The Effect of Low Back Pain History on Multifidus Co-Contraction During Common Lumbosacral Voluntary Stabilizing Contractions

The Effect of Low Back Pain History on Multifidus Co-contraction During Common Lumbosacral Voluntary Stabilizing Contractions

Mark P. Wilhelm, PT, DPT

A DISSERTATION

REHABILITATION SCIENCES

Submitted to the Graduate Faculty of Texas Tech University Health Sciences Center in Partial Fulfillment of the Requirements for the Degree of

DOCTOR OF PHILOSOPHY

Phillip S. Sizer Jr., PT, PhD Chair of Committee

Jean-Michel Brismée, PT, ScD C. Roger James, PhD Kerry K. Gilbert, PT, ScD Chad E. Cook, PT, PhD

Lori Rice-Spearman, PhD Dean of the School of Health Professions

May 2019

Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

ACKNOWLEDGMENTS There are many individuals to whom I am very grateful for their patience and assistance along the way. This has been a long process with many challenges along the way and I would not be in the position I am without their support. First and foremost, I thank my wife Karla and daughter Anna for their understanding during my time working late nights and their emotional support and encouraging words throughout the process. I thank my parents who instilled in me a strong work ethic at a young age that allowed me to continue on to complete the PhD program despite multiple hurdles. I also thank all the members of my committee for their assistance. Specifically, I thank my chair, advisor, mentor, and friend Phil Sizer for believing in me and mentoring me throughout the process and helping me become a better researcher, teacher, physical therapist and all- around person. I owe a great thanks to Ken Learman for allowing me to collect data at Youngstown State University and assisting with collecting data on all subjects. Being able to collect data here allowed me to spend more time with my family. Lastly, I thank Troy Hooper for his great assistance with the robust statistical analysis. His assistance allowed me to give the data the necessary scrutiny to answer the research questions.

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TABLE OF CONTENTS ACKNOWLEDGMENTS ...... II

ABSTRACT ...... VII

LIST OF TABLES...... X

LIST OF FIGURES ...... XI

I. INTRODUCTION ...... 1

Statement of the Problem ...... 1

Background and Theory ...... 2

Need for the Study ...... 5

Purpose...... 5

Research Questions ...... 6

Hypotheses ...... 7

II. LITERATURE REVIEW ...... 9

Epidemiology ...... 9

Low Back Pain Definition and Classification ...... 11

Lumbar Stability ...... 12

Stabilizing Systems ...... 13

Trunk Muscle Anatomy ...... 14

Global Muscle Anatomy ...... 16

Local Muscle Anatomy ...... 18

Multifidus Anatomy ...... 21

Muscular Contribution to Stability ...... 23

Stabilization from Global Muscles ...... 24

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Stabilization from Local Muscles ...... 25

Stabilizing Dysfunction ...... 28

Theories of Muscle Dysfunction in LBP ...... 37

Pain-Spasm-Pain Theory ...... 37

Pain Adaptation Theory ...... 38

Activity Redistribution Theory ...... 38

Clinical Spine Stabilization ...... 39

VPAC Disadvantages ...... 42

Co-contraction Evidence ...... 44

III. METHODS ...... 47

Operational Definitions ...... 47

Assumptions ...... 48

Design and Variables ...... 49

Setting ...... 50

Subjects ...... 50

Questionnaires ...... 51

Procedures ...... 53

Preparatory Procedures ...... 53

Testing Procedures ...... 53

Submaximal Reference Standard ...... 57

Co-Contraction Testing ...... 58

Data Reduction ...... 58

Statistical Analysis – Study 1...... 59

Statistical Analysis – Study 2...... 60 iv Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

IV. MULTIFIDUS CO-CONTRACTION DURING VOLITIONAL ABDOMINAL CONTRACTIONS IN HEALTHY INDIVIDUALS WITHOUT A RECENT HISTORY OF LOW BACK PAIN ...... 62

Abstract ...... 62

Introduction ...... 63

Methods ...... 64

Experimental Design ...... 64

Subjects ...... 65

Testing Procedures ...... 66

Data reduction ...... 67

Statistical Analysis ...... 68

Results ...... 68

Discussion ...... 69

Limitations ...... 72

Conclusion ...... 72

References ...... 74

V. MULTIFIDUS CO-CONTRACTION DURING VOLITIONAL ABDOMINAL CONTRACTIONS IN INDIVIDUALS WITH A RECENT HISTORY OF LOW BACK PAIN ...... 82

Abstract ...... 82

Introduction ...... 83

Methods ...... 84

Experimental Design ...... 84

Subjects ...... 85 v Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Testing Procedures ...... 86

Sensor Placement ...... 87

Data Reduction ...... 88

Statistical Analysis ...... 88

Results ...... 89

Discussion ...... 91

Limitations ...... 92

Conclusions ...... 93

References ...... 94

VI. DISCUSSION AND CONCLUSION ...... 104

Discussion ...... 104

Conclusion ...... 109

Limitations of the Study ...... 110

Delimitations of the Study ...... 111

Recommendations for Future Research ...... 112

References ...... 113

APPENDIX A ...... 130

Lumbar Spine Instability Questionnaire ...... 130

APPENDIX B ...... 131

Oswestry Disability Index ...... 131

APPENDIX C ...... 134

Tampa Scale for Kinesiophobia ...... 134

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ABSTRACT Nearly all individuals will experience a low back pain episode within their lifetime. Despite pain remission, individuals who experience one low back pain episode are four times more likely to experience another low back pain episode within the next year. As a result, low back pain is often viewed as a cyclical condition characterized by periodic pain followed by remission. Low back pain has been shown to relate to multifidus morphological and sensorimotor control changes that tend to persist despite pain remission, thus potentially increasing the likelihood of pain reoccurrence. The abdominal drawing in maneuver and abdominal bracing maneuver are two common clinical strategies used to provide spinal protection, improve multifidus morphology, and improve sensorimotor control in hopes to prevent low back pain reoccurrence. Although it was commonly believed that these strategies result in multifidus co-contraction, it was not until Matthijs et al (2014) empirically demonstrated superficial multifidus co- contraction during both abdominal contraction strategies in subjects without low back pain. Since these strategies are commonly used in a clinical population, it is important to identify whether these strategies result in deep and superficial multifidus co-contraction in patients with a history of low back pain as well as healthy controls. Therefore, the purposes of this dissertation were to determine: 1) if deep and superficial multifidus fibers demonstrate different co-contraction patterns during volitional abdominal contractions; 2) the effect of a LBP history on the ability of lumbar stabilizing muscles to co-contract with abdominal muscle activation compared to individuals without a LBP history; and 3) if co-contraction differences exist among abdominal activation strategies and common positions used in clinical practice. Muscular activity was assessed using surface EMG for the internal oblique, external oblique, superficial multifidus, and the longissimus thoracis as well as fine wire EMG for deep multifidus. Subjects were asked to perform abdominal drawing in maneuvers and abdominal bracing maneuvers in a standing and quadruped position. Each condition was repeated three times. Additionally, subjects were asked to perform a quadruped hip extension and hold exercise while holding an abdominal drawing in maneuver for additional data analysis at a later time. Baseline data were compared using a t-test while comparisons between groups, strategies,

vii Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 muscles, and positions were compared using ANOVAs. Post-hoc pairwise comparisons were used to locate significant differences. Study 1 used data from the 30 subjects (18 male and 12 female) between the ages of 18 and 65 (37.8 ± 14.46) years old without a recent history of LBP. Robust ANOVAs were completed to look for interactions and main effects of multifidus depth and abdominal contraction strategy. No significant differences were observed in co- contraction between deep and superficial multifidus fiber depth during any of the three abdominal activation strategies in either standing or quadruped positions. Both ADIM and ABM resulted in greater co-contraction in both the deep and superficial multifidus when compared to the resting condition. No multifidus co-contraction was found between ADIM and ABM. Study 2 use data from 30 subjects with a recent LBP history (36.83 ± 13.79 years of age) and 30 subjects without a recent history of low back pain (37.8 ± 14.46 years of age). Between-group differences in baseline variables were assessed using t-tests. Robust ANOVAs were calculated to identify differences in multifidus co-contraction between groups. Additionally, robust ANOVAs were calculated within the HxLBP group for main effects of multifidus fiber depth, abdominal activation strategy, and position. Interactions within all ANOVAs were also assessed. No significant differences were found between group for the demographic variables of sex, age, height, weight, and BMI. However, the history of LBP group had significantly higher scores for TSK, ODI, and the LSIQ. No significant interactions were identified between any variable combination examined. No difference in multifidus co-contraction was found between the HxLBP group and controls. Within the HxLBP group, inconsistent significant differences between deep and superficial multifidus fiber co-contraction were identified with small effect sizes. Both ADIM and ABM contraction resulted in greater multifidus co-contraction compared to the resting condition while no differences were observed between the ADIM and ABM co-contractions. A significant main effect for position was observed with all three abdominal contraction states resulting in greater multifidus co-contraction while in the standing position compared to the quadruped position.

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These results show the ADIM and ABM contractions do in fact cause multifidus co-contraction. Three possible explanations that may explain why this multifidus co- contraction occurs are: 1) ABM and ADIM contractions include multifidus contraction within the motor program and it is inherently part of the contraction, 2) an anatomical connection between the abdominal muscles and the multifidus muscles requires co- contraction for efficient stabilization, and 3) in order to maintain a static position, forces on each side of the motion segment axis must be balanced. Additionally, this study found that the amount of co-contraction may not be different between the deep and superficial multifidus fibers. The contraction activities in this study were static and may not have challenged individuals to a degree required to observe consistent differences between the superficial and deep multifidus fibers. This study also found that HxLBP subjects experienced similar multifidus co-contraction as control subjects, suggesting that those individuals with a history of LBP can utilize either the ADIM or ABM to stabilize the spine. Lastly, this study found significantly greater multifidus co-contraction during all three abdominal contraction states when in standing compared to the same contraction states in quadruped. This difference could be due to a difference in the direction of gravitational forces acting on the spine combined with the body having contact with the stable both cranial and caudal to the spine. Clinically, this demonstrates that both the ADIM and ABM contraction strategies can be used to stabilize the spine in preparation for a potentially painful functional activity. Furthermore, clinicians interested in educating patients on abdominal contractions to stabilize the spine during these activities can choose either the ADIM or ABM strategies based on which strategy the patient prefers to use.

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LIST OF TABLES Table 3.1. Testing conditions including all position, contraction, and repetition combinations ...... 58 Table 4.1. Contraction RMS values in standing and quadruped positions ...... 78

Table 4.2. ANOVA results in standing position ...... 78

Table 4.3. ANOVA results in quadruped position ...... 79

Table 5.1. Subject characteristics ...... 98

Table 5.2. Multifidus co-contraction RMS values ...... 98

Table 5.3. Group by multifidus depth ANOVA results ...... 99

Table 5.4. Multifidus depth by abdominal contraction strategy ANOVA results in standing position HxLBP group ...... 99 Table 5.5. Multifidus depth by abdominal contraction strategy ANOVA results in quadruped position HxLBP group ...... 100 Table 5.6. Position by multifidus depth ANOVA in HxLBP subjects ...... 100

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LIST OF FIGURES Figure 2.1. Representation of interspinalis and intertransversarii muscles ...... 19

Figure 2.2. Representation of deep multifidus (left fibers) and superficial multifidus (right fibers) ...... 23 Figure 3.1. Dorsal muscle electrode placement. A: Longissimus Thoracis, B: Superficial multifidus, and C: Deep multifidus ...... 56 Figure 4.1. EMG sensor placement for extensor muscles ...... 80

Figure 4.2. Abdominal contraction x multifidus depth interaction in standing ...... 81

Figure 4.3. Abdominal contraction x multifidus depth interaction in quadruped ...... 81

Figure 5.1. Group x multifidus depth main effects and interactions for multifidus co- contraction in A) Quadruped ADIM, B) Quadruped ABM, C) Standing ADIM, and D) Standing ABM ...... 101 Figure 5.2. Multifidus depth x contraction main effects and interactions for multifidus co-contraction in HxLBP subjects. A) Quadruped multifidus depth, B) Quadruped contraction, C) Standing multifidus depth, and D) Standing contraction ...... 102 Figure 5.3. Position x multifidus depth main effects and interactions for multifidus co- contraction in HxLBP subjects during A) ABM, B) ADIM, and C) Rest ...... 103

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CHAPTER I

INTRODUCTION

Statement of the Problem Low back pain (LBP) is a practically universal disorder with 70-85% of all individuals experiencing the condition at some point throughout their lifetime (Andersson, 1999; van Tulder et al., 2006). At any point in time, approximately 30% of all individuals are experiencing LBP (Andersson, 1999; Deyo, Mirza, & Martin, 2006), making it the most common pain experience reported by adults in the United States (Deyo et al., 2006). Overall, LBP is the second leading cause of disability in the United States (CDC, 2001) and the leading cause of activity limitation among adults under 45 years of age (Andersson, 1999). In the Unites States alone, total annual healthcare costs for individuals with back pain have reached more than 90 billion dollars, with over 26 billion being specifically attributed to back pain management (Katz, 2006; Luo, Pietrobon, Sun, Liu, & Hey, 2004). Although LBP affects all individuals differently, approximately 60-70% of back pain sufferers will recover within six weeks and 80-90% will recover within 12 weeks (Andersson, 1999). Despite acute LBP remission, individuals who have experienced LBP are four times more likely to experience LBP recurrence within the following year (Hestbaek et al., 2003). One possible explanation for such high recurrence rates is that underlying changes in morphology and sensorimotor control may persist despite pain resolution (Macdonald, Dawson, & Hodges, 2011; MacDonald, Moseley, & Hodges, 2009; 2010). Lumbar spine sensorimotor control is a complex process, involving numerous muscles and nervous system components. Of these stabilizing muscles, the lumbar multifidus is one of the most important stabilizing muscles (Moseley, Hodges, & Gandevia, 2002; Wilke, Wolf, Claes, Arand, & Wiesend, 1995). The multifidus muscle undergoes morphological and neuromotor changes in many cases of LBP, lending to altered spinal sensorimotor control (Suehiro et al., 2015; Teichtahl et al., 2015; Wallwork, Stanton, Freke, & Hides, 2009). These changes appear to affect the deep multifidus fibers more so than the superficial fibers (Arokoski, Valta, & Airaksinen, 2001; Pool-Goudzwaard, Vleeming, & Stoeckart, 1998). This persistent multifidus 1 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 dysfunction is thought to predispose the lumbar spine to further injury, instability and recurrent pain episodes (Cholewicki et al., 2005; Hides, Jull, & Richardson, 2001). While it has been suggested and generally accepted that abdominal activation results in co- contraction of the multifidus (O'Sullivan, 2000; O'Sullivan, Phyty, Twomey, & Allison, 1997), until recently no evidence existed confirming this co-contraction in healthy subjects (MacDonald, Lorimer Moseley, & Hodges, 2006; Pool-Goudzwaard et al., 1998). More recently, Matthijs et al. (2014) reported superficial multifidus co-contraction with the abdominal bracing maneuver (ABM) and abdominal drawing in maneuvers (ADIM) using surface EMG. This study was the first to observe superficial multifidus co- contraction during volitional abdominal muscle contraction in healthy subjects. However, it cannot be assumed that the deep multifidus fibers follow the same co-contraction pattern, due to different morphology and different muscular responses during perturbations (Macintosh & Bogduk, 1986; Macintosh, Valencia, Bogduk, & Munro, 1986; Moseley et al., 2002; Moseley, Hodges, & Gandevia, 2003). Moreover, while Matthijs et al (2014) provided evidence for multifidus co-contraction during volitional preemptive abdominal contraction (VPAC), this co-contraction was demonstrated in a healthy population without a recent history of LBP. One might suspect that this co- contraction response could be altered during LBP and remain altered even during LBP remission in individuals with a history of LBP. This is supported by Hides et al (2011) who demonstrated that individuals with chronic LBP who exhibited difficulty producing a voluntary transversus abdominis (TrA) contraction experience difficulty in voluntarily contracting the multifidus muscle. It is still unknown if a similar deep multifidus co- contraction pattern will be observed in normal subjects or those who have a history of LBP.

Background and Theory Low back pain often leads to spinal musculature control changes including morphological and histological changes, as well as changes in force production, proprioception, balance, and postural control (Brumagne, Janssens, Knapen, Claeys, & Suuden-Johanson, 2008; Henry, Hitt, Jones, & Bunn, 2006; Learman et al., 2009; Lee, Cholewicki, Reeves, Zazulak, & Mysliwiec, 2010; Navalgund, Buford, Briggs, & Givens,

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2013). These muscular changes can lend the spine to increased injury susceptibility in the presence of LBP. Since the spine is more susceptible to buckling and subsequent pain in the absence of sufficient muscular activity (Cholewicki & McGill, 1996; Crisco, Panjabi, Yamamoto, & Oxland, 1992), persisting dysfunction can contribute to a higher LBP recurrence rate despite pain resolution (Cholewicki et al., 2005; D'hooge et al., 2013; Hides et al., 2001). Agonist and antagonist trunk muscle activity can help to reduce spinal buckling by providing sufficient spinal stability (Kavcic, Grenier, & McGill, 2004; McGill, Grenier, Kavcic, & Cholewicki, 2003). Literature regarding exact muscular response during LBP episodes is inconsistent, demonstrating conflicting conclusions. This has led to multiple theories regarding muscular response during LBP. The three most prevalent theories are the Pain-Spasm-Pain theory (Lund, Donga, & Widmer, 1991), the Pain Adaptation theory (Roland, 1986), and more recently the Activity Redistribution Theory (Hodges & Tucker, 2011). The Pain-Spasm-Pain theory suggests that increased muscular activity in response to pain is dysfunctional and leads to consequential pain (Roland, 1986). The Pain Adaptation Theory on the other hand suggests that during a painful episode, agonist muscular activity will be reduced while antagonist activity will be increased and represents a normal protective mechanism that does not cause pain (Lund et al., 1991). More recently, Hodges & Tucker (2011) proposed the Activity Redistribution theory, which is based on five concepts regarding muscle adaptation to pain with the main idea that muscular adaptations exist to limit pain and protect vulnerable tissue. The multifidus muscle has been suggested to contribute up to 1/3 of spinal stability (Wilke et al., 1995). Superficial multifidus fibers are believed to assist in spinal stability, as well as assisting with lumbar lordosis (MacDonald et al., 2006; Macintosh & Bogduk, 1986) while deep multifidus fibers are better designed to contribute significantly to spinal stability without producing large spinal motions (Macintosh & Bogduk, 1986). The stabilizing role of the multifidus is highlighted by a study by Cholewicki and McGill demonstrating that even in the presence of significant global muscle activity, the spine would buckle if the stabilizing contributions of the multifidus and erector spinae were removed (Cholewicki & McGill, 1996). Given the important role of the lumbar

3 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 multifidus in producing lumbar spinal stability, it is important for the multifidus to demonstrate sufficient and appropriate activity during functional tasks when spinal stability is challenged (Cholewicki & McGill, 1996). However, selected subjects with current LBP may exhibit difficulty with voluntary multifidus contraction (Hides et al., 2011). Therefore, it is essential for these patients to find ways to activate the lumbar multifidus, even if this occurs through co-contraction with abdominal muscle activation. A variety of means have been identified for producing a volitional preemptive abdominal contraction (VPAC). Two prevalent VPAC methods, the abdominal drawing in maneuver (ADIM) and abdominal bracing maneuver (ABM) have been well documented in the literature (Grenier & McGill, 2007; Stanton & Kawchuk, 2008; Vera- Garcia, Elvira, Brown, & McGill, 2007). Many clinicians and researchers use these strategies as exercises to strengthen muscles and restore appropriate motor control parameters both during LBP episodes and during pain remission periods in order to reduce the LBP recurrence chance. Additionally, using either abdominal activation strategy has been shown to improve lumbar spinal stability (Grenier & McGill, 2007; Stanton & Kawchuk, 2008; Stokes, Gardner-Morse, & Henry, 2011). Although the local (deep) abdominal muscles are able to contribute to lumbar stability, one underlying mechanism of these strategies’ benefit is likely achieved through producing lumbar multifidus muscle co-contraction (Matthijs et al., 2014). Different studies serve as context for examining the multifidus co-contraction response to VPAC. Baeck and colleagues observed automatic multifidus activity with neuromuscular electrical stimulation of the TrA (Baek, Cho, et al., 2014b) and automatic TrA activity with multifidus stimulation (Baek, Ahn, et al., 2014a). These findings lend support to the notion that the TrA and multifidus are functionally connected either through an anatomical or neuromotor linkage. Hides et al (2011) demonstrated that chronic LBP patients who experience difficulty producing a voluntarily TrA contraction will likely have difficulty producing a voluntarily multifidus contraction. Matthijs et al (2014) were the first to objectify a co-contractive multifidus response to the ADIM and ABM in subjects without a history of or current LBP.

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Need for the Study Many studies have demonstrated neuromotor, morphological, and proprioceptive changes with LBP. It is important to note that these changes do not automatically resolve with LBP resolution, further promoting persistent lumbar dysfunction. Researchers have proposed using the ADIM and ABM as exercises and as dynamic spinal protective strategies during functional activities that may lead to spinal vulnerability. Many studies have demonstrated clinical symptom relief and biomechanical stabilizing benefits using these strategies. It has been generally accepted that these strategies result in multifidus co-contraction even in the dearth of empirical evidence supporting these beliefs. While Matthijs et al (2014) recently demonstrated that healthy subjects without a history of LBP in fact do experience superficial multifidus co-contraction during both ADIM and ABM. Deep and superficial multifidus fibers are differentially activated during functional movements, and multifidus activation changes have been demonstrated during LBP and after pain remission. Therefore, it is necessary to assess both superficial and deep multifidus co-contraction with abdominal activation strategies in patients without pain and with a history of LBP. This is the first study to assess deep lumbar multifidus co- contraction during volitional abdominal contractions in subjects without pain and subjects with a history of LBP.

Purpose The purposes of this study were to determine: 1) if deep and superficial multifidus fibers demonstrate different co-contraction patterns during volitional abdominal contractions; 2) the effect of a LBP history on the ability of lumbar stabilizing muscles to co-contract with abdominal muscle activation compared to individuals without a LBP history; and 3) if co-contraction differences exist among abdominal activation strategies and common positions used in clinical practice. This dissertation is divided into two separate studies with data collected simultaneously and subsequently analyzed separately to answer multiple research questions. Study 1 was performed with asymptomatic subjects without a history of LBP within the past two years and focused on studying the effects of subject position, abdominal activation strategies, and multifidus fiber depth. Study 2 compared these same

5 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 variables in subjects with a history of LBP within the past 2 years and determined the influence of subject LBP history on these variables.

Research Questions Study 1 Purpose 1: To determine if deep and superficial multifidus fibers demonstrate different co-contraction patterns during volitional abdominal contractions. RQ1) Is there a difference in co-contraction among activation strategies (resting, ADIM, and ABM) in the deep and superficial multifidus fibers in healthy subjects? RQ2) Is there a difference between deep and superficial multifidus co-contraction during each VPAC strategy in healthy subjects? Study 2 Purpose 2: To determine the effect of a LBP history on the ability of lumbar stabilizing muscles to co-contract with abdominal muscle activation compared to individuals without a LBP history. RQ1) Is there a difference in multifidus co-contraction between subjects with a LBP history when compared to healthy subjects without a LBP history during VPAC? Purpose 3: To determine if co-contraction differences exist among abdominal activation strategies and common positions used in clinical practice for subjects with a history of LBP. RQ2) Is there a difference in co-contraction among activation strategies (resting, ADIM, and ABM) in the deep and superficial multifidus fibers in subjects with a history of LBP? RQ3) Is there a difference in superficial and deep multifidus co-contraction in response to VPAC during standing versus quadruped positions in subjects with a history of LBP?

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Hypotheses Study 1 H1) It has been demonstrated that there was no difference in multifidus co- contraction frequency between ADIM and ABM in healthy subjects while both activation strategies had significantly greater co-contraction frequency compared to resting. However, because the ABM preferentially activates trunk flexors, a greater amount of extensor activity may be necessary to counteract the flexion forces. Therefore, it was hypothesized that the ADIM and ABM would both result in greater deep multifidus co-contraction than resting. H2) Despite the fact that superficial and deep multifidus fibers are both innervated by medial branches of the dorsal ramus of relevant spinal levels, previous research has demonstrated that these fibers activate differently during certain functional activities and in response to perturbations (Moseley et al., 2002; 2003). Additionally, differences between deep and superficial fibers exist on anatomical, biomechanical, histological, and neuromotor levels (Dickx, Cagnie, Achten, Vandemaele, Parlevliet, & Danneels, 2010a; MacDonald et al., 2009; Macintosh et al., 1986; Macintosh & Bogduk, 1986). Therefore, it was hypothesized that a difference would exist between deep and superficial multifidus co-contraction during VPAC. Study 2

H1) It has been observed that some individuals with current LBP demonstrate a reduced ability to perform an ADIM (Hides, Stanton, Freke, Wilson, McMahon, et al., 2008b). Additionally, a relationship has been established linking the ability to voluntarily activate the TrA with the ability to voluntarily contract the multifidus (Hides et al., 2011). Furthermore, multifidus muscular dysfunction persists after pain resolution in subjects with a LBP history (MacDonald et al., 2009). Therefore, it was hypothesized that subjects with a history of LBP would exhibit multifidus co-contraction in response to VPAC but this co-contraction activity would not be as high as the co-contraction level found in subjects without a LBP history. 7 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

H2) In individuals without LBP, both ADIM and ABM resulted in statistically similar multifidus co-contraction while no co-contraction was present at rest (Matthijs et al., 2014). Therefore, it was hypothesized that subjects with a history of LBP would demonstrate no difference in multifidus co-contractile response during ADIM and ABM, while resting would not result in multifidus co-contraction. H3) Although Matthijs et al (2014) did not statistically assess differences in multifidus co-contraction between standing and quadruped positions with healthy subjects, a visual analysis suggested that multifidus co-contraction occurred more frequently in standing than quadruped. Therefore, it was hypothesized that both ADIM and ABM would result in multifidus co- contraction in standing and quadruped positions, with greater co-contraction produced in standing for HxLBP subjects.

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CHAPTER II

LITERATURE REVIEW Low back pain (LBP) is associated with morphological and neuromotor changes of the multifidus muscles, which appears to affect the deep multifidus fibers more than the superficial multifidus fibers (Arokoski et al., 2001; Pool-Goudzwaard et al., 1998; Suehiro et al., 2015; Teichtahl et al., 2015; Wallwork et al., 2009). This dysfunction may lead to a greater susceptibility for further injury or reinjury (Cholewicki et al., 2005; Hides et al., 2001). Even after LBP has subsided, muscular changes and dysfunction may persist (D'hooge et al., 2012; Hides, Richardson, & Jull, 1996; MacDonald et al., 2009). Trunk muscle co-contraction has been shown to result in increased spinal stability (Stanton & Kawchuk, 2008; Vera-Garcia et al., 2007). Volitional pre-emptive abdominal contractions (VPAC) including the abdominal drawing in maneuver (ADIM) and the abdominal bracing maneuver (ABM) have been shown to result in superficial multifidus co-contraction in asymptomatic patients (Matthijs et al., 2014). However, it is currently unknown whether a similar co-contraction will be seen in the deep multifidus fibers or in subjects with a history of LBP. Therefore, the purposes of this study were to determine: 1) if deep and superficial multifidus fibers demonstrate different co-contraction patterns during volitional abdominal contractions; 2) the effect of a LBP history on the ability of lumbar stabilizing muscles to co-contract with abdominal muscle activation compared to individuals without a LBP history; and 3) if co-contraction differences exist among abdominal activation strategies and common positions used in clinical practice. This chapter serves to provide a comprehensive review of the current body of evidence pertaining to: 1) the epidemiology of LBP; 2) trunk stabilizing systems; 3) trunk muscle anatomy; 4) muscular contributions to spinal stability; 5) pain-related multifidus changes; 6) muscular dysfunction theories; and 7) VPAC contribution to spinal stability.

Epidemiology Low back pain is an almost universal disorder with 70-85% of all individuals experiencing LBP at some point throughout their lifetime (Andersson, 1999; van Tulder et al., 2006). At any point in time, approximately 30% of individuals are experiencing LBP (Andersson, 1999; Deyo et al., 2006) making it the most common form of pain 9 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 reported by adults in the United States (Deyo et al., 2006). Low back pain has progressively become more problematic with one-year acute LBP prevalence increasing dramatically between 1992 and 2006 (Freburger et al., 2009). Chronic LBP prevalence has increased from 3.9%-10.2% in the same time period (Freburger et al., 2009). Overall, LBP is the second leading cause of disability in the United States (CDC, 2001) and the leading cause of activity limitation among adults under the age of 45 (Andersson, 1999). Individuals with LBP not only experience the burden of pain, but also a significant financial burden. Those who experience LBP incur approximately 60% greater healthcare expenditure as compared to those who do not experience LBP (Luo et al., 2004). This financial burden is not limited to the individuals themselves, but has significant societal financial impact as well. In the United States alone, total healthcare costs for individuals with back pain have reached more than 90 billion dollars annually with over 26 billion dollars being attributed specifically to back pain management (Katz, 2006; Luo et al., 2004). Back pain has become the second most frequent reason for physician office visits, making up almost 3% of all physical visits (Andersson, 1999; Hart, Deyo, & Cherkin, 1995). Furthermore, it represents the fifth leading cause of hospital admission and the third most common cause of surgical procedures in the United States (Andersson, 1999). Despite the fact that only a small portion of individuals with LBP seek care in the emergency department, approximately 2.63 million emergency department visits can be attributed to LBP annually, making up approximately 2.3% of all emergency department visits (Friedman, Chilstrom, Bijur, & Gallagher, 2010). Low back pain presence has a large impact on the workforce, with approximately 2% of the workforce being compensated for back injuries each year (Andersson, 1999) and 5% of American workers missing at least one work day annually due to LBP (Katz, 2006). Length of disability has an inverse relationship with cost. This is demonstrated by LBP of less than 1 month duration accounting for 86% of all claims and 11% of total costs, along with 5% of the claims that lasted greater than one year explaining 65-75% of total costs (Dagenais, Caro, & Haldeman, 2008; Katz, 2006). Low back pain accounts for approximately 66.6 billion dollars in indirect economic consequences, such as lost wages and reduced productivity (Katz, 2006).

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Although LBP affects all individuals differently, approximately 60-70% of back pain sufferers will recover within six weeks and 80-90% will recover within 12 weeks (Andersson, 1999). Despite the fact that these numbers are encouraging and may support a historical belief that LBP is a self-limiting and benign disorder (Indahl, Velund, & Reikeraas, 1995; Waddell, 1987), individuals who experiences acute LBP are four times more likely to experience an incidence in the next year compared to those who have not had LBP (Hestbaek et al., 2003). In adolescents, LBP recurrence has become more prevalent with time (Burton, Clarke, McClune, & Tillotson, 1996). It has been suggested that since recurrence is so prevalent, it seems to be a component of the natural course of LBP. As a result, more recent literature suggests that LBP is rarely a self-limiting disorder but rather presents with periodic remissions (Hestbaek et al., 2003). One possible explanation for such high recurrence rates is that underlying morphological and control changes may persist despite pain resolution (Macdonald et al., 2011; MacDonald et al., 2009; 2010). Additionally, researchers have demonstrated that a LBP history is the single best predictor of future LBP (Cholewicki et al., 2005).

Low Back Pain Definition and Classification Low back pain can be defined as pain and discomfort between the costal margin and the inferior gluteal folds and can exist with or without accompanying leg pain (van Tulder et al., 2006). Low back pain can be classified a number of different ways (O'Sullivan, 2005). Accurate classification based on diagnosis may be difficult considering non-specific LBP is the most common LBP classification with approximately 85% of LBP being considered “non-specific”. This term is used for those cases with no identifiable cause (Henchoz & So, 2008) that are determined by exclusion (Deyo & Phillips, 1996; Frank, 1993). Most commonly, LBP is classified based on symptom duration, whereby LBP is divided into three categories including acute, subacute, and chronic LBP (van Tulder et al., 2006). Under this naming convention, acute LBP is pain persisting less than four to six weeks (Mehling et al., 2011; van Tulder et al., 2006), while subacute pain lasts between six and 12 weeks duration, and chronic LBP is pain that continues beyond 12 weeks (van Tulder et al., 2006). An additional subset of LBP sufferers can be considered

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“recurrent” if they experience a new episode of LBP after a symptom-free six-month period (van Tulder et al., 2006). Stanton and colleagues (2011) developed a more recent definition of recurrent LBP using a DELPHI study. In this study, recurrent LBP is defined as “LBP which occurred at least two times over the past year with each episode lasting at least 24 hours with a pain intensity of two or more on an 11 point numeric pain rating scale and with at least 30 pain-free days between episodes” (Stanton et al., 2011). Although symptom duration is a common method for LBP classification, other authors suggest that chronic LBP should not be defined solely by duration of symptoms as this suggests LBP is a disease with a linear course (Hestbaek et al., 2003). Instead, back pain can be classified based on disease characteristics. In this model, the term “chronic” describes those who’s pain and disability have become disproportionate to the original physical problem and have become associated with biopsychosocial characteristics such as fear-avoidance, psychological distress, depressive symptoms, and failure to cope (Cedraschi et al., 1999; Deyo & Phillips, 1996; O'Sullivan, 2005; Waddell, 1992).

Lumbar Stability Lumbar stability can be defined as the ability of the lumbar spine to maintain equilibrium or regain equilibrium despite a perturbative force (Bergmark, 1989; Grenier & McGill, 2007) and is affected by multiple restraints including muscle force/stiffness, posture, and load (Bergmark, 1989; Pope & Panjabi, 1985). However, if spinal behavior after a perturbation differs significantly from pre-perturbation behavior, then the spine could be considered unstable (Reeves, Narendra, & Cholewicki, 2007). Stability is critical for the spine to be able to carry out its functional goals including the spine’s ability to bear loads and allow movement while avoiding pain and injury (Reeves et al., 2007). Additionally, Kibler et al. (2006) included the ability to allow optimum force control, transfer, production and motion to the upper and lower extremities as part of the stability definition. Although the spine’s ability to maintain or regain equilibrium after a perturbation is necessary, it is not sufficient for stability. One must additionally consider the amplitude of movement resulting from different degrees of perturbation forces (Reeves et al., 2007). In a stable system, a small perturbation should result in small

12 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 oscillations while a larger force should result in larger oscillations. If however, oscillations are similar regardless of the perturbation force strength, the system (spine) would be considered unstable (Reeves et al., 2007). Furthermore, stability is task dependent, whereby stability must be considered within the task’s context (i.e. different system goals have different stability requirements). Reeves et al. (2007) presented an example where a forward step in standing resulting from a perturbation would be considered unstable while a forward step during a task requiring an individual to pick up a box, step forward, and place on a shelf would still be within the confines of stability. The authors go on to explain that if the task required the individual to lift a heavy box then place the box on a shelf, “stability” would be the ability to perform the task while avoiding injury due to excessive force and strain (Reeves et al., 2007). Considering the earlier definition of stability, the ability to prevent spinal injury would be based on sufficient muscle activation, posture, and load.

