A Thesis

entitled

Relationship Between Strength and Agonist-Antagonist Co-Activation

by

Meghan Gregoire

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

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

______Neal Glaviano, PhD, AT, ATC, Committee Member

______Amanda Murray, PT, DPT, PhD, Committee Member

______Lucinda Bouillon, PT, DPT, PhD, Committee Member

______Cyndee Gruden, PhD, Dean College of Graduate Studies

The University of Toledo

May 2019

Copyright 2019, Meghan Gregoire

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

Relationship Between Hamstring Strength and Agonist-Antagonist Co-Activation

by

Meghan Gregoire

Submitted to the Graduate Faculty as partial fulfillment of the requirements for the Master of Science Degree in Exercise Science

The University of Toledo May 2019

Introduction: Anterior cruciate ligament (ACL) injury is common among females due to several neuromuscular risk factors. Decreased to quadriceps (H:Q) ratio is one neuromuscular factor that place females at an increased risk of ACL injury. Increased activation of the hamstrings during functional tasks help assist the static stabilizes of the , decrease on the ACL and reduce anterior tibial translation. Objectives: The objective of this study was to (1) identify the relationship between H:Q strength and co- activation ratio in the medial and lateral compartments of the knee during the stance phase of walking gait as well as (2) compare H:Q ratio between high and low groups.

Methods: Ten healthy active females participated. Isokinetic flexion/extension contractions were assessed during five reputations at 60°/s, isokinetic peak torque

(Nm/kg) was recorded and normalized to body mass. Maximal voluntary isokinetic contraction of the knee extensors and flexors was assed at a joint angle of 60°.

Participants were asked to walk at three miles per hour for four minutes on a treadmill.

Participants were given a three-minute warm-up at a preselected speed of three miles per hour. At the end of the warm up patients were asked to quantify their rate of perceived exertion. Surface was used to quantify muscle activity of the

iv quadriceps (vastus lateralis and ) and hamstrings (semitendinosus and biceps femoris) during the last minute of the walking task and was normalized to the mean value of the MVIC data. Results: A significant moderate correlation was found between H:Q strength and co-activation in the lateral compartment (r= 0.663, p=0.052).

The low H:Q strength group had higher co-activation when compared to the high H:Q strength group. A significant difference (p=0.034) was found between low H:Q strength and co-activation in the lateral compartment. There was no relationship found in the medial compartment when comparing H:Q strength and co-activation. Conclusion: The results of this study indicate that lower hamstrings to quadriceps strength is associated with higher hamstrings to quadriceps co-activation in the lateral compartment during the loading response of walking.

v Acknowledgements

First and foremost, I would like to thank my committee chair and thesis advisor,

Dr. Grant Norte, without his unwavering support and expertise the completion of this study would not have been possible. I would also like to thank those on my thesis committee, Dr. Neal Glaviano, Dr. Amanda Murry and Dr. Lucinda Bouilion, for their contribution and continued involvement throughout the entire research process.

vi Table of Contents

Abstract iii

Acknowledgements vi

Table of Contents vii

List of Tables viii

List of Figures ix

List of Abbreviations x

I. Manuscript 1

A Introduction 1

B. Methods

a. Design 2

b. Participants 3

C. Procedures

a. Patient Reported Outcomes 3

b. Limb Dominance 3

c. Surface EMG Set-up 3

d. Isokinetic Strength 4

e. Maximal Voluntary Isometric Contraction 4

f. IMU Set-up 4

g. Walking Task 5

D. Data Processing 5

a. Statistical Analysis 5

E. Results 5

vii a. Medial Compartment 5

b. Lateral Compartment 6

F. Discussion 8

G. Conclusion 11

References 12

Appendices

A. The Problem 17

B. Literature Review 19

C. Additional Methods 26

D. Back Matter 51

E. Bibliography 54

viii List of Tables

Table 1 Physical Characteristics of the Subjects ...... 3

ix List of Figures

Figure 1 Relationship between H:Q strength and co-activation in the medial

compartment...... 6

Figure 2 Co-activation: High versus low strength in the medial compartment...... 7

Figure 3 Individual muscle response of the medial compartment...... 7

Figure 4 Relationship between strength and co-activation in the lateral compartment. ..7

Figure 5 Co-Activation: High versus low strength in the lateral compartment ...... 8

Figure 6 Individual muscle response of the lateral compartment ...... 8

Figure C1 Informed Consent ...... 31

Figure C2 Tegner Activity Scale ...... 37

Figure C3 Marx Activity Scale ...... 37

Figure C4 International Physical Activity Scale ...... 38

Figure C5 Eligibility Checklist ...... 42

Figure C6 Data Collection Form ...... 43

x List of Abbreviations

ACL...... Anterior Cruciate Ligament

EMG ...... Electromyography

H:Q ...... Hamstrings to Quadriceps

IMU ...... Inertial Measurement Units

MVIC ...... Maximal Voluntary Isometric Contraction

xi Chapter One

Manuscript

Introduction

Non-contact anterior cruciate ligament (ACL) injuries account for 70% of all

ACL injuries.1 The most common mechanism of injury occurs in sports that require pivoting, rapid change of direction, as well as frequent single-leg landings.2,3 It is important to recognize that females with muscular imbalances are more likely to suffer from any lower extremity injury.4 Also, female athletes are also four to six times more likely to suffer from a non-contact ACL injury than males.4,5 It has been noted that decreased strength of the quadriceps and hamstring muscles, decreased hamstring stiffness, delayed hamstring activation, decreased joint proprioception and decreased hamstrings to quadriceps (H:Q) strength ratio are all neuromuscular factors that have been identified to place females at increased risk of ACL injury.6-9

