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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
Approved: __________________________________________________________ John J. Jeka, Ph.D. Chair of the Department of Kinesiology and Applied Physiology
Approved: __________________________________________________________ Kathleen S. Matt, Ph.D. Dean of the College of Health Sciences
Approved: __________________________________________________________ Douglas J. Doren, Ph.D. Interim Vice Provost for Graduate and Professional Education
I certify that I have read this dissertation and that in my opinion it meets
the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.
Signed: __________________________________________________________ John J. Jeka, Ph.D. Professor in charge of dissertation I certify that I have read this dissertation and that in my opinion it meets
the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.
Signed: __________________________________________________________ Eric R. Anson, Ph.D. Member of dissertation committee I certify that I have read this dissertation and that in my opinion it meets
the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.
Signed: __________________________________________________________ Thomas Buckley, Ph.D. Member of dissertation committee I certify that I have read this dissertation and that in my opinion it meets
the academic and professional standard required by the University as a dissertation for the degree of Doctor of Philosophy.
Signed: __________________________________________________________ Matthew Hudson, Ph.D. Member of dissertation committee
iv
First of all, I would like to express my deepest appreciation to my dissertation
committee, Dr. John Jeka, Dr. Eric Anson, Dr. Thomas Buckley and Dr. Matthew
Hudson for being part of this dissertation and my graduate learning experience. A
special thanks to Dr. John Jeka, my advisor and chairman of my committee. This work
would not have been possible without his support and guidance. He played a key role
in my decision on moving from Brazil to the United States and the pursuit of a
Doctoral degree.
I am also grateful to all members of our lab, they were instrumental in helping
me from the most common daily activities to data collections and analysis. I’d also
like to recognize the effort that I received from Jaclyn Caccese Deckert, she extended
a great amount of assistance during the experiments from data collection to data
analysis and her insightful suggestions to my research.
Finally, I would like to thank my family and all the support given by my
mother, Rosa Maria Vanderlinde, and my father, Fernando Argemon dos Santos. They
were always there when I need it. I am thankful for all the effort and teachings shared
by them to make me a better person and persisting on my desire to obtain a higher
education.
ACKNOWLEDGMENTS
v
LIST OF TABLES ...................................................................................................... viii LIST OF FIGURES ....................................................................................................... ix ABSTRACT ................................................................................................................... x Chapter
1 BALANCE AND SENSORY IMPAIRMENT RELATED TO REPETITIVE HEAD IMPACT AND CONCUSSIONS: LITERATURE REVIEW ............................................................................................................. 1
3 THE EFFECT OF SOCCER HEADING IN SENSORY REWEIGHTING IN STANDING BALANCE ............................................................................. 29
4 SENSORY REWEIGHTING IN COLLISION SPORTS COLLEGE ATHLETES ...................................................................................................... 42
A IRB APPROVAL – CHAPTER ONE AND TWO .......................................... 68 B IRB APPROVAL – CHAPTER THREE ......................................................... 69
viii
Table 1. Balance mechanisms means and standard deviations .................................... 22
LIST OF TABLES
ix
Figure 1. The subjects walked in a foam surface, blindfolded and the GVS was applied on the second right heel strike as represented above. ................. 19
Figure 2. Example data – One subject data to illustrate the GVS response during one stride. RHS – right heel strike; LTO – left heel strike; LHS – left heel strike; RTO – right heel strike. ........................................................ 20
Figure 3. Foot placement strategy: foot placement, hip abduction and gluteus medius activity across 3 sessions (pre, post 0h and post 24h). ............... 23
Figure 4. Ankle roll strategy: CoM – CoP separation, ankle inversion and peroneus longus activity across 3 sessions (pre, post 0h and post 24h). ................ 23
Figure 5. Push off strategy: step length, ankle plantar flexion and medial gastrocnemius activity across 3 sessions (pre, post 0h and post 24h). .... 24
Figure 7. Gains of the soccer heading and control group for GVS, vibration and vision ....................................................................................................... 38
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
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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.
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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
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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
Figure 9. Gain to vision in collision vs no-contact athletes
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Figure 10. Gain to vibration in collision vs no-contact athletes
Figure 11. Gain to GVS in collision vs no-contact athletes.
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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
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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.
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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
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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
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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.
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