Stabilizing Systems Panjabi (1992a) originally described three subsystems that contribute to spinal stability. These subsystems include the active, passive, and neural components. The active system is comprised of muscles and tendons surrounding the spine while the passive system includes structures such as vertebrae, facet articulations, intervertebral discs, ligaments, joint capsule, and the passive or viscoelastic component of muscle (Panjabi, 1992a). The neural component includes various mechanoreceptors, which are imbedded in the active and passive subsystem structures, as well as the central and peripheral nervous systems. This neural subsystem receives feedback from the periphery and acts to influence the active subsystem’s activity, thus leading to appropriate stabilization responses. These three subsystems work together to produce appropriate stability in response to stabilization demands (Panjabi, 1992a). The passive system does not contribute significantly to stabilization in the neutral zone (NZ) due to lack of tissue tension in this zone. The NZ is the portion of the range of physiological intervertebral motion where motion is produced with little internal resistance and is an area of higher flexibility or laxity (Panjabi, 1992b). It is not until further into the range of motion that passive structures begin to become tension loaded,

13 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 and therefore contribute more significantly to stabilization. Although these passive structures do not produce tension that directly produces a significant contribution to NZ stabilization, mechanoreceptors (from the neural subsystem) imbedded in the passive tissue can still provide information regarding joint movement and position (Panjabi, 1992a). Afferent nerve stimulation from lumbar discs, capsules, and ligaments results in reflexive multifidus activation (S. Holm, Indahl, & Solomonow, 2002). The relationship among the active, passive, and neural components demonstrates an important interconnection among the three subsystems leading to appropriate spinal stabilization responses. Solomonow and colleagues have performed studies assessing the relationship between the passive, active and neural subsystems, which further strengthen our knowledge of subsystem interconnection (Solomonow et al., 2003; Solomonow, Zhou, Harris, Lu, & Baratta, 1998; Solomonow, Zhou, Baratta, Lu, & Harris, 1999). Solomonow et al (1998) observed multifidus activity from ligamentous electrical stimulation demonstrating a relationship between receptors in the supraspinous ligament and the multifidus muscle. During repetitive lumbar flexion/extension, stabilizing muscular reflex activity was reduced by 85% within the first five minutes, thereby decreasing lumbar stability and possibly exposing the spine to destabilizing injury. The observed muscular stabilizing decrease was shown to be the result of mechanoreceptor desensitization due to viscoelastic tissue laxity. This decrease occurred in absence of neurological habituation and muscular fatigue (Solomonow et al., 1999). Passive tissue creep deformation is of little consequence on its own since passive tissue restraint only occurs later in spinal range of motion (closer to end range). The mechanoreceptor desensitization due to ligamentous laxity is of more importance due to the subsequent decrease or possible elimination of the muscles’ reflexive stabilizing and, in response, protective ability (Solomonow et al., 1999).

Trunk Muscle Anatomy Muscle contraction of the active subsystem is critical for spinal stability (Jemmett, MacDonald, & Agur, 2004) considering that in the absence of muscular activity the lumbar spine becomes unstable when exposed to a 78 N load and buckles when exposed

14 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 to an 88 N axial load (Crisco et al., 1992). The presence of disc or facet injury results in spinal buckling beginning at significantly lower force values (Crisco et al., 1992; Crisco & Panjabi, 1991). Additionally, as little as two (2) degrees of lumbar spinal rotation can cause passive tissue damage (Gracovetsky, Farfan, & Helleur, 1985) making muscular activity crucial for protecting the passive structures. The need for muscular activity is further highlighted when considering that the in vivo spine can be exposed to approximately 6000 N of compression during demanding everyday tasks (McGill & Norman, 1986) and even up to 18,000 N during competitive lifting (Cholewicki, McGill, & Norman, 1991). The difference between the in vitro buckling behavior and in vivo stability can be partially attributed to spinal stabilizing muscles acting as guy wires to stabilize the spine (McGill et al., 2003; Panjabi, 1994). To maintain appropriate spinal stability, all stabilizing muscle must be activated with appropriate tension. If just one segment has decreased muscular contribution, buckling will occur at a reduced axial load and the segmental level undergoing buckling will predictably be the level with decreased muscular activity (McGill et al., 2003). Knowledge of specific trunk muscles can help enrich our understanding of how these muscles contribute to spinal stability. Although muscle architecture alone does not explain the exact role of muscles, it remains important for determining muscular function (Delp, Suryanarayanan, Murray, Uhlir, & Triolo, 2001). Trunk muscles can be divided into superficial (global) and deep (local) muscles (Bergmark, 1989). Using this classification, local muscles are generally considered to be more advantageous for producing stability while the global muscles are advantageous for producing spinal movement (Bergmark, 1989). Global muscles transfer the load between the thoracic cage and the pelvis and therefore mainly contribute to spinal motion while assisting the local muscles in stabilization. Global system muscles include the external oblique, rectus abdominis, erector spine, lateral parts of the quadratus lumborum, and the internal oblique (Bergmark, 1989). While Bergmark (1989) originally considered the internal oblique to be a global muscle, more recent literature demonstrates that the internal oblique co-activates with the TrA, which is considered a local abdominal muscle

15 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 and stabilizer (Ainscough-Potts, Morrissey, & Critchley, 2006). Local muscles include those that have their origin or insertion at the vertebrae. These local muscles help to maintain lumbar spine mechanical stability and control the spine’s curvature while providing sagittal and frontal plane stiffness (Bergmark, 1989). Local stabilizers include the multifidus, interspinalis and intertransverse muscles (Bergmark, 1989). Additionally, abdominal muscles including the TrA and internal oblique are considered to be local spinal stabilizers (Hodges, 1999; Richardson et al., 2002; Stanton & Kawchuk, 2008). Although Bergmark (1989) originally stated that the global system responds to changes from an outside load and the local system responds to lumbar spine posture, it has since been demonstrated that local muscles such as the multifidus, TrA, and internal oblique are activated in response to an outside perturbation as well as during extremity motion (Cholewicki et al., 2005; Hodges & Richardson, 1996; 1997; Radebold, Cholewicki, Polzhofer, & Greene, 2001; Silfies, Mehta, Smith, & Karduna, 2009).

Global Muscle Anatomy Global trunk muscles include the rectus abdominis, external oblique, erector spinae, and quadratus lumborum lateral fibers. As stated above, this global muscular system transfers forces between the thoracic cage and the pelvis and is responsible for gross movement (Bergmark, 1989). In the lumbar region, the erector spinae can be separated into the longissimus thoracis pars lumborum (medial fibers) and the iliocostalis lumborum pars lumborum (lateral fibers). The longissimus thoracis pars lumborum fibers attach anteriorly to the accessory process and the medial transverse process just lateral to the lumbar multifidus. Caudally, fibers from L1-L3 attach to the erector spinae aponeurosis while the fibers from L4 and L5 attach to the medial aspect of the iliac crest and the posterior superior iliac spine (Daggfeldt, Huang, & Thorstensson, 2000; Standring & Gray, 2008). Medially, these fibers are separated from the multifidus by a wide plane filled with adipose and veins (Standring & Gray, 2008). Lateral to the longissimus thoracis pars lumborum is the iliocostalis lumborum pars lumborum, which is the most lateral of the lumbar erector spinae muscles. Anteriorly, it attaches to the lateral portion of the transverse processes and the middle layer of the thoracolumbar fascia. Caudally, iliocostalis fibers from L1-L3 attach to the erector spinae aponeurosis

16 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 while fibers from L4 and L5 attach directly to the iliac crest (Daggfeldt et al., 2000) (Standring & Gray, 2008). The quadratus lumborum runs from the 12th rib to the iliac crest bilaterally. This muscle can be separated into medial and lateral fibers. The lateral fibers are considered global muscles while the medial fibers are considered local muscles (McGill, Juker, & Kropf, 1996a; 1996b). These global fibers span from the 12th rib to the iliac crest and are oriented vertically (Jemmett et al., 2004). The quadratus lumborum is innervated by the ventral rami originating from the 12th thoracic and first through fourth lumbar spinal nerves (Standring & Gray, 2008). The quadratus lumborum is believed to fix the 12th rib during respiration and produce ipsilateral lateral flexion when contracted ipsilaterally and extension when contracted bilaterally (McGill, Juker, & Kropf, 1996b; Standring & Gray, 2008). The rectus abdominis is a large strap-like muscle that is positioned bilaterally just lateral to the abdominal midline. Cranially, the rectus abdominis is attached to the costal cartilage of the 5th, 6th and 7th ribs and may additionally attach to the anterior end of the 5th rib. Caudally, the rectus abdominis attaches to the pubic tubercle. It is innervated by the lower intercostal and subcostal nerves, which are terminal branches of the lower six or seven thoracic spinal nerves (Standring & Gray, 2008). The rectus abdominis contributes to spinal flexion and maintains abdominal wall stiffness during straining tasks (Standring & Gray, 2008). The external oblique is the most superficial of the three lateral abdominal muscles. It attaches to the external and inferior surfaces of ribs 5-12 and has muscular attachments to the latissimus dorsi and serratus anterior. External oblique fibers course in an anterior/medial and inferior direction with most fibers attaching to the anterior aponeurosis while fibers from the lower two ribs are oriented more vertically and attach to the anterior portion of the iliac crest. External oblique fibers are innervated by the ventral rami via the intercostal and subcostal nerves (Standring & Gray, 2008). The external oblique is responsible for trunk lateral flexion and contralateral rotation when contracted unilaterally and abdominal tone maintenance/intra-abdominal pressure when contracted bilaterally (Standring & Gray, 2008).

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Local Muscle Anatomy Local trunk musculature includes the deep and superficial multifidus fibers, interspinales, intertransversarii, internal oblique, and TrA. Additionally, the posterior psoas fibers and medial quadratus lumborum fibers are considered local stabilizers (McGill, Juker, & Kropf, 1996a; 1996b). Although the psoas may contribute to spinal stability, its main role is hip flexion when contracted in the absence of many other spinal stabilizers (Hansen et al., 2006). The psoas major is positioned bilaterally on the anterolateral aspect of the lumbar spine from the T12 to L5 vertebral levels (Bogduk, Macintosh, & Pearcy, 1992; Jemmett et al., 2004). The psoas major originates from the transverse processes, vertebral bodies, and the intervertebral discs and inserts into the lesser trochanter of the femur via a common tendon with the iliacus muscle (Jemmett et al., 2004). Innervation is supplied by the ventral rami from L1 and L2 with possible contribution from L3 as well (Standring & Gray, 2008). Psoas major muscle fibers can be divided based on proximal attachment and depth. The psoas includes the vertebral and discal heads (based on origin at the vertebrae or disc) and both superficial (anterior) and deep (posterior) fibers (Jemmett et al., 2004). Discussion exists regarding the psoas major’s role in spinal motion. Selected theories regarding the psoas’ functional role include producing spinal lateral flexion, postural function during standing and sitting, and contributing large lumbar compressive and shear loads (Hansen et al., 2006). Some controversy over psoas activity may be due to different fibers contributing to different movements. Park and colleagues (2012) found that while psoas fibers from the vertebrae and the transverse processes were active during ipsilateral flexion, transverse process fibers were more active during extension while vertebral fibers were more active during flexion (Park et al., 2012). As stated above, quadratus lumborum medial fibers are considered local stabilizing muscles (McGill, Juker, & Kropf, 1996a; 1996b). The medial fibers span between the iliac crest and the L1 to L4 transverse processes. Medial quadratus lumborum fibers may span between adjacent transverse processes from L1 to L4 and can be continuous with the lateral fibers (Jemmett et al., 2004). Other studies have separated the quadratus lumborum into anterior and posterior fibers demonstrating that the anterior

18 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 and posterior fibers are activated differentially (Park et al., 2012; Park, Tsao, Cresswell, & Hodges, 2013; 2014). While the anterior fibers were activated in a direction specific manner, the posterior fibers were activated in a non-direction specific manner (Park et al., 2014). The interspinalis muscles attach to the vertebrae’s spine on both sides of the interspinous ligament while the intertransversarri originate and insert onto adjacent transverse processes. Both the interspinalis and intertransversarri are innervated by the dorsal rami of each spinal level (Standring & Gray, 2008). The interspinalis and intertransversarri are very small and deep spinal muscles and due to their small size are not likely to be able to produce enough force to be prime movers of the lumbar spine. However, the interspinalis and intertransversarri possess a high density of muscle spindles, which make these muscles ideal to function as proprioceptors for the lumbar spine. Therefore, they are likely to help control lumbar movement and position through proprioceptive function (Standring & Gray, 2008). A visual representation of the interspinalis and intertransversarii can be seen in Figure 2.1.

Figure 2.1. Representation of interspinalis and intertransversarii muscles

While the internal oblique and TrA are distinctly different muscles, these two muscles have been found to contract together or in a similar manner (Marshall & Murphy, 2003). As a result, they often are assessed together (Marshall & Murphy, 2003), 19 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 accompanied by the fact that previous research has observed similar surface electromyography muscular activity of the TrA/IO complex when compared to indwelling TrA muscular activity (Marshall & Murphy, 2003). Additionally, it is difficult to directly assess the electromyographic activity of the TrA due to its deep relation to the internal oblique without using indwelling sensors (Marshall & Murphy, 2003). The TrA is the deepest and thinnest of the abdominal muscles (Urquhart, Barker, Hodges, Story, & Briggs, 2005a). Muscular fibers are located in the lateral 1/3 of the abdomen’s circumference and are continuous posteriorly with the posterior, medial and anterior thoracolumbar fascia (Barker, Briggs, & Bogeski, 2004a; Bogduk & Macintosh, 1984; Jemmett et al., 2004). Additionally, the TrA fascia attaches posteriorly to the 11th and 12th ribs, lumbar transverse processes, and the lateral vertebral bodies while passing anteriorly to the linea alba (Jemmett et al., 2004). Muscular fibers in the upper TrA are oriented horizontally while the middle and lower fibers are oriented more inferomedially (Urquhart, Barker, Hodges, Story, & Briggs, 2005a). The internal oblique is the thickest of the lateral abdominal wall muscles and is positioned between the TrA and the more superficial external oblique (Urquhart, Barker, Hodges, Story, & Briggs, 2005a). The upper internal oblique fibers are oriented superomedially while fibers below the anterior superior iliac spine are oriented horizontally (Urquhart, Barker, Hodges, Story, & Briggs, 2005a). The TrA and internal oblique are both innervated by the ventral rami of the lower six thoracic and first lumbar spinal nerves via the intercostal, subcostal, iliohypogastric, and ilioinguinal nerves (Standring & Gray, 2008). Although many of the previously described muscles possess appropriate architectural characteristics to aid in spinal motion control, their ability to limit intervertebral shear and torsion is limited (Moseley et al., 2002; Panjabi, Abumi, Duranceau, & Oxland, 1989). However, certain multifidus fibers (deep fibers) possess an advantageous placement and alignment for limiting shear and torsion while providing intervertebral compression (Moseley et al., 2002). Additionally, the closeness of the deep multifidus fibers to the spinal segments affords these fibers a unique ability to produce spinal stabilizing compression without requiring strong flexor activity to counteract an

20 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 extension torque (Kaigle, Holm, & Hansson, 1995; Moseley et al., 2002; Panjabi et al., 1989).

Multifidus Anatomy The multifidus is considered one of the more important lumbar spinal stabilizing muscles (MacDonald et al., 2006; Macintosh & Bogduk, 1986; Moseley et al., 2002; Ward, 2009; Ward et al., 2009). However, inconsistencies exist in terminology despite its importance for spinal stability. While selected studies have recognized the deep and superficial multifidus fibers as separate entities (Dickx, Cagnie, Achten, Vandemaele, Parlevliet, & Danneels, 2010a; Jemmett et al., 2004; MacDonald et al., 2006; 2010; Macintosh et al., 1986; Moseley et al., 2002; Rosatelli & Ravichandiran, 2008), many studies continue to refer to the entire muscle as “multifidus” without differentiating between deep and superficial fibers (Beneck & Kulig, 2012; Hides, Gilmore, Stanton, & Bohlscheid, 2008a; Nabavi, Mosallanezhad, Haghighatkhah, & Mohseni Bandpeid, 2014; Wallwork et al., 2009; Ward et al., 2009). The superficial and deep multifidus fibers have observable differences from a number of perspectives including anatomical (Macintosh et al., 1986; Rosatelli & Ravichandiran, 2008), biomechanical (Bogduk et al., 1992; Macintosh & Bogduk, 1986), histological (Dickx, Cagnie, Achten, Vandemaele, Parlevliet, & Danneels, 2010a; Sirca, 1985), and neuromotor distinctions (MacDonald et al., 2009; Moseley et al., 2002; 2003). Additionally, Tsao and colleagues (2011) demonstrated that deep multifidus fibers have separate cortical representation from the more superficially located lumbar erector spinae. Although such does not directly compare cortical representation between deep and superficial multifidus fibers, it demonstrates that the cortex has the ability to separately control different fascicles of the lumbar paraspinal muscles (Tsao et al., 2011). However, it is currently unknown if cortical representation differences exist between deep and superficial multifidus fibers. The multifidus is composed of five separate muscle fiber bands originating cranially from the spinous process and the lamina of each lumbar vertebrae and inserting 2-5 levels below (Jemmett et al., 2004; Macintosh et al., 1986; Rosatelli & Ravichandiran, 2008). Some differences exist within the literature regarding which of the five fiber bands are categorized as superficial and deep fibers. Moseley and colleagues

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(2002) stated that deep multifidus fibers originate from the vertebrae’s laminae and the inferior edge of the spinous process and course caudal-lateral, inserting into the mammillary process two and three levels below. In contrast, Rosatelli and colleagues (2008) categorized fibers as superficial, intermediate and deep. According to these authors, only the fibers originating cranially from the lamina and inserting into the vertebral mammillary process two levels caudal are considered deep fibers. Intermediate fibers originate from the lateral aspect of the spinous process and travel three levels before inserting onto the mammillary process and sacrum (Rosatelli & Ravichandiran, 2008). The multiple authors did not differ on superficial multifidus anatomy. Superficial multifidus fibers emanate as a continuous band from the tip of the spinous process, coursing down its lateral side and inserting into multiple structures 4-5 levels caudal (Macintosh et al., 1986; Moseley et al., 2002; Rosatelli & Ravichandiran, 2008). The most superficial fibers fail to attach to bony landmarks caudally but instead attach to the anterior surface of the erector spinae aponeurosis. Both superficial and deep multifidus fibers appear to have at least some caudal attachment to the zygapophyseal joint capsule (Jemmett et al., 2004). A visual representation of the deep and superficial multifidus fibers can be seen in Figure 2.2. Although the multifidus was originally considered to be a transverso-spinalis muscle, more detailed dissections show that it may more accurately be considered a spino-transverse muscle based in innervation patterns (Macintosh et al., 1986). Overall, the multifidus has a large physiological cross sectional area with short muscle fibers (Ward, 2009). Ward and colleagues (2009) demonstrated that the multifidus operates within a small portion of the length tension relationship on the ascending and plateau portions, giving the multifidus an ideal length tension relationship to increase force production as the spine flexes forward. Careful dissection has demonstrated that both the deep and superficial multifidus fibers are innervated by the medial branch of the dorsal ramus that exits below the vertebrae where the multifidus is attached cranially (Macintosh et al., 1986). Using this description, the deep and superficial multifidus fibers would be considered to be mono- segmentally innervated (Macintosh et al., 1986). Although the deep and superficial multifidus muscles are both innervated by the medial branch of the dorsal ramus, recent

22 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 literature has demonstrated that electromyographical (EMG) activation difference exist between the deep and superficial multifidus fibers (MacDonald et al., 2006; Moseley et al., 2003). This differential activation between the deep and superficial fibers lends inductive support for the believe that the superficial multifidus controls spinal orientation and position while the deep fibers aid in controlling intersegmental motion (Moseley et al., 2002). Therefore, if this holds true, it could be deductively reasoned that muscular activations intended to stabilize the spine may result in differential co-contraction of the deep and superficial fibers.

Figure 2.2. Representation of deep multifidus (left fibers) and superficial multifidus (right fibers)

The caudal attachment of the superficial multifidus is oriented almost directly inferior to the attachment on the spinous process, creating approximately a 90 degree angle between the vertebral pedicle and the multifidus fibers in the sagittal plane (Macintosh & Bogduk, 1986). This makes the superficial fibers ideal to counteract the flexion moment produced by abdominal muscles (Macintosh & Bogduk, 1986).

Muscular Contribution to Stability Stabilizing muscles must act in concert to provide a stable base for the trunk and extremities while transferring forces to the lower body during activities of daily living.

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These muscles can contribute to stability by either acting as guy wires of different length spanning the bending spine or increasing intra-abdominal pressure (Cholewicki & McGill, 1996). Typically, spinal stabilizing muscles in the abdomen (e.g. TrA, internal oblique and external oblique) act to increase intra-abdominal pressure (IAP) while spinal muscles (e.g. multifidus, erector spinae, interspinalis, intertransversarii, quadratus lumborum, and psoas) act as guy wires to stabilize the spine. Additionally, lumbar spinal stability can be augmented through trunk muscular activation tensioning the thoracolumbar fascia (Vleeming, Schuenke, Danneels, & Willard, 2014). Due to the nonlinear nature of spinal structural stability, it is unlikely that any single muscle can be identified as the most important spinal stabilizer (Cholewicki & VanVliet, 2002). Although single spinal stabilizing muscles are unlikely to contract in isolation during normal function, each local and global muscle discussed earlier likely contributes to spinal stability to a certain degree. It is more likely that many stabilizing muscles contracting together would contribute more significantly to spine stability than single muscles contracting alone (Cholewicki & VanVliet, 2002; Gardner-Morse & Stokes, 1998; Jemmett et al., 2004; Stokes et al., 2011). Certain muscle characteristics that include moment arm length and attachment sites indicate that global muscles act to provide overall lumbosacral stability and movement production while local muscles provide more intersegmental stability. Additionally, trunk loading magnitude and direction, as observed during different functional tasks, will partially dictate muscular stabilizing response (Cholewicki & VanVliet, 2002; McGill et al., 2003; Wagner et al., 2005).

Stabilization from Global Muscles Multiple studies demonstrate increased spinal stiffness during global trunk muscle activation (Andersen, Essendrop, & Schibye, 2004; Crisco & Panjabi, 1991; Grenier & McGill, 2007; Stanton & Kawchuk, 2008; Vera-Garcia et al., 2007) despite the fact that their primary role is to act as spinal movers (Bergmark, 1989; Christophy, Faruk Senan, Lotz, & O’Reilly, 2012). Global muscles that include the erector spinae and rectus abdominis generally have greater moment arm lengths than local muscles, allowing the muscles to act on the lumbar segments with greater torque (Bogduk et al., 1992; Hansen

24 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 et al., 2006). For example, activity in the global trunk muscles significantly increases spinal stiffness when exposed to a posteriorly directed perturbation. This perturbation preferentially activates abdominal muscles and results in considerable latissimus dorsi and erector spinae activity (Vera-Garcia et al., 2007). When the spine experiences a perturbation from posterior to anterior, the erector spinae increases spinal stability. Additionally, pre-activation of the erector spinae further increases spinal stability and decreases the amount of activation required after the perturbation (Andersen et al., 2004). Cholewicki and VanVliet (2002) reported a significant decrease (30%) in spinal stability when the lumbar erector spinae was removed from a spinal stability model. This study demonstrates that the erector spinae muscles are most critical for stability in the directions of extension, lateral bending, and axial rotation as well as during lifting tasks. However, this is not the case during flexion and vertical loading. The rectus abdominis has not been shown to contribute significantly to spinal stability in any loading direction (Cholewicki & VanVliet, 2002). Activation of all global muscles as seen during an abdominal bracing maneuver (ABM) increases posterior-anterior spinal stiffness more so than activation of local stabilizing muscles alone (Stanton & Kawchuk, 2008). When a mass is suddenly and unpredictably dropped into a box held by subjects, the thoracic erector spinae is the first muscle (other than biceps brachii) to activate (Moseley et al., 2003). Local muscle activation follows shortly thereafter. The early activation of thoracic erector spinae may be due to the proximity to the perturbation force and serves to counter the spinal flexion moment produced by the added weight. Performance of an ABM results in a 32% increase in lumbar spinal stability while only increasing spinal compression by 15% (Grenier & McGill, 2007). The addition of co-contraction of spinal extensors and abdominal muscles as seen during an ABM, significantly increases spinal stability (Arjmand & Shirazi-Adl, 2006; Gardner-Morse & Stokes, 1998; Kavcic et al., 2004). Although spinal stability is increased, this does not result in movement prevention, but an improvement in movement control (Grenier & McGill, 2007).

Stabilization from Local Muscles The local spinal stabilizing muscles include those muscles that have attachment directly to lumbar spinal segments (Bergmark, 1989). These muscles are positioned well

25 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 to aid in producing spinal stability based on their proximity to joint axes of movement, and as a result, have the capacity to control segmental spinal stiffness near the NZ (Wilke et al., 1995). It has been observed that certain local muscles activate prior to extremity movements in a feedforward fashion regardless of movement direction (Hodges, 1999; Hodges & Richardson, 1997; Moseley et al., 2002). This early activation suggests that these muscles play an important role in spinal stabilization. The TrA is considered to be an important spinal stabilizer (Cholewicki & VanVliet, 2002; Hides et al., 2006; Hodges, 1999). Although it has been suggested that the TrA may be activated without global muscle activation (Richardson & Jull, 1995), internal oblique activation is believed to accompany TrA activation (Ainscough-Potts et al., 2006; Hides et al., 2006). In conjunction with the internal oblique, the TrA is partially responsible for increasing intra-abdominal pressure (IAP) (Cholewicki, Juluru, & McGill, 1999a; Hodges & Richardson, 1996; Macintosh, Bogduk, & Gracovetsky, 1987; Stokes et al., 2011) as well as tensioning the thoracolumbar fascia for producing spinal stability during volitional contraction, such as an abdominal drawing in maneuver (ADIM) (Hides et al., 2006). Diaphragm and pelvic floor contractions play a critical role in increasing IAP. This increased IAP has been compared to an inflated balloon in front of the spine. Transversus abdominis contraction, and the resultant thoracolumbar fascia tensioning, results in increased resistance to flexion loads especially near the spinal NZ (Barker et al., 2006). However, the TrA contributes little extension moment during lifting (Macintosh et al., 1987) and may even decrease resistance to extension (Barker et al., 2006). Transversus abdominis activation prior to upper extremity movement indicates that the TrA acts in a stabilizing fashion by being activated in a feed-forward manner by the central nervous system (Hodges & Richardson, 1997; Moseley et al., 2002). Grenier et al (2007) suggested that the TrA only contributes a small amount of spinal stability during an ABM. Additionally, McGill and Norman (1986) suggested that the role of IAP in reducing disc compression has been overstated in the literature and that increased IAP may pressurize the hoop-like abdominals, which act to stabilize the spine similar to mast rigging on a sailboat. Although there is conflicting evidence regarding the degree to which the TrA contributes to lumbar stabilization in isolation, most resources agree that

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TrA activation does result in spinal stabilization to some degree (Barker et al., 2006; Barker, Briggs, & Bogeski, 2004a; Hides et al., 2006; Macintosh et al., 1987; Stokes et al., 2011). Recent evidence demonstrated that IO/TrA activation as seen during an ADIM results in superficial multifidus co-contraction in healthy subjects (Matthijs et al., 2014). In addition to tensioning the thoracolumbar fascia and increasing intra-abdominal pressure, this co-contraction mechanism is likely an additional method of increasing spinal stability (Richardson & Jull, 1995). Spinal muscle expansion during co-contraction that results from abdominal drawing in and abdominal bracing maneuvers may tension the thoracolumbar fascia posterior layer producing increased spinal stabilization (Macintosh et al., 1987). More evidence has recently emerged supporting the role of multifidus as an important spinal stabilizer (MacDonald et al., 2006). Multifidus fibers have been suggested to provide up to 2/3 of the stability experienced at the lumbar spine in response to trunk muscle activation (Wilke et al., 1995). Superficial multifidus fibers are believed to not only assist in stability but additionally act as lumbar spinal extensors and rotators, as well as assist in maintaining lumbar lordosis (MacDonald et al., 2006; Macintosh & Bogduk, 1986). It has been suggested that based on biomechanical difference between superficial and deep multifidus fibers, the superficial fibers will result in more spinal compression while producing spinal stability. The superficial fibers are known to co- contract with abdominal activation during both the ADIM and ABM (Matthijs et al., 2014). As discussed earlier, deep and superficial multifidus fibers differ in a number of aspects. Both superficial and deep multifidus have a greater percentage of type I versus type II fibers (MacDonald et al., 2006). Although not consistently agreed upon, selected authors reported that the deep fibers have a higher percentage of type I muscle fibers compared to the superficial fibers (Dickx, Cagnie, Achten, Vandemaele, Parlevliet, & Danneels, 2010a; Sirca, 1985). While muscular activity is important for spinal stabilization, not all muscles stabilize equally. Even in the presence of significant muscular force from large muscles, if the multifidus and erector spinae are inactive, the spine will buckle (Cholewicki & McGill, 1996). This instability can be prevented by

27 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 coordinating activity of small muscular stabilizers like the multifidus or by increasing passive spinal stiffness (Cholewicki, Juluru, Radebold, Panjabi, & McGill, 1999b). MacDonald and colleagues (2006) reviewed a number of studies that suggest the deep multifidus is tonically active during numerous activities, such as gait and forward trunk flexion. However, many limitations in these early experiments lead to difficulty with interpretation and these results have not been supported (MacDonald et al., 2006). Activity differences have been observed between deep and superficial multifidus fibers (Moseley et al., 2002; 2003). Moseley and colleagues (2002) observed non-directional dependent deep multifidus and TrA activity during rapid arm movement while superficial multifidus and erector spinae activity is dependent upon arm movement direction. Differences can be further observed during external perturbation reactions. When individuals are aware of an impending perturbation, an increased deep multifidus baseline activity is observed along with shorter activation latency compared to when perturbation timing is not known. Additionally, deep multifidus loading response occurs earlier than superficial multifidus, and superficial multifidus baseline activity does not change with perturbation timing knowledge (Moseley et al., 2003). In a separate experiment, Silfies and colleagues (2009) observed feedforward activity of the contralateral multifidus, contralateral erector spinae, and contralateral external oblique in preparation for rapid shoulder flexion. Feedforward activation of deep versus superficial fibers prior to a predictably timed perturbation may serve to limit spinal compression while still maintaining an adequate stability level (Moseley et al., 2003). In contrast to the contralateral multifidus activation seen during shoulder flexion, Suehiro et al (2015) observed ipsilateral multifidus activation prior to semitendinosus activation during a prone hip extension exercise. When combined, these studies serve to demonstrate the importance of proper superficial and deep multifidus activation in producing spinal stability.

Stabilizing Dysfunction In a healthy spine, the three stabilizing systems as discussed by Panjabi (1992a) work together in an effective and efficient manner to provide sufficient stability to prevent injury. Lumbar spinal injury and resulting LBP can alter the contributions of

28 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 these three stabilizing systems. Dysfunction in one or more of these stabilizing systems can end in one of three results: successful compensation, altered stabilizing system (long term adaptation), or overall stabilizing dysfunction (LBP) (Panjabi, 1992a). Some forms of stabilizing system dysfunction can lead to compensation and despite this dysfunction, these individuals may not be easily identifiable considering the successful compensation and resulting lack of current LBP. Similarly, subjects with recurrent LBP in a period of remission may have an underlying stabilizing dysfunction that is overshadowed by successful stabilizing compensation. In the presence of stabilizing dysfunction, patients are often said to possess spinal instability. Lumbar spinal instability can be separated into two broad categories including radiological appreciable instability and clinical instability (Cook, Brismée, & Sizer, 2006). Radiological appreciable instability results from damage to osteoligamentous structures (passive system) and is more identifiable at end ranges of spinal motion whereas clinical instability is experienced in mid ranges of motion, is often associated with an increased NZ, and is not easily identifiable using imaging techniques (Cook et al., 2006; O'Sullivan, 2000; Panjabi, 1992a). Considering the large number of structures responsible for contributing to spinal stability, there are multiple pathways for dysfunction development. Radiological appreciable instability has been found to be related to intervertebral disc degeneration (Toyone et al., 1994) and annular tears (Bräm, Zanetti, Min, & Hodler, 1998). Clinical instability may be related to altered neuromuscular system function possibly resulting from damage to structures such as muscle spindles, golgi tendon organs, or other mechanoreceptors imbedded in passive tissue (Cook et al., 2006; Panjabi, 2006; Solomonow et al., 2003). Additionally, clinical instability can be due to damage to the passive tissues, making mechanoreceptors inactive through a larger joint range of motion (Solomonow et al., 2003). Panjabi (2006) developed a hypothesis that ligament sub-failure can lead to muscle control dysfunction. Panjabi theorized that macrotrauma or repetitive microtrauma can lead to spinal ligament sub-failure with resulting injury to the mechanoreceptors within these spinal ligaments. This damage inhibits the mechanoreceptor’s ability to accurately detect movement and position and therefore sends corrupted information back to the central nervous system.

