<<

A Thesis

entitled

Central Activation Ratio with a Superimposed Burst Technique to Assess Muscle

Activation of the Gluteus Medius and Gluteus Maximus

by

Daniel Gilfeather

Submitted to the Graduate Faculty as partial fulfillment of the requirements for the

Master of Science Degree in Exercise Science with a Concentration in Athletic Training

______Neal Glaviano, PhD, AT, ATC Committee Chair

______Grant Norte, PhD, AT, ATC, CSCS Committee Member

______Christopher Ingersoll, PhD, AT, ATC, FACSM, FNATA, FASAHP Committee Member

______Amanda Bryant-Friedrich, PhD, Dean College of Graduate Studies

The University of Toledo

May 2018

Copyright 2018, Daniel Paul Gilfeather

This document is copyrighted material. Under copyright law, no parts of this document may be reproduced without the expressed permission of the author. An Abstract of

Central Activation Ratio with a Superimposed Burst Technique to Assess Muscle Activation of the Gluteus Medius and Gluteus Maximus

by

Daniel Gilfeather

Submitted to the Graduate Faculty as partial fulfillment of the requirements for the Master of Science Degree in Exercise Science with a Concentration in Athletic Training

The University of Toledo May 2018

Context: The central activation ratio (CAR) is a common way to assess muscle inhibition and has primarily been studied on the quadriceps. There is no literature to our knowledge of the efficacy of this measurement and its reliability on the gluteus maximus/medius.

Objective: Quantify the CAR of the gluteus medius/maximus muscles in a healthy population and evaluate its reliability of these measures one week post initial testing.

Study Design: Descriptive Setting: Laboratory Participants: Twenty healthy participants were enrolled (9 male and 11 females: age 22.2 ± 1.4 years, height 173.4 ±

11.1 cm, mass 84.8 ± 25.8 kg). Intervention: CAR with the superimposed burst (SIB) technique were used to assess muscle inhibition of the gluteus medius/maximus muscles.

Main Outcome Measures: A MVIC at different percentages of the gluteus medius

/maximus and the CAR with a SIB was assessed initially along with a one week follow up testing session. Results: The gluteus medius CAR has excellent reliability within session (ICC [3,1] =.911). The gluteus maximus CAR was moderately reliable within session (ICC [3,1] = .704). Conclusions: CAR appears to be a reliable method to assess

iii gluteal function. Key Words: Gluteus Maximus, Gluteus Medius, Central Activation

Ratio, Superimposed Burst Technique, Maximal Voluntary Isometric Contraction

iv

Table of Contents

Abstract iii

Table of Contents iv

List of Figures vi

List of Abbreviations vii

I. Manuscript 1

A. Introduction 1

B. Methods 3

a. Study Design 3

b. Participants 3

c. Procedures 4

d. Data Analysis 6

e. Statistical Analysis 6

C. Results 7

D. Discussion 8

E. Conclusion 12

References 13

Appendices

A. The Problem 20

B. Literature Review 24

C. Additional Methods 38

D. Additional Results 50

v E. Back Matter 58

F. Bibliography 61

vi List of Figures

Figure 1 Gluteus Maximus Patient Set-Up ...... 17

Figure 2 Gluteus Medius Patient Set-Up ...... 18

Figure 3 Output at Rest ...... 19

Figure 4 Gluteal CAR between Day 1 & Day 2 ...... 54

Figure 5 Gluteal MVIC between Day 1 & Day 2...... 55

Figure 6 Gluteal SIB between Day 1 & Day 2 ...... 56

Figure 7 VAS between Day 1 & Day 2 ...... 56

Figure 8 Gluteus Medius CAR during Progressive Contractions ...... 57

Figure 9 Gluteus Maximus CAR during Progressive Contractions ...... 57

vii List of Abbreviations

ACLr ...... Anterior Cruciate Ligament Reconstruction AMI ...... Arthogenic Muscle Inhibition

CAR ...... Central Activation Ratio cm ...... Centimeter

ICC ...... Intra-Class Coefficient kg...... Kilograms

MVIC ...... Maximal Voluntary Isometric Contraction

Nm...... Newton Meter

PFP ...... Patellofemoral Pain

SIB ...... Superimposed Burst SIBT ...... Superimposed Burst Technique

VAS...... Visual Analog Scale

viii Chapter One

Manuscript

Introduction

Movements at the are controlled by groups of large extrinsic and small intrinsic muscles. Large muscle groups act to flex, extend and internally rotate the hip while the small intrinsic muscles serve to externally rotate the hip.1 The gluteus medius and gluteus maximus play a vital role in maintaining the horizontal position of the , frontal plane lower extremity movements and the ’s upright position during normal patterns.1 Therefore, it is important that these two muscle groups stay properly activated and are being used to their full potential. Emerging evidence has identified that gluteal weakness is present in a variety of such as individuals with low back pain2, ACL deficient patients,3 patellofemoral pain,4,5 and a variety of additional pathological patients.6,7

Muscle weakness is a common occurrence in pathological populations and several potential causes are injury, pain, and swelling. Pain and swelling have been reported to induce a neurological phenomenon, arthogenic muscle inhibition (AMI). AMI is an ongoing reflex inhibition of the musculature surrounding a joint following distension or damage to structures of that joint.8 When AMI is present, the targeted muscle group does not have the ability to recruit an adequate number of available motorneurons, resulting is central activation failure which is problematic for both the patient and clinician. If we are not activating our muscles enough during normal rehabilitation exercises, we could say that we are actually doing a disservice to our patients by not assessing and not addressing

1 the impairment. While strength is one way to assess weakness, it is limited to identify muscle inhibition. It is essential to find a novel way to assess gluteus medius and maximus function besides the standard strength assessment.

The central activiation ratio (CAR) with the superimposed burst technique (SIBT) is one method that has been used to assess muscle function, and previous research has been conducted in regards to the volitional activation of the quadriceps in a variety of pathologies.9-11 The CAR is a ratio between the volitional muscle activation and the muscle activation elicited by an exogenous electrical stimulus.11 The SIBT is the application of an electrical stimulation during a maximal voluntary contraction that in theory, activates all the remaining motor units that the patient was unable to do so during their maximal voluntary isometric contraction (MVIC).9 The CAR assessed by the SIBT is a valid and reliable measurement at assessing glutal muscle strength and central activation in a healthy population.12,13 This provides clinicians and researchers a way to measure any muscle inhibition that’s present.

While a variety of lower extremity pathologies have been assessed with by CAR, the research is mostly limited to the quadriceps.9,11-15 Expanding the use of this measurement on other superficial muscle groups provides the ability to assess if activation failure in additional muscle groups are present in common lower extremity conditions. Due to the importance of the gluteal muscles during daily activities and the emerging evidence of their weakness in a variety of conditions,16-18 it is essential to gain additional measurements of their function and evaluate if muscle inhibition may be present in the muscle group.

2 Therefore, the purpose of this project is to see if CAR is a valid method to assess muscle function of gluteus medius and gluteus maximus and if the measure is reliable over a 1-week test-retest interval. Second, we will examine if a relationship exist between progressive contractions of the gluteal muscles and torque output at different percentage of stimulus provided through the SIBT. We hypothesize that the CAR is a valid and reliable method to assess gluteal muscle activity. Additionally we hypothesize that there will be a linear relationship between percentage of stimulus and gluteus muscle activation.

Methods

Study Design: This study was a descriptive laboratory study. The dependent variables were gluteus medius and gluteus maximus activation assessed by the CAR and peak hip abduction and hip extension force measured by MVIC and normalized to body mass. The independent variables included percentages of the SIBT, progressive contractions of both gluteal muscles (25, 50, 75, 100%), and time intervals (session 1 and session 2). Pain during the CAR assessment was assessed for both muscles at both testing sessions with the visual analog scale (VAS)

Participants: Twenty healthy participants were recruited from the local university and community (9 male and 11 females: age 22.2 ± 1.4 years, height 173.4 ±

11.1 cm, mass 84.8 ± 25.8 kg) and were enrolled in the study. Subjects were included in the study if they were healthy adults ages 18-35 years old and physically active 2-3x per week. Subjects were excluded from the study if they worked out in the last 24-48 hours and were experiencing delayed onset muscle soreness (DOMS), previous surgery to lower body or back on the testing , previous injury to lower body or back in last 6

3 months on the testing limb. Additionally, subjects with history of neuropathy, biomedical devices (ie: pacemaker or defibrillators), muscular abnormalities, currently pregnant, hypersensitivity to electrical stimulation, or an active over or hip muscles were excluded. Before data collection, all participants signed an informed consent approved by the University of Toledo Institutional Review Board (IRB), which also approved the study.

Procedures: Participants reported to the laboratory where they completed an informed consent form. Next, subjective demographics were collected using an IRB approved questionnaire that listed all of our inclusion and exclusion criteria. Once the questionnaire was completed, the subjects signed and dated an informed consent form.

Randomization for order of muscles being tested was completed prior to the start of the study. The order of muscles being tested was maintained between sessions. For the gluteus maximus, two 2” X 3.5” self-adhesive electrodes were placed on the gluteal fold and inferior and distally to the posterior superior iliac spine (PSIS). Participants were positioned in a prone position with their and flexed at 90 degrees and had their placed in front of them (Figure 1). The axis of rotation was aligned with the subject’s greater trochanter and the participants were asked to maintain this position for the duration of the study. Additionally, participants were secured to their position with a distal pad located just proximal to the popliteal fossa and a strap going over the patients back to decrease excessive movement during the hip extension task.

