THE EFFECT OF REPETITIVE HEAD IMPACTS IN SENSORY

REWEIGHTING AND HUMAN BALANCE

by

Fernando Vanderlinde dos Santos

A dissertation submitted to the Faculty of the University of Delaware in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biomechanics and Movement Science

Spring 2019

© 2019 Fernando Vanderlinde dos Santos All Rights Reserved

THE EFFECT OF REPETITIVE HEAD IMPACTS IN SENSORY

REWEIGHTING AND HUMAN BALANCE

by

Fernando Vanderlinde dos Santos

Approved: __________________________________________________________ John J. Jeka, Ph.D. Chair of the Department of Kinesiology and Applied Physiology

Approved: __________________________________________________________ Kathleen S. Matt, Ph.D. Dean of the College of Health Sciences

Approved: __________________________________________________________ Douglas J. Doren, Ph.D. Interim Vice Provost for Graduate and Professional Education

I certify that I have read this dissertation and that in my opinion it meets

the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.

Signed: __________________________________________________________ John J. Jeka, Ph.D. Professor in charge of dissertation I certify that I have read this dissertation and that in my opinion it meets

the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.

Signed: __________________________________________________________ Eric R. Anson, Ph.D. Member of dissertation committee I certify that I have read this dissertation and that in my opinion it meets

the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.

Signed: __________________________________________________________ Thomas Buckley, Ph.D. Member of dissertation committee I certify that I have read this dissertation and that in my opinion it meets

the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.

Signed: __________________________________________________________ Matthew Hudson, Ph.D. Member of dissertation committee

iv

First of all, I would like to express my deepest appreciation to my dissertation

committee, Dr. John Jeka, Dr. Eric Anson, Dr. Thomas Buckley and Dr. Matthew

Hudson for being part of this dissertation and my graduate learning experience. A

special thanks to Dr. John Jeka, my advisor and chairman of my committee. This work

would not have been possible without his support and guidance. He played a key role

in my decision on moving from Brazil to the United States and the pursuit of a

Doctoral degree.

I am also grateful to all members of our lab, they were instrumental in helping

me from the most common daily activities to data collections and analysis. I’d also

like to recognize the effort that I received from Jaclyn Caccese Deckert, she extended

a great amount of assistance during the experiments from data collection to data

analysis and her insightful suggestions to my research.

Finally, I would like to thank my family and all the support given by my

mother, Rosa Maria Vanderlinde, and my father, Fernando Argemon dos Santos. They

were always there when I need it. I am thankful for all the effort and teachings shared

by them to make me a better person and persisting on my desire to obtain a higher

education.

ACKNOWLEDGMENTS

v

LIST OF TABLES ...................................................................................................... viii LIST OF FIGURES ....................................................................................................... ix ABSTRACT ................................................................................................................... x Chapter

1 BALANCE AND SENSORY IMPAIRMENT RELATED TO REPETITIVE HEAD IMPACT AND CONCUSSIONS: LITERATURE REVIEW ............................................................................................................. 1

1.1 Abstract ...................................................................................................... 1 1.2 Introduction ............................................................................................... 2 1.3 Methods ..................................................................................................... 3 1.4 Results ....................................................................................................... 4 1.5 Discussion .................................................................................................. 5

1.5.1 Visual System ................................................................................ 5 1.5.2 Somatosensory ............................................................................... 7 1.5.3 Vestibular System .......................................................................... 7 1.5.4 Postural Control ............................................................................. 8 1.5.5 Multisensory ................................................................................ 10

1.6 Limitations ............................................................................................... 10 1.7 Conclusion ............................................................................................... 11

2 VESTIBULAR FUNCTION AND BALANCE DURING WALKING FOLLOWING SOCCER HEADING ............................................................... 12

2.1 Abstract .................................................................................................... 12 2.2 Introduction ............................................................................................. 14 2.3 Methods ................................................................................................... 16

2.3.1 Participants .................................................................................. 16 2.3.2 Experimental Design ................................................................... 16 2.3.3 Soccer Heading Paradigm ........................................................... 17 2.3.4 Clinical Assessment ..................................................................... 17

TABLE OF CONTENTS

vi

2.3.5 Walking Balance Assessment ...................................................... 17 2.3.6 Data Analysis ............................................................................... 19 2.3.7 Statistical Analysis ...................................................................... 20

2.4 Results ..................................................................................................... 21 2.5 Discussion ................................................................................................ 24 2.6 Conclusion ............................................................................................... 28

3 THE EFFECT OF SOCCER HEADING IN SENSORY REWEIGHTING IN STANDING BALANCE ............................................................................. 29

3.1 Abstract .................................................................................................... 29 3.2 Introduction ............................................................................................. 30 3.3 Methods ................................................................................................... 31

3.3.1 Participants .................................................................................. 31 3.3.2 Experimental Design ................................................................... 32 3.3.3 Soccer Heading Paradigm ........................................................... 32 3.3.4 Clinical Assessment ..................................................................... 33 3.3.5 Standing Balance Assessment ..................................................... 33 3.3.6 Data Analysis ............................................................................... 35 3.3.7 Statistical Analysis ...................................................................... 36

3.4 Results ..................................................................................................... 36

3.4.1 Standing Balance Assessment – Leg AP Displacement .............. 36 3.4.2 Standing Balance Assessment – Trunk AP Displacement .......... 37

3.5 Discussion ................................................................................................ 38 3.6 Conclusion ............................................................................................... 41

4 SENSORY REWEIGHTING IN COLLISION SPORTS COLLEGE ATHLETES ...................................................................................................... 42

4.1 Abstract .................................................................................................... 42 4.2 Introduction ............................................................................................. 44 4.3 Methods ................................................................................................... 45

4.3.1 Participants .................................................................................. 45 4.3.2 Experimental Design ................................................................... 46 4.3.3 Standing Balance Assessment ..................................................... 46 4.3.4 Data Analysis ............................................................................... 48 4.3.5 Statistical Analysis ...................................................................... 49

vii

4.4 Results ..................................................................................................... 49

4.4.1 Standing Balance Assessment – Leg AP Displacement .............. 49 4.4.2 Standing Balance Assessment – Trunk AP Displacement .......... 49

4.5 Discussion ................................................................................................ 52 4.6 Conclusion ............................................................................................... 53

5 FINAL CONSIDERATIONS ........................................................................... 54

5.1 Limitations and Future Directions ........................................................... 54 5.2 Conclusion ............................................................................................... 55

REFERENCES ............................................................................................................. 57 Appendix

A IRB APPROVAL – CHAPTER ONE AND TWO .......................................... 68 B IRB APPROVAL – CHAPTER THREE ......................................................... 69

viii

Table 1. Balance mechanisms means and standard deviations .................................... 22

LIST OF TABLES

ix

Figure 1. The subjects walked in a foam surface, blindfolded and the GVS was applied on the second right heel strike as represented above. ................. 19

Figure 2. Example data – One subject data to illustrate the GVS response during one stride. RHS – right heel strike; LTO – left heel strike; LHS – left heel strike; RTO – right heel strike. ........................................................ 20

Figure 3. Foot placement strategy: foot placement, hip abduction and gluteus medius activity across 3 sessions (pre, post 0h and post 24h). ............... 23

Figure 4. Ankle roll strategy: CoM – CoP separation, ankle inversion and peroneus longus activity across 3 sessions (pre, post 0h and post 24h). ................ 23

Figure 5. Push off strategy: step length, ankle plantar flexion and medial gastrocnemius activity across 3 sessions (pre, post 0h and post 24h). .... 24

Figure 6. Standing Assessment representation ............................................................. 35

Figure 7. Gains of the soccer heading and control group for GVS, vibration and vision ....................................................................................................... 38

Figure 8. Standing assessment representation .............................................................. 48

Figure 9. Gain to vision in collision vs no-contact athletes ......................................... 50

Figure 10. Gain to vibration in collision vs no-contact athletes ................................... 51

Figure 11. Gain to GVS in collision vs no-contact athletes. ........................................ 51

LIST OF FIGURES

x

Repetitive subconcussive head impacts are common in contact sports such as

football, ice hockey, and soccer. Subconcussive head impacts are mild head impacts

that do not result in acute clinical signs and symptoms of a concussion but the

exposure to repetitive head impacts (RHI) is suggested to cause significant current and

future detrimental neurological effects. These RHI may be associated with short-term

and long-term white matter microstructural changes and impaired cognitive

performance, as well as later-life behavioral and mood changes. However,

contemporary studies do not explore potential deficits in balance and sensory

reweighting. Sensory reweighting is the process through which the central nervous

system adapts the processing of a particular sensory input due to neurological injury or

when environmental conditions change. For example, when visual cues are diminished

after entering a dark room, the nervous system must increase its emphasis on

somatosensory and vestibular information to maintain upright balance. The fusion of

visual, proprioceptive and vestibular inputs (i.e., multisensory fusion) has been shown

to play a key role in quiet standing balance in humans, and the lack of sensory

reweighting is related to a central processing impairment. Following mild traumatic

brain injury (mTBI), or concussion, there are deficits in sensorimotor function. In

addition, previous research has suggested that even repetitive subconcussive head

impacts may lead to subtle balance disturbances during standing. Specifically, our

research group demonstrated vestibular dysfunction following subconcussive impact

as evidenced by the diminished response to galvanic vestibular stimulation (GVS)

ABSTRACT

xi

while standing with eyes closed on foam and increased medial-lateral trunk

displacement and velocity during treadmill walking after mild head impact. This

disruption in vestibular processing could be an underlying mechanism of balance

problems after head impact. This project investigated the effect of repetitive head

impacts on sensory reweighting in college athletes that participate in contact sports.

Understanding changes in sensory reweighting in this population may help in early

brain damage detection and prevent future injuries through the development of better

training and rehabilitation for those with such deficits.

We studied sensory reweighting through a series of three experiments. The

first and second experiments investigated the effect of soccer headings on balance

control during walking (first experiment) and upright quiet stance (second

experiment). For both experiments, the participants were randomly assigned in two

groups: a soccer heading group and a control group. They were tested in three

sessions: a baseline (Pre), a post soccer heading (post 0h) and 24h (post 24h) post

soccer heading session. To assess whether vestibular processing was affected during

walking following soccer headings, we attempted to isolate this system by having the

subjects walk on a foam surface, blindfolded while perturbing the vestibular system

with galvanic vestibular stimulation (GVS). We then calculated the response to GVS

on balance mechanisms. No differences in GVS response on balance mechanisms post

soccer headings were found. Our results suggest that an acute bout of soccer headings

does not result in a balance deficit during walking. To study the effect of soccer

headings in sensory reweighting in upright stance we implemented a multisensory

fusion paradigm, consisting of simultaneous visual, somatosensory and vestibular

perturbations. The response of the trunk/leg segment movement was calculated

xii

relative to each modality (i.e., gain), pre and post soccer headings. This experiment

showed no alterations in sensory reweighting pre and post soccer heading. To

understand the effect of the continuous practice of collision sports and the effect of

repetitive subconcussive head impacts in collegiate athletes, our third experiment used

the same multisensory paradigm. We compared trunk/leg gains relative to each

sensory modality between collision sports players and no contact players. No

differences were found in sensory reweighting between collision and non-contact

sports athletes. Our result suggests that RHI are not sufficient to change sensory

reweighting and balance in collegiate athletes. We believe that head impact tolerance

might play a role in our results and more studies should be conducted to understand

the effect of repetitive head impact force and frequency on human balance.

1

BALANCE AND SENSORY IMPAIRMENT RELATED TO REPETITIVE HEAD IMPACT AND CONCUSSIONS: LITERATURE REVIEW

1.1 Abstract

Balance is impaired post-concussion, and to understand the underlying

mechanism of this impairment it is necessary to recognize the role of the sensory

systems that aid balance in humans. With that objective, we performed a literature

review of sensory systems impairments related to balance post-concussion and

repetitive head impacts (RHI). We used PubMed as the source for this review and

included articles published by January of 2019. A total of 658 studies were found and

thirty-three reports were identified with data referent to balance related to one or all

sensory systems. The vestibular and visual systems were most prevalent when related

to a single system, but the majority investigated postural control with no focus on a

specific sensory system. It is notable that associated deficits in vestibular processing

were related to dizziness, prolonged recovery, and balance post-concussion, with only

one study suggesting that a vestibular deficit was related to diminishing postural

control immediately post RHI.

Our results suggest that more studies are needed relating specific sensory

systems and sensory reweighing to balance impairment post-concussion, particularly

with regard to repetitive subconcussive head impact.

Chapter 1

2

1.2 Introduction

Concussive, subconcussive, and repetitive head impacts are themes in several

studies related to cognitive deficits, concussion screening, and time to recover, but

only a few investigate upright balance control. Although balance has been shown to be

impaired post-concussion, the underlying mechanisms of such impairment are unclear.