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Signals sent to the neuromuscular control unit may have altered spatial and temporal information compared to the normally expected signal leading to altered signal interpretation (Panjabi, 2006). The resulting muscular response patterns are corrupted, thus affecting spinal muscle spatial and temporal coordination (Panjabi, 2006). Low back pain has been associated with a number of morphological, psychomotor, and neuromuscular changes. Many of the LBP-associated morphological changes have been observed in the local (deep) stabilizing muscles including the multifidus and TrA (Bouche et al., 2011). Morphological changes can include increased fatty infiltrates (Battié, Niemelainen, Gibbons, & Dhillon, 2012; Brown et al., 2011; Chan et al., 2012; D'hooge et al., 2012; Hodges et al., 2015; Kjaer, Bendix, Sorensen, Korsholm, & Leboeuf-Yde, 2007; Lee, Cha, Kim, Kim, & Shin, 2008; Mengiardi et al., 2006; Teichtahl et al., 2015; Woodham, Woodham, Skeate, & Freeman, 2014; Zhao, Kawaguchi, Matsui, Kanamori, & Kimura, 2000) and decreased muscular cross sectional area (CSA) (Barker, Shamley, & Jackson, 2004b; Battié et al., 2012; Beneck & Kulig, 2012; Bouche et al., 2011; Chan et al., 2012; Danneels, Vanderstraeten, Cambier, Witvrouw, & de Cuyper, 2000; Fortin & Macedo, 2013; Hides, Stokes, Saide, Jull, & Cooper, 1994; Hides, Gilmore, Stanton, & Bohlscheid, 2008a; Hodges, Holm, Hansson, & Holm, 2006; Kulig et al., 2009; Lee et al., 2008; Wallwork et al., 2009; Woodham et al., 2014). A systematic review by Fortin and Macedo (2013) demonstrated that, in general, subjects with LBP have smaller paraspinal muscles when compared to those without pain. During acute LBP, segment specific unilateral multifidus atrophy has been observed using real time ultrasound imaging. The area of decreased CSA was found to be ipsilateral to the painful side and localized to the painful segment levels (Hides et al., 1994; 1996). Hodges and colleagues (2006) demonstrated that nerve injury can cause rapid multifidus atrophy along with increased fatty infiltrates, myofibril clustering and reduced muscle water content. Additionally, these authors noted that experimentally induced disc lesions resulted in level specific atrophy and morphological changes ipsilateral to the side of disc lesion. Although studies assessing acute LBP subjects demonstrate level-specific and ipsilateral morphology and CSA changes with some consistency, studies assessing these

30 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 changes in chronic LBP subjects are not as consistent. A number of studies using MRI and ultrasound imaging have demonstrated that subjects with chronic LBP have decreased multifidus cross-sectional area bilaterally (Beneck & Kulig, 2012; Hides, Gilmore, Stanton, & Bohlscheid, 2008a; Wallwork et al., 2009). Other studies have demonstrated a more ipsilateral decreased CSA presentation (Barker, Shamley, & Jackson, 2004b; Hides et al., 2011; Kulig et al., 2009). Although subjects who had unilateral chronic LBP did have bilateral decreased multifidus cross sectional area, the greatest size deficit has been observed ipsilateral to the painful side when compared to subjects with bilateral or central chronic LBP (Hides et al., 2011; Hides, Gilmore, Stanton, & Bohlscheid, 2008a; Kulig et al., 2009). Cross sectional area differences were 17.5% at L5 and 11.8% at the L4 level while higher levels showed less CSA decrease and less asymmetry (Hides, Gilmore, Stanton, & Bohlscheid, 2008a). Using magnetic resonance imaging (MRI), Kulig and colleagues (2009) noted that in most cases (17 of 20) the side of multifidus CSA loss was the same side of disc protrusion. These findings agree with another study using MRI, which found decreased ipsilateral multifidus CSA in patients with pain persisting longer than 12 weeks. Additionally, these authors noted smaller but still significant decreases in multifidus CSA at the levels above and below the painful segment (Barker, Shamley, & Jackson, 2004b). This multifidus CSA percentage decrease was positively correlated with symptom duration where subjects with longer LBP duration have greater multifidus CSA loss. Similarly, the psoas was found to have decreased CSA, which was correlated with pain intensity and the presence of nerve root compression (Barker, Shamley, & Jackson, 2004b). Using magnetic resonance spectroscopy, Mengiardi and colleagues (2006) found increased fatty infiltrates in the multifidus but not in the erector spinae. The authors observed fatty infiltrates accounting for 23.6% of multifidus CSA in subjects with chronic LBP whereas fatty infiltrates only accounted for 14.5% of multifidus CSA in asymptomatic subjects. Increased fat content has been shown to be associated with a history of ever having LBP (OR 9.2) and with having LBP within the last year (OR 4.1) demonstrating that even despite symptom resolution, multifidus morphological changes persist (Kjaer et al., 2007). Teichtahl and colleagues (2015) lend further support to this

31 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 relationship by demonstrating a correlation between increased multifidus fatty infiltrate at L3-L4 and an increased risk of high-intensity pain and disability (OR 12.6). These authors did not find a correlation between multifidus CSA and pain/disability. However, this study only assessed multifidus CSA at L3-L4 while many studies more commonly show decreased CSA at the L5 level. Morphological changes including increased fatty infiltrates have been observed ipsilaterally in patients with disc herniations, where the changes are ipsilateral to the herniation at that level and the level immediately below (Battié et al., 2012; Zhao et al., 2000). A specific cause for morphological changes and decreased multifidus CSA is not conclusive. However, Woodham and colleagues (2014) suggest that multifidus atrophy may be due to a facetogenic/discogenic reflex inhibition or dorsal ramus syndrome. Despite pain symptom remission, multifidus dysfunction may persist. Even in periods of pain remission, the multifidus can still have increased fatty infiltrates (D'hooge et al., 2012; Kjaer et al., 2007) and persistent atrophy (Hides et al., 1996). Patients with LBP not only have changes in resting muscle size (CSA) and fatty infiltration, but also experience changes in contractility and timing. Induced pain unilaterally directed at the multifidus resulted in decreased multifidus activity bilaterally at multiple levels (Dickx, Cagnie, Parlevliet, Lavens, & Danneels, 2010b). Wallwork and colleagues (2009) demonstrated a smaller thickness percent change in the multifidus during contraction in subjects with LBP compared to those without LBP. Chan and colleagues (2012) found increased multifidus stiffness (decreased elasticity) when subjects with LBP were in dependent weight bearing positions. However, similar muscular stiffness was not found when subjects were resting in prone. Instead, multifidus elasticity was similar to pain free controls in prone. Similarly, Brown and colleagues (2011) observed increased multifidus stiffness in fibers and fiber bundles but speculated that this may be due to collagen reorganization. More recently, Hodges and colleagues (2015) induced intervertebral disc lesions in 17 sheep and monitored multifidus characteristics at 3 and 6 months after injury. Contrary to the authors’ hypothesis, they did not observe multifidus atrophy, but instead observed increased adipose tissue and increased collagen formation. Although these authors did not observe atrophy, they do

32 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 not argue against the possibility of decreased multifidus CSA. Instead, they propose an injury response model including acute reflex inhibition, sub-acute to chronic slow to fast twitch muscle fiber transformation, and a later (more chronic) phase possibly including muscle atrophy due to disuse or denervation. Solomonow’s group has completed a number of studies assessing multifidus reflexive activity during different parameters of flexion activities. Solomonow and colleagues first demonstrated that cyclic loading resulted in viscoelastic tissue creep and subsequent mechanoreceptor desensitization resulting in drastically reduced multifidus activity (Solomonow et al., 1999). With two hours of rest, this loss of reflex multifidus activity was only restored to 20-30% of the baseline activity (Gedalia et al., 1999). Additionally, static or cyclic flexion loading for as little as 20 minutes resulted in similarly decreased multifidus reflexive activity along with superimposed multifidus spasms, and ligament inflammation. These authors concluded that the multifidus spasms were the result of the micro-damage and represent a reflexive spinal stabilizing strategy to limit the range of motion and unload (protect) the viscoelastic tissue (Solomonow et al., 2003). The human central nervous system incorporates a number of postural/spinal stabilizing strategies for stabilizing the spine during functional activities (Silfies et al., 2009). Silfies and colleagues (2009) described a number of these strategies including the following postural control strategies. In general, the selected strategy is partially dependent on the circumstances requiring stabilization. Muscular activation that occurs in preparation for movement and stiffens a joint or increases an individual’s base of support prior to a perturbation is termed “postural preparation”. When these adjustments are performed either at the same time as or prior to voluntary movements they are referred to as feedforward postural adjustments. These help provide stability and minimize the impact of a movement on posture. In contrast, postural adjustments that occur after a movement has been initiated are referred to as “feedback strategies” because they rely on input from sensory organs to initiate postural corrective strategies (Silfies et al., 2009). During episodes of LBP, some of these strategies can be altered leading to postural control impairments.

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A number of studies have assessed multifidus activity during voluntary postural perturbations. These studies help describe muscular activation in preparation for active movements (feedforward). When performing a prone hip extension exercise, chronic LBP subjects had delayed superficial multifidus onset bilaterally when compared to healthy controls (Suehiro et al., 2015). In healthy subjects, the ipsilateral multifidus was observed to activate before the semitendinosus during hip extension while subjects with chronic LBP did not have multifidus activation prior to semitendinosus activation (Suehiro et al., 2015). However, MacDonald and colleagues (2011) reported increased multifidus activity in subjects with recurrent LBP who were currently in remission from pain when compared to healthy controls during a prone hip extension. Different measurement techniques (surface EMG vs. Ultrasound CSA) and different activity parameters (onset timing vs. Muscle CSA) limit one’s ability to directly compare findings from these two studies. Additionally, one study demonstrated that LBP subjects in remission had greater trunk muscle co-contraction than healthy subjects during a voluntary trunk flexion activity. Of further interest is the fact that the authors found decreased deep multifidus and increased superficial multifidus activity on the previously painful side while there was decreased superficial multifidus and increased deep multifidus activity on the non- painful side (D'hooge et al., 2013). Similarly, MacDonald and colleagues (2009) found that during a rapid shoulder flexion or extension movement, LBP subjects in pain remission had earlier deep multifidus onset when compared to superficial multifidus on the non-painful side whereas on the previously painful side, deep multifidus was delayed to the point where there was no difference when compared to superficial multifidus. When recurrent LBP subjects in remission were presented with predictably or unpredictably timed loading to their hands, preparatory deep multifidus amplitude was decreased in recurrent LBP subjects compared to healthy controls on both the previously painful and non-painful sides. In contrast, superficial multifidus reached peak activity earlier on the previously painful side than the non-painful side (MacDonald et al., 2010). When combined, these studies may demonstrate the existence of compensatory strategies during periods of pain remission where deep multifidus is both delayed and less active forcing the superficial multifidus to compensate to provide sufficient stability. As a

34 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 result, it is important to identify whether or not commonly used abdominal muscle activation strategies result in deep multifidus co-contraction. The heterogeneous nature of study results regarding multifidus activity (i.e. increased vs. decreased activity) highlights the need for subject classification. Silfies and colleagues (2009) demonstrated that asymptomatic subjects had significantly earlier feedforward activity of the multifidus, erector spinae, and external oblique muscles when compared to a heterogeneous group with LBP. However, when these LBP subjects were separated into “instability” and “non-instability” groups, the instability group had significantly later multifidus and erector spinae activation when compared to the non- instability group. Dankaerts and colleagues (2006) found no difference in trunk muscle activity between subjects with chronic LBP and healthy controls. However, when the chronic LBP subjects were classified as having a flexion pattern (FP) or an active extension pattern (AEP), clear differences arose. These authors found that subjects classified as AEP (those who position themselves in an actively extended seated posture) have significantly greater superficial multifidus, TrA, IO, and iliocostalis lumborum pars thoracis activity compared to FP and control subjects. Of great interest in this study is the observation that subjects who had increased muscular activity (AEP group) had no pain at the time of testing, indicating that this pattern may not be driven by pain and may not be the driving force behind pain. In contrast, patients with decreased muscular activity (FP group) did complain of pain at the time of testing. The pain development in these subjects during prolonged flexed seated posture may be due to increased mechanical stress in passive tissues resulting from decreased protective muscular activity. In addition to the multitude of changes that occur with respect to the multifidus, changes occur on a whole-body level with LBP including balance and postural changes. When presented with a postural perturbation, patients with chronic LBP demonstrate delayed stabilizing trunk muscle activity when compared to healthy subjects (Radebold et al., 2001; Reeves, Cholewicki, & Narendra, 2009). Delayed trunk muscle activation in response to a perturbation results in increased NZ size, increased trunk displacement, and possible increased tissue strain (Reeves et al., 2009; van Dieën, Selen, & Cholewicki, 2003b). Mehta and colleagues (2010) found that trunk muscle activity including TrA/IO,

35 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 multifidus, rectus abdominis, and EO were all delayed in patients with LBP during rapid shoulder flexion/extension, and while the multifidus activated in a feedforward pattern in healthy subjects, no muscles activated in a feedforward manner in LBP patients. Additionally, it was observed that subjects with disc herniations demonstrated decreased feedforward multifidus activation during an expected perturbation when compared to healthy subjects (Leinonen et al., 2001). Muscle onset alterations can be seen in patients with long standing groin pain where these subjects were found to have delayed TrA activation during an active straight leg raise (Cowan, Schache, & Brukner, 2004). Delayed trunk muscle activity in response to a perturbation influences spinal stability and is inversely related to reflex amplitudes in order to retain spinal stability. In individuals with chronic LBP, the delayed muscular reflex activation may be accompanied by decreased reflex amplitude, which can only be compensated for by increased co- contraction of the antagonistic spinal stabilizing muscles in order to maintain spinal stability (Liebetrau, Puta, Anders, de Lussanet, & Wagner, 2013). Multiple studies have reported LBP-related alterations in balance properties including altered control strategies (Brumagne et al., 2008; Brumagne, Cordo, & Verschueren, 2004), decreased single limb stance duration (Ham, Kim, Baek, Lee, & Sung, 2010; Sung, Yoon, & Lee, 2010), delayed postural corrections (Henry et al., 2006), reduced limits of stability (Sipko & Kuczyński, 2013), and increased anterior-posterior sway (Volpe et al., 2006). In many cases, the postural control differences widened between LBP patients and healthy subjects when postural challenges increased and when visual input was removed (Ham et al., 2010; Mientjes & Frank, 1999; Radebold et al., 2001; Sipko & Kuczyński, 2013; Sung et al., 2010). These results suggest a sensory re- weighting within the somatosensory system (Brumagne et al., 2004; 2008) and from the somatosensory system to the visual system (Ham et al., 2010; Mientjes & Frank, 1999; Radebold et al., 2001; Sipko & Kuczyński, 2013; Sung et al., 2010). Other studies have assessed proprioception specifically at the spine and they have found decreased threshold to detection of passive motion (Learman et al., 2009; Lee et al., 2010; Leinonen et al., 2003) and greater joint repositioning error (Learman et al., 2009; O’Sullivan et al., 2003) when compared to healthy subjects.

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Theories of Muscle Dysfunction in LBP The findings within the literature regarding spinal muscular activity during LBP episodes and during remission vary greatly. While some studies demonstrate increased muscular activity, others demonstrate decreased muscular activity. Still others demonstrate increased muscular activity in select muscles with concomitant decreased activity in other muscles. This variability has led to a number of different LBP theories. The two most prevalent theories are the Pain-Spasm-Pain theory (Lund et al., 1991) and the Pain Adaptation theory (Roland, 1986). However, neither model explains all muscular response variation found within the literature (van Dieën, Selen, & Cholewicki, 2003b). This has led to other researchers developing theories in attempts to encompass the great variation observed with LBP patients.

Pain-Spasm-Pain Theory The Pain-Spasm-Pain theory (vicious cycle theory) is one of the older and more widely discussed theories for the description of muscular response to LBP. This theory suggests that many chronic pain conditions are due at least in some part to abnormal muscular activity that is considered to be dysfunctional. This dysfunctional muscular contraction predictably increases regardless of the task, leading to ischemia and consequential pain (Roland, 1986). Originally, the belief was the increased muscular activity was due to contractures or spasms. This theory predicts that muscular activity in LBP patients will always be greater than healthy subjects when performing submaximal contractions and at rest (van Dieën, Cholewicki, & Radebold, 2003a). Multiple research groups have reviewed the available literature regarding this theory (Hodges & Tucker, 2011; Lund et al., 1991; Roland, 1986). Roland (1986) presented a number of studies, some of which supported and some of which did not support the Pain-Spasm-Pain theory. These authors concluded that available evidence does not provide support for the Pain- Spasm-Pain theory, because pain and spasm can occur independently. While some evidence does exist in agreement with the Pain-Spasm-Pain theory, data exist that contradict this theory and its generalizability (Hodges & Tucker, 2011; van Dieën, Selen, & Cholewicki, 2003b).

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Pain Adaptation Theory While reviewing evidence supporting and refuting the Pain-Spasm-Pain theory, Lund and colleagues (1991) concluded that there was conflicting evidence regarding this theory, with some evidence supporting and some evidence refuting it. The authors went on to create a theory based on the observation that agonist muscles (muscles that are painful or produce a painful movement) demonstrate decreased activity while the antagonist muscles increase activity. They suggested that the increased antagonist activity and decreased force production, range, and velocity that represents the “dysfunction” is a normal protective adaptation that is not specifically the cause of pain (Lund et al., 1991). This became known as the Pain-Adaptation theory and helps to explain more pain response variations found within the literature (Hodges & Tucker, 2011). This increased muscular activity with subsequent decreased movement velocity and range serves to decrease the likelihood of further injury. This theory has been supported in part by other authors who have stated that the altered muscular activity unloads and protects viscoelastic tissue and decreases chance of further injury (Solomonow et al., 2003). While this theory explains more variation in muscular activity response to pain, there are still contradictory findings within the literature regarding how pain influences muscular activity (Hodges & Tucker, 2011). As a result, a more comprehensive theory was needed to encompass the muscular activation variation found within the literature.

Activity Redistribution Theory Both the Pain-Spasm-Pain and Pain-Adaptation theory describe stereotypical whole-muscle behavior. In contrast to these two theories, variable patterns have been found in the literature (Hodges & Tucker, 2011). Not satisfied with the contradictions in the literature regarding both the Pain-Spasm-Pain and the Pain-Adaptation theories, van Dieën and colleagues (2003b) theorized that muscle recruitment adaptations are task- dependent and variable between and within subjects. Additionally, this group theorized that trunk muscle adaptations (increased activity and co-contraction) are functional compensatory mechanisms since they reduce damaging stresses to passive tissues by increasing spinal stabilization and limiting range of motion (van Dieën, Cholewicki, & Radebold, 2003a). Similarly, Hodges and Tucker (2011) noted the limitations of the Pain-

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Spasm-Pain theory and the Pain-Adaptation theory. These authors developed a new theory that centered on the idea that muscle adaptations during pain exist to limit further pain and protect vulnerable tissue. This theory was developed around 5 concepts regarding muscle adaptation to pain, including: (1) activity is redistributed within and between muscles; (2) adaptation alters mechanical behavior including movement and stiffness changes; (3) adaptation works to protect from further tissue damage (and pain); (4) adaptation involves more in-depth changes than simple muscle excitability and these changes can be complimentary, additive or competitive; and (5) adaptation has short term benefits but may produce unwanted increased tissue stress (Hodges & Tucker, 2011). According to the Pain-Adaptation theory and the Activity Redistribution theory, these muscular changes are not dysfunctional, but instead unload and protect the viscoelastic tissue from further damage (Hodges & Tucker, 2011; Lund et al., 1991; Solomonow et al., 2003). These theories attempt to explain muscular response during movement but may not necessarily be applicable during isometric muscular contractions similar to those found in many low back rehabilitation programs where the abdominal muscles are activated voluntarily. Considering the importance of the deep and superficial multifidus fibers in stabilizing the spine, it is necessary to determine the muscular response of these muscles during isometric contractions and not just during spinal movements. Additionally, these theories attempt to explain muscular activity responses during episodes of pain and fail to explain persistent muscular activity dysfunction after LBP episodes.

Clinical Spine Stabilization The presence of LBP can result in a number of neuromuscular changes as previously discussed. These changes can lead to decreased lumbar spinal stability and an increased potential for further passive tissue damage (Leinonen et al., 2001; Panjabi et al., 1989; Reeves et al., 2009). Although clinical instability is not completely understood, these individuals may report a feeling of “giving way” or giving out” as well as pain during transitional activities and demonstrate poor neuromuscular control and poor proprioceptive function (Cook et al., 2006). Muscular changes associated with these signs may subject these individuals to further pain or passive tissue damage if additional steps

39 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 are not taken to stabilize the spine. This quest is not new, where different measures have been attempted to help patients stabilize the spine. For example the passive approach of using an abdominal belt to increase spinal stability has been examined (Cholewicki et al., 1999b; Ivancic, Cholewicki, & Radebold, 2002). However, this approach has no effect on increasing the muscle-generated lumbar spine stability and does not alter L4/L5 joint compressive forces (Ivancic et al., 2002). Furthermore, wearing a belt does not decrease risk of injury and may even increase injury risk after use has ceased (Reddell, Congleton, Dale Huchingson, & Montgomery, 1992). Because of the limited success associated with passive abdominal belt use, attention has turned to the role of volitional trunk muscle activation for spine stability. Given the impact of muscular activity in spinal stability, it is necessary to determine ways in which the local and global systems can be volitionally incorporated into active spinal stability in patients with altered neuromuscular control. Volitional pre-emptive abdominal contractions (VPAC) has been shown to increase intra-abdominal pressure and spinal stability (Arjmand & Shirazi-Adl, 2006). Trunk co-contraction is most commonly accomplished using two specific methods: the abdominal drawing in maneuver (ADIM) and the abdominal bracing maneuver (ABM). The ADIM is performed by asking the subject to “pull” the lower abdominal muscles (below the umbilicus) backwards toward the spine (Nagar, Hooper, Dedrick, Brismée, & Sizer, 2014). The ABM on the other hand is performed by asking the subject to tighten all abdominal muscles (Grenier & McGill, 2007) as if preparing to be punched in the stomach (Matthijs et al., 2014). Urquhart and colleagues observed the greatest TrA activity with inward motion of the abdomen in supine (Urquhart, Hodges, Allen, & Story, 2005c). Additionally, the ADIM has been shown to preferentially activate the internal oblique (Hides et al., 2006; Stanton & Kawchuk, 2008) and result in superficial multifidus co-contraction in asymptomatic subjects (Matthijs et al., 2014). While selected authors have suggested that it may be possible to activate the TrA in isolation (Richardson et al., 2002; Teyhen et al., 2008), others have demonstrated concurrent activation of the internal oblique and superficial multifidus (Hides et al., 2006; Matthijs et al., 2014; Vera-Garcia et al., 2007). Performing an ADIM results in decreased trunk cross sectional area, which would

40 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 indicate increased intra-abdominal pressure (Hides et al., 2006). During the ABM, authors have observed greater activation of the rectus abdominis, external oblique, internal oblique, thoracic erector spinae, lumbar erector spinae, and superficial multifidus (Matthijs et al., 2014; Stanton & Kawchuk, 2008; Urquhart, Hodges, Allen, & Story, 2005c). Interestingly, the ABM has been found to create greater external oblique activity than rectus abdominis activity (Urquhart, Hodges, Allen, & Story, 2005c) that reduces unwanted movement during the activity, being that the rectus abdominis acts more as a sagittal plane mover than a spinal stabilizer. Rectus abdominis and external oblique activity is significantly less during an ADIM than during the ABM (Vera-Garcia et al., 2007) with one study observing no increased RA and ES activity during an ADIM (Stanton & Kawchuk, 2008). Considering the specific muscular activation patterns present when performing an ADIM and ABM, Urquhart and colleagues (2005c) suggested that an ABM may not be ideal when attempting to preferentially activate the TrA or IO due to the ABM’s preferential EO/RA activation. Superficial multifidus fibers appear to be activated across both the ADIM and ABM (Matthijs et al., 2014), suggesting a co-contractive stabilizing affect. While the deep multifidus fibers contribute significantly to spinal stability, it remains to be seen whether or not the deep fibers follow a co-contraction pattern similar to the more superficial fibers. Although Urquhart et al (2005c) demonstrated that the ability to activate the TrA differs among different positions, Matthijs and colleagues (2014) demonstrated that all subjects were able to activate the TrA in standing, 4-point kneeling, and supine positions and that the superficial multifidus co-contracted in all three positions. Both the ADIM and ABM have been shown to increase spinal stability. Stanton et al. (2008) demonstrated that both ADIM and ABM produce increased P-A spinal stiffness when compared to no pre-activation. When exposed to a posteriorly directed perturbation, the ABM at 20% maximum voluntary contraction resulted in significantly greater spinal stability in the sagittal plane, reducing lumbar extension by 43% compared to no pre-activation condition (Vera-Garcia et al., 2007). This is likely explained by the increased rectus abdominis activity during the ABM that directly opposed the posteriorly directed perturbation force. These authors demonstrated that the ABM is an effective

41 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 method of stabilizing the spine in preparation for sudden loading. Grenier et al. (2007) demonstrated that while the ADIM did increase spinal stability, the ABM increased the spinal stability index by 32% above that produced by the ADIM alone. However, the ABM produced 15% greater spinal compression than the ADIM. Although this study did not account for increased IAP, it is likely that both ADIM and ABM would increase intra-abdominal pressure resulting in similar relative results. This study only assessed the stabilizing contribution from abdominal muscles and did not account for co-contraction of spinal muscles such as the multifidus, intertransversarii, interspinalis, or erector spinae, which may increase the spinal stability index. Therefore, in order to more accurately model the stabilizing effects of the ADIM and ABM, it is necessary to include deep and superficial multifidus activation in both models. This is especially important considering the important stabilizing role of the deep multifidus fibers as discussed earlier. Evidence exists demonstrating that subjects are able to perform an ADIM while simultaneously performing functional activities such as a forward reach (McGalliard et al., 2010; Nagar et al., 2014). Additionally, subjects with a history of LBP but no present symptoms appear to have greater TrA thickness than asymptomatic controls both during an ADIM contraction and during a forward reach, indicating that these subjects are able to employ a voluntary muscular contraction as a protective strategy during functional activities where decreased spinal stability may predispose these individuals to a greater risk of further tissue damage (McGalliard et al., 2010; Nagar et al., 2014). One aspect of the ADIM and ABM that has yet to be demonstrated empirically is whether or not the deep multifidus co-contracts when performing these volitional abdominal contractions.

VPAC Disadvantages Although there are a number of benefits of using a VPAC during functional activities, including increased spinal stability for passive tissue protection, there are potential drawbacks of VPAC use. According to the Pain-Spasm-Pain theory, forcing a painful muscle to contract with greater force may perpetuate the painful cycle (Roland, 1986). However, a number of studies have demonstrated limitations in this theory as it related to LBP (Hodges & Tucker, 2011; Lund et al., 1991). It has been demonstrated

42 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 through spine modeling and in vivo studies that increased co-contraction leads to an increase in spinal compression loads, which may has been linked to spinal pain and other spinal disorders (Gardner-Morse & Stokes, 1998; Grenier & McGill, 2007; Vera-Garcia et al., 2007). Vera-Garcia and colleagues (2007) demonstrated that the ABM and ADIM both increased spinal compression at each level of activation with the ABM producing greater stability and compression compared to the ADIM at each activation level. Additionally, Grenier and colleagues (2007) demonstrated that the ABM produced 15% more spinal compression than the ADIM. Therefore, not only is too little muscular activity potentially harmful for the spine, but too much activity may be harmful by creating increased compressive loads (McGill & Cholewicki, 2001). This may be the case under normal loading conditions, but in order for the spine to bear greater loads, greater muscular activity is required to increase spinal stability and reduce the chance of spinal buckling or unwanted displacement making increased muscular activity necessary for stability. Excessive shear forces are suspected to contribute to lumbar disc herniations (Costi et al., 2007). Flexion postures result in increased anterior shear forces, increasing intervertebral disc injury rate and requiring muscles to produce greater posterior shear and compressive forces to stabilize the spine (Costi et al., 2007; Shahvarpour, Shirazi- Adl, Larivière, & Bazrgari, 2015). Based on muscle fiber orientation in relation to intervertebral joints, the multifidus is capable of producing minimal posterior sheer, but is better suited to produce stabilizing compressive forces (Macintosh & Bogduk, 1986). Considering the injury risk produced by large shear forces, increasing axial compression loads in order to decrease shear loads may be a beneficial trade off of performing a VPAC in preparation for potentially harmful spinal loading. Although prolonged trunk muscle co-contraction may increase spinal loading, performing ADIM and ABM strategies facilitate co-contraction to temporarily protect the spine over a short period of time (Vera-Garcia et al., 2007). A number of studies have demonstrated decreased or delayed muscular activation during LBP episodes, potentially increasing the subject’s risk for spinal buckling and subsequent pain and structural damage (Cholewicki & McGill, 1996; Descarreaux, Lalonde, & Normand, 2007;

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MacDonald et al., 2009). It is during these activities that the spine may be vulnerable to damage and a protective abdominal activation strategy including multifidus (deep and superficial) contraction may temporarily improve spinal stability and decrease the likelihood of further damage. However, while it has been shown that the superficial multifidus fibers co-contract during ADIM and ABM strategies, it is unknown whether or not deep multifidus fibers contract as well. The need to specifically study deep multifidus co-contraction is further supported due to the differential activation of deep and superficial multifidus fibers during functional activities (MacDonald et al., 2010; Moseley et al., 2002; 2003).

Co-contraction Evidence The lack of direct evidence for deep multifidus co-contraction during volitional abdominal muscle activation certainly does not indicate that such co-contraction does not occur. In fact, there is a considerable amount of evidence in the literature lending credence to the theory of multifidus co-contraction during a VPAC response. Although the deep and superficial multifidus fibers have been shown to differ from a neuromotor perspective (MacDonald et al., 2010; Moseley et al., 2002; 2003), the superficial multifidus has been shown to co-contract during both ADIM and ABM in healthy subjects (Matthijs et al., 2014). Jemmett and colleagues (2004) noted during cadaveric dissection that the psoas, TrA, quadratus lumborum, and multifidus muscles were arranged continuously around the lumbar spinal column from anterolateral (psoas major) to the spinous processes (multifidus), thus providing muscular support that is well positioned to stabilize the spine in all directions. Although each specific global and local muscle may contribute to spinal stability, multiple muscles contracting simultaneously contribute significantly more to spinal stability (Jemmett et al., 2004) with the multifidus providing up to 60% of spinal stability (Wilke et al., 1995). Multifidus muscular contribution to spinal stability is necessary considering the TrA alone has only limited ability to provide spinal stability (Grenier & McGill, 2007). Baek and colleagues recently observed increased superficial and deep multifidus activity with neuromuscular electrical stimulation of the TrA (Baek, Cho, et al., 2014b). Similarly, in another study Baek and colleagues observed increased thickness of the

44 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 external oblique, internal oblique, and TrA with superficial multifidus stimulation (Baek, Ahn, et al., 2014a). Together these two studies indicate the possibility that co-contraction may travel in both directions in individuals without LBP. Subjects with LBP who had difficulty voluntarily contracting the TrA also had difficulty voluntarily contracting the multifidus while subjects who could perform a good TrA contraction were 4.45 times more likely to be able to perform a good multifidus contraction (Hides et al., 2011). Regardless of whether the LBP caused motor control changes or if motor control changes caused LBP, there appears to be a functional link between these two muscles. Vleeming and colleagues (2014) supply further evidence for TrA and multifidus co-contraction from an anatomical perspective. These authors demonstrate that activation of the common tendon of TrA/IO without paraspinal muscular contraction results in anterior and lateral movement of the paraspinal compartment resulting in insufficient tension production capability of the TrA/IO complex. Similarly, contraction of the paraspinal muscles in the absence of TrA/IO contraction resulted in a large posterior displacement of the paraspinal muscles. However, when both the paraspinal muscles and the TrA/IO are contracted, tension is channeled through the posterior layer of the thoracolumbar fascia producing a “girdling” of the paraspinal muscles (Vleeming et al., 2014). Many motor control exercise programs are aimed at correcting muscular activation patterns (reducing co-contraction) to resemble those patterns seen in asymptomatic subjects. While exercise programs may improve control and decrease dysfunction, clinicians should use caution when attempting to force LBP patients to adopt a “normal” muscular recruitment pattern. The “abnormal” muscular activity observed in some LBP patients represents a compensatory mechanism that functions to enhance spinal stability. The ability for clinicians to differentiate between adaptive co-contraction and unnecessarily persistent control changes can be problematic and may highlight the need to classify patients based on clinical findings (van Dieën, Selen, & Cholewicki, 2003b). Body position may influence the co-contraction response of the multifidus. Urquhart and colleagues (2005b) observed different abdominal muscular activity between

45 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 seated and standing positions when subjects were asked to perform rapid shoulder movements. Additionally, other authors have demonstrated that trunk and limb muscular activation is influenced by postural position changes (Hodges & Richardson, 1997). It has been suggested that muscular activation differences between positions may be explained by the amount of trunk stability in each position with different muscular stability requirement in sitting compared to standing positions due to several factors causing a more stable trunk in a sitting position (Urquhart, Hodges, & Story, 2005b). Although Matthijs et al (2014) did not statistically assess differences in multifidus co-contraction between standing and quadruped positions in healthy subjects, a visual analysis suggests that multifidus co-contraction occurred more frequently in standing than quadruped. Therefore, it is important to assess multifidus co-contraction level during a functional position of standing compared to a commonly used clinical position of quadruped. As seen above, a number of changes occur in the low back during LBP episodes. Many of these changes involve alterations specifically related to the multifidus muscle. These changes can include morphological changes such as increased fatty infiltrates and multifidus cross sectional area as well as activation timing and intensity alterations. Additionally, changes can include multiple aspects of balance and proprioceptive deficits. Even despite LBP remission, some of these dysfunctional changes have been known to persist. Considering the important stabilizing role of the multifidus and the observed pain related multifidus dysfunction, individuals in LBP remission may have an increased susceptibility to potential re-injury. Although in the past it has been generally accepted that the multifidus contracts during abdominal contraction strategies such as the ADIM and ABM, it appears that empirical evidence supporting this belief has been lacking until recently when Matthijs et al (2014) demonstrated superficial multifidus co-contraction during these abdominal activation strategies. However, this co-contraction was only observed in superficial multifidus in subjects without a history of LBP. As a result, it is important to assess the co-contraction response of both the superficial and deep multifidus in subjects with a LBP history as well as those without a LBP history.

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CHAPTER III

METHODS Despite acute LBP remission, individuals who have previously experienced LBP have an increased likelihood of LBP recurrence (Hestbaek et al., 2003). This may be due in part to the fact that underlying morphology and sensorimotor control changes may persist despite pain resolution (Macintosh et al., 1986; Macintosh & Bogduk, 1986; Moseley et al., 2002; 2003). Despite the common belief that the multifidus co-contracts with abdominal activation strategies, empirical evidence assessing this is lacking and currently only supports superficial multifidus co-contraction in healthy subjects. As a result, it was unknown whether a similar co-contraction occurs in the deep multifidus fibers or in subjects with a history of LBP. Therefore, the purposes of this study were to determine: 1) if deep and superficial multifidus fibers demonstrate different co- contraction patterns during volitional abdominal contractions; 2) the effect of a LBP history on the ability of lumbar stabilizing muscles to co-contract with abdominal muscle activation compared to individuals without a LBP history; and 3) if co-contraction differences exist among abdominal activation strategies and common positions used in clinical practice. This dissertation is divided into two separate studies with data collected simultaneously and subsequently analyzed separately to answer multiple research questions. Study 1 was performed using asymptomatic subjects without a history of LBP within the past two years and focused on assessing the effects of abdominal activation strategy and multifidus fiber depth. Study 2 assessed the influence of pain history on the ability of the multifidus to co-contract during abdominal activation strategies. Additionally, study 2 assessed the effects of position, abdominal activation strategy, and multifidus fiber depth in HxLBP subjects.