For the gluteus medius, two 2” X 3.5” self-adhesive electrodes were placed on just inferior to the iliac crest and just superior to the greater trochanter. The axis of rotation was aligned with the subject’s anterior superior iliac spine (ASIS) and the

4 participants were asked to maintain this position for the duration of the study. The participants were in a standing position facing the dynamometer with the Biodex chair on their contralateral side stabilizing their hips with a bolster on top of the chair to stabilize their trunk and limit excessive movement during the hip abduction task (Figure 2). There was a distal pad placed just superior to the patients lateral femoral condyle to stabilize the testing limb.

Hip extension and hip abduction torque were measured using the Biodex System

4 Pro (Shirley, NY). A remote access port digitized at 125 Hz served as the analog to digital converter, 16 bits, was used to export data19(MP150, BioPac Systems, Inc, Santa

Barbra, CA) and to record hip extension and hip abduction output. Gluteal CAR was measured through the Superimposed Burst (SIB) technique using a Grass Stimulator s48

(West. Warwick, RI) and Stimulus Isolation Unit (Grass Stimulator, West Warwick, RI).

The isolation unit delivered a 100-milisecond train of 10 square-wave pulses at an intensity of 125V with a pulse duration of 600 μs at a frequency of 100 pulses per second.

During each MVIC trial, the researcher manually administered the 125V electrical stimulus, at varying intensities, when a steady real-time torque output plateau was observed.

Participants were acclimated through a series of progressive contraction trials (25, 50,

75, and 100% of their max effort) to allow the participants to become adapted to the dynamometer and the task.12 Participants were instructed to perform the task by ramping up to the percentage of the maximal effort and maintain that intensity for 3-5 seconds.

During MVIC testing, participants were provided verbal and visual encouragement.

Once the participant felt comfortable with the task, they performed an MVIC and the SIB

5 was administered at increments of 25% until the maximal, 125V stimulus was delivered.

Two trials for the submaximal SIBs and three trials for the maximal SIB were collected, with one-minute of rest provided between trails. Following the 100% MVIC and 100%

SIB trials, all subjects completed a 10cm VAS to assess their pain levels during both gluteal muscles tested. The VAS was anchored with “no pain” and “worst pain imaginable”. Participants then completed rest trials, where they relaxed in the testing position and a SIB was administered at 25% increments (25%, 50%, 75%, and 100%).

Following the rest trials, the first testing session was then concluded. Participants returned to the lab one-week later for the second testing session. During this session, participants completed three MVICs with 100% SIB for both the gluteus maximus and gluteus medius muscles, with the VAS assessed following testing of each muscle.

Data Analysis: The progressive contraction output was normalized to the patient’s body mass in kilograms and converted to a torque output. The peak SIB torque output was also calculated with the same approach. The CAR was calculated by using a 100ms time epoch of the MVIC before the SIB stimulus and the combination of the MVIC and

SIB output from the stimulus (CAR=MVIC/MVIC+SIBTx100). VAS was scored by measuring, in centimeters, the distance between the “no pain” anchor and the vertical line placed by the participants. Measurement was measured with a standard tape measure, to the nearest tenth of a centimeter.

Statistical Analysis: Descriptive statistics were performed for participant’s demographics and both testing session’s CAR, MVIC, and VAS scores for the gluteus maximus and gluteus medius. Dependent t-tests were used to compare differences in

CAR, MVIC, and VAS scores between the two sessions, with alpha set at p<.05. Gluteal

6 CAR reliability was assessed by Intra-Class Correlation Coefficients (ICC) 3,1 and classified as poor (<0.5), moderate (0.5-0.75), good (0.75-0.90) and excellent (>0.90)20.

The relationship between stimulus percentage and torque output during rested testing condition was assessed. In addition, the CAR of the maximal stimulus at the progressive contractions for each muscle was assessed. Individual relationships were plotted to assess line of best fit and regressions were performed to calculate coefficient of determination.21 All statistical analyses were performed using Social Package Social

Sciences (SPSS) v23.0 (IBM Corporation, Armonk, NY).

Results

The gluteus medius CAR had excellent reliability (ICC [3,1] =.911) between session (Day 1: 96.1±3.37, Day 2: 96.6±3.16). The gluteus maximus CAR was moderately reliable (ICC [3,1] = .704) between session (Day 1: 86.5±7.5, Day 2:

87.2±10.7, p=0.737). There were no statistical differences in the CAR measurement between our initial testing period and the one week follow up testing session for either gluteus medius (p=0.599) or gluteus maximus (p=0.737). There was a decrease in VAS scores for both the gluteus medius (Day 1: 3.8±2.4, Day 2: 2.6±1.6, p=.002) and gluteus maximus (Day 1: 4.5±2.3, Day 2: 2.9±2.1, p<.001) with a lower pain score on the second testing session for both muscles.

No differences were detected between hip abduction MVIC (Day 1:

1.56±0.29Nm/kg, Day 2: 1.57±0.51Nm/kg, p=0.876) or SIB (Day 1: 1.59±0.31Nm/kg,

Day 2: 1.60±0.51, p=0.892). Moderate reliability was seen for both hip abduction MVIC,

ICC [3,1] =.606, and SIB, ICC [3,1] =.533. There were also no differences in hip extension

MVIC (Day 1: 2.54±0.69Nm/kg, Day 2: 2.64±1.15Nm/kg, p=0.695) or SIB (Day 1:

7 2.88±0.70Nm/kg, Day 2: 2.91±1.01, p=0.896). Hip abduction and SIB also had good reliability between testing session, ICC [3,1] =.805 and ICC [3,1] =.808, respectively.

Regression analyses with coefficient of determination (r2) resulted in a linear relationship as the line of best fit for progressive contraction torque output and percentage of stimulus administered during the subjects MVIC trials for both gluteus medius (r2=.409) and gluteus maximus (r2=.639). Third order polynomials demonstrated the line of best fit between the torque output at varying intensities of the SIB for both gluteus medius (r2=.156) and gluteus maximus (r2=.602). (Figure 3)

Discussion

The purpose of this study was to see if the CAR was a valid method to assess muscle function of gluteus medius and gluteus maximus and if the measure was reliable over a 1-week test-retest interval. Second, we wanted to examine if a relationship existed between progressive contractions and torque output at different percentage of stimuli provided through the SIBT. We found both measures to be reliable between both days with no difference between maximum torque output, SIB, and CAR. We found that by increasing our stimulus, there was a linear relationship in regards to stimulus percentage and gluteus muscle activation.

Previous literature combined with our clinical correlates with gluteal weakness is found in multiple lower extremity pathologies,2,4-7 yet literature of assessing muscle activation failure in these conditions is limited to the quadriceps.9,11-15 Due to the importance of the gluteal muscles during daily activities and the emerging evidence of their weakness in functional tasks, patient outcomes, and frontal plane control,16-18 it is

8 essential to find novel methods to assess the gluteal muscles and gain insight into central activation failure is present in the proximal lower extremity muscles.

The SIB has been a widely used clinical tool to assess muscle function. This technique has most often been researched with pathological groups such as PFP12 and anterior cruciate ligament reconstruction (ACLr) populations. However, to our knowledge there have been only a few studies which have measured the reliability of this measurement in both pathological groups and healthy subjects.12,13 A study looking at reliability of the SIB technique in a pathological group found the SIB technique to be a reliable tool to assess muscle function in patients with PFP. Although we used different

ICC calculations to establish the thresholds, our CAR ICC values for gluteus medius fell exactly in line with quadriceps CAR of the PFP patients. We also had similar ICC values for MVIC and SIB with gluteus maximus compared to the PFP patients. In this study, they also looked at the reliability in a healthy group as well. The healthy quadricep ICC values for MVIC and SIB were a little higher than ours were, while their CAR value fell right in line with our gluteus maximus ICC value. What was interesting was that our gluteus medius ICC value was much higher than that of the healthy quadricep CAR ICC value. We could infer that the gluteus medius is a much more reliable muscle for assessing central activation. This might be true because of the gluteus medius is a smaller muscle, that our electrode placement was much closer which would in theory recruit more motor units because of the smaller surface area. Also, larger muscle groups have more compensatory strategies to complete functional tasks.

Muscle activation has also been assessed in healthy populations as well.21

Stackhouse et al21 evaluated the relationship between CAR and the percent MVIC trials

9 and found that a second order polynomial was found to best fit the curvilinear relationship. Due to a decrease in motor units that were available to recruit, our findings were similar, we found that a third order polynomial to best fit the relationship. While this relationship differs from our original hypothesis, this may suggest that as the SIB intensity increased, we achieved stimulation of the majority of the available motor units.

One of the limitations with assessing CAR with the SIBT is patient discomfort, due to the stimulus targeting the free nerve endings. We found similar increases in patient discomfort during both testing sessions for the gluteus medius (VAS= 4.5 and 2.9 respectively) and gluteus maximus (3.8 and 2.6 respectively). Interestingly, we found lower VAS scores on the second day of testing, which may be due to the longer initial testing session. These findings may suggest that a familiarization session may be required when assessing gluteal CAR, which is supported in previous findings.12 Our gluteal VAS scores during the SIBT are similar to previous studies17 that have assessed

VAS during quadriceps testing, ranging from 2.2-5.3.