The most commonly reported strength ratio of the muscles of the knee is concentric hamstring-quadriceps ratio.10 H:Q ratios of 0.6 and greater have been reported to decrease the risk of hamstring and ACL injuries,11 where ratios closer to 1 indicate high activation of the hamstring muscles.12 However, H:Q ratio is dependent on many different factors including angular velocity, test position, population group and use of gravity compensation each one of these factors can change the results of the study.10 Isokinetic strength testing at an angular velocity of 60°/s is the most commonly reported parameter to establish H:Q strength. The average

H:Q strength ratio for females at an angular velocity of 60°/s has been reported as 0.53.13

Activation of the hamstrings during functional tasks such as running and jumping can reduce anterior tibial translation and decrease strain on the ACL. 14-16

1 Unbalanced co-activation of the hamstrings and quadriceps place females at increased risk for lower extremity injury.17,18 Co-activation is reported as the simultaneous activity of muscles acting around a joint.8 Co-activation of the hamstrings and quadriceps help assist the static stabilizers as well as helps balance the surface pressure on articular surfaces of the knee joint.19 Increased co-activation is essential in early ACL reconstruction rehabilitation to help reduce strain on the new ACL graft, to allow for graft healing.

Strength, recruitment and co-activation of the quadriceps and hamstring are vital components of successful stabilization and protection of the knee joint.20,21 However, increased co-activation could potentially have a negative long term effect on the knee joint.

Increased co-activation at the knee joint implies that there is an increase in compressive forces across the joint, which may lead to cartilage loss.22 Previous research has also shown that increased stability due to increased hamstring activity, can cause accelerated joint degeneration at the knee.23

To date there are no studies looking at the relationship between muscle imbalance and co-activation at the knee. Therefore the purpose of this study is to look at the relationship between hamstring to quadriceps coactivation relative to hamstring and quadriceps strength. We hypothesize that low H:Q strength ratio will have higher co-activation.

Methods

Design. We used a descriptive laboratory study with independent variable of hamstrings to quadriceps ratio, broken down into high hamstrings to quadriceps strength

(≥ 0.53) and low hamstrings to quadriceps strength (≤ 0.52). The dependent variable was co-activation of the hamstrings and quadriceps in the medial compartment (vastus medialis and semitendinosus) and lateral compartment (vastus lateralis and biceps femoris).

2 Participants. 10 healthy and active females volunteered to participate in this study (Table 1). The inclusion criteria were no history of lower extremity injuries within the last 12 months, no history of lower extremity surgery, physically active female defined as ≥ 5 on the Tegner Activity Scale. Written informed consent was obtained for all subjects in accordance with the requirements of the Biomedical Institutional Review

Board.

Table 1. Physical Characteristics of the Subjects

Characteristic Mean ± SD Age (y) 22.40 ± 1.17 Mass (kg) 69.86 ± 6.64 Height (cm) 168.50 ± 5.06 Tegner Activity Scale 5.40 ± 0.70

Procedures

Patient Reported Outcomes. Participants completed subjective questionnaires in a quiet room. Questionnaires included region-specific subjective function and physical activity level. The order of questionnaires was as follows, (1)International Knee

Documentation Committee (IKDC) Subjective Knee Evaluation, (2) Marx activity scale,

(3)Tegner activity scale, (4) International physical activity questionnaire (IPAQ).

Limb Dominance. Participants were asked to identify their dominant limb by answering the question, “which leg would they kick a ball with”. Limb dominance was recorded and used for all testing procedures.

Surface EMG Set-Up. Participants were asked to lie on a padded treatment plinth. The skin over 4 muscles (vastus lateralis, vastus medialis, biceps femoris, semitendinosus) was shaved, cleansed, and debrided. To assess muscle activity, one

3 disposable dual Ag-AgCl wireless surface EMG electrode was placed on each muscle listed above according to standard guidelines. After placement, the wireless transducers were secured to the skin with Cover-Roll to prevent any displacement during activity.

Isokinetic Strength. Isokinetic knee extension/flexion contractions were assessed during five repetitions at 60˚/second using a multimodal dynamometer (System 4, Biodex

Medical Systems, Inc.). An explanation of testing was provided, instructing participants to “kick out and pull back as hard and as fast as possible.” Following a brief period of familiarization, isokinetic peak torque (Nm/kg) was recorded and normalized to body mass.

Maximal Voluntary Isometric Contraction (MVIC). Isometric knee extension/flexion contractions were assessed during three maximal effort contractions.

Participants were seated upright in the dynamometer (as described above) with the knee flexed to 60˚. An explanation of testing was provided, instructing participants to “kick out as hard and as fast as possible for five seconds” (quadriceps) and to “pull back as hard and as fast as possible for five seconds” (hamstrings). Patients were allowed a progressive contraction warm-up of 25%, 50%, 75% and 100% of their MVIC, before completing testing. Isometric average peak torque, and EMG amplitude (muscle activity) were recorded.

IMU Set up. Small sensors (IMUs) were placed in flexible straps, and secured to participants’ upper thoracic (C7), lower thoracic(T12), pelvis, dominant thigh and shank, and bilateral feet. Participants were asked to stand still and upright during sensor calibration.

4 Walking Task. Participants were asked to walk at three miles per hour for four minutes on a treadmill (NordicTrack). Participants were instructed to “walk with their normal gait”. Participants were given a three-minute warm-up at three miles per hour. At the end of the warm up patients were asked to rate their rate of perceived exertion. EMG and IMU data were collected in the last minute of the trial. A small sensor was placed on participants’ shoes to synchronize EMG and IMU data.

Data Processing

EMG signals were band-pass filtered (20-500 Hz) and smoothed. For each MVIC trial, a two second epoch in the middle of each trial was visualized and recorded. EMG was then reduced to the gait cycle from initial toe-off, resulting in filtered EMG signals during the gait cycle averaged of 15-20 strides. Task EMG was normalized to MVIC

EMG (%MVIC). Co-activation ratios were calculated by dividing %MVIC the antagonist muscle by the antagonist muscle. The fist 15% of the gait cycle was then averaged to represent loading response, resulting in average co-activation of the loading response.