Mechanisms underlying the effects of subconcussive repetitive head impacts on

balance control are also poorly understood.

Subconcussive head impacts are mild head impacts that do not result in acute

clinical signs and symptoms of concussion (Broglio 2012). Previous research suggests

that repetitive subconcussive head impacts (RSHI) can lead to deficits in postural

control in quiet stance (Hwang 2017; Haran 2012) and that the interaction between the

visual, somatosensory and vestibular systems was an important factor for postural

control.

Concussions instigate neurometabolic changes that have been described as a

neurometabolic cascade of events. This series of events include bioenergetic

challenges, cytoskeletal and axonal alterations, impairments in neurotransmission,

vulnerability to delayed cell death and chronic dysfunction that can cause long-term

biological changes and sequelae (Giza 2014). Although the neurometabolic cascade

explains biological changes post-concussion, no specific biomarkers related to deficits

in sensory system processing and balance control have been identified.

To maintain upright balance, humans use three sensory systems:

somatosensory, vision and vestibular. The fusion of these systems provides an

estimate of self-motion which is critical for appropriate neuromuscular control of

balance. A deficit in the process of fusing the sensory systems is attributed to an

impairment in central nervous system processing (Hwang 2014; Peterka 2002; Horak

3

2006). Sensory reweighting is a dynamic process where the central nervous system

changes the relative emphasis of each sensory system contributing to maintaining

balance as a result of environmental changes. An example of sensory reweighting is

when a person walks into a dark room. Accurate visual sensory input is reduced, and

to maintain balance, the nervous system emphasizes somatosensory and vestibular

input and decreases reliance on vision (Hwang 2014).

The relationship between sensory reweighting and balance in concussion and

repetitive subconcussive head impacts is yet to be defined. Such knowledge may aid in

the development of more effective rehabilitation. The current literature review was

undertaken with the aim of determine the current state of knowledge in the field while

identifying current knowledge gaps within the framework of sensory weighting

deficits following repetitive head impacts and concussion.

1.3 Methods

For this systematic review, we searched PubMed for articles published

between 1998 and January 2019. The search was undertaken using the terms:

‘‘concussion’’, ‘‘head injury’’, ‘‘head impact’’, ‘‘mild traumatic brain injury’’ and

‘‘subconcussion’’. These terms were linked using the combinations of: ‘‘vision’’ or

‘‘visual’’, or ‘‘proprioception’’ or ‘‘somatosensory’’, or ‘‘vestibular’’ and ‘‘postural’’,

or ‘‘postural control’’, or ‘‘balance’’, or ‘‘gait’’. The references retrieved were then

filtered by English language, human subjects, and full text. Articles were screened by

the titles and by abstract reading. Studies focused on mild traumatic brain injury and

blast injuries were excluded. Papers chosen for this review were the ones with human

subjects, including clinical trials, and a defined balance task related to at least one of

4

the three sensory systems previously mentioned. The data extracted (when available)

included: balance test performed, population type and other relevant factors.

1.4 Results

We identified 658 studies and thirty-three reports contained data referent to

balance related to one or all sensory systems. No studies were identified investigating

isolated somatosensory system function in relation to balance post-concussion or

repetitive head impact, but rather as a part of multifaceted balance evaluations such as

the Sensory Organizational Test (SOT). The SOT is an instrumented force-plate based

balance test that provides a clinical picture of the relative role of the three main

sensory systems in balance. The SOT scores each sensory system (ie. vestibular,

somatosensory and visual system) and an overall balance composite score is calculated

using the weighted average of all scores (Guskiewicz, 2001, Pletcher, Erin R., et al

2017). The lower the score, the higher the impairment. Although the SOT can be used

to investigate each sensory contribution to balance, most of the studies focus on the

change in concussion symptoms relative to the overall balance composite (Zhou 2015;

Sosnoff 2011; Broglio 2009; Graves 2016; Cripps 2018).

In addition to the instrumented and computerized SOT, other more clinically

based balance tests are commonly used to investigate balance after concussion. One

commonly used balance test is the Balance Error Score System (BESS). The BESS is

a clinical test during which the participant stands in double stance, single stance and

tandem stance for twenty seconds, first on a firm and then on a foam surface, with

eyes open and closed (Bell et al 2011). Although the BESS test includes both eyes

open and closed portions, evaluating balance only based on the presence or absence of

vision cannot quantify how the use of vision for balance is changed post-concussion,

5

but the BESS may provide a gross indication of sensory reweighing capacity. A

significant limitation of the BESS is that it cannot detect subtle balance deficits that

might be present long after a concussion (Murray et al 2014; Bell et al 2011). Other

common balance tests used to investigate postural control after concussion include

Tandem Gait (TG), Center of Pressure (CoP) area, Functional Gait Assessment

(FGA), Dynamic Gait Index (DGI), Timed Up and Go, Five Times Sit to Stand

(FTSTS) and the root mean square (RMS) of the Center of Mass (CoM).

1.5 Discussion

Although a large number of studies discuss balance post-concussion and RHI,

few papers refer to specific sensory systems contributing to balance dysfunction post-

concussion and RHI. When related to a unique system, the majority of the studies are

related to the vestibular system. A possible reason why the vestibular system is the

most studied post-concussion may be because one of the most frequent symptoms

post-concussion is dizziness, which has been shown to be strongly related to the

vestibular system and prolonged recovery (Moore 2016). In this review, we attempted

to separate studies investigating individual sensory modalities when possible and

present the current state of knowledge relating to each sensory system individually to

balance. The studies that did not investigate a single system are allocated to the section

called multisensory postural control.

1.5.1 Visual System

Concussions can impact the visual system in several ways. Higher order visual

processing is impaired early and persists at 12 weeks after mild TBI (Brosseau-

Lachaine O, et al (2008); Padula et al 2017). In addition to higher order visual

6

processing errors concussion also detrimentally impacts oculomotor function resulting

in inaccurate object tracking (Cochrane et al (2019); Hoffer et al ;(2017); Hoffer et al.,

(2015)) and abnormal vergence eye movements (Storey et al (2017)). Master and

colleagues (2015) have shown that 69% of concussed adolescents were diagnosed with

visual impairments such as saccadic dysfunction, convergence insufficiency, and

accommodative disorder. Despite the growing literature demonstrating oculomotor

and visual processing dysfunction, the visual system impact on balance after head

impacts or concussion is less well studied.

In fact, only one study was found using vision as the main focus affecting

balance in a post-concussion population. For this study, the researchers used a

destabilizing field of motion to perturb vision in 8 concussed subjects (mean =

20.95yr) and 12 controls (mean = 20yr). Participants were tested on days 3-10-30

post-concussion. Center of pressure area was larger in the concussed subjects and

persisted through day 30, even though no behavioral and neuropsychological

abnormality was observed on day 30 (Slobounov 2006). This study also found that

visual perturbations provoked mTBI symptoms in the concussed group such as motion

sickness, dizziness, and disorientation.

Despite the lack of studies focusing on vision and balance alone, the vision has

been shown to be an important factor in post-concussion symptoms when combined

with vestibular processing. Although smooth pursuit has been related to prolonged

concussion recovery, vestibular deficits were more strongly linked to poor

performance on the BESS test than visual impairments (Master et al 2018). There is

clearly both a need and opportunity for further investigations to better characterize the

7

specific contributions of vision to postural control after concussion or repeated head

impacts.

1.5.2 Somatosensory

As stated previously, very few papers relate balance problems associated with

concussive or subconcussive head impacts to somatosensory or proprioceptive

deficits. When looking at repetitive subconcussive head impacts, Broglio and

collaborators used a soccer heading model to test subjects and to identify possible

differences in RMS of CoP. Subjects were tested 1-24-48 hours post heading 20

soccer balls at a speed of 88.71km/h (55mph) with the “foam and dome” test

(Shumway-Cook & Horak, 1986). Proprioceptive reliability is reduced in this protocol

by standing on a compliant foam surface. The authors found no significant difference

between the days and tasks post soccer heading. Using a similar protocol, Haran

(2017) found no alterations post soccer headings in the mean center of pressure and

total sway.

1.5.3 Vestibular System

The vestibular system is the main system of focus in several studies relating to

balance control and rehabilitation after concussion. When related to concussion and

vestibular system impairment, 46% of individuals with symptoms such as dizziness

and vertigo presented central vestibular disorder, otolith disorders, benign paroxysmal

positional vertigo (BPPV), labyrinthine concussion, perilymphatic fistula and

endolymphatic hydrops (Ernst, Arne, et al. 2005). The vestibulo-ocular reflex (VOR)

coordinates eye and head movement regulating gaze stabilization. The VOR functions

to keep gaze stable in space during head motion (Grossman et al 1989); a task

8

important for many daily life activities (eg, driving, walking and riding a bus) and

sports participation and was shown to be related to post concussion symptoms such as

dizziness and blurry vision (Wallace 2016). Similar to the other sensory systems, the

VOR has primarily been studied in isolation in previous concussion and repetitive

head impact studies. These studies have not investigated a vestibular specific

modulation on postural control after concussion or repeated head impacts.

Symptoms related to vestibular processing were shown to be related to

prolonged concussion recovery in children. Master (2018) demonstrated that when

post-concussion symptoms were provoked with VOR, smooth pursuits, abnormal

balance and accommodative amplitude (AA) predicted prolonged recovery time. In

addition, although not containing a balance component, a study using the vestibular

ocular motor screen (VOMS) found that 61% of the concussed athletes tested in the

study had concussion symptoms provoked during the VOMS test (Mucha 2014).

For RSHI only one study described specifically the vestibular system. This

study suggested that immediately after ten soccer headings the gain of postural sway

to galvanic vestibular stimulation was diminished suggesting an impairment in

postural control (Hwang 2017).

Overall, the few studies of concussion including vestibular processing are

consistent in pointing to the importance of this system to balance and symptom

recovery. More studies are necessary to understand the effect of RSHI on the

vestibular system.

1.5.4 Postural Control

A number of studies about postural control post-concussion and RSHI make

use of the BESS. The BESS is a reliable clinical test of balance after concussion

9

(Cushman et al 2018). Unfortunately, the BESS is a non-specific test with respect to

segregating sensory systems to identify underlying impairments in postural control

(Horak 2006). Despite this limitation, it is one of the most frequently used balance

assessments in concussed individuals (Yorke 2017; Master 2018; Miyashita 2017;

McDevit 2016; Guskiewicz 2001).

Postural control is affected post-concussion and that is demonstrated by

clinical balance tests as the SOT, Standardized Assessment of Concussion (SAC,

cognitive screening tool), and BESS, although a recent study suggests Tandem Gait to

be more sensitive than BESS (Oldham, et al. 2018). Laboratory tests such as the center

of mass and center of pressure analysis also show postural control impairment such as

increased sway post-concussion (Prangley 2016; Slobounov 2005; Cavanaugh 2005).

Studies of repetitive subconcussive head impacts and postural control suggest a

more complex relationship. Despite nearly all the studies investigating immediate

effects of repetitive head impacts showing no difference in postural control using

clinical or instrumented tests (Broglio 2004, Caccese 2018), a recent study, using the

BESS test, suggest impairment in balance control in collegiate lacrosse players when

compared pre and postseason (Miyashita 2017). Another study with young football

players found no difference pre and postseason also using the BESS test

(Campolettano 2018). The difference in results could be related to the sport, age of

exposure to repetitive subconcussive head impacts and even footwear used during the

test (Azad 2016).

In summary, postural control is well known to be impaired in individuals post-

concussion, but the effect of RSHI in balance is yet to be understood and more studies

should be conducted to elucidate the role of RSHI in postural control.

10

1.5.5 Multisensory

Sensory reweighting plays an important role in human balance (Peterka 2002,

Horak 2006, Hwang 2014) and to understand balance alterations related to concussion

or subconcussive head impacts, it is necessary to understand the effect of head impacts

in sensory reweighting. Concussion history and postural control was studied by

Sosnoff (2011) using the SOT, and although this test has a multisensory approach no

link or mention to sensory reweighting was made. Similar results demonstrating lower

performance on balance composite, visual, and vestibular scores has been reported by

others as well (Moore 2016; Masters 2018; Zhou 2015, Alsalaheen 2010).

RSHI was studied with pre and post soccer heading, also using the SOT

(Mangus, 2004). They found no difference in balance pre- and post-soccer headings.

Although the same study showed a higher score in condition 4 (eyes open, sway-

referenced support surface and fixed surround), which relates to somatosensory

processing in the context of posturally irrelevant visual input, no emphasis was made

in sensory reweighting.