The gluteus maximus muscle does present with a challenge in conducting a measure like the SIB, as the muscle is triplanar. Attention should be placed on this factor, as the patient positioning for gluteus maximus and the location of the electrodes on this muscle may influence torque output and the motor units stimulated. The gluteus medius and gluteus maximus play such a vital role in rotation, extension and abduction that finding a pad placement to optimize our muscle activation could be a potential source of measurement error. Previous literature has stated that the superior portion of the gluteus maximus produces greater EMG amplitude than the inferior portion during exercises that incorporated hip abduction and external rotation.22 Exercises that focused

10 purely on hip extension targeted both portions of the gluteus maximus. Another study23 confirmed this theory stating that the gluteus maximus is better suited for hip abduction because of its insertion on the fascia lata, while the inferior fibers are better suited for hip extension because of its larger moment . Seeing as our mean CAR and ICC values for the gluteus maximus were lower than those of the gluteus medius, we can infer that future research should be done to find correct optimal patient position and electrode placement when testing CAR of the gluteus maximus. Determining patient position and electrode placement on the gluteus maximus may improve the accuracy of assessing CAR of this muscle.

While finding optimal pad placement is vital in optimizing muscle activation, patient positioning during their MVIC trials may also play a big role in correctly assessing muscle activation. A limitation to the current study might have been our patient position during muscle strength testing for the gluteus medius and gluteus maximus. Previous studies24,25 have looked at assessing hip abduction strength in a side lying position compared to a standing position. We chose to have our patient standing in an effort to minimize the influence of gravity on the subject’s ability to provide maximal effort. Another study26 assessed hip extension with participant’s supine, with the hip and knee flexed to 90 degrees. The dynamometer was positioned on the posterior surface of the distal thigh, proximal to the knee joint. Future research should evaluate if the SIBT is reliable at assessing gluteal muscle activation in a variety of testing positions.

Additionally, evaluating the potential of central activation failure of the gluteal muscles in lower extremity pathological groups could have large clinically relevant findings.

11 Altered gluteal function has been linked to poor neuromuscular control during functional tasks, so this relationship would also warrant investigation.

Conclusion

The SIB technique has proven to be a valid and reliable measurement to assess gluteus medius and gluteus maximus CAR in healthy, active individuals. It appears that using similar parameters for assessing the quadriceps are appropriate for measuring gluteal muscle inhibition in a healthy population. Providing patient practice trials and improving their expectations with the SIBT should be considered when using these measures to decrease patient discomfort during testing. Further consideration using this technique in pathological cohorts must be made before extrapolating this data into clinical practice.

12 References

1. Chad Starkey SDB, Jeff Ryan. Examination of Orthopedic and Athletic Injuries.

Vol 3. Philadelphia, PA: F.A. Davis Company; 2010.

2. Cooper NA, Scavo KM, Strickland KJ, et al. Prevalence of gluteus medius

weakness in people with chronic compared to healthy controls.

European spine journal : official publication of the European Spine Society, the

European Spinal Deformity Society, and the European Section of the Cervical

Spine Research Society. Apr 2016;25(4):1258-1265.

3. Bell DR, Trigsted SM, Post EG, Walden CE. Hip Strength in Patients with

Quadriceps Strength Deficits after ACL Reconstruction. Medicine and science in

sports and exercise. Oct 2016;48(10):1886-1892.

4. Bolgla LA, Malone TR, Umberger BR, Uhl TL. Comparison of hip and knee

strength and neuromuscular activity in subjects with and without patellofemoral

pain syndrome. International journal of sports physical therapy. Dec

2011;6(4):285-296.

5. Boling MC, Padua DA, Alexander Creighton R. Concentric and eccentric torque

of the hip musculature in individuals with and without patellofemoral pain. J Athl

Train. Jan-Feb 2009;44(1):7-13.

6. Mucha MD, Caldwell W, Schlueter EL, Walters C, Hassen A. Hip abductor

strength and lower extremity related injury in distance runners: A

systematic review. Journal of science and medicine in sport. Apr 2017;20(4):349-

355.

13 7. Deasy M, Leahy E, Semciw AI. Hip Strength Deficits in People With

Symptomatic Knee Osteoarthritis: A Systematic Review With Meta-analysis. The

Journal of orthopaedic and sports physical therapy. Aug 2016;46(8):629-639.

8. Hopkins JT, Ingersoll CD. Arthrogenic Muscle inhibition: A Limiting Factor in

Joint Rehabilitation. Journal of sport rehabilitation. 2000;9(2):135-159.

9. Park J, Hopkins JT. Quadriceps activation normative values and the affect of

subcutaneous tissue thickness. Journal of electromyography and kinesiology :

official journal of the International Society of Electrophysiological Kinesiology.

Feb 2011;21(1):136-140.

10. Hart JM, Pietrosimone B, Hertel J, Ingersoll CD. Quadriceps Activation

Following Knee Injuries: A Systematic Review. Journal of Athletic Training. Jan-

Feb 2010;45(1):87-97.

11. Mizner RL, Stevens JE, Snyder-Mackler L. Voluntary activation and decreased

force production of the quadriceps femoris muscle after total knee .

Physical therapy. Apr 2003;83(4):359-365.

12. Norte GE, Frye JL, Hart JM. Reliability of the Superimposed-Burst Technique in

Patients With Patellofemoral Pain: A Technical Report. J Athl Train. Nov

2015;50(11):1207-1211.

13. Dousset E, Jammes Y. Reliability of burst superimposed technique to assess

central activation failure during fatiguing contraction. Journal of

electromyography and kinesiology : official journal of the International Society of

Electrophysiological Kinesiology. Apr 2003;13(2):103-111.

14 14. Newman SA, Jones G, Newham DJ. Quadriceps voluntary activation at different

joint angles measured by two stimulation techniques. European journal of applied

physiology. Jun 2003;89(5):496-499.

15. Palmieri RM, Ingersoll CD, Hoffman MA, et al. Arthrogenic muscle response to a

simulated joint effusion. British Journal of Sports Medicine. February 1,

2004 2004;38(1):26-30.

16. Drechsler WI, Cramp MC, Scott OM. Changes in muscle strength and EMG

median frequency after anterior cruciate ligament reconstruction. European

journal of applied physiology. Dec 2006;98(6):613-623.

17. Bolgla LA, Uhl TL. Electromyographic analysis of hip rehabilitation exercises in

a group of healthy subjects. The Journal of orthopaedic and sports physical

therapy. Aug 2005;35(8):487-494.

18. Marshall PW, Patel H, Callaghan JP. Gluteus medius strength, endurance, and co-

activation in the development of low back pain during prolonged standing.

Human movement science. Feb 2011;30(1):63-73.

19. Glaviano NR, Langston WT, Hart JM, Saliba S. Influence of patterned electrical

neuromuscular stimulation on quadriceps activation in individuals with knee joint

injury. International journal of sports physical therapy. Dec 2014;9(7):915-923.

20. Koo TK, Li MY. A Guideline of Selecting and Reporting Intraclass Correlation

Coefficients for Reliability Research. Journal of chiropractic medicine. Jun

2016;15(2):155-163.

15 21. Stackhouse SK, Dean JC, Lee SC, Binder-MacLeod SA. Measurement of central

activation failure of the quadriceps femoris in healthy adults. Muscle & nerve.

Nov 2000;23(11):1706-1712.

22. Selkowitz DM, Beneck GJ, Powers CM. Comparison of Electromyographic

Activity of the Superior and Inferior Portions of the Gluteus Maximus Muscle

During Common Therapeutic Exercises. The Journal of orthopaedic and sports

physical therapy. Sep 2016;46(9):794-799.

23. Stern JT, Jr. Anatomical and functional specializations of the human gluteus

maximus. American journal of physical anthropology. May 1972;36(3):315-339.

24. Kline PW, Burnham J, Yonz M, Johnson D, Ireland ML, Noehren B. Hip external

rotation strength predicts hop performance after anterior cruciate ligament

reconstruction. Knee surgery, sports traumatology, arthroscopy : official journal

of the ESSKA. Apr 4 2017.

25. Nakagawa TH, Muniz TB, Baldon RM, Maciel CD, Amorim CF, Serrao FV.

Electromyographic preactivation pattern of the gluteus medius during weight-

bearing functional tasks in women with and without anterior knee pain. Revista

brasileira de fisioterapia (Sao Carlos (Sao Paulo, Brazil)). Jan-Feb

2011;15(1):59-65.

26. Nguyen AD, Zuk EF, Baellow AL, Pfile KR, DiStefano LJ, Boling MC.

Longitudinal Changes in Hip Strength and in Female Youth

Soccer Players: Implications for ACL Injury, A Pilot Study. Journal of sport

rehabilitation. Sep 2017;26(5):358-364.