Statistical Analysis. Correlation coefficients was used to assess the relationship between H:Q strength ratios and co-activation of the medial (vastus medialis and semitendinosus) and lateral (vastus lateralis and biceps femoris) compartments.

Independent t-tests were used to compare levels of co-activation between individuals with high and low H:Q strength ratios. Effect sizes were calculated with 95% confidence intervals to determine the magnitude of between-group differences.

Results

Medial Compartment. There was no relationship between H:Q strength and co- activation in the medial compartment(r=0.449, p=0.239)(Figure 1). There was no

5 significant difference between groups (p=0.373, d= .0.64, 95% CI[-0.70, 1.99]) when further broken down with known values of high H:Q strength(≥ 0.53) and low H:Q strength(≤0.52) were compared to co-activation (Figure 2). There was a quadriceps mean difference of -9% MVIC and a hamstring mean difference of -12% MVIC was found in the medial compartment when low H:Q strength was compared to high H:Q strength

(Figure 3).

Lateral Compartment. It was found that there was a significant moderate correlation between H:Q strength and co-activation in the lateral compartment (r= 0.663, p=0.052)(Figure 4). When broken down between high H:Q strength and low H:Q strength, the low H:Q strength group had higher co-activation when compared to the high

H:Q strength group (p=0.034).(Figure 5). A large magnitude of difference (d= -1.81,

95%CI [-3.37, -0.25] was also found between low H:Q strength and co-activation on the lateral side (Figure 5). A quadriceps mean difference of -9% MVIC and hamstring mean difference of 3% MVIC, was found in the lateral compartment when low H:Q strength was compared to high H:Q strength (Figure 6).

Figure 1. Relationship between H:Q strength and co-activation in the medial compartment. Data above the horizontal black line indicates hamstring dominance, data bellow the black dashed line indicates quadriceps dominance. Participants with low H:Q strength had low co-activation in the medial compartment (r= 0.441, p=0.239).

6

Figure 2. Co-activation: High versus low strength in the medial compartment. Breakdown between high H:Q strength (≥ 0.53) and low H:Q strength (≤ 0.52). Individuals closer to 1 have a more balanced H:Q strength ratio. There was no significant difference between low H:Q strength and high H:Q strength (p=0.373).

Figure 3. Individual muscle response of the medial compartment. Low and high H:Q broken down by individual muscle, vastus medialis (quadriceps) and semitendinosus (hamstring). There is a mean difference of -9% MVIC of the quadriceps and a mean difference of -12% MVIC of the hamstrings between low H:Q strength and high H:Q strength.

Figure 4. Relationship between strength and co-activation in the lateral compartment. Data above the horizontal black line indicates hamstring dominance, data bellow the black line indicates quadriceps dominance. Participants with low H:Q strength had high co-activation in the lateral compartment (r=0.663, p=0.052).

7

Figure 5. Co-activation: High versus low strength in the lateral compartment. Breakdown between high H:Q strength (≥ 0.53) and low H:Q strength (≤ 0.52). Individuals closer to 1 have a more balanced H:Q strength ratio. There was a significant difference between low H:Q strength and high H:Q strength (p=0.034).

Figure 6. Individual muscle response og the lateral compartment. Low and high H:Q broken down by individual muscle, vastus lateralis (quadriceps) and biceps femoris (hamstring). There is a mean difference of -9% MVIC of the quadriceps and a mean difference of 3% MVIC of the hamstrings between low H:Q strength and high H:Q strength.

Discussion

Healthy females with a lower H:Q strength ratio have higher co-activation in the lateral compartment. In contrast there was no relationship between strength imbalance and co-activation in the medial compartment. Our results show that in the lateral compartment, participants with low H:Q strength had higher co-activation than in the high H:Q strength group. This difference was statistically significant (p=0.034), suggesting that individuals with decreased H:Q strength increase co-activation. When this

8 relationship was further broken down between individual muscle response between high and low H:Q strength in the lateral compartment, there was a mean difference of -9%

MVIC for the quadriceps (vastus lateralis) and a mean difference of 3% MVIC for the hamstrings (biceps femoris). This increase in lateral hamstring activity suggests that the lateral hamstring (bicep femoris) is adapting to increase co-activation. Our findings support our hypothesis that low hamstring to quadriceps strength ratio will have higer co- activation, however this was only observed in the lateral compartment.

Our findings of increased lateral compartment co-activation, is in agreement with a similar findings, that state, females primarily activate the lateral quadriceps and hamstrings during a as well as when landing from a jump.8 Our study found that females primarily activate the lateral hamstrings and quadriceps during a low impact task such as walking. This finding could be explained by a previous study that investigated the effects of lower limb to-in and toe-out walking, which stated there was higher activation of the lateral compartment with a toe-out walking pattern, when compared to toe-in walking.24 Although we did not investigate the relationship between muscle activity and gait biomechanics, it is possible that ncreased external rotation at the shank caused by toe-out walking, could cause increase muscle activity of the biceps femoris. Our finding of decreased medial compartment co-activation, are similar to those previous studies that found that females who have an increase in lateral hamstrings and quadriceps activation and a decrease in medial hamstrings and quadriceps may lead to an increase in knee valgus.25,26 There is also suggestion from previous studies that females who show an unbalance or lower medial to lateral co-activation ratio could lose the ability to control the excessive knee abduction force and anterior shear force.27-30 This decrease in medial

9 thigh muscle activation could be linked to the increase in ACL injuries in females.17,25,31

Although we did not look at the relationship between genders, our findings in females are consistent with previous research stating that females have an increase in lateral thigh muscle activity and a decrease in medial thigh activity.8

We found that there is an increase in co-activation in the lateral compartment, this finding suggest that an increase in co-activation is a response to a sense of instability throughout the knee. In a study by Hirokawa et al, they conclude that hamstring co- activation has a significant effect on maintaining knee joint stability, by working together with the ACL to prevent excessive anterior displacement and internal rotation of the .14 However, the hamstrings appear to be effective in reducing shear forces only when the knee is flexed more than 15-22°.32 It has also been found in previous studies, that in ACL deficient groups there is an increase in hamstring co-activation.33-35 Alkjaer et al. found that co-activation of the hamstrings significantly increases in the ACL deficient population.33 This is suggestive of the hamstrings compensating in order to counteract the shear forces as well as perceived instability at the knee joint.

