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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
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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
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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
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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
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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
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Table 1. Balance mechanisms means and standard deviations .................................... 22
LIST OF TABLES
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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
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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
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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
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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.
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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
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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
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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
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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,
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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
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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
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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
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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
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(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.
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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,
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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.
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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
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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.
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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
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Appendix - A
IRB APPROVAL – CHAPTER ONE AND TWO
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Appendix - B
IRB APPROVAL – CHAPTER THREE