16

Figure 1: Gluteus Maximus Patient Set-Up

17

Figure 2: Gluteus Medius Patient Set-Up

18

Gluteus Maximus Output at Varying Intensities during Rest

2.5

2 R² = 0.6027 1.5 1

TorqueOutput 0.5

0 0 25 50 75 100 Percent Stimulus

Gluteus Medius Output at Varying Intensities during Rest 0.8

0.7

0.6 R² = 0.1563 0.5 0.4 0.3

0.2 TorqueOutput 0.1 0 0 25 50 75 100

Percent Stimulus

Figure 3: Gluteal Torque Output at Varying Rest Intensities of the SIB

19 Appendix A

The Problem

Problem Statement The gluteus medius and gluteus maximus play a vital role in maintaining the horizontal position of the pelvis and the torso’s upright position during normal gait patterns.1 They also are important not just in gait patterns, but also in patients with weaknesses in their lower backs, ACL deficient patients and a variety of additional pathological patients. Therefore, it is important that these two muscle groups stay as strong as possible and are being used to their full potential. Muscle inhibition is a common occurrence in pathological populations due to an ample amount of phenomenon’s such as injury, pain, and swelling. This ongoing reflex inhibition of the musculature surrounding a joint following distension or damage to structures of that joint is termed arthrogenic muscle inhibition.2 When AMI is present, the targeted muscle group does not have the ability to contract to its maximal potential, resulting is muscle activation failure which is problematic for both the patient and clinician. If we are not using our muscles to their maximal potential during normal rehabilitation exercises, we could say that we are actually doing a disservice to our patients by not assessing and not addressing the impairment. It is essential to find a novel way to assess gluteus medius and maximus function besides the standard strength assessment. The central activation ratio with superimposed burst technique is one method that has been used to assess AMI, and ample amounts of research have been conducted in regards to the volitional activation of the quadriceps and hamstrings. Yet, there is very limited research done studying AMI in the gluteal muscle group to assess the presence of muscle activation failure. Therefore, the purpose of this project is to identify if the central activation ratio

20 with superimposed burst technique is a feasible and reliable source to measure gluteus medius and gluteus maximus inhibition. Additionally, we will examine if a relationship between hip muscle strength and the torque of the superimposed burst.

Research Question: In healthy patients, will a superimposed burst technique be a feasible and reliable source for measuring gluteus medius and gluteus maximus inhibition? Additionally, is there a relationship between strength and torque of the superimposed burst.

Experimental Hypothesis The superimposed burst technique will be a reliable and feasible source for measuring muscle inhibition of the gluteus medius and gluteus maximus. We hypothesize that the higher percentage of stimulus through the SIBT, there will be a correlated linear relationship between percentage of stimulus and gluteus muscle activation

Assumptions:

 Patient will provide maximal effort on all study tasks  Patient is honest when signing the consent form about meeting the inclusion and exclusion criteria for the study  Testing Position will accurately measure gluteus medius and gluteus maximus function

Delimitation:

 Subject population was limited to healthy individuals between the ages of 18 and 35 y/o  Patients with electrical stimulation contraindications are excluded from this study

21  Patient worked out 24-48 hours before testing strength and patient experienced DOMS during the task at  Patients who have a previous medical history of surgery on lower extremity/low back  Patients who have a previous medical history of injury of lower extremity/low back in the past 6 months

Limitations:

 One limitation of the current study may have been the pad placement for the gluteus maximus might not have correctly correlated with the superior and inferior fibers of the muscle.  Another limitation of the current study may have been that the patient was fatigued towards the end of each testing session

Operational Definitions:

 Arthogenic Muscle Inhibition (AMI): An ongoing reflex inhibition of the musculature surrounding a joint following distension or damage to structures of that joint  Superimposed Burst Technique (SIBT): An electrical stimulus placed on a patient in order to recruit any leftover motor units that were unable to be recruited following an MVIC.  Central Activation Ratio (CAR): a feasible measurement at assessing muscle strength and the inhibition associated with it.  Gluteus Medius: i. O: Gluteal Surface of Ilium ii. I: Greater Trochanter of iii. N: Superior Gluteal Nerve iv. A: Abduction, Hip Extension, Internal Rotation  Gluteus Maximus i. O: Gluteal surface of ilium, lumbar fascia, sacrum, sacrotuberous ligament ii. I: Gluteal tuberosity of the femur and iliotibial tract iii. N: Inferior Gluteal Nerve iv. A: Hip Extension and External Rotation  Maximal Voluntary Isometric Contraction (MVIC): Patient activates their muscle to their fullest potential without shortening or elongating the muscle.

22

Innovation:  This study may provide a novel way to assess gluteal muscle function, which can lead to future studies involving this same measurement but in pathological populations (i.e. PFP, LBP). By identifying novel assessment methods, clinicians and researchers may be able to develop more optimal treatment programs to treat these patients.

23 Appendix B

Literature Review

Gluteus Medius and Maximus

Anatomy: Movements at the hip are controlled by groups of large extrinsic and small intrinsic muscles. Large muscle groups act to flex, extend and internally rotate the hip while the small intrinsic muscles serve to externally rotate the hip 1. During most movements occurring at the hip joint, the hip abductors and adductors purpose is to stabilize the hip rather than produce force. There are four different compartments where muscles of the hip are located: anterior, medial, lateral, and posterior. The gluteus medius is located on the lateral side on the hip and is the most superficial of the lateral muscles. The gluteus medius originates at three different point: External surface of superior ilium, anterior gluteal line, and the gluteal aponeurosis. It inserts on the greater trochanter of the femur and is innervated by the superior gluteal nerve (Root L4, L5, S1)1.

The largest part of the is made up of the gluteus maximus. This muscle is a primary hip extensor, especially when the knee is flexed. This muscle has three origin points: posterior gluteal line of the ilium, posterior sacrum, and posterior coccyx. The gluteus maximus inserts on the gluteal tuberosity of the femur and through a fibrous band on the iliotibial tract. This muscle is innervated by the inferior gluteal nerve (Root L5,

S1, S2)1.

Function: The gluteus medius is a primary abductor of the hip joint. The anterior fibers also assist in hip flexion and hip internal rotation while the posterior fibers assist in hip extension and hip external rotation. Proximal factors, such as hip strength play a vital role in the biomechanics of the patellofemoral joint. During gait and normal weight

24 bearing activities, hip extensors and hip abductors eccentrically to control the femur from adducting and internally rotating. Excessive femur adduction can lead the patient to have knee valgus which would excessive lateral forces being placed on the patella.

Excessive internal rotation will also cause an abnormal tracking of the patella that causes unnecessary forces to act on the patella and lateral femoral condyles. Therefore, it is important to keep hip muscles especially gluteus medius and gluteus maximus as strong as possible seeing as they are hip extenders and hip abductors to reduce the amount of patella femoral pain that could occur in a patient 3. The gluteus medius is also important in maintaining the horizontal position of the pelvis and the torso’s upright posture during a gait pattern. For example, a Trendelenburg gait pattern is characterized by the dropping of the pelvis on the unaffected side of the body at the moment of strike on the affected side. In this deviation the pelvic drop during the cycle lasts until heel strike on the unaffected side and is accompanied by an apparent lateral protrusion of the affected hip. A person with a Trendelenburg gait also shortens the step on the unaffected side and displays a lateral deviation of the entire trunk and the affected side during the stance phase of the affected lower limb. This gait is one of the more common gait deviations (Medical Dictionary: The Free Dictionary.com). The gluteus maximus muscle is the most powerful extensor and external rotator of the hip. Furthermore it supports the stabilization of the hip joint. Its functions include hip extension, hip external rotation, hip adduction (inferior fibers), and hip abduction (superior fibers)4. It is found that with some rehabilitation protocols, we are not targeting the specific portions or fibers that need to be targeted in order to achieve a healthy outcome. Although the gluteus maximus is one large muscle, clinically, it is sought to have two very different functional

25 portions of the muscle. The superior portion of the muscle is much larger than that of the inferior portion. Powers et al. stated that the superior portion of the gluteus maximus is more responsible for hip abduction due to its insertion on the fascia lata, whereas the inferior portion of the gluteus maximus is more responsible for hip extension due to its larger moment arm 4. There have been multiple studies thus far to look at functional activation patterns of both the superior and inferior portions of the gluteus maximus. In this specific study done by Powers et al., twenty healthy patients were recruited. An

EMG system was used and electrodes were placed over the superior and inferior portions of the gluteus maximus. The patients were asked to do a maximal voluntary isometric contraction (MVIC) in four different positions in no specific order. The first test, hip extension was resisted using a strap across the posterior thigh, with the upper body prone on a treatment table, the hip at an angle of 45 degrees of flexion, and the knee at 90 degrees of flexion. For the second test, hip extension was resisted using a strap across the posterior thigh with the subject lying fully prone, with the knee flexed to 90 degrees. The third test was done in hip abduction side lying on the opposing treatment table. In 30 degrees of hip abduction and the knee fully extended, the patients exerted a maximal hip abduction force against a strap across the distal lateral leg. In the fourth test, the patient was in a similar position except the hip was abducted 30 degrees and flexed to 45 degrees and asked to perform a maximal hip abduction force against the strap 4. Between the two portions of the gluteus maximus, each test done revealed activation of the superior portion was much greater than that of the inferior portion during hip abduction in side lying, clam, side step, hip hike, and step up exercises. Both the inferior and superior portions of the gluteus maximus had equal activations when it came to exercises that

26 involved hip extension motions. The superior portion of the gluteus maximus produced the highest EMG signals during clam exercises due to its motion of hip abduction and external rotation. The inferior portion of the gluteus maximus produced the highest EMG signals during any motions that occurred in the sagittal planes, such as hip extension 4.

Role it has with knee, hip, and back problems:

Knee: In a study by Kim et al, he looked at the effect of gluteus medius strengthening on the knee joint function score and pain in meniscal surgery patients. Instability of knee joint can change neuromuscular control system of lower limbs followed by abnormal changes in core muscles that control hip joint such as gluteus maximus and gluteus medius.. An altered gluteus medius muscle along with a decrease in muscle fiber activation can cause the hip to adduct and internally rotate during a patients gait5. Seeing that this is the case, gluteus medius strengthening is a must following any type of knee surgery especially meniscal pathologies.