However, increased co-activation increases compressive forces across the joints, which may in turn, lead to cartilage loss.22 It is also suggested that, the mechanism of increased stability due to increased hamstring activity, has the potential for accelerated joint degeneration.23 Also, there is a significant increase in co-activation in the ACL deficient population.33 Increased co-activation during early ACL reconstruction rehabilitation, helps minimize strain on the ACL, however long-term co-activation could potentially place the knee at increased risk of knee joint degeneration. Our results show an increase in co-activation in the lateral compartment in healthy females during a simple

10 walking task, something that individuals do thousands of times a day. This increase in lateral compartment co-activation could place these individuals at increased risk of early knee joint degeneration.

Limitations of this study was there was a small sample size of only ten participants and we only looked at the relationship in females and not between genders.

This study also only looked at the relationship in the dominant limb and it is possible that there is a larger relationship in the participants non-dominant limb.

Conclusion

Our results indicate that lower hamstrings to quadriceps strength is associated with higher hamstring to quadriceps-coactivation in the lateral compartment during the loading response of walking.

11 References

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16 Appendix A

The Problem

There are approximately 200,000 Anterior cruciate ligament (ACL) injuries that occur per year in the United States.1 Low hamstrings to quadriceps ratio is a neuromuscular factor that has been identified to place females at an increased risk of ACL injury. 2-5 H:Q ratio is the most commonly reported strength ratio of the muscles of the knee,6 injury prevention by detection of muscle imbalances should be based off a minimum H:Q ratio of 0.60 at an angular velocity of 60°/s. 7 Activation of the hamstrings is important during functional tasks such as during running and jumping to help reduce anterior tibial translation and decrease strain on the ACL.8-10 Co-activation of the hamstrings help assist the static stabilizers of the knee joint.11-13 However, there is little evidence on the influence of H:Q strength ratio on co-activation of the hamstrings. Therefore, the purpose of this study is to examine the relationship between isokinetic hamstrings to quadriceps ratio and hamstrings to quadriceps co-activation during walking gait.

Research Question

• Does quadriceps to hamstring co-activation in healthy individuals differ between good and bad hamstring strength? • Does having weak hamstrings (as defined by H:Q ratio) lead to higher co- activation?

Experimental Hypotheses

• Higher co-activation of the hamstring and quadriceps muscles will increase knee joint loading. • Low H:Q strength ratio will have higher co-activation

Assumptions

• Subjects will provide maximum effort when performing the drop landing • Subjects will walk with a normal gait cycle

17 • Subjects will provide maximum effort when performing an isometric strength test • EMG placement will be normalized between each patient • EMG activity is representative of the whole muscle activity • Co-activation is proportional to joint loading

Delimitations

• The subject population was limited to physically active women individuals between the ages of 18 and 35 • The subject population was limited to individuals with no previous history of lower extremity injury

Limitations

• Small sample size of only 10 female participants • Outliers had to be removed for data analysis • Only examined the relationship between H:Q strength and co-activation of the dominant limb Operational Definitions • Co-activation- The simultaneous activity of the muscles acting around a joint.4 o Medial Co-activation: The simultaneous activity of the vastus medialis and semitendinosus. o Lateral Co-activation: The simultaneous activity of the vastus lateralis and biceps femoris. • Electromyography (EMG) Normalization (% MVIC) –EMG envelope from the task under investigation divided by a discrete value (mean or maximum) from a reference contraction of the same muscle.14 • Hamstrings: Quadriceps (H:Q) ratio – Hamstring peak torque at 60°/s divided by quadriceps peak isokinetic torque at 60°/s.15 Significance of the Study The significance of this study is that if hamstring weakness is associated with an increase in co-activation, we can infer that increased co-activation influences increased knee joint loading. If an increase in co-activation is present in healthy females while walking, something that is completed thousands of times a day, it would implicate the need for isolated hamstring strengthening in females.

18 Appendix B

Literature Review

What is the epidemiology of anterior cruciate ligament rupture?

There are an estimated 80,00 to 100,00 anterior cruciate ligament (ACL) repairs in the United States each year.1,2 Overall, high school athletes have lower rate of ACL injuries than do college athletes (5.5 vs 15 per 100,000 athlete exposures), but a similar injury distribution across sports.3 Most ACL injuries occur in persons in their late teens and early twenties, however the separation in ACL injuries by sex is apparent immediately after the beginning of puberty, with a disproportionate increase in females.4

Female athletes between the ages of 15 and 20 year of age account for the largest numbers of reported ACL injuries.5 At the high school level, ACL injury rates in gender- comparable sports are 2.5 to 6.2 times higher in girls compared with boys.5,6 In college athletics, ACL injury rates are 2.4 to 4.1 times higher for women, and at the professional level, ACL injury rates for men and women are essentially equal.5,7,8

The general indications for anterior cruciate ligament reconstruction (ACLR) include the patients inability to participate in sport, instability that affects activities of daily living, and or associated repairable meniscal tear or a knee injury with multiple torn ligaments.9 graft has been used as the gold standard in ACL reconstruction, however over the last decade the use of the hamstring graft has increased.10 Systematic reviews show that there is no evidence to indicate that one graft type is better than the other regarding knee stability, pain, range of motion, activity level or patient-reported function after surgical reconstruction.10-12