Operational Definitions 1. Chronic LBP - Low back pain with associated pain and disability that has become disproportionate to the original physical problem and has become associated with biopsychosocial characteristics such as fear-avoidance, psychological distress,

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depressive symptoms, and failure to cope (Cedraschi et al., 1999; Deyo & Phillips, 1996; O'Sullivan, 2005; Waddell, 1992) 2. Clinical instability - An increase in the NZ size without radiological appreciable instability findings. Clinical instability is often associated with passive structure damage leading to motor control dysfunction (Cook et al., 2006; Panjabi, 2006) 3. Low back pain - Pain and discomfort between the costal margin and the inferior gluteal folds with or without accompanying leg pain (van Tulder et al., 2006) 4. Low Back Pain History – Low back pain within the previous two years of sufficient severity to require medical or allied health intervention or impair the subject’s ability to participate in activities of daily living (MacDonald et al., 2010) 5. Lumbar stability - The ability of the lumbar spine to maintain equilibrium or regain equilibrium despite a perturbative force (Bergmark, 1989; Grenier & McGill, 2007) 6. Recurrent LBP - Low back pain which occurred at least two times over the past year with each episode lasting at least 24 hours with a pain intensity of two or more on an 11 point numeric pain rating scale and with at least 30 pain-free days between episodes (Stanton et al., 2011) 7. Co-contraction – Activation of the multifidus muscle during volitional abdominal contraction. Co-contraction was measured as a percentage of sub-max contraction and compared to resting activity.

Assumptions 1. Subjects accurately reported their medical and LBP history. 2. Subjects understood the VPAC instructions and performed VPAC properly. 3. Performing 5 practice trials limited (if not eliminated) a learning effect. 4. Randomization limited an order effect. 5. The EMG system is reliable and valid measure of muscular activity. 6. Insertion of fine wire EMG electrodes did not substantially alter contraction ability of the multifidus muscle. 7. Superficial EMG electrodes at L5 accurately assessed superficial multifidus with no cross-talk from lumbar erector spinae. 48 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

8. Any differences in multifidus activity between groups were related to a history of LBP.

Design and Variables This dissertation included two studies: a within-subjects repeated measures design for study 1 and a mixed-methods design with between-groups and repeated measures comparisons for study 2. The first study included three independent variables: 1) Superficial and deep multifidus layers; 2) resting, ADIM, and ABM VPAC strategies; and 3) standing and quadruped positions. Deep and superficial multifidus layers represent the two multifidus layers of interest. Recent evidence supports differences between the two layers in a number of different characteristics. Three levels of VPAC strategy represent a resting state along with two commonly used protective and exercise contraction strategies commonly found in the literature and in clinical use. Standing and quadruped position represent two positions commonly used for performing abdominal activation strategies. Although a supine position is commonly used in the clinic, it was not used in this study due to possible interference and discomfort with the indwelling fine wire EMG electrodes in the lumbar multifidus. This study included one dependent variable of myoelectrical activity expressed in RMS EMG activity. RMS EMG activity was expressed as a percentage of sub-MVC and was calculated for both the deep and superficial multifidus using Formula 1:

Formula 1: %�� ℎ = ∗ 100%

The second study incorporated four independent variables. The first independent variable was back pain status with two levels (non-painful controls and subjects with a history of LBP). The second independent variable was VPAC strategy with three levels (resting, ADIM, and ABM), the third independent variable was testing position with two levels (standing and quadruped), and the fourth was multifidus fiber depth with two levels (deep and superficial). This study included one dependent variable of myoelectrical activity of the multifidus expressed in RMS EMG activity. This was expressed as a

49 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 percentage of sub-MVC and was calculated for both the deep and superficial multifidus using Formula 1 above. Data for both studies were collected using the same set of procedures. Both studies incorporated subjects performing abdominal drawing in and abdominal bracing maneuvers in standing and quadruped positions. These two positions were chosen because they are commonly used clinical positions for performing both the ADIM and ABM. The supine hook-lying position is another commonly used position, but the use of indwelling fine wire EMG electrodes in the deep multifidus fibers excludes the use of this position. It has been suggested that the quadruped position is the easiest position for subjects to obtain a successful abdominal drawing in maneuver with TrA activation based on optimal stretch of the abdominal muscles by the abdominal contents lifted against gravity (Richardson & Jull, 1995). While performing the abdominal drawing in and abdominal bracing maneuvers may be more challenging in an upright position, this is a necessary position for retraining muscles in preparation for functional activities (Richardson & Jull, 1995). Additionally, the quadruped position demonstrated less IO activity when compared to other positions (Teyhen et al., 2008).

Setting The study was conducted within the physical therapy programs at Youngstown State University and Walsh University.

Subjects Subjects included males and females between the ages of 18 and 65 years old. The asymptomatic subject group consisted of individuals without a reported history of LBP causing them to seek professional medical attention within the last 2 years. Subjects in the HxLBP group reported one or more episodes of LBP within the past two years of sufficient severity to cause the subject to either seek medical or allied health care for their LBP or limit the ability to participate in activities of daily living. Exclusion criteria for both groups included: 1) Any diagnosed and presently active abdominal, respiratory, or gastrointestinal condition; 2) Self-report of pregnancy; 3) Significant spinal deformities or a diagnosed condition that included scoliosis, spina bifida, tumors, present fractures, and/or rheumatologic disorders; 4) Current urinary tract infection; 5) A history of lumbar 50 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 or abdominal surgery; 6) Current use of anticoagulant medications or blood clotting disorders; 7) Inability to voluntary recruit abdominal muscles during ADIM and ABM as observed by investigator palpation; and 8) Inability to assume a quadruped position for any reason. No studies have specifically assessed for differences between deep and superficial multifidus activity during VPAC activation, especially in a population with a history of LBP. Therefore, exact effect size values for sample size calculations were not available. Instead, studies assessing multifidus thickness changes using functional magnetic resonance imaging and ultrasound imaging during contraction (Dickx et al., 2008; Wallwork et al., 2009), and CSA differences between LBP patients and asymptomatic controls were reported (Bouche et al., 2011; Chan et al., 2012; Hides, Gilmore, Stanton, & Bohlscheid, 2008a). These studies demonstrated variable Cohen’s d effect sizes ranging from 0.31 - 3.67. Due to this wide effect size range and the clinically observable nature of multifidus activity changes in subjects with LBP, a large effect size (d = 0.8 or f = 0.4) was chosen for prospective power analysis including sample size calculations. With a desired power of 80% (1-beta = 80%), alpha = 0.05 and an estimated effect size of f = 0.4, a sample size of 26 was determined to be necessary for each group (Portney & Watkins, 2009). To account for approximately 10% attrition, a total sample size of 60 subjects (30 asymptomatic subjects and 30 subjects with a LBP history) were recruited for this study. Subjects were recruited through the local universities, rehabilitation centers, as well as the general public.

Questionnaires Upon enrolling in the study, all subjects completed a medical history questionnaire to ensure eligibility to participate this this study. Subjective assessment measures are an important aspect of clinical practice. These subjective measures allow clinicians to measure constructs that have no direct means of objective measurement. All subjects completed the Lumbar Spine Instability Questionnaire (LSIQ). Cook et al (2006) created a list of 15 subjective and 14 objective factors of consensus for clinical lumbar instability using a Delphi method. A more recent study by Macedo et al (2014) extracted the 15 subjective measures of clinical lumbar instability due to ease of application and

51 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 demonstrated that subjects with higher instability levels (≥9/15) responded better to motor control exercises while those with lower instability levels (<9/15) responded better to a graded exercise protocol. Furthermore, these authors demonstrated that neither ceiling nor floor effects are of concern with this instrument. The Cronbach’s alpha was 0.69, falling just below the lower bound of “moderate”. The Lumbar Spine Instability Questionnaire as developed by Cook et al (2006) and modified by Macedo et al (2014) is available in Appendix A. All subjects completed the Oswestry Disability Index (ODI) (Fairbank & Pynsent, 2000). The ODI is composed of 10 questions assessing the disability level experienced during different physical activities. Development of the ODI began in 1976 and was first published in 1980 (Fairbank, Couper, Davies, & OBrien, 1980). Scores for each question are based on a 6-point Likert scale with a score of 0 indicating no disability and 5 indicating maximum disability. Scores are summed and divided by maximum possible score from the answered questions and multiplied by 100% to calculate a disability percentage (range: 0-100%). If any sections are missed or not applicable, the summed score is divided by the maximum possible score using only the questions answered (Fairbank & Pynsent, 2000). A recent systematic review and meta-analysis assessed various measurement properties for the ODI indicating that the ODI possesses “good” test-retest reliability (Chiarotto et al., 2016). The standard error of measurement (SEM) in individuals with a history of LBP within the past year was 2.56% (5.12 points) (Dawson, Steele, Hodges, & Stewart, 2010). Davidson and colleagues (2002) assessed responsiveness of five of the most commonly used low back disability questionnaires and found no difference in responsiveness among any of the measures. Additionally, the ODI has demonstrated excellent construct validity when compared to pain and subjective feeling of improvement after surgical intervention (Haro, Maekawa, & Hamada, 2008). The ODI can be found in Appendix B. All subjects completed the Tampa Scale of Kinesiophobia (TSK). The TSK is a 17 item questionnaire designed to measure the subject’s fear of movement (Miller, Kori, & Todd, 1991). Each item is measured on a 4-point Likert scale scored from 1-4 with 1 representing strongly disagree and 4 representing strongly agree. Scores can range from

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17 to 68 with higher scores representing greater kinesiophobia. Reliability of the full 17 point scale has been shown to be high for both chronic LBP and acute LBP subjects (French, France, Vigneau, French, & Evans, 2007; Swinkels-Meewisse, Swinkels, Verbeek, Vlaeyen, & Oostendorp, 2003) and can be clinically beneficial for identifying pain-related fear in acute LBP patients. The TSK has been shown to have good internal consistency and substantial test-retest reliability (Swinkels-Meewisse et al., 2003). The TSK can be found in Appendix C. Data obtained from the subjects’ completion of these subjective questionnaires as well as the subjects’ health history form were used for descriptive purposes for study two.

Procedures

Preparatory Procedures Subjects reported to the Musculoskeletal Research Laboratories for testing. Subjects viewed a short video explaining the experimental procedures. Each subject then read and signed YSU approved informed consent for participation. Subjects then completed a demographic and medical history questionnaire to determine eligibility for this study. All subjects then completed three self-reported surveys including the Oswestry Disability Index (ODI), the Tampa Scale of Kinesiophobia (TSK), and the Lumbar Spine Instability Questionnaire (LSIQ).

Testing Procedures Following completion of the preparatory procedures, subjects underwent brief VPAC education where they were instructed in the proper method of VPAC performance including ADIM, ABM and resting. For ADIM training, patients were instructed to “pull the belly in as if they were putting on a tight pair of pants” or to “imagine pulling the two front hip bones (ASIS) together”. For ABM training, subjects were instructed to “tighten your stomach as if you were about to get hit in the stomach”. The investigator instructed the subjects to activate the abdominal muscles to a self-selected sub-maximum voluntary contraction. Subjects then practiced both ADIM and ABM contractions with an investigator confirming the presence of abdominal muscle activation through manual palpation and visual confirmation. Although a learning effect may have occurred, these practice trials gave the opportunity for any learning effect to occur prior to recorded 53 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 trials. After each subject completed the VPAC practice trials, the subject was fitted with EMG electrodes. Myoelectric activity was detected using a combination of surface and fine wire indwelling electrodes (Delsys Inc., Natick, MA). Surface electromyography has been established as a reliable and valid method of assessing trunk muscle myoelectric activity (Dankaerts, O’Sullivan, Burnett, Straker, & Danneels, 2004; Larivière, Arsenault, Gravel, Gagnon, & Loisel, 2003; Marshall & Murphy, 2003; Pitcher, Behm, & MacKinnon, 2008; Yang & Park, 2014). However, subject characteristics such as subcutaneous adipose thickness as well as electrode placement can affect the recorded EMG signal (De Luca, 1997; Huebner, Faenger, Schenk, Scholle, & Anders, 2015; Nordander et al., 2003). Fine wire electrodes were required to record deep multifidus activity due to the nature of the deep fibers being covered by superficial multifidus fibers. Additionally, fine wire EMG was used for deep multifidus to decrease the amount of cross-talk from other muscular fibers including the superficial multifidus, erector spinae, quadratus femoris, and psoas major. All myoelectric data in the present studies were sampled and recorded at 1926 Hz (Hodges & Bui, 1996). According to the Nyquist theorem, EMG data sampling should be at least twice the highest detectable frequency. Although a 1,000 Hz sampling frequency is sufficient for surface EMG sampling, indwelling EMG using fine wire electrodes requires sampling near 2,000 Hz. Areas of surface electrode placement were shaved if needed. All attachment sites were lightly abraded and cleaned with alcohol to reduce electrical impedance. All superficial muscle EMG data were collected using Trigno Flex sensors. The EMG surface sensors (Trigno Flex sensors) have a built-in butterworth band pass filter giving the sensor a frequency response from 20 to 450 Hz (10-850 Hz for fine wire EMG) with less than 2.5 microvolt baseline noise. The common mode rejection ratio was >80dB. Double differential surface electrodes decrease muscle cross-talk by subtracting out signals that come from further distances that likely emanate from muscles other than the intended muscle (De Luca, 1997). Data were collected using EMGWorks software (Delsys Inc., Natick, MA).

54 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Double differential surface EMG electrodes were placed bilaterally over the superficial multifidus, longissimus thoracis, internal oblique, and external oblique. Superficial multifidus electrodes were placed bilaterally one cm lateral to the spinous process at the level of L5 in a slightly superomedial to inferolateral direction (Lariviere, Arsenault, Gravel, & Gagnon, 2002). While the multifidus activity was the focus of this investigation, activity of other muscles was collected to confirm correct EMG electrode placement on the multifidus. Additionally, observation of abdominal muscle activity was necessary to confirm that subjects were activating these muscles during ADIM and ABM contractions. Longissimus thoracis electrodes were placed at the level of L1 three cm lateral to midline in a cranial to caudal direction (Lariviere et al., 2002). Surface electrodes over the internal oblique were placed two cm below the level of the ASIS just medial and superior to the inguinal ligament in a mostly horizontal orientation. This placement is lateral to the IZ (Boccia & Rainoldi, 2014; Huebner et al., 2015). External oblique electrodes were placed parallel to the line extending from the most inferior part of the costal margin to the opposite pubic tubercle, 14 cm lateral to the midline one cm below the umbilicus (Boccia & Rainoldi, 2014; Huebner et al., 2015) with electrodes oriented in an inferomedial to superolateral direction. Dorsal muscle electrode placement can be found in Figure 3.1. The subject was then positioned in a prone position. One investigator palpated for the subject’s posterior superior iliac spine (PSIS) bilaterally and subsequently identify the S2 spinous process between the two PSIS landmarks (McGaugh, Brismée, Dedrick, Jones, & Sizer, 2007). Bipolar intramuscular fine-wire electrodes (Motion Lab Systems Inc, Baton Rouge, LA) were used to record electromyographic activity of the deep multifidus fibers. Electrodes were inserted using 50mm 25-gauge hypodermic needles with two insulated fine wire electrodes already threaded through them. These electrodes had approximately one mm of insulation removed from the end and the tips were bent back approximately two mm from the end forming a flexible hook. The area of skin for insertion was cleaned using an alcohol swab. The investigator donned medical nitrile gloves prior to handling the electrodes. The needle with electrodes was then inserted four cm lateral to the L5 spinous process in a ventral and medial direction until it reached the

55 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 lamina (Moseley et al., 2002). This placement was used to ensure recording of the deep multifidus fibers adjacent to the L5 lamina, which most likely originate from the inferior edge of L4. The investigator applied gentle but firm pressure with the hand over the skin while removing the hypodermic needle to prevent the fine wire electrodes from being pulled out. The hypodermic needle was placed into a sharps container. The subject was then asked to perform a gentle muscular contraction to ensure there was no significant discomfort. The fine wire electrodes were taped to the subject’s skin to prevent excessive movement and subsequent EMG noise. A Trigno spring contact sensor (Delsys Inc., Natick, MA) was attached to the subject. The sensor head with spring contacts was attached near the site of fine-wire insertion while the sensor body with reference contacts was attached to the most bony and palpable aspect of the iliac crest just anterior to the mid-axillary line. A short portion of the fine wire electrode end that was not inserted into the subject was free of wire insulation. This portion was attached to the pre-sensor head via two spring contacts on the top sensor head. This procedure was repeated on the opposite side for bilateral EMG recording of the deep multifidus. Prior to sub maximal reference testing, each subject was asked to perform an ADIM and an ABM contraction to visually confirm abdominal muscle activation.

Figure 3.1. Dorsal muscle electrode placement. A: Longissimus Thoracis, B: Superficial multifidus, and C: Deep multifidus 56 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Submaximal Reference Standard To allow comparison of repeated contractions within subjects and between subjects, it was necessary to normalize the recorded EMG data. Normalization is defined by Dankaerts and colleagues (2004) as “the process by which the magnitude of muscle activation is expressed as a percentage of that muscle’s activity during a calibrated test condition.” It is important for normalization methods to be reliable when used within and between subjects. Signal can be normalized in comparison to EMG amplitude during a maximum voluntary contraction (MVC). Using this method, it would be important to normalize to both force and signal amplitude when comparing between subjects due to differences in moment arm lengths (De Luca, 1997). Although an MVC is often used to normalize activity between days and between muscles, using an MVC may not be the most reliable method for normalization (Dankaerts et al., 2004; Yang & Winter, 1983). Using MVC signal for normalization has a number of downfalls. First and foremost, the question must be raised as to whether or not the subject is performing a fully maximal contraction (De Luca, 1997). This lack of maximal contraction may be amplified in subjects with current LBP due to lack of motivation, reflexive inhibition, or pain related fear of maximal muscle contraction (Larivière et al., 2003). Dankaerts and colleagues (2004) analyzed the reliability of MVC and sub-maximal voluntary contractions (sub- MVC) in subjects with and without chronic LBP. These authors found that while there was no difference in reliability during a within-day comparison, sub-MVC contractions were significantly more reliable in between day comparisons. The fact that MVC is not more reliable than sub-MVC combined with the less demanding nature of the sub-MVC reference exercises, and a possible unwillingness of LBP subjects to perform MVC exercises due to fear related pain, sub-MVC exercises were used in the current study as described by Dankaerts and colleagues (2004). For sub-MVC normalization of the abdominal muscles (IO and EO) subjects were placed in a supine hook lying position with the hips flexed approximately 45 degrees and the knees flexed approximately 90 degrees. The subject was instructed to raise both legs off the supporting surface approximately one cm and hold this position for seven seconds. For normalization of back muscles including deep and superficial multifidus and

57 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 longissimus thoracis the subjects were placed in a prone position with both knees flexed to 90 degrees. The subjects were instructed to lift both knees off the supporting surface five cm and hold for seven seconds (Dankaerts et al., 2004). Due to possible discomfort resulting from the supine hook lying position after placement of the deep multifidus fine wire electrodes, abdominal surface EMG electrodes were placed first followed by abdominal muscle normalization procedures prior to deep multifidus fine wire EMG placement.

Co-Contraction Testing Following normalization trials, subjects began co-contraction testing in standing and quadruped positions (Table 3.1). Subjects performed three abdominal contraction conditions: 1) Resting, 2) ADIM contraction, and 3) ABM contraction. Subjects performed each of these three contractions in standing and quadruped and were instructed to hold each contraction for seven seconds. Each condition was repeated three times. Condition order was randomized using randomization without replacement. To limit subject position movement, all standing contractions were performed together and all quadruped contractions were performed together. To limit the effect of position order, each subject was randomized to begin either in a standing or quadruped position followed by all trials in that position.

Table 3.1. Testing conditions including all position, contraction, and repetition combinations Standing Quadruped

Resting 1. Standing Resting (3x) 4. Quadruped Resting (3x)

ADIM 2. Standing ADIM (3x) 5. Quadruped ADIM (3x)

ABM 3. Standing ABM (3x) 6. Quadruped ABM (3x)

ADIM: Abdominal Drawing in Maneuver; ABM: Abdominal Bracing Maneuver

Data Reduction After the initial hardware processing produced a recorded EMG signal in the 20- 450 Hz frequency range, all EMG data were imported into a custom MATLAB (The 58 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Mathworks, Natick, MA) data reduction program. Sub-MVC muscular activity was calculated using a two second period of EMG data (seconds 3 and 4) from the seven second sub-maximal voluntary contraction using an RMS function. Similarly, a two second portion (seconds 3 and 4) of each seven second VPAC trial was used to calculate RMS EMG activity. Root mean square values from each set of three trials were averaged and subsequently represented as a percentage of the sub-MVC reference activity for each condition.

Statistical Analysis – Study 1 The first study is a within-subjects repeated measures design. Descriptive statistics (mean ± SD) were calculated for all demographic variables including age, weight and height for all asymptomatic subjects. Data were tested for normality using Shapiro-Wilk test, skewness, and kurtosis. Data normality was operationally defined as at least two of the three tests indicating normality (non-significant Shapiro-Wilk test, skewness between -2 and +2, and kurtosis between -2 and +2). Based on normality testing, a large portion of co-contraction dependent variables were found to be in violation of two or more of the previously stated values, and therefore indicated non- normal distribution of the dependent variables. Although the standard repeated measures ANOVAs is not robust to violations of normality (Erceg-Hurn & Mirosevich, 2008), robust analyses are designed to control Type I error rate while maintaining power (Wilcox, 2016). As a result, robust statistics were used to analyze for differences in trimmed mean values (Wilcox, 2016). Winsorized means (20% trimmed) were calculated for all dependent variables. This trimmed mean value presents a more appropriate mean value in datasets with large outliers (Erceg-Hurn & Mirosevich, 2008). Bootstrapping was performed 2,000 times and 95% confidence intervals were calculated from the 2,000 bootstrapped mean values. These values were used for all statistical comparisons. Robust statistical methods require a measure of effect magnitude as an alternative to the commonly reported Cohen’s d. As a result, a robust heteroscedastic approach to measuring effect size (x - ksi) was used (Wilcox & Tian, 2011). Using this approach, an effect of x = 0.15 is considered small, x = 0.35 is medium, and x = 0.5 is large (Wilcox & Tian, 2011). In order to answer the two research questions associated with study 1, two 59 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

2x3 repeated measures ANOVAs were performed. Both ANOVAs were 2 (Multifidus Depth) x 3(strategy) repeated measures ANOVAs testing for main effects of multifidus depth (deep and superficial) and main effects of contraction strategy (resting, ADIM, and ABM) in subjects without a LBP history. One ANOVA was completed using data obtained from subjects in a standing position and one used data from the quadruped position. Post hoc robust t-tests were used to locate significant differences when significant main effects were identified. The level of statistical significance for this study was set at alpha < .05. All subject baseline characteristics were calculated using IBM SPSS version 25.0 (Armonk, NY) and all dependent variable descriptive statistics and robust analyses were calculated using R software.

Statistical Analysis – Study 2 The second study utilized both between groups and repeated measures comparisons. Descriptive statistics (mean ± SD) were calculated for all demographic variables including age, weight and height for both subject groups. For subjects with a history of LBP, descriptive statistics were calculated for LSIQ, FABQ, and TSK questionnaires. Normality of dependent variables was assessed using Shapiro-Wilk test, skewness, and kurtosis. Data normality was operationally identified as at least two of the three tests indicating normality (non-significant Shapiro-Wilk test, skewness between -2 and +2, and kurtosis between -2 and +2). An independent t-test was used to test for differences in selected demographic characteristics between groups. Similar to the dependent variables in study 1, a sufficient amount of normality violations were observed within the current dependent variables to necessitate the use of robust statistical methods. These robust methods were designed to reduce the chance of Type 1 error while maintaining adequate statistical power (Wilcox, 2016). Winsorized means (20% trimmed) were calculated for all dependent variables. This trimmed mean value represents a more appropriate mean value in datasets with large outliers (Erceg- Hurn & Mirosevich, 2008). Bootstrapping was performed 2,000 times and 95% confidence intervals were calculated from the 2,000 bootstrapped mean values. These values were used for all statistical comparisons. Robust statistical methods require a measure of effect magnitude as an alternative to the commonly reported Cohen’s d. As a

60 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 result, a robust heteroscedastic approach to measuring effect size (x - ksi) was used (Wilcox & Tian, 2011). Using this approach, an effect of x = 0.15 is considered small, x = 0.35 is medium, and x = 0.5 is large (Wilcox & Tian, 2011). In order to answer the research questions associated with study 2, multiple two- way ANOVAs were completed using the Winsorized means, confidence intervals and bootstrapping. The first ANOVAs were 2 (group) x 2 (multifidus depth) mixed model ANOVAs that were assessed for main effects of group (healthy controls and a history of LBP) and main effects of multifidus depth (deep and superficial) in both standing and quadruped. Next, two 2 (Multifidus depth) x 3 (strategy) repeated measures ANOVAs were calculated using data from subjects with a history of LBP. One ANOVA was calculated for the standing position and one for the quadruped position. These analyses assessed for main effects of multifidus depth (deep and superficial) and main effects of strategy (resting, ADIM, and ABM) in subjects with a history of LBP. Lastly, three 2 (position) x 2 (multifidus depth) repeated measures ANOVAs were calculated to assess main effects of position (standing and quadruped) and main effects for multifidus depth (deep and superficial). One ANOVA was completed for each of the three contraction types. If a significant main effect or interaction was identified, post hoc robust t-tests with 2,000 bootstrapped samples was used to locate significant differences. Alpha was set a priori at 0.05 for all statistical comparisons. All subject baseline characteristics were calculated using IBM SPSS version 25.0 (Armonk, NY). All dependent variable descriptive statistics and robust analyses were calculated using R software.

61 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

CHAPTER IV

MULTIFIDUS CO-CONTRACTION DURING VOLITIONAL ABDOMINAL CONTRACTIONS IN HEALTHY INDIVIDUALS WITHOUT A RECENT HISTORY OF LOW BACK PAIN

Abstract Objective: The purpose of this study was to determine if deep and superficial multifidus fibers demonstrate different co-contraction patterns during the abdominal drawing-in maneuver (ADIM) and abdominal bracing maneuver (ABM). A second purpose of this study was to determine if co-contraction differences exist among abdominal activation strategies used in clinical practice. Design: Quasi-experimental repeated measures within-subjects design Setting: University research laboratory Participants: Thirty subjects (18 male, 12 female) between the ages of 18 and 65 years old (37.8 ± 14.46) without a history of low back pain in the previous two years were recruited for this study. Interventions: Subjects completed three trials each of the ABM, ADIM, and resting in the positions of standing and quadruped. Main Outcome Measures: Root mean square EMG activity of the deep and superficial multifidus fibers were normalized to a submaximal reference contraction for all trials. Multifidus co-contraction activity was then averaged among the three trials per condition. Results: ANOVAs revealed no statistically significant differences in co-contraction between the deep and superficial multifidus fibers in standing (p=0.317) and quadruped (p=0.681) positions during the ABM or ADIM. A significant main effect for contraction type was identified in both standing (p=0.008) and quadruped (p=0.047) with both the ADIM and ABM resulting in greater co-contraction than the resting condition (p<0.001). No differences in multifidus co-contraction were identified between the ADIM and ABM conditions in standing (p=0.738) or quadruped (p=0.741) positions. Conclusion: This study demonstrates that the deep and superficial multifidus fibers co- contract during the ADIM and ABM in subjects without a recent history of low back

62 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 pain. However, neither contraction strategy facilitated greater multifidus co-contraction than the other.

Introduction Contraction of the paraspinal muscles is important for providing spinal stability (Jemmett et al., 2004) considering that in the absence of muscular activity the lumbar spine becomes unstable when exposed to a 78 N load and buckles when exposed to an 88 N axial load (Crisco et al., 1992). The in vivo spine can be exposed to significantly greater compression during demanding everyday tasks (McGill & Norman, 1986). No single muscle is solely responsible for spinal stabilization (McGill et al 2003). Instead, many muscles must work together (co-contract) to create an appropriate stability for daily activities (McGill et al., 2003). Excessive shear forces are suspected to contribute to lumbar spine dysfunction, including disc herniations (Costi et al., 2007). The multifidus is capable of only producing minimal posterior sheer, but is better suited to produce stabilizing compressive forces (Macintosh & Bogduk, 1986). Considering the injury risk produced by large shear forces, increasing axial compression loads in order to decrease shear loads may be the mulifidi’s valuable contribution towards reduce anterior sheer forces in some circumstances. The abdominal drawing in maneuver (ADIM) and abdominal bracing maneuver (ABM) are two distinct abdominal muscle activation methods. The ADIM results in greater internal oblique activity (Hides et al., 2006; Stanton & Kawchuk, 2008) while the ABM produces greater external oblique, rectus abdominis, thoracic erector spinae, lumbar erector spinae, and superficial multifidus co-contraction (Matthijs et al., 2014; Stanton & Kawchuk, 2008; Urquhart, Hodges, Allen, & Story, 2005c). The superficial and deep multifidus fibers demonstrate observable distinctions in from an anatomical (Macintosh et al., 1986; Rosatelli & Ravichandiran, 2008), biomechanical (Bogduk et al., 1992; Macintosh & Bogduk, 1986), histological (Dickx, Cagnie, Achten, Vandemaele, Parlevliet, & Danneels, 2010a; Sirca, 1985), and neuromotor perspective (MacDonald et al., 2009; Moseley et al., 2002; 2003). Electromyographical (EMG) activation differences have been observed between the deep

63 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 and superficial multifidus fibers (MacDonald et al., 2006; Moseley et al., 2003). This difference in activation between the deep versus superficial fibers supports the believe that the superficial multifidus controls spinal orientation and position while the deep fibers aid in controlling intersegmental motion (Moseley et al., 2002). Therefore, if this holds true, it could be reasoned that muscular activations intended to stabilize the spine may result in differential co-contraction of the deep and superficial fibers. However, it remains to be seen whether or not the deep fibers follow a co-contraction pattern similar to the more superficial fibers during the ADIM versus ABM. Body position may influence a multifidus co-contraction response. Urquhart and colleagues (2005b) observed different abdominal muscular activity between seated and standing positions during rapid shoulder movements. This may be due to the amount of trunk stability and stability requirements in each position (Urquhart, Hodges, & Story, 2005b). Therefore, it is important to assess multifidus co-contraction level during a functional standing position, as well as during a commonly used clinical quadruped position. Although in the past it has been generally accepted that the multifidus co- contracts during abdominal contraction strategies, only one study was identified that demonstrated superficial multifidus co-contraction during these abdominal activation strategies (Matthijs et al., 2014). However, this co-contraction was only observed in the superficial multifidus fibers. Therefore, the purpose of this study was to determine if deep and superficial multifidus fibers demonstrate different co-contraction patterns during volitional abdominal contractions. Moreover, the study aimed to determine if co- contraction differences exist among abdominal activation strategies used in clinical practice. It was hypothesized that a difference would exist between deep and superficial multifidus co-contraction during VPAC and that ADIM and ABM would both result in greater deep multifidus co-contraction than resting.

Methods

Experimental Design A two-factor within-subjects repeated measures design was used to examine superficial and deep multifidus fiber co-contraction during abdominal drawing in 64 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 maneuver (ADIM), abdominal bracing maneuver (ABM), and resting state in standing and quadruped positions.

Subjects A convenience sample of individuals between the ages of 18 and 65 years old was recruited for this study through two local universities, as well as the general public. The sample consisted of individuals without a reported history of LBP. Exclusion criteria included 1) A history of LBP causing them to seek professional medical attention or to limit their ability to participate in activities of daily living within the previous two years; 2) Any diagnosed and presently active abdominal, respiratory, or gastrointestinal condition; 3) Self-report of pregnancy; 4) Significant spinal deformities or a diagnosed condition that includes scoliosis, spina bifida, tumors, present fractures, and/or rheumatologic disorders; 5) Current urinary tract infection; 6) A history of lumbar or abdominal surgery; 7) Current use of anticoagulant medications or blood clotting disorders; 8) Inability to voluntary recruit abdominal muscles during ADIM and ABM as observed by investigator palpation; and 9) Inability to assume a quadruped position for any reason. No studies were identified within the literature that directly assessed the contraction magnitude differences between the deep and superficial multifidus during voluntary contractions. Studies assessing multifidus thickness changes using functional magnetic resonance imaging and ultrasound imaging during contraction (Dickx et al., 2008; Wallwork et al., 2009) and CSA differences between LBP patients and asymptomatic controls were reported (Bouche et al., 2011; Chan et al., 2012; Hides, Gilmore, Stanton, & Bohlscheid, 2008a) with variable Cohen’s d effect sizes ranging from 0.31 - 3.67. Due to this wide effect size range and previous studies demonstrating different onset timing for deep and superficial fibers, a large effect size (d = 0.8 OR f = 0.4) was chosen for prospective power analysis including sample size calculations. With a desired power of 80% (1-beta = 80%), alpha = 0.05 and an estimated effect size of f = 0.4, a sample size of 26 were required (Portney & Watkins, 2009). To account for attrition a sample size of 30 subjects were recruited for this study.