Hip: Appropriate gluteus medius strength has been directly correlated to improved physical performance5. Decreased strength and/or fatigue of the gluteus medius can result in excessive pelvic rotation and femoral internal rotation which can cause pain and other serious pathologies in the lower extremity6. A study was done by Philippon et al. to see if progressive hip exercises to strengthen the gluteus medius muscle could be identified that minimize concurrent iliopsoas muscle activation to reduce the risk of developing or aggravating hip flexor tendinitis 7. Muscle activation of the gluteus medius and iliopsoas was tested by 13 different rehabilitation exercises. “The 13 exercises included the double-leg bridge, singleleg bridge, prone heel squeeze, supine hip flexion, sidelying hip abduction with internal rotation, side-lying hip abduction with external

27 rotation, side-lying hip abduction against a wall, traditional hip clam, hip clam with hip in neutral, resisted terminal knee extension, resisted hip extension, resisted knee flexion, and stool hip rotation” 7,8. The study categorized each exercise into three different phases of rehabilitation. Phase 1 included the following exercises: Resisted terminal knee extension, resisted knee flexion, and double-leg bridges. Phase 2 included: Resisted hip extension, stool hip rotations, and side-lying hip abduction with wall-sliding. And Phase

3 included: Hip clam exercises with neutral hips may be used with caution in patients with hip flexor tendinitis. Prone heel squeezes, side-lying hip abduction with internal hip rotation, and single-leg bridges 7,9. This study helped us identify which exercises directly activate the gluteus medius without activation from the hip flexors. We can learn from this study by using the exercises directly activating the gluteus medius into our rehabilitation programs to better strengthen this muscle.

Back: Back pain is the most common injury brought to a secondary to upper respiratory tract . Physical rehabilitation is usually the first thing prescribed by a physician to treat back pain but knowing what types of exercise to prescribe and what muscles to specifically target still can be considered an uncertainty10. “Recent experimental studies have identified altered recruitment of gluteus medius as a predictive factor for who does, and does not develop pain in the low back during prolonged standing”11. A study done by Marshall et al, looked at a two hour prolonged standing task in previously asymptomatic patients and then looked at different functional movements of the gluteus medius. This study found that there was no significant difference between low gluteus medius strength and back pain but did find some differences of the endurance levels of those who reported back pain.

28 Ankle: When a significant lateral ankle sprain occurs, the term given to patients who undergo this issue an ample amount of times is called Chronic Ankle Instability (CAI).

CAI can be characterized three different ways: “1) mechanical instability related to anatomical changes in tissues surrounding the ankle, 2) functional or perceived instability related to neuromuscular changes, or 3) recurrent sprains in which a patient experiences repeated inversion injury with activity. Individuals with CAI may be subcategorized into

1 of these categories or a combination of the three” 12. A numerous amount of authors have hypothesized that CAI occurs in patients because of an altered peripheral neuromuscular control secondary to an injury. Impairments do not only occur to the ankle but to the whole lower extremity as well. CAI can effect , neuromuscular control, and strength down the entire kinetic chain, specifically at the hip.

Webster et al proposed that neuromuscular control at the hip, specifically at the gluteus medius and gluteus maximus contributes to positioning of the entire lower extremity and is possibly affected in patients with CAI 12. In this specific study by Webster et al, they had electromyography (EMG) interventions set in place for patients with CAI and had these patients perform a jump landing, specifically before and after functional fatigue and looked at the muscle activation of the tibialis anterior, peroneous longus, gluteus medius, and gluteus maximus12. The gluteus maximus demonstrated a higher activation in the

CAI group compared to the control group whereas there were no statistical differences between the CAI group and the control group when looking at the gluteus medius muscle.

Understanding and researching these possibilities of patients with CAI can help us in the future to implement better rehabilitation protocols to prevent future injuries.

29 Rehab/Strengthening Exercises: As previously stated, the gluteus medius plays a vital role stabilization at both the lower extremity and the pelvis. Keeping this muscle strong is a necessity for an active individual if they want to remain healthy. Tufano et al wrote a study looking at strengthening the gluteus medius using various bodyweight and resistance exercises13. They found that doing heavy loaded exercises is found to be more effective than single joint rehabilitation. They state “complex exercises such as squats, deadlifts, and step-ups can be heavily loaded, making them preferable compared to single-joint rehabilitation exercises in athletic populations because of their ability to progressively increase exercise intensity, increase the hormonal response, and result in satellite cell proliferation”13. Therefore, we suggest that heavy resistance exercises may be more effective at inducing functional strength gains of the gluteus medius in athletes because the force required to overcome external loads may be closer to the force required by an athlete during competition than the force required during unloaded, single-joint exercises 13. Gluteus medius strengthening is very important in sports because unilateral hip abduction weakness has been shown to increase the likely-hood of injuries in sports such as soccer and hockey. Tufano et al stated “gluteus medius strength may be even more important in sports when the center of mass changes direction unexpectedly, requiring strength and stabilization during unilateral stance” 13. Often clinicians prescribe rehabilitation exercises on unstable surfaces in an attempt to try and mimic the instability that occurs during competitions. As I previously stated, the gluteus medius plays a vital role in stabilization at both the knee and pelvis. Tufano et al found that “doing exercises on an unstable surface does not result in additional activation of the gluteus medius

30 during squatting. Thus, the application of resistance training on unstable surfaces is unwarranted, as it may not effectively increase gluteus medius activity”13.

Gluteal Dysfunction: The gluteus medius has two main jobs: 1) Abduct your leg, and 2)

Stabilization. When the gluteus medius becomes weak, it often causes a change in in height at the hip joints that can lead to lumbar pain/radiating pain down the lower extremity. Early research has shown to strengthen the gluteus medius by placing bands around the hip, knee, and ankle and performing sumo/monster walks. Recent research has shown to strengthen the gluteus medius in a position of slight hip flexion clam, side- lying abduction, and closed chain lateral lunges. Patients who are experiencing low back pain should focus on core stability and gluteal strengthening exercises14. A study done by Lee et al, looked at muscle activation of the posterior fibers when patients were placed under different load bearing conditions15. These patients would be standing on one leg and have four different loads placed on them: “the standard no-load condition, in which the non-weight bearing leg was lifted and kept parallel to the back and then pelvic or lumbar rotation was performed without rotation and the 0kg, 1kg, and 3kg load conditions, in which horizontal abduction was performed with a load of 0kg,

1kg, and 3kg added to the hand” 15. The posterior fibers of the gluteus medius are responsible for hip abduction, external rotation and assist in extension. Muscle activation was compared according to the load when the weight-bearing side was rotated externally in the one-leg standing position. This study revealed that the posterior fibers of the gluteus medius were activated most under the 3kg load placed while in the one-leg standing position. Also, the load on the upper extremity depends on the muscle activity of the contralateral lower extremity 15. There are a handful of injuries that can result

31 from having a weak gluteus medius: Iliotibial Band Syndrome (ITBS), Knee pain, Low back pain, etc. Iliotibial Band Syndrome is considered by most to be an overuse injury, commonly seen in runners and cyclists. The iliotibial band is a thick band that crosses the hip joint and inserts on the patella and . There are multiple reasons that someone could develop ITBS, but one common thought is because of weak gluteus medius. This condition is brought on because of the IT Band gets inflamed from rubbing over the lateral femoral epicondyle. Therefore, during Trendelenburg gait, an increase in hip drop causes the band to stretch over the trochanter of the femur. The band then gets tensioned over the greater trochanter causing it to tighten over the lateral femoral epicondyle on the knee. With a weak gluteus medius, you can also have medial knee pain. The job of this muscle is to abduct the leg. So when it’s not functioning properly, the leg starts to adduct which will place stress on the medial collateral ligaments. This increase stress could lead to pathologies such as Patello Femoral Pain (PFP) and increase stress on the Medial Patello-Femoral Ligament (MPFL) due to its increased valgus angle.

Low back pain is very common in patients with weak gluteus medius’. “As the lower back muscles compensate to get your head aligned properly, your quadratus lumborum muscles can tense up, develop trigger points, and ultimately cause back pain” 1. Proper stretching and trigger point release of both the quadratus lumborum and gluteus medius muscles might be needed. The pairing of the hip adductors on the same side and the opposite side quadratus lumborum forms the lateral subsystem of stability. Weak gluteus medius can also cause the leg to internally rotate which can lead to medial tibial stress syndrome and plantar fasciitis because of the change in gait that will occur. There are two different ways you can assess gluteus medius weakness: 1) Stand manual muscle test

32 or 2) Double leg stance to Single leg stance. For a manual muscle test you would have your patient side lying and resist an abduction motion of their affect limb. For the second way to assess gluteus medius weakness, you would have the patient stand directly in front of you and have your patient go from standing normally to raising one limb. You are looking at the structure of the pelvis and seeing if you notice any type of hip drop.

Arthogenic Muscle Inhibition (AMI)

Definition: Muscle inhibition is the diminished ability to contract a muscle voluntarily.

Arthrogenic muscle inhibition is “an ongoing reflex inhibition of the musculature surrounding a joint following distension or damage to structures of that joint”16. Muscle weakness following injury or surgery to a specific joint is very common as per the literature. This phenomenon is mostly researched in the quadriceps following knee injury or surgery. Hart et al did a systematic review titled “Quadriceps Activation Following

Knee Injuries: A Systematic Review” 17. The goal of this study was to look at how often and what the extent of damage was done to the quadriceps and their ability to contract following an injury to the knee. They categorized these patients into three different categories: Anterior Cruciate Ligament Deficient (ACLd), Anterior Cruciate Ligament

Reconstruction (ACLr), and Anterior Knee Pain (AKP) patients. They found that clinically, all three patients in these three categories found to have some sort of quadricep activation (QA) deficiency. They also found that the magintude of activation in AKP patients increased than patients who suffered from ligament injuries. AMI can best be described as the inability to contract a muscle despite having no damage done to it. Hart et al states that AMI could be a protective mechanism that the body undergoes following injury, but can cause serious limitations during rehabilitation 17. The exact mechanisms

33 causing and regulating quadriceps and hamstrings AMI after knee joint injury and Central

Activation Deficit (CAD) after surgery remain unclear. “The decreasing volitional force output associated with AMI and CAD may be caused by altered afferent input originating from mechanoreceptors within the diseased joint reflexively which reduce efferent output from quadriceps alpha motor neurons. Although poorly understood, cortical pathways may also contribute to reduced alpha motoneuron excitability 17. Other factors such as joint effusion, pain, and disuse may also contribute to quadricep inhibition after joint injury. The effused joint may reduce the excitatory input of the surrounding muscles by activating several gating mechanisms within the central nervous system.