Others studies using SOT focus on the relationship between symptoms and

balance control (Broglio 2009) or postural stability and return to play (Graves 2016).

But even though studies found a deficit in sensory systems post-concussion no studies

emphasized the importance of sensory reweighting relative to balance or the

implications of reweighting deficits after concussion. Future studies should focus on

understanding sensory reweighting impairments.

1.6 Limitations

This systematic review has a number of methodological limitations. First, the

only source used was PubMed, which constrains the number of papers found. Second,

11

there is a potential for language bias because we only included English language

studies. Third, we did not include any animal studies. Fourth, the articles selection was

made by only one individual.

1.7 Conclusion

Although balance is detrimentally impacted post-concussion and a number of

studies have evaluated balance in concussed subjects or in RSHI, few studies specify

or attempt to discuss the relative importance of each of the sensory systems. More

studies are necessary to understand the role of multisensory fusion and sensory

reweighing in this population.

12

VESTIBULAR FUNCTION AND BALANCE DURING WALKING FOLLOWING SOCCER HEADING

2.1 Abstract

Exposure to repetitive head impacts (RHI), specifically in sports such as

football, hockey, and soccer, might be associated with white matter microstructural

changes and cognitive performance. However, the effect of acute RSHI exposure on

vestibular processing and balance control during walking has not yet been studied. A

previous study using a soccer heading paradigm and galvanic vestibular stimulation

(GVS) provides evidence that vestibular function for postural control in quiet stance is

disrupted immediately after repetitive soccer heading. The objective of our study was

to investigate how acute RSHI affects vestibular balance control during walking.

Twenty adult amateur soccer players (10 males and 10 females, 22.3±4.5years,

170.5±9.8cm, 70.0±10.5kg) underwent a clinical assessment (SCAT5) and a walking

balance assessment. Subjects were assigned into two groups, soccer heading (EXP)

and control (CON), and tested across three sessions, baseline (PRE), immediately

following soccer heading (POST-0h), and 24 hours following soccer heading (POST-

24h). For the walking balance assessment, participants walked along a foam walkway

with their eyes closed under two conditions: with Galvanic vestibular stimulation

(GVS) (~40 trials) and without GVS (~40 trials). The response to GVS was calculated

(GVS – mean (without GVS)) for each balance mechanism outcome, that included

Chapter 2

13

mediolateral center-of-mass (CoM)–center-of-pressure (CoP) separation, foot

placement, mediolateral ankle roll, ankle push off, and hip adduction. Repeated

measures ANOVA (RMANOVA) was used to compare mean response variables

between groups (i.e. EXP vs. CON) across different time points (i.e. PRE, POST-0h,

POST-24h). There were no significant group x time interaction effects for any of the

balance mechanisms and muscle activities. There was no significant group x time

interaction to any of the variables collected with SCAT 5. The results of this study

suggest that although there may be a disruption in vestibular processing following

RSHI, this disruption does not lead to measurable changes in balance during walking.

14

2.2 Introduction

Common symptoms of concussion include dizziness and balance dysfunction,

both of which are associated with vestibular impairment (Valovich 2015), and an

initial presentation of vestibular dysfunction is one predictor of a protracted recovery

following a concussion (Lau 2009; Master 2018). Previous research has suggested that

even subconcussive head impacts may lead to subtle balance disturbances during quiet

standing (Hwang 2017). Repetitive subconcussive head impacts have been linked to

alterations in brain structure, although the implications are unclear as those individuals

are often asymptomatic (Mainwaring et al 2018). Subconcussive head impacts are

mild head impacts that do not result in acute clinical signs or symptoms of

neurological dysfunction but might have the ability to cause current and future

detrimental neurological effects when sustained repeatedly (Bailes 2013).

The vestibular system consists of three semicircular canals, which detect

angular acceleration and two otoliths, which detect linear acceleration (Schubert

2008). Galvanic vestibular stimulation (GVS) is used to probe vestibular function and

the balance system by applying a direct current through the skin over the mastoid

processes (Fitzpatrick 2004). GVS excites a wide range of vestibular neurons,

including those related to both the semicircular canals and the otoliths, and causes

head and/or body tilt during standing and an illusory fall during walking (Fitzpatrick

2004; Reimann 2017). One study reported diminished gain to GVS while standing

with eyes closed on foam following a controlled soccer heading paradigm, suggesting

that postural vestibular processing was disrupted following RSHI (Hwang 2017).

However, overall body sway amplitude was unchanged, which may not be surprising

15

considering the vestibular signal-to-noise ratio is quite small during stance, and

proprioception may have been used to compensate for this deficit (Hwang 2017).

Moreover, the “noisy” vestibular signal may not significantly perturb self-motion

estimation and subsequent corrective postural responses due to the low head

accelerations observed during quiet standing (Peterka 1995). Thus, transient disruption

of vestibular processing because of RSHI may have a greater impact during a task like

walking known to have faster head motions (Grossman et al 1989).

To gain an understanding of the potentially detrimental vestibular effects of

RSHI, we employed an experimental paradigm that allows for precise control of RSHI

with a soccer heading paradigm (Haran 2013; Higgins 2009; Dorminy 2015; Caccese

2017; Caccese 2018; Hwang 2017). This soccer heading paradigm has been used

extensively in the literature to understand the biomechanics of RSHI, as well as the

effects of RSHI on standing balance and biomarkers of head injury (Haran 2013;

Higgins 2009; Dorminy 2015; Caccese 2017; Caccese 2018; Hwang 2017).

Therefore, the purpose of this study was to investigate vestibular dysfunction

and balance during walking after RSHI. As humans make use of a number of balance

mechanisms while walking, here we used the foot placement, lateral ankle roll, and

push off mechanisms to characterize the balance response to GVS (Reimann 2017). A

depression on the balance mechanisms response to GVS would represent diminished

postural vestibular processing. In addition, we applied the Sports Concussion

Assessment Tool 5 (SCAT5), a tool used by healthcare professionals to recognize and

manage concussion (Echemendia et al 2017). We hypothesized that individuals would

have depressed vestibular balance mechanism responses to GVS during walking

immediately following the controlled soccer heading paradigm and that these balance

16

responses would recover to baseline levels within 24 hours. In addition, we

hypothesize that SCAT5 will remain unaltered post soccer headings.

2.3 Methods

2.3.1 Participants

Twenty healthy young adult soccer players (10 males, 10 females, 22.3 ± 4.5

years, 70.0 ± 10.5 kg, 170.5 ± 9.8 cm) from the Newark, Delaware region volunteer

for participation. All participants were active soccer players (i.e., collegiate,

intramural, club, professional) with at least 5 years of soccer heading experience and

field players (i.e. not goalkeepers). The exclusionary criteria were: any head, neck,

face, or lower extremity injury in the six months prior to participation; history of

balance problems or vestibular dysfunction; currently taking any medications affecting

balance; any neurological disorders; unstable cardiac or pulmonary disease;

goalkeepers. The University of Delaware institutional review board approved the

study and participants provided written informed consent.

2.3.2 Experimental Design

The experiment used a repeated measures design across three time points (pre-

heading, 0-hours post-heading, 24-hours post-heading) (Hwang 2017). At each time

point, participants completed a clinical assessment (SCAT) then a walking balance

assessment following the protocol described in the Walking Balance Assessment

section. The pre-heading session (PRE) was a baseline measurement. After

approximately 24 hours, participants performed 10 headers following the protocol

described in the Soccer Heading Paradigm section. The same measurements were

performed immediately following the heading (POST-0h) and then approximately 24

17

hours later (POST-24h). Subjects were randomly assigned to one of two groups, a

soccer heading group (EXP) that performed soccer headings on session two and a

control group (CON) that did not perform the soccer headings on any session.

Participants were instructed to not perform soccer headings in between the sessions.

2.3.3 Soccer Heading Paradigm

A controlled soccer heading paradigm was used as an in-vivo model of mild

mechanical head impact (Higgins 2009). Soccer balls (size 5, 450 g, inflated to 8 psi)

were projected using a JUGS soccer machine (JUGS Sports, Tualatin, OR); the initial

velocity was 11.2 m/s (25 mph), the angle of projection was 40 degrees, and the

distance to the participant was approximately 12 m (40 ft) (Higgins 2009; Haran 2013;

Caccese 2017; Caccese 2018). EXP participants performed 10 standing headers in 10

minutes (1 header per minute), while CON participants only performed the walking

assessment.

2.3.4 Clinical Assessment

In each session, subjects administered the Standard Concussion Assessment

Tool 5 (SCAT5), which included the symptom checklist, cognitive screening

(orientation, immediate memory, and concentration), balance examination (BESS) and

delayed recall.

2.3.5 Walking Balance Assessment

To minimize visual and proprioceptive inputs the participants walked

blindfolded along a 2-inch closed-cell foam walkway (Cohen 2008; Mulavara 2009).

Participants initiated gait with their right foot and took approximately six steps until

they were instructed to stop walking. GVS was delivered on the second heel strike of

18

the right foot and continued for 600ms (Figure 1). In the GVS condition, the anode

(LEFT) and cathode (RIGHT) created a perceived fall to the RIGHT. This perceived

fall to the RIGHT creates an actual fall to the LEFT as a result of the actively

generated motor response designed to catch the perceived fall (Heimann 2017). In the

control condition, NO stimulation was delivered. Each of the two conditions was

repeated 40 times, for a total of 80 trials. Conditions were randomized across all trials.

Trials were excluded if the participant did not have a complete right step on the force

plate. The maximum number of excluded trials per subject was 32. Throughout all

trials, participants wore a harness to prevent falling, although no such falling occurred.

Bilateral kinematics were collected at 120 Hz using a twelve-camera optical

motion analysis system (Qualisys, Goteborg, Sweden) and a 6-degree of freedom

(DOF) marker set. Kinetic data for the second right step were collected at 1200Hz

from a force plate (AMTI, Watertown, MA, USA). Binaural, bipolar GVS was

delivered from two round electrodes with 3.2 cm diameter (Axelgaard Manufacturing

Co., Ltd, Fallbrook, CA, USA), placed on the mastoid processes behind the ears. GVS

was triggered during the heel strike of the right foot, when the force measured by force

plate exceeded 10 N. When triggered, a custom-made LabVIEW program (National

Instruments Inc., Austin, TX, USA) generated an analog voltage, which was

transformed into a square wave of 1 mA current using the neuroConn DC-Stimulator

Plus (neuroCare Group, Munchen, Germany). For muscle activity we used a surface

EMG System (Trigno System, Delsys Inc., Natick, Massachusetts, USA) bilaterally in

three muscles; medial gastrocnemius, peroneus longus, and gluteus medius.

19

Figure 1. The subjects walked in a foam surface, blindfolded and the GVS was applied on the second right heel strike as represented above.

2.3.6 Data Analysis

All data were analyzed in Visual 3D (C-Motion, Inc., Germantown, MD).

Kinematic and kinetic data were filtered at 6 and 25Hz, respectively, using a zero-lag,

low-pass Butterworth filter. Kinematic and kinetic data were analyzed from right heel

strike (RON) to right toe off (ROFF). We computed balance variables, including

center-of-mass to center-of-pressure displacement (CoM-CoP Separation) during right

stance foot, mediolateral left heel position relative to CoM (Foot Placement), right

ankle inversion angle (Mediolateral Ankle Roll) on single stance, step length, right

ankle plantarflexion angle (Push Off), and right hip adduction angle (Hip Adduction).

For each mechanism, the response to GVS was calculated by subtracting the signal

mean across all none trials from the signal from each GVS trial (Figure 2). For each

subject and EMG channel, we calculated the average maximum activation across all

control strides for each surface condition and used this value to normalize EMG before

averaging across subjects.

20

Figure 2. Example data – One subject data to illustrate the GVS response during one stride. RHS – right heel strike; LTO – left heel strike; LHS – left heel strike; RTO – right heel strike.

2.3.7 Statistical Analysis

Repeated measures ANOVA (RMANOVA) was used to compare mean

response variables between groups (i.e. EXP vs. CON) across different time points

(i.e. PRE, POST-0h, POST-24h). Multivariate Wald test was computed and compared

to the reference chi-squared distribution to test for the interactions between group and

time. An unstructured covariance matrix was specified for underlying correlated

measures across time points.

Statistical analyses were carried out in SAS (SAS Institute Inc., Cary, NC). For

all tests, we used α = 0.05 as a threshold for statistical significance.

The outcome measures included the mean peak response to GVS for each

participant for each balance variable computed (CoM-CoP Separation, Foot

Placement, Mediolateral Ankle Roll, Push Off, and Hip Adduction). For the SCAT5

21

we calculated the mean score of symptoms, symptoms severity, orientation, immediate

memory, concentration, balance errors and delayed recall.