65 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Testing Procedures Subjects were asked to read and sign an informed consent form that had been approved by the affiliated Universities. Subjects then viewed a short video explaining the experimental procedures. After watching the video, subjects completed a demographic and medical history questionnaire to determine eligibility for this study, followed by three self-reported surveys including the Oswestry Disability Index (ODI) (Fairbank et al., 1980), the Tampa Scale of Kinesiophobia (TSK) (Miller et al., 1991), and the Lumbar Spine Instability Questionnaire (LSIQ) (Cook et al., 2006; Macedo et al., 2014). Following completion of the surveys, subjects were trained to complete the ADIM and ABM contractions. For ADIM training, patients were instructed to “pull the belly in as if they were putting on a tight pair of pants”. For ABM training, subjects were instructed to “tighten your stomach as if you were about to get hit in the stomach”. Appropriate ADIM technique was confirmed by an investigator through visualization of the lower abdominal muscles moving inward or manual palpation just medial to the Anterior Superior Iliac Spine (ASIS) when contractions were not easily visible. Following abdominal contraction training, subjects were fitted with surface and indwelling EMG sensors (Figure 4.1). Abdominal EMG sensors were placed on the right external oblique (14 cm lateral to the midline one cm below the umbilicus) and internal oblique (two cm below the level of the ASIS just medial and superior to the inguinal ligament) (Boccia & Rainoldi, 2014; Huebner et al., 2015). A submaximal voluntary contraction normalization of the abdominal muscles (IO and EO) was performed with the subject in a supine hook lying position with the hips flexed approximately 45 degrees and the knees flexed approximately 90 degrees. The subject was instructed to raise both legs off the supporting surface approximately one cm and hold this position for seven seconds (Dankaerts et al., 2004). Surface EMG sensors were then placed bilaterally over the superficial multifidus (one cm lateral to the spinous process at L5 in a slightly superomedial-to-inferolateral direction), longissimus thoracis (at L1 three cm lateral to midline in a cranial to caudal direction) (Lariviere et al., 2002). To record myoelectrical activity from the deep multifidus fibers, indwelling electrodes were inserted four cm lateral to the L5 spinous

66 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 process in a ventral and medial direction until the investigator felt contact with the lamina (Moseley et al., 2002). The fine wires were then connected to spring contact sensors with a local reference sensor placed over the most prominent aspect of the ipsilateral iliac crest. For submaximal normalization of back muscles, the subject was placed in a prone position with both knees flexed to 90 degrees. The subject was then instructed to lift both knees off the supporting surface approximately five cm and hold for seven seconds (Dankaerts et al., 2004). Submaximal contraction EMG signals were visually inspected to ensure myoelectrical activity recording. Following normalization trials, subjects completed all co-contraction testing in standing and quadruped positions. Subjects performed three variations of abdominal contraction: 1) Resting, 2) ADIM contraction, and 3) ABM contraction. Each contraction was held for seven seconds and was repeated three times. Condition order was randomized using randomization without replacement. To limit the effect of position order, each subject was randomized to begin either in a standing or quadruped position followed by all trials in that position. To limit subject position movement, all standing contractions were performed together and all quadruped contractions were performed together. All muscle activity was recorded using a 16-channel Delsys Trigno system and all muscles were recorded at 1926 Hz. The EMG surface sensors (Trigno Flex sensors) have a built-in butterworth band pass filter giving the sensor a frequency response from 20 to 450 Hz (10-850 for fine wire EMG) with less than 2.5 microvolt baseline noise. The common mode rejection ratio was >80dB.

Data reduction All raw myoelectrical data were imported into a custom MATLAB (The Mathworks, Natick, MA) data reduction program. The two indwelling signals (from deep multifidus fibers) were filtered using a 60Hz notch filter to reduce unwanted environmental noise. A 2-second sample (seconds 3-5) was extracted from each submaximal normalization and testing trial. A built-in MATLAB RMS function was used to calculate the root mean square averages (RMS) for each trial. The RMS values were averaged across the three repeated trials for each condition and were subsequently

67 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 compared to sub-MVC reference activity to create a percentage of sub-MVC for each trial.

Statistical Analysis Descriptive statistics (mean ± SD) were calculated for all demographic variables including age, weight and height for all subjects. Dependent variable data were tested for normality using Shapiro-Wilk test, skewness, and kurtosis. Data normality was operationally identified as at least two of the three tests indicating normality (non- significant Shapiro-Wilk test, skewness between -2 and +2, and kurtosis between -2 and +2). Based on normality testing, all co-contraction dependent variables were found to be in violation of 2 or more of the previously stated values, indicating non-normal distribution of the dependent variables. As a result, robust statistics were used to analyze for differences in trimmed mean values (Wilcox, 2016). Winsorized means (20% trimmed) were calculated for all dependent variables. Bootstrapping was performed 2,000 times and 95% confidence intervals were calculated from the 2,000 bootstrapped mean values. These values were used for all statistical comparisons. To illustrate the effect magnitude, a robust heteroscedastic approach to measuring effect size (x - ksi) was used (Wilcox & Tian, 2011). The Ksi effect size indicates the strength of association between predicted variation and actual variation based on effect of independent variable. Using this approach, an effect of x = 0.15 is considered small, x = 0.35 is medium, and x = 0.5 is large (Wilcox & Tian, 2011). Two 2x3 repeated measures ANOVAs were performed to assess main effects of multifidus depth and abdominal contraction strategy and interactions between these variables. Separate ANOVAs were completed for the analysis in standing and quadruped positions. Alpha values were set at 0.05. All subject baseline characteristics were calculated using IBM SPSS version 25.0 (Armonk, NY). All dependent variable descriptive statistics and robust analyses were calculated using R software.

Results A total of 30 subjects (18 Males and 12 Females) without a recent history of low back pain agreed to participate and completed all testing. Mean subject age was 37.8 (SD 68 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

14.46) and the mean body mass index was 24.30 (SD 3.56) kg/m2. No significant differences (P>0.05) were identified between right and left multifidus muscle at either the superficial or deep fibers for any contraction condition in any position. Therefore, right and left sides of the multifidus were combined for all analyses. Muscular contraction values expressed as Winsorized trimmed means and 95% bootstrapped confidence intervals of the percentage of submaximal RMS values were calculated (Table 4.1). Deep and superficial multifidus fibers did not differ in their co-contraction activity during any of the three abdominal contraction strategies. This similarity between deep and superficial was consistent across standing and quadruped positions. Robust ANOVAs revealed no significant interactions between the three different abdominal contraction strategies and multifidus depth (deep vs. superficial) in either standing (p=0.169) (Table 4.2) or quadruped positions (p=0.758) (Table 4.3). No significant differences were observed in co-contraction between deep and superficial multifidus depth during any of the three abdominal activation strategies in either standing (p=0.317) (Figure 4.2) or quadruped positions (p=0.681) (Figure 4.3). Both ADIM and ABM resulted in greater multifidus co-contraction than the resting condition. A significant main effect of abdominal activation strategy was identified. Post Hoc analysis revealed that compared to the resting condition, ADIM (p<.001) and ABM (p<.001) contractions each resulted in significantly greater multifidus co-contraction amplitudes in both standing and quadruped positions. However, no differences were found between ADIM and ABM in standing (p=0.738) or quadruped (p=0.741).

Discussion The purpose of this paper was to determine if there is a difference in co- contraction activity between the deep and superficial fibers of the multifidus. An additional purpose was to assess the amount of multifidus co-contraction during resting, ADIM, and ABM contractions. The primary finding within this study is that both ADIM and ABM produce significantly greater superficial and deep multifidus co-contraction compared to the resting condition in both standing and quadruped positions. No significant difference was identified between ADIM and ABM contractions for

69 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 multifidus co-contraction level in either position. Additionally, no differences were identified in co-contraction activity between the superficial and deep multifidus fibers. This study is the first to quantify deep and superficial multifidus co-contraction response during volitional abdominal contractions including both the ADIM and ABM. One previous study did identify that superficial multifidus co-contraction occurred during these same volitional contractions (Matthijs et al., 2014). However, multifidus co- contraction was dichotomized as “Yes” or “No” and only superficial multifidus was assessed. The findings of the current study agree with these previously published results in identifying that the superficial multifidus does co-contract during volitional abdominal contractions. Matthijs et al. (2014) observed a greater frequency of multifidus co- contraction responses during the ABM compared to the ADIM in the supine position. In quadruped and standing positions, no difference in frequency was observed (Matthijs et al., 2014). The current study supports this assessment by finding no difference between multifidus co-contraction amplitudes between ADIM and ABM contractions. These current findings support the theory that ADIM and ABM contractions can be used to increase spinal stability through multifidus muscle co-contraction and that this can be accomplished across multiple positions. Matthijs and colleagues (2014) proposed two potential methods of using this co-contraction response: (1) to increase segmental spinal stability in preparation for functional activities and (2) as a method to create a multifidus contraction during rehabilitative exercises. The co-contraction of both deep and superficial multifidus fibers during abdominal contractions supports that idea that these contractions could be used to increase spinal stability prior to functional activities as well as to facilitate multifidus contraction during rehabilitation exercises. Although this study adds to the evidence that there is a co-contraction during voluntary abdominal contractions, observing multifidus co-contraction during an ADIM or ABM does not necessarily explain why the multifidus co-contracts. Three possible explanations may describe why this co-contraction occurs. These three reasons are not necessarily mutually exclusive. One possible explanation is that the ABM and ADIM contractions include multifidus contraction within the motor program and it is inherently part of the contraction. Since the TrA alone has only limited ability to provide spinal

70 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 stability (Grenier & McGill, 2007), concurrent multifidus muscular contribution to spinal stability may be necessary. The second possible explanation is that there is an anatomical connection between the abdominal muscles through the common tendon of the TrA/IO and the paraspinal compartment. Vleeming and colleagues (2014) supply further evidence for TrA and multifidus co-contraction from an anatomical perspective. These authors demonstrate that activation of the common tendon of TrA/IO without paraspinal muscular contraction results in anterior and lateral movement of the paraspinal compartment resulting in insufficient tension production capability of the TrA/IO complex. Similarly, contraction of the paraspinal muscles in the absence of TrA/IO contraction resulted in a large posterior displacement of the paraspinal muscles. However, when both the paraspinal muscles and the TrA/IO are contracted, tension is channeled through the posterior layer of the thoracolumbar fascia producing a “girdling” of the paraspinal muscles (Vleeming et al., 2014). A third explanation for the observed co-contraction includes a balancing of muscular forces. Contraction of the abdominal muscles in the absence of activation of muscles posterior to the axis of movement (the spine) would result in a net movement into flexion. To maintain a static position, it may be necessary to balance the total moment of the muscles contracting posterior to the spine with the total moment anterior to the spine (Bergmark, 1989). Baek and colleagues observed increased superficial and deep multifidus activity with neuromuscular electrical stimulation of the TrA (Baek, Cho, et al., 2014b). Similarly, in another study Baek and colleagues observed increased thickness of the external oblique, internal oblique, and TrA with superficial multifidus stimulation (Baek, Ahn, et al., 2014a). Together these two studies indicate the possibility that co-contraction may travel in both directions in individuals without LBP and supports the idea of co-contraction to balance extensor and flexor muscle moments. In a sample of subjects with low back pain, Hides et al., (2011) found that the ability to produce a good voluntary contraction of the lumbar multifidus was related to the subject’s ability to produce a good voluntary contraction of the transverse abdominis.

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Multiple studies have observed neuromotor distinctions between the deep and superficial multifidus fibers (MacDonald et al., 2009; Moseley et al., 2002; 2003). Conversely, this study observed no differences in co-contraction intensity between the deep and superficial fiber systems during volitional abdominal contractions. This may be due to the differences in stability requirements among the tasks within the different studies due to the relatively dynamic nature of the activities. These previous studies included either an internal (rapid arm movement) or external (weight dropped into a bucket in the subjects’ hands) perturbation, whereas the subjects in the current study were performing abdominal contractions in static positions. MacDonald et al. (2006) reviewed a number of studies that demonstrated that the deep multifidus is tonically active while the superficial multifidus fibers are phasically active. However, during no contraction (resting) conditions, no difference was observed between deep and superficial multifidus activity, indicating that there is at least a baseline tone in both muscles during standing and quadruped static positions.

Limitations This study was completed in a sample of healthy individuals without a recent history of LBP. However, it is necessary to determine if deep and superficial multifidus co-contraction exists in those without LBP before this can be assessed in individuals who have LBP. The ADIM and ABM contraction intensity were not directly controlled, leading to high variability within the subjects. However, it was important to allow the subjects to self-select a contraction intensity in order to emphasize practical application. Placement of the indwelling electrodes in the deep multifidus fibers was not visually confirmed with ultrasound. However, placement methods were used that had previously been published by other authors and visually confirmed using ultrasound. Additionally, the electrodes were inserted until contact with the lamina was felt by the investigator inserting the needle.

Conclusion Both the superficial and deep multifidus fibers co-contract significantly more during ADIM and ABM voluntary contractions when compared to a resting condition. However, no differences were observed between the co-contraction intensity between the 72 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 deep and superficial multifidus fibers in this sample of individuals without a history of low back pain in the past two years. Since no multifidus co-contraction differences were observed between ADIM and ABM, clinicians can use either ADIM or ABM to facilitate both deep and superficial multifidus co-contraction in standing and quadruped positions. The choice to use either ADIM or ABM may be patient-specific and be determined by which strategy the patient prefers.

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References A Sirca, V. K. (1985). The fibre type composition of thoracic and lumbar paravertebral muscles in man. Journal of Anatomy, 141, 131–137. Baek, S. O., Ahn, S. H., Jones, R., Cho, H. K., Jung, G. S., Cho, Y. W., & Tak, H. J. (2014a). Activations of deep lumbar stabilizing muscles by transcutaneous neuromuscular electrical stimulation of lumbar paraspinal regions. Annals of Rehabilitation Medicine, 38(4), 506–8. http://doi.org/10.5535/arm.2014.38.4.506 Baek, S. O., Cho, H. K., Jung, G. S., Son, S. M., Cho, Y. W., & Ahn, S. H. (2014b). Verification of an optimized stimulation point on the abdominal wall for transcutaneous neuromuscular electrical stimulation for activation of deep lumbar stabilizing muscles. The Spine Journal: Official Journal of the North American Spine Society, 14(9), 2178–2183. http://doi.org/10.1016/j.spinee.2014.02.016 Bergmark, A. (1989). Stability of the lumbar spine: a study in mechanical engineering. Acta Orthopaedica. Boccia, G., & Rainoldi, A. (2014). Innervation zones location and optimal electrodes position of obliquus internus and obliquus externus abdominis muscles. Journal of Electromyography and Kinesiology, 24(1), 25–30. http://doi.org/10.1016/j.jelekin.2013.10.017 Bogduk, N., Macintosh, J. E., & Pearcy, M. J. (1992). A universal model of the lumbar back muscles in the upright position. Spine, 17(8), 897–913. Bouche, K. G., Vanovermeire, O., Stevens, V. K., Coorevits, P. L., Caemaert, J. J., Cambier, D. C., et al. (2011). Computed tomographic analysis of the quality of trunk muscles in asymptomatic and symptomatic lumbar discectomy patients. BMC Musculoskeletal Disorders, 12(1), 65. http://doi.org/10.1186/1471-2474-12-65 Chan, S.-T., Fung, P.-K., Ng, N.-Y., Ngan, T.-L., Chong, M.-Y., Tang, C.-N., et al. (2012). Dynamic changes of elasticity, cross-sectional area, and fat infiltration of multifidus at different postures in men with chronic low back pain. The Spine Journal: Official Journal of the North American Spine Society, 12(5), 381–388. http://doi.org/10.1016/j.spinee.2011.12.004 Cook, C., Brismée, J.-M., & Sizer, P. S., Jr. (2006). Subjective and objective descriptors of clinical lumbar spine instability: A Delphi study. Manual Therapy, 11(1), 11–21. http://doi.org/10.1016/j.math.2005.01.002 Costi, J. J., Stokes, I. A., Gardner-Morse, M., Laible, J. P., Scoffone, H. M., & Iatridis, J. C. (2007). Direct measurement of intervertebral disc maximum shear strain in six degrees of freedom: Motions that place disc tissue at risk of injury. Journal of Biomechanics, 40(11), 2457–2466. http://doi.org/10.1016/j.jbiomech.2006.11.006 Crisco, J. J., Panjabi, M. M., Yamamoto, I., & Oxland, T. R. (1992). Euler stability of the human ligamentous lumbar spine. Part II: Experiment. Clinical Biomechanics (Bristol, Avon), 7(1), 27–32. http://doi.org/10.1016/0268-0033(92)90004-N

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Dankaerts, W., O’Sullivan, P. B., Burnett, A. F., Straker, L. M., & Danneels, L. A. (2004). Reliability of EMG measurements for trunk muscles during maximal and sub-maximal voluntary isometric contractions in healthy controls and CLBP patients. Journal of Electromyography and Kinesiology, 14(3), 333–342. http://doi.org/10.1016/j.jelekin.2003.07.001 Dickx, N., Cagnie, B., Achten, E., Vandemaele, P., Parlevliet, T., & Danneels, L. (2008). Changes in lumbar muscle activity because of induced muscle pain evaluated by muscle functional magnetic resonance imaging. Spine, 33(26), E983–9. http://doi.org/10.1097/BRS.0b013e31818917d0 Dickx, N., Cagnie, B., Achten, E., Vandemaele, P., Parlevliet, T., & Danneels, L. (2010). Differentiation between deep and superficial fibers of the lumbar multifidus by magnetic resonance imaging. European Spine Journal, 19(1), 122–128. http://doi.org/10.1007/s00586-009-1171-x Fairbank, J. C. T., Couper, J., Davies, J., & OBrien, J. (1980). The Oswestry Low Back Pain Questionnaire. Physiotherapy, 66(8), 271–273. Grenier, S. G., & McGill, S. M. (2007). Quantification of Lumbar Stability by Using 2 Different Abdominal Activation Strategies. Archives of Physical Medicine and Rehabilitation, 88(1), 54–62. http://doi.org/10.1016/j.apmr.2006.10.014 Hides, J., Gilmore, C., Stanton, W., & Bohlscheid, E. (2008). Multifidus size and symmetry among chronic LBP and healthy asymptomatic subjects. Manual Therapy, 13(1), 43–49. http://doi.org/10.1016/j.math.2006.07.017 Hides, J., Stanton, W., Dilani Mendis, M., & Sexton, M. (2011). The relationship of transversus abdominis and lumbar multifidus clinical muscle tests in patients with chronic low back pain. Manual Therapy, 16(6), 573–577. http://doi.org/10.1016/j.math.2011.05.007 Hides, J., Wilson, S., Stanton, W., McMahon, S., Keto, H., McMahon, K., et al. (2006). An MRI investigation into the function of the transversus abdominis muscle during “drawing-in” of the abdominal wall. Spine, 31(6), E175–8. http://doi.org/10.1097/01.brs.0000202740.86338.df Huebner, A., Faenger, B., Schenk, P., Scholle, H.-C., & Anders, C. (2015). Alteration of Surface EMG amplitude levels of five major trunk muscles by defined electrode location displacement. Journal of Electromyography and Kinesiology, 25(2), 214– 223. http://doi.org/10.1016/j.jelekin.2014.11.008 Jemmett, R. S., MacDonald, D. A., & Agur, A. M. R. (2004). Anatomical relationships between selected segmental muscles of the lumbar spine in the context of multi- planar segmental motion: a preliminary investigation. Manual Therapy, 9(4), 203– 210. http://doi.org/10.1016/j.math.2004.07.006 Lariviere, C., Arsenault, A. B., Gravel, D., & Gagnon, D. (2002). Evaluation of measurement strategies to increase the reliability of EMG indices to assess back muscle fatigue and recovery. Journal of Electromyography and Kinesiology, 12(2), 91–102. http://doi.org/10.1016/S1050-6411(02)00011-1 75 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

MacDonald, D. A., Lorimer Moseley, G., & Hodges, P. W. (2006). The lumbar multifidus: Does the evidence support clinical beliefs? Manual Therapy, 11(4), 254– 263. http://doi.org/10.1016/j.math.2006.02.004 MacDonald, D., Moseley, G. L., & Hodges, P. W. (2009). Why do some patients keep hurting their back? Evidence of ongoing back muscle dysfunction during remission from recurrent back pain. Pain, 142(3), 183–188. http://doi.org/10.1016/j.pain.2008.12.002 Macedo, L. G., Maher, C. G., Hancock, M. J., Kamper, S. J., McAuley, J. H., Stanton, T. R., et al. (2014). Predicting response to motor control exercises and graded activity for patients with low back pain: preplanned secondary analysis of a randomized controlled trial. Physical Therapy, 94(11), 1543–1554. http://doi.org/10.2522/ptj.20140014 Macintosh, J. E., & Bogduk, N. (1986). The biomechanics of the lumbar multifidus. Clinical Biomechanics (Bristol, Avon), 1(4), 205–213. http://doi.org/10.1016/0268- 0033(86)90147-6 Macintosh, J. E., Valencia, F., Bogduk, N., & Munro, R. R. (1986). The morphology of the human lumbar multifidus. Clinical Biomechanics (Bristol, Avon), 1(4), 196–204. http://doi.org/10.1016/0268-0033(86)90146-4 Matthijs, O. C. G., Dedrick, G. S., James, C. R., Brismée, J.-M., Hooper, T. L., McGalliard, M. K., & Sizer, P. S. (2014). Co-contractive activation of the superficial multifidus during volitional preemptive abdominal contraction. PM&R: the Journal of Injury, Function, and Rehabilitation, 6(1), 13–21. http://doi.org/10.1016/j.pmrj.2013.08.606 McGill, S. M., & Norman, R. W. (1986). Partitioning of the L4-L5 dynamic moment into disc, ligamentous, and muscular components during lifting. Spine, 11(7), 666–678. McGill, S. M., Grenier, S., Kavcic, N., & Cholewicki, J. (2003). Coordination of muscle activity to assure stability of the lumbar spine. Journal of Electromyography and Kinesiology, 13(4), 353–359. http://doi.org/10.1016/S1050-6411(03)00043-9 Miller, R. P., Kori, S. H., & Todd, D. D. (1991). The Tampa Scale. Tampa, Fla. Moseley, G. L., Hodges, P. W., & Gandevia, S. C. (2002). Deep and superficial fibers of the lumbar multifidus muscle are differentially active during voluntary arm movements. Spine, 27(2), E29–36. Moseley, G. L., Hodges, P. W., & Gandevia, S. C. (2003). External perturbation of the trunk in standing humans differentially activates components of the medial back muscles. The Journal of Physiology, 547(Pt 2), 581–587. http://doi.org/10.1113/jphysiol.2002.024950 Portney, L. G., & Watkins, M. P. (2009). Foundations of clinical research: applications to practice. Pearson Education, Inc.

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Rosatelli, A. L., & Ravichandiran, K. (2008). Three-dimensional study of the musculotendinous architecture of lumbar multifidus and its functional implications. Clinical Anatomy, 21(6), 539-46. Stanton, T., & Kawchuk, G. (2008). The effect of abdominal stabilization contractions on posteroanterior spinal stiffness. Spine, 33(6), 694–701. http://doi.org/10.1097/BRS.0b013e318166e034 Urquhart, D. M., Hodges, P. W., & Story, I. H. (2005a). Postural activity of the abdominal muscles varies between regions of these muscles and between body positions. Gait & Posture, 22(4), 295–301. http://doi.org/10.1016/j.gaitpost.2004.09.012 Urquhart, D. M., Hodges, P. W., Allen, T. J., & Story, I. H. (2005b). Abdominal muscle recruitment during a range of voluntary exercises. Manual Therapy, 10(2), 144–153. http://doi.org/10.1016/j.math.2004.08.011 Vleeming, A., Schuenke, M. D., Danneels, L., & Willard, F. H. (2014). The functional coupling of the deep abdominal and paraspinal muscles: the effects of simulated paraspinal muscle contraction on force transfer to the middle and posterior layer of the thoracolumbar fascia. Journal of Anatomy, 225(4), 447–462. http://doi.org/10.1111/joa.12227 Wallwork, T. L., Stanton, W. R., Freke, M., & Hides, J. A. (2009). The effect of chronic low back pain on size and contraction of the lumbar multifidus muscle. Manual Therapy, 14(5), 496–500. http://doi.org/10.1016/j.math.2008.09.006 Wilcox, R. (2016). Introduction to Robust Estimation and Hypothesos Testing (Fourth). Waltham, MA: Academic Press. Wilcox, R. R., & Tian, T. S. (2011). Measuring effect size: a robust heteroscedastic approach for two or more groups. Journal of Applied Statistics, 38(7), 1359–1368. http://doi.org/10.1080/02664763.2010.498507

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Table 4.1. Contraction RMS values in standing and quadruped positions Resting ADIM ABM Standing IO 45.91 (37.13-56.73) 165.12 (130.17-210.21) 132.35 (102.10-182.45) EO 15.66 (12.3-19.81) 54.5 (44.85-63.80) 60.38 (49.20-72.0) SMF 12.16 (9.79-14.73) 27.19 (20.73-33.65) 29.15 (22.54-34.96) DMF 11.74 (8.76-14.42) 25.52 (16.42-32.04) 26.25 (18.64-32.43) Quadruped IO 19.38 (16.60-24.40) 99.44 (78.09-129.37) 90.85 (70.35-119.57) EO 14.09 (11.35-17.42) 40.79 (34.53-49.67) 48.23 (40.40-57.67) SMF 11.33 (7.05-14.59) 15.5 (10.78-19.32) 16.72 (11.61-21.47) DMF 10.56 (5.27-18.49) 15.17 (8.018-26.54) 19.74 (10.69-30.15) All values presented are Winsorized trimmed means with bootstrapped 95% confidence intervals and represent the percentage of root mean square submaximal contraction. Abbreviations: IO, internal oblique; EO, external oblique; SMF, superficial multifidus; DMF, deep multifidus.

Table 4.2. ANOVA results in standing position Comparison p-value Effect Size (x) Interaction p = .169 N/A MF Depth p = .317 N/A Contraction p = .008* N/A Post Hoc Test Results DMF vs. SMF p = .141 0.07 (Rest), 0.08 (ADIM), 0.14 (ABM) Rest vs. ADIM p < .001* 0.61 (DMF), 0.77 (SMF) Rest vs. ABM p < .001* 0.66 (DMF), 0.77 (SMF) ADIM vs. p = .738 0.05 (DMF), 0.13 (SMF) ABM Abbreviations: MF Depth, multifidus fiber depth; ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver; SMF, superficial multifidus; DMF, deep multifidus. * indicates significant differences.

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Table 4.3. ANOVA results in quadruped position Comparison p-value Effect Size (e) Interaction p = .758 N/A MF Depth p = .681 N/A Contraction p = .047* N/A Post Hoc Test Results DMF vs. SMF p = .586 0.24 (Rest), 0.003 (ADIM), .05 (ABM) Rest vs. ADIM p < .001* 0.29 (DMF), 0.48 (SMF) Rest vs. ABM p < .001* 0.30 (DMF), 0.43 (SMF) ADIM vs. ABM p = .741 0.04 (DMF), 0.009 (SMF) Abbreviations: MF Depth, multifidus fiber depth; ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver; SMF, superficial multifidus; DMF, deep multifidus. * indicates significant differences.

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Figure 4.1. EMG sensor placement for extensor muscles.

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Figure 4.2. Abdominal contraction x multifidus depth interaction in standing. Abbreviations: %MVC, percentage of root mean squared submaximal voluntary reference contraction; DMF, deep multifidus; SMF, superficial multifidus; ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver.

Figure 4.3. Abdominal contraction x multifidus depth interaction in quadruped. Abbreviations: %MVC, percentage of root mean squared submaximal voluntary reference contraction; DMF, deep multifidus; SMF, superficial multifidus; ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver.

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CHAPTER V

MULTIFIDUS CO-CONTRACTION DURING VOLITIONAL ABDOMINAL CONTRACTIONS IN INDIVIDUALS WITH A RECENT HISTORY OF LOW BACK PAIN

Abstract Objective: The objective of this study was to determine the effect of a low back pain (LBP) history on deep and superficial multifidus co-contraction during volitional abdominal contractions. Additionally, this study aimed to determine the influence of position and multifidus depth on the co-contraction response. Design: Quasi-experimental repeated measures with between subjects and within- subjects comparisons Setting: University Research Lab Methods: Thirty subjects with a recent LBP history (36.83 ± 13.79 years of age) and 30 subjects without a recent history of low back pain (37.8 ± 14.46 years of age) were included in this study. Each subject completed three trials each of the abdominal bracing maneuver (ABM), abdominal drawing-in maneuver (ADIM), and resting in standing and quadruped positions. Root mean square EMG activity of the superficial and deep multifidus fibers was normalized to submaximal reference contractions and averaged across each of the three repeated trials. Results: ANOVAs revealed no statistically significant differences between subjects with a LBP history and healthy controls. Within the HxLBP group, the ADIM and ABM resulted in significantly greater multifidus activity than the resting abdominal condition in both standing and quadruped positions (p<0.001). When comparing positions in the HxLBP group, multifidus co-contraction was significantly greater in standing than quadruped during resting (p=0.016), ADIM (p<0.001), and ABM (p<0.001). Significant differences in co-contraction activity were observed when comparing deep and superficial multifidus muscles during standing AIDM (p=0.04), quadruped resting (p<0.001), and quadruped ADIM (p=0.022). However, these differences were not

82 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 significant during standing resting (p=0.339), standing ABM (p=0.079), and quadruped ABM (p=0.111). Conclusion: Subjects with a LBP history are able to use both ADIM and ABM strategies to facilitate multifidus contraction similar to individuals without a recent history of LBP. Additionally, abdominal contractions in the functional position of standing resulted in greater multifidus co-contraction versus the same in a quadruped position.

Introduction Low back pain is an almost universal disorder with 70-85% of all individuals experiencing LBP at some point throughout their lifetime (Andersson, 1999; van Tulder et al., 2006). At any point in time, approximately 30% of individuals are experiencing LBP (Andersson, 1999; Deyo et al., 2006), making it the most common form of pain reported by adults in the United States (Deyo et al., 2006). Although LBP affects all individuals differently, approximately 60-70% of back pain sufferers will recover within six weeks and 80-90% will recover within 12 weeks (Andersson, 1999). Despite the fact that these numbers are encouraging and may support a historical belief that LBP is a self-limiting and benign disorder (Indahl et al., 1995; Waddell, 1987), individuals who experiences acute LBP are four times more likely to experience recurrence in the following year compared to those who have not experienced LBP (Hestbaek et al., 2003). One possible explanation for this high LBP recurrence rate is a change in lumbar muscular control resulting from the previous LBP episode. A number of studies have demonstrated decreased or delayed muscular activation during LBP episodes, potentially increasing the subject’s risk for spinal buckling and subsequent pain and structural damage (Cholewicki & McGill, 1996; Descarreaux et al., 2007; MacDonald et al., 2009). However, other studies have demonstrated increased reactive muscular activity in superficial back muscles in individuals with LBP (van Dieën, Cholewicki, & Radebold, 2003a). Although deep and superficial multifidus muscles are both innervated by the medial branch of the dorsal ramus, studies have demonstrated that electromyographical (EMG) activation difference exist between these fiber systems (MacDonald et al., 2006;

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Moseley et al., 2003). This differential activation between the deep and superficial fibers supports the belief that the superficial multifidus controls spinal orientation and position while the deep fibers aid in controlling intersegmental motion (Moseley et al., 2002). It could then be reasoned that muscular activations intended to stabilize the spine may result in differential co-contraction of the deep and superficial fibers. While it has been shown that the superficial multifidus fibers co-contract during ADIM and ABM strategies, it is unknown whether or not deep multifidus fibers contract as well. The need to specifically study deep multifidus co-contraction is further supported due to the differential activation of deep and superficial multifidus fibers during functional activities (MacDonald et al., 2010; Moseley et al., 2002; 2003). Additionally, although Matthijs et al (2014) demonstrated superficial multifidus co-contraction during the ADIM and ABM contractions, this was only demonstrated in individuals without a history of LBP. Therefore, the purpose of this study was to determine the effect of a LBP history on the ability of lumbar stabilizing muscles to co-contract with abdominal muscle activation compared to individuals without a LBP history. An additional purpose of this study was to determine if co-contraction differences exist among abdominal activation strategies and common positions used in clinical practice in individuals with a history of LBP. It was hypothesized that subjects with a history of LBP would exhibit multifidus co-contraction in response to VPAC but this co-contraction activity would not be as high as the co-contraction level found in subjects without a LBP history. A second hypothesis was that subjects with a history of LBP would demonstrate no difference in multifidus co-contractile response during ADIM and ABM, while resting would not result in multifidus co-contraction. A third hypothesis was that both ADIM and ABM would result in multifidus co-contraction in standing and quadruped positions, with greater co- contraction produced in standing for HxLBP subjects. Methods Experimental Design A mixed method, multi-factorial design was used to determine the influence of multifidus depth, abdominal activation strategy, position, and LBP history on multifidus co-contraction activity level.

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Subjects A convenience sample of individuals between the ages of 18-65 years old was recruited through two local universities and the general public. The sample consisted of two groups: 1) individuals with no history of LBP within the previous two years and 2) individuals with a history of LBP (HxLBP) within the previous two years. For the purpose of this study, the presence of LBP was operationally defined as one or more episodes of LBP of sufficient intensity to cause the subject to either seek medical or allied health intervention or for the LBP to limit the ability to participate in activities of daily living. Exclusion criteria for both groups included: 1) any diagnosed and presently active abdominal, respiratory, or gastrointestinal condition, 2) self-report of pregnancy, 3) significant spinal deformities or a diagnosed condition that includes scoliosis, spina bifida, tumors, present fractures, and/or rheumatologic disorders, 4) current urinary tract infection, 5) a history of lumbar or abdominal surgery, 6) current use of anticoagulant medications or blood clotting disorders, 7) inability to voluntary recruit abdominal muscles during ADIM and ABM as observed by investigator palpation, and 8) inability to assume a quadruped position for any reason. No studies were identified that directly compared multifidus co-contraction differences between individuals with a history of LBP and those without a history. As a result, studies measuring multifidus thickness characteristics including thickness change during contraction (Dickx et al., 2008; Wallwork et al., 2009) and cross-sectional area differences between LBP patients and healthy controls (Bouche et al., 2011; Chan et al., 2012; Hides, Gilmore, Stanton, & Bohlscheid, 2008a) were examined for establishing the effect size estimates in the current study. However, effect sizes within these identified studies varied significantly (d=0.31-3.67). As a result of this variability, a large effect size (d = 0.8 OR f = 0.4) was chosen for prospective sample size calculations. With alpha = 0.05, beta = 0.20, and an estimated effect size of f = 0.4, it was determined that a sample size of 26 was needed for each group (Portney & Watkins, 2009). To account for attrition, it was determined that 30 subjects would be recruited for each group.

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Testing Procedures Subjects were asked to read and sign an IRB approved informed consent form. Subjects then watched a brief video informing them of the experimental procedures. After watching the video, subjects were asked to complete a medical history questionnaire and three self-reported questionnaires including the Oswestry Disability Index (ODI), the Tampa Scale of Kinesiophobia (TSK) and the Lumber Spine Instability Questionnaire (LSIQ). The ODI is a 10-item questionnaire with each item scored from 0-5 with 0 indicating no disability and 5 indicating maximum disability for that item (Fairbank et al., 1980). Scores are converted to a percentage representing percentage disability. The ODI has demonstrated good test-retest reliability (Chiarotto et al., 2016) and excellent construct validity when compared to LBP patients’ pain and subjective feeling of improvement (Haro et al., 2008). The TSK is a 17-item questionnaire designed to measure a person’s fear of movement (Miller et al., 1991). Each item is scored from one to four with one representing strongly disagree and four representing strongly agree. Scores can range from 17 to 68, with higher scores representing greater kinesiophobia. Reliability of the full 17 point scale has been shown to be high for both chronic LBP and acute LBP subjects (French et al., 2007; Swinkels-Meewisse et al., 2003) and the instrument can be clinically beneficial for identifying pain-related fear in acute LBP patients. The LSIQ, originally developed as a set of 15 subjective and 14 objective factors for identifying clinical lumbar instability, was modified by Macedo et al (2014) to include only the 15 subjective factors. Each factor is scored as present or absent with a sum total score of all present factors. Macedo et al. (2014) demonstrated that subjects with higher instability levels (≥9/15) responded better to motor control exercises while those with lower instability levels (<9/15) responded better to a graded exercise protocol. More recently Saragiatto et al. (2018) demonstrated that the LSIQ is a unidimensional measure with adequate test-retest reliability. However, the authors demonstrated that the scale has poor internal consistency, unclear construct validity, and did not function as an interval-level measure (Saragiotto et al., 2018).