Central Activation Ratio (CAR):

What/ How it’s Measured: Quadricep activation is a vital part of normal gait.18,19

Mainintaing strength and enduracne throughout gait cycles plays an important role in normal knee joint function, so making sure that these varibilites are restored is an important component in the rehalibilation process following injury. 17 It has been studied often that the central activation ratio (CAR) is a feasible measurement at assessing muscle strength and the inhibition associated with it. These measurements have mainly been studied on the quadriceps and hamstrings which is why studying this measurement on the gluteus medius could have the potential to influence future research and interventions associated with weaknesses to the gluteus medius muscle. Current literature has evaluated the CAR of the quadriceps and hamstrings by having their patient perform a maximal voluntary isomestric (MVIC) contraction on the dynamometer. The patient would kick out as hard as they could and once they have plateaued, the researcher would initiate a superimposed burst technique (SIBT) which would then in theory,

34 acitvate all the remianing motor units that the patient was unable to do so during the

MVIC.20 Calculation of the central activation ratio using the superimposed burst technique is used to assess availiability of motoneurons for recruitment.20-22 It is stated in the literature that people who are able to activate, voluntarily more than 95% of their motor units are said to be fully activated.17,23 In a systematic review done by Hart et al., they looked at quadricep activation secondary to anterior cruciate ligament reconstruction. 17 The SIBT and ITT techniques were used for 99 participants to assess quadricep neural activation. The weighted mean was 86.5% (95% CI 5 78.1, 94.9) for the involved side, 84.0% (95% CI 5 74.8, 93.2) uninvolved side, and 98.3% (95% CI

=97.2, 99.4) for control participants. 17,23-25 Another three groups looked at quadricep activation with anterior knee pain (AKP). The weighted means of the 38 paitents with

AKP were 78.6% (95% CI=70.1, 87.0) on the involved side where as on the uninvolved side the weighted means were 77.7% (95% CI= 67.5, 87.9) with only one author reporting 97.6% (95% CI= 95.9, 99.3) quadricep activation in control patients. 17,26-28 We can conclude from this that patients who suffered from ACLr or AKP had significantly lower quadricep activation when comparing the involved limb to the uninvolved limb.

Patients who suffered from AKP had slightly lower quadricep activation than those who suffered from knee ligament damage.17

Central Activation Failure: Patients with quadricep dysfunction that they lack the ability to essentrically contract the quadricep in the hope to normalize their knee range of motion which is important in maintaining proper anatomical allignment within joint surfaces.29,30

There has been an ample amount of research done on treatment strategies in attempt to minimize the amount of inhibition that occurs during quadricep activation. Traditional

35 rehabilitation techniques that focus on quadricep strength training to normalize its function yet this strength training does not alter quadriceps activation.29 A new paradigm called disinhibitory interventions has been sought out to combine interventions that both provide optimal quadriceps activation while providing optimal strength training as well.2,29,31,32 Disinhibitory interventions are classified as the techniques used to change motor excitability after injury to a joint to improve voluntary quadriceps activation and to enhance therapeutic exercise.29,31 Harkey et al looked at viable techniques to disinhibit the quadriceps to attempt to provide optimal quadriceps activation.29 One method that they looked at was cryotherapy. Investigations of cryotherapy studies presented with

Oxford level of evidence with its highest level seen in patients with knee osteoarthritis.29,33,34 These studies focused on the immediate effects of the intervention by having post testing measurements at 20, 30 and 45 minutes. This intervention was at its best at 45 minutes seeing that this was when there was the largest increase in quadriceps activation.29,33,34 Another method that was assed was Transcutaneous

Electrical Nerve Stimulation (TENS). Investigations of TENS studies also presented with Oxford level of evidence with its highest level being seen in patients with knee osteoarthritis.29,34,35 One group reported its outcomes at 20, 30, and 45 minutes specifically. There was a small effect size at 20 minutes but the effect size greatly increased at 30 minutes and remained high at 45 minutes as well. The long term effects were also studied at 2 and 4 weeks, which was found to have even stronger effect sizes than those of the short term studies. Neither the short or long term effect sizes crossed zero.29,34,35 Current studies find that TENS is the most efficient at increasing quadriceps activation because it does not have any CI’s that cross zero and produced positive

36 homogeneous findings. The TENS unit is placed over the injured joint and it is hypothesized that it will target presynaptic reflex inhibitory mechanisms36 that lead to quadriceps dysfunction.37 Cryotherapy is also hypothesized to alter afferent stimuli ascending from the specific injured area, yet it’s still not found to be as effective as

TENS therapy.29 These methods have not been studied yet in the gluteus medius and gluteus maximus to attempt to treat central activation failure and the inhibition that occurs in these muscles. Researching the central activation ratio/failure in these two muscle groups will be beneficial to clinicians because it will give them a more accurate assessement of the strength of the patient compared to the novel way of manual muscle testing each muscle.

37 Appendix C

Additional Methods

I. Biodex Set-Up a. Make sure Biodex is plugged into outlet b. Turn on two green switches on back of Biodex in bottom left hand corner c. Turn on modem and monitor d. Open “Biodex Advantage” on computer e. For Gluteus Medius Isometric Contraction Set Up i. Patient will be standing, facing the dynamometer, perpendicular to the chair ii. The knee attachment will be placed on the dynamometer, making sure to match up the red dots from the attachment and the dynamometer itself iii. Axis of rotation will be aligned through the patients ASIS of the test limb. iv. The strap of the knee attachment will be placed 4 cm proximal to the patients lateral femoral condyle v. The chair will be set up in a 90 degree angle with a square block placed on the bottom part of the chair for patient support during isometric Contraction

38 f. For Gluteus Maximus Isometric Contraction Set Up i. The chair will be laid out flat ii. Patient will be positioned so that the trunk is flexed to 90 degrees and their are wrapped around the chair of the dynamometer to stabilize the trunk iii. The knee attachment will be placed on the dynamometer, making sure to match up the red dots from the attachment and the dynamometer itself iv. The axis of rotation for the dynamometer was aligned with the greater trochanter of the femur of the test limb v. The strap of the knee attachment will be placed on the patients posterior thigh, just superior (4cm) to the patients knee

II. Acknowledge Set-Up a. Turn on modem and monitor of the computer b. Open “Acknowledge Templet” c. Open “CAR” d. On the top of the screen, click on “MP150” e. Click on “Set up data acquisition” f. Click on “setup” in the top left hand corner of the screen g. Evaluate analog channel set up: (See picture below), then click “ok” h. Click start in the top left corner of the screen and perform an isometric contraction on the Biodex to make sure that you are getting a positive value III. Hardware Set-Up a. BIOPAC Systems, INC MP150 i. System should already be always on ii. Make sure that your torque wire is in channel 1

39

b. GRASS S48 Stimulator i. Train Rate: 10 ii. Train Duration: 1 iii. Stim Rate: 10 iv. Delay: 1 v. Duration: 6 vi. Volts: 4 (25%), 8 (50%), 12 (75%), 16, (100%) vii. Flip switch on lower left hand side of unit viii. Train Mode Repeat push down to administer stimulus

c. GRASS Stimulation Isolation Unit i. Attach one end of red wire to stim pad and to red output port of stimulus isolation unit

40 ii. Attach one end of black wire to stim pad and to black output port of stimulus isolation unit iii. On the bottom of the stimulus isolation unit, turn the switch to “on”

d. Electrode Pads & Placement i. For Gluteus Medius 1. Use “Self-Adhesive TENS/NMES/FES Stimulating Electrodes” 2. REF: 42181 3. Dura-Stick Plus 4. 2.in x 3.5 in (5cm x 9cm) ii. For Gluteus Maximus 1. Use “Self-Adhesive TENS/NMES/FES Stimulating Electrodes” 2. REF: 42045 3. Dura-Stick Plus 4. 2.in x 3.5 in (5cm x 9cm) iii. Placement of Electrodes for Gluteus Medius 1. One will be placed just inferior to the Iliac Crest 2. One will be placed just superior to the Greater Trochanter iv. Placement of Electrodes for Gluteus Maximus 1. One will be placed just inferior to PSIS, and just lateral to sacrum 2. One will be placed 4cm inferior and 4cm medial to greater trochanter IV. Set-Up Start to Finish