Statistical analyses were carried out in SPSS. For all tests, we used α = 0.05 as

a threshold for statistical significance.

2.4 Results

Figures 3 to 11 show the balance responses to GVS in both groups across three

time points. There were no significant group x time interaction effects for any of the

balance mechanism response variables in the studied balance mechanisms.

The high variability observed in the balance mechanisms (table 1) was

expected as observed with step width and step length in previous study (McLellan

2006).

22

Table 1. Balance mechanisms means and standard deviations

Measurement Pre mean ±SD Post 0H mean ±SD Post 24h mean ±SD

Control Heading Control Heading Control Heading

Ankle eversion (degrees)

5.61 ±2.8

8.2 ±2.6

5.47 ±3.18

6.34 ±1.71

4.22 ±2.6

5.51 ±3.03

Foot Placement (meters)

0.029 ±0.017

0.034 ±0.023

0.029 ±0.013

0.033 ±0.018

0.024 ±0.016

0.022 ±0.009

CoM – CoP (meters)

0.0015 ±0.0023

0.0032 ±0.0025

0.0011 ±0.0019

0.0018 ±0.0024

0.0017 ±0.0014

0.0027 ±0.0016

Gluteus Medius (μV)

0.0022 ±0.0069

0.0021 ±0.0089

0.0048 ±0.0034

0.0007 ±0.006

0.0046 ±0.0095

0.0040 ±0.0054

Medial Grastrocnemius (μV)

0.001 ±0.0089

0.0024 ±0.0133

0.0006 ±0.0054

0.0048 ±0.0094

0.0005 ±0.0070

0.0015 ±0.0080

Peroneus longus (μV)

0.0566 ±0.0434

0.0894 ±0.0518

0.0583 ±0.0489

0.0798 ±0.0465

0.0624 ±0.0488

0.0764 ±0.0464

Plantar flexion (degrees)

0.21 ±3.07

1.35 ±2.95

0.28 ±2.45

1.65 ±2.45

0.24 ±1.84

0.53 ±3.67

Step length (meters)

0.0066 ±0.0124

0.0111 ±0.0065

0.0065 ±0.0139

0.0106 ±0.0119

0.0079 ±0.0071

0.0057 ±0.0084

Hip abduction (degrees)

1.14 ±0.67

0.75 ±0.81

1.2 ±0.81

0.86 ±1.12

0.93 ±0.71

0.50 ±0.80

Foot placement strategy: foot placement change, F=0.563, p=0.574, η2=0.030;

hip abduction change, F=0.038, p=0.963, η2=0.002; integrated gluteus medius EMG

change, F= 0.537, p=0.589, η2=0.029.

23

Figure 3. Foot placement strategy: foot placement, hip abduction and gluteus medius activity across 3 sessions (pre, post 0h and post 24h).

Ankle roll: integrated relative CoP change, F=0.311, p=0.734, η2=0.017; ankle

inversion change, F=1.094, p=0.346, η2=0.057; integrated peroneus longus EMG

change, F=0.305, p=0.739, η2=0.017.

Figure 4. Ankle roll strategy: CoM – CoP separation, ankle inversion and peroneus longus activity across 3 sessions (pre, post 0h and post 24h).

24

Push off: step length change, F=0.909, p=0.412, η2=0.048; ankle plantar

flexion change, F=0.610, p=0.549, η2=0.033; integrated medial gastrocnemius EMG

change, F=0.547, p=0.583, η2=0.029.

Figure 5. Push off strategy: step length, ankle plantar flexion and medial gastrocnemius activity across 3 sessions (pre, post 0h and post 24h).

There was no significant difference group x time interaction (F 2, 36 =1.022,

p=0.370) to any of the variables collected with SCAT 5. The post priori power

analysis resulted in a power of 0.830 and above for the main variables of interest

demonstrating a sufficient sample size for all hypothesis testing.

2.5 Discussion

While the acute effects of concussion have been well characterized in the

literature, the effects of RSHI on neurological function is poorly understood with some

studies reporting functional impairments following RHI and others observing no

deficits (Gysland 2012, Breedlove 2012; Lipton 2013; Talavage 2014; Montenigro

2017; Stewart 2018; Sollmann 2018, Caccese 2019). We aimed to quantify changes in

25

neurological function through the assessment of vestibular processing and balance

during walking following a controlled soccer heading paradigm. We hypothesized that

individuals would have diminished balance responses to GVS during walking

immediately following the controlled soccer heading paradigm and that these balance

responses would recover within 24 hours. However, our findings do not support our

hypothesis and we did not observe any evidence of changes in balance mechanism

response variables as a result of the RSHI paradigm. We observed substantial

variability in how individuals use these balance mechanisms when walking on a foam

surface which was expected and previously described by MacLellan (2006). Although

the observed balance mechanisms allow for dynamic control in response to balance

perturbations, the variability within and across individuals makes it difficult to identify

systematic changes during walking attributable to the RSHI.

Previous work identified diminished gain to GVS while standing with eyes

closed on foam, suggesting that postural vestibular processing was disrupted following

RSHI (Hwang 2017). However gains to GVS during standing are small, which makes

changes in gains more difficult to identify and interpret. In healthy adults, vestibular

information plays a greater role in tasks in which the relationship between the CoM

and base of support is dynamic, such as during locomotor tasks (Bent 2005). For

example, in response to GVS, healthy adults modulate their CoM-CoP separation

about 2.5mm and their foot placement about 15mm in the direction of the perceived

fall while walking along a firm walkway (Reimann 2017). There are three primary

walking balance mechanisms investigated in our study which collectively are

described as a stepping strategy to control subsequent foot placement. The foot

placement is created by the variables foot placement, hip abduction and gluteus

26

medius. The second one is the lateral ankle roll, which is the mechanism responsible

for controlling the center of pressure under the stance foot. Lateral ankle roll strategy

is the combination of the center of mass and center of pressure separation, the ankle

eversion angle and peroneus longus activity. The last strategy is the push-off

mechanism that encompasses step length, ankle plantar/dorsiflexion and medial

gastrocnemius activity (Reimann 2017). When comparing to Reimann (2017) our

participants had a similar CoM-CoP separation response, but a much greater foot

placement response, which may be a result of walking along a foam walkway instead

of a firm walkway (MacLellan 2006). Although the vestibular contributions to

maintaining balance during walking are larger than during standing, humans have

several mechanisms available to maintain balance during walking (e.g. foot placement,

mediolateral ankle roll, push off). These complementary mechanisms allow for

dynamic control in response to balance perturbations, yet make it difficult to identify

changes in vestibular processing and balance during walking because of high

variability both within participants across trials and across participants. Therefore,

balance responses to GVS are not sensitive enough to identify the subtle, transient

changes in vestibular processing following RSHI.

The SCAT5 is broadly and successfully used for concussion assessment

(Echemendia et al. 2017). Our studied population was not acutely concussed

(exclusion criteria was any concussion in the past 6 months) and it was expected that

we wouldn’t find a difference between the three sessions. In addition, the participants

were soccer practitioners used to perform soccer headings. Therefore it was not

surprising that this cohort did not demonstrate any behavioral balance signs of

impairment after the RSHI protocol that mirrors their sport participation.

27

Limitations of this study included analyzing only the balance response to GVS.

Typical responses to GVS during walking are a combination of balance responses and

deviation of the walking path, and previous work in healthy adults has suggested that

the navigation response is at least partially decoupled from the balance response (Bent

2000; Bent 2005). The length of the foam walkway and the position of the force plates

within the lab limited the space available for assessing the deviation of the walking

path; however, incorporating measures of both balance response to GVS and deviation

of the walking path should be considered in future research. This study was the first to

use GVS to probe vestibular function during walking following head impact.

Therefore, we do not know how these balance mechanisms would change with greater

exposure to RSHI [in this study participants only completed 10 controlled soccer

headers], or with a more severe head impact, such as after a diagnosed concussion. In

addition, we speculated that because all the participants were soccer athletes that are

used to routinely performing soccer headings and at baseline may be different from

non-soccer players. Significant functional deficits associated with RSHI should be

placed in the context of frequency and magnitude of head impact and with respect to

other clinical measures or biomarkers of head injury. Finally, human walking balance

is a complex behavior and the fundamental properties of these balance mechanisms

are still being investigated. Future research may determine the interdependence of

balance mechanisms, which may provide additional insight in quantifying deficits in

populations with diminished balance control, in light of the large variability within and

across participants.

28

2.6 Conclusion

Although previous work demonstrated an effect to soccer headings in quiet

stance, our results suggest that an acute bout of soccer headings does not indicate a

balance deficit during walking. More research is necessary considering subconcussive

head impact frequencies and different sports population.

29

THE EFFECT OF SOCCER HEADING IN SENSORY REWEIGHTING IN STANDING BALANCE

3.1 Abstract

An important component of postural control is a complex, dynamic interaction

of multiple sensory systems which allow humans to maintain balance despite changes

in the environment or neurological state. Sensory reweighting is the process of

dynamic sensory regulation of balance control. The aim of this study is to investigate

the effects of purposeful soccer heading on sensory reweighting during quiet stance in

collegiate athletes. Thirty amateur adult soccer players were randomly assigned into

two groups, soccer heading (EXP) and control (CON). Both groups underwent a

clinical assessment (SCAT5) and a standing balance assessment. Subjects were tested

across three sessions: baseline (PRE), immediately following soccer heading (POST-

0h), and 24 hours following soccer heading (POST-24h). A standing balance

assessment, designed to simultaneously test all three sensory modalities -

somatosensory, vision, and the vestibular system was administered in all sessions.

Gains for leg and trunk angles relative to each modality were calculated and a

RMANOVA was used to compare means between groups across the three time points.

There were no changes in gain to vision, vibration, and GVS due to exposure to mild

head impact. The results of this study suggest that although there may be a disruption

in vestibular processing following RSHI, this disruption does not lead to measurable

changes in quiet standing balance and sensory reweighting remains unaltered.

Chapter 3

30

3.2 Introduction

In soccer, purposeful heading is integral and frequent in both practice and in

competition. Soccer headers can be characterized as repetitive head impacts (RHI) that

do not result in acute clinical signs and symptoms of concussion (Bailes 2013).

Current thinking views sub-concussion as an under-recognized phenomenon that has

the ability to cause significant current and future detrimental neurological effects,

although studies reporting these effects are inconclusive (Tarnutzer et al 2016).

Previous research suggests that alterations in vestibular function may impair postural

control during standing following an acute bout of soccer heading (Hwang et al.,

2017). Deficits in postural control may lead to an increased risk of lower extremity

injury following return to play (Howell 2015). Postural control impairments from sub-

concussive head impacts may have similar consequences.

Postural control is achieved due to a complex dynamic interaction of multiple

sensory systems (Horak 1996, 2006). This interaction between the somatosensory,

visual, and vestibular systems allows humans to maintain balance despite changes in

the environment. Dynamic sensory regulation is called sensory reweighting (Hwang

2014, Peterka 2002) and allows humans to balance in the presence of changing

environmental or neurological conditions. Sensory reweighting can also be

manipulated in a laboratory setting and a persistent adaptation process to sensory

stimuli can be noticed after appropriate training (Hwang 2014; Allison 2006).

There are deficits in sensorimotor function following mild traumatic brain

injury (mTBI) or concussion (Galea et al. 2018). Previous research has suggested that

even repetitive subconcussive head impacts may lead to subtle balance disturbances

during standing (Hwang 2017). Although previous studies have found no acute effect

31

in postural balance post soccer headings with eyes open or closed and in a foam

surface (Mangus 2004, Broglio 2004) other research demonstrated vestibular

dysfunction following subconcussive impact. Hwang et al (2014) found diminished

sway response to galvanic vestibular stimulation (GVS) while standing with eyes

closed on foam after mild head impact. This disruption in postural vestibular

processing could be an underlying mechanism of balance problems after head impact.

To investigate how purposeful soccer heading disrupts sensory feedback and

effects balance control in quiet stance, we used a soccer-heading model that controls

head impact number, magnitude, and direction. The model consists of controlled

soccer heading while assessing head impact kinematics and uses a sophisticated

approach to characterize balance mechanisms disrupted post-heading. Ball speed and

direction are controlled, and experienced soccer players simply stand and perform

headers to control head impact location and direction (Hwang 2017, Caccese 2018).

The purpose of this study was to investigate the effects of purposeful soccer

heading on sensory reweighting during quiet stance. We hypothesized that individuals

would have diminished gains to GVS immediately following the controlled soccer

heading paradigm that would be restored approximately twenty-four hours post

heading. In addition, visual and proprioceptive processing would remain unaltered

throughout the sessions.