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After survey completion, all subjects were trained how to perform the ADIM and ABM contractions. For the ADIM contraction, subjects were instructed to “pull the belly in as if they were putting on a tight pair of pants” and for the ABM subjects were instructed to “tighten your stomach as if you were about to get hit in the stomach”. Correct performance of the ADIM during training was confirmed visually or by manual palpation by one of the investigators just medial to the anterior superior iliac spine (ASIS) if needed.

Sensor Placement Muscular activity was recorded using a combination of surface and fine wire EMG sensors. Skin at all electrode locations was debrided and cleaned with alcohol swabs prior to sensor placement to improve signal acquisition. Surface EMG sensors were placed on the right external oblique (approximately 14 cm lateral to the umbilicus), right internal oblique (two cm below the ASIS just medial and superior to the inguinal ligament), bilaterally over the longissimus at L1 three cm lateral to midline (Lariviere et al., 2002), and bilateral superficial multifidus one cm lateral to midline at L5. Fine wire sensors were inserted bilaterally using a 50mm 25-gauge hypodermic needle into the deep multifidus approximately four cm lateral to midline in a ventral and medial direction until the spine segment lamina was reached (Moseley et al., 2002). Once inserted, the needle was removed and the fine wire left in place. Additionally, local reference sensors with spring connectors were attached to the skin bilaterally over the most prominent bony aspect of the iliac crest and the fine wires were attached. Submaximal normalization contractions were performed to allow comparison of repeated contractions within or between subjects. Submaximal normalization contractions were chosen to reduce the influence of motivation or pain-related fear on maximal muscle contraction intensity (Larivière et al., 2003). For sub-maximal normalization of the abdominal muscles, subjects were placed in a supine hook-lying position with the knees flexed to approximately 90 degrees and asked to lift their legs off the surface approximately one cm and hold this position for seven seconds (Dankaerts et al., 2004). Abdominal muscles sub-maximal contractions were performed prior to electrode placement on/in the back muscled to prevent testing discomfort. Sub-maximal

87 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 contraction normalization was then completed for the back muscles by having the subject lie prone with the knees flexed to 90 degrees and asking the subject lift their knees off the surface approximately five cm and hold for seven seconds (Dankaerts et al., 2004). After sub-max normalization trials were completed, subjects then completed all co-contraction trials in standing and quadruped positions. Subjects completed three trials each of the three abdominal contraction conditions including 1) resting, 2) ADIM, and 3) ABM. Position order (standing and quadruped) was randomized. To minimize position changes, once a position order was determined, abdominal contraction order was randomized within each position. A total of nine trials were performed in each of the two positions. Subjects were asked to hold each contraction for seven seconds. All muscle activity was recorded using a 16-channel wireless Delsys Trigno system and collected at 1926 Hz. The EMG surface sensors (Trigno Flex sensors) have a built-in butterworth band pass filter giving the sensor a frequency response from 20 to 450 Hz (10-850 for fine wire EMG) with less than 2.5 microvolt baseline noise. The common mode rejection ratio was >80dB.

Data Reduction Using a custom MATLAB program, indwelling channels (deep multifidus fibers) were notch filtered at 60 Hz for all trials including sub-maximal normalization trials. A 2- second sample (seconds 3-5) was extracted from each trial and used for RMS calculations. Root mean square values were averaged across the three trials and were subsequently divided by the sub-maximal normalization contraction for that respective muscle to create a percentage of sub-maximal contraction activity.

Statistical Analysis Descriptive statistics (mean ± SD) were calculated for all demographic variables for both controls and subjects with a LBP history. Data normality was defined as meeting two of three of the following characteristics (non-significant Shapiro-Wilk test, as well as skewness and kurtosis values between -2 and +2). Group differences in baseline characteristics were tested using independent t-tests. All muscular activity data did not meet the criteria of normality. As a result, robust statistics were used to analyze differences between trimmed mean values (Wilcox, 2016). Winsorized means (20% 88 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 trimmed) were calculated for all dependent variables. Bootstrapping was performed 2,000 times and 95% confidence intervals were calculated from the 2,000 bootstrapped mean values. These values were used for all statistical comparisons. To illustrate the effect magnitude, a robust heteroscedastic approach to measuring effect size (x - ksi) was used (Wilcox & Tian, 2011). Using this approach, an effect of x = 0.15 is considered small, x = 0.35 is medium, and x = 0.5 is large (Wilcox & Tian, 2011). To analyze main effects of and interactions between group and multifidus depth within all combinations of position and abdominal contraction, six 2 x 2 mixed model ANOVAs were used. Next, two 2 x 3 repeated measures ANOVAs were calculated using data from subjects with a history of LBP to assess interactions and main effects for multifidus depth and strategy. One ANOVA was calculated for the standing position and one for the quadruped position. Lastly, three 2 x 2 repeated measures ANOVAs were calculated to assess main effects of position and multifidus depth using data from HxLBP subjects. One ANOVA was completed for each of the three contraction types. If a significant main effect or interaction was identified, post hoc robust t-tests with 2,000 bootstrapped samples were used to locate significant differences. Alpha values were set at 0.05. All subject baseline characteristics were calculated using IBM SPSS version 25.0 (Armonk, NY). All dependent variable descriptive statistics and robust analyses were calculated using R software.

Results A total of 60 subjects (30 LBP history and 30 control) agreed to participate in this study and completed all testing. Subject demographics can be found in Table 5.1. There were no significant differences between the two groups for the demographic variables of sex, age (p=0.792), height (p=0.758), weight (p=0.254), and BMI (p=0.232). However, the history of LBP group had significantly higher scores for TSK (p<0.001), ODI (p<0.001), and the LSIQ (p<0.001). Multifidus co-contraction did not differ between HxLBP and control subjects. Additionally, deep and superficial multifidus fibers did not differ in the amount of co- contraction in response to abdominal contractions. Deep and superficial multifidus co- contraction values are presented in Table 5.2. These values are presented as percentages 89 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 of their corresponding RMS submaximal reference contraction values. The multifidus depth by group ANOVA revealed no statistically significant interactions between multifidus depth and group (p= 0.557 to 0.931). Additionally, no significant main effects for group were observed in standing (p=0.338 to 0.682) or quadruped (p=0.088 to 0.492) positions, or during any of the three contraction conditions (Table 5.3). Significant differences were found between the two multifidus fiber depths during standing ADIM contraction (p=0.040), quadruped resting (p<0.001), and quadruped ADIM contraction (p=0.022). No differences were seen between deep and superficial multifidus during standing resting (p=0.339), standing ABM (p=0.079), and quadruped ABM (p=0.111). In the HxLBP subjects, both ADIM and ABM resulted in greater multifidus co- contraction than the resting position. No significant interactions were observed between abdominal contraction strategy and multifidus depth in either standing (p=0.995) or quadruped (p=0.208) for patients in the HxLBP group. A statistically significant main effect for abdominal contraction strategy was identified in both standing (p=0.002) (Table 5.4) and quadruped (p=0.015) (Table 5.5) positions for individuals in the HxLBP group. Post hoc analysis indicated that both the ADIM (p<0.001) and ABM (p<0.001) contraction strategies resulted in significantly greater multifidus co-contraction when compared to the resting condition in both standing and quadruped. However, no difference in multifidus co-contraction was found between the ADIM and ABM strategies in either standing (p=0.068) or quadruped (p=0.172) positions. Across all three contraction strategies, standing resulted in greater multifidus co- contraction than quadruped for HxLBP subjects. Multifidus depth by position ANOVAs revealed no statistically significant interactions (p=0.503 to 0.986). A statistically significant main effect for position was observed (Table 5.6) for resting (p=0.016), ADIM (p<0.001), and ABM (p<0.001) within in the HxLBP group, with the standing position resulting in greater multifidus co-contraction than the quadruped position. No statistically significant main effects were identified for multifidus depth during resting (p=0.921), ADIM (p=0.954), or ABM (p=0.835).

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Discussion The primary purpose of this study was to determine the effect of a LBP history on the ability of lumbar stabilizing muscles to co-contract with abdominal muscle activation compared to individuals without a LBP history. A secondary purpose was to determine if co-contraction differences exist among abdominal activation strategies and common positions used in clinical practice in individuals with a history of LBP. Furthermore, this study aimed to assess effects of multifidus depth (deep vs. superficial) on the multifidus co-contraction response during three volitional abdominal contractions in individuals with a recent history of LBP. The primary finding of this study was that the multifidus muscle (both deep and superficial) co-contracts significantly more during ADIM and ABM contractions than during the resting condition, indicating that there is a co-contractive response during these contractions in individuals with a recent history of LBP. Within the HxLBP group, no difference was observed between multifidus co-contraction during the ADIM and ABM. Additionally, no significant difference was found in multifidus co-contraction between individuals who have not had LBP in the previous two years and those individuals who have had LBP in the past two years. Furthermore, this study identified a significant difference in co-contraction activity between the superficial and deep multifidus fibers in the multifidus depth by group ANOVA. However, this difference was not consistent across all position and strategy combinations. This ANOVA was the only analysis to include group as an independent variable and while assessing for multifidus depth main effect, combined the control and HxLBP groups into one group, causing a doubling of the sample size. Lastly, this study identified significantly greater multifidus activity in the standing position when compared to the quadruped position in the HxLBP group. This positional difference was consistently observed across ADIM, ABM, and resting conditions. The current study is the first to demonstrate a co-contractive response in the superficial and deep multifidus fibers in individuals with a history of LBP during volitional abdominal contractions. One previous study demonstrated the occurrence of superficial multifidus co-contraction during these abdominal activation strategies in

91 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 individuals without a history of LBP (Matthijs et al., 2014). The current findings demonstrate that individuals in both the HxLBP and control groups experience similar multifidus co-contraction regardless of LBP history. A number of studies have been conducted to assess activity of the multifidus muscle in individuals with a history of low back pain (D'hooge et al., 2013; Macdonald et al., 2011; MacDonald et al., 2009; 2010). When assessed together, these studies may demonstrate the existence of compensatory strategies during periods of pain remission where deep multifidus is both delayed and less active forcing the superficial multifidus to compensate to provide sufficient stability. However, in the current study, differences between deep and superficial multifidus were not consistent across positions or contraction strategies. Differences between deep and superficial multifidus fiber depths were significant in only three of the six combinations of positions and contractions. Effect sizes for these significant findings were small to moderate and may not indicate a clinically important difference. This could possibly be due to a lack of differentiation based on the previously painful side in the current study whereas previous studies have found differences in multifidus activity between the previously painful side and the non- painful side (D'hooge et al., 2013; MacDonald et al., 2009). Previous investigators demonstrated that altering an individual’s position results in altered muscular activity (O’Sullivan et al., 2002). However, positional dependency has not previously been observed for multifidus co-contraction activity during volitional abdominal activation. O’Sullivan et al., (2002) speculated that the neural control system may automatically alter muscular activity in spinal musculature based on posture and the amount of load shared with passive structures. The quadruped position has a larger number of contact points with the floor, a greater base of support, and a gravitation force that is approximately perpendicular to that experienced in standing. A combination of these positional differences may assist in explaining the different levels of multifidus co- contraction currently observed.

Limitations Although all subjects in the LBP history group had LBP within the last two years, data were not collected on number of LBP recurrences. As a result, it is possible that

92 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 subjects in this group have had varying numbers of LBP episodes. Some may have future episodes while others may not, and these groups may have different patterns of muscular activity. Additionally, data were not collected regarding the side of previous pain in order to more specifically determine the influence of ipsilateral vs. contralateral pain. However, recall bias may alter findings if subjects are asked to recall the painful side up to two years after the painful episode.

Conclusions Subjects with a history of LBP within the previous two years have a similar ability to incorporate the ADIM or ABM to facilitate multifidus co-contraction when compared to those individuals without a LBP history. The fact that there was no difference in multifidus co-contraction between the ADIM and ABM contractions indicates that individuals can use either the ADIM or ABM to facilitate multifidus contraction based on preference and, therefore, increase spinal stability. Performing the abdominal contractions in standing resulted in greater multifidus contraction than in quadruped. These positional differences may highlight different stability requirements between the two positions. Similar levels of multifidus activity were observed between the deep and superficial multifidus fibers. This was consistent across both subject groups indicating that the ADIM and ABM stabilizes the spine by activating both layers of the multifidus regardless of the HxLBP status. Clinicians interested in educating patients on abdominal contractions to stabilize the spine during potentially painful functional activities can choose either the ADIM or ABM strategies based on which strategy the patient prefers to use.

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References Andersson, G. B. (1999). Epidemiological features of chronic low-back pain. The Lancet, 354(9178), 581–585. http://doi.org/10.1016/S0140-6736(99)01312-4 Bouche, K. G., Vanovermeire, O., Stevens, V. K., Coorevits, P. L., Caemaert, J. J., Cambier, D. C., et al. (2011). Computed tomographic analysis of the quality of trunk muscles in asymptomatic and symptomatic lumbar discectomy patients. BMC Musculoskeletal Disorders, 12(1), 65. http://doi.org/10.1186/1471-2474-12-65 Chan, S.-T., Fung, P.-K., Ng, N.-Y., Ngan, T.-L., Chong, M.-Y., Tang, C.-N., et al. (2012). Dynamic changes of elasticity, cross-sectional area, and fat infiltration of multifidus at different postures in men with chronic low back pain. The Spine Journal: Official Journal of the North American Spine Society, 12(5), 381–388. http://doi.org/10.1016/j.spinee.2011.12.004 Chiarotto, A., Maxwell, L. J., Terwee, C. B., Wells, G. A., Tugwell, P., & Ostelo, R. W. (2016). Roland-morris disability questionnaire and oswestry disability index: which has better measurement properties for measuring physical functioning in nonspecific low back pain? systematic review and meta-analysis. Physical Therapy. http://doi.org/10.2522/ptj.20150420 Cholewicki, J., & McGill, S. M. (1996). Mechanical stability of the in vivo lumbar spine: implications for injury and chronic low back pain. Clinical Biomechanics, 11(1), 1– 15. http://doi.org/10.1016/0268-0033(95)00035-6 D'hooge, R., Hodges, P., Tsao, H., Hall, L., MacDonald, D., & Danneels, L. (2013). Altered trunk muscle coordination during rapid trunk flexion in people in remission of recurrent low back pain. Journal of Electromyography and Kinesiology, 23(1), 173–181. http://doi.org/10.1016/j.jelekin.2012.09.003 Dankaerts, W., O’Sullivan, P. B., Burnett, A. F., Straker, L. M., & Danneels, L. A. (2004). Reliability of EMG measurements for trunk muscles during maximal and sub-maximal voluntary isometric contractions in healthy controls and CLBP patients. Journal of Electromyography and Kinesiology, 14(3), 333–342. http://doi.org/10.1016/j.jelekin.2003.07.001 Descarreaux, M., Lalonde, C., & Normand, M. C. (2007). Isometric force parameters and trunk muscle recruitment strategies in a population with low back pain. Journal of Manipulative and Physiological Therapeutics, 30(2), 91–97. http://doi.org/10.1016/j.jmpt.2006.12.016 Deyo, R. A., Mirza, S. K., & Martin, B. I. (2006). Back pain prevalence and visit rates: estimates from U.S. national surveys, 2002. Spine, 31(23), 2724–2727. http://doi.org/10.1097/01.brs.0000244618.06877.cd Dickx, N., Cagnie, B., Achten, E., Vandemaele, P., Parlevliet, T., & Danneels, L. (2008). Changes in lumbar muscle activity because of induced muscle pain evaluated by muscle functional magnetic resonance imaging. Spine, 33(26), E983–9. http://doi.org/10.1097/BRS.0b013e31818917d0

94 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Fairbank, J. C. T., Couper, J., Davies, J., & OBrien, J. (1980). The Oswestry Low Back Pain Questionnaire. Physiotherapy, 66(8), 271–273. French, D. J., France, C. R., Vigneau, F., French, J. A., & Evans, T. R. (2007). Fear of movement/(re)injury in chronic pain: A psychometric assessment of the original English version of the Tampa scale for kinesiophobia (TSK). Pain, 127(1), 42–51. http://doi.org/10.1016/j.pain.2006.07.016 Haro, H., Maekawa, S., & Hamada, Y. (2008). Prospective analysis of clinical evaluation and self-assessment by patients after decompression surgery for degenerative lumbar canal stenosis. The Spine Journal, 8(2), 380–384. http://doi.org/10.1016/j.spinee.2007.01.010 Hestbaek, L., Leboeuf-Yde, C., Engberg, M., Lauritzen, T., Bruun, N. H., & Manniche, C. (2003). The course of low back pain in a general population. Results from a 5-year prospective study. Journal of Manipulative and Physiological Therapeutics, 26(4), 213–219. Hides, J., Gilmore, C., Stanton, W., & Bohlscheid, E. (2008). Multifidus size and symmetry among chronic LBP and healthy asymptomatic subjects. Manual Therapy, 13(1), 43–49. http://doi.org/10.1016/j.math.2006.07.017 Indahl, A., Velund, L., & Reikeraas, O. (1995). Good prognosis for low back pain when left untampered. A randomized clinical trial. Spine, 20(4), 473–477. Lariviere, C., Arsenault, A. B., Gravel, D., & Gagnon, D. (2002). Evaluation of measurement strategies to increase the reliability of EMG indices to assess back muscle fatigue and recovery. Journal of Electromyography and Kinesiology, 12(2), 91–102. http://doi.org/10.1016/S1050-6411(02)00011-1 Larivière, C., Arsenault, A. B., Gravel, D., Gagnon, D., & Loisel, P. (2003). Surface electromyography assessment of back muscle intrinsic properties. Journal of Electromyography and Kinesiology, 13(4), 305–318. http://doi.org/10.1016/S1050- 6411(03)00039-7 Macdonald, D. A., Dawson, A. P., & Hodges, P. W. (2011). Behavior of the lumbar multifidus during lower extremity movements in people with recurrent low back pain during symptom remission. Journal of Orthopaedic & Sports Physical Therapy, 41(3), 155–164. http://doi.org/10.2519/jospt.2011.3410 MacDonald, D. A., Lorimer Moseley, G., & Hodges, P. W. (2006). The lumbar multifidus: Does the evidence support clinical beliefs? Manual Therapy, 11(4), 254– 263. http://doi.org/10.1016/j.math.2006.02.004 MacDonald, D., Moseley, G. L., & Hodges, P. W. (2009). Why do some patients keep hurting their back? Evidence of ongoing back muscle dysfunction during remission from recurrent back pain. Pain, 142(3), 183–188. http://doi.org/10.1016/j.pain.2008.12.002 MacDonald, D., Moseley, G. L., & Hodges, P. W. (2010). People with recurrent low back pain respond differently to trunk loading despite remission from symptoms. Spine, 35(7), 818–824. http://doi.org/10.1097/BRS.0b013e3181bc98f1 95 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Macedo, L. G., Maher, C. G., Hancock, M. J., Kamper, S. J., McAuley, J. H., Stanton, T. R., et al. (2014). Predicting response to motor control exercises and graded activity for patients with low back pain: preplanned secondary analysis of a randomized controlled trial. Physical Therapy, 94(11), 1543–1554. http://doi.org/10.2522/ptj.20140014 Matthijs, O. C. G., Dedrick, G. S., James, C. R., Brismée, J.-M., Hooper, T. L., McGalliard, M. K., & Sizer, P. S. (2014). Co-contractive activation of the superficial multifidus during volitional preemptive abdominal contraction. PM&R: the Journal of Injury, Function, and Rehabilitation, 6(1), 13–21. http://doi.org/10.1016/j.pmrj.2013.08.606 Miller, R. P., Kori, S. H., & Todd, D. D. (1991). The Tampa Scale. Tampa, Fla. Moseley, G. L., Hodges, P. W., & Gandevia, S. C. (2002). Deep and superficial fibers of the lumbar multifidus muscle are differentially active during voluntary arm movements. Spine, 27(2), E29–36. Moseley, G. L., Hodges, P. W., & Gandevia, S. C. (2003). External perturbation of the trunk in standing humans differentially activates components of the medial back muscles. The Journal of Physiology, 547(Pt 2), 581–587. http://doi.org/10.1113/jphysiol.2002.024950 O’Sullivan, P. B., Grahamslaw, K. M., Kendell, M., Lapenskie, S. C., Möller, N. E., & Richards, K. V. (2002). The effect of different standing and sitting postures on trunk muscle activity in a pain-free population. Spine, 27(11), 1238–1244. Portney, L. G., & Watkins, M. P. (2009). Foundations of clinical research: applications to practice. Pearson Education, Inc. Saragiotto, B. T., Maher, C. G., New, C. H., Catley, M., Hancock, M. J., Cook, C., & Hodges, P. W. (2018). Clinimetric testing of the lumbar spine instability questionnaire. Journal of Orthopaedic & Sports Physical Therapy, 1–24. http://doi.org/10.2519/jospt.2018.7866 Swinkels-Meewisse, E. J. C. M., Swinkels, R. A. H. M., Verbeek, A. L. M., Vlaeyen, J. W. S., & Oostendorp, R. A. B. (2003). Psychometric properties of the tampa scale for kinesiophobia and the fear-avoidance beliefs questionnaire in acute low back pain. Manual Therapy, 8(1), 29–36. http://doi.org/10.1054/math.2002.0484 van Dieën, J. H., Cholewicki, J., & Radebold, A. (2003). Trunk muscle recruitment patterns in patients with low back pain enhance the stability of the lumbar spine. Spine, 28(8), 834–841. van Tulder, M., Becker, A., Bekkering, T., Breen, A., del Real, M. T. G., Hutchinson, A., et al. (2006, March). Chapter 3. European guidelines for the management of acute nonspecific low back pain in primary care. European Spine Journal. http://doi.org/10.1007/s00586-006-1071-2 Waddell, G. (1987). 1987 Volvo award in clinical sciences. A new clinical model for the treatment of low-back pain. Spine, 12(7), 632–644.

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Wallwork, T. L., Stanton, W. R., Freke, M., & Hides, J. A. (2009). The effect of chronic low back pain on size and contraction of the lumbar multifidus muscle. Manual Therapy, 14(5), 496–500. http://doi.org/10.1016/j.math.2008.09.006 Wilcox, R. (2016). Introduction to Robust Estimation and Hypothesos Testing (Fourth). Waltham, MA: Academic Press. Wilcox, R. R., & Tian, T. S. (2011). Measuring effect size: a robust heteroscedastic approach for two or more groups. Journal of Applied Statistics, 38(7), 1359–1368. http://doi.org/10.1080/02664763.2010.498507

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Table 5.1. Subject characteristics No Recent LBP HxLBP Group p-value Group Sex* 18 M, 12 F 18 M, 12 F N/A Age (Years) 37.8 (14.46) 36.83 (13.79) .792 Height (Inches) 69.08 (3.46) 69.39 (4.22) .758 Weight (Lbs) 165.77 (31.48) 177.1 (43.80) .254 BMI (kg/m2) 24.30 (3.65) 25.59 (4.66) .232 Time Since LBP (weeks) 17.42 (0.15-100)** N/A NPRS (last pain) N/A 5.74 (1.67) N/A ODI 1.47 (2.62)*** 11 (9.79) <.001 LSIQ 0.43 (1.07)*** 3.86 (3.26) <.001 TSK 22.17 (5.17) 29.57 (6.92) <.001 Abbreviations: LBP, low back pain; ODI, Oswestry disability index; LSIQ, lumbar spine instability questionnaire; HxLBP, history of low back pain group. *Sex presented as frequency. **Time since LBP presented as mean and range. *** only nine control group subjects reported ODI scores above 0. Only six subjects reported LSIQ scores above 0.

Table 5.2. Multifidus co-contraction RMS values Resting ADIM ABM Standing Control HxLBP Control HxLBP Control HxLBP SMF 12.16 15.11 27.19 27.78 29.15 30.37 (9.79- (11.21- (20.73- (21.32- (22.54- (21.05- 14.73) 18.95) 33.65) 33.27) 34.96) 37.05) DMF 11.74 15.97 25.52 30.45 26.25 30.96 (8.76- (10.31- (16.42- (18.29- (18.64- (19.98- 14.42) 22.29) 32.04) 41.70) 32.43) 41.37) Quadruped SMF 7.55 11.33 11.84 15.50 11.79 16.72 (5.92- (7.05- (9.08- (10.78- (8.72- (11.61- 9.77) 14.59) 14.28) 19.32) 14.63) 21.47) DMF 6.34 10.56 12.87 15.17 11.33 19.74 (4.29- (5.27- (6.37- (8.02- (6.78- (10.69- 13.02) 18.49) 20.09) 26.54) 19.26) 30.15) Abbreviations: SMF, superficial multifidus fibers, DMF, deep multifidus fibers, HxLBP, history of low back pain group. All presented values are Winsorized trimmed means with bootstrapped 95% confidence intervals. Value represent RMS percentage of submaximal reference contraction.

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Table 5.3. Group by multifidus depth ANOVA results Position Condition Effect p-value Effect Size (x) Stand Rest Interaction p=.628 N/A Group p=.338 0.23 (DMF), 0.22 (SMF) MF Depth p=.339 0.07(Control), 0.02 (HxLBP) ADIM Interaction p=.722 N/A Group p=.682 0.12 (DMF), 0.05 (SMF) MF Depth p=.040* 0.08 (Control), 0.02 (HxLBP) ABM Interaction p=.931 N/A Group p=.652 0.14 (DMF), 0.01 (SMF) MF Depth p=.079 0.14 (Control), 0.02 (HxLBP) Quadruped Rest Interaction p=.838 N/A Group p=.492 0.21 (DMF), 0.25 (SMF) MF Depth p<.001* 0.24 (Control), 0.06 (HxLBP) ADIM Interaction p=.557 N/A Group p=.414 0.09 (DMF), 0.25 (SMF) MF Depth p=.022* 0.003 (Control), 0.05 (HxLBP) ABM Interaction p=.802 N/A Group p=.088 0.29 (DMF), 0.33 (SMF) MF Depth p=.111 0.05 (Control), 0.09 (HxLBP) Abbreviations: MF Depth, multifidus fiber depth; ADIM, Abdominal Drawing-in Maneuver; ABM, Abdominal Bracing Maneuver; SMF, Superficial Multifidus; DMF, Deep Multifidus. * indicates significant differences

Table 5.4. Multifidus depth by abdominal contraction strategy ANOVA results in standing position HxLBP group Comparison p-value Effect Size (x) Interaction p = .995 N/A MF Depth p = .901 N/A Contraction p = .002* N/A Post Hoc Test Results DMF vs. SMF p = .714 0.02 (Rest), 0.02 (ADIM), 0.02 (ABM) Rest vs. ADIM p < .001* 0.38 (DMF), 0.60 (SMF) Rest vs. ABM p < .001* 0.47 (DMF), 0.64 (SMF) ADIM vs. ABM p = .068 0.04 (DMF), 0.07 (SMF) Abbreviations: MF Depth, multifidus fiber depth; ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver; SMF, superficial multifidus; DMF, deep multifidus. * indicates significant differences.

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Table 5.5. Multifidus depth by abdominal contraction strategy ANOVA results in quadruped position HxLBP group Comparison p-value Effect Size (x) Interaction p = .208 N/A MF Depth p = .994 N/A Contraction p = .015* N/A Post Hoc Test Results DMF vs. SMF p = .956 0.06 (Rest), 0.05 (ADIM), .09 (ABM) Rest vs. ADIM p < .001* 0.19 (DMF), 0.29 (SMF) Rest vs. ABM p < .001* 0.31 (DMF), 0.37 (SMF) ADIM vs. ABM p = .172 0.14 (DMF), 0.08 (SMF) Abbreviations: MF Depth, multifidus fiber depth; ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver; SMF, superficial multifidus; DMF, deep multifidus. * indicates significant differences.

Table 5.6. Position by multifidus depth ANOVA in HxLBP subjects Condition Effect p-value Rest Interaction p=.986 Position p=.016* MF Depth p=.921 ADIM Interaction p=.636 Position P<.001* MF Depth p=.954 ABM Interaction p=.503 Position P<.001* MF Depth p=.835 Abbreviations: MF Depth, multifidus fiber depth; ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver. * indicates significant differences.

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Figure 5.1. Group x multifidus depth main effects and interactions for multifidus co- contraction in A) Quadruped ADIM, B) Quadruped ABM, C) Standing ADIM, and D) Standing ABM. Abbreviations: ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver; DMF, deep multifidus fibers; SMF, superficial multifidus fibers; HxLBP, history of low back pain.

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Figure 5.2. Multifidus depth x contraction main effects and interactions for multifidus co- contraction in HxLBP subjects. A) Quadruped multifidus depth, B) Quadruped contraction, C) Standing multifidus depth, and D) Standing contraction. Abbreviations: ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver; DMF, deep multifidus fibers; SMF, superficial multifidus fibers.

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Figure 5.3. Position x multifidus depth main effects and interactions for multifidus co- contraction in HxLBP subjects during A) ABM, B) ADIM, and C) Rest. Abbreviations: ADIM, abdominal drawing-in maneuver; ABM, abdominal bracing maneuver; DMF, deep multifidus; SMF, superficial multifidus.

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CHAPTER VI

DISCUSSION AND CONCLUSION The multifidus is an important lumbar spine stabilizer (Jemmett et al., 2004; Wilke et al., 1995). The abdominal drawing in maneuver (ADIM) and abdominal bracing maneuver ABM) have long been considered to result in multifidus co-contraction but without supporting empirical evidence (MacDonald et al., 2006). More recent research demonstrates that the superficial multifidus co-contracts during both the ADIM and the ABM in individuals without low back pain (LBP) (Matthijs et al., 2014). A number of studies have observed activity differences between the deep and superficial multifidus in both healthy individuals (Moseley et al., 2003) and individuals with recurrent LBP without current symptoms (D'hooge et al., 2013; Macdonald et al., 2011; MacDonald et al., 2010). The purposes of this study were to determine: 1) if deep and superficial multifidus fibers demonstrate different co-contraction patterns during volitional abdominal contractions; 2) the effect of a LBP history on the ability of lumbar stabilizing muscles to co-contract with abdominal muscle activation compared to individuals without a LBP history; and 3) if co-contraction differences exist among abdominal activation strategies and common positions used in clinical practice. The purpose of this chapter is to provide a general discussion and conclusion of the findings from the two studies included in this dissertation.