19 What is the relationship between hamstring and quadriceps strength as a risk factor for ACL injury?

The role of the hamstring muscles during is to assist the ACL in preventing anterior tibial drawer force by increasing the posterior pull, increasing joint stiffness, and reducing anterior laxity force during quadriceps loading.13-15 This helps in preventing overextension, decelerates the prior to full extension and stabilizes the knee joint throughout the range of motion.15 Muscle strength, recruitment, and co-activation of the hamstring and quadriceps may be critical to the stabilization of the joint, as well as protecting the ACL from rupture.16 Imbalances in hamstring to quadriceps strength and bilateral hamstring strength correlate to greater incidence of lower extremity injury in female collegiate athletes.17 Hamstring muscle force production when compared to the quadriceps is thought to be a stronger predictor of lower limb injuries, including hamstring and ACL injury. 15,18-20 It has been noted that decreased strength of the quadriceps and hamstring muscles, decreased hamstring stiffness, delayed hamstring activation, decreased joint proprioception and decreased hamstring to quadriceps ratio

(H:Q) are all neuromuscular factors that have been identified to place females at increased risk of ACL injury. 21-24 Harput et al.21 found that females primarily activate the lateral quadriceps and hamstrings while also showing less medial thigh and hamstring muscle activation during a squat as well as when landing from a jump. Females are often found to be quadriceps dominate indicating that females preferentially activate their quadriceps over their hamstrings during functional movements, placing them at increased risk for injury.25

How is hamstring to quadriceps ratio quantified?

20 Traditional Method

The hamstring to quadriceps ratio is currently ranked as one of the five most common tests performed to quantify injury risk.20,26 The most frequently reported strength ratio of the knee has been the concentric hamstring to quadriceps ratio

(Hcon/Qcon).27 The conventional hamstring to quadriceps ratio, is an outcome derived from a test usually performed using slow velocity, alternating knee extension and flexion concentric contractions.27,28

Functional Method

In order to accurately assess the balancing nature of the hamstrings about the knee joint the hamstring to quadriceps ratio should be described either as an Hecc/Qcon ratio representing knee extension or an Hcon/Qecc ratio representing knee flextion.27 The functional ratio (H/Qfun) (eccentric hamstrings/concentric quadriceps) has been proposed to appropriately reflect co-contraction of the limb.29-33 Peak torque values for the hamstring and quadriceps during concentric and eccentric muscle actions occur during the mid-range of the movement.29-33 Hiemstra reported that the peak moments generated by the knee extensors and flexors occur at around 60˚ and 20˚ of knee flexion respectively33. In a study completed by Lee et al. 34 isokinetic knee extension/flexion was measured with each subject seated on a dynamometer with their trunk perpendicular to the floor, were flexed at 90 degrees, and the knee was flexed to 90 degrees34. Each patient completed five isokinetic extension flexion repetitions for each leg at 60 degrees/sec, with a rest time of 30 seconds between tests.

What is the relative hamstring to quadriceps ratio?

There is little consensus of a normative value for conventional hamstring to quadriceps ratio, however it appears that 0.6 has gained a general acceptance.27 Absolute knee flexion force

21 should exceed knee flexion force by a magnitude of 3:2 i.e. Hcon/Qcon of 0.66.27 A normal

Hcon/Qcon ratio of 0.6 is frequently used as an injury prevention and rehabilitation tool.18,35

Heiser et al.36 stated that injury prevention by detection of muscle imbalances should be based on a minimum Hcon/Qcon ratio of 0.6 at an angular velocity of 1.05 rad.s-1. Higher H:Q ratio would represent greater muscular balance.27 Donne et al.37 reported an average Hecc/Qcon moment ratio throughout the range of motion of 0.63. An Hecc/Qcon ratio of 1.0 indicated that the eccentrically acting hamstrings are able to fully break the action of the concentrically contracting quadriceps.27

What are the limitations of the hamstring to quadriceps ratio?

There are two major limitations when using peak moment ratios to describe normal knee function. First, the concentric quadriceps moment is normally compared with the concentric hamstring moment, this situation does not arise during functional movement.27 Secondly, they are normally cited irrespective of the joint angle at which they occur, which ignores the effect of muscle length.27 H:Q ratio is dependent on many different factors including angular velocity, test position, population group and use of gravity compensation, each one of these factors can change the result of the study.27 By failing to take into account the angle at which the moment is produced, inaccurate conclusions may arise regarding the normal functioning of the muscle at joint angles other than that at which the observation occurs.38 Assessing the muscle balance is considered important, but independently, the peak moment ratios and angle specific moment curves provide only a limited amount of information.27 Evaluation of isokinetic eccentric antagonist strength relative to concentric strength may provide a relationship of value in describing the maximal potential of the antagonist muscle group.27

What is the influence of injury on hamstring to quadriceps ratio?

22 Weakness of the knee extensor muscles after ACL reconstruction with patella tendon graft, and in the knee flexor muscles after reconstruction with a hamstring tendon graft has been observed up to twenty-four months.39 Ageberg et al.40 reported that subjects in the hamstring tendon graft group had 15% lower hamstring muscle power in their injured leg than the subjects in the patella tendon graft group. Ageberg et al.40 also reported that pateints with a hamstring tendon graft had an 11% decrease in isokinetic knee flexion. Due to the fact that the hamstring muscles are ACL agonists, recovery of the hamstring muscle strength is of importance after ACL reconstruction, and it may be argued that this is of particular importance after reconstruction with the hamstring tendon graft.40

What is the relationship between hamstring to quadriceps co-activation and knee joint loading?