3.3 Methods

3.3.1 Participants

Thirty amateur adult soccer players (15 males, 15 females, 21.8 ± 2.8 years,

69.9 ± 11.5 kg, 171.4 ± 8.2 cm) were randomly assigned into two groups, soccer

32

heading (EXP) and control (CON) from the Newark, Delaware region volunteered for

participation. All participants were active soccer players (i.e., collegiate, intramural,

club) who were field players (i.e. not goalkeepers) and had at least 5 years of soccer

heading experience. The exclusionary criteria were: any head, neck, face, or lower

extremity injury in the six months prior to participation; pregnancy; history of balance

problems or vestibular dysfunction; currently taking any medications affecting

balance; any neurological disorders; unstable cardiac or pulmonary disease;

goalkeepers. The University of Delaware institutional review board approved the

study and participants provided written informed consent. Participants were instructed

to abstain from performing soccer headings in between the sessions.

3.3.2 Experimental Design

The experiment used a repeated measures design across three time points (pre-

heading, 0-hours post-heading, 24-hours post-heading) (Hwang et al., 2017). At each

time point, participants completed a clinical assessment (SCAT) and a standing

balance assessment, following the protocol described in the Standing Balance

Assessment section. The pre-heading session (PRE) was a baseline measurement.

After approximately 24 hours, participants performed 10 headers following the

protocol described in the Soccer Heading Paradigm section below. The same

measurements were performed immediately following the heading (POST-0h) and

then approximately 24 hours later (POST-24h).

3.3.3 Soccer Heading Paradigm

A controlled soccer heading paradigm was used as an in-vivo model of mild

mechanical head impact (Higgins et al 2009). Soccer balls (size 5, 450 g, inflated to 8

33

psi) were projected using a JUGS soccer machine (JUGS Sports, Tualatin, OR); the

initial velocity was 11.2 m/s (25 mph), the angle of projection was 40 degrees, and the

distance to the participant was approximately 12 m (40 ft) (Higgins 2009, Haran 2013,

Caccese 2017, Caccese 2017, Caccese 2018). EXP participants performed 10 standing

headers in 10 minutes (1 header per minute), while CON participants did not perform

any soccer heading.

3.3.4 Clinical Assessment

In each session, subjects were administered the Standard Concussion

Assessment Tool 5 (SCAT5), a standardized tool to aid evaluation of sign and

symptoms of concussion, which included the symptom checklist, cognitive screening

(orientation, immediate memory, and concentration), balance examination (BESS),

and delayed recall.

3.3.5 Standing Balance Assessment

Participants were instructed to stand upright looking straight ahead while their

visual, somatosensory, and vestibular systems were perturbed as shown in Figure 6.

The visual feedback perturbation consisted of an oscillatory translation at 0.2 Hz of

500 3D pyramids randomly distributed projected on the surface of a dome that

surrounded the participant for 180 degrees of visual angle. Each pyramid had 30 cm of

height and was projected about 10 meters from the subject base of support. The visual

translation had two conditions: a low amplitude vision condition where the objects

translated 20 centimeters and a high amplitude vision condition where the objects

translated 80 centimeters. A pair of 20mm vibrators where strapped on each Achilles

tendon, vibrating at an amplitude of 1 mm and frequency of 80 Hz based on a square

34

wave with equal on and off durations corresponding to a frequency of 0.28 Hz. To

perturb the vestibular system, Galvanic Vestibular Stimulation (GVS) was

administered to evoke anterior-posterior sway. Binaural, bipolar GVS was delivered

from two round electrodes with 3.2 cm diameter (Axelgaard Manufacturing Co.,

Fallbrook, CA, USA). A custom LabVIEW program (National Instruments Inc.,

Austin, TX, USA) generated an analog voltage, which was transformed into a square

wave of 1 mA current using the neuroConn DC-Stimulator Plus (neuroCare Group,

Munchen, Germany). Electrodes were placed bilaterally on both the mastoid processes

and each scapula region approximately at the same height as the T2 spinous process.

The GVS stimulation was the same for both sides and consisted of ±1 mA as a

sinusoidal wave at 0.36 Hz. (Hwang et al 2014, 2017).

The trials were randomized in four conditions of different combinations of

sensory input. Condition one was a low vision, vibration, and GVS (LVG); condition

two was a low vision and GVS (LG); condition three was a high vision, vibration, and

GVS (HVG); and condition 4 was a high vision and GVS (HG). A total of twenty

trials of 135 seconds were collected, five trials per condition. Throughout all trials,

participants wore a harness to prevent falling, although no subjects lost balance during

the experiment. Gain and phase of leg and trunk segments displacement related to

each condition were calculated (refer to the data analysis section).

Twelve reflective markers were placed bilaterally on the temple (head),

acromion (shoulder), great trochanter (hip), lateral femoral epicondyle (knee), lateral

malleolus (ankle), and first metatarsal (foot). Kinematics were collected at 120 Hz

using a thirteen-camera optical motion analysis system (Qualisys, Goteborg, Sweden).

35

Figure 6. Standing Assessment representation

3.3.6 Data Analysis

All the data collected was processed and analyzed in Matlab (MathWorks

Inc.). The gain between each sensory input for leg and trunk segment displacements

were calculated between groups and across days. The leg segment was defined by

anteroposterior movement of the hip and ankle markers, and the trunk segment was

defined by the anteroposterior movement of the shoulder and hip markers. Gain is the

amplitude of the output (postural sway) divided by the amplitude of the input (sensory

perturbation) at each driving frequency. To calculate gain we applied the frequency

response function (FRF) analysis that is defined by the cross-spectral density divided

by the power spectral density of the input. For example, if the gain to the GVS input

36

equals one, it means that the amplitude of the segment displacement (output) and the

GVS perturbation (input) at the driving frequency are the same. Phase is a measure of

the temporal relationship between the input and output; the output may lead the input

(positive values) or lag behind it (negative values) (Hwang et al 2014).

3.3.7 Statistical Analysis

Repeated measures MANOVA (RMANOVA) was used to compare mean

response variables between groups (i.e. EXP vs. CON) across different time points

(i.e. PRE, POST-0h, POST-24h). Multivariate Wald test was computed and compared

to the reference chi-squared distribution to test for the interactions between group and

time. An unstructured covariance matrix was specified for underlying correlated

measures across time points. Statistical analyses were carried out in SAS (SAS

Institute Inc., Cary, NC). For all tests, we used α = 0.05 as a threshold for statistical

significance.

3.4 Results

The clinical assessment (SCAT5) presented no significant differences in group

x time (F2, 36=1.022, p=0.370) interactions.

3.4.1 Standing Balance Assessment – Leg AP Displacement

There were no changes in AP leg segment gain to vision (i.e. session X group

effect; F=0.798, p=0.455, η2=0.028), AP leg segment gain to GVS (F=0.246, p=0.782,

η2=0.009), or AP leg segment gain to vibration (F=0.662, p=0.520, η2=0.023) (Figure

1). In addition, there were no changes in sensory reweighting across any modality (i.e.

session X condition X group effect; vision, F=0.430, p=0.858, η2=0.015; GVS,

F=0.763, p=0.600, η2=0.027; vibration, F=0.430, p=0.653, η2=0.015) (Figure 7).

37

3.4.2 Standing Balance Assessment – Trunk AP Displacement

There were no changes in AP trunk segment gain to vision (i.e. session X

group effect; F=0.490, p=0.615, η2=0.017), AP trunk segment gain to GVS (F=0.205,

p=0.815, η2=0.007), or AP trunk segment gain to vibration (F=0.624, p=0.539,

η2=0.022). In addition, there were no changes in sensory reweighting across any

modality (i.e. session X condition X group effect; vision, F=0.395, p=0.881,

η2=0.014; GVS, F=0.906, p=0.492, η2=0.031; vibration, F=0.761, p=0.472,

η2=0.026) (Figure 7).

Soccer Heading Control

38

Figure 7. Gains of the soccer heading and control group for GVS, vibration and vision

3.5 Discussion

We examined the effects of purposeful soccer heading on sensory reweighting

during quiet stance in collegiate athletes before soccer heading (baseline), immediately

Soccer Heading Control

39

post heading, and twenty-four hours post heading. Although a previous study using a

similar soccer heading protocol had shown a diminished gain to GVS immediately

after soccer heading, our study results found no statistical difference in postural gain

to any sensory modality (GVS, vibration, and visual input).

As expected, we did not observe any significant changes in the SCAT5. The

SCAT5 has been shown to be sensitive to detect acute concussion (Echemendia et al.

2017); however, the RSHI experienced in this protocol was likely too small to alter

balance or cognition in these conditioned soccer athletes. Although the participants

were mostly recreational players, they all had at least five years of soccer experience

and were currently active and routinely performing soccer headings during training

and games. Our SCAT5 results show that repetitive soccer headings were not

sufficient to provoke concussion symptoms in our cohort.

Our hypothesis that the gain to GVS would be diminished immediately after

the controlled soccer headings was not confirmed. This result contrasts with a previous

study that used the same soccer heading paradigm (Hwang 2017). Methodological

differences may explain the differences in vestibular processing post soccer headings.

Our measurements and protocol were specifically multisensory oriented and Hwang

2017 had participants with eyes closed standing on a foam surface. In that scenario,

visual input was not available and proprioception was constantly less reliable, making

vestibular system the only reliable system (Cohen 1993; Anson 2018). Thus any

vestibular system modulation would likely be magnified since eyes closed represents

an extreme in visual sensory weighting. Our results corroborate other studies using

similar soccer heading paradigms that also found no difference immediately post

soccer headings (Mangus 2004, Scmitt 2003, Broglio 2004) when using the Balance

40

Error Score System (BESS), foam or no foam surface, and the Sensory Organizational

Test (SOT).

The effects of RHI on neurological function in balance is poorly understood

with only one study showing functional impairments following RHI (Miyashita 2017)

and several others observing no deficits (Gysland 2012, Breedlove 2012; Lipton 2013;

Talavage 2014; Montenigro 2017; Stewart 2018; Sollmann 2018). Miyashita (2017)

studied collegiate lacrosse players, although lacking in a control group, found a

difference in balance control measurements pre and post season when using BESS, but

a different study with football players, also administering BESS pre and post season,

found no difference in postural balance between both timelines (Campolettano 2018),

suggesting that the effects of repetitive head impact may be sport-dependent.

Tolerance for RHI is another factor that may contribute to the mixed results

noted in previous studies. It has been suggested that the tolerance to repeated head

impacts might be specific to the individual and may depend on variation in bone and

soft tissue morphology (Rowson, Steven, et al. 2018). We speculate that if an athlete is

exposed to repetitive mild repetitive head impacts with a certain acceleration, the

impact threshold which results in a concussion for that athlete will have to be a higher

acceleration than their prior exposure. Thus, the soccer athletes in our cohort may have

developed tolerance to soccer headings via previous training exposure. Increased

tolerance for RHI could explain why this cohort was not susceptible to changes in

balance and sensory reweighting following soccer heading. Tolerance to mild

repetitive head impacts leading to a possible neuroprotective mechanism to maintain

balance following head impacts remains theoretical at this point but is a possible

reason why no significant alterations in sensory reweighting occurred in our subjects.

41

Subjects that experience a number of mild repetitive head impacts (ie. soccer athletes)

may have a different threshold for sensory perturbations, facilitating balance control in

different environmental situations in function of their sport.

Overall a lack of difference in sensory reweighing and/or postural control pre

and post-acute soccer heading suggests that RHI are not, in the short term, detrimental

to balance in these athletes. A limitation to the controlled soccer heading protocol used

in this study was that the control group also consisted of soccer athletes and these

participants may already have an impairment or shifted baseline sensory weighting

compared to a population that does not experience voluntary repeated head impacts as

a sports practice. Further studies are necessary to understand if the practice of collision

sports are detrimental to balance control and sensory reweighing when compared to

non-contact sports.

3.6 Conclusion

Our result suggests that sensory reweighing remains intact following RSHI in a

collegiate soccer athlete population and no balance impairment was observed. In

addition, no symptoms of concussion were present following repeated soccer

headings. More studies are necessary to understand whether the type of sport directly

impacts sensory reweighing capacity for balance control.

42

SENSORY REWEIGHTING IN COLLISION SPORTS COLLEGE ATHLETES

4.1 Abstract

Increasing the understanding of sensory reweighting in college-aged collision

sports athletes may aid in the development of improved training and rehabilitation

methods focusing on a specific sensory system. Previous studies using a soccer

heading protocol have shown that sensory reweighing is unaltered immediately after

soccer headings, but it remains unknown whether athletes that are exposed to

repetitive head impacts (RHI) as part of their sport experience altered sensory

reweighting compared to athletes that don’t experience RHI.