Discussion The current dissertation adds information to the literature supporting previous wide-spread beliefs regarding multifidus co-contraction. This was accomplished by examining multifidus co-contraction in conditions that had not been studied to this date. Although this study was not the first to assess superficial multifidus co-contraction during ADIM and ABM contractions, this assessment was necessary to answer questions to other more novel queries. This study was the first to assess the co-contractive response of the deep multifidus in healthy subjects as well as those who have a recent history of LBP with no current symptoms (HxLBP), as well as to assess differences between deep and superficial multifidus responses. Additionally, this study was the first to assess the influence of a low back pain history on multifidus co-contractive responses during ADIM 104 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 and ABM contractions. Furthermore, this study examined differences in multifidus co- contraction between three abdominal contraction strategies (ADIM, ABM, and resting). Lastly, this study was the first to assess differences in multifidus co-contraction intensity between standing and quadruped positions. Voluntary abdominal activation strategies such as the ADIM and ABM have been used for years as methods to increase spinal stability (Richardson et al., 2002; Vera- Garcia et al., 2007). While it has been generally accepted that the multifidus co-contracts with the abdominal muscles during these abdominal activation strategies (MacDonald et al., 2006), very limited evidence exists to confirm this co-contraction (Matthijs et al., 2014). Study 1 asked whether a difference in multifidus co-contraction exists among abdominal activation strategies in the deep and superficial multifidus in healthy subjects. It was hypothesized that both ADIM and ABM contractions would result in greater multifidus co-contraction than the resting condition in healthy subjects. Results demonstrated that both the ADIM and ABM contractions resulted in significantly greater deep and superficial multifidus activity than was observed during the resting condition with no difference observed between the ADIM and ABM contractions. Three different explanations exist that may provide clarification as to why multifidus co-contraction occurs during voluntary abdominal contractions. These three reasons are not necessarily mutually exclusive. One possible explanation is that the ABM and ADIM contractions include multifidus contraction within the motor program and it is inherently part of the contraction. Since the TrA alone has only limited ability to provide spinal stability (Grenier & McGill, 2007), concurrent multifidus muscular contribution to spinal stability may be necessary. The second possible explanation is that an anatomical connection between the abdominal muscles and the multifidus muscles requires co- contraction for efficient stabilization. Vleeming et al. (2014) demonstrated through modeling on human cadavers that activation of the common tendon of the transverse abdominis (TrA) and internal oblique (IO) in the absence of paraspinal muscular activity results in an anterior and lateral displacement of the paraspinal muscle compartment. This would likely result in insufficient tension production of the TrA/IO common tendon. Similarly, when paraspinal muscles contract in the absence of TrA/IO contraction, a

105 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 posterior displacement of the posterior fascial layer was observed. When both muscle groups are contracted together, tension in the common TrA/IO tendon is counteracted by the posterior displacement of the posterior fascial layer of the paraspinal muscle compartment. These authors suggest that this creates a point of equal tension between the TrA/IO and the paraspinal muscles resulting in force closure and an increase in spinal stability (Vleeming et al., 2014). The third possible explanation for the existence of abdominal and multifidus co- contraction is that in order to maintain a static position, forces on each side of the motion segment axis must be balanced. Contraction of the abdominal muscles in the absence of activation of muscles posterior to the axis of movement (the spine) would result in a net movement into flexion. To maintain a static position, it is necessary to balance the total moment of the muscles contracting posterior to the spine with the total moment anterior to the spine (Bergmark, 1989). Baek et al. (2014b) recorded increased activity in the superficial and deep multifidus resulting from electrical stimulation of the TrA. In a separate study, Baek at al. (2014a) observed muscular activity in the external oblique, internal oblique, and TrA resulting from superficial multifidus electrical stimulation. This could indicate that the antagonist muscle group activates to balance muscular forces on each side of the movement axis. Whether the mechanism underlying multifidus co- contraction is based on a motor program, physical anatomical connections, resolution of forces across a motion segment axis, or a combination of these factors, it appears that both ADIM and ABM result in similar multifidus activity. These two contraction methods can both be used to create increased multifidus activity that increases spinal stability. Further research is needed to elucidate the role of these mechanisms in creating this co-contraction. The deep and superficial fibers of the multifidus have been shown to differ based upon anatomical (Macintosh et al., 1986), biomechanical (Bogduk et al., 1992), histological (Dickx, Cagnie, Achten, Vandemaele, Parlevliet, & Danneels, 2010a), and neuromotor factors (MacDonald et al., 2009). It has been suggested that the superficial multifidus controls spinal orientation and position while the deep fibers aid in controlling intersegmental motion (Moseley et al., 2002). Therefore, it could be deduced that

106 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 abdominal contractions intended to stabilize the spine could result in different co- contraction levels between the deep and superficial multifidus. As a result, study 1 asked “Is there a difference between deep and superficial multifidus co-contraction during each VPAC strategy in healthy subjects?” While it was hypothesized that a difference would be observed in co-contraction response between deep and superficial multifidus in healthy subjects, no significant difference in multifidus co-contraction was observed between the deep and superficial fibers. Many studies that have demonstrated differences in contraction intensity or onset timing between deep and superficial multifidus have observed these differences during voluntary limb movement or an external perturbation (D'hooge et al., 2013; MacDonald et al., 2009; Moseley et al., 2002; 2003). In the current study however, the subjects performed voluntary abdominal contractions that may not necessarily result in similar multifidus co-contraction than the previously published perturbations that resulted in differential deep and superficial multifidus activity. Low back pain results in many changes with regards to the lumbar multifidus including increased fatty infiltrates (Hodges et al., 2015), decreased cross sectional area (Fortin & Macedo, 2013), decreased multifidus activity (Dickx, Cagnie, Parlevliet, Lavens, & Danneels, 2010b), and decreased contractility (Wallwork et al., 2009). A number of studies demonstrated that alterations in multifidus timing and contraction intensity exist even after pain has subsided (D'hooge et al., 2013; Macdonald et al., 2011; MacDonald et al., 2009). As a result, study 2 asked “Is there a difference in multifidus co-contraction between subjects with a LBP history when compared to healthy subjects without a LBP history during VPAC?” For this question, it was hypothesized that subjects with a history of LBP would exhibit multifidus co-contraction in response to VPAC but this co-contraction activity would not be as high as the co-contraction level found in subjects without a LBP history. However, no significant differences were observed in multifidus co-contraction between the two groups. Additionally, all effect sizes for between group differences were small. This demonstrates that HxLBP subjects can incorporate the ADIM and ABM for activating the lumbar multifidus to stabilize the spine or as an alternate method of facilitating multifidus exercise. The three previously noted studies that demonstrated differences in muscular activity between healthy subjects

107 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 and HxLBP subjects observed these differences during dynamic movements, such as a rapid arm movement, leg movements, and rapid trunk flexion. In comparison to performing the ADIM and ABM, these are more dynamic movements and therefore, may require different activation strategies. Study 2 assessed co-contraction among activation strategies (resting, ADIM, and ABM) in the deep and superficial multifidus fibers in subjects with a history of LBP. It was hypothesized that subjects with a history of LBP would demonstrate no difference in multifidus co-contractile response during ADIM and ABM, while resting would not result in multifidus co-contraction. Similar to the findings in subjects without a recent history of LBP, the HxLBP subjects demonstrated significantly greater multifidus co- contraction during the ADIM and ABM compared to the resting conditions. Furthermore, no differences were found in co-contractive response between the ADIM and ABM contractions. This demonstrates that even when in remission from LBP, the functional coupling of the abdominal muscles is similar to the coupling found in subjects without LBP. However, it is still unknown whether this coupling remains consistent through an episode of LBP or if this coupling represents a return to “normal” after the pain has subsided. It has been demonstrated that different positions result in altered spinal musculature activity (O’Sullivan et al., 2002). Additionally, Matthijs et al. (2014) reported that upon a visual analysis of their data, multifidus co-contraction appeared to occur more frequently in standing than quadruped. As a result, Study 2 asked “Is there a difference in superficial and deep multifidus co-contraction in response to VPAC during standing versus quadruped positions in HxLBP subjects?” It was hypothesized that both ADIM and ABM would result in multifidus co-contraction in both standing and quadruped positions, with greater co-contraction produced in standing. Results supported this hypothesis by demonstrating greater multifidus co-contraction in standing than the quadruped position during both ADIM and ABM. Furthermore, results demonstrated that even during the abdominal resting condition, greater multifidus activity was observed in standing versus quadruped positions. This is likely due to differences in active system requirements between the positions. This difference could be due to a difference in the

108 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 direction of gravitational forces acting on the spine combined with the body having contact with the stable both cranial and caudal to the spine. Between the two tested positions, there is approximately a 90-degree difference in the gravitational force direction acting on the spine. This explanation is consistent with the earlier discussion describing the balancing of forces on either side of the spinal motion segment axis. In the quadruped position (with hands and knees both on the mat) stability is present both cranial and caudal to the lumbar spine. In the absence of muscular contraction, gravitational forces would increase the lordosis (increased extension). To maintain a static neutral position, the anterior abdominal muscles (flexors) are required to counteract the gravitational forces while these gravitation forces aid the multifidus in producing an extension moment. This would result in a greater ratio of abdominal muscle activity to multifidus activity as compared to the relative ratio observed in the standing position. In the standing position, the line of gravity falls anterior to the spinal column and therefore requires spinal extensor activity along with intermittent abdominal activation just to maintain a standing posture (Shumway-Cook & Woollacott, 2012). This may result in a mild activation of the multifidus prior to the onset of the abdominal muscles to just maintain a standing posture. The differences in co-contraction between positions can be utilized clinically by progressing from a lower intensity co-contraction in quadruped to the slightly stronger multifidus contraction in a standing position.

Conclusion The two studies in this dissertation demonstrated that both healthy and HxLBP subjects experience multifidus co-contraction during both ADIM and ABM contractions. Additionally, multifidus co-contraction does not differ between these two strategies, but both resulted in greater co-contraction than the resting conditions. Similar levels of multifidus activity were observed between the deep and superficial multifidus fibers. This was consistent across both subject groups indicating that the ADIM and ABM stabilize the spine by activating both layers of the multifidus regardless of the HxLBP status. Multifidus co-contraction was significantly greater in standing than quadruped for the HxLBP subjects. These findings indicate that HxLBP subjects can utilize ADIM and

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ABM contractions to facilitate multifidus contraction that will stabilize the spine in quadruped as well as the more functional position of standing.

Limitations of the Study There are several limitations within these two studies that require recognition. First, placement of the indwelling EMG sensors in the deep multifidus was not visually confirmed using ultrasound. Previous studies have incorporated ultrasound to confirm the location (Moseley et al., 2002). However, the placement methods utilized were consistent with this previous study. Ideally, visual confirmation of fine wire placement would have been confirmed using a diagnostic ultrasound. This was not possible since no ultrasound was available for our use. Second, voluntary contraction intensity for the ADIM and ABM was not controlled, possibly leading to high variability within the subjects and a number of outliers within the data. Contraction intensity could have been controlled to standardize the amount of abdominal muscle activity. Doing so may have reduced variability within the study, but may have caused subjects to contract at an intensity other than the intensity they would self-select during rehabilitation exercises or during functional activities. This would have increased the internal validity while decreasing the external validity of the study. Most variables violated the operational definition of data normality, causing the use of alternate statistical methods (robust statistics). These robust statistics decrease the influence of normality violations. Standardizing the abdominal contraction intensity may have decreased variability, reduced outliers, and ultimately improved normality allowing for the use of standard statistical test usage. However, previous literature demonstrates that even slight deviations from normality have large influences on statistical power and using a sample size of 30 or above based on the central limit theorem does little to normalize the data (Field & Wilcox, 2017). The presence of environmental noise resulted in EMG “noise” at 60 Hz and the harmonics. The utilization of a notch filter at 60 Hz resulted in removing a small portion of valid data from all subjects in the two deep multifidus muscles. Smaller amounts of noise at 120 and 180 Hz were not removed. Furthermore, additional environmental noise was randomly observed at 74 Hz and the harmonics and was not filtered from the EMG signal due to a resultant loss of a large amount of signal surrounding the 60-74 Hz frequencies. These

110 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019 noise frequencies were isolated to the sensors collecting deep multifidus activity and did not affect the surface sensors on the superficial multifidus. Data with representative noise were sent to Delsys for analysis with no resulting suggestion for reducing the 74 Hz noise. Skin prep and EMG reference sensor placement was altered minimally with a resulting slight reduction in 60Hz noise. Regarding subject demographic variables, data were not collected on number of previous LBP episodes to indicate whether subjects in HxLBP group had one-time acute pain or would be classified as recurrent pain sufferers. Data were not collected regarding the side of previous pain location, which may have provided further specificity as to the influence of previous pain. Recall bias may have influenced the subjects’ recollection of painful side and therefore may have influenced the measurement reliability. Future research could assess the influence of current and previous painful side on multifidus co-contraction.

Delimitations of the Study The subjects included in this dissertation comprise a sample of healthy subjects as well as those with a recent history of LBP. As a result, these findings should not be generalized to individuals with current LBP. Subject age range was limited to 18-65 years old for this dissertation. It is not known if individuals outside of this age range have similar co-contraction responses and therefore these results should not be generalized to these populations. In the HxLBP group, time since last LBP episode was variable with one subject being pain free less than one week and the subject having the last pain episode 100 weeks ago. Furthermore, based on the operational definition of no recent history of LBP, subjects were not excluded from the healthy group if they had pain greater than 104 weeks prior to data collection. This resulted in one subject who had LBP 120 weeks prior to data collection. Theoretically, it would be possible to surmise that someone with LBP 100 weeks ago may be more similar to another individual who had pain 120 weeks prior than they would be compared to someone who had LBP less than one week prior. Using a more restricting definition of recent LBP, such that subjects would only be included in the HxLBP group if their pain was within the last six months or one year, may have created a more homogenous subject group. Furthermore, the group without recent LBP could have been limited to those who have never experienced LBP.

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However, this may have been challenging to recruit subjects for this group considering 70-85% of all individuals experience LBP at some point in their lives (Andersson, 1999; van Tulder et al., 2006).

Recommendations for Future Research Voluntary abdominal contractions (ADIM and ABM) have now been shown to result in deep and superficial multifidus contraction in healthy subjects as well as HxLBP subjects. It is not currently possible to say whether the similarity in co-contractive response between the two groups is a result of return to normal after a LBP episode, or if it is due to no change in co-contractive response during LBP episodes. Therefore, future research should address many of these questions in subjects with current acute or chronic LBP to determine how these muscles interact during a pain episode. This dissertation only addressed ADIM and ABM performance during static positions. It is clear that dynamic actions such as the forward lean and picking an object up off the floor are more functional and my result in greater injury risk compared to a static quadruped or standing position. As a result, future studies should assess whether ADIM and ABM related multifidus co-contraction can be maintained during these types of functional and potentially vulnerable positions. In these studies, no differences were observed between the right and left multifidus. No data were collected in the current study to determine the side of previous pain. However, it could be assumed that HxLBP subjects did not all have pain on the same side. Therefore, it is likely subjects within the HxLBP group experienced a variation of right sided, left sided, and bilateral pain. If data had been collected regarding painful side, a comparison could have been made between ipsilateral and contralateral (to the previously painful side) multifidus co-contraction. Further investigation is warranted to determine if side-to-side differences in multifidus co- contraction exist based on pain location.

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References Ainscough-Potts, A.-M., Morrissey, M. C., & Critchley, D. (2006). The response of the transverse abdominis and internal oblique muscles to different postures. Manual Therapy, 11(1), 54–60. http://doi.org/10.1016/j.math.2005.03.007 Andersen, T. B., Essendrop, M., & Schibye, B. (2004). Movement of the upper body and muscle activity patterns following a rapidly applied load: the influence of pre-load alterations. European Journal of Applied Physiology, 91(4), 488–492. http://doi.org/10.1007/s00421-004-1040-6 Andersson, G. B. (1999). Epidemiological features of chronic low-back pain. The Lancet, 354(9178), 581–585. http://doi.org/10.1016/S0140-6736(99)01312-4 Arjmand, N., & Shirazi-Adl, A. (2006). Role of intra-abdominal pressure in the unloading and stabilization of the human spine during static lifting tasks. European Spine Journal, 15(8), 1265–1275. http://doi.org/10.1007/s00586-005-0012-9 Arokoski, J. P., Valta, T., & Airaksinen, O. (2001). Back and abdominal muscle function during stabilization exercises. Archives of Physical Medicine and Rehabilitation. http://doi.org/10.1053/apmr.2001.23819 Baek, Ahn, S. H., Jones, R., Cho, H. K., Jung, G. S., Cho, Y. W., & Tak, H. J. (2014a). Activations of deep lumbar stabilizing muscles by transcutaneous neuromuscular electrical stimulation of lumbar paraspinal regions. Annals of Rehabilitation Medicine, 38(4), 506–8. http://doi.org/10.5535/arm.2014.38.4.506 Baek, Cho, H. K., Jung, G. S., Son, S. M., Cho, Y. W., & Ahn, S. H. (2014b). Verification of an optimized stimulation point on the abdominal wall for transcutaneous neuromuscular electrical stimulation for activation of deep lumbar stabilizing muscles. The Spine Journal: Official Journal of the North American Spine Society, 14(9), 2178–2183. http://doi.org/10.1016/j.spinee.2014.02.016 Barker, Briggs, C. A., & Bogeski, G. (2004a). Tensile transmission across the lumbar fasciae in unembalmed cadavers: effects of tension to various muscular attachments. Spine, 29(2), 129–138. http://doi.org/10.1097/01.BRS.0000107005.62513.32 Barker, Guggenheimer, K. T., Grkovic, I., Briggs, C. A., Jones, D. C., Thomas, C. D. L., & Hodges, P. W. (2006). Effects of tensioning the lumbar fasciae on segmental stiffness during flexion and extension: Young Investigator Award winner. Spine, 31(4), 397–405. http://doi.org/10.1097/01.brs.0000195869.18844.56 Barker, Shamley, D. R., & Jackson, D. (2004b). Changes in the cross-sectional area of multifidus and psoas in patients with unilateral back pain: the relationship to pain and disability. Spine, 29(22), E515–9. Battié, M. C., Niemelainen, R., Gibbons, L. E., & Dhillon, S. (2012). Is level- and side- specific multifidus asymmetry a marker for lumbar disc pathology? The Spine Journal: Official Journal of the North American Spine Society, 12(10), 932–939. http://doi.org/10.1016/j.spinee.2012.08.020

113 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Beneck, G. J., & Kulig, K. (2012). Multifidus atrophy is localized and bilateral in active persons with chronic unilateral low back pain. Archives of Physical Medicine and Rehabilitation, 93(2), 300–306. http://doi.org/10.1016/j.apmr.2011.09.017 Bergmark, A. (1989). Stability of the lumbar spine: a study in mechanical engineering. Acta Orthopaedica. Boccia, G., & Rainoldi, A. (2014). Innervation zones location and optimal electrodes position of obliquus internus and obliquus externus abdominis muscles. Journal of Electromyography and Kinesiology, 24(1), 25–30. http://doi.org/10.1016/j.jelekin.2013.10.017 Bogduk, N., & Macintosh, J. E. (1984). The applied anatomy of the thoracolumbar fascia. Spine, 9(2), 164–170. Bogduk, N., Macintosh, J. E., & Pearcy, M. J. (1992). A universal model of the lumbar back muscles in the upright position. Spine, 17(8), 897–913. Bouche, K. G., Vanovermeire, O., Stevens, V. K., Coorevits, P. L., Caemaert, J. J., Cambier, D. C., et al. (2011). Computed tomographic analysis of the quality of trunk muscles in asymptomatic and symptomatic lumbar discectomy patients. BMC Musculoskeletal Disorders, 12(1), 65. http://doi.org/10.1186/1471-2474-12-65 Bräm, J., Zanetti, M., Min, K., & Hodler, J. (1998). MR abnormalities of the intervertebral disks and adjacent bone marrow as predictors of segmental instability of the lumbar spine. Acta Radiologica (Stockholm, Sweden : 1987), 39(1), 18–23. Brown, S. H. M., Gregory, D. E., Carr, J. A., Ward, S. R., Masuda, K., & Lieber, R. L. (2011). ISSLS prize winner: Adaptations to the multifidus muscle in response to experimentally induced intervertebral disc degeneration. Spine, 36(21), 1728–1736. http://doi.org/10.1097/BRS.0b013e318212b44b Brumagne, S., Cordo, P., & Verschueren, S. (2004). Proprioceptive weighting changes in persons with low back pain and elderly persons during upright standing. Neuroscience Letters, 366(1), 63–66. http://doi.org/10.1016/j.neulet.2004.05.013 Brumagne, S., Janssens, L., Knapen, S., Claeys, K., & Suuden-Johanson, E. (2008). Persons with recurrent low back pain exhibit a rigid postural control strategy. European Spine Journal, 17(9), 1177–1184. http://doi.org/10.1007/s00586-008- 0709-7 Burton, A. K., Clarke, R. D., McClune, T. D., & Tillotson, K. M. (1996). The natural history of low back pain in adolescents. Spine, 21(20), 2323–2328. CDC, F. D. C. A. P. (2001). Prevalence of disabilities and associated health conditions among adults--United States, 1999. JAMA, 285(12), 1568-1572. Cedraschi, C., Robert, J., Goerg, D., Perrin, E., Fischer, W., & Vischer, T. L. (1999). Is chronic non-specific low back pain chronic? Definitions of a problem and problems of a definition. The British Journal of General Practice: the Journal of the Royal College of General Practitioners, 49(442), 358–362.

114 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Chan, S.-T., Fung, P.-K., Ng, N.-Y., Ngan, T.-L., Chong, M.-Y., Tang, C.-N., et al. (2012). Dynamic changes of elasticity, cross-sectional area, and fat infiltration of multifidus at different postures in men with chronic low back pain. The Spine Journal: Official Journal of the North American Spine Society, 12(5), 381–388. http://doi.org/10.1016/j.spinee.2011.12.004 Chiarotto, A., Maxwell, L. J., Terwee, C. B., Wells, G. A., Tugwell, P., & Ostelo, R. W. (2016). Roland-morris disability questionnaire and oswestry disability index: which has better measurement properties for measuring physical functioning in nonspecific low back pain? systematic review and meta-analysis. Physical Therapy. http://doi.org/10.2522/ptj.20150420 Cholewicki, J., & McGill, S. M. (1996). Mechanical stability of the in vivo lumbar spine: implications for injury and chronic low back pain. Clinical Biomechanics, 11(1), 1– 15. http://doi.org/10.1016/0268-0033(95)00035-6 Cholewicki, J., & VanVliet, J. J. (2002). Relative contribution of trunk muscles to the stability of the lumbar spine during isometric exertions. Clinical Biomechanics (Bristol, Avon), 17(2), 99–105. Cholewicki, J., Juluru, K., & McGill, S. M. (1999a). Intra-abdominal pressure mechanism for stabilizing the lumbar spine. Journal of Biomechanics, 32(1), 13–17. Cholewicki, J., Juluru, K., Radebold, A., Panjabi, M. M., & McGill, S. M. (1999b). Lumbar spine stability can be augmented with an abdominal belt and/or increased intra-abdominal pressure. European Spine Journal, 8(5), 388–395. http://doi.org/10.1007/s005860050192 Cholewicki, J., McGill, S. M., & Norman, R. W. (1991). Lumbar spine loads during the lifting of extremely heavy weights. Medicine and Science in Sports and Exercise, 23(10), 1179–1186. Cholewicki, J., Silfies, S. P., Shah, R. A., Greene, H. S., Reeves, Alvi, K., & Goldberg, B. (2005). Delayed trunk muscle reflex responses increase the risk of low back injuries. Spine, 30(23), 2614–2620. Christophy, M., Faruk Senan, N. A., Lotz, J. C., & O’Reilly, O. M. (2012). A musculoskeletal model for the lumbar spine. Biomechanics and Modeling in Mechanobiology, 11(1-2), 19–34. http://doi.org/10.1007/s10237-011-0290-6 Cook, C., Brismée, J.-M., & Sizer, P. S., Jr. (2006). Subjective and objective descriptors of clinical lumbar spine instability: A Delphi study. Manual Therapy, 11(1), 11–21. http://doi.org/10.1016/j.math.2005.01.002 Costi, J. J., Stokes, I. A., Gardner-Morse, M., Laible, J. P., Scoffone, H. M., & Iatridis, J. C. (2007). Direct measurement of intervertebral disc maximum shear strain in six degrees of freedom: Motions that place disc tissue at risk of injury. Journal of Biomechanics, 40(11), 2457–2466. http://doi.org/10.1016/j.jbiomech.2006.11.006 Cowan, S. M., Schache, A. G., & Brukner, P. (2004). Delayed onset of transversus abdominus in long-standing groin pain. Medicine & Science in Sport and Exercise http://doi.org/10.1249/01.MSS.0000147587.81762.44 115 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Crisco, J. J. I., & Panjabi, M. M. (1991). The Intersegmental and multisegmental muscles of the lumbar spine: a biomechanical model comparing lateral stabilizing potential. Spine, 16(7), 793. Crisco, J. J., Panjabi, M. M., Yamamoto, I., & Oxland, T. R. (1992). Euler stability of the human ligamentous lumbar spine. Part II: Experiment. Clinical Biomechanics (Bristol, Avon), 7(1), 27–32. http://doi.org/10.1016/0268-0033(92)90004-N D'hooge, R., Cagnie, B., Crombez, G., Vanderstraeten, G., Dolphens, M., & Danneels, L. (2012). Increased intramuscular fatty infiltration without differences in lumbar muscle cross-sectional area during remission of unilateral recurrent low back pain. Manual Therapy, 17(6), 584–588. http://doi.org/10.1016/j.math.2012.06.007 D'hooge, R., Hodges, P., Tsao, H., Hall, L., MacDonald, D., & Danneels, L. (2013). Altered trunk muscle coordination during rapid trunk flexion in people in remission of recurrent low back pain. Journal of Electromyography and Kinesiology, 23(1), 173–181. http://doi.org/10.1016/j.jelekin.2012.09.003 Dagenais, S., Caro, J., & Haldeman, S. (2008). A systematic review of low back pain cost of illness studies in the United States and internationally. The Spine Journal, 8(1), 8– 20. http://doi.org/10.1016/j.spinee.2007.10.005 Daggfeldt, K., Huang, Q. M., & Thorstensson, A. (2000). The visible human anatomy of the lumbar erector spinae. Spine, 25(21), 2719–2725. Dankaerts, W., O'Sullivan, P., Burnett, A., & Straker, L. (2006). Altered patterns of superficial trunk muscle activation during sitting in nonspecific chronic low back pain patients: importance of subclassification. Spine, 31(17), 2017–2023. http://doi.org/10.1097/01.brs.0000228728.11076.82 Dankaerts, W., O’Sullivan, P. B., Burnett, A. F., Straker, L. M., & Danneels, L. A. (2004). Reliability of EMG measurements for trunk muscles during maximal and sub-maximal voluntary isometric contractions in healthy controls and CLBP patients. Journal of Electromyography and Kinesiology, 14(3), 333–342. http://doi.org/10.1016/j.jelekin.2003.07.001 Danneels, L. A., Vanderstraeten, G. G., Cambier, D. C., Witvrouw, E. E., & de Cuyper, H. J. (2000). CT imaging of trunk muscles in chronic low back pain patients and healthy control subjects. European Spine Journal, 9(4), 266–272. Davidson, M., & Keating, J. L. (2002). A comparison of five low back disability questionnaires: reliability and responsiveness. Physical Therapy, 82(1), 8–24. Dawson, A. P., Steele, E. J., Hodges, P. W., & Stewart, S. (2010). Utility of the Oswestry Disability Index for studies of back pain related disability in nurses: evaluation of psychometric and measurement properties. International Journal of Nursing Studies, 47(5), 604–607. http://doi.org/10.1016/j.ijnurstu.2009.10.013 De Luca, C. J. (1997). The use of surface electromyography in biomechanics. Journal of Applied Biomechanics, 13, 135-163.

116 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Delp, S. L., Suryanarayanan, S., Murray, W. M., Uhlir, J., & Triolo, R. J. (2001). Architecture of the rectus abdominis, quadratus lumborum, and erector spinae. Journal of Biomechanics, 34(3), 371–375. Descarreaux, M., Lalonde, C., & Normand, M. C. (2007). Isometric force parameters and trunk muscle recruitment strategies in a population with low back pain. Journal of Manipulative and Physiological Therapeutics, 30(2), 91–97. http://doi.org/10.1016/j.jmpt.2006.12.016 Deyo, R. A., & Phillips, W. R. (1996). Low back pain. A primary care challenge. Spine, 21(24), 2826–2832. Deyo, R. A., Mirza, S. K., & Martin, B. I. (2006). Back pain prevalence and visit rates: estimates from U.S. national surveys, 2002. Spine, 31(23), 2724–2727. http://doi.org/10.1097/01.brs.0000244618.06877.cd Dickx, N., Cagnie, B., Achten, E., Vandemaele, P., Parlevliet, T., & Danneels, L. (2008). Changes in lumbar muscle activity because of induced muscle pain evaluated by muscle functional magnetic resonance imaging. Spine, 33(26), E983–9. http://doi.org/10.1097/BRS.0b013e31818917d0 Dickx, N., Cagnie, B., Achten, E., Vandemaele, P., Parlevliet, T., & Danneels, L. (2010a). Differentiation between deep and superficial fibers of the lumbar multifidus by magnetic resonance imaging. European Spine Journal, 19(1), 122–128. http://doi.org/10.1007/s00586-009-1171-x Dickx, N., Cagnie, B., Parlevliet, T., Lavens, A., & Danneels, L. (2010b). The effect of unilateral muscle pain on recruitment of the lumbar multifidus during automatic contraction. An experimental pain study. Manual Therapy, 15(4), 364–369. http://doi.org/10.1016/j.math.2010.02.002 Erceg-Hurn, D. M., & Mirosevich, V. M. (2008). Modern robust statistical methods: an easy way to maximize the accuracy and power of your research. The American Psychologist, 63(7), 591–601. http://doi.org/10.1037/0003-066X.63.7.591 Fairbank, & Pynsent, P. B. (2000). The Oswestry disability index. Spine, 25(22),2940- 2953. Fairbank, Couper, J., Davies, J., & OBrien, J. (1980). The Oswestry Low Back Pain Questionnaire. Physiotherapy, 66(8), 271–273. Field, A. P., & Wilcox, R. R. (2017). Robust statistical methods: A primer for clinical psychology and experimental psychopathology researchers. Behaviour Research and Therapy, 98, 19–38. http://doi.org/10.1016/j.brat.2017.05.013 Fortin, M., & Macedo, L. G. (2013). Multifidus and paraspinal muscle group cross- sectional areas of patients with low back pain and control patients: a systematic review with a focus on blinding. Physical Therapy, 93(7), 873–888. http://doi.org/10.2522/ptj.20120457 Frank. (1993). Low back pain. BMJ (Clinical Research Ed.), 306(6882), 901–909.

117 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Freburger, J. K., Holmes, G. M., Agans, R. P., Jackman, A. M., Darter, J. D., Wallace, A. S., et al. (2009). The rising prevalence of chronic low back pain. Archives of Internal Medicine, 169(3), 251–258. http://doi.org/10.1001/archinternmed.2008.543 French, France, C. R., Vigneau, F., French, J. A., & Evans, T. R. (2007). Fear of movement/(re)injury in chronic pain: A psychometric assessment of the original English version of the Tampa scale for kinesiophobia (TSK). Pain, 127(1), 42–51. http://doi.org/10.1016/j.pain.2006.07.016 Friedman, B. W., Chilstrom, M., Bijur, P. E., & Gallagher, E. J. (2010). Diagnostic testing and treatment of low back pain in United States emergency departments: a national perspective. Spine, 35(24), E1406–11. http://doi.org/10.1097/BRS.0b013e3181d952a5 Gardner-Morse, M. G., & Stokes, I. A. (1998). The effects of abdominal muscle coactivation on lumbar spine stability. Spine, 23(1), 86–91– discussion 91–2. Gedalia, U., Solomonow, M., Zhou, B. H., Baratta, R. V., Lu, Y., & Harris, M. (1999). Biomechanics of increased exposure to lumbar injury caused by cyclic loading. Part 2. Recovery of reflexive muscular stability with rest. Spine, 24(23), 2461–2467. Gracovetsky, S., Farfan, H., & Helleur, C. (1985). The abdominal mechanism. Spine, 10(4), 317–324. Grenier, S. G., & McGill, S. M. (2007). Quantification of Lumbar Stability by Using 2 Different Abdominal Activation Strategies. Archives of Physical Medicine and Rehabilitation, 88(1), 54–62. http://doi.org/10.1016/j.apmr.2006.10.014 Ham, Y. W., Kim, D. M., Baek, J. Y., Lee, D. C., & Sung, P. S. (2010). Kinematic analyses of trunk stability in one leg standing for individuals with recurrent low back pain. Journal of Electromyography and Kinesiology, 1–7. http://doi.org/10.1016/j.jelekin.2010.05.011 Hansen, L., de Zee, M., Rasmussen, J., Andersen, T. B., Wong, C., & Simonsen, E. B. (2006). Anatomy and biomechanics of the back muscles in the lumbar spine with reference to biomechanical modeling. Spine, 31(17), 1888–1899. http://doi.org/10.1097/01.brs.0000229232.66090.58 Haro, H., Maekawa, S., & Hamada, Y. (2008). Prospective analysis of clinical evaluation and self-assessment by patients after decompression surgery for degenerative lumbar canal stenosis. The Spine Journal, 8(2), 380–384. http://doi.org/10.1016/j.spinee.2007.01.010 Hart, L. G., Deyo, R. A., & Cherkin, D. C. (1995). Physician office visits for low back pain. Frequency, clinical evaluation, and treatment patterns from a U.S. national survey. Spine, 20(1), 11–19. Henchoz, Y., & So, A. K.-L. (2008). Exercise and nonspecific low back pain: A literature review. Joint Bone Spine, 75(5), 533–539. http://doi.org/10.1016/j.jbspin.2008.03.003

118 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Henry, S. M., Hitt, J. R., Jones, S. L., & Bunn, J. Y. (2006). Decreased limits of stability in response to postural perturbations in subjects with low back pain. Clinical Biomechanics, 21(9), 881–892. http://doi.org/10.1016/j.clinbiomech.2006.04.016 Hestbaek, L., Leboeuf-Yde, C., Engberg, M., Lauritzen, T., Bruun, N. H., & Manniche, C. (2003). The course of low back pain in a general population. Results from a 5-year prospective study. Journal of Manipulative and Physiological Therapeutics, 26(4), 213–219. Hides, J. A., Jull, G. A., & Richardson, C. A. (2001). Long-term effects of specific stabilizing exercises for first-episode low back pain. Spine, 26(11), E243–8. Hides, J. A., Richardson, C. A., & Jull, G. A. (1996). Multifidus muscle recovery is not automatic after resolution of acute, first‐episode low back pain. Spine, 21(23), 2763. Hides, J. A., Stokes, M. J., Saide, M., Jull, G. A., & Cooper, D. H. (1994). Evidence of lumbar multifidus muscle wasting ipsilateral to symptoms in patients with acute/subacute low back pain. Spine, 19(2), 165–172. Hides, J., Gilmore, C., Stanton, W., & Bohlscheid, E. (2008a). Multifidus size and symmetry among chronic LBP and healthy asymptomatic subjects. Manual Therapy, 13(1), 43–49. http://doi.org/10.1016/j.math.2006.07.017 Hides, J., Stanton, W., Dilani Mendis, M., & Sexton, M. (2011). The relationship of transversus abdominis and lumbar multifidus clinical muscle tests in patients with chronic low back pain. Manual Therapy, 16(6), 573–577. http://doi.org/10.1016/j.math.2011.05.007 Hides, J., Stanton, W., Freke, M., Wilson, S., McMahon, S., & Richardson, C. (2008b). MRI study of the size, symmetry and function of the trunk muscles among elite cricketers with and without low back pain. British Journal of Sports Medicine, 42(10), 509–513. http://doi.org/10.1136/bjsm.2007.044024 Hides, J., Wilson, S., Stanton, W., McMahon, S., Keto, H., McMahon, K., et al. (2006). An MRI investigation into the function of the transversus abdominis muscle during “drawing-in” of the abdominal wall. Spine, 31(6), E175–8. http://doi.org/10.1097/01.brs.0000202740.86338.df Hodges, P. W. (1999). Is there a role for transversus abdominis in lumbo-pelvic stability? Manual Therapy, 4(2), 74–86. http://doi.org/10.1054/math.1999.0169 Hodges, P. W., & Bui, B. H. (1996). A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. Electroencephalography and Clinical Neurophysiology, 101(6), 511–519. Hodges, P. W., & Richardson, C. A. (1996). Inefficient muscular stabilization of the lumbar spine associated with low back pain: A motor control evaluation of transversus abdominis. Spine, 21(22), 2640.

119 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Hodges, P. W., & Richardson, C. A. (1997). Feedforward contraction of transversus abdominis is not influenced by the direction of arm movement. Experimental Brain Research, 114(2), 362–370. Hodges, P. W., & Tucker, K. (2011). Moving differently in pain: A new theory to explain the adaptation to pain. Pain, 152(S), S90–S98. http://doi.org/10.1016/j.pain.2010.10.020 Hodges, P. W., James, G., Blomster, L., Hall, L., Schmid, A., Shu, C., et al. (2015). Multifidus muscle changes after back injury are characterized by structural remodeling of muscle, adipose and connective tissue, but not muscle atrophy. Spine, 1–37. http://doi.org/10.1097/BRS.0000000000000972 Hodges, P., Holm, A. K., Hansson, T., & Holm, S. (2006). Rapid atrophy of the lumbar multifidus follows experimental disc or nerve root injury. Spine, 31(25), 2926–2933. http://doi.org/10.1097/01.brs.0000248453.51165.0b Holm, S., Indahl, A., & Solomonow, M. (2002). Sensorimotor control of the spine. Journal of Electromyography and Kinesiology, 12(3), 219–234. Huebner, A., Faenger, B., Schenk, P., Scholle, H.-C., & Anders, C. (2015). Alteration of Surface EMG amplitude levels of five major trunk muscles by defined electrode location displacement. Journal of Electromyography and Kinesiology, 25(2), 214– 223. http://doi.org/10.1016/j.jelekin.2014.11.008 Indahl, A., Velund, L., & Reikeraas, O. (1995). Good prognosis for low back pain when left untampered. A randomized clinical trial. Spine, 20(4), 473–477. Ivancic, P. C., Cholewicki, J., & Radebold, A. (2002). Effects of the abdominal belt on muscle-generated spinal stability and L4/L5 joint compression force. Ergonomics, 45(7), 501–513. http://doi.org/10.1080/00140130210136035 Jemmett, R. S., MacDonald, D. A., & Agur, A. M. R. (2004). Anatomical relationships between selected segmental muscles of the lumbar spine in the context of multi- planar segmental motion: a preliminary investigation. Manual Therapy, 9(4), 203– 210. http://doi.org/10.1016/j.math.2004.07.006 Kaigle, A. M., Holm, S. H., & Hansson, T. H. (1995). Experimental instability in the lumbar spine. Spine, 20(4), 421–430. Katz, J. N. (2006). Lumbar Disc Disorders and Low-Back Pain: Socioeconomic Factors and Consequences. The Journal of Bone and Joint Surgery (American), 88(suppl 2), 21–24. http://doi.org/10.2106/JBJS.E.01273 Kavcic, N., Grenier, S., & McGill, S. M. (2004). Quantifying tissue loads and spine stability while performing commonly prescribed low back stabilization exercises. Spine, 29(20), 2319–2329. Kibler, W. B., Press, J., & Sciascia, A. (2006). The role of core stability in athletic function. Sports Medicine, 36(3), 189–198.