Quadriceps and hamstring muscles, along with the gastrocnemii, are the largest contributors to articular loading at the knee during walking, and the impact the distribution of loads across the knee.41-45 Due to the fact that the quadriceps and hamstrings muscles influence loading patterns at the knee during walking, they would be related to knee cartilage health.46 External knee adduction moment is associated with greater load over the medial knee compartment41,47 and an increased risk of medial cartilage and meniscus damage, and may lead to medial knee osteoarthritis. 48-50 Greater quadriceps strength has been shown to be related to faster walking speed, which leads to higher knee adduction moment. 51-54 Larger quadriceps relative to hamstrings and larger medial quadriceps relative to lateral quadriceps are associated with greater fontal plane

23 loading.46 Higher frontal plane loading is known to be associated with onset and progression of knee osteoarthritis.50,55

Conclusion

There are an estimated 80,00 to 100,00 anterior cruciate ligament (ACL) repairs in the United States each year.1,2 Female athletes between the ages of 15 and 20 year of age account for the largest numbers of reported ACL injuries.5 The hamstring muscles play an important role during leg extension is to assist the ACL in preventing anterior tibial drawer force by increasing the posterior pull, increasing joint stiffness, and reducing anterior laxity force during quadriceps loading.13-15 Helping in prevention of overextension, decelerates the prior to full extension and stabilizes the knee joint throughout the range of motion.15 It has been noted that decreased strength of the quadriceps and hamstring muscles, decreased hamstring stiffness, delayed hamstring activation, decreased joint proprioception and decreased hamstring to quadriceps ratio

(H:Q) are all neuromuscular factors that have been identified to place females at increased risk of ACL injury. 21-24

The hamstring to quadriceps ratio is currently ranked as one of the five most common tests performed to quantify injury risk.20,26 Assessing the muscle balance is considered important, but independently, the peak moment ratios and angle specific moment curves provide only a limited amount of information.27 Evaluation of isokinetic eccentric antagonist strength relative to concentric strength may provide a relationship of value in describing the maximal potential of the antagonist muscle group.27

There is some evidence that suggest that Quadriceps and hamstring muscles, along with the gastrocnemii, are the largest contributors to articular loading at the knee during

24 walking, and the impact the distribution of loads across the knee.41-45 However, there is not much research to support that increased co-activation decreases sheer stress at the knee, and increases compressive stress. Much of the literature looks at the impacts of walking on joint loading at the knee but neglects the research on sheer forces at the knee and how they relate to articular cartilage breakdown.

25 Appendix C

Additional Methods

Executive Summary Motion Analysis & Integrative Neurophysiology Laboratory University of Toledo Title: The Relationship Between Hamstring Strength and Agonist-Antagonist Co- activation

Principal Investigator: Grant Norte, PhD, AT, ATC, CSCS, Assistant Professor

Research Team: Meghan Gregoire, AT, ATC

Neal Glaviano, PhD, AT, ATC

Amanda Murray, PT, DPT, PhD

Lucinda Bouillon, PT, DPT, PhD

Purpose: The purpose of this study was to examine the relationship between isokinetic hamstrings to quadriceps ratio and hamstrings to quadriceps co-activation during walking gait.

Participants: Healthy active female between the ages of 18-35 with no previous history of lower extremity surgery or injury within 12 months.

Inclusion Criteria:

• Females

• Physically active (≥ 5 on Tegner scale)

• Age 18-40

Exclusion Criteria:

• Previous lower extremity injury within 12 months

• Previous history of lower extremity surgery

26 Study Design: Descriptive Laboratory Study

Independent Variables:

• Hamstring to Quadriceps ratio

o High (≥ 0.53)

o Low (≤ 0.52)

Dependent Variables:

• Co-Activation

o Medial: Normalized medial hamstring EMG amplitude (% MVIC) divided

by normalized medial quadriceps EMG amplitude

o Lateral: Normalized lateral hamstring EMG amplitude (% MVIC) divided

by normalized lateral quadriceps EMG amplitude

Procedures: List of primary procedures in chronological order

• EMG set up

o Shave, debride, clean

o Vastus Lateralis

▪ 2/3 on the line of ASIS to lateral patella

o Rectus Femoris

▪ 50% from ASIS to superior patella

o Vastus Medialis

▪ 80% between ASIS and joint space in front of the anterior boarder

of medial ligament.

o Biceps Femoris

▪ 50% between and lateral epicondyle

27 o Semitendinosus

▪ 50% between ischial tuberosity and medial epicondyle

• Isokinetic strength at 60˚/sec (to quantify H:Q ratio)

• MVIC testing

o Quadriceps, 3 maximum effort contractions with a 5 second hold

o Hamstrings, 3 maximum effort contractions with a 5 second hold

• IMU set up

o Upper thoracic, lower thoracic, pelvis, dominant limb thigh and shank,

bilateral feet

• IMU calibration

• Walking trials

o 3 mph

o 3 minute warm up

o 1 minute of data collection

IRB Protocol:

Self-Reported Outcome Questionnaires: Participants will complete subjective questionnaires in a quiet room. Questionnaires will include region-specific subjective function and physical activity level. The order of questionnaires is included below: 1.

International Knee Documentation Committee (IKDC) Subjective Knee Evaluation 2.

Marx activity scale 3. Tegner activity scale 4. International physical activity questionnaire (IPAQ)

Estimated time: 5 minutes.

28 Isokinetic Strength: Isokinetic knee extension/flexion contractions will be assessed during five repetitions at 60˚/second using a multimodal dynamometer (System 4, Biodex

Medical Systems, Inc.). An explanation of testing will be provided, instructing participants to “kick out and pull back as hard and as fast as possible.” Isokinetic peak torque will be recorded .Following a brief period of familiarization, isokinetic peak torque (Nm/kg) will be recorded and normalized to body mass.