We compared sensory reweighting in two groups of collegiate athletes:

collision sports (rugby, American football, and ice hockey) and non-contact sports

(swimmers, triathletes and cross country/track). A standing balance assessment and

the SCAT5 were used to examine clinically relevant information about the

participants. The balance assessment consisted of a multisensory paradigm where

vision, the vestibular system, and proprioception were manipulated and sensory

reweighing was quantified. Visual input was manipulated by translating a virtual 3D

projection in an anterior and posterior direction, proprioception was perturbed by

vibrators located bilaterally on the Achilles tendon, and galvanic vestibular stimulation

(GVS) was used to influence the vestibular system. The gain of body segment

amplitude relative to GVS, vibration, and the visual stimulus amplitude were not

significantly different between the two cohorts. Our results suggest that sensory

Chapter 4

43

reweighting is not disrupted in collegiate collision sports athletes and there are no

differences compared to non-contact athletes.

44

4.2 Introduction

Collision sports such as football, ice hockey, and rugby are the sports with the

most concussions in male collegiate athletes during gameplay (Prien, et al. 2018).

Although concussions can cause symptoms (like headaches and dizziness) and

prolonged neurological impairments (Moser 2005), repetitive head impacts not

resulting in concussion may lead to detrimental neurological effects (Tarnutzer et al

2016, Bailes et al., 2013). It has been postulated that repetitive subconcussive head

impacts are associated with short-term and long-term white matter microstructural

changes and impaired cognitive performance, as well as later-life behavioral and mood

changes (Stamm et al., 2015; Baugh et al., 2012, Lipton et al., 2013).

Sensory reweighting is the process through which the central nervous system

dynamically shifts the processing of a particular sensory input in response to

neurological injury or sudden changes in environmental conditions. For example,

when visual cues are diminished after entering a dark room, the nervous system must

increase the relative weighting of somatosensory and vestibular information to

maintain upright balance because of the sudden reduction in posturally relevant visual

input. The fusion of visual, proprioceptive, and vestibular inputs (i.e., multisensory

fusion) has been shown to play a key role in quiet standing balance in humans and

lack of sensory reweighting to be related to a central processing impairment (Peterka

2002; Hwang 2017).

Following mild traumatic brain injury (mTBI) or concussion, there are frequent

deficits in sensorimotor function (Moore et al 2014). In addition, previous research has

suggested that repetitive subconcussive head impacts may lead to subtle balance

45

disturbances during standing (Hwang et al 2017). Specifically, our research group has

demonstrated vestibular dysfunction following subconcussive impact as evidenced by

the diminished response to galvanic vestibular stimulation (GVS) while standing with

eyes closed on foam and increased medial-lateral trunk displacement and velocity

during treadmill walking after mild head impact (Hwang et al 2017). This disruption

in vestibular processing and in the processing of other sensory modalities could be an

underlying mechanism of balance deficits after repeated or severe head impact.

To investigate the effect of repetitive head impacts on sensory reweighting in

collision sports college athletes we propose to apply a controlled multisensory

paradigm and compare responses from collision sport athletes to non-contact athletes.

We hypothesized that responses to GVS in collision athletes will be diminished when

compared to the non-contact athletes. Understanding changes in sensory reweighting

in this population may help in early brain damage detection and injury prevention

through the development of better training and rehabilitation for those with sensory

reweighting deficits.

4.3 Methods

4.3.1 Participants

Thirty current male collegiate student-athletes from the University of Delaware

participated in this study. Participants were grouped by sport type, including collision-

(rugby (N=4), football (N=2) and ice hockey (N=9), N=15, 21.2±2 years, 85.9 ± 13.8

kg, 179.7± 8.2 cm) and non-contact- (swimmers (N=3), triathletes (N = 2) and cross

country/track (N = 10), N=15, 20.8±2.1 years, 72.9 ± 4.8 kg, 178.3 ± 4.3 cm). The

exclusionary criteria were: any head, neck, face, or lower extremity injury in the six

46

months prior to participation; history of balance problems or vestibular dysfunction;

currently taking any medications affecting balance; any neurological disorders;

unstable cardiac or pulmonary disease. The University of Delaware institutional

review board approved the study and participants provided written informed consent.

4.3.2 Experimental Design

The experiment involved a single session where participants completed a

clinical assessment (SCAT5) and a standing balance assessment. As described in the

standing balance section.

4.3.3 Standing Balance Assessment

The participants stood in a virtual reality cave (Bertec Corporation, Columbus,

OH) while we perturbed their visual, somatosensory and vestibular systems as seen in

figure 8. To perturb the vestibular system and stimulate anterior-posterior sway we

applied Galvanic Vestibular Stimulation (GVS). A binaural, bipolar GVS was

delivered from two round electrodes with 3.2 cm diameter (Axelgaard Manufacturing

Co., Fallbrook, CA, USA). A custom-made LabVIEW program (National Instruments

Inc., Austin, TX, USA) generated an analog voltage, which was transformed into a

square wave of 1 mA current using the neuroConn DC-Stimulator Plus (neuroCare

Group, Munchen, Germany). Electrodes were placed bilaterally on both the mastoid

processes and each scapula region approximately at the same height as the spine of the

scapula. The GVS stimulation was the same for both sides and consisted of ±1 mA on

a sinusoidal wave at 0.36 Hz. (Hwang 2014, 2017). The vision was perturbed by a

projection of 500 randomly distributed pyramids (30 cm of height and projected 10

meters from the subject base of support) that moved in an oscillatory manner in a 0.2

47

Hz frequency. The pyramids translated in an anteroposterior direction in two

conditions: a low vision condition where the objects translated 20 centimeters and a

high vision condition where the objects translated 80 centimeters. A pair of 20mm

vibrators where strapped on each Achilles tendon, vibrating at an amplitude of 1 mm

and frequency of 80 Hz with a periodic square wave stimulus of 0.28 Hz.

Twenty trials of 135 seconds were collected (Hwang 2017). The trials were

randomized in four conditions as such as low vision, vibration, and GVS (LVG);

vision and GVS (LG); high vision, vibration, and GVS (HVG); high vision and GVS

(HG). Gain and phase of leg and trunk segments displacement related to each

condition were calculated (refer to the data analysis section).

Twelve reflective markers were placed bilaterally on the temple (head),

acromion, greater trochanter (hip), lateral epicondyle of the femur (knee), lateral

malleolus (ankle), and first metatarsal (foot). Kinematics were collected at 120 Hz

using a thirteen-camera optical motion analysis system (Qualisys, Goteborg, Sweden).

Binaural, bipolar GVS was delivered from two round electrodes with 3.2 cm diameter

(Axelgaard Manufacturing Co., Ltd, Fallbrook, CA, USA), placed on the mastoid

processes behind the ears. A custom-made LabVIEW program (National Instruments

Inc., Austin, TX, USA) generated an analog voltage, which was transformed into a

square wave of 1 mA current using the neuroConn DC-Stimulator Plus (neuroCare

Group, Munchen, Germany).

48

Figure 8. Standing assessment representation

4.3.4 Data Analysis

Kinematic data were collected using motion capture cameras (Qualisys AB,

Göteborg, Sweden). Data collected was processed and analyzed in Matlab

(MathWorks Inc.). The gain and phase between sensory input and leg/trunk

displacement were calculated between groups and across days. The leg segment was

defined by anteroposterior movement of the hip and ankle markers, and the trunk

segment was defined by the anteroposterior movement of the shoulder and hip

markers. Gain is the amplitude of the output divided by the amplitude of the input at

each driving frequency. For example, if the gain to the visual input equals one, it

means that the amplitude of the segment displacement (output) and the visual

49

perturbation (input) at the driving frequency are the same. Phase is a measure of the

temporal relationship between the input and output; the output may lead the input

(positive values) or lag behind it (negative values) (Hwang et al 2014).

4.3.5 Statistical Analysis

Six repeated measures ANOVAs were conducted to compare the effect of

collision sports on gains to GVS, vision, and vibration in leg and trunk segments

displacement. We used a Bonferroni correction for multiple comparisons and α =

0.008 was the threshold for statistical significance. Statistical analyses were carried

out in SAS (SAS Institute Inc., Cary, NC).

4.4 Results

There was no significant difference in group interaction (F6, 168 =2.575,

p=0.244) to any of the variables collected with SCAT 5.

4.4.1 Standing Balance Assessment – Leg AP Displacement

There were no changes in AP leg segment gain to vision (i.e. group effect; F3,

84=2.624, p=0.094, η2=0.086), AP leg segment gain to GVS (F3, 84=1.341, p=0.266,

η2=0.46), or AP leg segment gain to vibration (F1, 28=3.124, p=0.088, η2=0.100). In

addition, there were no changes in sensory reweighting for any modality (i.e. condition

X group effect; vision, F1, 28=0.074, p=0.788; GVS, F1, 28=0.547, p=0.547;

vibration, F1,28 = 0.734, p = 0.399) (Figure 9 - 11).

4.4.2 Standing Balance Assessment – Trunk AP Displacement

There were no changes in AP trunk segment gain to vision (i.e. group effect;

F3, 84=3.238, p=0.057, η2=0.104), AP trunk segment gain to GVS (F3, 84=1.046,

50

p=0.377, η2=0.036), or AP trunk segment gain to vibration (F1, 28 = 4.893, p=0.035,

η2=0.149). In addition, there were no changes in sensory reweighting for any modality

(i.e. condition X group effect; vision, F1, 28=0.101, p=0.754; GVS, F1, 28=0.547,

p=0.547; vibration, F1,28 = 0.503, p = 0.503) (Figure 9 - 11).

Figure 9. Gain to vision in collision vs no-contact athletes

51

Figure 10. Gain to vibration in collision vs no-contact athletes

Figure 11. Gain to GVS in collision vs no-contact athletes.

52

4.5 Discussion

The present study evaluated sensory reweighting in a collegiate population,

comparing athletes from collision to non-contact sports. We hypothesized that the

collision sports athletes would demonstrate a diminished gain to vestibular

manipulation via GVS, and that no difference would be noticed in vision and vibration

gains. However, our results demonstrated similar sensory reweighting behaviors

across all of the sensory modalities regardless of sports participation group.

A previous study that used a similar standing assessment (Hwang at al 2014)

showed that when proprioception is perturbed by vibration, gains of body segments

relative to the visual and vestibular systems are higher, suggesting that the central

nervous system places a greater emphasis on visual and vestibular input. This process

of reweighting was called an “inter-modal effect” because the altered reliability of one

sensory input dynamically influences the response to other sensory modalities. When

vision input was changed from a low amplitude to a high amplitude stimulus, gain to

vision decreases relative to the response to the low amplitude stimulus. This suggests

that a larger visual stimulus makes vision less reliable, and leading to a reduction in

the gain to vision in that condition. This scenario represents “intra-modal” reweighting

because the effects are observed within the same modality, in this example vision.

In the current study, both intra- and inter-modal sensory reweighting were

observed for both groups, with no difference in gains between groups. This suggests

that sensory reweighting in these collegiate collision athletes is not detrimentally

impacted by the repeated subconcussive head impacts experienced in their respective

sports. In contrast to the similarities in sensory reweighting capability in the current

53

study, a recent study described differences in BESS scores in collegiate lacrosse

players when tested pre and postseason (Miyashita, 2017). However, those differences

were only evident when the participants were tested on a foam surface (Miyashita,

2017). Using the same postural control test (BESS) and testing young football players,

another study reported no difference from pre to postseason (Campoletano 2018).

Since sensory reweighting likely reflects higher order central nervous system

processing (Karim et al. 2013), it is possible that results may differ at different time

points in the sports season. A previous study comparing collision (football, ice

hockey) to non-contact (track, crew, and Nordic skiing) collegiate athletes prior and

post season, suggested that academic learning was negatively impacted after the

season in contact athletes (McAllister 2012). There were no differences at baseline

between the collision and non-contact athletes. Although we did not control for when

subjects were tested relative to their sports season, the majority of athletes were mid-

season, which might be a reason why no difference in sensory output between the

collision and non-contact group was found.

4.6 Conclusion

Our results suggest that sensory reweighting between collegiate collision sports

athletes and non-contact athletes is similar. Future studies with different sports and

examining differences between pre-post season are necessary to better understand how

differences across sports contribute to changes in sensory reweighing.

54

FINAL CONSIDERATIONS

5.1 Limitations and Future Directions

The first limitation of our studies was the use of only soccer athletes. For

experiments 1 and 2 we only studied the differences between soccer players,

performing soccer heading or not. We believe that non-athletes would demonstrate a

different sensory reweighting paradigm after repetitive head impacts when compared

to athletes. For the third experiment, we focused on collision and non-contact athletes.

