PFPS is more prevalent in this subject population (Thomee, 1997). They participated in a larger study that examined hip and knee function, strength, EMG activity, and kinematics in this patient population (Bolgla et al., 2008). Data from seven females with PFPS (age = 22.9 ± 2.7 years, height = 1.7 ± 0.1 m, body mass = 60.0 ± 5.6 kg, symptom duration = 11.6 ± 13.8 months) were included in the current analysis. Inclusion criteria included the following: (1) anterior knee

Results

Subjects rated usual pain over the previous week an average of 4.8 ± 1.9 cm on the VAS. Table 1, Table 2 summarize means, standard deviations, ICCs, and SEMs for all dependent measures. Amplitudes during the LR and SLS intervals for all the muscles had an ICC3,5 greater than 0.70. During the preswing interval, ICC3,5 for the GM (0.95) was higher than the VM (0.40) and VL (0.53). Regarding timing differences, ICC3,5 for the VM–GM (0.83) and VL–GM (0.91) were higher than the VL–VM (0.70). Although

Discussion

Measurement reliability is critical for data analysis. It ensures that changes in a specific measure represent a true change in performance and not one from chance alone (Loudon et al., 2002). Overall, our results suggested that the methods used in the current study provided reliable measures for determining GM, VM, and VL amplitudes and onset timing differences in females with PFPS during a stair descent task.

Conclusion

Results from this study indicated acceptable reliability for most of our EMG measures used to assess the GM, VM, and VL. Overall, surface EMG provided reliable measures of amplitudes and timing differences for the GM, VM, and VL. Subjects completed the stair-stepping task at a standard rate; it is unknown if similar ICCs would be calculated using other cadences.

These findings have important implications from both a research and clinical standpoint. Researchers have reported different findings

Lori Bolgla, PhD, PT, ATC, is Assistant Professor in the Department of Physical Therapy, School of Allied Health Sciences at the Medical College of Georgia. Dr. Bolgla received her Bachelor in Science Degree in Physical Therapy from the Medical College of Georgia in 1993 and her Master in Science Degree in Physical Therapy from the Medical College of Georgia in 1998. She received her Doctor of Philosophy Degree in Rehabilitation Sciences from the University of Kentucky in 2005. Her research has

References (43)

  • J.C. Agre et al.

    Strength testing with a portable dynamometer: reliability for upper and lower extremities

    Arch Phys Med Rehabil

    (1987)
  • M.M. Bamman et al.

    Evaluation of surface electromyography during maximal voluntary contraction

    J Strength Cond Res

    (1997)
  • J.V. Basmajian et al.

    Apparatus, detection, and recording techniques, in muscles alive, their functions revealed by electromyography

    (1985)
  • L.A. Bolgla et al.

    Electromyographic analysis of hip rehabilitation exercises in a group of healthy subjects

    J Orthop Sports Phys Ther

    (2005)
  • L.A. Bolgla et al.

    Hip strength and hip and knee kinematics during stair descent in females with and without patellofemoral pain syndrome

    J Orthop Sports Phys Ther

    (2008)
  • T.J. Brindle et al.

    Electromyographic changes in the gluteus medius during stair ascent and descent in subjects with anterior knee pain

    Knee Surg Sports Traumatol Arthrosc

    (2003)
  • B. Campenella et al.

    Effect of visual feedback and verbal encouragement on concentric quadriceps and hamstrings peak torque of males and females

    Isokinet Exerc Sci

    (2000)
  • S.M. Cowan et al.

    Physical therapy alters recruitment of the vasti in patellofemoral pain syndrome

    Med Sci Sports Exerc

    (2002)
  • J.R. Cram et al.

    Introduction to surface electromyography

    (1998)
  • C.J. de Ruiter et al.

    Initial phase of maximal voluntary and electrically stimulated knee extension torque development at different knee angles

    J Appl Physiol

    (2004)
  • C. Denegar et al.

    Assessing reliability and precision of measurement: an introduction to intraclass correlation and standard error of measurement

    J Sport Rehabil

    (1993)
  • Cited by (33)

    • Reliability of surface electromyography for the gluteus medius muscle during gait in people with and without chronic nonspecific low back pain

      2020, Journal of Electromyography and Kinesiology
      Citation Excerpt :

      Surface EMG has been shown to be a reliable tool when assessing a number of paraspinal muscles in both people with and without chronic low back pain (Mohseni Bandpei et al., 2014), however there has been limited investigation for the gluteus medius muscle. Of the studies that have assessed reliability of surface EMG measurement of this muscle, the focus has been on submaximal and maximal contractions (Dankaerts et al., 2004), static tasks (Charlton et al., 2017, Norcross et al., 2010), and in the presence of specific pathologies such as hip osteoarthritis (French et al., 2015) or patellofemoral pain syndrome (Bolgla et al., 2010), or using submaximal and maximal contractions for normalisation of dynamic activity in healthy people (Nishijima et al., 2010, Tabard-Fougere et al., 2018). Intramuscular EMG reliability of this muscle has been shown to have high levels of between session reliability (Green et al., 2019), but given the inherent differences between fine wire and surface EMG, the reliability of surface EMG for the gluteus medius muscle during walking gait needs to be established.

    View all citing articles on Scopus

    Lori Bolgla, PhD, PT, ATC, is Assistant Professor in the Department of Physical Therapy, School of Allied Health Sciences at the Medical College of Georgia. Dr. Bolgla received her Bachelor in Science Degree in Physical Therapy from the Medical College of Georgia in 1993 and her Master in Science Degree in Physical Therapy from the Medical College of Georgia in 1998. She received her Doctor of Philosophy Degree in Rehabilitation Sciences from the University of Kentucky in 2005. Her research has focused on the evaluation and rehabilitation of lower extremity overuse injuries.

    Terry Malone, EdD, PT, ATC, FAPTA, received his Baccalaureate Degree from Bluffton College (1973), his MS – Certificate of Physical Therapy – from Duke University (1975) followed by his EdD in 1985. He has been active in Sports Medicine and has published widely on shoulder and knee conditions. He is a Professor in the Division of Physical Therapy and Rehabilitation Sciences Doctoral Program at the University of Kentucky.

    Brian Umberger, PhD, is an Assistant Professor in the Department of Kinesiology, School of Public Health and Health Sciences at the University of Massachusetts Amherst. He received his Doctorate in Exercise Science from Arizona State University in 2003. From 2003 to 2006 he was an Assistant Professor in the Department of Kinesiology and Health Promotion at the University of Kentucky. His research is focused on the biomechanics and energetics of human locomotion in health and disease. In his research he uses both experimental procedures and computational modeling techniques.

    Tim Uhl, PhD, ATC, PT, received his Bachelors in Health Science from the University of Kentucky in Physical Therapy and Athletic Training in 1985. He received a Masters’ Degree in Kinesiology from the University of Michigan. He completed his Doctorate in Sports Medicine from the University of Virginia in 1998 where he studied shoulder proprioception. He is presently an Associate Professor in the Department of Rehabilitation Sciences at the University of Kentucky where his research focus is on upper extremity during functional activities and rehabilitation.

    No monies were received in support of this study. The protocol for this study was approved by the University of Kentucky Institutional Review Board.

    View full text