Estimated Time: 5 minutes.

EMG Preparation: Participants will be asked to lie on a padded treatment plinth. The skin over 6 muscles (vastus lateralis, vastus medialis, biceps femoris, semitendinosus, medial gastrocnemius, and lateral gastrocnemius) will be shaved, cleansed, and debrided.

To assess muscle activity, one disposable Ag-AgCl wireless surface EMG electrode will be placed on each muscle listed above according to standard guidelines.

Estimated Time: 10 minutes

Isometric Strength: Isometric knee extension/flexion contractions will be assessed during three maximal effort contractions. Participants will be seated upright in the dynamometer (as described above) with the knee flexed to 60˚. An explanation of testing will be provided, instructing participants to “kick out as hard and as fast as possible for five seconds” (quadriceps) and to “pull back as hard and as fast as possible for five seconds” (hamstrings). Isometric average peak torque, and EMG amplitude (muscle activity) will be recorded.

Estimated Time: 10 minutes.

29 IMU Placement: Small sensors (IMUs) will be placed in flexible straps, and secured to participants’ feet, legs, , and waist. Participants will be asked to stand still and upright during sensor calibration.

Estimated time: 5 minutes.

Functional Task Progression: EMG and IMU data will be collected during five functional tasks (walking, jogging, double-leg landing, single-leg landing, and single-leg hopping).

Participants will complete walking (5 minutes @ 3 miles per hour) and jogging (5 minutes @ 6 miles per hour) trials on a treadmill (NordicTrack) while wearing standardized shoes (Asics gel-contend 3 running shoe). A small sensor will be placed on participants’ shoes to synchronize EMG and IMU data. Next, participants will perform three double-leg and single-leg landing trials from a 30 centimeter high platform. Finally, participants will perform three single-leg hop for distance trials on a flat surface.

Estimated Time: 20 minutes.

Statistical Analysis:

1. Assess the relationship between H:Q strength ratio and hamstrings to quadriceps

co-activation during walking for the medial and lateral compartments (Pearson’s r

Correlation Coefficients)

2. Compare H:Q strength ratio between high and low groups (Independent T-test)

Research Hypothesis:

1. Hamstring-to-quadriceps co-activation will be higher in females with low H:Q

ratio

30

Figure C1. Informed consent

31

32

33

34

35

36

Figure C2. Tegner Activity Scale.

Figure C3. Marx Activity Scale.

37

Figure C4. International Physical Activity Scale

38

39

40

41

Figure C5. Eligibility Checklist

42

Figure C6. Data Collection Form.

43 Order of Operation

1. Consent

2. Eligibility

3. Patient biometrics (age, height, weight, dominant limb)

4. EMG electrode placement

a. Shave, clean and debride each EMG location i. Vastus Lateralis (EMG 1) 1. Electrode Placement: a. 2/3 on the line of ASIS to lateral patella 2. Transmitter Placement: a. ii. Vastus Medialis (EMG 2) 1. Electrode Placement: a. 80% between ASIS and joint space in front of the anterior boarder of medial ligament. 2. Transmitter Placement: a. iii. Biceps Femoris (EMG 3) 1. Electrode Placement: a. 50% between ischial tuberosity and lateral epicondyle 2. Transmitter Placement: a. iv. Semitendinosus (EMG 4) 1. Electrode Placement: a. 50% between ischial tuberosity and medial epicondyle 2. Transmitter Placement: a. v. Gastrocnemius Lateralis (EMG 5) 1. Electrode Placement: a. 1/3 the line between the head of the and the heel 2. Transmitter Placement: a. vi. Gastrocnemius Medialis (EMG 6) 1. Electrode Placement a. Most prominent bulge of the muscle 2. Transmitter Placement: a. b. Place double sided tape on the back of all sensors c. Place a strip of cover roll over all transmitters in a quarter squat position

44 i. Don’t cover EMG electrodes or connecting wires 5. Biodex Set up

a. Click Biodex software, initialize if prompted

b. Make sure the black pad is placed on the chair, accommodate EMG placement to

fit in cutouts

c. Place subject in the chair, make sure they are sitting up straight and all the way

back

d. Adjust head rest

e. Line lateral epicondyle to the axis of rotation

f. Secure leg pad 2 finger breaths above malleoli

g. Place strap over lap and shoulders

6. Noraxon Software

a. Log into computer

b. MR3

i. Change subject name

ii. Choose configuration in myomuscle dependent on limb

iii. Click Measure

7. Nondominant isokinetic peak torque

a. Patient

i. Label each patient

ii. Add patient test limb

iii. Add patient weight

iv. Add patient involved limb (none)

b. Protocol

i. Identify test limb

ii. Clear limits

45 1. Kick all the way out

a. Set limit

2. Kick all the way back

a. Set limit

iii. Calibrate position at 90°

iv. Set limb weight at 30˚

1. Instruct patient to completely relax

c. Give the patient a warm-up period, when they are ready, have them stay

completely still

d. 5 trials at 60°/s

e. Instruct patient to “pull back and kick out as hard and as fast as you can”

i. Verbal encouragement is also given during testing

8. Nondominant Isometric Testing in Biodex

a. 60˚ knee flexion

b. VMO & VL

i. 3 trials of knee extension, 30 second break (if they need more OK)

ii. Instruct patient to “Kick out as hard and as fast as they can”

iii. Save after all trials are complete

c. BF & ST

i. 3 trials of knee flexion, 30 second break (if they need more OK)

ii. Instruct patient to “Pull back as hard and as fast as they can”

iii. Save after the trials are completed

9. Dominant Limb isokinetic peak torque

a. Patient

i. Label each patient

ii. Add patient test limb

46 iii. Add patient weight

iv. Add patient involved limb (none)

b. Protocol

i. Identify test limb

ii. Clear limits

1. Kick all the way out

a. Set limit

2. Kick all the way back

a. Set limit

iii. Calibrate position at 90°

iv. Set limb weight at 30˚

1. Instruct patient to completely relax

c. Give the patient a warm-up period, when they are ready, have them stay

completely still

d. After practice trails, hit record on noraxon software

i. Spot check signal!