We did not choose a specific sport or time of the season. Some studies demonstrate

differences in sports and levels of play when compared to repetitive head impacts, the

same should be considered when studying sensory reweighing. It is possible that

athletes in sports that have a higher occurrence of head impacts might present an

altered sensory reweighing, such as a set point shift. There may be sport specific

benefits to an altered sensory weighting scheme such as not falling over during a game

after heading the soccer ball. Future studies should explore not only the difference

across sports, but also examine the influence of season timing (pre, postseason), and

sedentary populations.

Another aspect to be explored is the cumulative effect of repeated

subconcussive head impacts throughout life. A better understanding of the progression

of symptoms and possible balance deficits in the lifespan of these individuals will help

devise appropriate interventions to enhance the quality of life and safety for former

athletes.

Chapter 5

55

5.2 Conclusion

In these three studies, we sought to examine sensory reweighting in a cohort of

collegiate athletes. The two first experiments explored the acute stage of

subconcussive head impacts, and the third experiment explored the effect of regular

participation in collision sports on sensory reweighing.

Although there might be a disruption in vestibular processing following

repetitive subconcussive head impacts, as seen in previous research, we found no

measurable changes in balance mechanisms during walking. Due to the complex

nature of gait and its many degrees of freedom, even if the vestibular system is

disrupted immediately following a session of ten soccer headings, that disruption may

not be sufficient to disrupt balance. Furthermore, all participants tested were current

soccer players, who were used to practicing and performing soccer heading weekly.

To further our studies on sensory reweighing and RSHI, in our second

experiment we analyzed not only the vestibular system but also visual and

somatosensory systems using an experimental design previously utilized by our

laboratory, including the same controlled soccer heading protocol. In this experiment,

visual, somatosensory, and vestibular perturbations were applied to understand if

sensory reweighing was altered immediately following a short bout of soccer heading.

Our results showed no change in the response to visual, vestibular, somatosensory

input when compared to a group that did not perform the soccer headings. We

speculate that tolerance to mild repetitive head impacts and a possible neuroprotective

mechanism to maintain balance following head impacts might have played a role in

our results. Individuals that experience a number of RHI (ie. soccer athletes) might

have a higher threshold for sensory perturbations to maintain balance in different

56

environmental situations. It is possible that RHI may only lead to an impairment in

later life, but this is speculative.

To understand if participation in collision sports could alter sensory

reweighing, our third experiment looked for differences in sensory reweighting

between collision and non-contact collegiate athletes using the same standing balance

assessment used in the previous study. Both collision and non-contact athletes

demonstrate a similar capacity for sensory reweighting. This suggests that across the

collegiate level (young, highly-trained) athletes, the central nervous system exhibits a

remarkable capacity for sensory reweighting that is not detrimentally impacted by

current participation in collision sports.

Using sensitive measurements we were able to observe sensory reweighting in

our cohort, and detected no change in sensory reweighting or balance control during

walking and quiet stance following RSHI in collegiate athletes.

57

Allison, Leslie K., Tim Kiemel, and John J. Jeka. "Multisensory reweighting of vision and touch is intact in healthy and fall-prone older adults." Experimental brain research 175.2 (2006): 342-352.

Alosco, M. L., et al. "Age of first exposure to American football and long-term neuropsychiatric and cognitive outcomes." Translational psychiatry 7.9 (2017): e1236.

Alsalaheen, Bara A., et al. "Relationship between cognitive assessment and balance measures in adolescents referred for vestibular physical therapy after concussion." Clinical journal of sport medicine: official journal of the Canadian Academy of Sport Medicine 26.1 (2016): 46.

Alsalaheen, Bara A., et al. "Vestibular rehabilitation for dizziness and balance disorders after concussion." Journal of Neurologic Physical Therapy 34.2 (2010): 87-93.

Anson, Eric, et al. "Failure on the Foam Eyes Closed Test of Standing Balance Associated With Reduced Semicircular Canal Function in Healthy Older Adults." Ear and hearing 40.2 (2019): 340-344.

Azad AM, Al Juma S, Bhatti JA, Delaney JS (2016) Modified Balance Error Scoring System (M-BESS) test scores in athletes wearing protective equipment and cleats. BMJ Open Sport Exerc Med 2:e000117. doi: 10.1136/bmjsem-2016-000117

Bailes JE, Petraglia AL, Omalu BI, Nauman E, Talavage T. Role of subconcussion in repetitive mild traumatic brain injury: A review. J Neurosurg. 2013;119(5):1235-1245.

Bailes, J. E., Petraglia, A. L., Omalu, B. I., Nauman, E., & Talavage, T. (2013). Role of subconcussion in repetitive mild traumatic brain injury: a review. Journal of neurosurgery, 119(5), 1235-1245.

Baugh, Christine M., et al. "Chronic traumatic encephalopathy: neurodegeneration following repetitive concussive and subconcussive brain trauma." Brain imaging and behavior 6.2 (2012): 244-254.

REFERENCES

58

Bell, David R., et al. "Systematic review of the balance error scoring system." Sports health 3.3 (2011): 287-295.

Bent LR, McFadyen BJ, Inglis JT. Vestibular contributions during human locomotor tasks. Exerc Sport Sci Rev. 2005;33(3):107-113.

Bent LR, McFadyen BJ, Merkley VF, Kennedy PM, Inglis JT. Magnitude effects of galvanic vestibular stimulation on the trajectory of human gait. Neurosci Lett. 2000;279(3):157-160.

Brainard LL, Beckwith JG, Chu JJ, et al. Gender differences in head impacts sustained by collegiate ice hockey players. Med Sci Sports Exerc. 2012;44(2):297.

Breedlove EL, Robinson M, Talavage TM, et al. Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. J Biomech. 2012;45(7):1265-1272.

Broglio SP, Eckner JT, Martini D, Sosnoff JJ, Kutcher JS, Randolph C. Cumulative head impact burden in high school football. J Neurotrauma. 2011;28(10):2069-2078.

Broglio, S. P., et al. "No acute changes in postural control after soccer heading." British journal of sports medicine 38.5 (2004): 561-567.

Broglio, S. P., Guskiewicz, K. M., Sell, T. C., & Lephart, S. M. (2004). No acute changes in postural control after soccer heading. British journal of sports medicine, 38(5), 561-567.

Broglio, Steven P., et al. "Cognitive decline and aging: the role of concussive and subconcussive impacts." Exercise and sport sciences reviews 40.3 (2012): 138.

Broglio, Steven P., Jacob J. Sosnoff, and Michael S. Ferrara. "The relationship of athlete-reported concussion symptoms and objective measures of neurocognitive function and postural control." Clinical Journal of Sport Medicine 19.5 (2009): 377-382.

Brosseau-Lachaine O, Gagnon I, Forget R, Faubert J (2008) Mild traumatic brain injury induces prolonged visual processing deficits in children. Brain Inj 22:657–668. doi: 10.1080/02699050802203353

Caccese JB, Buckley TA, Tierney RT, et al. Head and neck size and neck strength predict linear and rotational acceleration during purposeful soccer heading. Sports biomechanics. 2017:1-15.

59

Caccese JB, Buckley TA, Tierney RT, Rose WC, Glutting JJ, Kaminski TW. Sex and age differences in head acceleration during purposeful soccer heading. Research in sports medicine. 2018;26(1):64-74.

Caccese JB, Lamond LC, Buckley TA, Kaminski TW. Reducing purposeful headers from goal kicks and punts may reduce cumulative exposure to head acceleration. Research in sports medicine. 2016;24(4):407-415.

Caccese JB. Head accelerations across collegiate, high school and youth female and male soccer players. Br J Sports Med. 2017:097118.

Caccese, Jaclyn B., et al. "Effects of Repetitive Head Impacts on a Concussion Assessment Battery." Medicine and science in sports and exercise (2019).

Caccese, Jaclyn B., et al. "Postural Control Deficits After Repetitive Soccer Heading." Clinical journal of sport medicine: official journal of the Canadian Academy of Sport Medicine(2018).

Campolettano, Eamon T., Gunnar Brolinson, and Steven Rowson. "Postural control and head impact exposure in youth football players: comparison of the Balance Error Scoring System and a Force Plate Protocol." Journal of applied biomechanics 34.2 (2017): 127-133.

Cavanaugh, James T., et al. "Detecting altered postural control after cerebral concussion in athletes with normal postural stability." British journal of sports medicine 39.11 (2005): 805-811.

Cohen, Helen S., and Kay T. Kimball. "Usefulness of some current balance tests for identifying individuals with disequilibrium due to vestibular impairments." Journal of Vestibular Research 18.5, 6 (2008): 295-303.

Covassin, Tracey, et al. "The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion." The American journal of sports medicine40.6 (2012): 1303-1312.

Cripps, Andrea, et al. "Visual perturbation impacts upright postural stability in athletes with an acute concussion." Brain injury 32.12 (2018): 1566-1575.

Crisco JJ, Fiore R, Beckwith JG, et al. Frequency and location of head impact exposures in individual collegiate football players. Journal of athletic training. 2010;45(6):549-559.

Crisco JJ, Wilcox BJ, Beckwith JG, et al. Head impact exposure in collegiate football players. J Biomech. 2011;44(15):2673-2678.

60

Cushman D, Hendrick J, Teramoto M, et al (2018) Reliability of the balance error scoring system in a population with protracted recovery from mild traumatic brain injury. Brain Inj 32:569–574. doi: 10.1080/02699052.2018.1432891

De Waele, C., et al. "Vestibular projections in the human cortex." Experimental brain research 141.4 (2001): 541-551.

Dorminy M, Hoogeveen A, Tierney RT, Higgins M, McDevitt JK, Kretzschmar J. Effect of soccer heading ball speed on S100B, sideline concussion assessments and head impact kinematics. Brain injury. 2015;29(10):1158-1164.

Echemendia, Ruben J., et al. "The sport concussion assessment tool 5th edition (SCAT5): background and rationale." Br J Sports Med 51.11 (2017): 848-850.

Ernst, Arne, et al. "Management of posttraumatic vertigo." Otolaryngology—Head and Neck Surgery 132.4 (2005): 554-558.

Fitzpatrick RC, Day BL. Probing the human vestibular system with galvanic stimulation. J Appl Physiol. 2004;96(6):2301-2316.

Fitzpatrick RC, Wardman DL, Taylor JL. Effects of galvanic vestibular stimulation during human walking. J Physiol (Lond ). 1999;517(3):931-939.

Graves, Barbara Sue. "University football players, postural stability, and concussions." The Journal of Strength & Conditioning Research 30.2 (2016): 579-583.

Grossman GE, Leigh RJ, Bruce EN, Huebner WP, Lanska DJ. Performance of the human vestibuloocular reflex during locomotion. J Neurophysiol. 1989;62(1):264–72.

Guskiewicz KM, Ross SE, Marshall SW. Postural stability and neuropsychological deficits after concussion in collegiate athletes. J Athl Train. 2001;36(3):263–273.

Guskiewicz, Kevin M., Scott E. Ross, and Stephen W. Marshall. "Postural stability and neuropsychological deficits after concussion in collegiate athletes." Journal of athletic training 36.3 (2001): 263.

Gysland SM, Mihalik JP, Register-Mihalik JK, Trulock SC, Shields EW, Guskiewicz KM. The relationship between subconcussive impacts and concussion history on clinical measures of neurologic function in collegiate football players. Ann Biomed Eng. 2012;40(1):14-22.

61

Haran FJ, Tierney R, Wright WG, Keshner E, Silter M. Acute changes in postural control after soccer heading. Int J Sports Med. 2013;34(04):350-354.

Haran, F. J., et al. "Acute changes in postural control after soccer heading." International journal of sports medicine 34.04 (2013): 350-354.

Hides, Julie A., et al. "A prospective investigation of changes in the sensorimotor system following sports concussion. An exploratory study." Musculoskeletal science and practice 29 (2017): 7-19.

Higgins MJ, Tierney RT, Caswell S, Driban JB, Mansell J, Clegg S. An in-vivo model of functional head impact testing in non-helmeted athletes. Proceedings of the Institution of Mechanical Engineers, Part P: Journal of Sports Engineering and Technology. 2009;223(3):117-123.

Horak FB, Macpherson JM. Postural orientation and equilibrium. In: Rowell LB, Shepard JT, eds. Handbook of Physiology: Section 12, Exercise Regulation and Integration of Multiple Systems. New York: Oxford University Press, 1996; 255–92.

Horak, Fay B. "Postural orientation and equilibrium: what do we need to know about neural control of balance to prevent falls?." Age and ageing 35.suppl_2 (2006): ii7-ii11.

Howell, David R., Louis R. Osternig, and Li-Shan Chou. "Adolescents demonstrate greater gait balance control deficits after concussion than young adults." The American journal of sports medicine 43.3 (2015): 625-632.