41 a. Turn on the Biodex b. Set up dynamometer and Biodex chair to patients height c. Attach knee attachment to the dynamometer d. Make sure axis of rotation is set up to specific anatomical landmark for the task at hand e. Open up Acknowledge software f. Open up “Dan CAR” template g. Attach stim pads on specific areas as described above h. Attach wires from isolation unit to stim pads as described above i. Strap the patient into their specific position as described above j. Turn on Grass Stimulator and make sure dials are all set to their specific numbers as described above k. Once patient is all set up and the instruments are ready to go, have the patient perform 1 MVIC (maximal voluntary isometric contraction) practice trials i. 25% MVIC 1. 30 second rest ii. 50% MVIC 1. 30 second rest iii. 75% MVIC 1. 30 second rest iv. 100% MVIC 1. 30 second rest l. The patient will then perform 4 resting trials with 4 different stimulus administered i. Resting Trial with 25% Stimulus 1. 30 second rest ii. Resting Trial with 50% Stimulus 1. 30 second rest iii. Resting Trial with 75% Stimulus 1. 30 second rest iv. Resting Trial with 100% Stimulus 1. 30 second rest m. The patient will then perform the following: i. (2) 25% MVIC with 100% Stimulus 1. 30 second rest between each MVIC ii. (2) 50% MVIC with 100% Stimulus 1. 30 second rest between each MVIC iii. (2) 75% MVIC with 100% Stimulus 1. 30 second rest between each MVIC

42 iv. (3) 100% MVIC with 100% Stimulus 1. 30 second rest between each MVIC V. Participant will return to the lab one week later a. Identical warm up and pad placement will be utilized b. Complete (3) 100% MVIC with 100% Stimulus trials for the gluteus medius c. Complete (3) 100% MVIC with 100% Stimulus trials for the gluteus maximus

Executive Summary University of Toledo

Title: Central Activation Ratio with a Super Imposed Burst Technique to Assess Muscle Activation of the Gluteus Medius and Gluteus Maximus Principal Investigator: Neal Glaviano, PhD, AT, ATC Research Team: Daniel Gilfeather, AT, ATC -Grant Norte, PhD, AT, ATC -Christopher Ingersoll, PhD, AT, ATC, FNATA, FACSM Purpose: • The purpose of this project is to quantify the Central Activation Ratio (CAR) with the Super Imposed Burst Technique (SIBT) of the gluteus medius and gluteus maximus is an appropriate method to assess muscle strength and muscle activation. • To identify if a relationship exists between strength and torque of the SIBT. • Evaluate the reliability of these measures one week post initial testing period

Participants: 15-20 Participants from local university and community Inclusion Criteria: • Healthy individuals18-35 y/o • Physically active at least 3x/week

Exclusion Criteria: • Patients with electrical stimulation contraindications are excluded from this study • Patient worked out 24-48 hours before testing strength and patient experienced DOMS during the task at hand • Patients who have a previous medical history of surgery on lower extremity/low back • Patients who have a previous medical history of injury of lower extremity/low back in the past 6 months

43 Study Design: Descriptive Laboratory Study Independent Variable: • Time intervals (Session 1, Session 2) • Percent of stimulus (25%, 50%, 75%, 100%)

Dependent Variables: • Muscle activation measured by the Central Activation Ratio using the SIBT

Procedures: 1. Recruit healthy subjects from local community and university 2. Have subjects sign informed consent 3. Have subjects take the Tegner Activity Level Scale 4. Subjects will have electrical stimulus pads on their gluteus medius 5. Subjects will be set up on the Biodex specific to the muscle that’s being tested 6. Subjects will perform three MVIC’s at 25%, 50%, 75%, and 100% 7. Subjects will undergo four rest trials while researcher administers a stimulus at 25%, 50%, 75%, and 100% 8. Subjects will perform two, 25% MVIC while researcher administers a 100% stimulus 9. Subjects will perform two, 50% MVIC while researcher administers a 100% stimulus 10. Subjects will perform two, 75% MVIC while researcher administers a 100% stimulus 11. Subjects will perform three, 100% MVIC while researcher administers a 100% stimulus 12. Subject will have electrical stimulus pads on their gluteus maximus 13. Subjects will repeat steps 5-11 14. Subjects and/or researcher will remove any stimulus pads and wires from the subject 15. Subjects will return to laboratory for maximum CAR assessment for both gluteus muscles one week later 16. Subjects will be dismissed

IRB Protocol: 202210 Statistical Analysis: • Pearson R Correlations will be used to evaluate the relationship of our dependent variables. The reliability of the gluteal activation ratio will be assessed by Intra-Class Correlation Coefficients (ICC)

Research Hypothesis: • CAR in a healthy population in the gluteal muscles is a feasible and reliable measurement

44 • We hypothesize that the higher percentage of stimulus through the SIBT, there will be a correlated linear relationship between percentage of stimulus and gluteus muscle activation.

45

46

47

48

49 Appendix D

Additional Results

50

GMax ICC

51 GMed ICC

52 Paired Samples Statistics

Mean N Std. Deviation Std. Error Mean Pair 1 MVIC_GMax_D1 1.4586 19 .48567 .11142 MVIC_GMax_D2 1.4986 19 .67333 .15447 Pair 2 SIB_GMax_D1 1.6468 19 .47861 .10980 SIB_GMax_D2 1.6461 19 .61281 .14059 Pair 3 MVIC_GMed_D1 .9179 19 .35600 .08167 MVIC_GMed_D2 .9149 19 .33253 .07629 Pair 4 SIB_GMed_D1 .9319 19 .35111 .08055 SIB_GMed_D2 .9318 19 .34237 .07855

Paired Samples Correlations

N Correlation Sig. Pair 1 MVIC_GMax_D1 & 19 .493 .032 MVIC_GMax_D2 Pair 2 SIB_GMax_D1 & 19 .438 .061 SIB_GMax_D2 Pair 3 MVIC_GMed_D1 & 19 .702 .001 MVIC_GMed_D2 Pair 4 SIB_GMed_D1 & 19 .706 .001 SIB_GMed_D2

53

54

55

56 Gluteus Medius CAR during Progressive Contractions

100 R² = 0.4094

90

80

70

60

50

40

CentralActivation (%) Ratio 30

20

10

0 0 10 20 30 40 50 60 70 80 90 100 Progressive Contraction (% )

Gluteus Maximus CAR during Progressive Contractions 100

90 R² = 0.6396

80

70

60

50

40

30 CentralActivation (%) Ratio 20

10

0 0 25 50 75 100 Progressive Contraction (%)

57 Appendix E

Back Matter

Future Considerations

 CAR has been a common method for assessing muscle inhibition specifically on the quadriceps in both healthy and pathological groups. This method should also be done on the gluteus medius and gluteus maximus in pathological groups such as PFP, LBP, and ACLr patients.  Patient positioning for hip abduction should be further looked into to decide what the best position for assessing muscle strength. Previous studies have looked into assessing hip muscle strength via a sidelying patient position.  Locating the correct pad placement to optimize stimulation for the superior and inferior muscle fibers of the gluteus maximus is essential for correctly assessing muscle activation.  The relationship between increasing the stimulus and patient discomfort may be a limiting factor for measuring CAR. Previous authors have evaluated ways to improve patient comfort when assessing muscle inhibition. One way has been measuring inhibition by the Interpolation Twitch vs. SIB Technique.  Patient fatigue might have played role in lower gluteus maximus CAR values. Switching the three trials of 100% MVIC/100% stimulus to the first trials during session one could improve gluteus maximus CAR values.

58 NATA Abstract

Context: Hip weakness is a common consequence of many lower extremity injuries and may contribute to altered frontal plane motion. Gluteal strength is the traditional method to measure function; however other measurements of neuromuscular function are essential. The central activation ratio (CAR) is a common way to assess muscle inhibition and has primarily been studied on the quadriceps. However, there is no literature on this measurement on the gluteus medius and gluteus maximus. Objective: Quantify the CAR of the gluteus medius and gluteus maximus muscles in a healthy population and evaluate its reliability over a one-week period. Study Design: Descriptive Setting: Laboratory Participants: Twenty healthy participants (9 male and 11 females: age 22.2 ± 1.4 years, height 173.4 ± 11.1 cm, mass 84.8 ± 25.8 kg) were recruited from the local university and community were enrolled in this study. Intervention: Hip abduction and extension at progressive intensities (25%, 50%, 75%) and maximal voluntary isometric contraction (MVIC) were assessed in a stationary dynamometer. Gluteal activation was assessed with the superimposed burst (SIB) technique, with gluteus medius assessed in hip abduction and gluteus maximus during hip extension. Measures were repeated one-week later. Main Outcome Measures: Primary outcome measures included (1) gluteal medius and maximus central activation ratio (CAR) (2) normalized hip abduction and extension MVIC and SIB (Nm/kg), and (3) CAR at progressive contractions during hip abduction and extension (25%, 50%, 75%, 100%). Paired t-tests were used to compare differences in outcome measures between the two testing sessions. Interclass correlated coefficients (ICC) were used to calculate test-retest reliability. A line of best fit was used to evaluate the relationship between CAR and varying progressive contractions for hip abduction and extension, and coefficient of determination (r2) were used with regression analysis. Results: The gluteus medius CAR (Day 1: 96.1±3.37, Day 2: 96.6±3.16, p=0.599) has excellent reliability (ICC -[3,1] =.911). The gluteus maximus CAR (Day 1: 86.5±7.5, Day 2: 87.2± 10.7, p=0.737) was moderately reliable (ICC -[3,1] = .704). No differences were seen between hip abduction MVIC (Day 1: 1.56±0.29Nm/kg, Day 2: 1.57±0.51Nm/kg, p=0.876) or SIB (Day 1: 1.59±0.31Nm/kg, Day 2: 1.60±0.51, p=0.892) or hip extension (Day 1: 2.54±0.69Nm/kg, Day 2: 2.64±1.15Nm/kg, p=0.695) or SIB (Day 1: 2.88±0.70Nm/kg, Day 2: 2.91±1.01, p=0.896.) A linear relationship demonstrated the line of best fit for both gluteus medius CAR during hip abduction (r2=0.409) and gluteus maximus CAR during hip extension (r2=0.639). Conclusions: CAR appears to be a reliable method to assess gluteal function in a healthy population within a one-week period. The SIB technique appears to be a valid method to stimulate the gluteal muscles and assess inhibition of the gluteus medius and maximus.