e. 5 trials at 60°/s

f. Instruct the patient to “Pull back and kick out as hard and as fast as you can”

i. Verbal encouragement is also given during testing

g. Hit stop on noraxon and bidoex software

10. Dominant Isometric Testing in Biodex

a. 60˚ knee flexion

b. VMO & VL

i. 3 trials of knee extension, 30 second break (if they need more OK)

1. Make sure to spot check signal

ii. Instruct patient to “Kick out as hard and as fast as they can”

47 iii. Hit record on biodex and noraxon software

iv. Hit stop

v. Safe after all trials are complete

c. BF & ST

i. 3 trials of knee flexion, 30 second break (if they need more OK)

1. Make sure to spot check signal

ii. Instruct patient to “Pull back as hard and as fast as they can”

iii. Hit record on biodex and noraxon software

iv. Hit stop

v. Save after the trials are completed

11. IMU set up

a. Secure with straps

i. Lower Thoracic

1. T12

ii. Pelvis

1. Over Sacrum

iii. Thigh

1. Mid-thigh

iv. Shank

1. Above medial gastroc sensor

b. Secure with double sided tape and powerflex

i. Upper Thoracic

1. C7

ii. Right

1. On top of laces, X axis down

iii. Left Foot

48 1. On top of laces, X axis down

12. Reflective Marker Placement

a. Secure with double sided tape and cover roll

i. Greater Trochanter

ii. Lateral femoral condyle

iii. Lateral malleolus

13. Computer placement

a. 10 feet from side of the treadmill

i. Make sure to have computer at a 90 degree angle

ii. Make sure you can see writing on the side of the treadmill

14. Noraxon Software

i. Choose configuration in myomotion dependent on limb

ii. Set bone lengths to patients’ height in inches

iii. Click Measure

iv. Click Treadmill Mode

v. Calibration

1. Have patient on standing on a wooden box in a predetermined

area

2. Have subject stand as still as possible in anatomical position

3. All sensors should be white (Not magenta)

vi. Click Calibrate

15. Walking Trials at 3.0 mph

a. 3 minute warm up

i. Ask how everything feels

ii. Get RPE

iii. Spot check EMG & IMU data

49 b. After warm up click record on Noraxon software

i. 1 minute data collection

c. After 1 minute hit stop

d. Save data

16. Dismiss subject

Sample Size Estimation

Pilot data from our lab indicated that a sample of 11 participants in each group

(low strength, high strength) would yield a moderate effect size. To account for a 15% attrition or screen fail rate, we will supplement to n = 25.

50 Appendix D

Back Matter

Recommendations for Future Research

Further research must be conducted to fully understand the relationship between hamstring strength and H:Q ratio. This study only examined the relationship between hamstring strength and H:Q ratio in a healthy female population. Future research should include the addition of males as well as looking at the relationship of co-activation and

H:Q ratio between gender. Future research should also include looking at the relationship between a pathological population (ACL deficient, knee osteoarthritis) and a healthy population.

51 NATA Conference Abstract

Context: Anterior cruciate ligament (ACL) injury is common among females due to several neuromuscular risk factors. Decreased hamstrings to quadriceps (H:Q) ratio is one neuromuscular factor that place females at an increased risk of ACL injury. Increased activation of the hamstrings during functional tasks help assist the static stabilizes of the knee, decrease strain on the ACL and reduce anterior tibial translation. The objective of this study was to (1) identify the relationship between H:Q strength and co-activation ratio in the medial and lateral compartments of the knee during the stance phase of walking gait as well as (2) compare H:Q ratio between high and low groups.

Methods: 10 healthy and active females (age 22.40 ± 1.17 years, mass 69.86 ±

6.64 kg, height 168.50 ± 5.06 cm) particiapated in this descriptive laboratory study.

Isokinetic flexion/extension contractions were assessed during five reputations at 60°/s, isokinetic peak torque (Nm/kg) was recorded and normalized to body mass. Maximal voluntary isokinetic contraction of the knee extensors and flexors were assessed during three maximal effort contractions at a knee joint angle of 60°. Surface electromyography was used to quantify muscle activity of the quadriceps (vastus lateralis and vastus medialis) and hamstrings (semitendinosus and biceps femoris) the mean value of three

MVIC trials were used for the normalization of the EMG data obtained during the walking task. The EMG signals were band-pass filtered (20-500 Hz) and smoothed. Heel strike and toe-off were identified from IMU data, and an average of 10-15 strides were selected for each subject. Correlation coefficients was used to assess the relationship between H:Q strength ratios and co-activation of the medial (vastus medialis and semitendinosus) and lateral (vastus lateralis and biceps femoris) compartments.

52 Independent t-tests were used to compare levels of co-activation between individuals with high and low H:Q strength ratios. Effect sizes will be calculated with 95% confidence intervals to determine the magnitude of between-group differences.

Results: It was found that there was a significant moderate correlation between H:Q strength and co-activation in the lateral compartment (r= 0.663, p=0.052). It was also found that there was a significant difference (p=0.034) between low H:Q strength and co- activation in the lateral compartment. A large magnitude of difference (d= -1.81, 95%CI

[-3.37, -0.25]) was also found between low H:Q strength and co-activation on the lateral side.

Conclusion: Healthy females with a lower H:Q strength ratio have higher co-activation in the lateral compartment. In contrast there was no relationship between strength imbalance and co-activation in the medial compartment

53

Figure 1E. NATA Research Poster

54 Appendix E

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