Hwang, Sungjae, et al. "A central processing sensory deficit with Parkinson’s disease." Experimental brain research 234.8 (2016): 2369-2379.

Hwang, Sungjae, et al. "Dynamic reweighting of three modalities for sensor fusion." PloS one 9.1 (2014): e88132.

Hwang, Sungjae, et al. "Vestibular dysfunction after subconcussive head impact." Journal of neurotrauma 34.1 (2017): 8-15.

Karim, Helmet, et al. "Functional brain imaging of multi-sensory vestibular processing during computerized dynamic posturography using near-infrared spectroscopy." Neuroimage74 (2013): 318-325.

King D, Hume PA, Brughelli M, Gissane C. Instrumented mouthguard acceleration analyses for head impacts in amateur rugby union players over a season of matches. Am J Sports Med. 2015;43(3):614-624.

62

King LA, Mancini M, Fino PC, et al (2017) Sensor-Based Balance Measures Outperform Modified Balance Error Scoring System in Identifying Acute Concussion. Ann Biomed Eng 45:2135–2145. doi: 10.1007/s10439-017-1856-y

Kleffelgaard, Ingerid, et al. "Vestibular rehabilitation after traumatic brain injury: case series." Physical therapy 96.6 (2016): 839-849.

Lamond LC, Caccese JB, Buckley TA, Glutting J, Kaminski TW. Linear acceleration in direct head contact across impact type, player position, and playing scenario in collegiate women's soccer players. Journal of athletic training. 2018;53(2):115-121.

Lau B, Lovell MR, Collins MW, Pardini J. Neurocognitive and symptom predictors of recovery in high school athletes. Clinical Journal of Sport Medicine. 2009;19(3):216-221.

Lipton ML, Kim N, Zimmerman ME, et al. Soccer heading is associated with white matter microstructural and cognitive abnormalities. Radiology. 2013;268(3):850-857.

Logan, David, Tim Kiemel, and John J. Jeka. "Asymmetric sensory reweighting in human upright stance." PLoS One 9.6 (2014): e100418.

Lynall RC, Clark MD, Grand EE, et al. Head impact biomechanics in women's college soccer. Med Sci Sports Exerc. 2016;48(9):1772-1778.

Lynall, Robert C., et al. "Acute Lower Extremity Injury Rates Increase after Concussion in College Athletes." Medicine and science in sports and exercise 47.12 (2015): 2487-2492.

MacLellan, Michael J., and Aftab E. Patla. "Adaptations of walking pattern on a compliant surface to regulate dynamic stability." Experimental brain research 173.3 (2006): 521-530.

MacLellan, Michael J., and Aftab E. Patla. "Adaptations of walking pattern on a compliant surface to regulate dynamic stability." Experimental brain research 173.3 (2006): 521-530.

Mainwaring L, Ferdinand Pennock KM, Mylabathula S, Alavie BZ (2018) Subconcussive head impacts in sport: A systematic review of the evidence. Int J Psychophysiol 132:39–54. doi: 10.1016/J.IJPSYCHO.2018.01.007

Mangus, Brent C., Harvey W. Wallmann, and Matthew Ledford. "Soccer: Analysis of

63

postural stability in collegiate soccer players before and after an acute bout of heading multiple Soccer balls." Sports biomechanics 3.2 (2004): 209-220.

Master, Christina L., et al. "Vision and vestibular system dysfunction predicts prolonged concussion recovery in children." Clinical journal of sport medicine 28.2 (2018): 139-145.

Master, Christina L., et al. "Vision diagnoses are common after concussion in adolescents." Clinical pediatrics 55.3 (2016): 260-267.

McAllister, Thomas W., et al. "Cognitive effects of one season of head impacts in a cohort of collegiate contact sport athletes." Neurology 78.22 (2012): 1777-1784.

McCuen E, Svaldi D, Breedlove K, et al. Collegiate women's soccer players suffer greater cumulative head impacts than their high school counterparts. J Biomech. 2015;48(13):3729-3732.

McDevitt, J., et al. "Vestibular and oculomotor assessments may increase accuracy of subacute concussion assessment." International journal of sports medicine 37.09 (2016): 738-747.

McKee AC, Cantu RC, Nowinski CJ, et al. Chronic traumatic encephalopathy in athletes: Progressive tauopathy after repetitive head injury. Journal of Neuropathology & Experimental Neurology. 2009;68(7):709-735.

McLeod, Tamara C. Valovich, et al. "Serial administration of clinical concussion assessments and learning effects in healthy young athletes." Clinical Journal of Sport Medicine14.5 (2004): 287-295.

Mihalik JP, Bell DR, Marshall SW, Guskiewicz KM. Measurement of head impacts in collegiate football players: An investigation of positional and event-type differences. Neurosurgery. 2007;61(6):1229-1235.

Miyashita, Theresa L., Eleni Diakogeorgiou, and Kaitlyn Marrie. "Correlation of head impacts to change in Balance Error Scoring System scores in Division I men’s lacrosse players." Sports health 9.4 (2017): 318-323.

Montenigro, Philip H., et al. "Cumulative head impact exposure predicts later-life depression, apathy, executive dysfunction, and cognitive impairment in former high school and college football players." Journal of neurotrauma 34.2 (2017): 328-340.

Moore, Brian M., Joseph T. Adams, and Edward Barakatt. "Outcomes Following a

64

Vestibular Rehabilitation and Aerobic Training Program to Address Persistent Post-Concussion Symptoms An Exploratory Study." Journal of allied health 45.4 (2016): 59E-68E.

Moser, Rosemarie Scolaro, Philip Schatz, and Barry D. Jordan. "Prolonged effects of concussion in high school athletes." Neurosurgery 57.2 (2005): 300-306.

Mucha A, Collins MW, Elbin RJ, et al. A brief vestibular/ocular motor screening (VOMS) assessment to evaluate concussions: preliminary findings. Am J Sports Med. 2014;42(10):2479–2486.

Mulavara, Ajitkumar P., Helen S. Cohen, and Jacob J. Bloomberg. "Critical features of training that facilitate adaptive generalization of over ground locomotion." Gait & posture 29.2 (2009): 242-248.

Oldham, Jessie R., et al. "Efficacy of Tandem Gait to Identify Impaired Postural Control after Concussion." Medicine and science in sports and exercise 50.6 (2018): 1162-1168.

Padula W V., Capo-Aponte JE, Padula W V., et al (2017) The consequence of spatial visual processing dysfunction caused by traumatic brain injury (TBI). Brain Inj 31:589–600. doi: 10.1080/02699052.2017.1291991

Paniccia, Melissa, et al. "Postural stability in healthy child and youth athletes: the effect of age, sex, and concussion-related factors on performance." Sports health 10.2 (2018): 175-182.

Peterka, R. J. "Sensorimotor integration in human postural control." Journal of neurophysiology 88.3 (2002): 1097-1118.

Peterka, Robert J., and Martha S. Benolken. "Role of somatosensory and vestibular cues in attenuating visually induced human postural sway." Experimental brain research 105.1 (1995): 101-110.

Peterson, Connie L., et al. "Evaluation of neuropsychological domain scores and postural stability following cerebral concussion in sports." Clinical Journal of Sport Medicine 13.4 (2003): 230-237.

Pletcher, Erin R., et al. "Normative data for the NeuroCom sensory organization test in US military special operations forces." Journal of athletic training 52.2 (2017): 129-136.

Prangley, Alyssa, Mathew Aggerholm, and Michael Cinelli. "Improvements in balance control in individuals with PCS detected following vestibular training:

65

A case study." Gait & posture 58 (2017): 229-231.

Press JN, Rowson S. Quantifying head impact exposure in collegiate women's soccer. Clinical journal of sport medicine. 2017;27(2):104-110.

Prien, Annika, et al. "Epidemiology of head injuries focusing on concussions in team contact sports: A systematic review." Sports medicine 48.4 (2018): 953-969.

Reimann H, Fettrow TD, Thompson ED, Agada P, McFadyen BJ, Jeka JJ. Complementary mechanisms for upright balance during walking. PloS one. 2017;12(2):e0172215.

Reynolds BB, Patrie J, Henry EJ, et al. Effects of sex and event type on head impact in collegiate soccer. Orthopaedic journal of sports medicine. 2017;5(4):2325967117701708.

Rochefort C, Walters-Stewart C, Aglipay M, et al (2017) Balance Markers in Adolescents at 1 Month Postconcussion. Orthop J Sport Med 5:232596711769550. doi: 10.1177/2325967117695507

Rowson, Steven, et al. "Correlation of concussion symptom profile with head impact biomechanics: a case for individual-specific injury tolerance." Journal of neurotrauma 35.4 (2018): 681-690.

Schmidt, Julianne D., et al. "Balance regularity among former high school football players with or without a history of concussion." Journal of athletic training 53.2 (2018): 109-114.

Schmitt, D. M., et al. "Effect of an acute bout of soccer heading on postural control and self-reported concussion symptoms." International journal of sports medicine 25.05 (2004): 326-331.

Schubert MC, Shepard NT, Jacobson GP, Shepard NT. Practical anatomy and physiology of the vestibular system. Balance function assessment and management. 2008:1-12.

Shumway-Cook, Anne, and Fay Bahling Horak. "Assessing the influence of sensory interaction on balance: suggestion from the field." Physical therapy 66.10 (1986): 1548-1550.

Skóra, Wojciech, et al. "Vestibular system dysfunction in patients after mild traumatic brain injury." Annals of agricultural and environmental medicine: AAEM 25.4 (2018): 665-668.

66

Slobounov, Semyon, et al. "Alteration of postural responses to visual field motion in mild traumatic brain injury." Neurosurgery59.1 (2006): 134-193.

Sollmann N, Echlin PS, Schultz V, et al. Sex differences in white matter alterations following repetitive subconcussive head impacts in collegiate ice hockey players. Neuroimage: clinical. 2018;17:642-649.

Sosnoff, Jacob J., et al. "Previous mild traumatic brain injury and postural-control dynamics." Journal of athletic training46.1 (2011): 85-91.

Stamm, Julie M., et al. "Age at first exposure to football is associated with altered corpus callosum white matter microstructure in former professional football players." Journal of neurotrauma 32.22 (2015): 1768-1776.

Stewart WF, Kim N, Ifrah C, et al. Heading frequency is more strongly related to cognitive performance than unintentional head impacts in amateur soccer players. Frontiers in neurology. 2018;9.

Storey EP, Master SR, Lockyer JE, et al (2017) Near Point of Convergence after Concussion in Children. Optom Vis Sci 94:96–100. doi: 10.1097/OPX.0000000000000910

Talavage TM, Nauman EA, Breedlove EL, et al. Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. J Neurotrauma. 2014;31(4):327-338.

Tarnutzer, Alexander A., et al. "Persistent effects of playing football and associated (subconcussive) head trauma on brain structure and function: a systematic review of the literature." Br J Sports Med (2016): bjsports-2016.

Tierney RT, Higgins M, Caswell SV, et al. Sex differences in head acceleration during heading while wearing soccer headgear. Journal of athletic training. 2008;43(6):578-584.

Valovich McLeod TC, Hale TD. Vestibular and balance issues following sport-related concussion. Brain injury. 2015;29(2):175-184.

Walker, W. C., Cifu, D. X., & Lew, H. L. (2012). Sensorintegrative dysfunction underlying vestibular disorders after traumatic brain injury: a review. Journal of rehabilitation research and development, 49(7), 985.

Wallace, Bridgett, and Jonathan Lifshitz. "Traumatic brain injury and vestibulo-ocular function: current challenges and future prospects." Eye and brain 8 (2016): 153.

67

Wilcox BJ, Beckwith JG, Greenwald RM, et al. Head impact exposure in male and female collegiate ice hockey players. J Biomech. 2014;47(1):109-114.

Winter, David A. "Human balance and posture control during standing and walking." Gait & posture 3.4 (1995): 193-214.

Wright, W. G., R. T. Tierney, and J. McDevitt. "Visual-vestibular processing deficits in mild traumatic brain injury." Journal of Vestibular Research 27.1 (2017): 27-37.

Yorke, Amy M., et al. "Validity and reliability of the vestibular/ocular motor screening and associations with common concussion screening tools." Sports health 9.2 (2017): 174-180.

Zhou, Guangwei, and Jacob R. Brodsky. "Objective vestibular testing of children with dizziness and balance complaints following sports-related concussions." Otolaryngology--Head and Neck Surgery 152.6 (2015): 1133-1139.

68

Appendix - A

IRB APPROVAL – CHAPTER ONE AND TWO

69

Appendix - B

IRB APPROVAL – CHAPTER THREE