120 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Kjaer, P., Bendix, T., Sorensen, J. S., Korsholm, L., & Leboeuf-Yde, C. (2007). Are MRI-defined fat infiltrations in the multifidus muscles associated with low back pain? BMC Medicine, 5, 2. http://doi.org/10.1186/1741-7015-5-2 Kulig, K., Scheid, A. R., Beauregard, R., Popovich, J. M., Jr, Beneck, G. J., & Colletti, P. M. (2009). Multifidus morphology in persons scheduled for single-level lumbar microdiscectomy. American Journal of Physical Medicine & Rehabilitation, 88(5), 355–361. http://doi.org/10.1097/PHM.0b013e31819c506d Lariviere, C., Arsenault, A. B., Gravel, D., & Gagnon, D. (2002). Evaluation of measurement strategies to increase the reliability of EMG indices to assess back muscle fatigue and recovery. Journal of Electromyography and Kinesiology, 12(2), 91–102. http://doi.org/10.1016/S1050-6411(02)00011-1 Larivière, C., Arsenault, A. B., Gravel, D., Gagnon, D., & Loisel, P. (2003). Surface electromyography assessment of back muscle intrinsic properties. Journal of Electromyography and Kinesiology, 13(4), 305–318. http://doi.org/10.1016/S1050- 6411(03)00039-7 Learman, K. E., Myers, J. B., Lephart, S. M., Sell, T. C., Kerns, G. J., & Cook, C. E. (2009). Effects of spinal manipulation on trunk proprioception in subjects with chronic low back pain during symptom remission. Journal of Manipulative and Physiological Therapeutics, 32(2), 118–126. http://doi.org/10.1016/j.jmpt.2008.12.004 Lee, Cha, J.-G., Kim, Y., Kim, Y.-I., & Shin, B.-J. (2008). Quantitative analysis of back muscle degeneration in the patients with the degenerative lumbar flat back using a digital image analysis: comparison with the normal controls. Spine, 33(3), 318–325. http://doi.org/10.1097/BRS.0b013e318162458f Lee, Cholewicki, J., Reeves, N. P., Zazulak, B. T., & Mysliwiec, L. W. (2010). Comparison of Trunk Proprioception Between Patients With Low Back Pain and Healthy Controls. Archives of Physical Medicine and Rehabilitation, 91(9), 1327– 1331. http://doi.org/10.1016/j.apmr.2010.06.004 Leinonen, V., Kankaanpää, M., Luukkonen, M., Hänninen, O., Airaksinen, O., & Taimela, S. (2001). Disc herniation-related back pain impairs feed-forward control of paraspinal muscles. Spine, 26(16), E367–72. Leinonen, V., Kankaanpää, M., Luukkonen, M., Kansanen, M., Hänninen, O., Airaksinen, O., & Taimela, S. (2003). Lumbar paraspinal muscle function, perception of lumbar position, and postural control in disc herniation-related back pain. Spine, 28(8), 842–848. Liebetrau, A., Puta, C., Anders, C., de Lussanet, M. H. E., & Wagner, H. (2013). Influence of delayed muscle reflexes on spinal stability: model-based predictions allow alternative interpretations of experimental data. Human Movement Science, 32(5), 954–970. http://doi.org/10.1016/j.humov.2013.03.006

121 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Lund, J. P., Donga, R., & Widmer, C. G. (1991). The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity. Canadian Journal of …, 69(5), 683–694. http://doi.org/10.1139/y91-102 Luo, X., Pietrobon, R., Sun, S. X., Liu, G. G., & Hey, L. (2004). Estimates and patterns of direct health care expenditures among individuals with back pain in the United States. Spine, 29(1), 79–86. http://doi.org/10.1097/01.BRS.0000105527.13866.0F Macdonald, D. A., Dawson, A. P., & Hodges, P. W. (2011). Behavior of the lumbar multifidus during lower extremity movements in people with recurrent low back pain during symptom remission. Journal of Orthopaedic & Sports Physical Therapy, 41(3), 155–164. http://doi.org/10.2519/jospt.2011.3410 MacDonald, D. A., Lorimer Moseley, G., & Hodges, P. W. (2006). The lumbar multifidus: Does the evidence support clinical beliefs? Manual Therapy, 11(4), 254– 263. http://doi.org/10.1016/j.math.2006.02.004 MacDonald, D., Moseley, G. L., & Hodges, P. W. (2009). Why do some patients keep hurting their back? Evidence of ongoing back muscle dysfunction during remission from recurrent back pain. Pain, 142(3), 183–188. http://doi.org/10.1016/j.pain.2008.12.002 MacDonald, D., Moseley, G. L., & Hodges, P. W. (2010). People with recurrent low back pain respond differently to trunk loading despite remission from symptoms. Spine, 35(7), 818–824. http://doi.org/10.1097/BRS.0b013e3181bc98f1 Macedo, L. G., Maher, C. G., Hancock, M. J., Kamper, S. J., McAuley, J. H., Stanton, T. R., et al. (2014). Predicting response to motor control exercises and graded activity for patients with low back pain: Preplanned secondary analysis of a randomized controlled trial. Physical Therapy, 94(11), 1543–1554. http://doi.org/10.2522/ptj.20140014 Macintosh, J. E., & Bogduk, N. (1986). The biomechanics of the lumbar multifidus. Clinical Biomechanics (Bristol, Avon), 1(4), 205–213. http://doi.org/10.1016/0268- 0033(86)90147-6 Macintosh, J. E., Bogduk, N., & Gracovetsky, S. (1987). The biomechanics of the thoracolumbar fascia. Clinical Biomechanics (Bristol, Avon), 2(2), 78–83. http://doi.org/10.1016/0268-0033(87)90132-X Macintosh, J. E., Valencia, F., Bogduk, N., & Munro, R. R. (1986). The morphology of the human lumbar multifidus. Clinical Biomechanics (Bristol, Avon), 1(4), 196–204. http://doi.org/10.1016/0268-0033(86)90146-4 Marshall, P., & Murphy, B. (2003). The validity and reliability of surface EMG to assess the neuromuscular response of the abdominal muscles to rapid limb movement. Journal of Electromyography and Kinesiology, 13(5), 477–489. http://doi.org/10.1016/S1050-6411(03)00027-0 Matthijs, O. C. G., Dedrick, G. S., James, C. R., Brismée, J.-M., Hooper, T. L., McGalliard, M. K., & Sizer, P. S. (2014). Co-contractive activation of the superficial multifidus during volitional preemptive abdominal contraction. PM&R: the Journal 122 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

of Injury, Function, and Rehabilitation, 6(1), 13–21. http://doi.org/10.1016/j.pmrj.2013.08.606 McGalliard, M. K., Dedrick, G. S., Brismée, J. M., Cook, C. E., Apte, G. G., & Sizer, P. S. (2010). Changes in transversus abdominis thickness with use of the abdominal drawing-in maneuver during a functional task. PM&R, 2(3), 187–194. http://doi.org/10.1016/j.pmrj.2010.01.015 McGaugh, J. M., Brismée, J. M., Dedrick, G. S., Jones, E. A., & Sizer, P. S. (2007). Comparing the anatomical consistency of the posterior superior iliac spine to the iliac crest as reference landmarks for the lumbopelvic spine: a retrospective radiological study. Clinical Anatomy, 20(7), 819–825. http://doi.org/10.1002/ca.20531 McGill, S. M., & Cholewicki, J. (2001). Biomechanical basis for stability: an explanation to enhance clinical utility. Journal of Orthopaedic & Sports Physical Therapy, 31(2), 96–100. http://doi.org/10.2519/jospt.2001.31.2.96 McGill, S. M., & Norman, R. W. (1986). Partitioning of the L4-L5 dynamic moment into disc, ligamentous, and muscular components during lifting. Spine, 11(7), 666–678. McGill, S. M., Grenier, S., Kavcic, N., & Cholewicki, J. (2003). Coordination of muscle activity to assure stability of the lumbar spine. Journal of Electromyography and Kinesiology, 13(4), 353–359. http://doi.org/10.1016/S1050-6411(03)00043-9 McGill, S., Juker, D., & Kropf, P. (1996a). Appropriately placed surface EMG electrodes reflect deep muscle activity (psoas, quadratus lumborum, abdominal wall) in the lumbar spine. Journal of Biomechanics, 29(11), 1503–1507. McGill, S., Juker, D., & Kropf, P. (1996b). Quantitative intramuscular myoelectric activity of quadratus lumborum during a wide variety of tasks. Clinical Biomechanics (Bristol, Avon), 11(3), 170–172. Mehling, W. E., Gopisetty, V., Acree, M., Pressman, A., Carey, T., Goldberg, H., et al. (2011). Acute low back pain and primary care. Spine, 36(26), 2316–2323. http://doi.org/10.1097/BRS.0b013e31820c01a6 Mehta, R., Cannella, M., Smith, S. S., & Silfies, S. P. (2010). Altered trunk motor planning in patients with nonspecific low back pain. Journal of Motor Behavior, 42(2), 135–144. http://doi.org/10.1080/00222891003612789 Mengiardi, B., Schmid, M. R., Boos, N., Pfirrmann, C. W. A., Brunner, F., Elfering, A., & Hodler, J. (2006). Fat content of lumbar paraspinal muscles in patients with chronic low back pain and in asymptomatic volunteers: quantification with mr spectroscopy 1. Radiology, 240(3), 786–792. http://doi.org/10.1148/radiol.2403050820 Mientjes, M. I., & Frank, J. S. (1999). Balance in chronic low back pain patients compared to healthy people under various conditions in upright standing. Clinical Biomechanics (Bristol, Avon), 14(10), 710–716. Miller, R. P., Kori, S. H., & Todd, D. D. (1991). The Tampa Scale. Tampa, Fla.

123 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Moseley, G. L., Hodges, P. W., & Gandevia, S. C. (2002). Deep and superficial fibers of the lumbar multifidus muscle are differentially active during voluntary arm movements. Spine, 27(2), E29–36. Moseley, G. L., Hodges, P. W., & Gandevia, S. C. (2003). External perturbation of the trunk in standing humans differentially activates components of the medial back muscles. The Journal of Physiology, 547(Pt 2), 581–587. http://doi.org/10.1113/jphysiol.2002.024950 Nabavi, N., Mosallanezhad, Z., Haghighatkhah, H. R., & Mohseni Bandpeid, M. A. (2014). Reliability of rehabilitative ultrasonography to measure transverse abdominis and multifidus muscle dimensions. Iranian Journal of Radiology, 11(3), 1–4. http://doi.org/10.5812/iranjradiol.21008 Nagar, V. R., Hooper, T. L., Dedrick, G. S., Brismée, J.-M., & Sizer, P. S., Jr. (2014). Effect of recurrent low back pain history on volitional pre-emptive abdominal activation during a loaded functional reach activity. Spine, 39(2), E89–E96. http://doi.org/10.1097/BRS.0000000000000091 Navalgund, A., Buford, J. A., Briggs, M. S., & Givens, D. L. (2013). Trunk muscle reflex amplitudes increased in patients with subacute, recurrent LBP treated with a 10-week stabilization exercise program. Motor Control, 17(1), 1–17. Nordander, C., Willner, J., Hansson, G., Larsson, B., Unge, J., Granquist, L., & Skerfving, S. (2003). Influence of the subcutaneous fat layer, as measured by ultrasound, skinfold calipers and BMI, on the EMG amplitude. European Journal of Applied Physiology, 89(6), 514–519. http://doi.org/10.1007/s00421-003-0819-1 O'Sullivan, P. (2005). Diagnosis and classification of chronic low back pain disorders: Maladaptive movement and motor control impairments as underlying mechanism. Manual Therapy, 10(4), 242–255. http://doi.org/10.1016/j.math.2005.07.001 O'Sullivan, P. B. (2000). Masterclass. Lumbar segmental “instability”: clinical presentation and specific stabilizing exercise management. Manual Therapy, 5(1), 2– 12. http://doi.org/10.1054/math.1999.0213 O'Sullivan, P. B., Phyty, G. D., Twomey, L. T., & Allison, G. T. (1997). Evaluation of specific stabilizing exercise in the treatment of chronic low back pain with radiologic diagnosis of spondylolysis or spondylolisthesis. Spine, 22(24), 2959–2967. O’Sullivan, P. B., Burnett, A., Floyd, A. N., Gadsdon, K., Logiudice, J., Miller, D., & Quirke, H. (2003). Lumbar repositioning deficit in a specific low back pain population. Spine, 28(10), 1074–1079. http://doi.org/10.1097/01.BRS.0000061990.56113.6F O’Sullivan, P. B., Grahamslaw, K. M., Kendell, M., Lapenskie, S. C., Möller, N. E., & Richards, K. V. (2002). The effect of different standing and sitting postures on trunk muscle activity in a pain-free population. Spine, 27(11), 1238–1244. Panjabi, M. M. (1992a). The stabilizing system of the spine. Part I. Function, dysfunction, adaptation, and enhancement. Journal of Spinal Disorders, 5(4), 383–9– discussion 397. 124 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Panjabi, M. M. (1992b). The stabilizing system of the spine. Part II. Neutral zone and instability hypothesis. Journal of Spinal Disorders & Techniques, 5(4), 390. Panjabi, M. M. (1994). Lumbar spine instability: a biochemical challenge. Current Orthopaedics, 8(2), 100–105. http://doi.org/10.1016/S0268-0890(05)80060-X Panjabi, M. M. (2006). A hypothesis of chronic back pain: ligament subfailure injuries lead to muscle control dysfunction. European Spine Journal, 15(5), 668–676. http://doi.org/10.1007/s00586-005-0925-3 Panjabi, M., Abumi, K., Duranceau, J., & Oxland, T. (1989). Spinal stability and intersegmental muscle forces. A biomechanical model. Spine, 14(2), 194–200. Park, Tsao, H., Cresswell, A. G., & Hodges, P. W. (2012). Differential activity of regions of the psoas major and quadratus lumborum during submaximal isometric trunk efforts. Journal of Orthopaedic Research, 30(2), 311–318. http://doi.org/10.1002/jor.21499 Park, Tsao, H., Cresswell, A. G., & Hodges, P. W. (2013). Changes in direction-specific activity of psoas major and quadratus lumborum in people with recurring back pain differ between muscle regions and patient groups. Journal of Electromyography and Kinesiology, 23(3), 734–740. http://doi.org/10.1016/j.jelekin.2013.01.010 Park, Tsao, H., Cresswell, A. G., & Hodges, P. W. (2014). Anticipatory postural activity of the deep trunk muscles differs between anatomical regions based on their mechanical advantage. Neuroscience, 261(C), 161–172. http://doi.org/10.1016/j.neuroscience.2013.12.037 Pitcher, M. J., Behm, D. G., & MacKinnon, S. N. (2008). Reliability of electromyographic and force measures during prone isometric back extension in subjects with and without low back pain. Applied Physiology, Nutrition, and Metabolism, 33(1), 52–60. http://doi.org/10.1139/H07-132 Pool-Goudzwaard, A. L., Vleeming, A., & Stoeckart, R. (1998). Insufficient lumbopelvic stability: a clinical, anatomical and biomechanical approach to “a-specific”low back pain. Manual Therapy, 3(1), 12–20. http://doi.org/10.1054/math.1998.0311 Pope, M. H., & Panjabi, M. (1985). Biomechanical definitions of spinal instability. Spine, 10(3), 255-256. Portney, L. G., & Watkins, M. P. (2009). Foundations of clinical research: applications to practice. Pearson Education, Inc. Radebold, A., Cholewicki, J., Polzhofer, G. K., & Greene, H. S. (2001). Impaired postural control of the lumbar spine is associated with delayed muscle response times in patients with chronic idiopathic low back pain. Spine, 26(7), 724–730. Reddell, C. R., Congleton, J. J., Dale Huchingson, R., & Montgomery, J. F. (1992). An evaluation of a weightlifting belt and back injury prevention training class for airline baggage handlers. Applied Ergonomics, 23(5), 319–329.

125 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Reeves, Cholewicki, J., & Narendra, K. S. (2009). Effects of reflex delays on postural control during unstable seated balance. Journal of Biomechanics, 42(2), 164–170. http://doi.org/10.1016/j.jbiomech.2008.10.016 Reeves, Narendra, K. S., & Cholewicki, J. (2007). Spine stability: the six blind men and the elephant. Clinical Biomechanics (Bristol, Avon), 22(3), 266–274. http://doi.org/10.1016/j.clinbiomech.2006.11.011 Richardson, C. A., & Jull, G. A. (1995). Muscle control-pain control. What exercises would you prescribe? Manual Therapy, 1(1), 2–10. http://doi.org/10.1054/math.1995.0243 Richardson, C. A., Snijders, C. J., Hides, J. A., Damen, L., Pas, M. S., & Storm, J. (2002). The relation between the transversus abdominis muscles, sacroiliac joint mechanics, and low back pain. Spine, 27(4), 399–405. Roland, M. O. (1986). A critical review of the evidence for a pain-spasm-pain cycle in spinal disorders. Clinical Biomechanics (Bristol, Avon), 1(2), 102–109. http://doi.org/10.1016/0268-0033(86)90085-9 Rosatelli, A. L., & Ravichandiran, K. (2008). Three-dimensional study of the musculotendinous architecture of lumbar multifidus and its functional implications. Clinical Anatomy, 21, 539-546. Saragiotto, B. T., Maher, C. G., New, C. H., Catley, M., Hancock, M. J., Cook, C., & Hodges, P. W. (2018). Clinimetric testing of the lumbar spine instability questionnaire. Journal of Orthopaedic & Sports Physical Therapy, 1–24. http://doi.org/10.2519/jospt.2018.7866 Shahvarpour, A., Shirazi-Adl, A., Larivière, C., & Bazrgari, B. (2015). Trunk active response and spinal forces in sudden forward loading – analysis of the role of perturbation load and pre-perturbation conditions by a kinematics-driven model. Journal of Biomchanics, 48(1), 44–52. http://doi.org/10.1016/j.jbiomech.2014.11.006 Shumway-Cook, A., & Woollacott, M. H. (2012). Motor control: translating research into clinical practice (Fourth). Baltimore. Silfies, S. P., Mehta, R., Smith, S. S., & Karduna, A. R. (2009). Differences in feedforward trunk muscle activity in subgroups of patients with mechanical low back pain. Archives of Physical Medicine and Rehabilitation, 90(7), 1159–1169. http://doi.org/10.1016/j.apmr.2008.10.033 Sipko, T., & Kuczyński, M. (2013). The effect of chronic pain intensity on the stability limits in patients with low back pain. Journal of Manipulative and Physiological Therapeutics, 36(9), 612–618. http://doi.org/10.1016/j.jmpt.2013.08.005 Sirca. (1985). The fibre type composition of thoracic and lumbar paravertebral muscles in man. Journal of Anatomy, 141, 131–137. Solomonow, M., Baratta, R. V., Zhou, B. H., Burger, E., Zieske, A., & Gedalia, A. (2003). Muscular dysfunction elicited by creep of lumbar viscoelastic tissue. Journal

126 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

of Electromyography and Kinesiology, 13(4), 381–396. http://doi.org/10.1016/S1050-6411(03)00045-2 Solomonow, M., Zhou, B. H., Harris, M., Lu, Y., & Baratta, R. V. (1998). The ligamento-muscular stabilizing system of the spine. Spine, 23(23), 2552–2562. Solomonow, M., Zhou, B.-H., Baratta, R. V., Lu, Y., & Harris, M. (1999). 1999 Volvo Award Winner in Biomechanical Studies: Biomechanics of increased exposure to lumbar injury caused by cyclic loading: Part 1. Loss of reflexive muscular stabilization. Spine, 24(23), 2426. Standring, S., & Gray, H. (2008). Gray's Anatomy: The Anatomical Basis of Clinical Practice (40 ed.). Edinburgh: Churchill Livingstone/Elsevier. Stanton, & Kawchuk, G. (2008). The effect of abdominal stabilization contractions on posteroanterior spinal stiffness. Spine, 33(6), 694–701. http://doi.org/10.1097/BRS.0b013e318166e034 Stanton, Latimer, J., Maher, C. G., & Hancock, M. J. (2011). A modified Delphi approach to standardize low back pain recurrence terminology. European Spine Journal, 20(5), 744–752. http://doi.org/10.1007/s00586-010-1671-8 Stokes, Gardner-Morse, M. G., & Henry, S. M. (2011). Abdominal muscle activation increases lumbar spinal stability: Analysis of contributions of different muscle groups. Clinical Biomechanics (Bristol, Avon), 26(8), 797–803. http://doi.org/10.1016/j.clinbiomech.2011.04.006 Suehiro, T., Mizutani, M., Ishida, H., Kobara, K., Osaka, H., & Watanabe, S. (2015). Individuals with chronic low back pain demonstrate delayed onset of the back muscle activity during prone hip extension. Journal of Electromyography and Kinesiology, 25(4), 675–680. http://doi.org/10.1016/j.jelekin.2015.04.013 Sung, P. S., Yoon, B., & Lee, D. C. (2010). Lumbar spine stability for subjects with and without low back pain during one-leg standing test. Spine, 35(16), E753–60. http://doi.org/10.1097/BRS.0b013e3181d53b9c Swinkels-Meewisse, E. J. C. M., Swinkels, R. A. H. M., Verbeek, A. L. M., Vlaeyen, J. W. S., & Oostendorp, R. A. B. (2003). Psychometric properties of the Tampa Scale for kinesiophobia and the fear-avoidance beliefs questionnaire in acute low back pain. Manual Therapy, 8(1), 29–36. http://doi.org/10.1054/math.2002.0484 Teichtahl, A. J., Urquhart, D. M., Wang, Y., Wluka, A. E., Wijethilake, P., O'Sullivan, R., & Cicuttini, F. M. (2015). Fat infiltration of paraspinal muscles is associated with low back pain, disability, and structural abnormalities in community-based adults. The Spine Journal, 15(7), 1593–1601. http://doi.org/10.1016/j.spinee.2015.03.039 Teyhen, D. S., Rieger, J. L., Westrick, R. B., Miller, A. C., Molloy, J. M., & Childs, J. D. (2008). Changes in deep abdominal muscle thickness during common trunk- strengthening exercises using ultrasound imaging. Journal of Orthopaedic & Sports Physical Therapy, 38(10), 596–605. http://doi.org/10.2519/jospt.2008.2897

127 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Toyone, T., Takahashi, K., Kitahara, H., Yamagata, M., Murakami, M., & Moriya, H. (1994). Vertebral bone-marrow changes in degenerative lumbar disc disease. An MRI study of 74 patients with low back pain. Journal of Bone & Joint Surgery, British Volume, 76-B(5), 757–764. Tsao, H., Danneels, L., & Hodges, P. W. (2011). Individual fascicles of the paraspinal muscles are activated by discrete cortical networks in humans. Clinical Neurophysiology, 122(8), 1580–1587. http://doi.org/10.1016/j.clinph.2011.01.048 Urquhart, D. M., Barker, Hodges, P. W., Story, I. H., & Briggs, C. A. (2005a). Regional morphology of the transversus abdominis and obliquus internus and externus abdominis muscles. Clinical Biomechanics, 20(3), 233–241. http://doi.org/10.1016/j.clinbiomech.2004.11.007 Urquhart, D. M., Hodges, P. W., & Story, I. H. (2005b). Postural activity of the abdominal muscles varies between regions of these muscles and between body positions. Gait & Posture, 22(4), 295–301. http://doi.org/10.1016/j.gaitpost.2004.09.012 Urquhart, D. M., Hodges, P. W., Allen, T. J., & Story, I. H. (2005c). Abdominal muscle recruitment during a range of voluntary exercises. Manual Therapy, 10(2), 144–153. http://doi.org/10.1016/j.math.2004.08.011 van Dieën, J. H., Cholewicki, J., & Radebold, A. (2003a). Trunk muscle recruitment patterns in patients with low back pain enhance the stability of the lumbar spine. Spine, 28(8), 834–841. van Dieën, J. H., Selen, L. P. J., & Cholewicki, J. (2003b). Trunk muscle activation in low-back pain patients, an analysis of the literature. Journal of Electromyography and Kinesiology, 13(4), 333–351. http://doi.org/10.1016/S1050-6411(03)00041-5 van Tulder, M., Becker, A., Bekkering, T., Breen, A., del Real, M. T. G., Hutchinson, A., et al. (2006, March). Chapter 3. European guidelines for the management of acute nonspecific low back pain in primary care. European Spine Journal. http://doi.org/10.1007/s00586-006-1071-2 Vera-Garcia, F. J., Elvira, J. L. L., Brown, S. H. M., & McGill, S. M. (2007). Effects of abdominal stabilization maneuvers on the control of spine motion and stability against sudden trunk perturbations. Journal of Electromyography and Kinesiology, 17(5), 556–567. http://doi.org/10.1016/j.jelekin.2006.07.004 Vleeming, A., Schuenke, M. D., Danneels, L., & Willard, F. H. (2014). The functional coupling of the deep abdominal and paraspinal muscles: the effects of simulated paraspinal muscle contraction on force transfer to the middle and posterior layer of the thoracolumbar fascia. Journal of Anatomy, 225(4), 447–462. http://doi.org/10.1111/joa.12227 Volpe, della, R., Popa, T., Ginanneschi, F., Spidalieri, R., Mazzocchio, R., & Rossi, A. (2006). Changes in coordination of postural control during dynamic stance in chronic low back pain patients. Gait & Posture, 24(3), 349–355. http://doi.org/10.1016/j.gaitpost.2005.10.009 128 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

Waddell, G. (1987). 1987 Volvo award in clinical sciences. A new clinical model for the treatment of low-back pain. Spine, 12(7), 632–644. Waddell, G. (1992). Biopsychosocial analysis of low back pain. Baillière's Clinical Rheumatology, 6(3), 523–557. Wagner, H., Anders, C., Puta, C., Petrovitch, A., Mörl, F., Schilling, N., et al. (2005). Musculoskeletal support of lumbar spine stability. Pathophysiology, 12(4), 257–265. http://doi.org/10.1016/j.pathophys.2005.09.007 Wallwork, T. L., Stanton, W. R., Freke, M., & Hides, J. A. (2009). The effect of chronic low back pain on size and contraction of the lumbar multifidus muscle. Manual Therapy, 14(5), 496–500. http://doi.org/10.1016/j.math.2008.09.006 Ward, S. R. (2009). Architectural analysis and intraoperative measurements demonstrate the unique design of the multifidus muscle for lumbar spine stability. The Journal of Bone and Joint Surgery (American), 91(1), 176–10. http://doi.org/10.2106/JBJS.G.01311 Ward, S. R., Tomiya, A., Regev, G. J., Thacker, B. E., Benzl, R. C., Kim, C. W., & Lieber, R. L. (2009). Passive mechanical properties of the lumbar multifidus muscle support its role as a stabilizer. Journal of Biomechanics, 42(10), 1384–1389. http://doi.org/10.1016/j.jbiomech.2008.09.042 Wilcox, R. (2016). Introduction to Robust Estimation and Hypothesos Testing (Fourth). Waltham, MA: Academic Press. Wilcox, R. R., & Tian, T. S. (2011). Measuring effect size: a robust heteroscedastic approach for two or more groups. Journal of Applied Statistics, 38(7), 1359–1368. http://doi.org/10.1080/02664763.2010.498507 Wilke, H. J., Wolf, S., Claes, L. E., Arand, M., & Wiesend, A. (1995). Stability increase of the lumbar spine with different muscle groups. A biomechanical in vitro study. Spine, 20(2), 192–198. Woodham, Woodham, A. W., Skeate, J. W., & Freeman, M. D. (2014). Long-term lumbar multifidus muscle atrophy changes documented with magnetic resonance imaging: A case series. Journal of Radiology Case Reports, 8(5), 1–8. http://doi.org/10.3941/jrcr.v8i5.1401 Yang, & Park, D.-J. (2014). Reliability of ultrasound in combination with surface electromyogram for evaluating the activity of abdominal muscles in individuals with and without low back pain. Journal of Exercise Rehabilitation, 10(4), 230–235. http://doi.org/10.12965/jer.140138 Yang, & Winter, D. A. (1983). Electromyography reliability in maximal and submaximal isometric contractions. American Journal of Physical Medicine and Rehabilitation, 64(9), 417–420. Zhao, W. P., Kawaguchi, Y., Matsui, H., Kanamori, M., & Kimura, T. (2000). Histochemistry and morphology of the multifidus muscle in lumbar disc herniation: comparative study between diseased and normal sides. Spine, 25(17), 2191–2199. 129 Texas Tech University Health Sciences Center, Mark P. Wilhelm, May 2019

APPENDIX A

Lumbar Spine Instability Questionnaire

Please identify if the following activities, positions, or descriptions are appropriate in describing your current low back condition. You may check as many of the indicators that you feel are appropriate.

Please mark the YES if the following descriptions are appropriate in describing your current condition and NO if the description does not describe your current condition.

Yes No I feel like my back is going to “give way” or “give out” on me I feel the need to frequently pop my back to reduce the pain I have frequent times when my pain occurs throughout the day I have a past history where my back catches or locks when I twist or bend my spine I have pain when I sit to stand or stand to sit I have a lot of pain when I sit up from lying down if I don’t raise up the right way My pain is sometimes increased with quick, unexpected, or mild movements I have difficulty sitting without a back support like a chair and feel better with a supportive backrest I cannot tolerate prolonged positions when I can’t move It seems like my condition is getting worse over time I have had this problem a long time I sometimes get temporary relief with back brace or corset I have many occasions when I get muscle spasms I sometimes am fearful to move because of my pain I have had a back injury from trauma in the past

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APPENDIX B Oswestry Disability Index

Instructions This questionnaire has been designed to give us information as to how your back or leg pain is affecting your ability to manage in everyday life. Please answer by checking ONE box in each section for the statement which best applies to you. We realize you may consider that two or more statements in any one section apply but please just shade out the spot that indicates the statement which most clearly describes your problem.

Section 1 – Pain Intensity Section 3 - Lifting I have no pain at the moment I can lift heavy weights without extra pain The pain is very mild at the I can lift heavy weights but it gives moment extra pain

The pain is moderate at the moment Pain prevents me from lifting heavy weights off the floor, but I can manage if they are conveniently placed eg. on a table The pain is fairly severe at the Pain prevents me from lifting heavy moment weights, but I can manage light to medium weights if they are conveniently positioned

The pain is very severe at the I can lift very light weights moment

The pain is the worst imaginable at I cannot lift or carry anything at all the moment

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Section 2 – Personal care (washing, Section 4 - Walking dressing etc) I can look after myself normally Pain does not prevent me walking without causing extra pain any distance I can look after myself normally but Pain prevents me from walking more it causes extra pain than 1 mile It is painful to look after myself and Pain prevents me from walking more I am slow and careful than ½ mile I need some help but manage most Pain prevents me from walking more of my personal care than 100 yards I need help every day in most I can only walk using a stick or aspects of self-care crutches

I do not get dressed, I wash with I am in bed most of the time difficulty and stay in bed

Section 5 - Sitting Section 8 – Sex life (if applicable)

I can sit in any chair as long as I like My sex life is normal and causes no extra pain I can only sit in my favorite chair as My sex life is normal but causes some long as I like extra pain Pain prevents me sitting more than My sex life is nearly normal but is very one hour painful Pain prevents me from sitting more My sex life is severely restricted by than 30 minutes pain Pain prevents me from sitting more My sex life is nearly absent because of than 10 minutes pain

Pain prevents me from sitting at all Pain prevents any sex life at all

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Section 6 - Standing Section 9 – Social life I can stand as long as I want without My social life is normal and gives me extra pain no extra pain I can stand as long as I want but it My social life is normal but increases gives me extra pain the degree of pain Pain prevents me from standing for Pain has no significant effect on my more than 1 hour social life apart from limiting my more energetic interests eg, sport Pain prevents me from standing for Pain has restricted my social life and I more than 30 minutes do not go out as often Pain prevents me from standing for Pain has restricted my social life to my more than 10 minutes home

Pain prevents me from standing at all I have no social life because of pain

Section 7 - Sleeping Section 10 - Traveling

My sleep is never disturbed by pain I can travel anywhere without pain My sleep is occasionally disturbed I can travel anywhere but it gives me by pain extra pain Because of pain I have less than 6 Pain is bad but I manage journeys over hours sleep two hours Because of pain I have less than 4 Pain restricts me to journeys of less hours sleep than one hour Because of pain I have less than 2 Pain restricts me to short necessary hours sleep journeys under 30 minutes

Pain prevents me from sleeping at all Pain prevents me from travelling except to receive treatment

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APPENDIX C Tampa Scale for Kinesiophobia

1 = Strongly Disagree, 2 = Disagree, 3 = Agree, 4 = Strongly Agree 1. I’m afraid that I might injure myself if I exercise 1 2 3 4 2. If I were to try to overcome it, my pain would increase 1 2 3 4 3. My body is telling me I have something dangerously 1 2 3 4 wrong 4. My pain would probably be relieved if I were to exercise 1 2 3 4 5. People aren’t taking my medical condition seriously 1 2 3 4 enough 6. My accident has put my body at risk for the rest of my 1 2 3 4 life 7. Pain always means I have injured my body 1 2 3 4 8. Just because something aggravates my pain does not 1 2 3 4 mean it is dangerous 9. I am afraid that I might injure myself accidentally 1 2 3 4 10. Simply being careful that I do not make any unnecessary 1 2 3 4 movements is the safest thing I can do to prevent my pain from worsening 11. I wouldn’t have this much pain if there weren’t 1 2 3 4 something potentially dangerous going on in my body 12. Although my condition is painful, I would be better off if 1 2 3 4 I were physically active 13. Pain lets me know when to stop exercising so that I don’t 1 2 3 4 injure myself 14. It’s really not safe for a person with a condition like mine 1 2 3 4 to be physically active 15. I can’t do all the things normal people do because it’s too 1 2 3 4 easy for me to get injured 16 Even though something is causing me a lot of pain, I 1 2 3 4 don’t think it’s actually dangerous 17. No one should have to exercise when he/she is in pain 1 2 3 4

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