59 Gluteal CAR should be measured within a pathological population to assess potential neuromuscular impairments. Key Words: Gluteal Activation, Neuromuscular Function

NATA Poster

60 Appendix F

Bibliography

1. Chad Starkey SDB, Jeff Ryan. Examination of Orthopedic and Athletic Injuries.

Vol 3. Philadelphia, PA: F.A. Davis Company; 2010.

2. Hopkins JT, Ingersoll CD. Arthrogenic Muscle inhibition: A Limiting Factor in

Joint Rehabilitation. Journal of sport rehabilitation. 2000;9(2):135-159.

3. Nakagawa TH, Muniz TB, Baldon RM, Maciel CD, Amorim CF, Serrao FV.

Electromyographic preactivation pattern of the gluteus medius during weight-

bearing functional tasks in women with and without anterior knee pain. Revista

brasileira de fisioterapia (Sao Carlos (Sao Paulo, Brazil)). Jan-Feb

2011;15(1):59-65.

4. Selkowitz DM, Beneck GJ, Powers CM. Comparison of Electromyographic

Activity of the Superior and Inferior Portions of the Gluteus Maximus Muscle

During Common Therapeutic Exercises. The Journal of orthopaedic and sports

physical therapy. Sep 2016;46(9):794-799.

5. Kim EK. The effect of gluteus medius strengthening on the knee joint function

score and pain in meniscal surgery patients. Journal of physical therapy science.

Oct 2016;28(10):2751-2753.

6. Monteiro RL, Facchini JH, de Freitas DG, Callegaric B, Amado Joao SM. Hip

Rotations Influence Electromyographic Activity of Gluteus Medius Muscle

During Pelvic Drop Exercise. Journal of sport rehabilitation. Aug 24 2016:1-21.

7. Philippon MJ, Decker MJ, Giphart JE, Torry MR, Wahoff MS, LaPrade RF.

Rehabilitation exercise progression for the gluteus medius muscle with

61 consideration for iliopsoas tendinitis: an in vivo electromyography study. The

American journal of sports medicine. Aug 2011;39(8):1777-1785.

8. Ebert JR, Edwards PK, Fick DP, Janes GC. A Systematic Review of

Rehabilitation Exercises to Progressively Load Gluteus Medius. Journal of sport

rehabilitation. Aug 24 2016:1-35.

9. Bolgla LA, Uhl TL. Electromyographic analysis of hip rehabilitation exercises in

a group of healthy subjects. The Journal of orthopaedic and sports physical

therapy. Aug 2005;35(8):487-494.

10. Nelson-Wong E, Callaghan JP. Is muscle co-activation a predisposing factor for

low back pain development during standing? A multifactorial approach for early

identification of at-risk individuals. Journal of electromyography and kinesiology

: official journal of the International Society of Electrophysiological Kinesiology.

Apr 2010;20(2):256-263.

11. Marshall PW, Patel H, Callaghan JP. Gluteus medius strength, endurance, and co-

activation in the development of low back pain during prolonged standing.

Human movement science. Feb 2011;30(1):63-73.

12. Webster KA PB, Gribble PA. Muscle Activation During Landing Before and

After Fatigue in Individuals With or Without Chronic Ankle Instability. Journal

of Athletic Training. September 14th 2016;51(8):629-636.

13. Stastny P, Tufano JJ, Golas A, Petr M. Strengthening the Gluteus Medius Using

Various Bodyweight and Resistance Exercises. Strength and conditioning journal.

Jun 2016;38(3):91-101.

62 14. Semciw A, Neate R, Pizzari T. Running related gluteus medius function in health

and injury: A systematic review with meta-analysis. Journal of electromyography

and kinesiology : official journal of the International Society of

Electrophysiological Kinesiology. Oct 2016;30:98-110.

15. Lee JW, Kim YJ, Koo HM. Activation of the gluteus medius according to load

during horizontal hip abduction in a one-leg stance. Journal of physical therapy

science. Aug 2015;27(8):2601-2603.

16. Palmieri RM, Ingersoll CD, Hoffman MA, et al. Arthrogenic muscle response to a

simulated ankle joint effusion. British Journal of Sports Medicine. February 1,

2004 2004;38(1):26-30.

17. Hart JM, Pietrosimone B, Hertel J, Ingersoll CD. Quadriceps Activation

Following Knee Injuries: A Systematic Review. Journal of Athletic Training. Jan-

Feb 2010;45(1):87-97.

18. Torry MR, Decker MJ, Viola RW, O'Connor DD, Steadman JR. Intra-articular

knee joint effusion induces quadriceps avoidance gait patterns. Clinical

biomechanics (Bristol, Avon). Mar 2000;15(3):147-159.

19. Hurley MV. The role of muscle weakness in the of osteoarthritis.

Rheumatic clinics of North America. May 1999;25(2):283-298, vi.

20. Park J, Hopkins JT. Quadriceps activation normative values and the affect of

subcutaneous tissue thickness. Journal of electromyography and kinesiology :

official journal of the International Society of Electrophysiological Kinesiology.

Feb 2011;21(1):136-140.

63 21. Newman SA, Jones G, Newham DJ. Quadriceps voluntary activation at different

joint angles measured by two stimulation techniques. European journal of applied

physiology. Jun 2003;89(5):496-499.

22. Mizner RL, Stevens JE, Snyder-Mackler L. Voluntary activation and decreased

force production of the quadriceps femoris muscle after total knee arthroplasty.

Physical therapy. Apr 2003;83(4):359-365.

23. Urbach D, Nebelung W, Becker R, Awiszus F. Effects of reconstruction of the

anterior cruciate ligament on voluntary activation of quadriceps femoris a

prospective twitch interpolation study. The Journal of bone and joint surgery.

British volume. Nov 2001;83(8):1104-1110.

24. Drechsler WI, Cramp MC, Scott OM. Changes in muscle strength and EMG

median frequency after anterior cruciate ligament reconstruction. European

journal of applied physiology. Dec 2006;98(6):613-623.

25. Pfeifer K, Banzer W. Motor performance in different dynamic tests in knee

rehabilitation. Scandinavian journal of medicine & science in sports. Feb

1999;9(1):19-27.

26. Drover JM, Forand DR, Herzog W. Influence of active release technique on

quadriceps inhibition and strength: a pilot study. Journal of manipulative and

physiological therapeutics. Jul-Aug 2004;27(6):408-413.

27. Thomee R, Grimby G, Svantesson U, Osterberg U. Quadriceps muscle

performance in sitting and standing in young women with patellofemoral pain

syndrome and young healthy women. Scandinavian journal of medicine &

science in sports. Aug 1996;6(4):233-241.

64 28. Suter E, McMorland G, Herzog W, Bray R. Decrease in quadriceps inhibition

after sacroiliac joint manipulation in patients with anterior knee pain. Journal of

manipulative and physiological therapeutics. Mar-Apr 1999;22(3):149-153.

29. Harkey MS, Gribble PA, Pietrosimone BG. Disinhibitory interventions and

voluntary quadriceps activation: a systematic review. J Athl Train. May-Jun

2014;49(3):411-421.

30. Palmieri-Smith RM, Thomas AC. A neuromuscular mechanism of posttraumatic

osteoarthritis associated with ACL injury. Exercise and sport sciences reviews.

Jul 2009;37(3):147-153.

31. Dolan MG, Pietrosimone BG, Hopkins JT, Ingersoll CD. The Role of

Disinhibitory Modalities in Joint Injury Rehabilitation. Athletic Therapy Today.

2008;13(6):2-5.

32. Rice DA, McNair PJ. Quadriceps arthrogenic muscle inhibition: neural

mechanisms and treatment perspectives. Seminars in and rheumatism.

Dec 2010;40(3):250-266.

33. Pietrosimone BG, Hart JM, Saliba SA, Hertel J, Ingersoll CD. Immediate effects

of transcutaneous electrical nerve stimulation and focal knee joint cooling on

quadriceps activation. Medicine and science in sports and exercise. Jun

2009;41(6):1175-1181.

34. Pietrosimone BG, Ingersoll CD. Focal knee joint cooling increases the quadriceps

central activation ratio. Journal of sports sciences. Jun 2009;27(8):873-879.

35. Pietrosimone BG, Saliba SA, Hart JM, Hertel J, Kerrigan DC, Ingersoll CD.

Effects of transcutaneous electrical nerve stimulation and therapeutic exercise on

65 quadriceps activation in people with tibiofemoral osteoarthritis. The Journal of

orthopaedic and sports physical therapy. Jan 2011;41(1):4-12.

36. Iles JF. Evidence for cutaneous and corticospinal modulation of presynaptic

inhibition of Ia afferents from the human lower limb. The Journal of physiology.

Feb 15 1996;491 ( Pt 1):197-207.

37. Palmieri RM, Tom JA, Edwards JE, et al. Arthrogenic muscle response induced

by an experimental knee joint effusion is mediated by pre- and post-synaptic

spinal mechanisms. Journal of electromyography and kinesiology : official

journal of the International Society of Electrophysiological Kinesiology. Dec

2004;14(6):631-640.

66